Costa Rican Ecosystems 9780226121642

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Costa Rican Ecosystems

Costa Rican Ecosystems

Edited by Maarten Kappelle

The University of Chicago Press Chicago and London

Maarten Kappelle is currently coordinator for the United Nations Environment Programme’s global Chemicals and Waste Subprogramme and has previously held science and leadership roles in the World Wide Fund for Nature (WWF), The Nature Conservancy (TNC), Costa Rica’s Instituto Nacional de Biodiversidad (INBio), and several universities in the Netherlands and abroad. He is author, editor, or coeditor of many scientific books in Spanish and English, including Ecology and Conservation of Neotropical Montane Oak Forests, Biodiversity of the Oak Forests of Tropical America, Páramos de Costa Rica, and Diccionario de Biodiversidad. He lives and works in Nairobi, Kenya. The University of Chicago Press, Chicago 60637 The University of Chicago Press, Ltd., London © 2016 by The University of Chicago All rights reserved. Published 2016. Printed in the United States of America 24 23 22 21 20 19 18 17 16

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ISBN-13: 978-0-226-12150-5 (cloth) ISBN-13: 978-0-226-27893-3 (paper) ISBN-13: 978-0-226-12164-2 (e-book) DOI: 10.7208/chicago/9780226121642.001.0001 This publication is funded in part by the Gordon and Betty Moore Foundation. Front cover photograph taken by Yamil Sáenz. Library of Congress Cataloging- in- Pub lic ation Data Costa Rican ecosystems / edited by Maarten Kappelle. pages ; cm Includes bibliographical references and index. ISBN 978-0-226-12150-5 (cloth : alk. paper)—ISBN 978-0-22627893-3 (pbk. : alk. paper)—ISBN 978-0-226-12164-2 (e-book) 1. Ecology—Costa Rica. I. Kappelle, Maarten, editor. QH108.C6C664 2015 577.097286—dc23 2015011315 ♾ This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

Contents

Dedication

ix

List of Contributors Foreword

xi

xv

Thomas E. Lovejoy

Presentation

xvii

Rodrigo Gámez Lobo

Preface

xix

Maarten Kappelle

Part I. Introduction 1 Costa Rica’s Ecosystems: Setting the Stage 3 Maarten Kappelle

Part II. The Physical Environment 2 Climate of Costa Rica 19 Wilberth Herrera

3 Geology, Tectonics, and Geomorphology of Costa Rica: A Natural History Approach 30 Guillermo E. Alvarado and Guaria Cárdenes

4 Soils of Costa Rica: An Agroecological Approach 64 Alfredo Alvarado and Rafael Mata

Part III. The Pacific Ocean and Isla del Coco 5 The Pacific Coastal and Marine Ecosystems 97 Jorge Cortés

6 The Gulf of Nicoya Estuarine Ecosystem 139 José A. Vargas

7 Isla del Coco: Coastal and Marine Ecosystems 162 Jorge Cortés

8 Isla del Coco: Terrestrial Ecosystems 192 Michel Montoya

v

Part IV. The Northern Pacific Dry Lowlands 9 The Northern Pacific Lowland Seasonal Dry Forests of Guanacaste and the Nicoya Peninsula 247 Quírico Jiménez M., Eduardo Carrillo J., and Maarten Kappelle

10 Biodiversity Conservation History and Future in Costa Rica: The Case of Área de Conservación Guanacaste (ACG) 290 Daniel H. Janzen and Winnie Hallwachs

Part V. The Central and Southern Pacific Seasonally Moist Lowlands and Central Valley 11 The Central Pacific Seasonal Forests of Puntarenas and the Central Valley 345 Quírico Jiménez M. and Eduardo Carrillo J.

12 The Southern Pacific Lowland Evergreen Moist Forest of the Osa Region 360 Lawrence E. Gilbert, Catherine A. Christen, Mariana Altrichter, John T. Longino, Peter M. Sherman, Rob Plowes, Monica B. Swartz, Kirk O. Winemiller, Jennifer A. Weghorst, Andres Vega, Pamela Phillips, Christopher Vaughan, and Maarten Kappelle

Part VI. The Moist and Clouded Highlands 13 The Montane Cloud Forests of the Volcanic Cordilleras 415 Robert O. Lawton, Marcy F. Lawton, R. Michael Lawton, and James D. Daniels

14 The Montane Cloud Forests of the Cordillera de Talamanca 451 Maarten Kappelle

15 The Páramo Ecosystem of Costa Rica’s Highlands 492 Maarten Kappelle and Sally P. Horn

Part VII. The Wet Caribbean Lowlands 16 The Caribbean Lowland Evergreen Moist and Wet Forests 527 Deedra McClearn, J. Pablo Arroyo-Mora, Enrique Castro, Ronald C. Coleman, Javier F. Espeleta, Carlos García-Robledo, Alex Gilman, José González, Armond T. Joyce, Erin Kuprewicz, John T. Longino, Nicole L. Michel, Carlos Manuel Rodríguez, Andrea Romero, Carlomagno Soto, Orlando Vargas, Amanda Wendt, Steven Whitfield, and Robert M. Timm

Part VIII. The Caribbean Sea and Shore 17 The Caribbean Coastal and Marine Ecosystems 591 Jorge Cortés

Part IX. The Rivers, Lakes, and Wetlands 18 Rivers of Costa Rica 621 Catherine M. Pringle, Elizabeth P. Anderson, Marcelo Ardón, Rebecca J. Bixby, Scott Connelly, John H. Duff, Alan P. Jackman, Pia Paaby, Alonso Ramírez, Gaston E. Small, Marcia N. Snyder, Carissa N. Ganong, and Frank J. Triska

19 Lakes of Costa Rica 656 Sally P. Horn and Kurt A. Haberyan

20 Bogs, Marshes, and Swamps of Costa Rica 683 Jorge A. Jiménez

Part X. Conclusion 21 Costa Rican Ecosystems: A Brief Summary 709 Maarten Kappelle

Acronyms

723

Subject Index

727

Systematic Index of Common Names

747

Systematic Index of Scientific Names

757

In Memory of Dr. Luis Diego Gómez Pignataro (1944– 2009) The editor wishes to dedicate this book on Costa Rican ecosystems to Dr. Luis Diego Gómez Pignataro. His untimely death due to leukemia over five years ago occurred as this publication was being written and edited. Luis Diego Gómez P., Costa Rican biologist, botanist, geologist, and palaeontologist, was in his life a great naturalist, an unstoppable explorer, and a true uomo universale who mastered Latin— a neo-Renaissance person pur sang in the community of tropical scientists in Central America. Having learnt from generosos maestros like Paul W. Richards and Leslie R. Holdridge, he held a PhD from the Universidad de Loyola in Spain and a PhD honoris causa from the European Academy of Sciences. Luis Diego discovered the flora of the most remote parts of the country, from the inaccessible sectors of Parque Internacional La Amistad and Parque Nacional Chirripó, to the botanically unexplored core of Isla del Coco. And, as Jorge Arturo Jiménez pointed out, Luis “was capable of moving easily from an organismic perspective to an ecosystemic viewpoint, . . . as a true son of Humboldtian science”— something not often seen among scholars today. His vast knowledge of the arts and sciences went way beyond his in-depth understanding of the taxonomy and ecology of Neotropical ferns and mushrooms for which he was globally renowned as an outstanding eminence. For instance, he was an excellent piano player and cofounder of the Costa Rican music institution Fundación Ars Musica. Moreover, he published on fossils and early indigenous cultures. From 1970 to 1985, Luis served as General Director of the Museo Nacional de Costa Rica in San José. Under his leadership the Herbario Nacional flourished and attracted dozens of international botanists— including the editor of this book— who contributed enormously to the national plant collection by donating their duplicates. During his administration he was able to form a dream team of Costa Rican plant scientists including Luis Poveda, Nelson Zamora, Pablo Sánchez, and Quírico Jiménez, among many others. To ensure the sharing of scientific knowledge among Costa Rican scientists he launched the biological journal Brenesia, in honor of Alberto Brenes Mora, the famous botanist from San Ramón. Later on, from 1986 to 2005 Luis headed the Organization for Tropical Studies (OTS)– administered Estación ix

Biológica Las Cruces near San Vito de Java, Coto Brus, in southern Costa Rica. Here, he turned the Wilson Botanical Garden, founded in 1962 by Catherine and Robert Wilson, into a world-class research facility for plant taxonomists and ecologists alike. After the 1994 fire that destroyed the station’s library, herbarium, and other facilities he made sure the station was rebuilt and the library collection restored. After his retirement from Las Cruces, a new herbarium was established in his honor (Herbario Luis Diego Gómez [HLDG]) for his distinguished contributions to research, knowledge sharing, and land acquisition around the station. From 2005 to 2007 he served as Director of the OTS-administered Estación Biológica La Selva near Puerto Viejo de Sarapiquí, in northern Costa Rica. For more than twenty years, Luis worked for OTS as a professor of many courses, including ecology, ethnobiology, and tropical medicine. Luis’ visionary approach made him cofound Costa Rican organizations like Fundación de Parques Nacionales (FPN), the Academia Nacional de Ciencias, and the Instituto Nacional de Biodiversidad (INBio). During his prolific career he published over two hundred scientific articles and several books on, amongst others, Costa Rican plant taxonomy, ecology, and palaeontology, as well as a number of maps of the country’s vegetation and biotic units. In fact, he was the first national palaeontologist in Costa Rica doing research in the country and publishing his findings in scientific journals and magazines, including the description of new fossils. Some 30 years ago I first met Luis. It was in November 1985, when I walked into the herbarium of the Museo Nacional where he served as its director. He was sitting at his desk reviewing and identifying a number of ferns that he and others had collected in remote sectors of southern Costa Rica. I asked him if he could help me identify the dozens of ferns I had just collected for my master studies on the plant diversity and ecology of the montane oak forests of the Cordillera de Talamanca. He immediately started to put names on the newspapers that contained the specimens I had brought, explaining to me how I could recognize the different genera. Wow, how blessed I was to count on his taxonomic brilliance! We spent all afternoon going through the never-ending pile; he even came across a specimen of Thelypteris gomeziana, named after him by renowned fern taxonomist David Lellinger! At that moment we became

x Dedication

friends forever and worked closely for years on the pteridophytic flora of the tall oak forests and páramos of the high Talamancas. Twenty years after our first encounter in 1985, I started to develop the idea for the current volume and decided to discuss the plan with Luis in order to hear his viewpoint and invite him to serve as coeditor. Luis was enthusiastic from the first moment and provided helpful suggestions. Unfortunately, his progressing disease and the fatigue that immediately came with it did not allow him to play a role as coeditor, nor to write any piece of text for this volume. However, he continually encouraged me to work on the book and make sure I would finish it. When I learnt about his sudden departure on November 13, 2009, I was in shock. His death affected my energy levels and drive, and caused a setback in the development of the book. However, to this day I remember the last words he said to me only two weeks before he passed away: “Martín, asegúrete que se publique este libro! El pais lo necesita!”— “Martin, make sure this book gets published! The country needs it!” Although Luis Diego’s departure has left us with an immense void, his life and works remain to inspire young Costa Rican and visiting researchers, students, and naturalists. His first-ever studies on the classification and mapping of Costa Rica’s vegetation and biotic units, his papers on the Costa Rican ferns and fungi, as well as his numerous contributions on paleontological features and fossils, will continue to serve the many people who have an interest in the knowledge and conservation of the unique biodiversity that characterizes Costa Rica as a pioneer and leader in making sustainability work for people and nature alike in the twentyfirst century. Science will remember him through the twentyseven newly described species that bear his name today. We will remember “Luigi” (as he used to sign off his

Luis Diego enjoys a restful moment on a downed log in a Costa Rican forest. Photo courtesy: Rebeca Brenes.

letters) or “Ludovicus” (as he wrote under his Latin comments on collected plant specimens) as an extraordinarily knowledgeable man, a sensible friend, and a wonderful colleague. Someone who always took the time to listen and share his knowledge and experience with others— always with a great sense of humour. We will dearly miss him. Maarten Kappelle, editor

Contributors

Mariana Altrichter

Guaria Cárdenes

Jorge Cortés

Prescott College Prescott, AZ 86301 USA

Escuela Centroamericana de Geología Centro de Investigaciones en Ciencias Geológicas (CICG) Universidad de Costa Rica (UCR) San Pedro de Montes de Oca Costa Rica and Biology Department Florida Institute of Technology Florida USA

Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) and Escuela de Biología Universidad de Costa Rica (UCR) San Pedro de Montes de Oca Costa Rica

Alfredo Alvarado Centro de Investigaciones Agronómicas Facultad de Ciencias Agroalimentarias Universidad de Costa Rica (UCR) San Pedro de Montes de Oca Costa Rica

Guillermo E. Alvarado Área de Amenazas y Auscultación Sísmica y Volcánica Instituto Costarricense de Electricidad (ICE) San José Costa Rica

James D. Daniels Department of Biology and Cell Biology Huntingdon College Montgomery, AL 36106 USA

Eduardo Carrillo J. Instituto Internacional en Conservación y Manejo en Vida Silvestre (ICOMVIS) Universidad Nacional Heredia Costa Rica

Elizabeth P. Anderson

John H. Duff US Geological Survey Menlo Park, CA USA

Javier F. Espeleta

Department on Earth & the Environment Florida International University Miami, FL USA

Enrique Castro La Selva Biological Station Organization for Tropical Studies San Pedro de Montes de Oca Costa Rica

Marcelo Ardón Department of Biology East Carolina University Greenville, NC USA

Catherine A. Christen

J. Pablo Arroyo-Mora

Ronald C. Coleman

Department of Geography McGill University Montreal, Quebec Canada

Department of Biological Sciences California State University Sacramento Sacramento, CA 95819-6077 USA

Rebecca J. Bixby

Scott Connelly

Department of Biology University of New Mexico Albuquerque, NM USA

Odum School of Ecology University of Georgia Athens, GA 30602 USA

Smithsonian Conservation Biology Institute Front Royal, VA 22630 USA

xi

Tropical Science Center San José Costa Rica

Rodrigo Gámez Lobo Instituto Nacional de Biodiversidad (INBio) Santo Domingo de Heredia Costa Rica

Carlos García-Robledo Laboratory of Interactions and Global Change Department of Multitrophic Interactions Institute of Ecology (INECOL) Mexico and National Museum of Natural History Departments of Botany and Entomology Smithsonian Institution Washington, DC 20013-7012 USA

xii Contributors

Lawrence E. Gilbert

Daniel H. Janzen

R. Michael Lawton

Section of Integrative Biology and Brackenridge Field Laboratory University of Texas Austin, TX 78712 USA

Department of Biology University of Pennsylvania Philadelphia, PA 19104 USA

Department of Ecology and Evolutionary Biology University of Tennessee Knoxville, TN 37996 USA

Jorge A. Jiménez Alex Gilman La Selva Biological Station Organization for Tropical Studies San Pedro de Montes de Oca Costa Rica

Carissa N. Ganong Odum School of Ecology University of Georgia Athens, GA 30602 USA

José González La Selva Biological Station Organization for Tropical Studies San Pedro de Montes de Oca Costa Rica

Kurt A. Haberyan Department of Natural Sciences Northwest Missouri State University Maryville, MO 64468 USA

Winnie Hallwachs Department of Biology University of Pennsylvania Philadelphia, PA 19104 USA

Wilberth Herrera Apartado 2183-4050 Alajuela Costa Rica

Sally P. Horn Department of Geography University of Tennessee Knoxville, TN 37996 USA

Alan P. Jackman Department of Chemical Engineering University of California Davis, CA USA

Fundación MarViva Santa Ana Costa Rica

Quírico Jiménez Empresa de Servicios Públicos de Heredia (ESPH) Heredia Costa Rica

Armand T. Joyce 1408 Eastwood Drive Slidell, LA 70458 USA

Maarten Kappelle World Wide Fund for Nature ( WWF International) Gland Switzerland and Department of Geography University of Tennessee Knoxville, TN 37996 USA

Erin Kuprewicz National Museum of Natural History Department of Botany Smithsonian Institution Washington, DC 20013 USA

Marcy F. Lawton Monte Sano Learning Center Huntsville, AL 35801 USA

John T. (Jack) Longino Department of Biology University of Utah Salt Lake City, UT 84112 USA

Thomas E. Lovejoy Environmental Science and Policy George Mason University Fairfax, VA 22030 USA

Rafael Mata Centro de Investigaciones Agronómicas Facultad de Ciencias Agroalimentarias Universidad de Costa Rica (UCR) San Pedro de Montes de Oca Costa Rica

Deedra McClearn National Museum of Natural History Department of Botany Smithsonian Institution Washington, DC 20013 USA and DKU Program Office Duke University Durham, NC 27708 USA

Nicole L. Michel Department of Animal and Poultry Science University of Saskatchewan Saskatoon, SK S7N 5A6 Canada

Michel Montoya Robert O. Lawton Department of Biological Sciences University of Alabama Huntsville, AL 35899 USA

Fundación Amigos de la Isla del Coco (FAICO) San Pedro de Montes de Oca Costa Rica

Pia Paaby Organization for Tropical Studies (OTS) San Pedro de Montes de Oca Costa Rica

Contributors xiii

Pamela Phillips

Marcia N. Snyder

Christopher Vaughan

Livestock Insects Research Laboratory Agricultural Research Service United States Department of Agriculture Kerrville, TX 78028 USA

Odum School of Ecology University of Georgia Athens, GA 30602 USA

ICOMVIS Universidad Nacional Heredia Costa Rica and Department of Forest and Wildlife Ecology University of Wisconsin Madison, WI 53706 USA

Carlomagno Soto Rob Plowes Section of Integrative Biology Brackenridge Field Laboratory University of Texas Austin, TX 78712 USA

Catherine M. Pringle Odum School of Ecology University of Georgia Athens, GA 30602 USA

La Selva Biological Station Organization for Tropical Studies San Pedro de Montes de Oca Costa Rica

Andres Vega Monica B. Swartz Section of Integrative Biology Brackenridge Field Laboratory University of Texas Austin, TX 78712 USA

Robert M. Timm Alonso Ramírez Institute for Tropical Ecosystem Studies University of Puerto Rico Rio Piedras Puerto Rico

Department of Ecology and Evolutionary Biology & Biodiversity Institute University of Kansas Lawrence, KS 66045 USA

Carlos Manuel Rodríguez

Frank J. Triska

Conservation International San José Costa Rica

US Geological Survey Menlo Park, CA USA

Andrea Romero

José A. Vargas

University of Wisconsin-Whitewater Whitewater, WI 53190 USA

Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) Universidad de Costa Rica (UCR) San Pedro de Montes de Oca Costa Rica

AMBICOR Tibas Costa Rica

Jennifer A. Weghorst Natural History Museum and Biodiversity Research Center University of Kansas Lawrence, KS 66045 USA

Amanda Wendt Department of Ecology and Evolutionary Biology University of Connecticut Storrs, CT 06269-3043 USA

Steven Whitfield

Peter M. Sherman Prescott College Prescott, AZ 86301 USA

Gaston E. Small University of St. Thomas Saint Paul, MN USA

Orlando Vargas La Selva Biological Station Organization for Tropical Studies San Pedro de Montes de Oca Costa Rica

Zoo Miami Conservation and Research Department Miami, FL 33177 USA

Kirk O. Winemiller Department of Wildlife and Fisheries Sciences Texas A&M University College Station, TX 77843 USA

Foreword

It was inevitable that my path would lead to Costa Rica and its dazzling array of ecosystems. For decades the main entry point for North American students to tropical biology was through the Organization for Tropical Studies (OTS) and its field stations, most especially La Selva. I was a major exception in that I did my dissertation in the Brazilian Amazon, but I almost immediately (1971) made a pilgrimage to Central America to broaden my perspective. Just to get to La Selva involved a lengthy trip from San José: along the Cordillera, then up through the cloud forest and over a pass, and then down into the lowlands with the last leg of the journey up the Sarapiqui River by boat. It was a splendid partial introduction to Costa Rica’s ecosystems. In a sense I knew them already, but only in the abstract. The logical framework of Leslie R. Holdridge’s Life Zone System was fundamental for every tropical biology student, with its elegant simplicity constructed from gradients of temperature, moisture, and altitude. As important as that construct was and is, it paled in contrast with the biological reality of the ecosystems in question. Rich as the scientific knowledge of Costa Rica’s ecosystems was 40 years ago it is dwarfed by that of today. That stems from important scientific institutions in addition to the Organization for Tropical Studies: among others, the Tropical Science Center (TSC) of Holdridge and Joseph Tosi in San Pedro, the Tropical Agricultural Research and Higher Education Center (CATIE) at Turrialba, the epicenter of tropical dry forest ecology at Santa Rosa in Guanacaste, continually sparked by Dan Janzen, and the visionary Instituto Nacional de Biodiversidad (INBio). As a consequence this book on Costa Rica’s ecosystems— really the first for any tropical country— is long overdue but has a lot to build from. There have been extremely significant works on individual ecosystems (La Selva’s rainforests, Monteverde’s cloud forests, and the tropical alpine treeless páramos), but no comprehensive overview— other than the visitor experience on the grounds at INBioparque.

xv

In the same four decades Costa Rica has gone from being the Central American country with the most national parks to being the self-styled “Green Republic”— one that is often globally in the forefront as a major innovator in environment and sustainability. At the Earth Summit in Rio de Janeiro in 1992 Costa Rica was very much the showcase country in both biodiversity science and in conservation. Costa Rica wasn’t perfect, though. Much needed to be done in protecting marine and freshwater ecosystems, but Costa Rica was in every sense the leading nation in the tropics and to a major extent globally. Now with Rio+20 behind us— the United Nations Conference on Sustainable Development held in Rio de Janeiro, Brazil, on June 20– 22, 2012— and as the nations of the planet struggle with defining Sustainable Development Goals (SDGs), the environmental horizon is very dark indeed. The Stockholm Environment Institute’s diagnosis of Planetary Boundaries shows three major transgressions: in the carbon cycle (climate change), the nitrogen cycle (and proliferating dead zones in coastal waters), and, above all, in biodiversity. What is needed is a transition to planetary management, where this planet that we call “home” is managed as the biophysical system that it actually is. That, in turn, means conservation, management, Sustainable Development Goals that explicitly incorporate ecosystems and biodiversity, and, indeed, restoration of ecosystems at scale. That is the only way in which humanity can avoid a train wreck with climate change and the distorted nitrogen cycle with consequent staggering additional loss of biodiversity. It is also the only way that Latin America and the Caribbean can realize their potential as what the United Nations Development Program (UNDP) terms the Biodiversity Superpower. So, the book Costa Rican Ecosystems, edited by Dr. Maarten Kappelle, comes at an extraordinarily opportune time. The culmination of decades of scientific achievement and experience, it provides an intellectual template upon which sustainability can be built for Costa Rica. It also

xvi Foreword

serves as a model for an ecosystems overview that all nations should aspire to and emulate. When— not if— global sustainability is achieved, it will be recognized that one of the places that it started was in this remarkable country and with this equally remarkable book. Dr. Thomas Eugene (Tom) Lovejoy Senior Fellow, United Nations Foundation Professor of Environmental Science and Policy at George Mason University Member of the Council of the World Wildlife Fund (WWF-US) Washington, DC USA Dr. Thomas Eugene (Tom) Lovejoy.

Presentation

During the second half of the twentieth century and the first decade of the twenty-first century, Costa Rica’s natural environment underwent profound changes due to the socioeconomic development processes that took place. Costa Rica’s increasing hunger for food, water, energy, infrastructure, and urban development has had a considerable, negative impact on its ecosystems and the environmental services on which its population depends— though the magnitude of this impact may be less severe when compared to other countries or regions. This has become clear from global environmental evaluations like the 2006 Millennium Ecosystem Assessment (MA), a multi-stakeholder effort endorsed by the United Nations (UN). Moreover, on top of these negative pressures occurred a series of environmental problems triggered by modern climate change. In the environmental arena, and especially in the field of biodiversity, Costa Rica has made great strides to conserve and use its extraordinary natural richness in a smart way, thanks to its particular social and political conditions. Consequently, today more than 26% of its surface is managed under some kind of formally established public protection. Additionally, an approximate 2% is safeguarded in private reserves, while another 14% of privately owned land is maintained as forest through innovative funding schemes based on the concept of payments for environmental services (PES). Thanks to such incentives, Costa Rica has recovered a large portion of the dense forest cover that it harbored in previous decades, either through natural regeneration or by planting trees. In fact, the Costa Rican landscape has recently changed favorably due to this novel instrument. Simultaneously, scientific knowledge about biodiversity— especially at the species level— has increased significantly during the past two decades, thanks to efforts of national scientific institutions with support from external parties. The generation of information and knowledge on the environment in general and biodiversity in particular, as well as their use in public and informal education, has increased in an equally important manner in the public domain. As a result, Costa Rica’s society is now much more aware of the enormous biological richness that inhabits the country. Costa Ricans have become truly conscious about the need to protect the nation’s biodiversity and use it sustainably. These particular conditions have enabled the simultaneous xvii

development of the natural tourism sector as a key industry at national level. In fact, nature-based tourism has now turned into an important source of income to many Costa Ricans and has positioned the country as a truly green destiny in the world. At the same time the corporate sector is gradually becoming more involved in conservation efforts. Awareness about the need for corporate social responsibility (CSR) has increased among entrepreneurs. Now, they begin to understand that taking such responsibility is also in their own, for-profit interest. This change in attitude leads to innovative opportunities for action in the field of biodiversity conservation— action that had previously not been foreseen. Simultaneously, a modern political and legal framework for implementation is being developed, allowing the country to establish solid rules that guarantee the conservation, use, and equal distribution of benefits derived from its biodiversity. However, as Costa Rica’s program on the State of the Nation in Human Sustainable Development (Programa Estado de la Nación en Desarrollo Humano Sostenible) clearly states, at present the country is starting to face important internal and political conflicts related to the environment; the unsustainable use of land for urban, coastal, or touristic purposes; the generation of electricity; mining and oil exploration; and extensive export-driven agriculture, among others. The availability, quality, and quantity of suitable drinking water as well as the management of solid waste are also prime topics that attract considerable attention from civil society today. Never before has Costa Rica so much felt the need for a broad, knowledge-based, integrated vision on the use of its territory and natural resources. Above all, it is now much more aware of the need to develop and implement a fully integrated management approach, beyond the establishment of protected wildlife areas. Adopting such an approach is the key to managing conservation areas in a way that will guarantee the delivery of essential ecosystem services for human benefits in the coming future. That is exactly why the book Costa Rican Ecosystems appears at the right moment. Although some authors previously published essential works about the ecology and natural history of individual sectors of Costa Rica, no other volume has yet dealt with terrestrial, freshwater, and

xviii Presentation

marine ecosystems in a more holistic and integrated manner than this book, bringing together and analyzing the existing wealth of ecological information and knowledge now available— a feature that makes this volume a unique contribution to our shared knowledge. The editor of the book and author of various chapters therein, Dr. Maarten Kappelle, is highly qualified to lead and conduct the immense task of assembling a book of this proportion. He possesses a broad and in-depth knowledge of the country, both at the ecological and cultural level. Highly motivated, he lived and worked for long periods in Costa Rica and has shown a special appreciation for our country and its biodiversity. These characteristics allowed him to bring together a group of outstanding authors, environmental scientists and specialists alike, very familiar with this particular nation and knowledgeable about a wide range of its biodiversity aspects. This book will, without doubt, serve as a key piece of study and reference for all who are interested to learn about Costa Rican biodiversity and its conservation from a scientific angle. The volume has enormous educational value as it focuses on ecosystems on the basis of characteristics that are easily visible and understandable by any student, any individual citizen, or tourist. It will notably contribute to our capability to value the magnitude of Costa Rica’s natural richness, since its ecological perspective will allow the reader to visualize, understand, and better appreciate the extraordinary variety of landscapes and seascapes that thrive in this small corner of the world. It will be, for sure, an invaluable book that will serve much-needed land use planning efforts, taking into account

social, economic, and ecological dimensions. It will help ensure that we choose the appropriate type of resource use for each place, allowing current and future generations to enjoy Costa Rica’s biodiversity and essential ecosystem services on which we depend so strongly. Such are choices that ultimately will allow Earth’s evolutionary life processes to continue progressively in our beloved country and beyond. Dr. Rodrigo Gámez Lobo President and Former Director General of Instituto Nacional de Biodiversidad (INBio) Former Advisor to the President of the Republic of Costa Rica Former Director of the Escuela de Fitotécnia and Vice Rector of Research of the Universidad de Costa Rica Santo Domingo de Heredia Costa Rica

Dr. Rodrigo Gámez Lobo.

Preface

More than thirty years ago, in 1983, Daniel H. Janzen published his now classic book Costa Rican Natural History at the University of Chicago Press. In that magnum opus a total of 174 contributors shared with us their knowledge on Costa Rica’s biophysical aspects and the natural history of the cornucopia of plants and animals that inhabit this tiny tropical country. Until that crucial moment, only Leslie Holdridge’s Forest Environments in Tropical Life Zones: A Pilot Study (Holdridge et al. 1971) provided a national overview of diversity, though looking at the country’s forest types from a forester’s perspective. At the time Dan Janzen’s colossal volume appeared, remote areas of the country’s hinterland, such as the Atlantic slopes of the Cordillera de Talamanca, had not yet been inventoried in detail. Specific fields of study such as the marine realm or soil microfauna had received very little attention as yet. Innovative techniques ranging from the interpretation of satellite imagery and the use of radio collars to track vertebrates, to DNA sequencing and bar-coding were just being developed and far from being “common business practice.” Since the publication of Janzen’s monumental work hundreds if not thousands of scientific articles and technical reports on every aspect of Costa Rica’s biodiversity have seen the light, including the description of hundreds of new species, genera, and even new families of flowering plants such as the Ticodendraceae— literally a family of tico (i.e., Costa Rican) trees (Gómez-Laurito and Gómez 1991). In this context, it is worthwhile to mention the 1986 book Vegetación de Costa Rica by Luis Diego Gómez, to whom this book is dedicated. The publication of that work now almost thirty years ago represented another milestone in biological sciences in the country. It dealt with Costa Rica’s plant communities from the viewpoint of a taxonomist and biogeographer. However, most biological and ecological research conducted in Costa Rica during the last quarter of the twentieth century focused on selected species and their biotic and/or physical environment, often from a reductionist, organismic, or population biological viewpoint rather than from a holistic, ecosystem-based approach. These studies were mainly carried out at well-equipped facilities (see, e.g. Hartshorn 1983), including the OTS-administered biological stations at La Selva (Atlantic lowland rain forest in the xix

northeast), Palo Verde (Pacific wetlands along the Tempisque river), and Las Cruces (Pacific premontane forest in the south), the TSC-administered Monteverde research facility (montane forests in the Cordillera de Tilarán), the ACGmanaged Santa Rosa station (dry forests along Guanacaste’s northern Pacific coast), the UNA- and CATIE-managed site facilities in the Cordillera de Talamanca (montane oak forests near La Esperanza, San Gerardo de Dota, and Villa Mills, respectively), and marine biological stations such as the establishment at Punta Morales north of the city of Puntarenas. In the recent past research results from several of these places have been assembled in single volumes (McDade et al. 1994, on lowland rainforests at La Selva; Kappelle 1996, on montane oak forests in the Cordillera de Talamanca; Nadkarni and Wheelwright 2000, on cloud forests at Monteverde; Frankie et al. 2004, on seasonal dry forests in Guanacaste; Kappelle and Horn 2005, on alpine páramos; Wehrtmann and Cortés 2009, on marine biodiversity). Still, no single account had treated Costa Rica’s biodiversity in an ecosystemic and integrated manner or made an attempt to summarize the huge body of ecological knowledge that has appeared over the past decades throughout the country. Hence, twenty-five years after Janzen’s milestone book, I felt the need to produce a comprehensive volume that would look at Costa Rica’s biodiversity from an ecological perspective, paying extensive attention to the full range of the country’s major ecosystems in a holistic way: from lowland to highland, from dryland to wetland, from Atlantic to Pacific, from freshwater to brackish and salty, from land to sea, and from continent to oceanic island— covering the wide variety of ecosystems that are the home of Costa Rica’s extraordinary, alpha, beta, and gamma diversity. Thus, in 2005 I contacted the late Luis Diego Gómez Pignataro to discuss the idea. As Costa Rica’s most experienced, all-round vegetation scientist familiar with every corner of the country, he would be best positioned to serve as sparring partner and discuss the plan with me. I invited him to join the project and he gladly accepted. Immediately after, we proposed the idea to the University of Chicago Press, which enthusiastically joined the cause in 2006. Very sadly, shortly after, Luis became terminally ill. His worsened health condition did not allow him to become actively

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involved in the development of the book itself (see the dedicatory section “In Memory of Dr. Luis Diego Gómez Pignataro (1944– 2009)” in this volume). Since then it took nine years to come to the final product that is lying in front of us: the first scientific volume on Costa Rican ecosystems. Although the book is not meant to provide a definitive statement about Costa Rican ecosystems, it is meant to serve as a good start to the reader who wants to get a grasp of the unique ecological variety of one of the planet’s most species-dense countries, if not the densest. Dan Janzen, in the preface of his 1983 book Costa Rican Natural History, wrote: “I hope this book will be out of date in ten or twenty years; some sections were out of date as they were being written. Those who read it will make it obsolete. . . . I have been impressed with how fragmentary is the knowledge each of us has even of our own areas of specialization and of the organisms we are supposed to be familiar with. Rather than being scornful of this sorry state of tropical biology, however, I encourage the reader to work doubly hard to rectify it.” These same thoughts and words apply to this volume today. Hence, the editor hopes that this book will encourage young students to further investigate Costa Rica’s ecosystems and the species of which they are composed, their relations with other species and the environment, and the interaction with human society. The objective of this book is to introduce to the reader the entire range of principal ecosystems that dominate Costa Rica’s landscapes and seascapes: its dry, seasonally-moist, rain and cloud forests; its lowland and highland woodlands, and alpine páramos; its rivers and lakes; its bogs, marshes, and swamps; and its estuaries, mangroves, sandy and rocky beaches, coral reefs, pelagic seas, and unique oceanic island, Isla del Coco. These chapters are geophysically put in perspective by providing an overview of the country’s climate, geology, geomorphology, and soils. Each of the sixteen ecological chapters explores a particular type of ecosystem, discussing its physical environment, biogeography, species diversity, community composition, species interactions, structure and functioning, land use history, and conservation. By analyzing, integrating, and synthesizing data from literature, museum collections, observational measurements, and field experiments– from tissues to plots to landscapes– the authors provide a vast array of state-of-the-art information and knowledge necessary to understand the diversity and complexity of these ecological systems. The editor hopes that the readers will be able to visualize the continuum that exists among these ecosystems. Moreover, it is hoped that the book will trigger the curious among the readers to conduct much-needed innovative research that will fill the many gaps that remain in our understanding

of Costa Rica’s ecosystems. Similarly, the book is intended to motivate people in general to make an extra effort to conserve this country’s extraordinary biological riches in the long run, for people and nature alike. Without the active help and encouragement of many individuals and organizations the present book would not have seen the light. I thank the 65 contributors who collaborated with their chapters without charging any fee for their efforts. In particular I express my gratitude to the lead authors for their huge effort to develop the chapters as well as for their unparalleled patience awaiting final publication of the book: Alfredo Alvarado, Bob Lawton, Cathy Pringle, Dan Janzen, Deedra McClearn, Guillermo Alvarado, Jorge Cortés, Jorge Jiménez, José Vargas, Larry Gilbert, Michel Montoya, Quírico Jiménez, Sally Horn, and Wilberth Herrera. Numerous anonymous specialists are kindly thanked for their help in reviewing the twenty chapters on a voluntary basis. Costa Rican institutions like CATIE, INBio, Fundación MarViva, MINAET (and its predecessors SPN and MIRENEM), OTS, TSC, UCR, and UNA: all provided technical support to the project. INBio, TNC, and WWF— my employers over the past years— continually encouraged me to finish the book. I owe a special acknowledgment to the late Luis Diego Gómez for the many inspiring discussions we had about the idea that led to this book. I also would like to acknowledge the University of Chicago Press for its great interest in publishing the book. Particularly, I am thankful to Christie Henry, editorial director for sciences and social sciences at the press, who showed interest in the development of the book since the very beginning of this journey in 2006 and helped to make sure we got to the final stages of publishing in 2015. Amy Krynak assisted energetically in formatting the volume for publication at the press, while Mary Corrado was instrumental in copyediting all chapters in a very professional manner. Gary S. Hartshorn and an anonymous reviewer were so kind to take the time and effort to review the entire volume and provided many constructive comments that helped improve the manuscript as a whole. The Gordon and Betty Moore Foundation is much thanked for its generous financial contribution that made it possible to include a large series of color illustrations. A special thanks goes to Steve McCormick, Guillermo Castilleja, Jennifer Rae, and Cathy Manovi, who facilitated the Moore Foundation’s financial support. Finally, I am very grateful to Antoine Cleef and the late Adelaida Chaverri who first brought me to Costa Rica in 1985 to study its montane oak forests and páramos. I am indebted to the Dutch research funding organization NWO and Amsterdam-based UvA university that together funded

Preface xxi

part of my studies in Costa Rica. Rodrigo Gámez Lobo at INBio gave me in 1998 the opportunity to study Costa Rica’s ecosystems at a national scale. At the same time, my parents, Mary E. Mohr and the late Dirk Kappelle, supported me in every step along the road of life, enabling me to get to today’s result. Ultimately, it was my wife, Marta E. Juárez Ruiz, who encouraged me unconditionally during the past twenty-five years to make sure that the knowledge we generated on Costa Rica’s extraordinary nature was shared more broadly and made available to the people in the country. Costa Rican Ecosystems would not have come to fruition without her never-ending optimism, drive, and motivation. Now, it is up to the next generation— the generation of our two sons, Derk Frederik and Bernard Floris— to ensure that Costa Rica’s ecological systems will thrive well into the future, healthy and abundant, serving humankind in the twenty-first century. Dr. Maarten Kappelle Director of Programme Office Conservation Performance

at the World Wide Fund for Nature (WWF International), Gland, Switzerland, outposted in Nairobi, Kenya Adjunct Associate Professor in Geography at the University of Tennessee, Knoxville, TN, USA Visiting Professor at the UN-mandated University for Peace, Ciudad Colon, Costa Rica

Dr. Maarten Kappelle.

Abbreviations ACG: Área de Conservación Guanacaste (Guanacaste Conservation Area). Management unit of SINAC (Sistema Nacional de Áreas de Conservación), Costa Rica’s National System of Conservation Areas. CATIE: Centro Agronómico Tropical de Investigación y Enseñanza (Tropical Agronomical Center for Research and Education), Turrialba, Costa Rica. INBio: Instituto Nacional de Biodiversidad (National Institute for Biodiversity), Santo Domingo de Heredia, Costa Rica. MINAET: Ministerio de Ambiente, Energía y Tecnología (Ministry of Environment, Energy and Technology), San José, Costa Rica. MIRENEM: Ministerio de Recursos Naturales, Energía y Minas (Ministry for Natural Resources, Energy and Mines), San José, Costa Rica. NWO: Nederlandse Organisatie voor Wetenschappelijk Onderzoek

(Netherlands Organisation for Scientific Research), The Hague, the Netherlands. OTS: Organization for Tropical Studies, San Pedro de Montes de Oca, Costa Rica. SPN: Servicio de Parques Nacionales (National Park Service), San José, Costa Rica. TNC: The Nature Conservancy, Washington, DC, USA. TSC: Tropical Science Center, San José, Costa Rica. UCR: Universidad de Costa Rica (University of Costa Rica), San Pedro de Montes de Oca, Costa Rica, UNA: Universidad Nacional (National University), Heredia, Costa Rica. UvA: Universiteit van Amsterdam (University of Amsterdam), Amsterdam, the Netherlands. WWF: World Wide Fund for Nature, Gland, Switzerland.

References Frankie, G.W., A. Mata-Jiménez, and S.B. Vinson, eds. 2004. Biodiversity Conservation in Costa Rica: Learning the Lessons in a Seasonal Dry Forest. Berkeley: University of California Press. 341 pp. Gómez, L.D. 1986. Vegetación de Costa Rica. Vol. 1 of L.D. Gómez, ed., Vegetación y Clima de Costa Rica. With 10 maps (scale 1:200,000). San José: EUNED. Gómez-Laurito, J., and L.D. Gómez. 1991. Ticodendraceae: a new family of flowering plants. Annals of the Missouri Botanical Garden 78: 87– 88. Hartshorn, G.S. 1983. Plants: introduction. In D.H. Janzen, ed., Costa Rican Natural History, 118– 57. Chicago: University of Chicago Press. Holdridge, L.R., W.C. Grenke, W.H. Hatheway, T. Liang, and J.A. Tosi.

1971. Forest Environments in Tropical Life Zones: A Pilot Study. Oxford: Pergamon Press. 735 pp. Janzen, D.H., ed. 1983. Costa Rican Natural History. Chicago: University of Chicago Press. Kappelle, M. 1996. Los Bosques de Roble (Quercus) de la Cordillera de Talamanca, Costa Rica: Biodiversidad, Ecología, Conservación y Desarrollo. Amsterdam: University of Amsterdam. 336 pp. Kappelle, M., and S.P. Horn, eds. 2005. Páramos de Costa Rica. Instituto Nacional de Biodiversidad (INBio)— The Nature Conservancy— WOTRO Foundation. Santo Domingo de Heredia, Costa Rica: INBio Press. 767 pp. McDade, L.A., K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds.

xxii Preface 1994. La Selva: Ecology and Natural History of a Neotropical Rain Forest. Chicago: University of Chicago Press. Nadkarni, N.M., and N. Wheelwright, eds. 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. New York: Oxford University Press. Wehrtmann, I.S., and J. Cortés, eds. 2009. Marine Biodiversity of Costa Rica, Central America. Berlin: Springer 538 pp.

Chapter 1 Costa Rica’s Ecosystems: Setting the Stage

Maarten Kappelle1 We should preserve every scrap of biodiversity as priceless while we learn to use it and come to understand what it means to humanity. — Edward O. Wilson, Professor Emeritus, Harvard University No other area of equal size anywhere in America possesses so rich and varied flora, and none in North America is at all comparable in these respects. It is improbable that in any part of the Earth there can be found an equal area of greater botanical interest. . . . In few countries of the world, I believe, would it be possible to travel so much and find only pleasant and ever varied scenes, and be received everywhere with simple and sincere hospitality. — Paul C. Standley, in Flora of Costa Rica, October 12, 1937

Ecosystem Discovery, Exploitation, Conservation, and Sustainability Some twenty years after Christopher Columbus visited in 1502 the coast of today’s Puerto Limón on his fourth and final voyage to the New World, the Spanish conquistador Gil González D’Ávila, while on a royal expedition sailing from Panama to Nicaragua, named the country Costa Rica, or Rich Coast. He did so because of the golden objects that were used by pre-Columbian indigenous tribes for body decoration and rank distinction, including necklaces, nose plugs, ear plugs, bracelets, and bells (Quilter and Hoopes 2003). However, ultimately it was not the golden treasures that justified the name of Costa Rica, but rather its biological richess: its huge variety of life, piled up in a small corner of the world (Gómez and Savage 1983). Ever since foreign naturalists like Anders Sandoe Ørsted, William More Gabb, Karl Sapper, Karl Hoffmann, Alexander von Frantzius, Karl 1 World Wide Fund for Nature (WWF International), Gland, Switzerland; Department of Geography, University of Tennessee, Knoxville, Tennessee

3

Wercklé, and Henri François Pittier visited the country and were astonished by its rich flora and fauna, Costa Rica and its ecosystems have been considered by specialists and laymen a true Valhalla of biotic diversity in all its senses (Pittier 1908, Gómez and Savage 1983, Hartshorn 1983, Gómez 1986). However, over the past 150 years Costa Rica’s lush ecosystems have become more and more threatened, pricipally as a result of land conversion for cattle ranching, coffee growing, and large-scale banana production (Hall 1985). Particularly since World War II when the interest in precious hardwoods increased and construction of highways flourished (Merker et al. 1943), accelerated deforestation became the prime driver of biodiversity loss in the country (Sader and Joyce 1988). During the past few decades forest conversion together with other stress factors— such as climate change, overfishing, the introduction of aggressive invasive alien species, the construction of large infrastructure features such as roads and dams, sedimentation, environmental pollution, urban sprawl, and coastal encroachment— have begun to put ever-increasing pressures

4 Chapter 1

on the fragile cornucopia of Costa Rica’s ecological systems, impoverishing and reshaping them in already fragmented landscapes and seascapes. While during the second half of the twentieth century Costa Rica lost almost half of its forest cover, since the early 1970s to date (2015) the country has been able to save millions of hectares in 169 protected areas, ranging from absolute reserves and national parks to forest reserves and protective zones (Gámez and Ugalde 1988, Boza 1992, Wallace 1992, SINAC 2009, Obando 2011). Together, Costa Rica’s protected areas cover 26.2% of the country’s territory today. The development of the national park system initially occurred simultaneously with massive deforestation in unprotected areas, a phenomenon now known as the “Grand Contradiction” (Evans 1999). The first wildlife area that received formal protection was created in 1945. It concerned the montane oak forest zone just south of Cartago, along both sides of the InterAmerican Highway (Kappelle 1996). From 1969 to the late 1970s this and other early protected areas, including the Reserva Natural Absoluta Cabo Blanco and the Volcán Turrialba and Volcán Irazú national parks, were formally administered by the Departamento de Parques Nacionales. Then in 1977, protected area management passed on to the Servicio de Parques Nacionales (SPN), which was formally created as a specialized unit under direction of the Ministerio de Agricultura y Ganadería (MAG). Key protected areas like the now famous Cahuita, Chirripó, Corcovado, Santa Rosa, and Tortuguero national parks were created during that decade, as the environmental movement became stronger and focused hard on safeguarding the country’s last remaining wild places (Gámez and Ugalde 1988, Wallace 1992, Boza 1993). At the end of the next decade, in 1988, SPN was incorporated into the new Ministerio de Recursos Naturales, Energía y Minas (MIRENEM). Then, in 1995, new responsibilities were added while MIRENEM was restructured. It became the Ministerio del Ambiente y Energía (MINAE). In that same year, SPN was merged with both the Dirección General Forestal (DGF) and the Dirección General de Vida Silvestre (DGVS) into the innovative Sistema Nacional de Áreas de Conservación (SINAC), a subdivision of the young MINAE (Evans 1999). During the second administration of President Oscar Arias Sánchez (2006 to 2010) the telecommunications sector was added to MINAE, to become the Ministerio del Ambiente, Energía y Telecomunicaciones (MINAET). In 2013 MINAET became again MINAE, as the telecommunication department was moved to another ministry. As of 2014, MINAE is also referred to as the Ministerio del Ambiente, Energía, Aguas y Mares, recognizing

the growing importance of the freshwater and marine resources for the country. SINAC was foremost created to serve as a facilitating mechanism necessary to administer all protected areas in an integrated manner at regional level (SINAC 2009). In total, eleven Áreas de Conservación (ACs) were established as part of SINAC, covering the full territory of the country. Costa Rica’s 1998 biodiversity law (Ley de Biodiversidad) legally formalized and strengthened this organizational structure and its holistic, decentralized, and inclusive approach. Thanks to extraordinary efforts in the past, Costa Rica has now been able to devote nearly a third of its territory to the conservation into perpetuity of its rich biological diversity, spread over eleven conservation areas (for a more detailed historical account, see Wallace 1992, García 1997, Evans 1999, and Gámez 2003). Therefore, today Costa Rica serves as a successful model of biodiversity research and conservation. It is a country in which many innovative ideas were first conceptualized, tested, and implemented (Fournier 1991, Wallace 1992, Evans 1999). These ideas range from all-taxa biodiversity inventories (ATBI) ( Janzen and Gámez 1997) and biological prospecting meant to discover wild species with medicinal properties (Tamayo et al. 2004) to avant-garde bar-coding of plant and insect specimens in ex situ collections (Gámez 1999); from an out-of-the-box means of linking debt reduction with environmental protection measures through Debt-for-Nature Swaps proposed by Tom Lovejoy in 1984 (Thapa 1998) to revolutionary Payments for Environmental Services (PES; Pagiola 2008, and see Arriagada et al. 2012); and from ecosystem-based sustainable tourism models (Aylward et al. 1996) to leadership in climate change discussions (Castro et al. 2000), mostly recently about Reduced Emissions from Deforestation and forest Degradation (REDD and REDD+; Karousakis 2007). Hence, since the early 1970s Costa Rica has been at the forefront in developing and implementing new and bold ideas to study and safeguard its extraordinary biodiversity. Over the coming decades, such novel approaches will allow the country to catalyze its human sustainable development model based on twenty-first-century principles of a truly green economy. In this context it is important to mention that Costa Rica has announced its intention to become the first carbon dioxide– neutral country in 2030. Another very hopeful sign is the fact that Costa Rica has recently recorded a change from having a net loss of forests to having a net gain in forest area (UNEP/GRID-Arendal 2009): while in 1991, 29 percent (ca 14,000 km2) of Costa Rica’s land cover qualified as closed forest (Sánchez-Azofeifa et al. 2006), by 2010 thanks to forest-related interventions up to

Costa Rica’s Ecosystems: Setting the Stage 5

51 percent of its land area could be classified again as closed forest (UNEP/GRID-Arendal 2009, Stone 2011)— a unique success story at global level!

History of Costa Rica’s Biogeography To understand the diversity and complexity of Costa Rica’s ecosystems today, it is essential to get a grasp of their biogeographic history. When did these ecosystems actually originate and how did they develop over time? As Coates and Obando (1996) discussed in their treatment of the geologic evolution of the Central American Isthmus, its formation has indeed been a complex and extended process that stretched over the last 15 million years and had huge consequences to ocean circulation, global climatic patterns, biogeography, ecology, and the evolution of both terrestrial and marine organisms in the region (also, see Jones and Hasson 1985, and Stehli and Webb 1985). Today the rise of the isthmus is considered to be the culmination of an extended geologic history involving the growth and migration of the Central American volcanic arc, at the junction of the Pacific and Caribbean Plates, and its collision with South America (Coates and Obando 1996). The formation and closure of the Central American land bridge about 2.7 million years (Ma) triggered the migration of plants and animals from North America (the Nearctic region) into South America (the Neotropical region) and vice versa, contributing to today’s extraordinary isthmian biodiversity at all levels, from genes to landscapes (Rich and Rich 1983, Stehli and Webb 1985, Webb 2006). Recently, some authors concluded that the Central American closure took place some ten million years earlier (Montes et al. 2015). As a result land mammal faunas from North and South America mingled on a continental scale, including North American ungulates that found their way to South America (tapirs, deer, horses, pumas, canids, bears, and a number of rodents), while glyptodonts— more heavily armored relatives of modern armadillos— and giant anteaters (Myrmecophaga spp.), among others, migrated along the inverse route, from South to North America (Rich and Rich 1983, Webb 2006). Some families of northern land mammals diversified at moderate rates (Procyonidae, Felidae, Tayassuidae, and Camelidae), while others such as Canidae, Mustelidae, Cervidae, and especially Muridae, evolved explosively (Webb 2006). Today this hemispherical process of species migration is known as the Great American Biotic Interchange (GABI), which in fact was first observed by the nineteenth-century English naturalist Alfred Russell Wallace (1876).

At the same time, the Pliocene closure of the isthmus separated the Pacific and Atlantic Oceans that had been connected since the Mesozoic by an interoceanic seaway through the Central American volcanic island arc. As a result, two marine floras and faunas became disconnected, allowing evolution to take place among the now-separated Atlantic and Pacific species populations (Cronin and Dowsett 1996). On top of that, the occurrence of past glaciations on the highest mountains (Kappelle and Horn, chapter 15 of this volume), differences in seasonal patterns of rainfall superimposed on discontinuous mountain chains, temperature gradients changing over short altitudinal ranges (Herrera, chapter 2 of this volume), and the development of rich mineral soils on rugged terrain and lowland plains (Alvarado and Mata, chapter 4 of this volume), led to even higher levels of biotic diversity and ecosystem complexity (Burger 1980, Stehli and Webb 1985, Gómez 1986, Kappelle et al. 1992, Alvarado and Cárdenes, chapter 3 of this volume).

Costa Rican Biodiversity at the Species Level Over the past three decades, biodiversity inventories in Costa Rica and the world have increased and improved considerably, allowing us to make relatively good estimates of current species diversity (Groombridge 1992, Obando 2002). A recent review of Costa Rican species data shows that out of about 2 million species that have been discovered on Earth, around 95,000 are found in Costa Rica (Obando 2011). That is about 5% of all species officially known to exist on our planet. Similarly, it is expected that around half a million species thrive in Costa Rica, including all the species unknown until date. That is about 3.6% of the 14 million species that have been estimated to live on Earth (Obando 2002, 2011). Thus, it is believed that so far only 19% of all species living in Costa Rica have been formally discovered and scientifically described. This small percentage underlines the need to continue to invest in species inventories and— in the case of species new to science— prepare and publish formal species descriptions. However, the lack of trained taxonomists and curators needed to conduct the correct identification of biological specimens— a problem known as the Taxonomic Impediment and first observed by the International Union of Biological Sciences (IUBS) and its DIVERSITAS Programme— withholds the country from quickly raising the number of formally known native species, while limiting its ability to conserve, use, and share the benefits of its biological diversity in a socially just manner.

6 Chapter 1

Today, Costa Rica is home to at least 125 species of viruses, 213 Monera (among others, bacteria), 2,300 fungi (with ca. 700 Ascomycota and 1,300 Basidiomycota), 564 algae (including 205 microalgae), 11,467 plants including some 2,000 tree species, 670 Protozoa, 88 nematodes, 66,000 insects (including 16,000 Lepidoptera or butterflies), 1,550 mollusks, 916 fish (781 marine species and 135 freshwater fish), 189 amphibians, 234 reptiles, 854 birds, and 237 mammals of which 107 are bats and 20 are marine mammals (Herrera and Obando 2009). These data reveal that 75% of the 87,000 species known from Costa Rica actually are insects. It also demonstrates that almost 10% of all bird species in the world are indeed found in Costa Rica. Furthermore, Mug et al. (2001) report that a total of about 5,000 species (that is 5.7% of 87,000 known species) are coastal-marine in distribution, with at least 3,650 species known from the Pacific Ocean and coast, and over 1,325 species known from the Caribbean Sea and shores. These data demonstrate that the Pacific waters of Costa Rica are almost three times as rich in species compared with the country’s portion of the Caribbean Sea. In this regard, the reader should be aware that the 1,100 km Pacific coast line is five times as long as the Caribbean coast line (ca. 200 km), and that the Economic Exclusive Zone (EEZ) of Costa Rica amounts to ca. 570,000 km2 in the Pacific Ocean but extends over only approximately 24,000 km2 in the waters of the Caribbean Sea (Mug et al. 2001, Obando 2002). All together, Costa Rica’s marine territory is eleven times bigger than its land surface. On a global scale, Costa Rica is certainly among the twenty most species-rich countries (Groombridge 1992). At the same time, Costa Rica’s land surface covers a mere 51,100 km2, which corresponds to only 0.03% of the global land surface. Hence the notion, that Costa Rica is the world’s number one country in terms of species density (i.e., the number of species present per 1,000 km2; see García 1996, and Obando 2002). Although other so-called megadiverse countries do contain more species in absolute numbers (e.g., Australia, Brazil, Colombia, Indonesia, and Mexico), they are 22 (Colombia) to 150 (Australia) times bigger in size (measured as land surface). When looking at the potentially unique presence of these many species, it turns out Costa Rica is a country with moderate levels of endemism. This is due to the fact that important Costa Rican ecosystems are shared with neighboring countries: for instance, the dry forest of Guanacaste extends into northern Pacific Nicaragua, the northern Caribbean lowland rainforests of Sarapiquí and San Carlos are similar to forest types found across the border in the Atlantic sector of Nicaragua, and the montane forests and páramos of the southern highlands extend into the Panamanian sec-

tor of the Cordillera de Talamanca. However, still some 1,200 species of plants (that is, 12% of all plant species), including some 177 tree species, are unique to Costa Rica (Obando 2002). Similarly, around 14% of all freshwater fish species, 20% of amphibians, 16% of reptiles, 0.8% of birds, and 2.5% of mammals, are endemic to Costa Rica (Obando 2002). Areas richest in endemic plant species are the volcanic cordilleras (Guanacaste, Tilarán, and Central) and the Osa Peninsula. Other important endemic regions include the high Talamancas, the central Pacific sector, and the Pacific oceanic island Isla del Coco (Marco V. Castro C., pers. com.; Obando 2002). On the other hand, levels of endemicity— and species distributions in general— may be due to some kind of collection bias: historically, not all parts of the country have been sampled with the same level of intensity, and sites along easily accessible roads and near biological field stations may suffer from oversampling by taxonomists and other collectors (Marco V. Castro C., pers. com.). Unfortunately, many species thriving in Costa Rica are becoming threatened by a variety of stress factors mentioned earlier in this chapter. Obando (2011) estimates, that populations of about 2% of the species known from Costa Rica are severely under pressure, some of which are actually threatened with extinction. Amphibians are perhaps the species group that is most threatened; some species such as the golden toad (Bufo periglenes) are believed to have gone extinct over the past 25 years (Pounds 2001, Pounds and Crump 1994).

Costa Rican Biodiversity at the Ecosystem Level The thousands of native species (alpha diversity) that thrive in Costa Rica compose a wide array of complex ecological systems. In fact, all main terrestrial Central American ecosystems— that is, tropical rainforest, seasonally dry tropical forest, tropical cloud forest, temperate (oak) forests, and high-elevation ecosystems such as páramo— are found in tiny Costa Rica (Dirzo 2001). This country is therefore perhaps the best representative of Central America’s land-based ecodiversity. Its complex geological history, variety of climates, and topographic heterogeneity make it a kaleidoscope of terrestrial ecosystems found in the region (Burger 1980, Gómez 1986). On the salty side, the presence of estuaries, mangroves, coastal channels, sandy beaches, rocky intertidal zones, intertidal mud flats, seagrass beds, coral reefs, rodolith beds, pelagic systems, deep benthic zones, various kinds of islets, and a tropical fjord turn Costa Rica into a coastal-marine biodiversity paradise, a mecca for both oceanographers

Costa Rica’s Ecosystems: Setting the Stage 7

and marine biologists (Mug et al. 2001, Wehrtmann and Cortés 2009; and see various chapters by Cortés, this volume). Freshwater ecosystems are no less numerous, though less species-rich. Throughout the country, one can observe wetlands such as rivers and rivulets, lakes and lagoons, as well as swamps, marshes, and peatbogs. They occur in alpine páramos, in mountainous areas, along hilly terrains, in lowland regions, and in coastal zones. Environmental heterogeneity along gradients (beta diversity) and in and among broad landscapes and seascapes (gamma diversity) is overwhelming. One can take an imaginary walk from coast to coast, along a cross-section, starting at the dry Peninsula de Santa Elena along the northern Pacific coast where cacti locally dominate rocky beaches, through the seasonally dry forests of Guanacaste, on to the steep volcanic cordilleras with their epiphyte-laden montane cloud forests near Monteverde and subalpine dwarf forests at the summit of Volcán Barva; then hike towards the páramo patches and volcanic lakes at elevations over 3,000 m on top of Volcán Irazú and V. Turrialba, or further south at Cerro Chirripó, and walk down into the Atlantic zone with its lush premontane and lowland tropical rainforests and broad rivers meandering through the plains of San Carlos, Sarapiqui, and Limón; and then continue to the southeast through the dense, humid and hot forests along the lower slopes of the Cordillera de Talamanca, and end near Cahuita and Gandoca-Manzanillo where sandy palm beaches and coral reefs dot the coast line. Hence, over a length of a few hundred kilometers, one traverses the full array of tropical ecosystems, over land from ocean to ocean. Nowhere else in the tropics one can do such a complete “ecological triathlon,” while observing a dozen magnificent ecosystems and thousands of unique biological species!

Brief Overview of Existing Ecosystem Classifications in Costa Rica It is well known that species communities occur as continua, some species decreasing in importance as others become more common along environmental gradients. On the other hand, scientists and practitioners find it useful to classify assemblages of plants, animals, and even microorganisms into species communities and— at higher levels of organization— ecosystems. Graphic visualizations of community or ecosystem-level units as expressed in maps are essential to understand and delineate the geographic distribution of species combinations and landscape patches. Such spatial tools and related geographic information systems (GIS) are vital to revealing landscape patterns, assessing land cover change, conducting land use zoning, and con-

serving biodiversity along ecological gradients, among other actions (Savitsky and Lacher 1998). Edward O. Wilson defines biodiversity as “the totality of the inherited variation of all forms of life across all levels of variation, from ecosystem to species to gene.” In the case of Costa Rica, biodiversity at the species level has received relatively considerable attention from scientists (e.g., Janzen 1983, Gámez 1991, Obando 2002, Hammel et al. 2004, Wehrtmann and Cortés 2009, and see the website of the Costa Rican Instituto Nacional de Biodiversidad, INBio, at www.inbio.ac.cr). Not so the diversity at the level of ecosystems. Those few scholars who actually did study Costa Rican species communities or ecosystem-level units, however, did not necessarily agree on how they should be defined or classified (Gómez 1986). Hence, the historic development of ecosystem classifications and country-wide maps that use different hierarchical systems and distinct nomenclatures. Below, the most important ecological classifications and maps that exist for Costa Rica at a national level— in particular regarding its land-based vegetation— are briefly discussed. Although foreign scholars like Anders Ørsted, Karl Hoffmann, Helmuth Polakowsky, Karl Wercklé (1909), Otto Porsch, and Paul H. Allen each made an attempt to classify and describe (part of) Costa Rica’s vegetation and flora (Gómez 1986), it was not until Leslie R. Holdridge and his coworkers published their classic field study of Forest Environments in Tropical Life Zones (1971) that a full overview of all Costa Rica’s vegetation formations and their structure and composition was first assembled (see fig. 1.1.). Holdridge’s overview of Costa Rican vegetation was based on forest stand data collected in 1964– 1966. It had its roots in his earlier, more methodological studies (Holdridge 1947, 1967), which detailed the theoretical fundamentals of a global bioclimatic scheme for the classification of land areas known as life zones (Spanish: zonas de vida). The three climatic axes of the triangular system with its 30+ hexagons are defined by annual precipitation, mean annual biotemperature (based on temperature and the length of the growing season), and potential evapotranspiration ratio (PET) (Holdridge 1967). By incorporating biotemperature changes as they occur along an altitudinal gradient Holdridge followed in the footsteps of geographer Alexander von Humboldt: the German nineteenth-century naturalist was the first to notice, while traveling through the South American Andes, that tropical temperatures drop with increasing elevation above sea level and that vegetation changes accordingly (von Humboldt and Bonpland 1814). According to Holdridge’s assessment, Costa Rica’s small land surface is home to twelve life zones that include dry, moist, wet, and rain forests, altitudinally distributed over

8 Chapter 1

Fig. 1.1 Maarten Kappelle (left) and Leslie (Les) R. Holdridge (1907– 1999) in the garden behind Holdridge’s house in San Isidro de Heredia, Costa Rica. Photo taken by Mrs. Holdridge in April 1986.

tropical (i.e., lowland), premontane, lower montane, and montane belts (Holdridge et al. 1971, and see Hartshorn 1983). Additionally, six climatic transitions occur in the country, ranging from warm to cool-dry and cool-wet transitions. At elevations over 3,000 m (e.g, at the summit of Cerro Chirripó; see Kappelle and Horn, chapter 15 of this volume), Costa Rica’s only non-forest life zone is found: the sub-alpine rain páramo. To visualize the potential distribution of Holdridge’s life zones and transitions in Costa Rica, their extent was mapped by Holdridge’s colleague Joseph Tosi (1969), and thirty years later remapped with more precision and geographic detail by Rafael Angel Bolaños et al. (1999). Some ten years ago, descriptions of Holdridge’s life zones together with Tosi’s map served as key input data to determine the carbon absorption capacity of Costa Rican forests with the aim to facilitate negotiations for joint implementation projects within the framework of the Kyoto Protocol (Obando 2002), a key international agreement that focuses at stabilizing greenhouse gas (GHG) concentrations in the atmosphere at a level that would prevent dangerous anthropogenic interference with the climate system. Growing empirical evidence, however, has called into question the predictive power of the climate-based Holdridge model (Cornell 1998). As a reply to the life zone system, Luis Diego Gómez (1986) proposed a classification of 53 vegetation macrotypes (Spanish: macrotipos de vegetación) that are principally defined by vegetation morphol-

ogy (i.e., physiognomy), stand structure, species composition, and soil characteristics. An essential climate feature that the Holdridge system lacked but that was incorporated by Gómez, concerned the seasonal distribution of rainfall as expressed in the length of the dry season measured in months (Gómez 1986, and see Herrera 1986 and chapter 2 of this volume). Gómez’ approach was inspired by the kind of vegetation analyses conducted previously in other parts of the tropics by scholars like Beard (1944) and Grubb et al. (1963). It followed a floristic-ecological method to classify vegetation types and associations in the European plant sociological tradition of Braun-Blanquet (1932; and see Westhoff and Van der Maarel 1973). When possible, Gómez adopted the associated plant community nomenclature that was originally ratified during the Sixth International Botanical Congress held in 1935 in Amsterdam, the Netherlands (Gómez 1986). During the mid-1990s Gómez’ map of vegetation macrotypes (scale 1:200,000) proved extremely useful in assessing gaps in Costa Rica’s protected area system (García 1996)— much more than, for example, Savitsky et al.’s (1995) coarse map of Costa Rican habitats (scale 1:500,000). That gap analysis— known as the GRUAS I project— together with additional fieldwork in remote areas, led to the establishment of new nature reserves such as Parque Nacional Maquenque in northeastern Costa Rica, a park that attempts to protect the habitat of the endangered Great Green Macaw (Ara ambigua) (Chassot and Monge 2002). Complementary to Gómez’ national vegetation classification, Zamora et al. (2004) described a total of 24 geographically defined botanical or floristic regions present in Costa Rica. These floristic regions were mapped by Marco V. Castro Campos and colorfully published in Hammel et al. (2004). The result is very useful when locating plant species populations or herbarium collection sites. Seven years after Gómez’ classification of vegetation macrotypes he merged his plant ecological scheme with Wilberth Herrera’s (1986) elaborate climate types (also, see Herrera, chapter 2 of this volume). This integration led to the definition, classification, and mapping of Costa Rica’s biotic units (Spanish: unidades bióticas; Herrera and Gómez 1993). More than in the case of the vegetation macrotypes, the newly combined system took into account physiographic and climatic data, as well as distributional data on flora and fauna. Since the biotic unit itself was defined by its ecological and other biotic features it could easily be distinguished in the field and spatially visualized in a distribution map. During the late 1990s, the biotic units system was used to select novel collection sites necessary to complete Costa Rica’s national biodiversity inventory un-

Costa Rica’s Ecosystems: Setting the Stage 9

der the auspices of the Instituto Nacional de Biodiversidad (INBio) (Obando 2002). Following the creation of Costa Rica’s biodiversity law, INBio and SINAC/MINAE joined forces in 1998 and created the ECOMAPAS Project with Dutch governmental aid. Its purpose was to establish a decision-support tool that could monitor changes in terrestrial ecosystem cover at a national level and guide management for ecosystem health in protected areas and surrounding buffer zones. The project’s first step was a GIS-based mapping of ecosystems at a scale of 1:50,000 (Kappelle et al. 2003a). A set of four out of eleven Áreas de Conservación (ACs) were prioritized for mapping: Osa (ACOSA), La Amistad-Pacífico (ACLA-P), La Amistad-Caribe (ACLA-C), and Pacífico Central (ACOPAC). Mapping was done on the basis of the interpretation of 1995– 1996 aerial photographs at scales of 1:25,000 to 1:40,000 and produced by the German company Hansa-Luftbild using funding provided by the Global Environmental Facility (GEF). Applying the well-established Rapid Ecological Assessment (REA) methodology presented in Sayre et al. (2000), map data were verified through extensive ground-truthing in the field, which included hundreds of sample points in situ (Kappelle et al. 2003a). Ecosystem categorization followed UNESCO’s (1973) physiognomic vegetation classification system, which is grounded in the methodology proposed by Mueller-Dombois and Ellenberg (1974)— two scholars who built upon the legacy inherited from the plant sociologist Braun-Blanquet (1932). Then, with the aim to develop a thorough landscape-ecological classification sensu Troll (1939) and Zonneveld (1995), the ECOMAPAS team crossed vegetational data with a series of thematic layers covering geological units, land forms, soil types, temperature provinces, and rainfall regimes (Kappelle et al. 2003a, 2003b). So far, two printed volumes have been published within the ECOMAPAS framework: one covering the ecosystems of ACOSA (Kappelle et al. 2003b) and one focusing on systems found in a portion of ACOPAC— that is, the Rio Savegre watershed (Acevedo et al. 2002). Owing to limited resources, further hard-copy publication has been put on hold, but distributional data on ecosystems— now available for about half of the country and its ACs— can be easily accessed in digital formats through INBio’s website and SINAC/ MINAET. Only a few years ago (2007), a second national gap assessment was conducted to identify remaining weaknesses in Costa Rica’s protected area system. This process, known as GRUAS II, included terrestrial, freshwater, and marine components (SINAC 2007, Arias et al. 2008). The landbased analysis (including the land portion of Isla del Coco) was performed on the basis of a newly assembled map that

displayed the distribution of 33 so-called phytogeographic units (Spanish: mapa de unidades fitogeográficas) (Zamora 2008). These “coarse filter” units were the result of a GIS exercise in which the 53 vegetation macrotypes of Gómez (1986) were overlain on top of the 24 floristic regions of Zamora et al. (2004) (for details, see SINAC 2007, and Arias et al. 2008). Currently, the GRUAS II map of phytogeographic units is informing policy decision making to establish new protected areas and, above all, biological corridors that connect core areas (B. Herrera, Tropical Agricultural Research and Higher Education Center, CATIE, pers. com., and see Arias et al. 2008). An example of the latter is the Amistosa corridor initiative that links Parque Internacional La Amistad with the Peninsula de Osa (F. Carazo, The Nature Conservancy, pers. comm.). All of the above-mentioned classifications dealt with land-based systems, ranging from life zones, to vegetation (macro)types, biotic units, botanical regions, landscapeecological types, and ultimately, phytogeographical units. Almost none of them, however, addressed marine ecosystems, and only a few provided major details on freshwater systems. An example of the latter is Kappelle et al.’s (2003b) classification, mapping, and description of Osa’s freshwater and coastal-marine plant-dominated ecosystems. These included floating vegetation in freshwater lakes (e.g., Laguna Corcovado), Symphonia globulifera forest swamps, brackish Raphia taedigera palm swamps, flooded Acrostichum aureum fernlands, and Rhizophora mangle mangrove forests. Nomenclature of these aquatic ecosystem types followed a combination of UNESCO’s (1973) vegetation classification system and Cowardin et al.’s (1979) hierarchy of wetland types. Fortunately, there are a few more accounts that actually discuss aquatic ecosystems, though still in a concise fashion. For instance, Gómez (1984) provided an overview of aquatic plants and their habitats, while Jiménez (1994) described the mangrove ecosystems of the Pacific coast. Obando (2002), in turn, briefly listed the most important aquatic systems in the country. She reported that Costa Rica harbors some 350 wetlands that all in all make up for 7% of its territory. The most significant freshwater wetland types are flooded forests, swamps, marshes, bogs, lakes, and lagoons. Many of these wetland systems have been evaluated at the ecoregional level by The Nature Conservancy (TNC; 2009) with the aim to identify priority sites for freshwater conservation in Costa Rica and neighboring countries. The most significant coastal-marine ecosystems, on the other hand, have been briefly described by Mug et al. (2001). They cover mangrove systems, sandy beaches, coastal rock formations, estuaries, coastal channels and brackish lagoons (e.g., such as found in Parque Nacional Tortuguero),

10 Chapter 1

coral reefs, rocky reefs, island coasts, mud flats and rocky banks, pelagic and oceanic environments, deep sea benthic environments, and a kind of tropical, anoxic fjord (i.e., the Golfo Dulce in southern Costa Rica). Complementing the ecosystem-level outline of Mug and coworkers, Wehrtmann and Cortés (2009) provided a comprehensive overview of the species that inhabit the ecological systems of the seas and shores of Costa Rica (also, see several chapters by Cortés, this volume). Additionally, ecological data for Costa Rican portions of four coastal-marine ecoregions (Nicoya, Panama Bight, Isla del Coco, and Southwestern Caribbean) were recently analyzed by TNC (2008) to help select key areas for marine conservation purposes.

The Ecosystem Concept within the Context of this Book Strangely enough, so far no scientific book has dealt in an integrated manner with the full range of terrestrial, freshwater, and marine ecosystems that occur in Costa Rica. At the same time, none of the above-described classifications of forests, vegetation, land cover types, wetlands, and coastalmarine ecosystems have been formalized and officially adopted by the Costa Rican government or other national entities. Hence, there is a clear need to publish a book that provides an overview of Costa Rica’s main ecosystems by compiling what we know today about their physical setting, biogeography, species diversity, community composition, species interactions, structure, functioning, land use history, and conservation. Ecosystems have been defined by the Convention on Biological Diversity (CBD) as “dynamic complexes of plant, animal and micro-organism communities and their non-living environment interacting as a functional unit.” This definition is valid within the context of this book, applies well to all its chapters, and is in line with Eugene P. Odum’s key fundamentals of ecology (Odum 1971). In order to keep it simple, I decided to avoid the use of existing national ecosystem classification systems like those developed by Leslie R. Holdridge, Luis Diego Gómez, or Nelson Zamora. The main reason is that their classifications are too detailed within the scope of this book. At the same time, they do not treat marine ecosystems or discuss any freshwater system in an in-depth manner. Rather, I tried to use a higher level modus operandi, more or less close to the concept of the “biome” (Campbell 1996) and “ecoregion” (Brunckhorst 2000). However, following such an approach in its strict sense probably would have led to a classification too coarse for the purpose of this book. There are indeed only three ter-

restrial biomes occurring in Costa Rica: tropical rain forest, tropical dry forest, and tundra— the latter in a tropical fashion (that is, with a diurnal climate) and regionally known as páramo. Similarly, only five terrestrial ecoregions occur in the country if one excludes the mangroves (Olson et al. 2001). One of these is the “Talamancan montane forest,” which ranges from the volcanoes of southern Nicaragua southeastward across Costa Rica into central Panama (Olson et al. 2001). Hence, Olson et al. (2001) erroneously classify the volcanic cordilleras of northern and central Costa Rica as “Talamancan” and wrongly incorporate, under “montane forest,” the biome-level, tundra-like treeless páramos. The other four terrestrial ecoregions (sensu Olson et al. 2001) that are observed in Costa Rica and have been evaluated for conservation purposes by Calderón et al. (2004) are the Central American Dry Forest in Guanacaste (dealt with in this volume by Q. Jiménez et al. [chapter 9] and by D.H. Janzen and W. Hallwachs [chapter 10]), the Costa Rican Seasonal Moist Forest in the southern sector of Peninsula de Nicoya and in the Valle Central (see Q. Jiménez and E. Carrillo, chapter 11 of this volume), the Isthmian Pacific Moist Forest in the south including the Peninsula de Osa (L. Gilbert et al., chapter 12 of this volume), and the Isthmian Atlantic Moist Forest in the Caribbean lowlands that range from Upala and Los Chiles to Sixaola (D. McClearn et al., chapter 16 of this volume). Therefore, in this book I have included some fifteen large natural ecosystems that cover all of Costa Rica’s territorial lands and waters. Eight are terrestrial in distribution and correspond mostly to forests. The land-based ecosystem of the oceanic island Isla del Coco is treated as a distinct system (M. Montoya, chapter 8 of this volume), whereas montane forests along the volcanic cordilleras in the North (R. Lawton et al., chapter 13 of this volume) are considered distinctively from the montane forests found in the Cordillera de Talamanca (M. Kappelle, chapter 14 of this volume), as they clearly differ in structure and composition. Freshwater ecosystems, in turn, are separated in rivers (C. Pringle et al., chapter 18 of this volume), lakes (S.P. Horn and K. Haberyan, chapter 19 of this volume), and other wetlands like swamps, marshes, and bogs (J. Jiménez, chapter 20 of this volume). Coastal-marine ecosystems, on the other hand, are defined and discussed for the Pacific Ocean and Caribbean Sea (J. Cortés, chapters 5 and 17 of this volume), as well as more specifically for the estuary of the Golfo de Nicoya (J.A. Vargas, chapter 6 of this volume) and the oceanic waters around Isla del Coco ( J. Cortés, chapter 7 of this volume). In summary, the natural ecosystems dealt with in this book are as follows:

Costa Rica’s Ecosystems: Setting the Stage 11 Fig. 1.2 Map of the main terrestrial and marine ecosystems treated in this book. Freshwater ecosystems are embedded within the terrestrial units and have not been specifically indicated. Legend: 1. The terrestrial ecosystem of Isla del Coco. 2. The coastal-marine ecosystem of Isla del Coco. 3. The coastalmarine ecosystem of the Pacific Ocean. 4.  The seasonal dry forests of Guanacaste and Nicoya. 5. The seasonal forests of the central Pacific zone and Central Valley. 6. The southern Pacific lowland evergreen moist forest of the Peninsula de Osa and surroundings. 7. The montane cloud forests of the volcanic cordilleras. 8. The evergreen moist forests of the Caribbean lowlands. 9. The montane cloud forests of the Cordillera de Talamanca. 10. The alpine páramos of Costa Rica’s highlands. 11. The coastal-marine ecosystem of the Caribbean Sea. Map prepared by Marco V. Castro.

A) Terrestrial ecosystems: i) The terrestrial ecosystem of Isla del Coco; ii) The seasonal dry forests of Guanacaste and Nicoya in the northern Pacific lowlands; iii) The seasonal forests of the central Pacific zone and Central Valley; iv) The southern Pacific lowland evergreen moist forest of the Peninsula de Osa; v) The evergreen moist forests of the Caribbean lowlands; vi) The montane cloud forests of the volcanic cordilleras in the North; vii) The montane cloud forests of the Cordillera de Talamanca in the south; viii) The alpine páramos of Costa Rica’s highlands; B) Freshwater ecosystems: i) Costa Rican rivers; ii) Costa Rican lakes; iii) Costa Rican bogs, marshes, and swamps;

C) Coastal-marine ecosystems: i) The coastal-marine ecosystem of Isla del Coco; ii) The coastal-marine ecosystem of the Pacific Ocean; iii) The estuary of the Gulf of Nicoya; and iv) The coastal-marine ecosystem of the Caribbean Sea. The map provided in Fig. 1.2 clearly shows the distribution of the terrestrial and marine natural ecosystems at a national scale. Each ecosystem chapter of this book deals with one of these systems, evaluating its diversity and complexity, and discussing its resource use and conservation. The sequence in which they are presented reflects a journey over land and sea: a fly-over from the southwest to the northeast, from the land and waters of Isla del Coco towards the Pacific coast of continental Costa Rica, into the high cordilleras and down to the Atlantic forests, then into to the Caribbean lowlands and coast. Fig. 1.3 gives a good photographic impression of the variety of the ecological systems

Costa Rica’s Ecosystems: Setting the Stage 13

one may encounter when making such a Grand Tour across the seas, shores, and inlands of Tiquicia, as Costa Rica is often amically called by its inhabitants. This journey-wise sequence will allow the reader to get familiar with the ecological systems she or he may find in the field, when visiting rural regions and coastal zones, from west to east, from south to north, and vice versa. It will help her or him to understand the full range of varied seascapes and landscapes as they intergrade with each other. This touring approach was selected over a merely technical or even clinical overview of hierarchically categorized ecosystems, for such a framework would suggest the use of a thoroughly developed classification system— which is neither the case nor pretended by the editor. Before each of Costa Rica’s ecosystems is presented, three introductory chapters treat the non-biotic environment of the country: its climate, geology, and soils. Learning about Costa Rica’s geophysical factors, patterns, and processes is essential to understand the medium or entorno in which its ecosystems have developed over time, and how they function. All three chapters have been prepared by outstanding national scholars in physical sciences: Wilberth Herrera (climate), Guillermo Alvarado and Guaria Cárdenes (geology and geomorphology), and Alfredo Alvarado and Rafael Mata (soils). As the reader may have noted while interpreting the deliberations made in this chapter, this book’s emphasis is definitely not on man-made ecosystems or anthropic “biomes” such as croplands, rangelands, tree plantations, urban parks, or villages and dense settlements. However, such non-natural, semi-natural, and sometimes truly cultural ecosystems are occasionally treated within the scope of Fig. 1.3 Photographic impressions of Costa Rican ecosystems. First row (upper row): left: Cyathea treeferns at Isla del Coco; center: Porites-dominated coral reef at Isla del Coco; right: Punta Uvita south of Dominical along the Pacific shore showing the “tombolo,” a narrow sandbar that connects the reef to the coast. Second row: left: vegetated sedimentary rocks at Isla del Caño, Pacific Ocean; center: Pelliciera mangroves at Río Estero, close to Bahía Drake, Península de Osa; right: Raphia palm swamp in the Térraba-Sierpe national wetland, north of the Península de Osa. Third row: left: large buttresses at the base of a moist forest tree in Corcovado National Park, Península de Osa; center: wetlands along the Río Tempisque in Palo Verde National Park; right: dense moist forest at Carara National Park. Fourth row: left: mid-elevation cloud forest along the ridges of the Pacific south; center: Blechnum-dominated peatbog in the upper montane belt of La Amistad International Park; right: Chusquea-dominated páramo near Cerro Urán, Chirripo National Park. Fifth row (bottom row): far left: seasonal dry forest in April at Santa Rosa, Guanacaste; center left: Laguna Hule in the northern volcanic highlands; center right: lowland creek at La Selva in the Caribbean moist forest region; far right: Quercus-dominated montane forest near San Gerardo de Dota in the Cordillera de Talamanca. Photo credits— First row (upper row): left: Bárbara Sperl; center: Jorge Cortés; right: Yamil Sáenz. Second row: left: Jorge Cortés; center: Luis González; right: Luis González. Third row: left: Larry Gilbert; center: Garret Crow; right: Quírico Jiménez. Fourth row: left: Yamil Sáenz; center: Luis González; right: Felipe Carazo. Fifth row (bottom row): far left: Dan Janzen; center left: Kurt Haberyan; center right: Cathy Pringle; far right: Maarten Kappelle.

the predominant natural ecosystems that provide the matrix of human-influenced mosaics of landscapes or seascapes. Hence, human-influenced forest restoration, for instance, is discussed in detail in the chapters on seasonal dry forests of Guanacaste and Nicoya (Janzen and Hallwachs, chapter 10 of this volume). Similarly, human threats like deforestation or overfishing are treated extensively in chapters on montane forests (Lawton et al. [chapter 13] and Kappelle [chapter 14]) and coastal-marine ecosystems (chapters 5, 7, and 17 by Cortés and chapter 6 by Vargas), respectively. Future works, however, should make an attempt to assess, describe, and discuss much more specifically the man-made and often novel ecosystems that are spreading throughout the country (e.g., coffee and banana plantations, grasslands for dairy cattle, central parks in villages, dam reservoir waters, and fish ponds), and their impact on biodiversity (e.g., see Banks et al. 2013). An interesting example of a novel ecosystem is the young forest that is currently developing in the core area of INBioparque in Santo Domingo de Heredia. It is the result of human-assisted, accelerated restoration on a former coffee plantation. Many similar restoration efforts are underway elsewhere in the country. On a final note, it is important to mention that the contributors who prepared the chapters of this book include national and foreign scientists who are outstanding experts on the ecosystems they present and analyze. Their contributions are often based on many decades of intense field study that includes both observational and experimental research. Each of them has done a major job in compiling the current knowledge that has been generated over the past fifty years or so. Owing to their extraordinary efforts that knowledge is now made available to academic scientists, students, natural history guides, conservationists, educators, park guards, and visitors alike. The editor expresses the hope that this vast scientific knowledge, now integrated and available in a single, comprehensive volume, will serve all who are interested in understanding the diversity and complexity of these marvelous natural ecosystems— knowledge necessary to be able to safeguard and sustainably use Costa Rica’s natural riches. In this way, societies like Costa Rica’s will be able to work towards true sustainable development in sync with frameworks such as provided by The Future We Want 2 and the Sustainable Development Goals currently being implemented. 2 The Future We Want is the outcome document that was adopted by world leaders at Rio+20, the United Nations Conference on Sustainable Development (UNCSD) that was held in Rio de Janeiro, Brazil, 20– 22 June 2012. This global meeting took place precisely twenty years after the 1992 Rio Conference during which the Convention on Biological Diversity (CBD) was established.

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References Acevedo, H., J. Bustamante, L. Paniagua, R. Chaves, and F. Quesada. 2002. Ecosistemas de la Cuenca Hidrográfica del Río Savegre, Costa Rica. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio) and Ministerio de Ambiente y Energía (MINAE). 352 pp. Arias, E., O. Chacón, G. Induni, B. Herrera-F., H. Acevedo, L. Corrales, J.R. Barborak, M. Coto, J. Cubero, and P. Paaby. 2008. Identificación de vacíos en la representatividad de ecosistemas terrestres en el Sistema Nacional de Áreas Protegidas de Costa Rica. Recursos Naturales y Ambiente 54: 21– 27. Arriagada, R.A., P.J. Ferraro, E.O. Sills, K.P. Subhrendu, and S. CorderoSancho. 2012. Do payments for environmental services affect forest cover? A farm-level evaluation from Costa Rica. Land Economics 88: 382– 99. Aylward, B., K. Allen, J. Echeverría, and J. Tosi. 1996. Sustainable ecotourism in Costa Rica: the Monteverde Cloud Forest Preserve. Biodiversity and Conservation 5: 315– 43. Banks, J. E., L. Hannon, P. Hanson, T. Dietsch, S. Castro, N. Ureña, and M. Chandler. 2013. Effects of proximity to forest habitat on hymenoptera diversity in a Costa Rican coffee agroecosystem. Pan-Pacific Entomologist 89: 60– 68. Beard, J.S. 1944. Climax vegetation in tropical America. Ecology 25: 127– 58. Bolaños, R., V. Watson, and J.A. Tosi. 1999. Mapa Ecológico de Costa Rica (Zonas de Vida) según el Sistema de Clasificación de Zonas de Vida del Mundo de L.R. Holdridge. San Pedro de Montes de Oca, Costa Rica: Tropical Science Center ( TSC). Boza, M.A. 1992. Costa Rica National Parks. Madrid, Spain: INCAFO. 91 pp. Boza, M.A. 1993. Conservation in action: past, present, and future of the National Park System of Costa Rica. Conservation Biology 7(2): 239– 47. Braun-Blanquet, J. 1932. Plant Sociology: The Study of Plant Communities. (Transl. from German by G.D. Fuller and H.S. Conard. Original title: Pflanzensoziologie: Grundzüge der Vegetationskunde). New York: McGraw-Hill. 458 pp. Brunckhorst, D. 2000. Bioregional planning: resource management beyond the new millennium. Sydney, Australia: Harwood Academic Publishers. Burger, W.C. 1980. Why are there so many kinds of flowering plants in Costa Rica? Brenesia 17: 371– 88. Calderón, R., T. Boucher, M. Bryer, L. Sotomayor, and M. Kappelle. 2004. Setting Biodiversity Conservation Priorities in Central America: Action Site Selection for the Development of a First Portfolio. San José, Costa Rica: The Nature Conservancy ( TNC). 32 pp. Campbell, N.A. 1996. Biology. 4th ed. Menlo Park, CA: Benjamin/ Cummings. Castro, R., F. Tattenbach, L. Gámez, and N. Olson. 2000. The Costa Rican experience with market instruments to mitigate climate change and conserve biodiversity. Environmental Monitoring and Assessment 61(1): 75– 92. Chassot, O., and G. Monge. 2002. Great Green Macaw: flagship species of Costa Rica. PsittaScene 53: 6– 7.

Coates, A.G., and J.A. Obando. 1996. The geologic evolution of the Central American Isthmus. In J.B.C. Jackson, A.F. Budd, and A.G. Coates, eds., Evolution and Environment in Tropical America, 21– 56. Chicago: University of Chicago Press. Cornell, J.D. 1998. The status of the Holdridge life zone model on its 50th anniversary. In Abstracts of the Annual Meeting (August 2– 6, 1998) of the Association for Tropical Biology (ATB) and the American Institute of Biological Sciences (AIBS). Published as a supplement to Biotropica 30(2). Baltimore, MD. Cowardin, L.M., V. Carter, F.C. Golet, and E.T. LaRoe. 1979. Classification of Wetlands and Deepwater Habitat of the United States. Publication No. FWS/OBS-79/31. Washington, DC: Biological Service Program, US Fish and Wildlife Service. Cronin, T.M., and H.J. Dowsett. 1996. Biotic and oceanographic response to the Pliocene closing of the Central American Isthmus. In J.B.C. Jackson, A.F. Budd, and A.G. Coates, eds., Evolution and Environment in Tropical America, 76– 104. Chicago: University of Chicago Press. Dirzo, R. 2001. Ecosystems of Central America. In S.A. Levin, ed., Encyclopedia of Biodiversity. Vol. I, 665– 76. San Diego, CA: Academic Press. Evans, S. 1999. The Green Republic: A Conservation History of Costa Rica. Austin: University of Texas Press. 317 pp. Fournier, L.A. 1991. Desarrollo y Perspectivas del Movimiento Conservacionista Costarricense. San José, Costa Rica: Editorial de la Universidad de Costa Rica (EUCR). 113 pp. Gámez, R. 1991. Biodiversity conservation through the facilitation of its sustainable use: Costa Rica´s National Biodiversity Institute. Trends in Ecology and Evolution 6: 377– 78. Gámez, R. 1999. De Biodiversidad, Gentes y Utopías: Reflexiones en los 10 Años del INBio. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Gámez, R. 2003.The Link between Biodiversity and Sustainable Development: Lessons from INBio’s Bioprospecting Program in Costa Rica. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Gámez, R., and A. Ugalde. 1988. Costa Rica´s National Park System and the preservation of biological diversity: linking conservation with socio-economic development. In F. Almeda and C.M. Pringle, eds., Tropical Rainforests: Diversity and Conservation, 131– 42. San Francisco: California Academy of Sciences. García, R. 1996. Propuesta Técnica de Ordenamiento Territorial con Fines de Conservación de Biodiversidad en Costa Rica: Proyecto GRUAS. San José, Costa Rica: SINAC, MINAE. 114 pp. García, R. 1997. Biología de la Conservación y Áreas Silvestres Protegidas: Situación Actual y Perspectivas en Costa Rica. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Gómez, L.D. 1984. Las Plantas Acuáticas y Anfibias de Costa Rica y Centroamérica. San José, Costa Rica: Editorial Universidad Estatal a Distancia (EUNED). Gómez, L.D. 1986. Vegetación de Costa Rica: Apuntes para una Biogeografía Costarricense. San José, Costa Rica: Editorial Universidad Estatal a Distancia (EUNED).

Costa Rica’s Ecosystems: Setting the Stage 15 Gómez, L.D., and J.M. Savage. 1983. Searchers on that rich coast: Costa Rican field biology, 1400– 1980. In D.H. Janzen, ed., Costa Rican Natural History, 1– 11. Chicago: University of Chicago Press. Groombridge, B. 1992. Global Biodiversity: Status of the Earth’s Living Resources. World Conservation Monitoring Centre ( WCMC). New York: Chapman and Hall. 585 pp. Grubb, P.J., J.R. Lloyd, T.D. Pennington, and T.C. Whitmore. 1963. A comparison of montane and lowland rain forest in Ecuador. I. The forest structure, physiognomy, and floristics. Journal of Ecology 51: 567– 601. Hall, C. 1985. Costa Rica, a Geographical Interpretation in Historical Perspective. Boulder, CO: Westview. 348 pp. Hammel, B.E., M.H. Grayum, C. Herrera, and N. Zamora. 2004. Manual de Plantas de Costa Rica. Vol. 1: Introducción. Monographs in Systematic Botany from the Missouri Botanical Garden 97: 1– 300. Hartshorn, G.S. 1983. Plants: introduction. In D.H. Janzen, ed., Costa Rican Natural History. Chicago: University of Chicago Press. Herrera, A., and V. Obando. 2009. Algunos datos sobre biodiversidad de Costa Rica. In SINAC (Sistema Nacional de Áreas de Conservación). IV. Informe de País sobre la implementación del Convenio sobre la Diversidad Biológica. SINAC. San José, Costa Rica. Accessed October 22, 2011: http://www.inbio.ac.cr/estrategia/default.html Herrera, W. 1986. Clima de Costa Rica. San José, Costa Rica: Editorial Universidad Estatal a Distancia (EUNED). Herrera, W., and L.D. Gómez. 1993. Mapa de Unidades Bióticas de Costa Rica. Scale 1:685,000. US Fish and Wildlife Service— TNC— INCAFO— CBCCR— INBio— Fundación Gómez-Dueñas. San José, Costa Rica. Holdridge, L.R. 1947. Determination of world plant formations from simple climatic data. Science 105(2727): 367– 68. Holdridge, L.R. 1967. Life Zone Ecology. San José, Costa Rica: Tropical Science Center. Holdridge, L.R., W.C. Grenke, W.H. Hatheway, T. Liang, and J.A. Tosi. 1971. Forest Environments in Tropical Life Zones: A Pilot Study. Oxford: Pergamon. 735 pp. von Humboldt, A., and A. Bonpland. 1814. Relation Historique du Voyage aux Régions Équinoxiales du Nouveau Continent fait en 1799, 1800, 1801, 1802, 1803 et 1804. Paris: Dufour. Janzen, D.H., ed. 1983. Costa Rican Natural History. Chicago: University of Chicago Press. Janzen, D.H., and R. Gámez. 1997. Assessing information needs for sustainable use and conservation of biodiversity. In P.M. Hawksworth and S. Dextre Clarke, eds., Biodiversity Information: Needs and Options, 21– 29. Wallingford, Oxon, UK: CAB International. Jiménez, J.A. 1994. Los Manglares del Pacífico de Centroamérica. Heredia, Costa Rica: Editorial Fundación Universidad Nacional. 352 pp. Jones, D.S., and P.F. Hasson. 1985. History and development of the marine invertebrate faunas separated by the Central American Isthmus. In F.G. Stehli and S.D. Webb, eds., The Great American Biotic Interchange, 325– 55. New York: Plenum. Kappelle, M. 1996. Los Bosques de Roble (Quercus) de la Cordillera de Talamanca, Costa Rica: Biodiversidad, Ecología, Conservación y Desarrollo. Amsterdam: Universidad de Amsterdam. 336 pp. Kappelle, M., A.M. Cleef, and A. Chaverri. 1992. Phytogeography of Talamanca montane Quercus forests, Costa Rica. Journal of Biogeography 19(3): 299– 315.

Kappelle, M., M. Castro, H. Acevedo, P. Cordero, L. González, E. Méndez, and H. Monge. 2003a. A rapid method in ecosystem mapping and monitoring as a tool for managing Costa Rican ecosystem health. In D.J. Rapport, W.L. Lasley, D.E. Rolston, N.O. Nielsen, C.O. Qualset, and A.B. Damania, eds., Managing for Healthy Ecosystems, 449– 58. Boca Raton, FL: Lewis. Kappelle, M., M. Castro, H. Acevedo, L. González, and H. Monge. 2003b. Ecosystems of the Osa Conservation Area, Costa Rica. Bilingual ed. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio) and Ministerio de Ambiente y Energía (MINAE). 496 pp. Karousakis, K. 2007. Incentives to Reduce GHG Emissions from Deforestation: Lessons Learned from Costa Rica and Mexico. Paris: Organisation for Economic Co-operation and Development (OECD). 50 pp. Merker, C.A., W.R. Barbour, J.A. Scholten, and W.A. Dayton. 1943. The Forests of Costa Rica: A General Report on the Forest Resources of Costa Rica. Washington, DC: Forest Service of the US Department of Agriculture (USDA) and Office for the Coordinator of Inter-American Affairs. 84 + 49 pp. Montes, C., A. Cardona, C. Jaramillo, A. Pardo, J.C. Silva, V. Valencia, C. Ayala, I.C. Pérez-Angel, L.A. Rodríguez-Parra, V. Ramírez, and H. Niño. 2015. Middle Miocene closure of the Central American Seaway. Science 348(6231): 226–29. Mueller-Dombois, D., and H. Ellenberg. 1974. Aims and Methods of Vegetation Ecology. New York: John Wiley and Sons. Mug, M., M.A. Bolaños, J. Sheffield, and F. Liebinger. 2001. Diagnóstico sobre la Investigación Marino-Costera en Costa Rica: Informe final. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio) and Ministerio de Ambiente y Energía (MINAE). 31 pp. Obando, V. 2002. Biodiversidad en Costa Rica: Estado del Conocimiento y Gestión. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). 81 pp. Obando, V. 2011. Algunos datos sobre la biodiversidad en Costa Rica. Lecture held at Instituto Nacional de Biodiversidad (INBio). Santo Domingo de Heredia, Costa Rica. Odum, E.P. 1971. Fundamentals of Ecology. 3rd ed. Philadelphia: Saunders. 574 pp. Olson, D.M., E. Dinerstein, E.D. Wikramanayake, N.D. Burgess, G.V.N. Powell, E.C. Underwood, J.A. D’Amico, I. Itoua, H.E. Strand, J.C. Morrison, C.J. Loucks, T.F. Allnutt, T.H. Ricketts, Y. Kura, J.F. Lamoreux, W.W. Wettengel, P. Hedao, and K.R. Kassem. 2001. Terrestrial ecoregions of the world: a new map of life on Earth. BioScience 51(11): 933– 38. Pagiola, S. 2008. Payments for environmental services in Costa Rica. Ecological Economics 65: 712– 24. Pittier, H. 1908. Ensayo sobre las Plantas Usuales de Costa Rica. Washington, DC: H.L. and J.B. McQueen. Pounds, J.A. 2001. Climate and amphibian declines. Nature 410: 639– 40. Pounds, J.A., and M.L. Crump. 1994. Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conservation Biology 8: 72– 85. Quilter, J., and J.W. Hoopes. 2003. Gold and Power in Ancient Costa Rica, Panama, and Colombia. Washington, DC: Dumbarton Oaks Publications. 428 pp.

16 Chapter 1 Rich, P.V., and T.H. Rich. 1983. The Central American dispersal route: biotic history and paleogeography. In D.H. Janzen, ed., Costa Rican Natural History, 12– 34. Chicago: University of Chicago Press. Sader, S., and A. Joyce. 1988. Deforestation rates and trends in Costa Rica, 1940– 1983. Biotropica 20: 11– 19. Sánchez-Azofeifa, G.A., R.C. Harris, and D.L. Skole. 2006. Deforestation in Costa Rica: a quantitative analysis using remote sensing imagery. Biotropica 33(3): 378– 84. Savitsky, B., and T.E. Lacher Jr., eds. 1998. GIS Methodologies for Developing Conservation Strategies: Tropical Forest Recovery and Wildlife Management in Costa Rica. New York: Columbia University Press. Savitsky, B.G., D. Tarbox, D. van Blaricom, T.E. Lacher, Jr., and J. Fallas. 1995. Habitats of Costa Rica: an annotated map. Scale 1:500,000. Strom Thurmond Institute and Archbold Tropical Research Center, Clemson University. Clemson, SC. Sayre, R., E. Roca, G. Sedaghatkish, B. Young, S. Keel, R. Roca, and S. Sheppard. 2000. Nature in Focus: Rapid Ecological Assessment. Washington, DC: The Nature Conservancy ( TNC) and Island Press. 182 pp. SINAC (Sistema Nacional de Áreas de Conservación). 2007. GRUAS II: Propuesta de Ordenamiento Territorial para la Conservación de la Biodiversidad de Costa Rica. Volumen 1: Análisis de Vacíos en la Representatividad e Integridad de la Biodiversidad Terrestre. San José, Costa Rica: SINAC, Ministerio de Ambiente y Energía (MINAE). 100 pp. SINAC (Sistema Nacional de Áreas de Conservación). 2009. IV Informe de País sobre la implementación del Convenio sobre la Diversidad Biológica. San José, Costa Rica: SINAC. Accessed October 22, 2011: http://www.inbio.ac.cr/estrategia/default.html Standley, P.C. 1937. Flora of Costa Rica, part I. Chicago: Field Museum of Natural History. Stehli, F.G., and S.D. Webb, eds. 1985. The Great American Biotic Interchange. New York: Plenum. Stone, S. 2011. Forests in a Green Economy. Presentation on World Environment Day, June 5, 2011. Economics and Trade Branch, United Nations Environment Programme (UNEP). Geneva, Switzerland. Tamayo, G., L. Guevara, and R. Gámez. 2004. Biodiversity prospecting: the INBio experience. In A.T. Bull, ed., Microbial Diversity and Bioprospecting, 445– 49. Washington, DC: ASM. Thapa, B. 1998. Debt-for-nature swaps: an overview. International Journal of Sustainable Development & World Ecology 5(4): 249– 62. TNC (The Nature Conservancy). 2008. Evaluación de Ecorregiones Ma-

rinas en Mesoamérica: Sitios Prioritarios para la Conservación en las Ecorregiones Bahía de Panamá, Isla del Coco y Nicoya del Pacífico Tropical Oriental, y en el Caribe Suroccidental de Costa Rica y Panamá. San José, Costa Rica: The Nature Conservancy ( TNC). 165 pp. TNC ( The Nature Conservancy). 2009. Evaluación de Ecorregiones de Agua Dulce de Mesoamérica: Sitios Prioritarios para la Conservación en las Ecorregiones de Chiápas a Darién. San José, Costa Rica: The Nature Conservancy ( TNC). 515 pp. Tosi, J.A. 1969. Mapa Ecológico de Costa Rica, Basado en la Clasificación Vegetal Mundial de L.R. Holdridge. Scale 1: 750,000. San Pedro de Montes de Oca, Costa Rica: Tropical Science Center (TSC). Troll, C. 1939. Luftbildplan and ökologische Bodenforschung. Zeitschrift der Gesellschaft für Erdkunde zu Berlin 7– 8: 1– 58. UNEP/GRID-Arendal. 2009. Change Forest Cover Costa Rica. UNEP/ GRID-Arendal Maps and Graphics Library. Accessed August 18, 2011: http://maps.grida.no/go/graphic/change-forest-cover-costa -rica UNESCO (United Nations Educational, Scientific and Cultural Organization). 1973. International Classification and Mapping of Vegetation. Paris: UNESCO. Wallace, A.R. 1876. The Geographical Distribution of Animals, with a Study of the Relations of Living and Extinct Faunas as Elucidating the Past Changes of the Earth’s Surface. New York: Harper and Brothers. Wallace, D.R. 1992. The Quetzal and the Macaw: The Story of Costa Rica’s National Parks. San Francisco: Sierra Club Books. 222 pp. Webb, S.D. 2006. The great American biotic interchange: patterns and processes. Annals of the Missouri Botanical Garden 93(2): 245– 57. Wehrtmann, I.S., and J. Cortés, eds. 2009. Marine Biodiversity of Costa Rica, Central America. Berlin: Springer. 538 pp. Wercklé, C. 1909. La Subregión Fitogeográfica Costarricense. San José, Costa Rica: Tipografia Nacional. 55 pp. Westhoff, V., and E. van der Maarel. 1973. The Braun-Blanquet approach of phytosociology. In R.H. Whittaker, ed., Manual of Vegetation Science. Vol. 5: Junk, 619– 726. The Netherlands: The Hague. Zamora, N. 2008. Unidades fitogeográficas para la clasificación de ecosistemas terrestres en Costa Rica. Recursos Naturales y Ambiente 54: 14– 20. Zamora, N., B.E. Hammel, and M.H. Grayum. 2004. Vegetation. In B.E. Hammel, M.H. Grayum, C. Herrera, and N. Zamora, eds. Manual de Plantas de Costa Rica. Vol. 1: Introducción. Monographs in Systematic Botany from the Missouri Botanical Garden 97: 91– 216. Zonneveld, I.S. 1995. Land Ecology. Amsterdam: SPB Academic. 199 pp.

Chapter 2 Climate of Costa Rica

Wilberth Herrera1

Introduction Costa Rica is a territory located in the Central American isthmus, between 8º 22’ 26” and 11º 13’ 12” North latitude and 82º 33’ 48”and 85º 57’ 57” West longitude. It is bounded on the north by Nicaragua (300 km), on the southeast by Panama (363 km), on the east by the Caribbean Sea (212 km), and on the south and west by the Pacific Ocean (1,016 km). The country covers a total area of 51,100 square kilometers, of which 50,980 km2 are continental territory, and 120 km2 are insular territories, notably Chira Island (43 km2) located in the Gulf of Nicoya and Cocos Island, a 24-km2 territory of volcanic mountain origin in the Pacific Ocean, 498 kilometers off the coast of the Osa Peninsula (Punta Llorona), at 5º 33´ North latitude and 87º 03´ West longitude. Despite its small size, 95 Climate Groups (Herrera 1986) and 55 Biotic Units (Herrera and Gómez 1993) have been identified in the country, ranging from the sub-moist dry and very warm climate of the lowlands of Guanacaste Province to the very wet, cold climate of the Talamanca Mountain Range. The three main factors that determine Costa Rica’s climate are its orography, its latitude, and the fact that it is an isthmus or land bridge.

northeast and east of this system is the Caribbean slope, with an area of 24,395 km2, and to the west and southwest is the Pacific slope with a coverage of 26,585 km2. In the case of both slopes, 51% of the territory corresponds to warm lands below 300 meters elevation. This mountainous feature, together with the other orographic systems that run parallel to the coastline and intercept air masses coming from both oceans, produces very different climatic characteristics in a territory as small as Costa Rica. Within a single slope, along a stretch of only 14 kilometers but with an altitudinal difference of 700 meters, moisture gradients vary from humid to pluvial; the dry period ranges from zero to five months; the sheets of rain vary from 1,900 to 7,600 mm, and there is a gradient of 180 to 318 rainy days. Other climatic elements, such as solar radiation and hours of sunlight, are highly influenced by the configuration of the orographic system. Windward slopes and mountain passes are generally very cloudy sites, where hours of sunlight are less than 50% of what they would normally be on the basis of their latitudinal position. Considerable amounts of cloud form above 2,200 meters and water deficit conditions and high radiation rates may occur, along with strong winds, mainly during the period of January, February, March, and April.

Climate and Orography

Climate and Latitudinal Position

The country is divided into two parts of almost equal size by a central mountain range that runs from northwest to southeast and rises to an elevation of 3,819 meters. To the

Costa Rica is located in the Equatorial Tropical belt with a median latitude of 10º North. This means that the sun’s rays attain zenith positions twice a year (April and August), with twelve hours of sunlight per day. Monthly thermal variation is less than 4ºC and the coasts are affected by the

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Costa Rican Coastal Current in the Pacific, and by a branch of the union of the North Equatorial Current and the South Equatorial Current in the Caribbean Sea (Martínez 1970). Owing to its latitudinal position, the atmospheric systems that determine the country’s thermal and pluvial regimes are the Intertropical Convergence Zone (ITCZ), cold fronts, the easterly waves, and marine and terrestrial breezes.

continental divides with light rains and drizzle, but produce clear, rain-free skies in the North Pacific, the Central Pacific, and the Central Valley regions. By contrast, the South Pacific region may experience isolated storms coming from the Pacific Ocean, even when the Caribbean is under the influence of a cold front. Easterly Waves

Intertropical Convergence Zone

The Intertropical Convergence Zone (ITCZ) is the area of interaction where the northeastern Trade Winds of the Northern Hemisphere meet the southeastern Trade Winds of the Southern Hemisphere (Zárate 1978). The ITCZ is a convergence zone of up to 200 km in width where cloud systems develop that are composed of layers or tiers of cumulonimbus, cumulus, altostratus, or other clouds, which generate strong rains, storms, turbulence, and winds predominately from the southwest (Equatorial Westerlies or “anti-trades” winds). The ITCZ shifts from north to south and vice versa, depending on the zenith position of the sun. It affects Costa Rica, particularly the Pacific slope, with copious and strong rains in the afternoons during the wet season from April to December. During the months that the country is influenced by the ITCZ, winds from the southwest blow along the entire Pacific slope, especially in the afternoons. These winds are weak, but they are heavily laden with clouds. As the ITCZ weakens or is displaced farther to the south of Costa Rica, the trade winds gather strength, blowing from the east and northeast, generating a water deficit on the Pacific slope and persistent rains on the Caribbean slope, mainly in the months of November, December, July, and August. Cold Fronts

At the beginning of the Northern Hemisphere winter, and as the Bermuda Anticyclone (Bermuda High) is displaced farther to the south of its usual position (30º N), the ITCZ weakens, and trade winds from the northeast affect the whole of Central America, pushing modified cold front air masses that generate strong precipitation and floods on Central America’s Caribbean slope. According to Martínez (1970), these polar air masses become warmer and acquire greater moisture when they move through the Gulf of Mexico, but maintain some of their original conditions when they cross the Mexican Meseta. If they enter Costa Rica, they can cause rains for nearly 24 hours a day during three consecutive days, saturating the soil and causing floods with substantial losses in the productive sector. As these air masses rise they shower the hills, mountain passes, and

Easterly waves are atmospheric disturbances that are characteristic of the tropical region and result from the elongation of cyclones, which sporadically generate convergence, instability, and bad weather, especially from June to October. These are disturbances of the trade winds that do not cross the Intertropical Convergence line (Andrade 1968). According to Chorley and Barry (1972), the easterly waves are closed low pressure zones in the middle troposphere. Behind the trough or thalweg (the deepest parts of a valley or watercourse), convective systems and storms develop that affect large areas of the Caribbean slope for one or two days. The rest of the territory is affected by the same phenomenon but with less intensity in temporal, quantitative, and spatial terms. The Isthmian Effect

The Costa Rican territory is influenced by both the Atlantic and the Pacific Oceans and, due to the narrowness of its territory (minimum 119 km, maximum 464 km), the atmospheric systems that originate in the Atlantic affect the Pacific region within a matter of hours, and the systems that station themselves in the Pacific can alter weather conditions on the Caribbean slope; however, the central mountainous system exerts a barrier effect on wind flow, cloudiness, and rains, giving rise to a mosaic of climates and ecosystems. For example, according to Costa Rica’s National Meteorological Institute (IMN), in July 1979 the country was influenced 61% of the time by an atmospheric condition originating in the Pacific Ocean, 29% by one in the Atlantic Ocean, and the rest of the time (10%) by a mixed condition. The degree of modification exerted by the continental territory on the air masses that cross it can be expressed using an index of continentality (terrestrial coefficient; +) or oceanicity (maritime coefficient; − ). The continental index ranges from 0 to 100% and the oceanicity index from 0 to − 20%. Herrera (1986) reports an extreme continentality index of +4.7% in Alajuela, a town located in the center of the country between the mountain chains, and an oceanicity index of − 10.6% in Sanatorio Durán, a site on the southern slope of the Cordillera Central (Costa Rica’s central mountain range).

Climate of Costa Rica 21

Temporal and Spatial Climate Variations in Costa Rica A general outline follows on the temporal and spatial variations in temperature, solar radiation and hours of sunlight, precipitation, and relative humidity in Costa Rica. The presented analysis includes all available data up to 2004, from more than 600 stations of the National Meteorological Institute (IMN), the Costa Rican Electricity Institute (ICE), and the National Aqueduct and Sewerage System (AyA). Temperature

The mean annual temperature varies from 27.6º C on the North Pacific coast and 26ºC on the Caribbean coast, to 6º C on Cerro Chirripó, the highest peak in the country (3,819 m). The annual thermal gradient is 5.7º C for every 1,000-meter increase in altitude on the Pacific slope, and 5.2º C for every 1,000-meter increase in altitude on the Caribbean slope. Minimum temperature extremes of − 3º C have been recorded in areas above 3,000 meters, and maximum extremes of 41ºC in the hot, dry lowlands of the Tempisque River Basin. The mean monthly temperature oscillation does not exceed 4ºC between the hottest months— usually March or April with zenith sun positions— and November, the coolest month. Figure 2.1 shows the hourly temperature variations on mountain peaks, on plains, and in valleys. Hours of Sunlight and Solar Radiation

At 10º mean latitude for Costa Rica, and in the absence of cloud cover, the sun is above the horizon for 11.41 hours on the winter solstice (December 22) and 12.58 hours on the summer solstice ( June 21). However, abundant cloud cover, particularly from 600 to 2,200 meters, reduces hours of sunlight by at least 50% throughout the Caribbean slope, and in some areas the daily mean is less than 2.5 hours during periods of strong rain activity. If there is less

sunshine due to the presence of clouds, the radiation is also reduced. At the top of the atmosphere above the 10th parallel, the rate of solar radiation varies from 37.5 megajoules (MJ) per square meter in April to 30.7 MJ/m2 in November; however, the total daily average recorded is 23 MJ/m2 in the dry season and the minimum is 13 MJ/m2 at very cloudy sites. Radiation rates are also affected by the inclination and orientation of hillsides. For example, on the summer solstice, a 30º north-facing slope receives 29 MJ/m2 (clear sky) while a south-facing slope would receive 16 MJ/m2. This situation gives rise to hillside microclimates that are particularly important for biodiversity, especially above 3,000 meters elevation. Figures 2.2 and 2.3 show monthly patterns of solar radiation and hours of sunlight at sites with opposite climates. Precipitation

Annual sheets of rain vary from 1,300 millimeters in the dry climates of Guanacaste Province to 7,467 mm in the watershed of the Río Grande de Orosí on the Caribbean slope, where there is no dry season and precipitation exceeds potential evapotranspiration during every month of the year. The monthly and hourly rainfall patterns are very variable, depending on the location— the Caribbean slope or Pacific slope, mountain passes, continental divides, sites that are windward or leeward to the trade winds, and the position of the Intertropical Convergence Zone. In continental and insular areas, there are three precipitation regimes (Fig. 2.4): the Pacific, the Atlantic, and the Coastal Atlantic. The Coastal Atlantic regime comprises the coastal strip and the plains. A dry season does not occur in this regime; however, rainfall decreases considerably in March, April, September, and October. Precipitation occurs during the night and the morning, but does not have a defined pattern during the diurnal period. The Atlantic Regime, characteristic of areas from 500 to 2,700 meters elevation on the Caribbean slope, receives

Fig. 2.1 Mean hourly temperatures at continental divides, plains, and valleys.

22 Chapter 2 CARIBLANCO, CARIBBEAN SLOPE Lat. 10º16 Long 84º12W. Altitude: 970 m.

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50

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40

10 8 6 4 2 0

30

Radiation (MJ/m2) 16 Hours of sunlight12

% sunlight % extra-terrestrial

20

Radiation

10 J

F M A M J

J A S O N D J

0

Fig. 2.4

Pluviometric regimes of Costa Rica.

Fig. 2.5

Rainy days (precipitation >0.1 mm).

month Radiation (MJ/m2)

Sunlight (daily hours)

% sunlight

% extraterrestrial radiation

Fig. 2.2 Monthly variation in solar radiation and hours of sunlight at the cloudiest site in Costa Rica.

lowlands, it rains only 60 days per year, with a minimum of one day in January to 27 days in October. Some of the rainiest sites are located on the continental divides below 2,500 meters, some in mountain passes, and others on hillsides that are perpendicular to the trade wind flow (Fig. 2.5).

Fig. 2.3 Monthly variation in solar radiation and hours of sunlight at the sunniest site of Costa Rica.

maximum rainfall in the afternoon and the early hours of the evening in the months of May, June, July, August, September, October, and November. From December to April, the rains are distributed over 24 hours of the day, with a maximum at night. The Pacific regime is characterized by rainfall during the afternoons and the early hours of the evening in the months of April, May, June, July, August, September, October, November, and December. The entire Pacific slope and the plains of Los Guatusos are affected. On the mountain summits of both slopes, the pluvial regime is a mixture of both regimes. In Costa Rica there are very marked contrasts in the monthly and annual rainfall levels and in the number of rainy days (precipitation ≥ 0.1 mm). At the rainiest site (Río Grande de Orosí basin) there is activity on 325 days of the year, with a minimum of 22 days in January and 31 days in September. At the least rainy site in the Guanacaste

Relative Humidity

Average monthly relative humidity in these climates varies between 65 and 90%, and average hourly relative humidity varies from 52 to 98% (Fig. 2.6). In sites above 3,000 meters, in the period February– April, with little cloud cover, hourly relative humidity drops to 20 or 25%, favoring desiccation and the propagation of forest fires. The same situation occurs in the Central Valley, between Turrúcares and Alajuela, during the same period. In the narrow valleys and lowlands of the South Pacific, leeward to the trade winds, morning cloud banks form, an indication of the high relative humidity rates above 90%. The morning fog phenomenon in the valleys and plains is partly explained by the accumulation of cold air in the thalwegs, weak winds, soil humidity that is always near field capacity, and the presence of vegetative cover. In Costa Rica’s páramos— areas above 3,200 m— in calm wind conditions, the necessary hygrothermic conditions are generated for white frosts (hoarfrosts) and black frosts on more than 34 days from December to April. A

Climate of Costa Rica 23

Fig. 2.6

Hourly relative humidity at continental divides, valleys, and plains.

black frost causes the death of a plant or its sensitive parts, due to cold exposure. This limits the growth of arboreal vegetation above 3,300 meters elevation (Herrera 2005). Hydric Balance

The comprehensive relationship between land-atmosphere systems is expressed using soil moisture balance, an approach that allows us to determine potential and actual evapotranspiration rates, levels of water deficits and surpluses, periods of field capacity, periods of moisture extraction, and hydric recharge seasons. Using this method, it is possible to integrate and quantify the behavior of the climatic elements and their effects on different ecosystems. In different regions of Costa Rica, soil climatology conditions are generally analyzed to a depth of one meter, using the model developed by Thornthwaite and Mather (1955, 1957) and the graphic modeling of Rolim et al. (1998) to examine climatic hydric balance. In this study, a conditional drought period is when there is a water deficit in the soil but the permanent wilting point has not been reached, and absolute drought is the period when water reserves have fallen below the permanent wilting point value. The water deficit is the difference between the water that is actually evapotranspirating and the maximum that could evapotranspirate. Water deficits occur when rains and water reserves are not sufficient to satisfy the climatic demand (potential evapotranspiration).

Climate Regions San Carlos Plains and Los Guatusos Plains

Annual precipitation in the San Carlos and Los Guatusos plains ranges from 2,500 to 4,000 mm, with a considerable decline in the rains during the months of March, April, and May. The need for water (potential evapotranspiration),

Fig. 2.7 2004).

Monthly water balance for the San Jorge de Los Chiles station (1980–

according to climate, ranges from 116 millimeters in January to 165 mm in May, for a potential sheet of rain of 1,618 mm per year. One balance for San Jorge (Fig. 2.7) indicates that vegetation with a rhizosphere at one meter depth suffers a water deficit after the sixth day without rain, a situation that occurs in February. In March and April, the deficit is so great that water reserves fall below the wilting point, giving rise to an absolute drought. For May and June the soil recharges moisture, and by the end of June there may already be a small water surplus, which is maintained for a period of seven consecutive months (June– December). Tortuguero Plains

The plains of Sarapiquí, Tortuguero, Guápiles and Matina have abundant rainfall, which ranges from 3,000 to 6,000 mm annually. Precipitation occurs on more than 170 days of the year; however, in March and April the amount of rain and the number of rainy days decline considerably, forcing the vegetation to extract moisture from the soil, which is then recharged in the next month. Although the monthly balances do not indicate the presence of absolute drought, this phenomenon occurs with some recurrence. For example, in the decade 1993– 2003, absolute droughts were recorded in March, April, and May 1994; and in January and March of 1998, a year that was under the influence of the warm phase of the El Niño Southern Oscillation (ENSO), also referred to as El Niño. On the hot and wet lands of the plains, beginning with the soil at field capacity, the vegetation experiences deficit following the fifth day without rain. The extraction of moisture occurs in March; recharge occurs in April, and the rest of the year there is a water surplus in the soil (Fig. 2.8). Occasionally deficits may occur in September and/or October.

24 Chapter 2

Fig. 2.8

Water balance of the Tortuguero Plains.

Fig. 2.9

Water balance of Valle de la Estrella.

From December to February, the soil can remain saturated with pools or puddles with the passage of modified cold fronts that contribute copious and persistent rains for three consecutive days. Southern Caribbean

The small coastal plains of the Southern Caribbean, located between the 10th parallel and the border with Panama, have a climatic and edapho-climatic regime that is different from the rest of the Caribbean slope. Here there are two peaks of pluvial activity, one in July and the other in November, altered by three water deficit periods. Mean annual precipitation ranges from 1,800 to 3,500 mm. The water balance (Fig. 2.9) indicates that the rains are insufficient to cover potential evapotranspiration in the months of March, May, September, and October, and that there is a water deficit, mainly in March. Average water reserves are always maintained well above the wilting point; however, the absence of rains can provoke an absolute drought phenomenon in this region, of the same frequency and magnitude as occurs on the Tortuguero Plains— in other words, with a probability of twice every ten years. The amount and distribution of the monthly rains is not sufficient to recharge soils to field capacity during seven months of the year. If the Caribbean slope were to be affected by droughts as a result of global climate change, the soil climatology of the southern Caribbean could suffer a major impact. South Pacific Plains

The Coto 47 station, located in the lower watershed of the Río Coto Colorado, represents in part the soil climatology conditions that prevail on most of the western coast

Fig. 2.10

Water balance of Valle de Coto Colorado.

of Golfo Dulce; a very warm, wet territory with precipitation from 3,000 to 6,000 mm, with potential needs below 1,800 mm. During the months of January, February, and March, intense evapotranspiration reduces water levels below the wilting point, and the entire region is affected by the absolute drought phenomenon. In April and May, the rains exceed needs and recharge occurs until mid-May, a period when the water surplus begins to increase, with peaks of 458 mm in October. The surplus infiltrates to deep layers and/or runs off via the drainage network. Excess water in the soil occurs over nine months: from May to December, with a total amount of 2,349 mm (Fig. 2.10). Some areas in the South Pacific region— on the plains between the north coast and the Brunqueña Range— have very

Climate of Costa Rica 25

Fig. 2.11

Water balance of Piedras Blancas, South Pacific.

special climates without dry seasons. This situation occurs because of the sheltered conditions provided by the high Talamanca Mountains and the Brunqueña Range against the trade winds from the north and northeast. This favors the incursion of a moist breeze from the Pacific throughout the year, although with less frequency from January to April, which generates convective and orographic rains year-round as it tries to rise up the Brunqueña Range. One station that is typical of this condition is Piedras Blancas (Fig. 2.11). Mean monthly values indicate that a deficit does not occur, but the sequential balances reveal that once every three years water deficits occur in January, February, or March. The Térraba Basin

The Térraba Basin covers an area of 5,079.4 km2 and contains the El General Valley and the Valley of Coto Brus. It is bounded on the north by the Talamanca Mountain Range, with maximum elevations of 3,820 meters; to the south, the Cal Range and the Brunqueña Range separate it from the Pacific Ocean. This geographic situation produces a Pacific-type precipitation regime in the high, middle, and lowland areas of the basin. The Pindeco station in the Buenos Aires district is a very good example of the functioning of soil climatology, principally at 200 to 1,000 meters elevation (Fig. 2.12). Mean precipitation in the basin ranges from 1,800 mm at Maíz de Boruca on the leeward side of the Cal Range, to 7,000 mm on the southern Talamanca slopes. At Buenos Aires, annual mean precipitation is 3,317 mm; water needs reach 1,721 mm, varying from 119 mm in November to 170 mm in March, a month of high temperatures, elevated sun positions, and low relative

Fig. 2.12

Water balance at Buenos Aires, Río Grande de Térraba Basin.

humidity. By mid-December, soil moisture falls rapidly and gives rise to a conditional drought, which is accentuated in the months of January, February, and March, attaining levels of absolute drought. The rains start in April and the soils begin to recharge moisture in mid-May, when they begin to reach field capacity and there is excess water for the next seven months, for a total of 1,750 mm. According to the classification system of Thornthwaite and Mather (1955, 1957), the aridity at Buenos Aires is low (9% of the evapotranspiration potential) and the surplus is very large (109% of annual evapotranspiration). Continental Divides

Above 3,000 meters elevation, climate conditions can be very changeable within a period of hours. Between the months of December and March, Irazú Volcano, Turrialba Volcano, and all the continental divide regions of the Talamanca Cordillera are affected by strong trade winds from the north and northeast, and by abundant fog, rain, and drizzle. However, for several days or hours, the weather can become sunny and windy, with relative humidity below 35%, high evapotranspiration rates, and no rain. These are times of soil water deficits (Fig. 2.13), very low temperatures, black and white frosts, and possibly forest fire propagation. By contrast, during the rest of the year, cloudy and very cloudy skies predominate with low rates of evapotranspiration and cold, moist winds. Central Pacific Plains

The Central Pacific Plains, between the Tulín and Térraba rivers, are slightly or moderately arid. The drought here is not as severe as on the plains and hills of Guanacaste

26 Chapter 2

Fig. 2.13

Water balance of Irazú Volcano, continental divide.

Fig. 2.15

Water balance at San José, Río Grande de Tárcoles Basin.

rainfall for the entire Pacific slope of Costa Rica has been recorded, with an annual precipitation of 6,500 mm. Monthly precipitation varies from 109 (March) to 1,027 mm (October). Conditions similar to this also occur in the hills of the western slope of the Corcovado Peninsula in the South Pacific region. Río Grande de Tárcoles Basin

Fig. 2.14

Water balance at Puerto Quepos, Central Pacific.

province, nor is it as slight as the drought that occurs in the Coto Colorado valley. The hydric balance at Puerto Quepos shows seven months of water surplus and four months of absolute drought. According to the classification system of Thornthwaite and Mather (1955, 1957), the climate is very wet, with a small water deficit and a surplus that exceeds needs by 116% (Fig. 2.14). In the Central Pacific region the mountain chains run parallel to the coast and at a distance of less than 15 km from the shore. These cordilleras provoke intense orographic rains, mainly when a hurricane is present in the Caribbean. Precipitation can exceed 300 mm in one day and, as a consequence, the soils become saturated with pools or puddles for periods of two to three days, mainly in September and October. At Naranjillo, at 700 m elevation, the most intensive

The Río Grande de Tárcoles Basin encompasses an area of 2,116 square kilometers, with the Central Mountain Range to the north, the Talamanca Range to the south, and the Aguacate Hills on the west. Nearly the entire area has a Pacific regime climate; however in the mountain passes and on the peaks of the Central Mountain Range, the climatic condition is a mixture of the Atlantic mountain regime and that of the Pacific, with rains throughout the year and at any hour. Precipitation in the Tárcoles Basin varies from 1,600 mm in Santa Ana, to 4,650 mm in Gallito, on the continental divide of the Cordillera Central. The thermic, pluviometric, and soil climatology gradients vary considerably from north to south and vice versa. For example, in the country’s capital city, San José, there is a pronounced dry season from December to April (Fig. 2.15), with an absolute drought during four consecutive months. Surplus water in the soil occurs over six consecutive months, from June to November. If the country is affected by the warm phase of the El Niño or ENSO phenomenon, soil moisture can decrease until it attains the conditional drought category in July or August, during the short dry period known as the Veranillo de San Juan. In the case of the Gallito Station (2,120 m elevation) located at a distance of 18 km northwest of San José, there is no dry season and a surplus, on average, is present every month.

Climate of Costa Rica 27

Fig. 2.16

Water balance at Bagaces, Baja del Río Tempisque Basin.

North Pacific

The North Pacific Region includes the Río Tempisque basin (5,460.2 km2), the Nicoya Peninsula, and part of the dry coastal strip to the east of the Gulf of Nicoya. The Pacific precipitation regime predominates in nearly the entire region, with afternoon rains in the period from May to November. However, in the mountain passes, and on the continental divide of the Guanacaste Mountain Range and the Tilarán or Minera Range, where maximum elevations do not exceed 2,000 meters, a mixed rain regime occurs, in-between a mountain Atlantic and a Pacific regime. From November to February, rains and drizzle fall on these peaks and mountain passes from air masses transported by the trade winds. The Föhn effect leaves copious rains on the windward side (Caribbean slope) and near the divide; however, below 600 meters on the leeward side, clear skies predominate with strong winds, low relative humidity, high temperatures, and dry soils. From May to November, the entire region receives moderate rains, interrupted by the normal occurrence of the Veranillo de San Juan or Canícula in July and August. Annual precipitation varies from 1,200 to 4,000 mm, from zero in January to 700 mm in October. In September and October, the presence of low pressure systems in the Pacific or hurricanes in the Caribbean gives rise to rains that persist for three days, known as temporales, which are often accompanied by flooding episodes. In the month of April, with zenith sun positions, moderate to weak winds, and low relative humidity, potential evapotranspiration reaches 190 mm per month. The annual amount of this same element— potential evapotranspiration— exceeds 1,900 mm in some sites such as Filadelfia and Nicoya. The influence of El Niño can

Fig. 2.17 Water balance at Santa Cruz, the boundary between dry and moist climates of the North Pacific.

trigger periods of water deficit throughout the lower and middle watershed for 33 consecutive months. In the southern part of the peninsula the rains are more abundant and the dry episodes are less severe than in the rest of the Northern Region. The monthly humidity balance of Bagaces, a site at 90 meters elevation, reflects the soil-related climatology of areas with less pluvial activity in Costa Rica (Fig. 2.16). These soil-related climatic conditions are (1) uninterrupted water deficit for eight months (November, December, January, February, March, April, July, August); (2) absolute drought for five consecutive months: December, January, February, March, and April; (3) uninterrupted water recharge for four months: May and June, September and October; and (4) only 75% of annual water needs (1,883 mm) are satisfied. Soil-related climatology conditions in the moist and submoist climate regions of the North Pacific are differentiated from those that prevail at Bagaces (sub-moist dry climate). The absolute drought begins in December and ends in April; the soil recharges in May, June, July, and August. There is a surplus in only two months: September and October (Fig. 2.17).

Perspectives on Climate Change and Ecosystems in Costa Rica2 Past climate change in Costa Rica has been documented by Islebe and Hooghiemstra (1997) who studied the presence and abundance of fossil pollen in soil cores from montane 2 This chapter’s section on Perspectives on Climate Change and Ecosystems in Costa Rica was prepared and contributed by Maarten Kappelle.

28 Chapter 2

(2,300 m) peatbog locations in the Cordillera de Talamanca (Trinidad, La Chonta). These palynologists noted that Central American climate change during the mid-Holocene seems more affected by changes in humidity than temperature. They reconstructed distribution maps of paramó and montane vegetation in Costa Rica for periods between 10,000 and 18,000 years before present. Their data indicate that during the Last Glacial Maximum a paramó vegetation corridor existed between Costa Rica and Panama. At the same time, it seems that future climate change will be significant in Costa Rica. Recent studies on modern climate change in the country suggest the possibility of a twodegree increase in temperature by the middle of the twentyfirst century in tropical forest regions, and an increase of 1ºC in tropical cloud forests (Pounds et al. 1997, 1999, Karmalkar et al. 2008). Should this trend be consolidated, the existing cloud forest patches in Costa Rica would be located 200 meters higher than their current positions and tropical forests would tend to occupy more territory, between 3,100 and 3,400 meters elevation (Lawton et al. 2001, Nair et al. 2003). As a result, the current area of páramo vegetation would be reduced to a small, restricted area between 3,400 and 3,820 meters elevation; by the middle of the century, only the area of Cerro Chirripó would offer suitable climate conditions that would allow the survival of páramo vegetation in Costa Rica (Herrera 2005). In a detailed simulation for doubled atmospheric carbon dioxide concentration (2 x CO2) conditions in tropical montane cloud forests like those in Costa Rica, Still et al. (1999) found that the relative humidity surface is shifted upwards by hundreds of meters during the dry winter season when these forests typically rely mostly on moisture from cloud contact. At the same time, these authors noted an increase in the warmth index that could imply an increased level of evapotranspiration. According to these authors, this combination of reduced cloud contact and increased evapotranspiration could have serious conservation implications, given that these ecosystems typically harbor a high proportion of endemic species and in Costa Rica are often situated on mountain tops or ridge lines. Enquist (2002) predicted regional impacts of climate change on the geographical distribution and diversity of tropical forests in Costa Rica. On basis of climate change scenarios she concluded that elevation-associated life zones and ecosystems in Costa Rica may be particularly vulnerable to future climatic changes. This is also true for lowland seasonally dry forest. Geographical regions in Costa Rica that contain these life zones are likely to warrant special management and conservation attention in the event of predicted climate change, she pointed out. The small patches of middle-elevation cloud forests that

are currently found on mountain chains or on isolated peaks, on both the Caribbean and the Pacific slopes, will be replaced by tropical lowland vegetation. This is the case of the Nicoya Peninsula, the Central Pacific, and the South Pacific. Other mountain chains with cloud forests at lower elevations today, such as the Sierra Minera de Tilarán, are already reporting the loss of amphibian species due to global warming and to the altitudinal migration of the level of the condensation line (Pounds & Crump 1994, Pounds et al. 1997, 1999, Lawton et al. 2001, Ray et al. 2006). The degree of impact that climate change is having on ecosystems is highly variable, both spatially and temporally, and depends on the location of the ecosystem with respect to the mountain chains, directions of the dominant winds, land use, proximity to the sea, elevation, and soil moisture retention capacity, among other factors. Future changes in temperature and precipitation could alter cloud cover at the vegetation level and seriously affect mountain ecosystems (Lawton et al. 2001, Ray et al. 2006, Karmalkar et al. 2008). The disappearance or reduction of cloud forest would also cause a reduction in the water volumes of rivers on the Pacific, which benefit from the cloud forests’ sponge effect, capturing passing clouds and/or favoring condensation, mainly during low water periods (Lawton et al. 2001). It is assumed that in the lowlands, where moist and wet forests predominate, and to a lesser extent, in the sub-moist dry forests, evapotranspiration will increase and thus the current boundaries could be displaced to one side or the other, depending on the variation in annual precipitation. However, the variation could be of lower impact than in the sub-tropical thermal, temperate, cold temperate and boreal provinces, where altitudinal variation implies major climate changes in reduced spaces. Much more integrated climatological research is needed to better understand the full impact of modern climate change on Costa Rican ecosystems and human society. A holistic, interdisciplinary approach will be essential to get a full picture of human-driven climate change in the twentyfirst century. Only by understanding the full scope and impact of current and potential climate change on our lives, in every sense, will we be able to mitigate and manage adaptively, thus ensuring a sustainable future for both mankind and nature in biodiverse tropical countries like Costa Rica. To mitigate modern and future climate change in Costa Rica— and hence safeguard the country’s rich biological diversity— it will be crucial to develop and apply sciencebased, integrated systems and tools. One key example is presented by Castro et al. (2000) who discuss Costa Rica’s policy framework that provides an appropriate context for the actual and proposed development of market-based instruments designed to attract capital investments for carbon

Climate of Costa Rica 29

sequestration and biodiversity conservation. Such a framework allows the establishment of mechanisms to use those funds to compensate owners for the environmental services provided by their land to the society. As a developing economy, they point out, Costa Rica is striving to internalize

the benefits from the environmental services it offers, as a cornerstone of its sustainable development strategy. It is this kind of win-win tool that will help Costa Rica get a grip on climate change while protecting its lush nature.

References Andrade, E. 1968. Introducción a la Meteorología en Honduras. Tegucigalpa. Castro, R., F. Tattenbach, L. Gámez, and N. Olson. 2000. The Costa Rican experience with market instruments to mitigate climate change and conserve biodiversity. Environmental Monitoring and Assessment 61(1): 75– 92. Chorley, R., and R. Barry. 1972. Atmósfera, Tiempo y Clima. Barcelona: Ediciones Omega. Enquist, C.A.F. 2002. Predicted regional impacts of climate change on the geographical distribution and diversity of tropical forests in Costa Rica. Journal of Biogeography 29(4): 519– 34. Herrera, W. 1986. Clima de Costa Rica. In L. D. Gómez, ed., Vegetación y Clima de Costa Rica. San José, Costa Rica: Editorial EUNED. 118 pp. Herrera, W. 2005. El clima de los Páramos de Costa Rica. In M. Kappelle and S. Horn, eds., Páramos de Costa Rica, 113– 28. Costa Rica: Editorial INBio. Herrera, W., and L. Gómez. 1993. Mapa de Unidades Bióticas de Costa Rica. US Fish and Wildlife Service, The Nature Conservancy, INBio. San José, Costa Rica: INCAFO. Islebe, G.A., and H. Hooghiemstra. 1997. Vegetation and climate history of montane Costa Rica since the last glacial Quaternary. Science Reviews 16(6): 589– 604. Karmalkar, A.V., R.S. Bradley, and H.F. Diaz. 2008. Climate change scenario for Costa Rican montane forests. Geophysical Research Letters 35: L11702. doi:10.1029/2008GL033940 Lawton, R.O., U.S. Nair, R.A. Pielke, Sr., and R.M. Welch. 2001. Climatic impact of tropical lowland deforestation on nearby montane cloud forests. Science 294: 584– 87. Martínez, A. 1970. Anexo A. Meteorología e Hidrología Istmo Centroamericano. Naciones Unidas, Consejo Económico y Social, Costa Rica. Nair, U.S., R.O. Lawton, R.M. Welch, and R.A. Pielke. 2003. Impact of land use on Costa Rican tropical montane cloud forests: sensitivity of

cumulus cloud field characteristics to lowland deforestation. Journal of Geophysical Research– Atmospheres 108: 193. Pounds, J.A., and M.L. Crump. 1994. Amphibian declines and climate disturbance: the case of the golden toad and the harlequin frog. Conservation Biology 8: 72– 85. Pounds, J.A., M.P.L. Fogden, and J.H. Campbell. 1999. Biological response to climate change on a tropical mountain. Nature 398: 611– 15. Pounds, J.A., M.P.L. Fogden, J.M. Savage, and G.C. Gorman. 1997. Tests of null models for amphibian declines on a tropical mountain. Conservation Biology 11: 1307– 22. Ray, D.K., U.S. Nair, R.O. Lawton, R.M. Welch, and R.A. Pielke. 2006. Impact of land use on Costa Rican tropical montane cloud forests: sensitivity of orographic cloud formation to deforestation in the plains. Journal of Geophysical Research– Atmospheres 204: 111. Rolim, G., P. Sentelhas, and V. Barbieri. 1998. Planilhas no ambiente excel para os cálculos de balanços hídricos: normal, sequencial, de cultura e de produtividade real e potencial. Revista Brasileira de Agrometeorologia, Santa Maria 6(1): 133– 37. Still, C.J., P.N. Foster, and S.H. Schneider. 1999. Simulating the effects of climate change on tropical montane cloud forests. Nature 398: 608– 10. Thornthwaite, C.W., and J.R. Mather. 1955. The water balance. Centerton, NJ: Laboratory of Climatology, Publications in Climatology, vol. 8, no. 1, p. 1– 104. Thornthwaite, C.W., and J.R. Mather. 1957. Instructions and tables for computing potential evapotranspiration and the water balance. Centerton, NJ: Laboratory of Climatology, Publications in Climatology, vol. 10, no. 3, p. 185– 311. Zárate, E. 1978. Comportamiento del viento en Costa Rica. Instituto Meteorológico Nacional. Nota Técnica de investigación No. 2. San José, Costa Rica.

Chapter 3 Geology, Tectonics, and Geomorphology of Costa Rica: A Natural History Approach

Guillermo E. Alvarado1,* and Guaria Cárdenes2,3

Introduction Costa Rica occupies an interoceanic and intercontinental position at the narrow Central American isthmus, which separates North America from South America and the Atlantic Ocean from the Pacific Ocean. The unique location of Costa Rica along this land-bridge and the country’s long geological, biological, and climatological history have motivated researchers to conduct studies in these fields using the country as a natural, long-term laboratory. The resulting laboratory experiment has led to an intricate mosaic of dynamic landscapes shaped by a wide range of processes, such as volcanism, tectonics, fluvial and marine erosion and deposition, weathering, and hydrothermal, karst, glacial, and periglacial processes, and its consequent deposits.The result is a physiography characterized by a heterogeneous array of geomorphic and tectonic provinces, each featuring a distinctive assemblage of landforms that contains a unique history of landscape evolution. Costa Rica also hosts a wide variety of climatic and ecological zones, ranging from humid tropical rainforests in the Caribbean and southern Pacific lowlands, with >4,000 mm/yr of rainfall (see McClearn et al., chapter 16 of this volume, and Gilbert et al., chapter 12), to the dry tropical vegetation of the northern Pacific coastal plains, with 1 m affected the Nicoya Peninsula’s central Pacific coastline during the Mw 7.7 subduction earthquake of 1950 (Marshall and Anderson 1995). The Nicoya Peninsula coastline has a particular morphology; the western part is an emerging coast, typified by an intercalation of cliffs and sandy beaches, and the eastern one is a submerging coast, along which there are well-developed mangroves (e.g., the Nicoya GulfTempisque estuarine system; see Vargas, chapter 6 of this volume). The continuing uplift has been recorded by a sequence of Quaternary marine and fluvial terraces at the Nicoya Peninsula. High-elevation remnants (400– 1,000 m above sea level [m a.s.l.]) of a Pliocene-Pleistocene marine erosion surface (Cerro Azul surface) are preserved at the mountain block of the Peninsula. Deformation of this surface manifests a differential uplift across a series of mountain block faults. The lower elevation alluvial terrace (La Mansión surface) occupies interior river valleys at 4– 10 m above local base level. Also, two laterally extensive, Holocene marine terraces are well developed along 40 km of nearly perpendicular coastlines at the tip of the Nicoya Peninsula, which extend nearly 1 km inland and are locally covered with

36 Chapter 3

up to 2 m of fossiliferous, intertidal sand and beach rocks (Marshall 1991, Gardner et al. 2001, Denyer et al. 2014). Thus, several paleo-beach ridges and beach rock layers are evident in the topography of the continuous blanket of unconsolidated Holocene beach deposits that cover the wavecut platform from Cabuya to Montezuma. The upper Cabuya surface is a 1.5 m thick unconsolidated deposit of shell-rich beach sand and gravels overlying the paleoplatform at an elevation of 12.5– 15.0 m above the highest high tide; the sand and gravel yielded calibrated radiocarbon ages of 4,190 ± 100 yr before present (BP) and 4,690 ± 220 yr BP, respectively. In the case of the lower Cabuya surface, the most prominent of these reaches a height of over 1.5 m, and is continuous for over 500 m. The calibrated radiocarbon ages varied from 2,330 ± 70 yr BP and 700 ± 90 yr BP, for elevations of 8.3 and 2.5 m above the highest high tide, respectively (Marshall 1991). A small coastal bluff at the Cabuya-Montezuma coast, ranging in height from 0.5 m to over 6 m, is composed of high-energy, shell-rich, pebble-cobble beach deposits— an upward fining sequence of gravels and sand, overlain by alluvial gravels, sands, and muds. The estimated age of these deposits is ca. 650 yr BP. Similarly, the Isla Cabuya is surrounded at high tide by water, but as the tide falls, it exposes the modern intertidal platform and the island becomes connected to the mainland and can be reached by foot. The upper part of the platform has a 0.5 m thick unconsolidated beach deposit predominantly composed of marine shells and coral fragments of a 14C calibrated age of 490 ± 60 yr BP. The uplifted wavecut platform beneath this deposit is about 2 m elevation above the present highest high tide (Marshall 1991). This uplift and tilting of Holocene terraces to the southeastof the Nicoya Peninsula is occurring in response to subduction of seamounts along the projected trend of the Fisher seamount chain, onto the Pacific margin of the Caribbean plate (Fig. 3.4). Uplift rates decrease linearly from a maximum of about 6.0 m/ka near the tip of Cabo Blanco to less 1.0 ka/m along both coastlines (Gardner et al. 2001). Turrubares Block and Quepos Promontory

The basement is composed of basic igneous rocks (basalts, gabbros, volcaniclastic sediments) of Cretaceous to Early Eocene age (ca. 65– 45 Ma), exposed mainly in the Herradura block but also in the Quepos promontory (Hauff et al. 2000, Arias 2003). The Herradura headland exhibits the highest topographic relief within the Chorotega forearc (>1,700 m). This fault-bounded block exposes Late Cretaceous oceanic basalts, which have been stripped of their sedimentary cover by rapid Quaternary uplift and erosion. The differential up-

lift between the Herradura block and adjacent lower-relief blocks is accommodated by dip slip along steep marginperpendicular faults. Holocene river terraces and wavecut benches attest to rapid uplift along the Herradura headland. The Turrubares-Quepos-Sierpe segment of the Middle America trench is a known source of large (Mw ≤ 7.0) subduction earthquakes (Montero 1986, Protti et al. 1995). Osa Peninsula and Punta Burica

The Osa Peninsula is a 62 km long, northwest trending, outer forearc, high inboard of the subducting submarine volcanic Cordillera del Coco. The Peninsula consists of a narrow coastal piedmont surrounding a northwest trending mountainous core that locally exceeds 700 m elevation. The rocks cropping out along the Osa Peninsula are a Middle Eocene-Middle Miocene (45– 15 Ma) mélange (mixture) dominated by basalt, cherts, and limestone resulting from accretion of seamounts. At the end of Miocene time, the subduction of a paleo-Cordillera del Coco caused uplift and severe tectonic erosion of the accretionary edifice allowing exhumation of the mélange. The mélange is overlain by a clastic sequence of Pliocene-Quaternary age, represented by conglomerates, mudstone ,and siltstone with finegrained volcanoclastic turbiditic layers. Locally there are megabreccias formed by slumps and calcareous greywacke turbidities (Corrigan et al. 1990, Berrangé 1992, di Marco et al. 1995, Vannucchi et al. 2006). Late Pleistocene fossiliferous marine sands unconformably overly beveled surfaces that cut across the competent rocks of the mélange basement. Nowadays, exposures of these rocks are found more than 75 m a.s.l., requiring uplift rates in excess of 6 m/ka. Furthermore, analysis suggests that the arrival of the blunt-tipped leading edge of the Cordillera del Coco likely resulted in a short-lived (ca. 42 ka) interval of an initial period of very rapid (ca. 30 m/ka) surface uplift (Sak et al. 2004). The elongate Burica Peninsula juts southward into the Pacific Ocean forming a 25-km-long promontory at the Costa Rica-Panama border (Fig. 3.1 and 3.4). This emergent fragment of the Cretaceous-Paleogene oceanic basalts basement is overlaid unconformably by a Plio-Pleistocene sequence of marine sands, conglomerates, and turbidities beds. The relationships of facies and faunal assemblages indicate that the Pliocence subsidence was interrupted by a rapid Pleistocene uplift. The Pio-Pleistocene sediments exhibit significant folding and vertical displacement along a prominent north-trending fault valley that bisects the Peninsula. Uplifted wavecut platforms along the Osa Peninsula coast attest to ongoing deformation (Corrigan et al. 1990, Morell et al. 2011). The Osa Peninsula segment of the Middle America

Geology, Tectonics, and Geomorphology of Costa Rica 37 Fig. 3.4 Volcanic edifices and marine coast morphology of Costa Rica. Volcanic edifices after Alvarado 2000, and marine coast morphology after Denyer and Cárdenes 2000.

trench is a known source of large (Mw ≥ 7.0) subduction earthquakes associated with underthrusting of the buoyant Cordillera del Coco (Montero 1986, Tajima and Kikuchi 1995). The elongate N-S form of the Burica Peninsula is a consequence of the Panama Fracture Zone, also known as a source of large (Mw 7) strike-slip earthquakes. Several N-S faults in the southern inner forearc (Cordillera Costeña and San Vito plain) are the response of the subduction of the Panama Fracture Zone (Arroyo 2001, Morell et al. 2008, 2011). The Golfo Dulce goldfield has been mined since preColumbian times and has produced at least twice as much gold as the entire Tilarán-Aguacate gold province in northern Costa Rica. The gold occurs in alluvial, colluvial, and beach placers (mainly gravels or conglomerates) of Pliocene to Holocene age, overlying the basic igneous complexes of

Late Cretaceous to Eocene age (Berrangé 1992; Alvarado and Gans 2012). Marine Basins between the Forearc and the Magmatic Arc Tempisque, Nicoya, and Orotina Basins

At the Nicoya Peninsula, deep water sedimentary rocks (calciturbidites and mass flow deposits) of Late Cretaceous origin rest unconformably on basalts of the Nicoya Complex. Pelagic limestone clasts with planktonic foraminifera and abundant rudist fragments. The Barra Honda limestone, of Late Paleocene-Lower Eocene age, represents remnants of a formerly continuous carbonate platform from a restricted to open marine environment ( Jaccard et al. 2001). Barra Honda limestone

38 Chapter 3 Fig. 3.5 Geomorphological evolution of Puntarenas sand bar. Modified after Denyer et al. 2005.

exposures in the hill flanks do not exceed 90 m in thickness; however, caves extend to depths of 200 m, suggesting the development of syn-sedimentary loading and deformation in the central part of the platform, where continuous deposition caused subsequent weight-subsidence in the center of the hills (Mora 1979). Although there are some extensive cave systems and peripheral springs, the karst landforms are restricted to sinkholes and dry valleys (Day 2007, Ulloa et al. 2011). In the offshore region of the Nicoya Gulf there is about 3.5 km of Cretaceous-Quaternary sediment extending toward the northeast on the on-shore region, limited in the south by a shallow uplift of the basement. The sediments represent a typical shallowing, upward prograding succession of sediments that grade from pelagic sediments to slope and continental deposits; alluvial and lahar sediments represent the most recent ones (Barboza et al. 1995).

Along a stretch of 150 km of coastline south of the Nicoya Peninsula, major trunk rivers draining the inner forearc flow along a system of active, coast-orthogonal faults. These steep faults segment the inner forearc coastline into several fault-bounded blocks with sharply differing Quaternary uplift rates as determined from elevated marine and fluvial terraces (Fig. 3.1 and 3.4). The rivers follow fault-controlled valleys incised within Neogene-Quaternary nearshore sediments, volcaniclastic debris, and pyroclastic deposits. The Barranca, Jesús María, and Tárcoles faults form the boundaries of the Esparza and Orotina fault blocks (Marshall et al. 2003, Marshall 2007, Denyer et al. 2010). The low-lying Orotina fault block between the Jesús María and Tárcoles rivers is covered by a >100 m thick Quaternary sequence of lahar-derived debris avalanche deposits, ignimbrites, and their fluvial gravels equivalents. During the early Quaternary (about 0.6 Ma), a series of

Geology, Tectonics, and Geomorphology of Costa Rica 39 Fig. 3.6 (a) Distribution of sedimentary facies at part of Barranca river, (b) Migration of the main channel of the Barranca river during the last 40 years. After Denyer et al. 2005.

eruption-generated debris avalanches, diluted by water incorporation into lahars, descended from the volcanic front onto the coastal plain, forming the framework of a 25-km-wide debris fan (Orotina fan). Meandering paleochannels of the Tárcoles River are preserved across the fan surface as inverted topographic ridges of welded tuff overlying river gravels (Marshall et al. 2003, Denyer et al. 2010, Alvarado and Gans 2010). Up to five late Quaternary alluvial fill terraces (10– 260 m elevation) occur along the lower reaches of the faultcontrolled Barranca and Tárcoles rivers. The total number of terraces, and the vertical spacing between them, varies along the coast with respect to the magnitude of local tectonic uplift rates. This relationship suggests that terrace generation along this coastline is strongly controlled by the interaction of rock uplift and eustatic sea level fluctuation (Marshall et al. 2000, 2003).

The Puntarenas sand spit (part of the Gulf of NicoyaTempisque estuarine system), which is the foundation of the capital of the province, appears in maps dating from the eighteenth century. It is 600 m wide, 7 km long, and has an average elevation of 3 m above sea level. Based on historical maps, aerial photographs (since 1860), and geophysical data, Denyer et al. (2004) concluded that Puntarenas is part of an estuarine system growing southward. The sand bar shows lateral growth, primarily at the end (“La Punta”) where the lateral southwards growing rate is 14 m/year (prior to human control), so the origin of the spit could be extrapolated from about 500 years ago, and it is related to the sediment transportation for the marine currents from the Barranca estuarine system (see Fig. 3.5 and 3.6 for actualized analysis). Denyer et al. (2004) conclude that the origin of this sand bar is the NW to SE migration of the Barranca channel, driven by neotectonic activity on

40 Chapter 3 Fig. 3.7 Distribution of sedimentary deposits at Parrita-Quepos area. Based on Drake 1989 and Cárdenes 2003.

the Barranca fault. The distribution of recent sedimentary facies at Puntarenas documents the extraordinary preservation of extended paleo-beaches, flood plains, and estuary sediments, which could indicate that the estuarine system is actually progradating. Parrita-Térraba-Golfo Dulce basins

The Late Cretaceous to Quaternary sequence in the Parrita, Térraba, and Golfo Dulce basins of southwestern Costa Rica includes more than 4.5 km of strata ranging from pelagic limestones and turbidites of Late Cretaceous to Paleocene rocks, shallow-marine carbonate sedimentation of Middle Eocene, deep water Oligocene to Miocene sedimentation (mudstone and sandstone), and shallow water to subaerial Miocene to Pliocene mudstone and sandstone, followed by Pliocene to Lower Quaternary volcaniclastic rocks and non-marine sands and gravels of Quaternary age. These basins are located off-shore and on-shore, limited in the south by a shallow uplift of the basement. The sedimentary rocks represent a typical shallowing, upward prograding succession of sediments that grade from pelagics to slope and continental deposits; and alluvial and deltaic paralic sediments representing the most recent ones (Coates et al. 1992, Corrigan et al. 1990, Barboza et al. 1995, di Marco et al. 1995). The Golfo Dulce is a tropical fjord, 215 m deep (Hebbeln and Cortés 2001, and see Cortés, chapter 5 of this volume). Several recent sedimentary environments have been recognized at the central Pacific coast of Costa Rica. Alluvial deposits including alluvial plains, active and inactive meandering channels, active braided river channels, and colluvial and small lacustrine deposits represent a continental environment. The main rivers like Tárcoles, Parrita, Savegre, and others, which are meandering systems with flood plains limited at the north by the ranges, correspond with steep dip-slip fault zones. For this reason, the analysis of the

morphological and sedimentological changes associated with the local tectonic setting suggests a SE inclination of the Parrita area. The alluvial system presents a meandering belt (Parrita river), which migrated SE to the actual alluvial plain. This abnormal situation would have been generated by the SE inclination of the area (Cárdenes 2003). The drainage networks on the Parrita coastal plain are deflected around the Quepos highland and exhibit at least four late Quaternary terraces that attest to active uplifting (see Marshall 2007, and references therein). The oldest unit is composed of laminated, fine-grained red and grey clay containing foraminifera and poorly preserved bivalves. The deposit is mottled extensively with purple mottles in a blue-grey matrix, and a minimum thickness of 10 m, and typically forms low flat-topped hills with elevations of 25– 35 m. The most recent units are composed of coarse-grained alluvium, highly weathered fluvial deposits, 2.5 to 30 m thick, distal fine-grained deposits, and buried soils, with local fluvial channels. From regional correlation and local 14 C dating, the ages of the terraces are estimated from less than 34,000 years old to about only 400 yrs BP. Average incision rates (0.5– 3.0 m/ka) are estimated from the terrace sequence and apparently reflect regional uplift rates (Drake 1989) (Fig. 3.7). The coastal environment presents a series of sandy beaches including gravel, sand bars, and tombolos. A common feature is the built-bar-estuaries system, which is colonized by mangrove vegetation (Fig. 3.8 and 3.9). The sand bars and beaches are the result of NW-SE littoral currents, and a mesotidal range. Additionally, there are erosional platforms made up of sedimentary rocks, which are affected by faults and synsedimentary deformation (Fig. 3.10). The most striking change at the coastal zone over the last 50 years is the Damas bar migration. These dramatic changes have caused the destruction of about 15 houses and one aquaculture business. The possible causes of

Fig. 3.8 (a) and (b) Bioerosion of sedimentary rocks at Punta Judas erosive platform, (c) Sandy beach at central Pacific coast, (d) Rocky beach at south Pacific coast, (e) Erosive platform at Dominical, (f) Erosive platform at Punta Judas (e and f at central Pacific coast).

Fig. 3.9 Coastal geomorphology: (a) San Juan river deltaic system at north Caribbean coast, (b) Parrita river estuarine system at central Pacific coast, (c) Cahuita coral reef at Limón, (d) Punta Catedral tombolo, (e) Punta Uvita tombolo (d and e at central Pacific coast), (f) Paleo-beaches at Violines island at south Pacific coast.

Geology, Tectonics, and Geomorphology of Costa Rica 43

Fig. 3.10 (a) Erosive platform at Dominical, (b) Marine erosion through a fault in the basaltic platform of Herradura, Playa Hermosa, (c) At least three different erosive levels in the marine platform due to tectonic uplift during the Quaternary.

this migration are a combination of local agents (e.g., tectonic setting), the increase of volume of water transported by the principal stream channels, and an increase of wave, tides, and currents’ energy (Cárdenes 2003). Drake (1989) reports the presence of several terraces, which are the sedimentary response to the neotectonic activity of the area (Fig. 3.7 and 3.10). According to our observations, it is possible to count 2 to 5 raised paleo-beach ridges, which are locally visible as part of the topography characterized by a

continuous blanket of unconsolidated Holocene beach deposits that occur from Savegre to the Playa Ballena beaches. One of these has been dated, using radiocarbon techniques, at 5,540 ± 70 yr (Fisher et al. 2004). Main geomorphic features are the natural tunnels and arcs that appear at the Ventanas beach, between the sandy beach area and the rock promontory that is affected by the intertidal area. These natural tunnels and arcs were produced by marine erosion occurring along tectonic faults and fractures.

Fig. 3.11 (a) Laguna Hule explosion caldera (maar) formed 6,200 years ago, (b) Cones of Barva andesitic shield volcano, (c) Turrialba volcanic graben with craters, (d) The twin cones of Arenal volcano in March 1987, (e) Cave in lahar created when a tree was putrefied after burial, (f) Cave in a lava flow. (a) photo by G.E. Alvarado, (b) photo courtesy of Raúl Mora, (c) photo courtesy of Raúl Mora-Amador, (d) photo by G.E. Alvarado, (e) photo courtesy of Leonel Rojas, (f) photo by Leonel Rojas.

Geology, Tectonics, and Geomorphology of Costa Rica 45

Quaternary marine sands, beach ridges, and alluvial gravels along the Osa Peninsula shorelines show high rates of tectonic uplift (6.5– 2.1 m/ka) that decrease along an arc-ward trend from the Peninsula’s interior, northeastward toward the Dulce Gulf. Along the northeastern coastal piedmont, a sequence of uplifted beach ridges yield radiocarbon ages ranging from 30 ka at an elevation of 25 m. Rivers draining the coastal piedmont exhibit two extensive Pleistocene gravel terraces that form a thick alluvial apron across the fault-bounded mountain front. These deposits overlie nearshore marine sediments dated at >30 ka. Two lower terraces with late Holocene radiocarbon ages occur adjacent to active channels attesting to continued uplift (see Marshall 2007 and references therein). The Holocene development history of the fringing reef at Punta Islotes (Golfo Dulce) was reconstructed. It can be divided into four different stages: (a) an initial stage (5,500– 4,000 yr BP), which includes the settling of Pocillopora damicornis and formation of a small fringing reef; (b) a reef establishment stage (4,000– 1,500 yr BP), showing continuous growth of a branching, massive coral facies, and a drop in accumulation rates of the fore-reef talus facies; (c) a stage characterized by rapid vertical growth (1,500– 500 yr BP), with accumulation rates of 5– 8.3 m/1,000 yr, and growth of most of the reef’s framework; and (d) a final stage (500 yr BP to present), in which accumulation rates decline, owing first to an increase in freshwater, and then to a presence of terrigenous sediments related to deforestation on adjacent shores (Cortés 1991, and see Cortés, chapter 5 of this volume). Magmatic Arc

Truly speaking, the magmatic (volcanic and intrusive) chain in all of Central America is no arcuate form, but for convenience and tradition, it is classified as an island arc. The magmatic arc is the axis of Costa Rica formed by two active volcanic ranges, the Cordillera Central and Cordillera de Guanacaste, and by two extinct ranges, the Cordillera de Tilarán-Aguacate, and the Cordillera de Talamanca. The latter two ranges do not have huge stratovolcanoes because they are mostly extinct and deeply eroded. There is isolated and local evidence of relatively recent volcanic activity during the Quaternary, as shown by the huge Monteverde volcanic plateau (2.1– 1.1 Ma), the Perdidos-Chato-Arenal volcanoes (0.1– 0 Ma), and the volcanic domes in Talamanca (4– 0.1 Ma). For details, see Alvarado (2000) and Alvarado and Gans (2012). The major volcanic centers in the Quaternary ranges are

more or less regularly spaced, 22 km apart, with one exception between Barva and Irazú, which is filled by the Zurquí hills. Volcán Arenal is also isolated, being only separated from the Cordillera de Guanacaste (Volcán Tenorio) and the Cordillera Central (Volcán Platanar) by recent volcanic gaps of 40 and 42 km each, respectively (see Figs. 3.1, 3.4, 3.8). Cordillera de Guanacaste and Santa Rosa Ignimbrite Plateau

The Cordillera de Guanacaste is located in northern Costa Rica. Geologically, it comprises an 110 km long chain of four major stratovolcanic complexes (Orosí-Cacao, Rincón de la Vieja-Santa María, Miravalles-Zapote, and TenorioMontezuma) oriented NW-SE. Rincón de la Vieja is the only volcano active in historical time. The Quaternary volcanoes (basalts to andesites, with rare dacites) of Guanacaste grew about 0.6 Ma over a regional basaltic to dacitic basement of Late Miocene to Lower Pleistocene age. Two remnant calderas occur along the Cordillera de Guanacaste, the Alcántaro-Guachipelín and the Guayabo calderas. An extended fluvio-lacustrine sequence (ca. 100 km2) with a strong volcanic influence (volcanic sandstones and siltstones) and diatomite deposits represent the sediments of an ancient lake that originated within the Alcántaro-Guachipelín caldera (Zamora et al. 2004). Other local diatomite deposits, interbedded with fluvial and ash flow deposits, are present around Montano and La Ese localities, representing a lacustrine sequence filling in the small local lake basins. The oldest volcanic rocks exposed in this area consist of a pile of pyroclastic flow deposits (ignimbrites) with minor interbedded lava flows and terrigenous and paralic sediments of Upper Miocene (8 Ma) to Middle Pleistocene age, about 0.6 Ma (Alvarado et al. 1992, Carr et al. 2007, Alvarado and Gans 2012). These units form a broad plateau (2,000 km2) that extends seaward from the base of the volcanic chain, consisting of ignimbrites emitted from old stratovolcanoes. They form a gently undulating plain that ends in an abrupt 100– 150 m high escarpment near the modern Pacific coast. Rivers draining the volcanic range have incised deep valleys and canyons (i.e., Río Liberia) into the plateau. Owing to tectonic uplift since the Pliocene, several rivers near the Pacific coast drained to the Tempisque River instead of taking a more straighfoward path towards the ocean (Madrigal and Rojas 1980). Cordillera de Tilarán and Montes del Aguacate

The extinct Cordillera de Tilarán and Montes del Aguacate (105 km long) consist of heavily dissected remnants of stratovolcanoes, andesitic shield volcanoes, and old vol-

46 Chapter 3

canic calderas composed of Miocene-Lower Pleistocene basaltic to andesitic lavas, rare dacites, and volcaniclastic rocks (breccias, conglomerates, and tuffs). Hydrothermal alteration and deep tropical weathering have destabilized the steep slopes of these ranges, resulting in pervasive landsliding (Alvarado et al. 1992, 2007; Alvarado and Gans 2012). Throughout the central Montes del Aguacate, an extinct volcanic range, deeply incised linear canyons have developed along active, northwest-and-northeast-trending faults of the Central Costa Rica deformed belt. The Río Grande de Tárcoles cuts a deep gorge through the Montes del Aguacate, connecting rivers of the Valle Central basin with the Pacific coastal plain to the southwest. Along the Tárcoles canyon and many of its tributaries, resistant ignimbrite deposits form level benches and isolated hilltops 50– 100 m above the valley floor. On the basis of late Quaternary isotopic ages for the ignimbrites, the bedrock incision rates range is 0.1 to 0.5 mm/yr (Marshall et al. 2003). A large former lake basin (>50 km2) developed during the Middle Pleistocene in the Palmares and San Ramón area, and persists today as a depression within the Pliocene volcanic terrain. Within this basin is a thick sequence (up to 90 m) of lacustrine and fluvial sediments with beds of diatomites, pumiceous conglomerates, tuffaceous siltstones, and sandstones. The lake drained via the impressive canyon of the Río Grande that flows eastwards (Rojas 2013). Other diatomite deposits are also known to fill smaller lake basins in Turrúcares and Agua Caliente. Small lenticular (5– 30 m thick) diatomite and fluvial outcrops are also present along the Santa Rosa and San José rivers, south of Líbano, and near Peñas Blancas (Mathers 1989). The Los Perdidos domes (active about 90 ka), and the Chato (40– 3.4 ka) and Arenal (7– 0 ka) volcanoes (Alvarado 2000, Alvarado and Gans 2012), are isolated Upper Quaternary vents located on the northern slope of the Cordillera de Tilarán, showing the same trend as the other volcano alignments (Cordillera de Guanacaste and Central). Arenal was one of the 16 most active volcanoes in the world between 1968 and 2010. Cordillera Central

The stratovolcanoes and complex andesitic shield volcanoes of the Cordillera Central form a 130 km-long volcanic chain including Platanar-Porvenir, Poás, Barva, Irazú and Turrialba volcanoes. Minor but important volcanic centers include Congo, Hule, Río Cuarto, and Cacho Negro, along with a dozen parasitic small pyroclastic cones (i.e., Sabana Redonda, Monte de la Cruz, Pasquí, and Armado cones). The Cordillera Central contains the largest volcanoes (el-

evations ranging from 2,000– 3,400 m), in both area and volume, of the entire Central American volcanic front (Fig. 3.11). Their summits exhibit multiple craters and transverse alignments of parasitic cones, and collapsed scarps formed extensive volcanic slides that generated volcanic debris avalanche deposits. Poás, Irazú, and Turrialba have been active in historical time; Barva and Hule were active in Holocene time (Alvarado 2000). The Turrialba Volcano erupted several times between 2010 and 2015, particularly on March 12, 2015, causing explosions of gas and spreading gray ash across parts of Costa Rica, in Coronado, San José, Alajuela, and Heredia. The international airport Juan Santamaría had to be temporarily closed during the fall of Turrialba’s volcanic ash. A strong climatic gradient across the range results in greater weathering and erosion including fluvial canyons (i.e., La Vieja, Aguas Zarcas, Toro, Sarapiquí, Río Sucio, Toro Amarillo, etc.), waterfalls, and more frequent landslides on the humid Caribbean slope (Alvarado 2000, Marshall 2007). Along both flanks of the Cordillera Central, gravitational spreading of the volcanic massif generates prominent fault-propagation-fold scarps along the base of the mountains (Borgia et al. 1990). Rare, small, non-carbonate caves are found on the volcanic range of Cordillera Central (Fig. 3.11). Some are related to marine erosion on the rock (lahar/debris avalanche deposits) cliffs (i.e., Guacalillo beach), or due to lateral fluvial erosion of lavas by mountain rivers (i.e., Toro Amarillo river), or volcanic caves in lava flows (i.e., Cervantes and Ángeles lava fields), or more strangely, due to natural putrefaction of large trees in lahar deposits (i.e., El General Hydroelectrical Plant). Cordillera de Talamanca

The Cordillera de Talamanca (200 km long in Costa Rica) is conspicuous and unique within Central America. It is the highest mountain range in Costa Rica, with maximum elevations over 3,500 m, and generally above 2,000 m, and represents an uplifted inactive segment of the Central American Magmatic arc (Fig. 3.1). The topography of the Cordillera de Talamanca is asymmetric in cross-section. The SW flank is steep, whereas the NE slope is moderately inclined but with profound large scarps. It constitutes the magmatic axis in the southeast part of Costa Rica, and is composed of intrusive batholiths and stocks of quartz-diorites and monzonites. Subordinate granites and gabbros are pervasive intruding sedimentary and volcanic rocks. The sedimentary rocks are predominantly volcarenites, breccias, fossiliferous calcarenites, and sandy black shales. Most of the intrusive rocks of Talamanca are Miocene

Geology, Tectonics, and Geomorphology of Costa Rica 47

Fig. 3.12

(a– c) Glaciar morphology at the Chirripó National Park, (d) The Puente de Piedra, a natural bridge and arch of ignimbrite, Tacares, Grecia.

in age between 8 and 12 Ma. There are only a few intrusive rocks with questionable ages as old as the Early Miocene to Late Eocene (19– 35 Ma) or as recent as the Pliocene age in Dota-Candelaria and Guacimal, in the Cordillera de Tilarán (23.5– 6.3 Ma) (de Boer et al. 1995; Alvarado and Gans 2012). Dacites and andesites produced by the partial melting of hydrated oceanic crust (called adakites) erupted as the latest phase of magmatic activity at the location of previously voluminous calc-alkaline arc magmatism (Abrattis and Wörner 2001). One of the most conspicuous characteristics of the Cordillera de Talamanca is the glacial and periglacial geomorphology, which is best expressed in the Chirripó National Park (Weyl 1971, Hastenrath 1973). The largest scale erosional landforms are U-shaped valleys excavated by Pleistocene glaciers in preexisting fluvial valleys, the cirques,

horns, and minor features such as whalebacks, striated, grooved, and polished bedrock (Fig. 3.12). Lateral, terminal, and medial moraines (glacial and subglacial tills) are the most prominent depositional feature, but there are also fluvioglacial terraces and glacial lakes. The area of glaciers in the Cordillera de Talamanca was estimated to be about 35 km2 in the Chirripó National Park, but there is an additional 14 km2 in neighboring areas (Cerro de la Muerte, 5 km2; Cerro Urán, 5 km2; Kamuk, 2 km2; and Cuericí, 2 km2). The uplift rate for the Talamanca has been estimated at 1.4 ± 0.5 km/my, with the beginning of exhumation at 3.5 Ma (Grafe et al. 2002). The thick accumulation (up to 2 km) and growth of alluvial fans in the Valle del General indicate uplift of the Cordillera de Talamanca during the glacial and interglacial time (Kesel 1983). The presence

48 Chapter 3

of striated boulders at lower elevations in the Valle de El General, and the rectangular shaped valleys some 1,000 m below clear glacial features (Protti 1996), are products of erosive debris flows instead of glacial erosion. Intra-Magmatic Axis Basins Arenal Depression

The Arenal lake with a WNW-ESE trend (ca. 80 x 5 km, 600 m elevation) is a complex tectonic depression limited by active strike slip and normal faults. It is situated between the Arenal volcano and the eroding remnants of Monteverde volcanism (2.1– 1.1 Ma). Several earthquakes of intermediate magnitude (5 < Mw < 6.5) have affected the region (Montero 1986). Valle Central

The elongate Valle Central of Costa Rica consists of an east– west trending (ca. 70 x 10 km) basin (600– 1,500 m elevation) situated between the active volcanoes of the Cordillera Central and the eroding volcanic remnants of the Montes del Aguacate and Cordillera de Talamanca. Throughout the Quaternary, this highland basin filled with a thick accumulation (>1 km) of volcanic products (andesitic to dacitic lavas, pyroclastic rocks, lahar and debris avalanche deposits). The Valle Central consists of a low-relief upland surface with deeply incised river canyons (i.e., Río Virilla) cut into the underlying Quaternary volcanic rocks and less deeply into the Miocene sedimentary sequence. The Quaternary migration of the magmatic front shifted volcanism northeastward to the Caribbean slope, creating a new topographic divide and forming the Valle Central basin (Marshall et al. 2003). The fault-controlled drainage networks of the Valle Central feed into the Tárcoles gorge, a prominent canyon cut through the eroded highlands of the Montes del Aguacate, which provides a link between the Valle Central rivers and the Pacific coastal plain downstream. During the Middle-Late Pleistocene, the Tárcoles river breached the Montes del Aguacate drainage system, leading to progressive capture and re-routing of Valle Central drainage networks toward the Pacific slope (Marshall et al. 2000, 2003). Neotectonic and seismic data show that the Central Costa Rica Deformed Belt is a wide, diffuse, active fault system through the central part of the country (Montero 2001, Marshall et al. 2000). Paleoseismicity and historical studies include the occurrence of intermediate magnitude earthquakes (Mw < 6.5) and seismic swarms, related mostly to NW dextral strike slip faults and ENE to NE sinestral strike slip faults.

General and Coto Brus Valleys

The General and Coto Brus valleys occupy an elongate structural basin (100– 1000 m elevation) that stretches over 90 km in length and 10 km in width and is located between the Pacific slopes of the Cordillera de Talamanca and the Cordillera Costeña. A series of broad alluvial fans, which coalesce along the foot of the Cordillera de Talamanca, form an extensive piedmont surface on the valley bottom. Tributaries of the General and Coto Brus rivers, which drain the Talamanca highlands, have deeply incised this fan complex, leaving a sequence of terrace remnants along canyon margins. These alluvial surfaces are distinguished from one another on the basis of geomorphic settings, sediment texture, and morphologic and chemical characteristics of the soils. The oldest geomorphic surfaces coincide with the extensive piedmont upland in the northwestern portion of the General valley. These well-drained upland surfaces exhibit dark-red, deeply weathered lateritic Oxisols. A series of lower fan surfaces with less-developed soils yield Late Pleistocene to Holocene radiocarbon ages. The youngest alluvial surfaces consist of low elevation agradational terraces in-set along river canyons and abandoned braided channel bars of the General and Coto Brus rivers (Mora 1979, Kesel 1983). In the Río Corredor basin, in southeastern Costa Rica, karst has developed in limestones of Late Eocene age, outcropping the Fila de Cal (part of the Cordillera Costeña), particularly where surface drainage is directed onto it from overlying sandstones and siltstones. Karst features like dolines and dry valleys are well developed in the basin, particularly in fault locations, but are relatively young in age and maturity. Where surface streams encounter the clastic/ limestone contacts or faults, they are captured via large insurgences that ultimately supply resurgence 100– 200 m lower in the Quebrada Seca or Corredor river valleys. Caves are largely fault-controlled, and two main levels separated by an elevational difference of about 25 m may reflect rapid uplift during the Quaternary (see Day 2007, Ulloa et al. 2011, and references therein). Thrust-Fold Deformation Belts

A complex tectonic system of reverse faults (thrust faults) and folds forms a range that in literature is referred to as the thrust-fold deformation belt. In Costa Rica this system is present at both the Pacific and Caribbean sides of the Talamanca range. Along the Pacific it forms part of the forearc system and is called the Cordillera Costeña and Fila Bustamante. On the Caribbean side it is called Baja Talamanca and forms part of the back-arc system. Both are grouped

Geology, Tectonics, and Geomorphology of Costa Rica 49

here in the thrust-fold deformation belts for its similar tectonic origin and structures (Fig. 3.1 and 3.2). Cordillera Costeña and Fila Bustamente

At the forearc, the Cordillera Costeña is a 150-km-long and 15– 25-km-wide mountain range with peak elevations of 1,100– 1,400 m. It runs NW-SE parallel to the south Pacific coast. The Fila Bustamante is a morphologically less defined, 64-km-long and 25– 35-km-wide mountain range with peak elevations of 1,400– 2,500 m. Morphometric analysis of mountain front sinuosity and facet development indicate rapid uplift of the Cordillera Costeña in response to compressional tectonism (Weyl 1971, Wells et al. 1998, Fisher et al. 2004). Major thrust faults generally bound the exterior and interior of the mountain front that imbricate the EoceneMiocene forearc basin sequence of the Térraba basin. Another distinct strike slip fault (mainly in the eastern part) can be observed perpendicular to the Cordillera Costeña. Bedrock has a predominant NW strike and NE dip of 20º– 45º (Mora 1979, Fisher et al. 2004). The sedimentary sequence includes Middle to Late Eocene bioclastic carbonate rocks and a transitional zone to the turbiditic sequence (mudstones and volcaniclastic rocks) of Early to Late Oligocene, indicating a deeper marine environment. The existence of a very local Pliocene marine mudstone (Kesel 1983) is one indicator that thrusting within the Térraba basin began after the Pliocene, sometime before 5.3 Ma. The sedimentary rocks are intruded by gabbroic and hypoabysal (dolerite, basalt, andesite) dikes of Middle Miocene and Pliocene age (McMillan et al. 2004). The coalescence of the General and Coto Brus rivers forms the Río Grande de Térraba, which cuts the Cordillera Costeña, indicating an antecedent river cut during the uplift of the range (Henningsen 1966). Significant Quaternary deposits (mainly debris and hypoconcentrated flows) within the Cordillera Costeña are limited to four discontinuous fluvial terraces up to 100 m above river levels, but their ages are poorly constrained (Bullard 2002). Baja Talamanca

The Panama block moves independently from both the Nazca and Caribbean Plates and is bounded to the north by subduction of the Caribbean Plate along a series of foldand-thrust belts called the Northern Panama Thrust Belt. These faults currently propagate west toward the coast, generating thrust faulting and earthquakes. Some authors include the Baja Talamanca as part of the back-arc area. Fossiliferous and non-fossiliferous sandstones and limestones are composed of coral fragments in a sandy matrix,

indicating a shallow marine enviroment (littoral to sublittoral with patch reefs), in which growth was interrupted by the fast sedimentation and/or uplifting of alluvial delta fan deposits (Aguilar and Denyer 1994). In the back-arc, the faulting and the thrust and folds system shows a NW trend and near Turrialba a combining dextral strike slip and reverse faulting (Denyer et al. 2003). Uplift was clearly observed during the April 22, 1991, Limón earthquake, reaching 4.46 m inland and between 0.5 and 1.85 m in the Caribbean coast (Denyer et al. 2003). As a consequence of the presence of coral material in the ancient uplifted platform, it was possible to study the Holocene tectonic history in the area. On the basis of 14C calibrated ages and the current elevation, corrected with eustatic sea level curves, it was possible to determine an average uplift of about 1.75 m/ka (Denyer 2007). Sediments and the marine currents’ system at GandocaManzanillo define two sedimentary environments. One is between Punta Uva and Manzanillo, where sediments were derived from the coral reefs and local geological formations (Miocene to Pliocene clastic sedimentary rocks), and the other lies between Punta Mona and Río Sixaola, where sediments arrive primarily from outside the area (Fig. 3.9). Back-Arc Region

The back-arc region of Costa Rica is not completely a passive margin, because the Limón basin can be divided into northern and southern sub-basins, which are characterized by different structural settings. Firstly, very low-magnitude historical earthquakes (typical of passive continental margin) and an extension tectonic regime (normal listric faults) dominate the North Limón basin and the Llanuras de Tortuguero. Secondly, the South Limón basin has a strong compressional regime with several large earthquakes, a topic that is treated in the previous Baja Talamanca section (Fig. 3.1). The San Carlos-Caño Negro-Tortuguero Plain and Low Hills

The regional basement contains serpentinized peridotites, Albian siliceous pelagites, and Paleocene to Middle Eocene turbidites, covered by a thick Miocene to Pliocene volcanic sequence. Quaternary fine alluvial and palustrine deposits represent the recent deposits (Gazel et al. 2005, Alvarado et al. 2007, and references therein). The lowlands encompass an extensive alluvial plain (usually less than 100 m in elevation) and a low volcanic relief (less than 300 m) that reaches 35– 150 km seaward from the base of the Quaternary volcanic range. A series of major rivers draining the volcanic range traverse the

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alluvial lowlands, transporting a high sediment load for deposition across broad inland flood plains and a coalescing delta complex at the coast. A sequence of massive alluvial fans has developed along the foot of the volcanic range where the major rivers exit the mountain front. In many cases, modern rivers have incised below extensive upland fan surfaces comprising thick accumulations of Pleistocene fluvial gravels, capped by well-developed, deep-red, clayrich soils. At several locations, the low-relief landscape is interrupted by abrupt hills generated by Lower Miocene to Pliocene volcanism (the Sarapiquí arc, a former remnant volcanic arc), and isolated Quaternary basaltic volcanism. The volcanic rocks usually are deeply eroded and covered by deep-red, clay-rich soils (up to 50 m thick). In some geological and geomorphological maps these features are incorrectly mapped as alluvial terraces, instead of lithological terraces. The north Caribbean coast of Costa Rica is receiving abundant fluvial discharge from the Colorado, San Juan, and Tortuguero rivers (Fig. 3.9), but despite abundant sediment discharge, the regional wave climate has been sufficient to inhibit delta-plain progradation into the Caribbean Sea. Instead, a relatively straight coastal plain, consisting of fluvial-deltaic sands capped by wet forest and palm swamp detritus, has formed along a passive continental margin (Parkinson et al. 1998). Thus, along the Tortuguero coast, the low-relief, sediment-laden shoreline traces a broad, continuous arc for over 120 km between the San Juan River in the north and the Limón headland in the south. This coastline consists of a 10– 15 km wide band of prograding, shore-parallel, beach ridges that stretch along the margin of the vast alluvial plain. The lower reaches of rivers approaching the coastline are often deflected between the shore-parallel beach ridges, resulting in a coastal morphology of elongate lagoons and narrow barrier islands (Marshall 2007). North Limón Basin

The North Limón basin on the Caribbean Sea has a wide and structurally homogeneous depocenter developed in a relative tectonic quiescent area, however, with normal listric faults, particularly active during the Quaternary (Brandes et al. 2007). Some small earthquakes (Mw < 5) are reported by the Parismina nest and along the Hess Scarp (Fernández et al. 1994). South Limón Basin

Compressional tectonics have created a different structural history in the South Limón basin at the Caribbean Sea. It is defined by a shortening due to a heterogeneous

Fig. 3.13 Map of the Pleistocene fossil mega-mammal localities of Costa Rica, distribution of Paleoindian spear point, and distribution of the vegetation. No reconstruction of the coastline was done considering that the sea level varied at the end of the Last Glacial Event while tectonic uplift took place. Map based on and modified after Alvarado 1986, Gómez 1986, Lucas et al. 1997, Laurito et al. 2005.

pattern of accommodation space and sediment thickness, where a number of small depocenters have been active since the Middle Miocene and their location changed continually through time. The hinges are most obvious in the Pliocene-Pleistocene, where a succession of piggy-back basins evolved in response to off-shore activity of the Limón fold-and-thrust belt. This pattern of tectonics causes topographic breaks at the sea-floor that control the position of recent submarine channels (Barboza et al. 1995, Denyer et al. 2003, Brandes et al. 2007).

Pleistocene Fossil Mammals Fossil mammals are known from more than 45 localities of Pleistocene age in Costa Rica (Fig. 3.13). Most of these mammals are proboscideans referred to as the gomphothere Cuvieronius hyodon (Laurito 1988). One occurrence of Mammuthus columbi is known from Costa Rica (Lucas et al. 1997), being the southernmost record of Mammuthus in Central America (Alvarado 1994, Lucas and Alvarado 2010). Less well documented are occurrences of a pampathere, megatheriid (Eremotherium sp.) and mylodontid (Glossotherium aff. tropicorum) ground sloths and glyptodonts (Glyptotherium aff. texanum, Glyptotherium cf. arizonae, Pachyarmatherium) (Gómez 1986, Lucas et al. 1997, Mead

Geology, Tectonics, and Geomorphology of Costa Rica 51

et al. 2006, Pérez 2013). Equus (i.e., E. conversidens) is poorly known from several localities (Gómez 1986, Laurito et al. 1993, 2005, Lucas et al. 1997, Valerio and Laurito 2004), and the toxodont Mixotoxodon larensis is well known from a single locality (Laurito 1993). Canis latrans and Tapirus sp., cf. T. terrestris is also recorded for the Pleistocene of Costa Rica (Lucas et al. 1997). A fossil record of the family Camelidae (Palaeolama mirifica) is described from old lacustrine deposits found near the Río Grande (Pérez 2013). A rodent fossil fauna is also described with four species: Tylomys watsoni, Reithrodontomys mexicanus, Sigmodon hispidus, and Proechimys semispinosus (Laurito 2003). The Costa Rican Pleistocene fossil record is from numerous localities, but consists of one or a few taxa of large mammals and little research on small mammals at each site has been done. It suggests a probable bias towards preservation in high-energy fluvial deposits, alluvial, ignimbrites, and lahars, and a collecting and/or preservation bias toward fossils of large size. None of the Costa Rican Pleistocene mammals is directly associated with human artifacts or remains (Lucas et al. 1997) (Figs. 3.13 and 3.14).

Central America has acted as a filter to dispersal and/ or as a center of evolution during the great American interchange, but there is no evidence of this in its Pleistocene mammal record. Most Pleistocene mammal taxa from Central America are of North American origin (leporids, felids, canids, gomphotheriids, mammutids, elephantids, tapirids, equids, tayassuids, camelids, cervids, and bovids); the remainder belongs to families of South American origin (dasypodids, glyptodontids, megalonychids, megatheriids, mylodontids, hydrochoerids, and toxodontids). If Central America acted as a filter, then that filter prevented strongly the dispersal of mammals from South America to North America than the reverse. No evidence of an endemic center of evolution is evident in the Central American record of Pleistocene mammals. The Pleistocene record of mammals from Costa Rica documented here reinforces these conclusions. Most Costa Rican Pleistocene taxa were of North American origin; the others are of South American origin, and there are no endemic taxa (Lucas et al. 1997, 2007) (Fig. 3.14). The Late Pleistocene record of Mammuthus columbi may be part of a late Pleistocene maximum range of this

Fig. 3.14 A Pleistocene scene in the present San Carlos plains, based on some of the fossils found in Costa Rica. Horses, mastodon, and glyptodont dominate the landscape. A megatheriid and mylodontid were also present. In the foreground is the eastern part of the Nicaragua Lake during the Pleistocene, in today’s Costa Rican territory (before drying and being restricted to the present Nicaraguan territory), as well as the active volcanoes of Guanacaste. The vegetation consists of savanna and sparse deciduous forest. The present coastline is represented by discontinuous lines.

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species from North America far into Central America. The Early Pleistocene (or Late Pliocene) record at Bajo Barrantes consists only of taxa of South American origin (Mixotoxodon larensis) and may predate the arrival in Costa Rica of North American immigrants (Lucas et al. 1997).

Fossil Plants In this section we will present a summary of the fossil plants that have been reported, and the locality where they were found. Paleobotanical research in Costa Rica began in 1921, when William Berry did his study on “Tertiary fossil plants from Costa Rica.” Berry described a Talamancan fossil flora found at Sixaola. The species he described are Annona costaricana, Ficus talamanca, Heliconia sp., Nectandra aerolata, Nectandra woodringi, Phyllites costaricensis, Piperites cordatus, Piperites quinquecostatus, and Inga sheroliensis. Lohmann and Brinkman (1931) reported Lithothamnion and Lithophorella from the Fila de Cal Formation, at Las Animas, Turrialba. Also, Gómez (1973) reported calcareous fossils of Cryptonemiales: Archaeolithophyllum, Goniolithon, and Lithothamnion. Gómez (1970) studied several fragments of rocks that have prints of fern-like Pteropsida. The samples were collected in Río General valley. The specimens were described as resembling the Pecopteris and Mixonera types of Paleozoic era and some actual species of Thelypteris. In 1971, Gómez analysed some specimens found at the junction of Parrita and Candelaria rivers at the central Pacific coast. He reported a new species under the name Palmacites berryanum, which could be related to the modern genera of the Palmae. The first fossil record of Bromeliaceae in Costa Rica was actually a new species, Karatophyllum bromeliodes. The specimen was found in “Tertiary” rocks in the central part of the country, at San Ramón de Alajuela (Gómez 1972). These rocks are probably Pliocene or Quaternary in age. Also, the fossil impressions of leaves of Ficus padifolia were found in diatomitic rocks in Guanacaste (Gómez 1974), and in 1978 Luis Diego Gómez reported Equisetum aff. giganteum in calacareous rocks at Navarro, Cartago. During the 1980s and 1990s paleo-research focused especially on fossil pollen collected from soils, lake sediments, and peat bogs. This paleobotanical research provided important information on paleoclimatic conditions during the late Pleistocene and early Holocene (Hooghiemstra et al. 1992, Islebe and Hooghiemstra 1997, Islebe et al. 2005,

Kappelle et al. 2005, Horn 2007). Palynological evidence from peat bogs near La Chonta close to El Empalme in the northwestern portion of the Cordillera de Talamanca demonstrated how plant species of mountain forests and páramo vegetation types moved up and down mountain slopes as a result of iterative warming and cooling that took place during the glacial-interglacial cycles of the Quaternary (Hooghiemstra et al. 1992). These studies reported a series of plant genera that were recorded as fossilized pollen in peat and clayey soils: Alchornea, Alnus, Drimys, Grammitis, Hedyosmum, Hymenophyllum, Hypericum, Ilex, Jamesonia, Myrica, Podocarpus, Puya, Quercus, Viburnum, and Weinmannia. Plant families present with unidentified genera that were also reported as fossils from this area include Apiaceae, Araliaceae, Asteraceae, Cyatheaceae, Ericaceae, Gentianaceae, Poaceae, Solanaceae, and Urticaceae (Hooghiemstra et al. 1992, Islebe and Hooghiemstra 1997, Islebe et al. 2005, Kappelle et al. 2005, Horn 2007). All these genera and families are still found in today’s highland vegetation (e.g, Kappelle and Horn 2005; and see of this volume: Kappelle, chapter 14, and Kappelle and Horn, chapter 15). The fossil plants record of Costa Rica is limited. The studies and reports on the fossil flora are very few and most of them concern palynological studies, which provide paleoclimatic information (see Islebe and Hooghiemstra 1997, Horn 2007). There are a few other reports on the fossil flora of Costa Rica, especially on black shales, or from petrified wood. Most of these studies indicate the presence of leaves, wood, or other plant materials, but none of them report any classified specimen (see Obando 1986 and others). Woody species in the Valle del General suggest that the woodland there used to be a dry forest type, in which Byrsonima, a major component of most savannas (grasslands) since the Late Pleistocene, was once present (Kesel 1983). Later, Pérez (1998) reported in detail on the fossil plants found at La Palmera, Alajuela, the locality with the most diverse and abundant flora of Costa Rica. He found five families: Bromeliaceae, Araliaceae, Lauraceae, Piperaceae, and Moraceae. Pérez and Laurito (2003) described twenty-one impressions of acorns of Quercus corrugata, from the La Palmera locality in San Carlos. They confirm an important decrease in temperature during the Pleistocene, which corresponds with the maximum glacial between 50,000 to 13,000 years BP. Pérez and Laurito (2003) also found and described Juglans olanchana for the first time in southern Central America. The material they studied at La Palmera was composed of two nuts and an impressed leaf of Pleistocene age.

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Paleoenvironments and Climate Change during the Pleistocene and Holocene The paleoenvironment and climate have been little addressed in geological studies on Costa Rica, and much of the existing information to date comprises puzzling and incidental fragments and isolated pieces of evidence that often lack a good geochronological control (see a summary in Gómez 1986). For a more complete, though still preliminary, summary of the last 100,000 years in Costa Rica and 36,000 years for the entire Central America region, we refer to Lachniet and Asmerom (2007) and Horn (2007). Several periods in the last 100 ka were as wet as the Holocene (11– 0 ka), with a minimum at ca. 60 ka, and several rainfall maxima between 100– 65 ka and at around 37 ka, with a lesser extent during the Holocene (Lachniet and Asmerom 2007). During Pleistocene glacial epochs, snow accumulated and glaciers formed on top of the Talamanca range (i.e., the peaks of Chirripó, Kámuk, and in some instances Cerro de la Muerte) and perhaps on the highest volcanoes as well (i.e., Irazú and Turrialba). The equilibrium line altitudes (ELAs) of permanent ice (the Pleistocene snowline) were about 3,500 m a.s.l. (Weyl 1971, Orvis and Horn 2000, Kappelle and Horn 2005). The lowest reconstructed extent of the glacier tongues at Chirripó was about 3,100 m high (Orvis and Horn 2000), with a maximum ice thickness of 150– 175 m (Lachniet 2007). Pollen in the La Chonta bog indicates that the last glacier interval (ca. 50,000– 15,600 yr BP) was 7– 8º C cooler than present, and the treeless páramo extended down to 2,100 m elevation (Hooghiemstra et al. 1992, Islebe and Hooghiemstra 1997, Horn 2007). About 16 ka after the Last Glacial Maximum, the climate was so dry that it permitted the formation of sand dunes at Islas Murciélago (Denyer et al. 2005), at the moment in which the ocean level was about 100– 120 m lower than the present-day level (i.e., Pinter and Garner 1989). During the beginning of the last deglaciation (15,600– 13,000 yr) the upper forest limit rose as high as 2,700– 2,800 m, indicating a temperature increase of up to 4.6ºC, and precipitation may have increased. The upper forest limit dropped 300– 400 m during the Younger Dryas from 13,100– 12,300 yr, indicating a temperature decline of 2– 3ºC. From 12,300– 11,200 yr, the glaciers retreated above 3,500 m, and subalpine rain forest was gradually replaced by mountain rain forest as both the forest limit and temperatures rose toward present-day values (Hooghiemstra et al. 1992, Islebe and Hooghiemstra 1997, Horn 2007). Also, at least a limited distribution of savanna has existed as is indicated by fossils of grazing mammals, such as

horses and mammoths, during the Late Pleistocene (Lucas et al. 1997). Unfortunately, the Pleistocene record of mammals in Costa Rica is too diffuse and biased (see above) to allow many conclusions to be drawn from this rough temporal organization. Cleary, glyptodonts, Cuvieronius, and Equus were present throughout the Middle-Late Pleistocene, at altitudes at least up to 300, 1,200, and 1,850 m a.s.l., respectively, precisely in proposed savanna-like areas, and in correspondence with the isolated and rare occurrence of Paleo-Indian (about 13,500– 9,000 yr BP) spear points found in Costa Rica (Fig. 3.12 and 3.13). Analyses of pollen, diatoms, and microscopic and macroscopic charcoal in sediment cores from lakes and bogs in the Cordillera de Talamanca suggest wetter conditions during the early Holocene, especially between 7,700– 4,800 yr BP, with minor changes in temperatures (Islebe and Hooghiemstra 1997, Horn 2007). A brief early-Holocene dry period (8,300– 8,000 yr BP) is evident in a speleothem record from northern Costa Rica and may correspond with the high-latitude 8,200 yr BP cold event, but afterwards a stable, relatively wetter monsoon climate was established ca. 7,600 yr BP. In the late Holocene a trend toward distinctively drier climates began about 3,200 yr BP throughout much of the circum-Caribbean region, including Costa Rica (see Horn 2007).

Brief Summary of Costa Rica’s Geological History The early Caribbean basin began as a narrow seaway between the Pacific and Proto-Caribbean, when the last physical connection between North and South America ended about 170 Ma. The next intercontinental connection occurred ca. 75 Ma ago and lasted for about 4– 6 Ma (Bonaparte 1984 a, b), when the proto-Antilles formed a land-bridge between the Americas in the current position of Central America. Another period of ephemeral landbridge formation in the ancestral Antilles also occurred during the Paleocene (Alvarado 1994, Lucas and Alvarado 1994 and references therein). The emplacement of the oceanic plateaus (the Caribbean Large Igneous Province and other mafic igneous events around 69– 139 Ma) between the Americas and the interaction of the Galápagos hotspot track with the Central American volcanic front (between 70 Ma to present), played a fundamental role in the formation of land bridges (ancestral Antilles) between the Americas during the Campanian, Paleocene, and Pliocene (Central America isthmus) (Hoernle et al. 2002, 2004, Alvarado and Gans 2012). In the Late Cretaceous, an intraoceanic arc formed along

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the western margin of the Caribbean Plate. This arc marked the beginning of the subduction of the Farallón Plate in the region. The present territory of Costa Rica emerged above sea-level several times, as a consequence of tectonic events, mostly related to subduction. Andesitic calc-alkaline clasts in submarine sediments give evidence that arc volcanism dates back to the Campanian (Kuijpers 1980). During the Middle Eocene, the areas now occupied by the Tempisque, Nicoya, Parrita, and Térraba basins were part of a major forearc system that spanned along the Pacific margin of Costa Rica. The present structural configuration of the Parrita and Nicoya basins began in the Middle Eocene, related to shear stresses caused by the rotation in clockwise direction of the southern portion of the Costa Rican territory along a main transcurrent fault zone. Such movement displaced the Tempisque and Térraba in the south and north, respectively, developing the half-graben configuration and the system of strike-slip faults of the transtensive basins of Parrita and Nicoya (Barboza et al. 1995). The northern part of Costa Rica emerged and was subjected to erosion during the Oligocene, whereas in the southern part, sedimentation continued. The modern tectonic configuration began during the Late Oligocene to Early Miocene (27– 25 Ma), when the Farallón Plate broke up into the Cocos and Nazca plates separated by the newly formed Galápagos rift zone (Hey 1977, Wortel and Cloetingh 1981). Since the Miocene, shallow marine deposition has been widespread in all of Costa Rica. There are few Oligocene intrusions in Costa Rica; it was not until the Miocene that magmatism began on a wide scale. Subduction of the young lithosphere 14– 25 Ma (von Huene et al. 2000) could have caused migration of volcanism landward in central and north Costa Rica. The Late Oligocene-Miocene (29– 8 Ma) was a period of high volcanic activity throughout Costa Rica (Alvarado et al. 1992, Alvarado and Gans 2012). In Costa Rica there has been a 30° counterclockwise rotation of the arc from its Middle Miocene position close to the modern volcanic front. This occurred from 15 to 8 Ma and is attributed to deformation in the overriding plate (shortening in the south coeval with extension in the NW), accompanied by a trench retreat in the north (McMillan et al. 2004) (Fig. 3.15). Tectonic and magmatic activity during the Middle Miocene to Pliocene in Costa Rica was characterized by an uplift, intrusions along the inner arc, extensive volcanism, and folding with reverse and thrust faulting. Since 8 Ma the arc has been parallel to the modern volcanic front but progressively retreated to the northeast in Costa Rica. Adakite restrictive volcanism in Talamanca, represented by small volcanic domes (4.4– 0.9 Ma), corresponds in space and

Fig. 3.15 Paleographic reconstruction of Costa Rica during the past 16 m.y. Modified after Alvarado et al. 2007.

time with the subduction of a large scarp associated with a tectonic boundary in southern Panama (McMillan et al. 2004). Subduction of the Cordillera del Coco produced a shallow ridge indentation (Montero 1994), affected the southern part of Costa Rica by basement-rooted thrusting, back

Geology, Tectonics, and Geomorphology of Costa Rica 55

arc and intra-arc compression (Rivier 1985, Kolarsky et al. 1995), volcanic arc extinction (McGeary et al. 1985), and uplift of the costal zone (Cross and Pilger 1982, Madrigal and Rojas 1980; see also Marshall 2007 and references therein). The rise of the Talamanca range was caused by the subduction of the Cordillera del Coco beneath the volcanic front (Rivier 1985, Kolarsky et al. 1995), and the collision of the arc with the South American plate led to the development of the Panama microplate (Mann and Burke 1984, de Boer et al. 1995). The age of the Cordillera del Coco collision with the Middle America Trench is still, however, a matter of debate. A few authors claim the age of collision of a older Cordillera del Coco as early as Middle Miocene, on the basis of geological evidence (Rivier 1985), although the most accepted age at present is around 5– 6.5 Ma (see Vannucchi et al. 2003, Alvarado and Gans 2012). Where the crustal shortening is larger in the Cordillera Costeña, the highest mountains of Talamanca (cerros Buenavista, Chirripó, and Kámuk) are present (Fig. 3.1 and 3.2). During the Pliocene the Panamanian basins filled with marine and continental clastic sediments (fan and braided delta to alluvium fans) (Fig. 3.15). In the higher mountains, glaciers and snowcaps were present. Melting of the ice and snow together with volcanic activity in a tropical environment contributed to generate very thick lahars and alluvial deposits. The Isthmus of Panama began to close 15.2– 13 Ma ago (Duque-Caro 1990, Haug and Tiedemann 1998, Montes et al. 2015). In Costa Rica, the coast consisted of a shallowmarine embayment during the Neogene. Vertebrate paleontology strongly suggests that Central America became a peninsula of North America in the Miocene, as land vertebrates of North American affinity are known from Miocene fossils recovered from Guatemala to Panama. The arrival of South American mammals like Xenarthrans in southern Central America (today’s Costa Rica and Panama) around 8.5 to 6.5 Ma resulted from their capacity to swim and hop from island to island at the time Panamanian territory was close to South America (Laurito and Valerio 2012, Montes et al. 2015). This Central American peninsula clearly became connected to South America circa 3.5 Ma ago (see Lucas 2014, and references therein). In fact, fossils indicate that the closure of the Isthmus of Panama was almost complete at 3.7– 3.6 Ma (Coates et al. 1992). The final closure allowed a land mammal exchange at 2.7 Ma (Marshall 1988), coinciding with the glacial-induced sea-level fall during the peak of the northern hemisphere ice-sheet growth (Haug and Tiedemann 1998). Most authors (i.e., Coates 1997) assume that the closure took place in the Panama-Costa Rica region (“Panamanian isthmus” [Fig. 3.15]), but Gartner et al. (1987) argue that

the last interchange of waters between the tropical Atlantic and Pacific was across the isthmus of Tehuantepec, from the Gulf of Tehuantepec into the Gulf of Mexico (Fig. 3.14). The last significant change in the planktonic foraminiferal assemblage occurs around 1.9 Ma and is related to the last closure of the isthmus of Panama (Keller et al. 1989). The Panama land bridge permitted the great American biotic interchange of terrestrial animals (mastodons, saber-tooth cats, tapirs, ground sloths, armadillos, etc.) and plants between North and South America. In several cases it also worked as a biological filter (or biogeographic frontier) owing to differences in topography, vegetation, climate, and geological evolution along the isthmus (see Gómez 1986, Alvarado 1994, Lucas and Alvarado 1994, Kohlmann and Wilkinson 2007). The beginning of rapid (0.55– 0.6 km/Ma) marine subsidence of the Pacific margin of Costa Rica at 6.5– 5 Ma is coincident with the arrival of the Cordillera del Coco crest at the Costa Rica trench (Vanucchi et al. 2003); the arc volcanism extended along the length of Costa Rica more or less coincident with the modern volcanic front (Alvarado and Gans 2012). The Pliocene subduction of the Cordillera del Coco about 5.4 Ma led to uplift and increased exhumation of the Cordillera de Talamanca in the southeast, such that stratovolcanoes are preserved and active to the north and south of the Cordillera de Talamanca, whereas in the area of major uplift they were eroded to deeper crustal levels. This exhumation was characterized by a sudden increase in uplift rates between 5.5 and 3.5 Ma (Gräfe et al. 2002). There is a clear biogeographic frontier formed by the border between the Pacific dry forest (Mexican Pacific Coast Province) and the Pacific rain forest (Western Panamanian Isthmus Province) at the Río Grande de Tárcoles river, possibly related to the Talamanca cordillera (Kohlmann and Wilkinson 2007). The glaciations in Costa Rica would have occurred when the Cordillera de Talamanca was uplifted sufficiently high (>3,100 m high) and some volcanoes grew above this altitude; the precise ages of the first glaciations that took place in the modern territory of Costa Rica are still unclear, but it is clear that the last glaciation affected the country between ca. 18 and 11 ka. At the end of the Pleistocene, an intensification of continental glaciation resulted in sea-level changes with a stronger amplitude (Haug and Tiedemann 1998). At Isla del Coco, submarine erosive arcs and platforms (90– 110 m and 183 m depth) are probably the result of erosion that occurred during the last two glacial maxima (sea levels fell to about 130 to 160 m depth around 18 ka, and 130– 155 m depth about 130 ka), besides slow subsidence events of Coco Island due to thermal cooling of the volcanic shield and oceanic crust (Rojas and Alvarado 2012). Marine sediments deposited from 11,300 to 9,600 years

56 Chapter 3

ago contain evidence of an apparent downslope migration of some mountain forest taxa, interpreted to reflect cooler climatic conditions during this period, especially since deglaciation about 10,000 yr BP (Horn 1993). The second dramatic subsidence of the Pacific margin was very close to the Pliocene-Pleistocene transition (1.8 Ma; Vannucchi et al. 2003), just contemporaneous with the initiation of Monteverde volcanism (2.1– 1.1 Ma old). It was followed by the present Middle-Late Quaternary volcanic activity, the Guanacaste and Central ranges, which grew mainly during the last 1 Ma, with major episodes of cone/ shield building at 1.61– 0.85 Ma (Proto-Cordillera), 0.74– 0.20 Ma (Paleo-Cordillera), and 0.25 Ma (Neo-Cordillera) separated by 0.1– 0.3 Ma intervals of dormancy (erosion) and/or explosive silicic volcanism (Alvarado and Gans 2012). Finally, as a note of interest, both the oldest and the most recent volcanic rocks of Costa Rica are found in the magmatic arc. One of the oldest rocks found in Costa Rica corresponds to a very exotic rock, which is the case of sighting and recovering a meteorite in Costa Rica that happened on April 1, 1857, in Heredia. It consists of an H5 Chondrite that probably originated in asteroid 6 Hebe (Soto 2004). In

opposition, the most recent rocks in Costa Rica were produced by persistent eruption (lava flows and pyroclastic rocks) at Arenal Volcano, active for 42 years, until the start of its new dormancy phase at the end of 2010, and more recently by the eruption at Turrialba Volcano in 2014– 2015.

Acknowledgments The authors thank David Szymanski, Thomal Vogel, and Roland von Huene for their valuable comments at the early preliminary draft of this chapter, and Maarten Kappelle for review of the final versions. Matthew Lachniet, Sally Horn, and Ken Orvis provided valuable comments on the glacial and paleoclimate aspects. Our studies have been supported by the Escuela Centroamericana de Geología, and Centro de Investigaciones en Ciencias Geológicas, both at the University of Costa Rica (UCR), and also by the Instituto Costarricense de Electricidad (ICE). Cristian Corrales, Maikol Rojas, and Krista Thiele helped with figures. We thank the project SFB-574 of the University of Kiel and the IFMGEOMAR (Germany) for their continuous support to our research.

References Abrattis, M., and G. Wörner. 2001. Ridge collision, slab-window formation, and the flux of Pacific asthenosphere into the Caribbean realm. Geology 29: 127– 30. Aguilar, T., and P. Denyer. 1994. Bioestratigrafía del parche arrecifal de la Quebrada Brazo Seco, Plio-Pleistoceno, Limón, Costa Rica. Revista Geológica de América Central 17: 55– 66. Alvarado, G.E. 1994. Historia Natural Antigua: Los Intercambios Biológicos Interamericanos. San José: Ed. Tecnológica de Costa Rica. Alvarado, G.E. 2000. Los Volcanes de Costa Rica: Geología, Historia y Riqueza Natural. 2nd ed. San José: EUNED. Alvarado, G.E., and P.B. Gans. 2012. Síntesis geocronológica del magmatismo, metamorfismo y metalogenia de Costa Rica, América Central. Revista Geológica de América Central 46: 7– 122. Alvarado, G.E., C. Dengo, U. Martens, J. Bundschuh, T. Aguilar, and S.B. Bonis. 2007. Stratigraphy and geologic history. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, 1: 345– 94. London: Taylor and Francis. Alvarado, G.E., S. Kussmaul, S. Chiesa, P.-Y. Gillot, G. Wörner, and C. Rundle. 1992. Cuadro cronoestratigráfico de las rocas ígneas de Costa Rica basado en dataciones radiométricas. Journal of South American Earth Sciences 6(3): 151– 68. Arias, O. 2003. Redefinición de la Formación Tulín (MaastrichtianoEoceno Inferior) del pacífico central de Costa Rica. Revista Geológica de América Central 28: 47– 68. Arroyo, I.G. 2001. Sismicidad y Neotectónica en la region de influencia del proyecto Boruca: hacia una major definición sismogénica del

sureste de Costa Rica. San Pedro de Montes de Oca, Costa Rica: Escuela Centroamericana de Geología, University of Costa Rica. 162 pp. [Lic. thesis]. Barboza, G., J. Barrientos, and A. Astorga. 1995. Tectonic evolution and sequence stratigraphy of the Central Pacific margin of Costa Rica. Revista Geológica de América Central 18: 43– 63. Bellon, H., R. Sáenz, and J. Tournon. 1983. K/Ar radiometric ages of lavas from Cocos Island (Eastern Pacific). Marine Geology 54: M17-M23. Berrangé, J.P. 1992. Gold in Costa Rica. Mining Magazine 402– 7. Berry, E.W. 1921. Tertiary fossil plants from Costa Rica. Proceedings of the United States National Museum 59: 169– 85. Bilek, S.L., S.Y. Schwartz, and H.R. de Shon. 2003. Control of seafloor roughness on earthquake rupture behaviour. Geology 31: 455– 58. Bohrmann, G., C. Jung, K. Heeschen, W. Weinrebe, B. Baranov, B. Cailleux, R. Heath, V. Huehnerbach, M. Hort, T. Kath, D. Masson, and I. Trummer. 2002. Widespread fluid expulsion along the seafloor of the Costa Rica convergent margin. Terra Nova 14: 69– 79. Bonaparte, J.F. 1984a. Nuevas pruebas de la conexión física entre Sudamérica y Norteamérica en el Cretácico Tardío (Campaniano). Actas  III Congreso Argentino de Paleontología y Bioestratigrafía 141– 49. Bonaparte, J.F. 1984b. El intercambio faunístico de vertebrados continentales entre América del Sur y del Norte a fines del Cretácico. Mememorias III Congreso Latinoamericano de Palaontología, Oaxtepec 438– 50. Borgia, A., J. Burr, W. Montero, L.D. Morales, and G. Alvarado. 1990.

Geology, Tectonics, and Geomorphology of Costa Rica 57 Fault-propagation folds induced by gravitational failure and slumping of the Costa Rica volcanic range: implications for large terrestrial and Martian edifices. Journal of Geophysical Research 95(B9): 14357– 82. Brandes, C., A. Astorga, S. Back, and R. Littke. 2007. Fault controls on sediment distribution patterns, Limón Basin, Costa Rica. Journal of Petroleum Geology 20(1): 25– 40. Bullard, T.F. 2002. Geomorphic history and fluvial responses to active tectonics and climate change in an uplifted forearc region, Pacific coast of southern Costa Rica, Central America. Zeitschrift für Geomorphologie 129: 1– 29. Bundschuh, J., and G.E. Alvarado. 2007. Central America: Geology, Resources and Hazards. 2 vol. London: Taylor and Francis. Burke, K.C., and J.T. Wilson. 1976. Hot spots on the Earth’s surface. Scientific American 235: 46– 57. Cárdenes, G. 2003. Evolución de los sistemas sedimentarios costero y aluvial de la región de Parrita, Pacífico Central de Costa Rica. Revista Geológica de América Central 29: 69– 76. Carr, M.J., I. Saginor, G.E. Alvarado, L.L. Bolge, F.N. Lindsay, K. Milidakis, B.D. Turrin, M.D. Feigenson, and C.C. Swisher III. 2007. Element fluxes from the volcanic front of Nicaragua and Costa Rica. Geochemistry Geophysics Geosystems 8: Q06001. doi:10.1029/2006GC001396 Castillo, P., R. Batiza, D. Vanko, R. Malavassi, J. Barquero, and E. Fernández. 1988. Anomalously young volcanoes and old hot-spot traces, I: geology and petrology of Cocos Island. Geological Society of America Bulletin 100: 1400– 1414. Coates, A.G., ed. 1997. Central America: A Natural and Cultural History. New Haven: Yale University Press. Coates, A.G., J.B.C. Jackson, L.S. Collins, T.M. Cronin, H.J. Dowsett, L.M. Bybell, P. Jung, and J.A. Obando. 1992. Closure of the Isthmus of Panama: the near-shore marine record of Costa Rica and western Panama. Geological Society of America Bulletin 104: 814– 28. Corrigan, J.D., P. Mann, and J.C. Ingle. 1990. Forearc response to subduction of the Cocos ridge, Panama-Costa Rica. Geological Society of America Bulletin 102: 628– 52. Cortés, J. 1991. Los arrecifes coralinos de Golfo Dulce, Costa Rica: aspectos geológicos. Revista Geológica de América Central 13: 15– 24. Cross, T.A., and R.H. Pilger. 1982. Controls of subduction geometry, location of magmatic arcs, and tectonics of arc and back-arc regions. Geological Society of America Bulletin 93: 545– 62. Day, M.J. 2007. Karst landscapes. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, 1: 154– 70. London: Taylor and Francis. de Boer, J.Z., M.S. Drummond, M. Bordelon, M.J. Defant, H. Bellon, and R.C. Maury. 1995. Cenozoic magmatic phases of the Costa Rica island arc (Cordillera de Talamanca). In P. Mann, ed., Geologic and tectonic development of the Caribbean plate boundary in Southern Central America. Geological Society of America Special Papers 295: 35– 55. Denyer, P. 2007. Tectonically controlled uplifting of the Caribbean coast of Costa Rica. Abstracts of 20th Colloquium on Latin American Earth Sciences, Kiel, Germany, April 11– 13, pp. 99– 100. Denyer, P., and G.E. Alvarado. 2007. Mapa Geológico de Costa Rica (1: 400,000). Librería Francesa, San José. Denyer, P., A.T. Aguilar, and G.E. Alvarado. 2000. Geología y estratigrafía de la hoja Barranca, Costa Rica. Revista Geológica de América Central 29: 105– 25.

Denyer, P., and G.E. Alvarado. 2000. Desarrollo y evolución de la geología. In P. Denyer and S. Kussmaul, eds., Geología de Costa Rica, 471– 92. Cartago: Ed. Tecnológica de Costa Rica. Denyer, P., and G. Cárdenes. 2000. Costas marinas. In P. Denyer and S. Kussmaul, eds., Geología de Costa Rica, 185– 218. Cartago: Ed. Tecnológica de Costa Rica. Denyer, P., J. Cortés, and G. Cárdenes. 2005. Hallazgo de dunas fósiles de final del Pleistoceno en las islas Murciélago, Costa Rica. Revista Geológica de América Central 33: 29– 44. Denyer, P., S. Kruse, and G. Cárdenes. 2004. Registro histórico y evolución de la barra arenosa de Puntarenas, golfo de Nicoya, Costa Rica. Revista Geológica de América Central 31: 45– 59. Denyer, P., W. Montero, and G.E. Alvarado. 2003. Atlas Tectónico de Costa Rica. San José: Ed. Univ. Costa Rica. Denyer, P., A. Teresita, and W. Montero. 2014. Cartografía geológica de la península de Nicoya, Costa Rica: estratigrafía y tectónica. San José: Ed. Univ. Costa Rica. di Marco, J., P.O. Baumgartner, and J.E. Channel. 1995. Late Cretaceousearly Tertiary paleomagnetic data and a revised tectonostratigraphic subdivision of Costa Rica and western Panama. In P. Mann, ed., Geologic and tectonic development of the Caribbean plate boundary in Southern Central America. Geological Society of America Special Papers 295: 1– 27. Drake, P.G. 1989. Quaternary geology and tectonic geomorphology of the coastal piedmont and range, Puerto Quepos area, Costa Rica. University of New Mexico, p. 183. [M.Sc. thesis]. Duque-Caro, H. 1990. Neogene stratigraphy, paleoceanography and paleobiogeography in northwest South America and the evolution of the Panama Seaway. Palaeogeography, Palaeoclimatology, Palaeoecology 77: 203– 34. Fernández, J.A., G. Bottazzi, G. Barboza, and A. Astorga. 1994. Tectónica y estratigrafía de la Cuenca Limón Sur. Revista Geológica de América Central, vol. esp. Terremoto de Limón, 15– 28. Fisher, D.M., T.W.Gardner, P.B. Sak, J.D. Sanchez, K. Murphy, and P.  Vannucchi. 2004. Active thrusting in the inner forearc of an erosive convergent margin, Pacific coast, Costa Rica. Tectonics 23. doi:10.1029/2002TC001464 Gardner, T., J. Marshall, D. Merritts, B. Bee, R. Burgette, E. Burton, J. Cooke, N. Kehrwald, and M. Protti. 2001. Holocene forearc block rotation in response to seamount subduction, southeastern Península de Nicoya, Costa Rica. Geology 29(2):151– 54. Gartner, S., J. Chow, and R.J. Stanton. 1987. Late Neogene paleooceanography of the eastern Caribbean, Gulf of Mexico and eastern equatorial Pacific. Marine Micropaleontology 12: 255– 304. Gazel, E., G.E. Alvarado, J. Obando, and A. Alfaro. 2005. Geología y evolución magmática del arco de Sarapiquí, Costa Rica. Revista Geológica de América Central 32: 13– 31. Gómez, L.D. 1970. A first report of fossil fern-like Pteropsida from Costa Rica. Revista de Biologia Tropical 16(2): 255– 58. Gómez, L.D. 1971. Palmacites berryanum, a new palm fossil from the Costa Rican Tertiary. Revista de Biologia Tropical 19(1,2): 121– 32. Gómez, L.D. 1972. Karatophyllum bromelioides (Bromeliaceae), nov. gen. et sp., del Terciario Medio de Costa Rica. Revista de Biologia Tropical 20(2): 221– 29. Gómez, L.D. 1973. Criptonemiales calcáreas fósiles en las calizas terciarias de Patarrá, Costa Rica. Revista de Biologia Tropical 21(1): 107– 10.

58 Chapter 3 Gómez, L.D. 1974. Ficus padifolia H.B.K. en la diatomite pliocena/pleistocena de la Formación Bagaces, Guanacaste, Costa Rica. Veröff. Uberseemuseum Bremen, Reihe A 4(15): 141– 48. Gómez, L.D. 1978. Preliminary note on a fossil Equisetum from Costa Rica. Fern Gazette (London) 11(6): 401– 4. Gómez, L.D. 1986. Vegetación de Costa Rica. San José: EUNED. Gräfe, K., W. Frisch, I.M. Villa, and M. Meschede. 2002. Geodynamic evolution of southern Costa Rica related to low-angle subduction of the Cocos Ridge: constraints from thermochronology. Tectonophysics 348: 187– 204. Hastenrath, S. 1973. On the Pleistocene glaciation of the Cordillera de Talamanca, Costa Rica. Zeitschrift fur Gletscherkunde und Glazial 9: 105– 12. Hauff, F., K. Hoernle, P. van der Bogaard, G. Alvarado, and D. GarbeSchönberg. 2000. Age and geochemistry of basaltic complexes in western Costa Rica: contributions to the geotectonic evolution of Central America. Geochemistry, Geophysics, Geosystems 1: 5. doi:10.1029/1999GC000020 Haug, G.H., and R. Tiedemann. 1998. Effect of the formation of the Isthmus of Panama on Atlantic Ocean thermohaline circulation. Nature 393: 673– 76. Hebbeln, D., and J. Cortés. 2001. Sedimentation in a tropical fjord: Golfo Dulce, Costa Rica. Geo-Marine Letters 20: 142– 48. Henningsen, D. 1966. Notes on stratigraphy and paleontology of Upper Cretaceous and Tertiary sediments in Southern Costa Rica. Bulletin of the American Association of Petroleum Geologists 50: 562– 66. Hey, R. 1977. Tectonic evolution of the Cocos-Nazca spreading center. Geological Society of America Bulletin 88: 1404– 20. Hoernle, K., P. van der Bogaard, R. Werner, B. Lissina, F. Hauff, G. Alvarado, and D. Garbe-Schönberg. 2002. Missing history (16– 71 Ma) of the Galápagos hotspot: implications for the tectonic and biological evolution of the Americas. Geology 30: 795– 98. Hoernle, K., F. Hauff, and P. van der Bogaard. 2004. A 70 m.y. history (139– 69 Ma) for the Caribbean large igneous province. Geology 32: 697– 700. Hooghiemstra, H., A.M. Cleef, G. Noldus, and M. Kappelle. 1992. Upper Quaternary vegetation dynamics and palaeoclimatology of the La Chonta bog area (Cordillera de Talamanca, Costa Rica). Journal of Quaternary Science 7(3): 205– 225. Horn, S.P. 1993. Postglacial vegetation and fire history in the Chirripó Páramo of Costa Rica. Quaternary Research 40: 107– 16. Horn, S.P. 2007. Late Quaternary lake and swamp sediments: recorders of climate and environment. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, 423– 41. London: Taylor and Francis. Islebe, G.A., and H. Hooghiemstra. 1997. Vegetation and climate history of montane Costa Rica since the Last Glacial. Quaternary Science Reviews 16: 589– 604. Islebe, G.A., H. Hooghiemstra, and R. van ´t Veer. 2005. Historia holocénica de la vegetación y del nivel de agua en dos turberas de la cordillera de Talamanca, Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 237– 52. Santo Domingo de Heredia, Costa Rica: Ed. Instituto Nacional de Biodiversidad, INBio. Jaccard, S., M. Münster, P.O. Baumgartner, C. Baumgartner-Mora, and P. Denyer. 2001. Barra Honda (Upper Paleocene-Lower Eocene) and El Viejo (Campanian-Maastrichtian) carbonate platforms in the Tem-

pisque area (Guanacaste, Costa Rica). Revista Geológica de América Central 24: 9– 28. Kappelle, M., ed. 2006. Ecology and Conservation of Neotropical Montane Oak Forests. Ecological Studies Series, Vol. 185. Berlin— Heidelberg— New York: Springer. 483 pp. Kappelle, M., and S.P. Horn, eds. 2005. Páramos de Costa Rica. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad, INBio. 767 pp. Kappelle, M., K.A. Haberyan, and S.P. Horn. 2005. Algas fósiles y recientes de los páramos de Costa Rica (Fossil and recent algae from the Costa Rican páramos). In M. Kappelle and S. Horn, eds., Páramos de Costa Rica, 331– 41. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad, INBio. Kappelle, M., J.G. van Uffelen, and A.M. Cleef. 1995. Altitudinal zonation of montane Quercus forests along two transects in the Chirripó National Park, Costa Rica. Vegetatio 119: 119– 153. Keller, G., C.E. Zenker, and S.M. Stone. 1989. Late Neogene history of the Pacific-Caribbean gateway. Journal of South American Earth Sciences 2: 73– 108. Kesel, R.H. 1983. Quaternary history of the Río General valley, Costa Rica. National Geographic Society Research Report 15: 339– 58. Kimura, G., E.A. Silver, and P. Blum, et al. 1997. Introduction. Proceedings of the Ocean Drilling Program, Initial Reports 170: 1– 17. Kohlmann, B., and M.J. Wilkinson. 2007. The Tárcoles Line: biogeographic effects of the Talamanca Range in lower Central America. Giornale Italiano di Entomologia 54(12): 1– 30. Kolarsky, R.A., P. Mann, and S. Monechi. 1995. Stratigraphic development of southwestern Panama as determined from integration of marine seismic data and onshore geology. In P. Mann, ed., Geologic and tectonic development of the Caribbean plate boundary in Southern Central America. Geological Society of America Special Paper 295. Kuijpers, E. 1980. The geologic history of the Nicoya ophiolite complex, Costa Rica and its geotectonic significance. Tectonophysics 68: 233– 55. Lachniet, M.S. 2007. Glacial geology and geomorphology. In J. Bundschuh J, and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, 1: 171– 84. London: Taylor and Francis. Lachniet, M.S., and Y. Asmerom. 2007. Central American rainfall variations over the past 100,000 yr from Costa Rican stalagmites: a proxy for cross-isthmian water vapor transport. AGU Joint Assembly, Acapulco, Mexico. Laurito, C. 1988. Los proboscídeos fósiles de Costa Rica y su contexto en la América Central. Vínculos 14(1– 2): 29– 58. Laurito, C. 1993. Análisis topológico y sistemático del toxodonte de Bajo de los Barrantes, Provincia de Alajuela, Costa Rica. Revista Geológica de América Central 16: 61– 68. Laurito, C. 2003. Roedores fósiles del Pleistoceno Superior de la localidad La Palmera de San Carlos, Provincia de Alajuela, Costa Rica. Revista Geológica de América Central 29: 43– 52. Laurito, C., and A.L. Valerio. 2012. Paleobiogeografía del arribo de mamíferos suramericanos al sur de América Central de previo algran intercambio biótico Americano: un vistazo al GABI en América Central. Revista Geológica de América Central 46: 123– 44. Laurito, C., A.L. Valerio, and E.A. Pérez. 2005. Los xenarthras fósiles de la localidad de Buenos Aires de Palmares (Blancano Tardío-

Geology, Tectonics, and Geomorphology of Costa Rica 59 Irvingtoniano Temprano), Provincia de Alajuela, Costa Rica. Revista Geológica de América Central 33: 83– 90. Laurito, C., W. Valerio, and E. Vega. 1993. Nuevos hallazgos paleovertebradológicos en la Península de Nicoya: implicaciones paleoambientales y culturales de la fauna de Nacaome. Revista Geológica de América Central 16: 113– 15. Linkimer, L., I. Arroyo, M.M. Mora, A. Vargas, G.J. Soto, R. Barquero, W. Rojas, W. Taylor, and M. Taylor. 2013. El terremoto de Sámara (Costa Rica) del 5 de setiembre del 2012 (Mw 7,6). Revista Geológica de América Central 49: 73– 82. Lohmann, W., and M. Brinkmann. 1931. Uber Obereocäne Kalke, Gabbros und Andesite von Costa Rica. Central Journal of Mineralogy, Geology and Paleontology in connection with the New Year Book of Mineralogy, Geology and Paleontology 1931: 553– 59. Lucas, S.G. 2014. Vertebrate paleontology in Central America: 30 years of progress. Revista Geológica de América Central, Número Especial 2014: 30 Aniversario: 139– 55. doi:10.15517/rgac.v0.16576 Lucas, S.G., and G.E. Alvarado. 1994. Role of Central America in landvertebrate dispersal during the Late Cretaceous and Cenozoic. Profil 7: 401– 12. Lucas, S.G., and G.E. Alvarado. 2010. Fossil Proboscidea from the Upper Cenozoic of Central America: taxonomy, evolutinary and paleobiogeographic significance. Revista Geológica de América Central 42: 9– 16. Lucas, S.G., G.E. Alvarado, R. García, E. Espinoza, J.C. Cisneros, and U. Martens. 2007. Vertebrate paleontology. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, 1: 443– 51. London: Taylor and Francis. Lucas, S.G., G.E. Alvarado, and E. Vega. 1997. The Pleistocene mammals of Costa Rica. Journal of Vertebrate Paleontology 17(2): 413– 27. Lücke, O.H., H.-J. Götze, and G.E. Alvarado, 2010. A constrained 3D density model of the upper crust from gravity data interpretation for Central Costa Rica. International Journal Geophysics 2010: 860902. doi:10.1155/2010/860902 Madrigal, R., and E. Rojas. 1980. Manual Descriptivo del Mapa Geomorfológico de Costa Rica (escala 1: 20,000). San José: SEPSA Imprenta Nacional. Mann, P., and K. Burke. 1984. Neotectonics of the Caribbean. Reviews of Geophysics and Space Physics 22(4): 309– 62. Marshall, J.S. 1991. Neotectonics of the Nicoya Peninsula, Costa Rica: a look at forearc response to subduction at the Middle America trench. University of California, Santa Cruz. 196 pp. [M.Sc. thesis]. Marshall, J.S. 2007. Geomorphology and physiographic provinces. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, 1: 75– 122. London: Taylor and Francis. Marshall, J.S., and R.S. Anderson. 1995. Quaternary uplift and seismic cycle deformation, Península de Nicoya, Costa Rica. Geological Society of America Bulletin 107: 463– 73. Marshall, J.S., D.M. Fisher, and T.W. Gardner. 2000. Central Costa Rica deformed belt: kinematics of diffuse faulting across the western Panama block. Tectonics 19(3): 468– 92. Marshall, J.S., B.D. Idleman, T.W. Gardner, and D.M. Fisher. 2003. Landscape evolution within a retreating volcanic arc, Costa Rica, Central America. Geology 31(5): 419– 22. Marshall, J.S., and P. Vannuchi. 2003. Forearc deformation influenced by subducting plate morphology and upper plate discontinuity, Pa-

cific Coast, Costa Rica. Geological Society of America Abstracts with Programs 35: 74. Marshall, L.G. 1988. Land mammals and the Great Interchange. American Scientist 76: 380– 88. Mathers, S. 1989. Costa Rican diatomite: a review of existing knowledge and future potential. Revista Geológica de América Central 10: 3– 17. Matumoto, T., M. Ohtake, G. Latham, and J.E. Umaña. 1977. Crustal structure in Southern Central America. Bulletin of the Seismological Society of America 67: 121– 34. McGeary, S., A. Nur, and Z. Ben-Avraham. 1985. Spatial gaps in arc volcanism: the effect of collision or subduction of oceanic plateaus. Tectonophysics 119: 195– 221. McIntosh, K., E.A. Silver, and T. Shipley. 1993. Evidence and mechanisms for forearc extension at the accretionary Costa Rica convergent margin. Tectonics 12: 1380– 92. McMillan, I., P. Gans, and G. Alvarado. 2004. Middle Miocene to present plate tectonic history of the southern Central American Volcanic Arc. Tectonophysics 392: 325– 48. Mead, J.I., R. Cubero, A.L. Valerio Zamora, S.L. Swift, C. Laurito, and L.D. Gómez. 2006. Plio-Pleistocene Crocodylus (Crocodylia) from southwestern Costa Rica. Studies on Neotropical Fauna and Environment 41: 1– 7. Meschede, M., U. Barckahusen, and H.-U. Worm. 1998. Extinct spreading on the Cocos Ridge. Terra Nova 10: 211– 16. Montero, W. 1986. Períodos de recurrencia y tipos de secuencias sísmicas de los temblores interplaca e intraplaca en la región de Costa Rica. Revista Geológica de América Central 5: 35– 72. Montero, W. 1994. Neotectonics and related stress distribution in a subduction-collisional zone: Costa Rica. Profil 7: 125– 41. Montero, W. 2001. Neotectónica de la región central de Costa Rica: frontera oeste de la microplaca de Panamá. Revista Geológica de América Central 24: 29– 56. Montes, C., A. Cardona, C. Jaramillo, A. Pardo, J.C. Silva, V. Valencia, C. Ayala, I.C. Pérez-Angel, L.A. Rodríguez-Parra, V. Ramírez, and H. Niño. 2015. Middle Miocene closure of the Central American Seaway. Science 348(6231): 226–29. Mora, S. 1979. Estudio Geológico de una parte de la región Sureste del Valle del General, Provincia de Puntarenas, Costa Rica. San Pedro de Montes de Oca, Costa Rica: Escuela Centroamericana de Geología, Universidad de Costa Rica (UCR). 188 pp. [Lic. thesis]. Mora, S. 1981. Clasificación morfotectónica de Costa Rica. Informe Julio-Diciembre 1981. Instituto Geografico Nacional 33– 55. Morell, K.D., D.M. Fisher, and T.W. Gardner. 2008. Inner forearc response to subduction of the Panama Fracture Zone, southern Central America. Earth and Planetary Science Letters 265: 82– 95. Morell, K.D., D.M. Fisher, T.W. Gardner, P. La Femina, D. Davidson, and A. Telezke. 2011. Quaternary outer fore-arc deformation and uplift inboard of the Panama Triple Junction, Burica Peninsula. Journal Geophysical Research 116: B05402. doi:10.1029/2010JB007979 Mörz, T., N. Fekete, A. Kopf, W. Brückmann, S. Kreiter, V. Huehnerbach, D. Masson, D.A. Hepp, M. Schmidt, S. Kutterolf, H. Sahling, F. Abegg, V. Spiess, E. Suwss, and C.R. Ranero. 2004. Styles and Productivity of Mud Diapirism along the Middle American Margin, 2: Mound Culebra and Mounds 11 and 12. NATO Science Series. Dordrecht, Netherlands: Kluwer Academic.

60 Chapter 3 Obando, L.G. 1986. Estratigrafía de la Formación Venado y rocas sobreyacentes (Mioceno-Reciente). Provincia de Alajuela, Costa Rica. Revista Geológica de América Central 5: 73– 104. O’Connor, J.M., P. Stoffers, J.R. Wijbrans, and T.R. Worthington. 2007. Migration of widespread long-lived volcanism across the Galapagos Volcanic Province: evidence for a broad hotspot melting anomaly? Earth and Planetary Science Letters 263: 339– 54. Orvis, K.H., and S.P. Horn. 2000. Quaternary glaciers and climate on Cerro Chirripó, Costa Rica. Quaternary Research 54: 24– 37. Parkinson, R.W., J. Cortés, and P. Denyer. 1998. Passive margin sedimentation on Costa Rica’s north Caribbean coastal plain, Río Colorado. International Coastal Symposium 1998 Proceedings. Journal of Coastal Research Special Issue 26: 110– 22. Pecher, I.A., C.R. Ranero, R. von Huene, T.A. Minshull, and S.C. Singh. 1998. The nature and distribution of bottom simulating reflectors at the Costa Rican convergent margin. Geophysical Journal International 133: 219– 29. Pérez, E.A. 1998. Evaluación paleoambiental de una localidad con flora fósil del Pleistoceno, La Palmera de San Carlos, Provincia de Alajuela. Final report, Bachiller en Manejo de Recursos Naturales, Universidad Estatal a Distancia. Pérez, E.A. 2003. Presencia de Juglans olanchana standley & LO Williams (Juglandaceae) en el territorio costarricense durante el pleistoceno. Revista Geológica de América Central 28: 77– 81. Pérez, E.A. 2003. Los mamíferos fósiles del distrito de Puente de Piedra (Xenarthra, Glypodontidae; Artiodactlyla, Camelidae, Lamini), Grecia. Revista Geológica de América Central 49: 33– 44. Pérez, E.A., and C.A. Laurito. 2003. Quercus corrugata Hooker (Fagaceae) como indicador paleoclimático del Pleistoceno de Costa Rica. Revista Geológica de América Central 28: 83– 90. Pichler, H., and R. Weyl. 1975. Magmatism and crustal evolution in Costa Rica (Central America). Geologische Rundschau 64: 457– 75. Pinter, N., and T.W. Gardner. 1989. Construction of a polynomial model of glacio-eustatic fluctuation: estimating paleo-sea levels continuously through time. Geology 7: 295– 98. Protti, M., F. Güendel, and E. Malavassi. 2001. Evaluación del Potencial Sísmico de la Península de Nicoya. Heredia: Editorial Fundación UNA. Protti, M., F. Güendel, and K. McNally. 1995. Correlation between the age of the subducting Cocos plate and the geometry of the WadatiBenioff zone under Nicaragua and Costa Rica. In P. Mann, ed., Geologic and tectonic development of the Caribbean plate boundary in Southern Central America. Special Paper– Geological Society of America 295: 309– 26. Protti, M., V. González, J. Freymueller, and S. Doelger. 2012. Isla del Coco, on Cocos Plate, converges with Isla de San Andrés, on the Caribbean Plate, at 78 mm/year. Revista de Biología Tropical 60 (Suppl. 3): 33– 41. Protti, R. 1996. Evidencias de glaciación en el Valle del General (Costa Rica) durante el Pleistoceno Tardío. Revista Geológica de América Central 19/20:75– 85. Ranero, C.R., and R. von Huene. 2000. Subduction erosion along the Middle America convergent margin. Nature 404: 748– 52. Rivier, F. 1985. Sección geológica del Pacífico al Atlántico a través de Costa Rica. Revista Geológica de América Central 2: 23– 31. Rojas, K.V. 2013. Relación entre los procesos volcano-sedimentarios y el neotectonismo de la Cuenca lacustrina de Palmares y San Ramón, Costa Rica. San Pedro de Montes de Oca, Costa Rica: Escuela Cen-

troamericana de Geología, University of Costa Rica. 150 pp.[Lic. thesis]. Rojas, W. and G.E. Alvarado. 2012. Marco geológico y tectónico de la Isla del Coco y la región maritima circunvecina, Costa Rica. Revista de Biología Tropical 60 (Suppl. 3): 15– 33. Sak, P.B., D.M. Fisher, and T.W. Gardner. 2004. Effects of subducting seafloor roughness on upper plate vertical tectonism: Osa Península, Costa Rica. Tectonics 23: TC1017. doi:10.10290/2002TC001474 Soto, G.J. 2004. Meteoritos y meteoros en Costa Rica (verdaderos, posibles, falsos). Revista Geológica de América Central 31: 7– 23. Tajima, F., and M. Kikuchi. 1995. Tectonic implications of the seismic ruptures associated with the 1983 and 1991 Costa Rica earthquakes. In P. Mann, ed., Geologic and tectonic development of the Caribbean plate boundary in South America. Special Paper– Geological Society of America 295: 327– 40. Ulloa, A., T. Aguilar, C. Goicoechea, and R. Ramírez. 2011. Descripción, clasificación y aspectos geológicos de las zonas kársticas de Costa Rica. Revista Geológica de América Central 45: 53– 74. Valerio, A., and C. Laurito. 2004. Paleofauna de Aguacaliente de Cartago, Costa Rica, I: Equus cf. E. conversidens Owen, 1869. Revista Geológica de América Central 31: 87– 92. Vannucchi, P., D.M. Fisher, S. Bier, and T.W. Gardner. 2006. From seamount accretion to tectonic erosion: formation of Osa Mélange and the effects of Cocos Ridge subduction in southern Costa Rica. Tectonics. doi:10.1029/2005TC001855 Vannucchi, P., C. Ranero, S. Galeotti, S.M. Straub, D.W. Scholl, and K. McDougall-Ried. 2003. Fast rates of subduction erosion along the Costa Rica Pacific margin: implications for nonsteady rates of crustal recycling at subduction zones. Journal of Geophysical Research 108(B11): 2511. doi:10.1029/2002JB002207 Vannucchi, P., and H. Tobin. 2000. Deformation structures and implications for fluid flow at the Costa Rica convergent margin, ODP Sites 1040 and 1043, Leg 170. Journal of Structural Geology 22: 1087– 103. Vogel, T.A., L.C. Patino, G.E. Alvarado, and P.B. Gans. 2004. Silicic ignimbrites within the Costa Rican volcanic front: evidence for the formation of continental crust. Earth Planetary Science Letters 226: 149– 59. von Huene, R., J. Azéma, W.T. Coulbourn, D.S. Cowan, J.A. Curiale, C.A. Dengo, R.W. Faas, R. Harrison, R. Hesse, J.W. Ladd, N. Muzilev, T. Shiki, P.R. Thompson, and J. Westberg. 1985. Initial Reports of the Deep Sea Drilling Project. Washington, DC: Government Printing Office, vol. 67. von Huene, R., C. Ranero, and P. Watts. 2003. Tsunamigenic slope failure along the Middle America Trench in two tectonic settings. Marine Geology 3415: 1– 15. von Huene, R., C.R. Ranero, W. Weinrebe, and K. Hinz. 2000. Quaternary convergent margin tectonics of Costa Rica, segmentation of the Cocos Plate and Central American volcanism. Tectonics 19 (2): 314– 34. Walther, C. 2002. Crustal structure of the Cocos Ridge off Costa Rica. Journal of Geophysical Research 108. doi:10.1029/2001JB000888 Wells, S., T.F. Bullard, C.M. Menges, P.G. Drake, P.A. Karas, K.I. Kelson, J.B. Rutter, and J.R. Wesling. 1998. Regional variations in tectonic geomorphology along segmented convergent plate boundary, Pacific coast of Costa Rica. Geomorphology 1: 239– 65. Werner, R., K. Hoernle, P. van der Bogaard, C. Ranero, R. von Huene,

Geology, Tectonics, and Geomorphology of Costa Rica 61 and D. Korivh. 1999. Drowned 14-m.y. old Galápagos archipelago off the coast of Costa Rica: implications for tectonic and evolutionary models. Geology 27 6: 499– 502. Weyl, R. 1971. La clasificación morfotectónica de Costa Rica (América Central). Informe Julio-Diciembre. Instituto Geografico Nacional 107– 25. Weyl, R. 1980. Geology of Central America. Berlin: Gebrüder Borntraeger.

Wortel, R., and S. Cloetingh. 1981. On the origin of the Cocos-Nazca spreading center. Geology 9: 425– 30. Zamora, N., J. Méndez, M. Barahona, and L. Sjöbohm. 2004. Volcanoestratigrafía asociada al campo de domos de Cañas Dulces, Guanacaste, Costa Rica. Revista Geológica de América Central 30: 41– 58.

Glossary Andesite: A dark-colored, fine-grained extrusive rock (SiO2: 52– 63%) that could be composed primarily of plagioclase crysts (phenocrysts) and one or more of the mafic minerals, with a groundmass composed generally of the same minerals. Anticline: A fold, generally convex upward, whose core contains the stratigraphically older rocks. Arch: Natural arch. A basement doming. Aseismic: Area that is not subject to large or even minor earthquakes. Basalt: A general term for dark-colored mafic igneous rocks (SiO2 < 52%), commonly extrusive, composed chiefly of calcic plagioclase, clinopyroxene, and olivine. Basement: The undifferentiated complex of rocks that underlies the rocks of interest in an area. Basic: Said of an igneous rock having relatively low silica content, sometimes delimited arbitrarily as 45 to 52%. Beachrock: A friable to well-cemented sedimentary rock, formed in the intertidal zone in a tropical or subtropical region (beach line zone), consisting of sand or gravel (detrital and/or skeletal, including sandy coral beach or rich in shell fragments) cemented with calcium carbonate (aragonite). Bioturbation: The churning and stirring of sediment by organisms. BP: Before present (that is, before the year 1950). Breccia: A coarse-grained clastic rock composed of angular broken rock fragments held together by cement or in a fine-grained matrix; it differs from conglomerate in that the fragments have sharp edges and unworn corners. Breccia may originate as a result of talus accumulation, igneous processes, disturbance during sedimentation, collapse of rock material, or tectonic processes. Calciturbidites: Type of rock formed by carbonate talud sediments. Caldera: A large, basin-shaped volcanic depression, more or less circular or rectangualar in form, the diameter of which is more than 1.5 km. Chondrite: A stony meteorite containing spheroidal granules embedded in a fine-grained matrix of pyroxene, olivine, and Fe-Ti minerals, with or without glass. Cirques: A deep steep-walled half-bowl-like recess or hollow, variously described as horseshoe-or crescent-shaped or semicircular in plan, situated high on the side of a mountain and commonly at the head of a glacial valley, and produced by the erosive activity of a glacier. It often contains a small round lake, and it may or may not be occupied by ice or snow. Colluvial: Pertaining to colluvium or colluvial deposits. Colluvium: General term applied to loose and incoherent deposits, usually at the foot of a slope or cliff as a result from gravity, chiefly. Conglomerate: A coarse-grained clastic sedimentary rock, composed of rounded to subangular fragments larger than 2 mm in diameter set in a fined-grained matrix of sand or silt, and commonly cemented by calcium carbonate, iron oxide, silica, or hardened clay. Cretaceous: The final period of the Mesozoic era, thought to have covered the span of time between 135 and 65 million years ago.

Debris Avalanche: The very rapid and usually sudden megasliding and flowage of incoherent, unsorted mixtures of soil and weathered bedrock. Debris Flow: A high-density moving mass of rock fragments, soil, mud, and water; more than half of the particles being larger than sand size. Delta: The low, nearly flat, alluvial tract of land at or near the mouth of a river, commonly forming a triangular or fan-shaped plain of considerable area, crossed by many distributaries of the main river, perhaps extending beyond the general trend of the coast, and resulting from the accumulation of sediment supplied by the river in such quantities that it is not removed by tides, waves, and currents. Most deltas are partly subaerial and partly submerged. Diatomite: A light-colored soft friable siliceous sedimentary rock, consisting chiefly of opaline frustules of the diatom, a unicellular aquatic plant related to the algae. Dolerite: In British usage, the preferred term for what is called diabase in reference to the fine-grained character of the rock between a microgabbro and a basalt. Doline: A karst depression. Estuarine: Pertaining to or formed or living in an estuary; esp. said of deposits and of the sedimentary or biological environment of an estuary. Eustatic: Pertaining to worldwide changes of sea level that affect all the oceans. Eustatic changes may have various causes, but the changes dominant in the last few million years were caused by additions of water to, or removing water from, the continental icecaps. Fault-propagation Fold: A fold formed in front of a fault surface, commonly associated with the upward termination of a thrust fault. Fold: A curve or bend of a planar structure such as rock strata, bedding planes, foliation, or cleavage. A fold is usually a product of deformation, although its definition is descriptive and not generic and may include primary structures. Foraminifera: Any protozoan belonging to the subclass Sarcodina, order Foraminifera, characterized by the presence of a test of one to many chambers composed of secreted calcite (rarely silica or aragonite) or of agglutinated particles. Most foraminifers are marine but freshwater forms are known. Range from Cambrian to the present. Fracture Zone: On the deep-sea floor, an elongate zone of unusually irregular topography that often separates regions of different depths. Such zones commonly cross and apparently displace the mid-oceanic ridge by faulting. Gabbro: A group of dark-colored, mafic intrusive igneous rock composed principally of basic plagioclase (commonly labradorite or bytownite) and clinopyroxene (augite), with or without olivine and orthopyroxene. Geomorphology: The science that treats the general configuration of the Earth’s surface; specifically, the study of the classification, description, nature, origin, and development of present landforms and their relationship to underlying structures, and of the history

62 Chapter 3 of geological changes as recorded by these surface features. The term is applied to the general interpretation of landforms, but has also been restricted to features produced only by erosion or sedimentation. Graben: An elongate, relatively depressed crustal unit or block that is bounded by faults on its long sides. It is a structural form that may or may not be geomorphologically expressed as a valley. Greywacke: An old rock name that has been variously defined but is now generally applied to a dark gray firmly indurate coarsegrained sandstone that consists of poorly sorted angular to subangular grains of quartz and feldspar, with a variety of dark rock and mineral fragments embedded in a compact clayey matrix having the general composition of slate and containing an abundance of clay minerals. The original German word grauwacke means a grey, earthy rock. Holocene: An epoch of the Quaternary period, from the end of the Pleistocene, at 11,500 years ago, to the present time. Horn: A high, rocky, sharp-pointed mountain peak with prominent faces and ridges, bounded by the intersecting walls of three or more cirques that have been cut back into the mountain by the headward erosion of glaciers. Hypobysal: Subvolcanic rock or igneous intrusion emplaced at shallow level between plutonic and volcanic (subaerial) manifestations. Ignimbrite: The rock formed by widespread deposition and consolidation of pyroclastic ash flow deposits. The term originally implied dense welding but there is no longer such a restriction, so that the term includes rock types such as welded to non-welded pyroclastic pumice flow deposits. Intrusion: The process of emplacement of magma in preexisting rock; magmatic activity; also the igneous rock mass formed within the surrounding rock. Karst: A type of topography that is formed on limestone, gypsum, and other rocks by dissolution and that is characterized by sinkholes, caves, and underground drainage. The word is of GermanSlovenian origin and refers to the Karst Plateau— a region in Slovenia partially extending into Italy. Lahar: A mudflow (debris flow to hypoconcentrated flow) composed chiefly of volcaniclastic materials, water, and other detritus on the flank of a volcano. Listric: A curvilinear, usually concave-upward surface of fracture that curves, at first gently and then more steeply, from a horizontal position. Listric surfaces bound wedge-shaped masses, appearing to be thrust against or along each other. Lithosphere: A layer of strength relative to the underlying asthenosphere for deformation at geologic rates. It includes the crust and part of the upper mantle and is of the order of 100 km in thickness. Margin: A continent-ocean basin transition marked by an active plate boundary (active continental margin), in most of the cases a subduction zone, or not marked by an active plate boundary (passive margin). Mass Flow: A unit movement of a portion of the land surface; specif. mass wasting or the gravitative transfer of material down a slope. Matrix: The finer-grained material enclosing, or filling the interstices between, the larger grains of particles of a sediment or sedimentary rock; the natural material in which a sedimentary particle is embedded. mbsf: Meters below sea floor. It is a convention for depths below the seabed used in geology. Meander: One of a series of regular, freely developing sinuous curves, bends, loops, turns, or windings in the course of a stream. Mélange: A mappable body of rock characterized by the inclusion of fragments and blocks of all sizes, both exotic and native, embedded

in a fragmented and generally sheared matrix of more tractable material. Mode or origin could be tectonic, sedimentary, or a mix. Moraine: A mound, ridge, or other distinct accumulation of unsorted, unstratified glacial drift, predominantly till, deposited chiefly by direct action of glacier ice, in a variety of topographic landforms that are independent of control by the surface on which the drift lies. Mudstone: An indurated mud having the texture and composition of shale, but lacking its fine lamination or fissility; a blocky or massive, fine-grained sedimentary rock in which the proportions of clay and silt are approximately equal, a non-fissile mud shale, or when it is desirable to characterize the whole family of fined-grained sedimentary rocks (as distinguished from sandstones, conglomerates, and limestones). Normal Fault: A fault in which the handing wall appears to have moved downward relative to the footwall. The angle of the fault is usually 45– 90º. There is dip separation but there may or may not be dip slip. Olivine: An olive-green, grayish-green, or brown orthorhombic mineral: (Mg, Fe)2 SiO4. Olivine is a common rock-forming mineral of basic, ultrabasic, and low-silica igneous rock (gabbro, basalt, peridotite, dunite). Ophiolite: A group of mafic and ultramafic igneous rocks ranging from basalt to gabbro and peridotite, including serpentinite derived from them by later metamorphism, whose origin is usually associated with tectonic emplaced oceanic lithosphere. Overthrust: A low-angle thrust fault of large scale, with displacement generally measured in kilometers. Paralic: Said of sedimentary deposits formed along the margin of the sea, in shallow water subject to marine invasion, and of environments (such as lagoonal or littoral) of the marine borders. Also said of basins, platforms, marshes, swamps, and other features marked by thick terrigenous deposits intimately associated with estuarine and continental deposits, such as deltas formed on the heavily alluviated continental shelves. Parasitic Cone: Said of a volcanic cone, crater that occurs on the side of a larger cone; it is a subsidiary form. Periglacial: Said of the processes, conditions, areas, climates, and topographic features at the immediate margins of former and existing glaciers and ice sheets, and influenced by the cold temperature of the ice. By extension, said of the environment in which frost action is an important factor, or of phenomena induced by a periglacial climate beyond the periphery of the ice. Planktonic: Said of that type of pelagic organism that floats. Plate: A torsionally rigid, thin segment of the earth’s lithosphere, which may be assumed to move horizontally and adjoins other plates along zones of seismic activity. Ca. 100 km thick. Pleistocene: An epoch of the Quaternary period that began 2.59 million years ago and lasted until the start of the Holocene (11,500 years ago). If the Quaternary is designated as an era, then the Pleistocene is considered to be a period. Progradating: The building forward or outward toward the sea of a shoreline or coastline (as of a beach, delta, or fan) by nearshore deposition of river-borne sediments or by continuous accumulation of beach material thrown up by water or moved by longshore drifting. Pyroclastic Cone: Cone made of particles ejected during a volcanic eruption, usually of small size. Pyroclastic Flow: Fluidized mass of hot ash. Term often used in a more general sense. Quaternary: Geological era that began 2.59 million years ago and extends to the present. Rift: A long, narrow continental trough that is bounded by normal

Geology, Tectonics, and Geomorphology of Costa Rica 63 faults; a graben of regional extent. It marks a zone along which the entire thickness of the lithosphere has ruptured under extension. Rudist: Any bivalve mollusk belonging to the superfamily Hippuritacea, characterized by an inequivalve shell, usually attached to a substrate, and either solitary or gregarious in reeflike masses. They are frequently found in association with corals. Range: Upper Jurassic to Upper Cretaceous, possibly Paleocene. Sand Spit: A spit consisting chiefly of sand. Sandstone: A medium-grained clastic sedimentary rock composed of abundant rounded or angular fragments of sand size set in a fine-grained matrix (silt or clay) and more or less firmly united by a cementing material (commonly silica, iron, oxide, or calcium carbonate); the consolidated equivalent of sand, intermediate in texture between conglomerate and shale. Seamount: An elevation of the sea floor, 1,000 m or higher, either flattopped (called a guyot) or peaked (called a seapeak). Seamounts may be discrete, arranged in a linear or random grouping, or connected at their bases and aligned along a ridge or rise. Seismic Gap: A segment of an active fault zone that has not experienced a principal earthquake during a time interval when most other segments of the zone have. Seismologists commonly consider seismic gaps to have a high future-earthquake potential. Shield Volcano: A volcano in the shape of a flattened dome, broad and low, built by lava flows or even ignimbrites. Siltstone: A rock whose composition is intermediate between those of sandstone and shale and of which at least two-thirds is material of silt size; it tends to be flaggy, containing hard, durable, generally thin layers, and often showing various primary current structures. Sinkhole: A circular depression in a karst area. Its drainage is subterranean, its size is measured in meters or tens of meters, and it is commonly funnel-shaped. Stratovolcano: A conical volcano that is constructed of alternating layers of lava and pyroclastic deposits. Subduction: The process of one lithospheric plate descending beneath another. Subduction Erosion: Erosion caused in the narrow belt in which subduction takes place. Sublittoral: Said of that part of the littoral zone that is between low tide and a depth of about 100 m. Syncline: A fold of which the core contains the stratigraphically younger rocks; it is generally concave upward. Terrace: Any long, narrow, relatively level or gently inclined surface, generally less broad than a plain, bounded along one edge by a steeper descending slope and along the other by a steeper ascending slope; a large bench or steplike ledge breaking the continuity of a

slope. The term is usually applied to both the lower or front slope (the riser) and the flattish surface (the tread), and it commonly denotes a valley-contained, aggradational form composed of unconsolidated material as contrasted with a bench eroded in solid rock. Terranes: An exotic megablock (several km2) of different rocks tectonically accreted. The term is used in a general sense and does not imply a specific rock unit. Tombolo: A bar or barrier that connects an island with the mainland. Tuff: A general term for all consolidated ash. Turbidite: Sediment of rock deposited from, or inferred to have been deposited from, a turbidity current. It is characterized by graded bedding, moderate sorting, and well-developed primary structures in the sequence. Ultramafic: Said of an igneous rock (SiO2 < 45%) composed chiefly of mafic minerals, e.g., monomineralic rocks composed of olivine and augite. Unconformity: A substantial break or gap in the geologic record where a rock unit is overlain by another that is not next in stratigraphic succession, such as an interruption in the continuity of a depositional sequence of sedimentary rocks or a break between eroded igneous rocks and younger sedimentary strata. It results from a change that caused deposition to cease for a considerable span of time, and it normally implies uplift and erosion with loss of the previously formed record. U-Shaped Valley: A valley having a pronounced parabolic cross-profile suggesting the form of a broad letter “U,” with steep walls and a broad, nearly flat floor; specifically, a valley carved by glacial erosion, such as a glacial trough. Volcanic Dome: A steep-sided, rounded extrusion of highly viscous lava squeezed out from a volcano, and forming a dome-shaped or bulbous mass of congealed lava above and around the volcanic vent. The structure generally develops inside a volcanic crater or on the flank of a large volcano, and is usually much fissured and brecciated. Volcanic Gap: Sector without volcanic activity in a specific time. Volcanic Plateau: Surface formed by extensive lava or ash flows that cover topographic irregularities. Wadati-Benioff: A narrow zone of earthquake foci that seismically illuminates a subduction zone. Whaleback: A large mound or hill having the general shape of a whale’s back, especially a smooth elongated ridge of a glacier plain having a rounded crest and ranging widely in size, about 300 km long, 1– 3 km wide, and perhaps 50 m high. It forms a coarsegrained clastic pedestal build up and left behind by a succession of longitudinal glacial deposits along the same path.

Chapter 4 Soils of Costa Rica: An Agroecological Approach

Alfredo Alvarado1,* and Rafael Mata1

Introduction While investigating the geology of Central America, Sapper (1903) depicts the first soil map of the region, including the territory of Costa Rica. However, soil science in the country begins a little later when Prescott (1918) and Bennett (1926) selected lands to plant lowland crops in the Caribbean Region. During the 1940s, the University of Costa Rica (UCR) reopens and the Inter American Institute of Agricultural Sciences (IICA, Turrialba) starts operations in Costa Rica. This was a remarkable landmark for the country’s agricultural research, since many areas of knowledge were housed in Faculties or Departments at UCR, and medium-term agricultural (soil) research projects were carried out at IICA. During these years the first works on soil analysis for soil fertility purposes were conducted in a small laboratory at UCR in collaboration with the Departamento Nacional de Agricultura de la Secretaría de Agricultura and Ganadería (Ramírez 2001). At the beginning of the 1950s, with the expansion of medium- and high-altitude crops (mainly coffee, sugarcane, and vegetables), soil studies were carried out in the Central Valley (Dondoli and Torres 1954, COSTA RICA-MAI 1958). Government-sponsored colonization programs for the northern region in the 1950s and 1960s led to increased soil knowledge for this region (COSTA RICA-ITCO 1964, Sandner et al. 1966). In December 1955 the Agricultural Research Center of UCR was established as an institution 1 Centro de Investigaciones Agronómicas, Facultad de Ciencias Agroalimentarias, Universidad de Costa Rica (UCR), San Pedro de Montes de Oca, Costa Rica * Corresponding author

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that produced important research papers on Costa Rican soils until date. It is during the 1960s that a group of soil scientists at IICA, Turrialba (now CATIE), promoted soil science knowledge in Latin America; as a result of this effort, other areas of soil science developed, and books in Spanish were prepared on soil microbiology (Blasco 1970), soil chemistry (Fassbender 1975), soil physics (Gavande 1973, Forsythe 1975), and later on soil genesis and classification (Alvarado 1985), soil clay mineralogy (Besoain 1985), and soil and forest ecosystems (de las Salas 1987). Most of the knowledge generated until 1960 allowed the drafting of the first maps of potential land use in Costa Rica at a scale of 1:750,000 (Plath and van der Sluis 1965, Coto and Torres 1970), as well as the first semi-detailed taxonomic soil map of the country (USAID 1965) and the characterization of Costa Rican soils on the Soil Map of the World (FAOUNESCO 1976). In 1960, the Programa Cooperativo Oficina de Café-MAG initiated activities related to nutrition and fertilization of coffee plantations. At the end of the decade Fertilizantes de Centroamérica (Costa Rica) S.A. (FERTICA) began operations, a company that for more than 30 years dominated the market of this type of products and promoted its use exponentially. By the mid-1960s, the Tropical Science Center (TSC; a.k.a. Centro Científico Tropical, CCT, in Spanish) and the Organization for Tropical Studies (OTS, or OET in Spanish) initiated their activities in Costa Rica. Until the mid-1980s TSC focused its attention mostly on life zone ecology and land use capability / suitability studies throughout the country. Examples of their land use assessments are the evaluations conducted in the Salitre indigenous reserve (Tosi

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1967a), in Guanacaste (Tosi 1967b), in the Boruca area south of San Isidro del General (Tosi and Zadroga 1975), and in the northern zone (Gow et al. 1988). These land use– oriented environmental assessments evaluated the potential capability and suitability of the land for future agricultural and forestry use. Interestingly, some 40 years ago, foresters and soil experts Joseph Tosi, Leslie Holdridge, and Gary Hartshorn, together with other TSC and OTS colleagues, already stressed the need to maintain natural vegetation in those areas where slopes were steep and the terrain was rugged. In the particular case of Salitre, for instance, they pleaded for the establishment of a Forestry Reserve that should be preserved in the long run, in order to avoid loss of vegetation and soil erosion. Quite an advanced viewpoint, at that time in history. Since then, many studies on the relationship between soil and vegetation have been published by visiting professors and their students. Soil science developed quickly in Costa Rica and soil maps of the entire country were prepared at a detailed scale (1:200,000 by Pérez et al. 1978 and Vásquez 1979). The soil laboratory of MAG improved its facilities at the end of the decade, allowing it to contribute significantly to soil analysis for agricultural uses. During the 1980s the Soil Science Society of Costa Rica was created with a mandate to organize the VII Latin American Soil Science Congress, and by the 1990s published 12 books on soil science topics. In the late 1980s and early 1990s soils of Talamancan montane cloud forests and páramo vegetation received particular attention (van Uffelen 1991, Kappelle and van Uffelen 2005, 2006, and see Kappelle and Horn, chapter 15 of this volume). More recently a new group of authors contributed to the knowledge of the soils in the Talamanca Range (Winowiecki 2008, Schembre 2009, Chinchilla et al. 2011a,b,c,d, Salazar 2014). In 1991, Servicios Eléctricos Potosí S.A. (SEPSA) published a soil map of the country, incorporating detailed studies prepared for two large hydroelectric development projects in mountainous regions, irrigation projects in Guanacaste, banana expansion in the Atlantic region, and rural development at the border with Panama. Furthermore, several studies have already integrated geographic information systems (GIS) with modern concepts of sustainable development (e.g., see Stoorvogel and Eppink 1995, Arroyo 1996, Ugalde 1996).

Description of Major Soil Orders This section describes the usefulness and importance of Costa Rican soils for agriculture, following soil taxonomy

standards. The analysis includes a summary of the type of areas occupied by each major soil type; the crops planted there; its geographic distribution within the country and position in the landscape; its probable means of origin; the principal mineralogical, physical, and nutritional characteristics of each group; and the management practices that could be applied to each to achieve best its productive potential. In this way, this section can be considered an update to the findings presented by Bertsch et al. (2000). It is possible to find in Costa Rica all 12 major soil orders recognized by soil taxonomists except desert soils (Aridisols) and frost soils (Gelisols). Six of these 10 have major agricultural relevance: Inceptisols (38.6%), Ultisols (21%), Andisols (14.4%), Entisols (12.4%), Alfisols (9.6%), and Vertisols (1.6%); the percentages mentioned represent the relative area each soil order covers (Mata 1991). Entisols

Entisols are very recent soils that exhibit little development. Therefore it is not possible to distinguish any defined horizon sequence in the profile. The most common Entisol suborders in the country are fluvents, aquents, orthents, and psamments (i.e., soils derived from recent alluvial deposits, under stagnant water, shallow soils on hard rock, and sandy textured materials, respectively). The presence of psamments in coastal beach fronts or elevated coastal structures is a consequence of continental uplift due to plate tectonics activity (Fig. 4.1). Recent alluvial deposits lead to the formation of fluvents in areas where frequent flooding does not allow soils to remain undisturbed long enough to permit the development of horizons. Under these conditions, a sequence of layers of contrasting particle sizes occurs. In the same geomorphic surfaces, these soils turn into aquents when the water table remains near or above the soil surface and restricts soil development for long periods of time. Orthents, being the most abundant Entisols, prevail on rocky hillsides with low temperatures and/or very erosive rains, recent volcanic depositions such as ashes or lava, and the presence of parental material resistant to weathering. Other Orthents are found in low relief portions in regions of rhyolithic origin with less than 1500 mm of precipitation in the dry Pacific areas. Most Entisols are of limited agricultural potential due to their high flood risk, restricted soil rooting depth, low fertility status, or location on steep slopes. Their use by humans should be restricted to forestry or conservation activities. Nevertheless, in Costa Rica these soils are frequently used for annual crops, and extensive cattle operations on both

66 Chapter 4

Fig. 4.1

Distribution and characteristics of Entisols of Costa Rica.

flat and steep lands. Owing to their minimal development, these soils reflect the properties of the parent material out of which they were formed, which is why they display a very varied mineralogy. In general, they are not very suitable for agricultural purposes because of shallow rooting depth, reduced conditions, and, as noted, frequent flooding and high susceptibility to hydric and aeolian erosion. In wetlands, aquents and fluvents are associated with aquepts (Inceptisols) at the Caribbean side covered by natural vegetation dominated by yolillo palms (Raphia spp.) and cativo trees (Prioria copaifera) and mangrove vegetation in the Pacific coast, recently exploited for banana and oil palm production, later for charcoal production and today in danger by a possible large sediment deposition if the proposed hydroelectrical plant at Diquís becomes a reality (Torrealba et al. 2011). Once drained, these soils are used to plant bananas,

cocoa, and oil palm. Orthents form on thin volcanic ash deposits over lava flows (e.g., in Cervantes, Cartago province, and Paso Canoas, Puntarenas province). Although they are not very productive, they may be heavily fertilized and planted with vegetables serving nearby markets. In other regions, where the exposed rock is not really hard (e.g., as in the case of rhyolithic materials in Guanacaste) they are used for ranching purposes and, recently (and with very little success), for forestry. At the hillsides in the Southern and Central Pacific regions orthents are commonly used for low technology bean planting (“frijol tapado”). Inceptisols

Inceptisols are widely distributed in Costa Rica. Because the country is geologically and geomorphologically relatively young, Inceptisols cover about 39 percent of the coun-

Soils of Costa Rica 67

try’s territory. The young age of the soils also implies that they strongly reflect their parent material, including Lithic (rock), Fluventic (riverine), Andic (volcanic), Vertic (clay mineralogy), or Oxic (trivalent cation accumulation) properties. They are common on hillsides where erosion due to a combination of earthquakes and heavy rainstorms induces landslides, which limit soil formation to a profile with very weak horizon development. Under these conditions, a typical Udepts toposequence includes Vitrandic Dystrudepts (high volcanic glass, coarse textured soils) in the upper positions, Humic Dystrudepts (high organic matter content soil) in the middle positions, and Typic Dystrudepts (soils with low bases status) in the lower positions of the landscape. The Ustepts are found in rolling and flat geomorphic surfaces. Among these, Dystrustepts (low base saturation) and Haplustepts (little soil development) form from the weathering of relatively old alluvial and/or colluvial fans.

Fig. 4.2

Distribution and characteristics of Inceptisols of Costa Rica.

In the same environment, Inceptisols classified as Aquepts are found when there is a perched water table. These are the most important soils for agriculture of the lowlands less than 100 meters above sea level. A sulfidic horizon forms where brackish water and mangrove vegetation occurs along coastal back swamps. These are classified as Sulfaquepts. The most important Inceptisols are found in alluvial valleys in the coastal plains. These soils have the highest agricultural potential of the country and can be found in the valleys of the Tempisque, Bebedero, Tárcoles, Parrita, Térraba, Sierpe, and Coto rivers on the Pacific side, and the Matina, Reventazón, Parismina, Pacuare, Estrella, and Sixaola rivers on the Caribbean side (Fig. 4.2). In many cases these soils develop from basic parent materials such as limestone, from which they inherited their high base saturation, adequate texture, and moisture retention. Inceptisols (except those with poor drainage) generally

68 Chapter 4

have good characteristics for management, since they do not possess the properties of more developed soils, such as cation depletion, that affect management adversely. For this reason, they can be used for a large range of agricultural production activities, including banana, oil palm, sugarcane, cocoa, coffee, staple crops, livestock, forestry and, recently, non-traditional crops such as mango, avocado, cantaloupe, pepper, roots and tubers, tropical flowers, etc. Even the Sulfaquepts along the coast are important for mangrove forestry, shrimp aquaculture, and extraction of salt. Chemical and mineralogical properties of Inceptisols vary according to their origin. Therefore, their range of chemical characteristics is broad. Each soil tends to include many clay mineral types mixed together, including smectites, allophane, kaolinites, and organic and oxidic coatings (Alvarado et al. 2014a,b). When there is a preponderance of volcanic ash materials some amorphous clay develops. In the alluvial valleys of both the Caribbean and the Pacific sides, montmorillonite is found. The extreme weathering conditions in tropical environments of the El General River Valley result in the formation of 1:1 fractions of clays and oxides in red soils of very high acidity values, and cation depletion. These are the most infertile Inceptisols of the country. Those Inceptisols used for commercial plantations in the poorly drained lowlands require drainage (Epi- and Endoaquepts). For example, as Eastern banana plantations spread from the slopes toward Limon extensive networks of 1- to 2-meter-deep ditches are required. Such ditches are economically viable only when flood frequency remains low. The fertility of Inceptisols in the North Atlantic Zone is much higher than in the South Atlantic Region because they are developed from volcanic materials spread downslope by rivers. In the South Atlantic Region of the country Inceptisols were formed from much less productive calcareous materials, and are also subject to much greater frequency of flooding. The fertility of Inceptisols in the Guanacaste lowlands can be greatly enhanced with applications of S and Zn, especially in rice plantations (Bornemisza 1990, Cordero 1994). Moisture availability is critical on these Inceptisols in ustic (long dry season) environments. These properties have been mapped, and used for categories of crop insurance (IICA 1979). Rice cultivars on Inceptisols in the South Pacific Valleys have been subject to Cu toxicity generated by massive applications of copper-containing Bordeaux fungicides to banana plantations in the 1940s and 1950s (Cordero and Ramírez 1979). Much of this very fertile land had to be abandoned and owing to silt deposition by river flooding they have been rehabilitated for annual crops. During the early days,

these lowlands were planted with banana and cocoa without any fertilizer application; at present, improved varieties and higher productivity of oil palm and banana plantations require large amounts of complete fertilizer formulas and drainage systems. Small farmers, living in government settlements in the Northern and Atlantic regions of the country, plant cereals and roots and tubers using low inputs. Because of the predominantly perudic environments in these regions, the traditional slash and burn system is not practiced since the slashed vegetation does not dry and cannot be burned. This particular problem does not allow for obtaining beneficial effects from liming and fertilizing with added ashes. Normally, the accumulated biomass slowly decomposes with time, releasing nutrients only gradually (Bertsch and Vega 1991). Andisols

A comprehensive summary of Andisols of Costa Rica is presented by Alvarado et al. (2001). Andisols are formed from volcanic ash deposits and occupy: (a) the Central Valley and surrounding mountains; (b) hillsides of the Guanacaste Mountain Range, (c) the region between Coto Brus and the border with Panama influenced by the Barú Volcano’s ashes, and (d) some regions of the Northern and Atlantic zones where fluvio-volcanic depositions occur (Fig. 4.3). Volcanoes are still quite active in Costa Rica, and their activity influences agricultural potential directly as well as indirectly through soil building and acid rain depositions (Alvarado and Cárdenes, chapter 3 of this volume). The emissions of acidic clouds from volcanoes turn into acid rain in nearby zones, which leads to an intensive weathering of the land system, enhancing basic cation leaching and causing considerable loss of crop yields. Although Andisols cover only 14 percent of the nation’s territory, many major agricultural products like coffee, sugarcane, vegetables, non-traditional export crops (flowers, ferns, strawberry), and dairy products like milk and cheese are indeed produced on lands dominated by these soils. Part of the latest large banana boom of the 1990s was settled on volcanic soils of the Northern Zone and parts of the Atlantic Region. In the lowlands, in terms of non-traditional crops, Andisols can produce very good roots and tubers, heart of palm, and a huge range of tropical ornamental plants. The frequent rejuvenation of these soils by andesitic volcanic ash additions constantly enriched the environment with nutrients. Large depositions of debris, particularly near the craters, allows the formation of Vitrands, while Udands form under repetitive deposition of thin volcanic layers in the middle positions of the landscape in udic environments.

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Fig. 4.3

Distribution and characteristics of Andisols of Costa Rica.

In the lower parts of the landscape, where a distinctive dry season occurs, Ustands are predominant. Andisols of lighter color are found along the Guanacaste Mountain Range, in the north of the country, and originated from the deposition of rhyolithic/dacitic ashes. Andesitic basaltic ashes predominate in the central and southern parts of the country, and give rise to dark-colored soils. The effective depth of the top soil layer of Andisols generally depends on the magnitude of the volcanic deposition that formed that layer. Deep soils tend to be formed from the deposition of many small layers of ashes, while thin Andisols are formed by one event, which can be of small or large magnitude. It is possible to observe the ash deposition frequency and magnitude in deep road cuts, as well as the presence of paleosols with a different degree of weathering. Soil particles are generated and distributed initially by the nature of the original volcanic activity, and then sorted

by prevailing winds according to particle size and density, creating a textural gradient along the hillsides of volcanic craters. Coarser material is deposited in the vicinity of craters, resulting in sandy to sandy-loam materials. Further away silty loam or loam textures are predominant. Finer textures are found farther away from the volcano, particularly in the B horizons of well-developed soils. This textural gradient notoriously affects nutrient availability and irrigation needs. Once the original deposition has taken place climate forces predominate. For example, if a moist and cold environment ensues near the volcano, this allows for a weak weathering process of volcanic glass, releasing small amounts of Si, Al, and Fe oxides and hydroxides. If long periods of volcanic inactivity follow, the translocation of the oxides will form a cemented layer (called a placic horizon) wherever an abrupt textural change is present. Farther from

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the crater, allophane becomes predominant. This type of clay is an amorphous and hydrated colloid, which forms organomineral compounds and represents required products of volcanic ash decomposition in humid zones (Alvarado et al. 2014a). Allophane is an unstable clay-size particle of high reactivity that gives a peculiar behavior to these soils. Secondary organomineral compounds possess a very large hydration capacity that enables them to enlarge their total surface, therefore increasing their capacity to retain or exchange cations and anions. In the Central Valley, farther away from the volcanoes, rainfall decreases and a long dry period permits the formation of a 1:1 crystalline clay named halloisite. This type of clay has shrink and swell properties, low water retention characteristics, and less nutrient retention than allophanes. They are predominant in the brown-yellowish soils of the coffee and sugarcane plantations of the Central Valley. Each mineral type gives a characteristic color to the soils that are formed from them. Dark-colored Andisols are associated with a high allophane content; brown yellowish Andisols are dominated by halloisite; while brown reddish Andisols are related to kaolinite. White-colored Andisols are associated with the presence of gibbsite (Colmet Daage et al. 1973, Besoain 1985). Owing to the presence of highly stable organomineral compounds, especially in the A horizon, Andisols tend to be very well structured. This results in a high infiltration capacity leading to both good drainage, and good moisture retention characteristics. One unfortunate consequence of these properties is that these soils promote the leaching of nitrate from agricultural systems and human sewage down to underground waters, contaminating ground waters and reducing their value for human use (Reynolds 1991), although these relationships have a variety of applications (Radulovich et al. 1992) that are currently being studied. These soils have low bulk density and low resistance to tangential forces, making them easy to plow. In Costa Rica this task should be done by animal traction in order to prevent erosion, instead of using heavy machinery that tends to compact the soil (RELACO 1996). Overgrazing causes a similar effect. During periods of high volcanic activity, large amounts of very unstable ashes are deposited as blankets that cover the landscape. This material partially dissolves when subject to alternating dry and moist periods, inducing redistribution of soluble elements at the surface, cementing small pores, and reducing infiltration by crusting. This phenomenon develops into massive erosion, which encourages the formation of colluvio-alluvial fans at the bottom of the landscape. This is the main factor generating catastrophic events when deposited as “lahars” or “debris avalanches” (Alvarado, Vega, et al. 2004) in populated ar-

eas. Also, these soils are intensively used for agricultural activities that greatly trigger their erosion and cause silting of hydroelectric dams. Most Andisols have a moderate fertility depending on the composition of their parent material. In general, soils formed from the ashes of the Irazú Volcano are richer in bases than those formed from Poás Volcano materials (Alvarado 1975); Andisols around Barú Volcano in the Southern Region are even poorer than those of the Central Valley. Nutrient leaching in volcanic areas is counterbalanced by new additions of volcanic ash; this process enables nature to maintain the base saturation of the ecosystem. Generally, Andisols have pH values near neutral except in agricultural areas with poor management or where the decomposition of abundant organic matter content of Andisols gradually acidify soils, particularly when large amounts of N are applied. When this happens they do respond to liming with calcitic (Ca carbonate) or dolomitic (Ca and Mg carbonates) products. The soil fertility potential of Andisols can be estimated by the sum of cations (Ca, Mg, K, Na). Higher values indicate a better condition for crop development and imply that other nutrients are also abundant. In Andisols of the Southern Region, the predominance of plagioclases over orthoclases creates a pronounced K deficiency (Molina et al. 1986, Henriquez and Bertsch 1994). In recent volcanic ashes, N is the most limiting factor for crop production. But P, although abundant in total, creates difficulties for farmers too. P is held tightly by the clay lattices of Andisols so that it is not available to plants. Retention is generally over 70 percent, which is very high, and it can easily reach values of 95 percent. This problem constitutes by far the major limitation for crop development on these soils (Alvarado 1982, Canessa et al. 1987). In addition, B and S can also be tightly held as anions. The application of these two elements is essential for coffee production all over Costa Rica. Andisols formed in the lowlands of fluviovolcanic origin of the Northern Zone and part of the Atlantic Region, along the Sarapiquí, Sucio, Chirripó, Tortuguero, and Destierro rivers, are poorly understood. Under very high temperature and rainfall conditions, they seem to weather to form soils with more nutritional problems than those of the highlands. In addition, the low relief of these areas enables water to accumulate on the surface, thus enhancing soil compaction, particularly in pasture lands. Owing to the high P retention of Andisols, most crops require large fertilizer applications with soluble P. The exact location and granule size of such fertilizers are important; it should be applied along with light applications of lime that increase the availability of P retained in organic materials. N is also a limiting factor for crop production, except when

Soils of Costa Rica 71

legume species are planted to fix N, such as when white clover is planted with kikuyo grass. Large applications of ammonium N result in the release of hydrogen ions, enhancing acidification of extensive areas, particularly in grasslands and coffee plantations. To correct for this condition, frequent applications of lime are required to get good yields, as has been used for sugarcane (Chaves and Alvarado 1994). Other elements, such as Mg, can limit crop performance if the parent material is low in Mg (Poás slopes, primarily) or when large K applications induce nutrient antagonisms. As with B and Zn, foliar and soil analyses should be run on a regular base to correct for deficiencies. Tree-shaded coffee plantations require smaller additions of fertilizer than new full-sun varieties since shading reduces photosynthesis of coffee plants. If the shading tree is a legume species, such as Erythrina and Inga, biologically fixed N is added to the system. Coffee plantations also are associated with contour planting, use of tills, windbreak barriers, and hedge rows, practices which are necessary to reduce erosion, particularly during crop establishment. The use of agrochemical products on these types of soils have different effects over long times. In the case of potato fields many years of fertilization generates P accumulation. In areas where potatoes have been cropped for more than 25 years, concentrations of more than 80 ppm of available P have been found. In the case of cupric fungicides, used as disease protectors in intensively managed coffee plantations, however, Cu accumulates at a rate of approximately 1 ppm/year, which might become a long-term problem because plant toxicity begins at 100 ppm (Cabalceta et al. 1996). Vertisols

Vertisols are found mainly in the Northwest Dry Pacific region of Costa Rica (see chapter 9 on Nicoya and Guanacaste by Jiménez, Carrillo, and Kappelle, this volume), on either plains or depressions where the dry season extends from 4 to 6 months, and are often associated with small patches of similar Mollisols. Although most Vertisols have a neutral or basic status, a few of them located near the border of Nicaragua are acid. Vertisols occupy only 2 percent of the country’s area, and are restricted to depressional areas in the most important alluvial valleys of the Dry Pacific, and to similar locations in the western part of the Central Valley (Santa Ana, Pozos, Lindora, Ciruelas) (Fig. 4.4). Vertisols are used intensively for both agricultural practices and— in the Central Valley— for urban development. During the rainy season the main crop on these soils is rice, either flooded or rain-fed. With irrigation and adequate soil water management sugarcane, soybean, melon, cotton, or even hot chili pepper and sauce tomato can be grown. Trees

grow poorly on these soils, owing to root damage caused by alternate seasonal periods of dryness and water excess. Thus, commercial forests are neither abundant nor recommended on Vertisols. Even though pastures are found there, their management is very difficult and beef production remains very poor. Vertisols in Costa Rica originate mostly from rhyolithic tuffs high in biotitic micas, with some recent additions of very fine volcanic ash. The confluence of several factors is necessary for Vertisols to form: the presence of a depressional zone, which prevents a good drainage; the occurrence of materials rich in Si, Ca, and Mg that accumulate in dry alluvial and/or fluvio-lacustrine deposits; and a well-defined season. An exception occurs in the Central Valley, where climatic and tectonic dynamics first created and then eliminated lakes, which served the same functions as depressional areas. The conditions necessary for Vertisols also favor the formation of 2:1 montmorillonite type clays, which have very high Si content and the strongest colloidal properties of all clays (Alvarado et al. 2014b). This generates Si films interlayered between, but very poorly bonded with, montmorillonite particles. The result is very small, highly individual particles with unlimited and reversible water absorption capacity. The resulting soil is highly expandable, and has high specific surface activity, cohesiveness, adhesiveness, plasticity, and water retention capacity. What this means is that these soils can get both very wet and very dry, change their shape greatly, crack when they get dry, and become extremely slippery and sticky when wet. Even with their large water holding capacity, the difference between their field capacity and the permanent wilting point is rather low, so they dry out easily from a plant’s perspective. Overall Vertisols are poorly suited for most agricultural and engineering operations owing to their contractions and expansions in response to seasonal fluctuations of rainfall. Most Vertisols (usually Usterts) are less than 1 meter deep, are dark colored, and have little horizon differentiation and a clayish texture. Shallower Vertisols tend to lay over low permeability tuffs, and become water saturated and anoxic during the rainy season. Because of the reduced conditions grayish subsurface horizons (aquerts) are present. When the dry season arrives, Vertisols dry very drastically, forming massive blocks with open cracks in between that affect irrigation, electric poles, and engineering operations. At the onset of the rains, a vertical water flow runs down the cracks, causing the subsoil clays to expand rapidly. This process effectively seals the whole system, causing heavy floods as the rains increase. The use of mechanized cultivation on these soils is difficult and expensive. Vertisols are potentially quite fertile soils, with high

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Fig. 4.4

Distribution and characteristics of Vertisols of Costa Rica.

pH, Ca, and Mg contents. Thus, the constraints for high productivity on Vertisols are mainly physical rather than nutritional. Nevertheless there are many nutritional problems that get in the way of its high potential fertility being expressed by high plant growth. Organic matter additions under flooding conditions may induce the reduction of Fe and Mn to toxic levels for most crops. The high Ca and Mg concentrations generate additional problems leading to difficult uptake of other nutrients by plants, and hence poor plant growth, especially when the K content is low. Even though Ca phosphate complexes are the most soluble among all phosphates, a plant’s ability to use P is limited owing to its binding to Ca. Additionally, the content of minor cations is low in response to the high pH. All of these lead to serious limitations on plant growth. The basic nutrient management strategy for Vertisols is

maintenance fertilization with particular consideration of the levels of K and Zn (Sancho et al.1984). Sulfur fertilization may also be useful (Bornemisza 1990). The 2:1 clays display a high cation retention capacity, especially for K and NH4, on both the external and the internal surfaces, resulting in peculiar behaviors of these cations. To reduce K-induced deficiencies, this element needs to be applied, particularly for annual crops. The use of pesticides must be planned carefully when crop rotation is practiced since the active ingredients can be trapped in clay particles during the first culture cycle to be released later when irrigation is applied during the second cycle. Irrigation of Vertisols in Costa Rica will be possible soon because of the hydropower plant projects taking place in Guanacaste Province. Significant investments in infrastructure, such as canals, need to be done in order to achieve a sustainable and profitable use of such irrigation. Research and technology adaptation

Soils of Costa Rica 73

programs are needed to ensure, for example, that the expandable clays will not destroy the new infrastructure. Alfisols and Ultisols

The oldest and most weathered soils of Costa Rica belong to these orders, the differences being chemical and found in the subhorizon. Alfisols have more basic subhorizons and, particularly in Costa Rica, occur in dryer environments. In agronomic terms, both types of soils have a very similar “plow layer.” The real differences arise after intensive use, when Ultisols start exhibiting more marked fertility problems. In Costa Rica, these soils occupy a large area: about 31 percent of the territory (21 percent Ultisols, 10 percent Alfisols). In older times, and in other regions of the tropics today, the prevalent land use for these soils was slash-and-burn agriculture. This is not relevant in Costa Rica today because of the high input agricultural system, the wet climatic conditions where natural vegetation cannot be burned, and the high quality requirements for agricultural products. In general, they are considered marginal for contemporary agriculture because of their low and rapidly declining fertility, and only some of them are in use, particularly for roots, tubers, and pineapple. During the beef cattle boom of the 1970s, these soils were most preferred for grazing purposes. However, the cattle degraded these soils rapidly. Most of these pastures were abandoned, leading to abandoned grasslands, secondary shrublands, and, eventually, to secondary forests. These soils, however, have some good functions when properly managed. Virtually all the pineapple produced in Costa Rica is grown on these soils, as well as significant amounts of citrus, mango, avocado, palm heart (palmito), sugarcane, roots and tubers, etc. In the Southern Pacific Region, large coffee plantations and Gmelina arborea plantations for pulp production are being established, although both face severe nutritional constraints. The acidity problems of many Ultisols might be reduced by liming, which decreases Al and increases fertility, or through the selection of species, varieties, or strains tolerant to acid soils and low P contents (Acuña and Uribe 1996, Uribe 1994). Ultisols are found in the Northern Zone of Costa Rica in Sarapiquí, San Carlos, and Cutris districts; in areas of the Southern portion of the country in Pérez Zeledón and Buenos Aires district and in the proximity of the border with Panama, as well as the foothills (Atlantic and Pacific) of the Talamanca Mountain Range (Fig. 4.5).The main areas containing Alfisols are located on the Nicoya Peninsula and, associated with Vertisols, on the flood plains of the Tempisque River. In these areas, commercial plantation forests of Tectona grandis, Bombacopsis quinata, and Gmelina ar-

borea have been successfully established, along with small coffee plantations. Alfisols also occur in the Central Pacific Zone in Grecia, Atenas, Orotina, and San Mateo districts, where small-scale fruit plantations (mango, tamarind, cashew, caimito) and recreational villas are the main forms of land use. Wherever they are found, these soils occupy the highest positions in the watersheds and along the slopes; that is, Alfisols are not subject to frequent addition of fresh materials and/or, are exposed to mild leaching conditions with consequent base accumulation at the subsoil (Fig. 4.6). These soils originate from the downward flow of water through the soil profile over long periods of time, under high temperature conditions and from practically any parent material. Their main feature is the presence of an argillic clay horizon formed from the water-borne migration of clay particles from the superficial horizons to the deepest layers of the soil. For this movement to occur, precipitation must be higher than potential evapotranspiration under freedrainage conditions, that is, the water table must extend very deep into the soil and be separated from the surface. This process involves the loss of Na, K, Ca, and Mg from the soil profile, leaving behind high concentrations of Al, Fe, and Si (tri and tetravalent cations) in greater extent in Ultisols than Alfisols. The high concentration of hydrated iron accounts for the reddish color of these soils. More specifically, they are brownish red to reddish in the concave parts of the relief and brownish yellow to yellow in the convex depressions when Fe is bound with water molecules. The most relevant criterion considered for classification of Ultisols and Alfisols is the presence of an argillic and/or kandic subsurface horizon, which is acid in Ultisols (humid tropics) and neutral or basic in Alfisols (dry/humid tropics). Kaolinites (1:1 clays) as well as Fe and Al oxides predominate in these soils (Alvarado et al. 2014b). Even when composed of fine materials, the formation of H bonds in 1:1 clays fosters particle aggregation and, therefore, a more developed structure. As these aggregates get coated by oxides a larger particle known as “pseudosand” is formed. In some regions, Fe and Al accumulation is so high as to allow their exploitation as bauxite. Such deposits, also known as plinthite, display a white mottled surface over a red matrix in which gibbsite can be found. The presence of stable aggregates in granular structures gives these soils excellent physical properties for agriculture, especially with respect to drainage. Overgrazing and intensive mechanization, however, can deteriorate their favorable physical properties irreversibly. Liming improves fertility, but when excessive, increases erosion by favoring clay deflocculation. Such effects influence productivity much more drastically in Ultisols, because of their low fertility. Unfor-

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tunately the good aggregation qualities of these soils also result in ideal conditions for nutrient losses, especially bases (Ca, Mg, K). This in turn, brings about severe acidity problems, including toxicity caused by Al and to a lesser extent Mn, and P availability problems due to its fixation on Fe and Al oxides and hydroxides surfaces. The rapid leaching also results in poor Effective Cation Exchange Capacity (ECEC) owing to a restricted specific surface of clay particle aggregation. Because no favorable conditions for organic matter accumulation are present, nitrates are easily lost by leaching and N availability is always limited (Schwartz 1998). Leaching of micronutrients due to acidity results in deficiencies more commonly observed in even older soils highly exposed to run-off. All of these properties in turn account for the low fertility of Alfisols and especially Ultisols. The priority in managing these soils is replacing the lost Ca and Mg by liming, along with the selection of acid tolerant

Fig. 4.5

Distribution and characteristics of Ultisols of Costa Rica.

germplasm. Agriculture is possible in these soils with an intense and well-balanced N-P-K fertilization program if an adequate supply of minor elements is included. The use of organic fertilizers, along with liming, can be an important source of nutrients while at the same time improving the physical properties altered by soil mismanagement.

Environmental Relationships between Soils, Litter, and Organisms Soil as a Habitat

Many different types of animals live in and around the soil, leaving imprints in soil formation, nutrient recycling, and environmental biodegradation of organic residues (including pesticides), which have long been reported in tropical environments. Among the types of effects that animals

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Fig. 4.6

Distribution and characteristics of Alfisols of Costa Rica.

leave in the soil, secretion of binding substances, burrows, and soil particle transportation (including organic matter/ plant residues, clay, silt and sand particles), are mostly mentioned. Earthworms, termites, and ants are most visible, but other animals, like rodents, birds, and crabs, contribute to mixing soil material in specific environments as well. There is a group of animals that just live on the soil, causing little effect on its properties, including snails, snakes, and deer (Fig. 4.7).The various ways animals affect soil properties vary among them, mainly because of their size and number in the soils. The following sections intend to document these effects on Costa Rican soils. Bacteria and Fungi

Bacteria and fungi in soil and soil litter are the most abundant organisms. From the agricultural perspective most of

these microorganisms are harmful and well-studied, particularly when they turn into diseases for agricultural crops. Here, we describe several free N-fixing microorganisms and their host plants: Rhizobium/Phaseolus leguminosarum (bean), Rhizobium/Erythrina (poró), and Frankia/ Alnus acuminata (alder). Mycorrhizae are discussed when related to forestry species (Fig. 4.8). Numerous publications address the beneficial effects of Rhizobium to the production of common Phaseolus beans, as well as the various soil properties that negatively affect the symbiotic relationship between the two partners (Ramírez and Alexander 1980a,b, Araya et al. 1986, Uribe et al. 1990, Acuña and Ramírez 1992a, Uribe 1993a,b, Castro et al. 1993, Acuña and Uribe 1996); similarly other studies emphasize the relationship between Rhizobium/Glycine max (Acuña and Ramírez1992b, Acuña et al. 1987, Ortiz et al. 1986, 1990), and others explain the relationship Rhizobium/Erythrina (Escobar et al.

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Fig. 4.7

Snails in gardens and snakes in teak plantations in Costa Rica. Both are animals that live on top of the soil but have little effect on its properties.

Fig. 4.8

Arbuscular mycorrhizae in teak roots and Frankia nodules in Alnus acuminata roots growing in Costa Rican Alfisols and Andisols, respectively.

1994, Ramírez and Flores 1994, Gross et al. 1993, Nygren and Ramírez 1993, 1995, Nygren et al. 1993). The symbiosis between Frankia and A. acuminata is also documented in various papers (Álvarez 1956, Russo 1989, Meza 1994, Segura et al. 2006). In the case of the mycorrhizae the available information mainly discusses the effects of its interaction with seedlings and trees in forestry nurseries and forest plantations (Vega 1964, Rojas 1992, Gadea et al. 2004, Alvarado et al. 2004). Nematodes

Most nematodes are plant-parasitic species (e.g., see López and Salazar 1987), although a few free living nematodes exist in Costa Rica (Zullini et al. 2002). Various authors

describe how soil texture, humidity, cation exchange capacity, pH, and organic matter content affect nematode population dynamics, directly and indirectly, by affecting the growth of living vegetation. In general, plant-parasitic nematode populations decrease with soil depth owing to a reduction in root biomass in the least aerated subsoil horizons; this has been proven for Meloidogyne incognita and Rotylenchulus reniformis on papaya plantations ( Jiménez and López 1987), and rice fields all over Costa Rica (López and Salazar 1987, López 1988), with the exception of Longidorus sp. and Criconemella palustris. However, the population of nematodes depends to a major degree on the parasitic species they feed upon (López 1981), the crop phenology (Esquivel 1994), and the crop distribution in the field (Meneses et al. 2003). In order to control nematodes

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in banana plantations, nematicides were used in the past, causing human infertility to employees spraying the chemical, as reported by Ramírez and Ramírez (1980). Arthropods

McGlynn et al. (2007) tested the effects of soil and litter nutrient stoichiometry on the invertebrate litter fauna of a Costa Rican tropical rain forest. Animal densities were estimated from 15 sites across a phosphorus gradient. The density of the invertebrate litter fauna varied, and was strongly tied to soil and litter phosphorus concentrations. An increase in phosphorus concentration corresponded with an equally proportionate increase in animal densities. Natural variation in nutrient levels can thus serve as a predictor of density in a highly diverse tropical animal community. Haggar and Ewel (1994) found that on fertile soils in the humid lowlands at La Selva Biological Station, phosphorus is abundant and preliminary data indicate that much of the organically bound P is under microbial control. Under the dry-wet climatic conditions of the Central Valley of Costa Rica, Herrera and Fournier (1977) and Fraile and Serafino (1978) found that soil and litter moisture availability plays an important role in determining the density and vertical distribution of soil microarthropods; Collembola, Protura, Symphyla, and Acarina were those most adversely affected by rainfall, while Coccoidea and other groups were unaffected by it (Fraile and Serafino 1978). Also, the invertebrate population was more diverse and stable in the oldest forest, but populations increased when litter moisture content increased with the first rains (Herrera and Fournier 1977). Populations of arthropods decrease with elevation above sea level (Bruhl et al.1999). Atkin and Proctor (1988) studied the litter and

Fig. 4.9

soil fauna in1 ha plots at six altitudes along a transect ranging from 100 to 2,600 m a.s.l. on the Caribbean slope of Barva Volcano. They showed that the invertebrate biomass in soils at 100 and 500 m a.s.l. seem to be the highest ever recorded for tropical rainforests. This is partially attributed to the presence of a clear soil temperature gradient (Fig. 4.9). Springtails

Guillén et al. (2006a) studied the diversity and abundance of soil springtails (Collembola) in a primary forest, a secondary forest, and a coffee plantation, in Tapantí National Park. Each month, eight soil samples were taken in each ecosystem, totaling 360 samples. A total of 23,751 springtails were found, belonging to 9 families and 16 species. Of the three ecosystems, the primary forest was the most diverse (H’ = 2.406), followed by the secondary forest (H’ = 2.174), and the coffee plantation presented the lowest diversity (H’ = 1.651). In contrast with diversity, the greatest abundance of springtails was found in the coffee plantation with 10,111 individuals. Guillén et al. (2006b) also found that the largest springtail biomass is associated with the highest organic matter content, lower penetration resistance, and lower pH values of the primary forest. The results showed an association between these variables and some collembolan species, which indicates that changes in the structure of collembolan communities can be used as biological indicators of soil quality and management of ecosystems. Ants and Termites

In Costa Rica, 85 genera and at least 620 species of ant have been identified so far (Longino and Hanson 1995,

Examples of Quilopoda and Diplopoda, common in soil litter of Costa Rican soils at mid-elevation.

78 Chapter 4

Hölldobler and Wilson 1990). However, the number of genera and species present in different agroecosystems varies between 9– 16 genera and 13– 23 species in coffee plantations (Benítez and Perfecto 1989, Perfecto and Vandermeer1994, Barbera 2001), and 10– 19 genera and 16– 26 species in cacao plantations (Young 1986). The influence of some of these species on Costa Rican soil properties is also being recognized. Araya and Alvarado (1978) and Araya (1980) determined the influence of leaf-cutter ants (Atta cephalotes) on the chemical and morphological properties of soil of the Premontane Wet forest (Fabio Baudrit Experimental Station), the Premontane Wet forest transition to lowland (Santa Rosa National Park), and the Tropical Wet forest transition to per-humid conditions (La Lola farm). Results shows that vertical translocation of materials from the upper to the lower soil horizons and vice versa is large, and varies in different ecosystems; values of cation exchange capacity in ant-affected and undisturbed soil were 30 and 50 cmol(+) 100g− 1, respectively, while Ca, Mg, and K contents were 2 and 23, 1 and 28, and 0.36 and 1.6 cmol(+) 100g− 1, respectively. Other soil properties, like organic matter content, available P, pH, and sand, silt, and clay content, were also affected significantly. Alvarado et al. (1981) studied the influence of leaf-cutter ants (A. cephalotes) on the morphology of twenty-seven soil profiles of Andisols distributed within a 2.5-ha site in Turrialba, Costa Rica. Leaf-cutter ant influence on each profile was noted in 85% of the soil profiles or pedons. The influence on each profile was estimated, and out of all profiles, 37% had low, 26% medium, and 22% high disturbance. The surface area covered by leaf-cutter mounds was 38.9% of the study area; only 1% of the aboveground disturbed area was active, however. Leaf-cutter ants transport material from the AB and B horizons to the soil surface, producing a new A1 horizon. In addition, some subsoil chambers are filled with plant material. Knowledge of termites that are active at soil level is still scanty, however (Fig. 4.10). Worms

Monge and Alfaro (1995) studied the geographical variation of habitats in Costa Rican velvet worms (Onychophora: Peripatidae), comparing 20 onychophoran localities from the seasonally dry western Pacific forest to the rainforests of the Caribbean. The authors found that the Costa Rican species Epiperipatus biolleyi Bouvier, compared with the Brazilian species Peripatus acacioi, was found (1) in sandy, not clay-rich, soil, (2) closer to the surface, and (3) in burrows whose temperature is more similar to the external air temperature. For both species the sod humidity (mean, 35%) and acidity (pH = 5.2– 6.2) were similar. The E. biolleyi

Fig. 4.10 Leaf-cutter ant (Atta cephalotes) (top) and termite mounts (bottom) in grasslands.

population density was 0.25 individuals m− 2, and no clearcut trends in associated flora and fauna were found but the animals preferred rotten to non-rotten wood, and watersoaked soil to oven-dried soil, during periods of inactivity. Earthworms

The knowledge of soil-born native earthworm species of Costa Rica is limited. Esquivel (1997) found no relationship between density of earthworms and different agroecosystem properties in the wet humid lowlands of the Atlantic Zone; the author found an average of 194 individuals m− 2, with Pontoscolex corethrurus being the dominant species owing to its high adaptability to disturbed ecosystems. López and Kass (1996) found that Erythrina mulch and mucuna green manure treatments resulted in better phosphorus balances and higher earthworm populations and increased the yield of common bean (Phaseolus vulgaris).While sampling earthworm communities at eight sites of the Caribbean Coast to assess the distribution of the peregrine pantropical species P. corethrurus and its

Soils of Costa Rica 79

Fig. 4.11

Earthworms and earthworm casts in Inceptisol grasslands of Guanacaste, Costa Rica.

relationships with native species depending on the type of land use, Lapied and Lavelle (2003) found that this species is largely dominant in almost all habitat types with a density range of 143 to 182 individuals m− 2.The species became dominant even in remaining plots of primary forests. In contrast, the species has not yet penetrated the large primary forest of the northeast of the country, where only native species could be found, and reached a maximum density of ca. 361 individuals m− 2 in banana plantation sites. In all sites, a density increase of this species corresponds significantly with a reduction of the rest of the earthworm fauna except for Dichogaster sp. Where P. corethrurus was absent, density of other species reached 34.4 individuals m− 2. In southern Costa Rica, human immigration and sustained activities probably favored the establishment of P. corethrurus. León, Bolaños, and Fraile (1993) studied the relationship between edaphic conditions and the abundance and biomass of earthworms at eight sites in Costa Rica where organic waste accumulates, finding that the abundance and the biomass of P. corethrurus follows models that depend on soil carbon percentages (Fig. 4.11). Crabs

The land crab Gecarcinus quadratus (Gecarcinidae) lives in densities exceeding 10,000 adults ha− 1 in the coastal forests of Corcovado National Park, Costa Rica (Fig. 4.12). Crabs, living solitarily in half-meter deep burrows, forage nocturnally, transporting plant propagules and fallen leaves to subterranean chambers. The influence of G. quadratus on the distribution of soil organic carbon and root distribution in a Costa Rican rain forest was studied by Sherman (2006). Percent organic carbon in the crabzone (CZ) soils decreased

with depth. The carbonless zone (CLZ) soils contained significantly more carbon at the topsoil and 32 cm depths but significantly less carbon at 72 cm. Carbon values at these depths, however, differed in regards to season. Vertical root profiles taken from the adjacent zones all indicated greater densities at the surface soils than below. The CZ had relatively lower root densities in the top 15 cm of the soil than the nearby CLZ. Surface densities of very fine and fine roots were 50% and 72% lower in the CZ than in the CLZ respectively. Rodents

Many rodent species spend their lives in and around the soil, where they mix large amounts of material while digging the ground to build their nests and tunnels. According to Reid (1997) rodents of Costa Rica include 2 suborders, 8 families, and 48 species. Among the families, 33 species of rats and mice are most abundant in soil ecosystems. They belong to the families Muridae, Heteromyidae, and Echimyidae; the remaining rodents belong to Sciuridae (5 species of squirrels), Geomyidae (4 species of pocket gophers or taltuzas), and one species each in the Erethizontidae (porcupine), Dasyproctidae (guatusa), and Agoutidae (agouti, tepezcuintle) (Fig. 4.13). Rodents can be grouped by size, according to Javier Monge (University of Costa Rica, pers. comm.), as follows: (1) large rodents (>2 kg/adult) such as the agouti or tepezcuintle (Agouti paca), the guatusa (Dasyprocta punctata), and the porcupine (Coendou mexicanus); (2) medium-sized rodents (0.1– 1 kg/adult), including squirrels (Sciuridae), taltuzas (Geomyidae), and large rats (Echimyidae), and (3) small rodents (< 0.1 kg/adult) that includes other rats and mice

80 Chapter 4

Fig. 4.12

Crabs on a sandy beach close to a mangrove forest at Montezuma, Guanacaste, Costa Rica.

(Muridae and Heteromyidae). The pocket gophers occupy many ecological niches, except those with clayey soils. To give an idea of the amount of soil material reworked by this species: their nesting chamber might be up to 60 x 110 x 30 cm in width, length, and height, respectively; their tunnels can be as long as 192 m but average values lie between 30– 80 m, disturbing an area of around 200– 325 m2 per individual (Monge 2006). According to Rodríguez and Vaughan (1985), a female agouti (D. punctata) has a home range of 3.9 ha, and maximum and minimum distances travelled daily reach 1,800 and 727 m, respectively. When roaming around in the La Selva tropical rain forest, agoutis not only mix soil materials but also help transport Carapa guianensis seeds (Arias 2001). The species is also the main secondary disperser of large seeds in the cloud forest of Monteverde (Wenny 2002). Fig. 4.13 An agouti ( Agouti paca, tepezcuintle) in captivity, Buenos Aires, Puntarenas, Costa Rica.

Cattle

In the dry tropical ecosystems of Guanacaste, various authors have found that cattle grazing: (1) improves seed

Soils of Costa Rica 81

Fig. 4.14

Soil compaction under shading trees (left) and hillside erosion (right) caused by cattle trampling in Guanacaste grasslands, Costa Rica.

dispersion via excreta of Enterolobium cyclocarpum and Crescentia alata ( Janzen 1982a,b, Alvarado et al. 1982), (2) increases soil P availability, (3) reduces bulk density under dung droppings from 1.05 to 0.93 g cm− 3, (4) increases soil porosity from 13 to 21% (Herrick and Lal 1995, 1996), and (5) decreases aboveground residue accumulation, thus reducing fire frequency in dry tropical environments (Barbosa 1994). Changes in chemical properties of the soils are not as clear (Daubenmire 1972, Johnson and Wedin 1997). While evaluating the compaction and compactability of agricultural and cattle-raising soils in Guanacaste, Agüero and Alvarado (1983) found in cattle areas compaction average values of 62 kg cm− 2, values that doubled the ones found in cropping lands (average 30 kg cm− 2). These effects on the soil physical characteristics delay the regeneration of natural forest. The effect of cattle dung on the physical properties of the dry tropical pasture lands of Guanacaste was studied by Herrick and Lal (1995, 1996); these authors found an increase of soil porosity from 13 to 21% in the soil without dung, and under dung additions, respectively (Fig. 4.14).

Soils and Vegetation As previously stated, to a certain extent soils can help determine the best land use. However, land use naturally affects soil properties, effects enhanced by human activities. As an example, the distribution of the cloud forest (wet tropical montane forest) and páramo vegetation at Cerro de la Muerte and Cerro Chirripó is associated with climatic and edaphic altitudinal gradients (Kappelle and van Uffelen

2005, 2006, Kappelle and Horn, chapter 15 of this volume). Inversely, in the same region, Blaser and Camacho (1990) described the occurrence of two types of soils developed from volcanic ash under different vegetation cover. Below the cover of mixed oak forest (Chusquea talamancensis, Quercus costaricensis, Grammadenia myricoides, Prunus cornifolia, and Vaccinium consanguineum), Placudands are dominant. However, below the white oak forest cover (Chusquea tomentosa, Ardisia glandulosa-marginata, Quercus copeyensis, Weinmannia pinnata, Ocotea spp., Nectandra spp., Styrax argenteus, and Ilex spp.), Dystrudands are dominant. The difference between the two soils is considerable, since Placudands present a thin hard layer of iron known as “placic horizon” formed by preferential movement of Fe, chelated by organic substances produced under the specific oak trees, thus impeding good drainage. Among the various reasons explaining shifting cultivation in tropical environments, Sánchez (1985) mentions soil fertility decline, weed invasion, and the impact of insects and diseases on crop yield over time. The issue of soil fertility decline is strongly related to low-input agricultural systems, and usually associated with soil organic matter depletion, nutrient leaching and retention in highly weathered soils, and nutrient extraction via agricultural and forestry products (Hartemink 2003). Recently, studies on soil carbon sequestration tend to provide an alternative to identify proper land uses, with the purpose of recycling residues, planting crops that enhance soil organic matter accumulation, and applying environmentally friendly soil practices (Lal et al. 2006). The next paragraphs describe the main factors that affect Soil Organic Matter (SOM) in Costa Rica.

82 Chapter 4

Soil Organic Matter Differences in Soil Organic Matter (SOM) by Life Zone

Data collected by Alvarado (2006) show that Soil Organic Matter (SOM) content in Costa Rica increases from the tropical (warm) to the montane (cool) belt, both in the topsoil and subsoil (Table 4.1). The amount of residues added to the ecosystem in natural forests of Costa Rica decreases with altitude above sea level (Heaney and Proctor1989), 9.0, 6.6, 5.8, and 5.3 t ha− 1 year− 1 at elevations of 100, 1,000, 2,000, and 2,600 m a.s.l., respectively. This is due to lower photosynthesis rates and exposition of vegetation to strong winds. However, the accumulation of residues under cool mountainous weather ecosystems is explained in terms of having low N content (Heaney and Proctor 1989), being hard and waxy (Holdridge et al.1971), containing high amounts of phenols (Montagnini and Jordan 2002), and having a low population of arthropods (Bruhl et al. 1999), all of them contributing to a reduction of residues’ mineralization rates (Tanner et al. 1998). Powers and Schlesinger (2002a) also attribute this accumulation to the occurrence of amorphous clay minerals in mid-elevation Andisols in Costa Rica. These minerals make it difficult for organic materials to easily decompose. Table 4.1.

As precipitation increases along vegetation gradients, soil organic matter increases, although the effect of temperature is more acute than that of moisture. Residue in lowland humid tropical forests undergoes a fast and efficient recycling process, hence its short life span in the ecosystem (Montagnini 2002). In tropical forests, the production of residue increases with average annual rainfall (Bernhard and Loumeto 2002) and its accumulation lasts only for the length of the dry season period. On the basis of Holdridge’s Life Zone distribution and area (ha) in Costa Rica, a total of 1,348.2 Tg of SOM was calculated for the country (Table 4.2). The life zones that contribute the most to SOM in Costa Rica are Premontane Wet Forest (391.0 Tg), Tropical Moist Forest (203.2 Tg), and Premontane Moist Forest (172.9 Tg), respectively. Differences in Soil Organic Matter (SOM) by Soil Type

Small areas of peat deposits (Histisols) have been found in Costa Rica as the following: (1) thin blanket deposits about 1 m thick in the highlands of the Talamanca Range (e.g., at La Chonta close to El Empalme along the Inter-American Highway), such as in Sphagnofibrists (Kappelle and van Uffelen 2005), (2) peat layers interbedded with alluvium layers

Soil Organic Matter (SOM %a) Content as Related to Holdridge’s Life Zones in Costa Rica

Life Zone

Dry

Moist

Wet

Tropical Premontane L. Montane Montane

3.3/1.0 (7)

3.3/0.9 (7) 6.3/2.8 (2) 4.9/1.6 (1)

4.3/1.3 (13) 6.9/2.20 (6) 19.1/4.9 (1)

AVERAGE

3.3/1.0 (7)

4.8/1.8 (10)

10.1/2.8 (20)

Rain forest

AVERAGE

6.6/2.0 (5) 20.4/6.7 (3) 19.8/Rock (1)

3.6/1.1 (27) 6.6/2.3 (13) 14.8/4.4 (5) 19.8/Rock (1)

15.6/4.3 (9)

SOM (0– 0.30 m) / SOM (0.31– 1.00 m) (Number of samples). Source: Alvarado 2006.

a

Table 4.2.

Soil Organic Matter (SOM) Stock in Costa Rica Calculated by Holdridge’s Life Zones

LIFE ZONE (LZ)

Extension (Ha x 1,000)

Tropical dry forest Tropical moist forest Tropical wet forest Premontane moist forest Premontane wet forest Premontane rain forest Lower montane rain forest Montane moist forest Montane wet forest Montane rain forest COSTA RICA

150.3 1,058.2 1,083.6 556.7 1,217.7 445.3 137.6 335.5 1.9 118.7 5,105.6

NOTE. nd = no data are available. Source: Alvarado 2006.

Mg SOM to a depth of (m) x = 0.3

y=1

SOM / LZ (Tg)

No. of samples

82.7 119.9 86.9 193.5 191.6 86.1 309.6 188.2 228.3 244.3

142.9 192.0 144.4 310.5 321.1 291.2 586.2 342.0 420.8 651.6

21.5 203.2 156.5 172.9 391.0 129.7 80.7 114.7 0.8 77.3 1348.2

7 7 13 2 6 5 3 1 1 6 51

Regression equation

Regression coefficient

y = 1.2697x + 37.852 y = 1.4993x + 49.034 y = 1.1008x + 4.7945 nd y = 2.6939x − 59.582 y = 6.283x − 249.47 y = 1.7414x + 220.37 nd nd y = 1.4338x − 24.441

0.955 0.5945 0.9127 nd 0.9598 0.9803 0.9994 nd nd 0.9372

Soils of Costa Rica 83

south of Lake Nicaragua (Cocibolca), and (3) thick layers of peat at the Parismina River Basin. The accumulation of organic materials is the result of tectonism and volcanism (Cohen et al. 1986), including the burial of large amounts of vegetation by volcanic debris, and low temperature in the highlands. Apart from catastrophic events, above- and belowground factors that decrease or increase carbon pools in soils are those presented in Lal and Kimble (2000) and Buurman et al. (2004). A study conducted in Costa Rica by Cabalceta (1993) to evaluate different methods for extracting soil-available nutrients also included SOM determinations as a part of the soils’ characterization. In this study, 25 topsoils of each of the 4 major soil orders of the country were sampled, and results are presented in Table 4.3. The author reported a sequence for SOM content in the A soil horizon, in the following order: Vertisols < Inceptisols < Ultisols < Andisols. It is noteworthy that the larger the average of SOM of a particular soil order, the larger the range of its Soil Organic Content (SOC) is. Under natural conditions, the sequestration of SOC in each soil order can be increased up to the maximum value of its range. However, unpublished results in organic farming systems show that in spite of the large amounts of compost or organic residues applied (10– 30 Mg/ha), the total amount of C in soils rarely increases. According to

Table 4.3. Soil Organic Matter (SOM %) Content in 100 Samples of Vertisols, Inceptisols, Ultisols, and Andisols (25 A Horizons of Each Order) from Costa Rica Soil Order

Minimum

Maximum

Average

Vertisols Inceptisols Ultisols Andisols

1.6 1.0 1.9 4.8

5.9 9.9 9.7 24.0

3.5 4.2 5.7 10.9

Adapted from Cabalceta 1993.

Table 4.4.

Schlesinger (2000), only a small sink for SOC in soils may derive from the adoption of conservation tillage and the regrowth of native vegetation on abandoned agricultural land, but no net sink for SOC is likely to occur through application of manure to agricultural lands. Soil organic matter contents for the country calculated by soil order (Alvarado 2006), came to a total of 1,445.7 Tg (Table 4.4), which is in fact a larger amount than found when using the Life Zone approach (Table 4.2), though within reasonable assumptions. SOM depends on soil order, reflecting their genesis: Entisols 10 m broad. Other hemiepiphytes, like species of the melastome genera Blakea and Topobea, produce multiple trunked, shelf-like crowns extending 5 m or more from the trunks of their hosts. Some hemiepiphytes, such as the large herbaceous shrub Begonia estrellensis, are pendent from the limbs of their hosts. The line between lianas and hemiepiphytes is often blurred in cloud forest. Plants like Marcgravia brownei and Hydrangea peruviana are scrambling climbers, with feeding roots running down the host trunk to the ground, and

multiple points at which the clustered stems comprising the crowns are lashed to the host with webs of attachment roots (Williams-Linera and Lawton 1995). Such scramblers may also have specialized colonizing or traveling stems, with very long internodes and reduced leaves, and functioning much like stolons, but running as far as 10 or 15 m between adjacent tree crowns. Stranglers are conspicuous in the montane forests of northern Costa Rica. Most are urostigmoid figs, the classical tropical strangler figs; in the Monteverde region, there are six species. The cloud forest habitat, however, seems to favor the evolution of strangling, probably because juvenile establishment is relatively easy in the well-developed and nearly permanently moist epiphytic soils. A fig in the subgenus Pharmacosycea, F. crassiuscula, has independently evolved the strangling habit from a free-standing ancestor (Lawton 1986, 1991). F. crassiuscula begins life as a sprawling vine growing on tree trunks and logs, and at this stage exhibits no host preferences. In successful individuals a single leader metamorphoses into an erect, free-standing stem, usually occurring 5– 12 m up the trunk of a host canopy tree. This occurs more commonly on species of Guarea, particularly G. kunthiana, than the abundance of these host species would suggest (Daniels and Lawton 1991). Subsequent growth to maturity involves extension of the trunk above that of the host, expansion of the crown, and thickening and limited ramification of the roots into a strangling “trunk”; this too is more likely than expected on Guarea. In addition to the Urostigma figs and F. crassiuscula, a number of other tree species sometimes successfully strangle their hosts. Some are more commonly free-standing trees that facultatively grow as hemiepiphytes, but may outgrow their hosts and become self-supporting. Weinmannia pinnata is the most conspicuous of this group. Others are commonly hemiepiphytic, but may also outgrow their host. This is most common in the elfin forests, where this group includes Clusia sp., Schefflera rodriguesiana (= Didymopanax pittieri), Cosmibuena valerii, and Oreopanax nubigenus. Quantitative comparisons of growth form diversity among habitats will require the development of clearly defined measures of growth form characteristics. Phenology

Patterns of fruiting and flowering have wide-ranging impacts on other species. Groups as disparate as pollinators, seed dispersers, and herbivores often structure their reproductive efforts to take advantage of the predictable patterns of increased resource availability that fruits and flowers represent. In the Monteverde area at least 10% of tree species (~60 species) are fruiting or flowering in any given month

The Montane Cloud Forests of the Volcanic Cordilleras 433

(Haber 2000). Many species (~100) bloom in the late dry season (March-May) to take advantage of the clear dry season days that make it easy for pollinators (and/or pollen) to fly, and to use the increased moisture availability of the upcoming rainy season to aid in fruit/seed set and maturation. Likewise there is a flowering minimum during the times where pollinator/pollen movement would be difficult: during the heavy rains from September to November, and during the high winds of December (Haber 2000). Most species (excepting figs) flower and fruit only once a year, at about the same time each year (Haber 2000). Many species, however, do respond to variation in the weather. During El Niño years some species shifted flowering by 6 months, others flowered twice, and still others did not flower at all (Haber 2000). The impacts of a changing climate on patterns of flowering and fruiting remain to be explored.

Animals Our knowledge of animals in the mountains of northern Costa Rica is the product of a long history of collection, and a diverse series of studies with particular aims rather than systematic efforts to assess the fauna as a whole. Those studies in the Cordillera de Tilarán have been well summarized in the chapters of Nadkarni and Wheelwright (2000). Our aim here is to summarize more recent research, and briefly present some of the important elements of the earlier studies, particularly as they illustrate how species activities, ranges, and interactions might be influenced by changing environmental circumstances. Arthropods

Arthropods are staggeringly diverse. Our current knowledge, however, of the natural history, ecology, evolution, and distributions of arthropod taxa is relatively sparse. This is no less true in the mountains of northern Costa Rica than in the rest of the world. The majority of current knowledge of arthropods in this region consists of small studies of particular arthropod systems, much of which is nicely reviewed in Hanson (2000). The predominant theme in the literature seems to be lamentation about the lack of extensive sampling of arthropods. No large-scale sampling such as the ALAS project in La Selva, Costa Rica, has been conducted along cloud forest elevational gradients in northern Costa Rica. However, some taxa have received careful scrutiny. For example, Longino (2006) recently carried out a detailed examination of the neotropical arboreal ant genus Myrmelachista. Much of what is known about montane

arthropods in northern Costa Rica has resulted from work conducted in Monteverde (750– 1,850 m) and Zurquí de Moravia (1,600 m). One of the things that sets montane cloud forest apart from lowland forest is a huge increase in epiphytic biomass. These epiphytic mats provide a very interesting microhabitat in which arthropods can specialize. Montane cloud forests in northern Costa Rica have a rich diversity of arboreal arthropods that live in epiphytic mats (Hanson 2000). Examples of recent work that has examined these arboreal arthropod communities in Monteverde are Yanoviak et al. (2004, 2007) and Schonberg et al. (2004). Yanoviak et al. (2004) examined the differences in arthropod communities in vegetative and humic portions of epiphytic mats. Schonberg et al. (2004) investigated the differences between arboreal ant assemblages in primary forest, secondary forest, and pasture trees, finding that arboreal ant species density is reduced as primary forest is converted to secondary forest and that pasture trees may serve as repositories for primary forest arboreal ant assemblages. Though arthropod diversity generally decreases with increasing altitude, the mountains of Costa Rica are by no means depauperate. There is a large diversity of known arthropods in these mountains, and many of the more cryptic species as well as those living in habitat that is harder to access undoubtedly remain without sampling. This does not mean, however, that there is a paucity of interesting arthropods that have been collected. Among the more exotic known arthropods in the Cordillera de Tilarán is the grasshopper Tropidacris cristata, which has a body up to 15 cm in length, making it one of the largest grasshoppers in the world (Hanson 2000). Altitudinal gradients have been shown to be important for arthropods in Costa Rica. For example, O’Donnell and Kumar (2006) recently showed that increasing elevation in Monteverde affects army ant community structure and behavior. Army ants (Ecitoninae, and behaviorally convergent Ponerinae) form large foraging groups that raid the forest floor, canopy, and human habitations. The rate of these raids, which appear to drive a number of interesting ecological interactions with birds and other organisms, decreases with increasing altitude. The strong altitudinal gradients in Costa Rican mountains are also very important for butterflies, over half of which are altitudinal migrants in Monteverde (360 out of 658 species) (Hanson 2000). As most arthropods have relatively narrow altitudinal distributions they may be quite susceptible to climate change. The increasing frequency of dry spells in the dry season and lifting cloud base heights could both affect arthropod distributions and behaviors (Lawton et al. 2001). As moisture and temperature gradients change with changing

434 Chapter 13

regional climate, the distributions of many arthropods will shift as well. Yanoviak et al. (2007) recently found that arthropod morphospecies richness in epiphytic mats decreases in the dry season, presumably because desiccation-sensitive arthropods are going dormant or hiding very deep in the mats. Longer dry spells in the dry season could substantially alter the wetting and drying cycle of these epiphyte habitats and thereby disrupt the population and community dynamics of arboreal arthropods. Another group particularly sensitive to this sort of change may be migratory insects such as butterflies, which depend on two or more habitat types at different altitudes (Hanson 2000). Amphibians and Reptiles

Studies in the cloud forests of northern Costa Rica have strongly influenced the ongoing discussion about the causes of the global amphibian decline (Pounds and Crump 1994, Pounds et al. 1997, 1999, 2005, Pounds 2000, 2001, Pounds and Puschendorf 2004). Such studies illustrate how important it is to know local environments and patterns of species distribution in order to interpret ecological trends at larger spatial and temporal scales. Herpetofaunal Diversity

Knowledge of the herpetofauna rests on the work of Van Devender (1980) and Hayes et al. (1989). An updated checklist is provided by Pounds and Fogden (2000). From montane habitats in the Cordillera de Tilarán 161 species have been recorded— 60 amphibians (including 2 caecilians, 5 salamanders, and 53 anurans) and 100 reptiles (29 lizards and 71 snakes). This listing is probably incomplete for several reasons (Pounds 2000). First, there has been less collecting in peripheral and hard-to-reach areas. Second, secretive taxa, and those that occur at low density, are less likely to be encountered. Finally, some diverse and numerous groups, for example, the genus Eleutherodactylus, may contain as yet unrecognized species. Hayes et al. (1989) have described six zones in the Monteverde area marked by distinctive herpetological communities. These are related to elevation, and distributed as follows: Zone 1 on the lower Pacific slope from 690 to 1,300 m, Zone 2 on the mid-Pacific slope from 1,300 to 1,450 m, Zone 3 from 1,450 to 1,600 m on the upper Pacific slope, Zone 4 from 1,850 to 1,450 on the Caribbean slope (a zone commonly called “Continental Divide”), Zone 5 from 1,450 to 950 m on the upper Caribbean slope, and Zone 6 from 950 to 600 m on the lower Caribbean slope. From Zones 3 and 4, a total of 79 species of amphibians and reptiles are known, compared to 135 in a similar area at La Selva. The 161 species known above 600 m in the

Cordillera compares well, however, with the lowland fauna from La Selva, which emphasizes the importance of the diversity of local environments in the maintenance of herpetological diversity (Pounds 2000). No zone has a species list containing more than 52% of the species known from the range. Sixty-four percent of the species are found on only one side of the range; 60% of the snakes are found on the Pacific slope, while only 30% of the amphibians are. Amphibian Declines

Early studies of anuran population collapses at Monteverde focused on the golden toad, Bufo periglenes, and the harlequin frog, Atelopus varius (Crump et al. 1992, Pounds and Crump 1994). Following the initial collapse in 1987/88, a 2 x 15 km transect across the Cordillera de Tilarán was established in 1990 to monitor the herpetofauna (Pounds et al. 1997). From the pre-collapse information in Hayes et al. (1989), 50 anuran species were expected, but 25 of these were missing in 1990, although 5 reappeared in 1991– 1994, and one reappeared in 1997. These “reappearances” may be the result of colonization from outlying areas, since the reappearances were on the periphery of the study area, and 5 of the 6 were species found also in the lowlands, where there is little evidence of population collapses (Pounds 2000). Early discussions of the causes of the amphibian declines have been reviewed by Pounds (2000). Recently attention has been focused on the role of an emergent epidemic caused by the chytrid fungus, Batrachochytrium dendrobatidis (Pounds et al. 2005, Lips et al. 2006). Pounds et al. (2005) suggest that, as a result of global warming, tropical montane climates are changing in ways that both stress anurans, increasing their susceptibility to infection, and favor the growth of Batrachochytrium. In particular, they note that, although diurnal temperatures have declined in many neotropical cloud forest settings, nocturnal temperatures have risen more, increasing the mean temperature and decreasing the diurnal temperature range. This could be caused by an increase in the base height of orographic cloud banks and an increase in cloud cover. This combination would result in drier montane habitats with cooler days and warmer nights. At this point, coupled epidemiological and cloud climatological studies are needed to investigate the coupling of chytridiomycosis outbreaks and changing local climates in tropical mountains. Interestingly, some reptile populations declined along with the anurans in the Cordillera de Tilarán (Pounds 2000). Some of this is clearly due to trophic connections. The disappearances in 1987 of Drymobius melanotropis (the green frog eater), the fourth most commonly seen snake in the Peñas Blancas valley on the Caribbean slope, and in

The Montane Cloud Forests of the Volcanic Cordilleras 435

1988 of Chironius exoletus (the green keelback), the third most commonly seen snake of the upper Pacific slopes, are undoubtedly due to the loss of their primary prey (Pounds 2000). More intriguing are the declines in two anoline lizards, Norops altae and N. tropidolepis (Pounds 2000). The former originally occupied zones 3 and 4, while the latter was found in zones 2– 4. Both were common in primary forest at 1,540 m on the upper Pacific slope, but disappeared at that elevation, although they persist at higher sites. Their local decline and retreat to higher elevations is not directly caused by a chytrid outbreak, nor is it due to a loss of anuran prey. N. tropidolepis lives in shaded understory and its body temperature follows ambient air temperatures (Pounds 1988). It is active at the low temperatures of shaded cloud forest interiors, but feeds at low rates, and grows slowly. Females take nine months to reach maturity at 42 mm (snout-vent), while females of N. intermedius, found at warmer sites at lower elevations, reach maturity at 39 mm in only four months (Fitch 1973). The slow growth and longer generation time would hinder population recovery following collapse, but the primary factor prompting the retreat to higher elevations remains unclear. Clearly, detailed local demographic studies will be required to clarify the responses of such animals to changing climatic conditions. Birds

Most of the research on birds in the montane areas of northern Costa Rica has been concentrated in the Monteverde area of the central Cordillera de Tilarán. The local topographic diversity and microhabitat variety found within a small area— about 20 km2— has given ornithologists access to an area of high α- and β-diversity. Within the Monteverde area 6 Holdridge life zones are home to 425 bird species (Young and McDonald 2000, Fogden 2000). The richest life zone, Premontane Rain Forest, has 315 species, while the least rich, Lower Montane Rain Forest, has only 121, perhaps in part because of the limited area along the crest of the Cordillera in this life zone. Changes in the altitudinal ranges of bird species have contributed to the formation of the “lifting cloud base hypothesis” concerning faunal changes in the mountains of northern Costa Rica (Pounds et al. 1999), and have prompted renewed interest in the way bird community structure changes along the steep environmental gradients on the upper lee (Pacific) slope of the Cordillera de Tilarán ( Jankowski 2004, Jankowski and Rabenold 2007). Auditory species counts and capture data show nearly complete turnover in avian community composition in the upper 600 m in elevation of the upper Pacific slope— a distance of ~3 km from the continental

divide (Jankowski 2004). Transition in community composition is more gradual on the upper Caribbean slope, where there is a 32% Sørenson’s similarity between opposite ends of a 700 m elevation transect. This contrast between the slopes appears due to a more rapid transition in dry season moisture availability, and thus a more rapid transition from cloud forest to drier forest types on the upper Pacific slope. Much of the ornithological work in the Monteverde area has focused on birds as pollinators or seed dispersers; this work is discussed below in Pollination and in Seed Dispersal. Since many of the hummingbirds and avian frugivores are altitudinal migrants, the problems of habitat fragmentation, both on the Pacific slope of the Cordilleras and in adjacent lowlands, have been a matter of concern. There is considerable evidence that deforestation in seasonally critical habitats has put several local migrants at risk (Powell and Bjork 1994, Powell et al. 2000), and that forest fragments may play a vital role in maintaining populations of large obligate frugivores, such as the three-wattled bellbird and the resplendent quetzal (Guindon 1996, 2000). There has, in addition, been considerable work on mixed species foraging flocks (Buskirk 1976, Powell 1979, 1980, 1985, Valburg 1992, 2000, Shopland 2000), and autecological investigations of assorted species— for example, the house wren (Young 1993, 1994a,b, 1996, Winnett-Murray 2000), the emerald toucanet (Riley 1986, Riley and Smith 1992), and the yellow-throated euphonia (Sargent 1993). Long-term investigations have revealed much about cooperative behaviors in two systems: cooperative breeding of the brown jay (Cyanocorax morio), a social corvid (Lawton and Lawton 1980, 1985, 1986, Lawton and Guindon 1981, Lawton 1983, Williams et al. 1994, Williams and Lawton 2000, Hale et al. 2003, Williams 2004, Williams et al. 2004, Williams and Rabenold 2005, Williams and Hale 2006), and coordinated lek mating displays by male long-tailed manakins (Chiroxiphia linearis) (McDonald 1989a,b, 1993a,b, 2000, 2007, Trainer and McDonald 1993, 1995, McDonald and Potts 1994). Study of the nesting behavior of brown jays led Skutch (1935) to describe cooperative breeding, in which nonbreeding members of a group help the breeders raise their young. Cooperative breeding and helping at the nest excited much interest, due to the evolutionary questions raised by seemingly altruistic behaviors (Lawton 1982). A series of studies at Monteverde have clarified the social structure, the activities of helpers, the genetic structure of groups, the population and group dynamics, and the nature of competition for breeding status. Brown jays live in large, territorial flocks (6– 20 birds), in which all members collaborate to build the nest; feed the breeding females, nestlings, and fledglings; defend the territory; and harass potential preda-

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tors (Skutch 1935, Lawton and Guindon 1981, Lawton and Lawton 1985, Williams and Lawton 2000). Brown jays, which are absent from closed evergreen forest, did not occur in the complex of pastures, woodlots, and windbreaks of the Monteverde community prior to the early 1960s, but after colonization from the farmlands of the San Luis valley below, grew in abundance, reaching 101 birds in 14 flocks prior to the breeding season in 1978 within an area of about 4 km2. Groups ranged in size from 6 to 10 with a mean of 7.2 (Lawton and Lawton 1985). The population grew substantially by 1995, the 8 flocks south of the Río Guacimal (an area of about 2 km2) increased to 19, and the mean flock size increased to 10.5. Brown jays appear to be obligately social; they have never been observed to breed as pairs, even where suitable empty territory exists (Lawton and Lawton 1985). Flocks are complex, consisting of extended families and unrelated individuals (Williams et al. 2004). There is typically a single, dominant breeding female, although additional females may participate in nest building and incubation, and even contribute to the clutch (Lawton and Lawton 1985, Williams 2004, Williams and Rabenold 2005). All young stay with the groups in which they were born for at least one year and 90% remain for a second year (Williams and Rabenold 2005). Generally 1- and 2-year-olds account for about one-quarter of the flock. Dispersal is male biased, although 50% of males >2 years old and 84% of females stay with their natal flock (Williams and Rabenold 2005). As a result older females within a group are closely related (r = 0.25; the degree of relationship of half-sibs), but older males are often unrelated to other flock members. Dispersing birds tend to move to neighboring flocks, although on occasion individuals disperse far; brown jays banded in Monteverde have been recovered 6, 8, and 10 km away (Williams and Rabenold 2005). In general, survivorship of brown jays is high, and breeding is delayed; on average both males and females first breed in their sixth year (Williams and Rabenold 2005). Helpers provide ~70% of the food brought to nestlings, but their performance is uneven. Older helpers bring more than younger, particularly early in the breeding season, and the performance of young helpers improves markedly as nestling age (Lawton and Guindon 1981). When the population was expanding, fledging success was greater in flocks with more older helpers (Lawton and Lawton 1985), but in the denser population of the 1990s each helper increases reproductive success by just 0.1 offspring (Williams and Hale 2006). Development of a series of microsatellite loci (Williams et al. 2004) has allowed parentage to be evaluated and relatedness among flock members determined.

Helpers are on average related as half-sibs (r = 0.24) to the nestlings they feed. Given their relatedness and the numbers of helpers and offspring the indirect fitness benefits of helping raise kin are not large. This is in part because some flock members are immigrants from neighboring flocks, and so unrelated to the breeders, and in part because the dominant breeding females may take several mates (Williams and Rabenold 2005). Male consorts of the breeding female account for 20% of the offspring, more than any other group of males, but males from nearby flocks father some nestlings in 22% of genetically analyzed broods (Williams and Rabenold 2005). Clearly brown jay life is complex, so it is perhaps naive to expect helping at the nest to have a simple cause. The benefits to a cooperative life may be widespread, including some indirect fitness benefits from helping to raise related birds, but also benefits involving protection from predation, territory defense, and eventual acquisition of breeding status (Williams and Lawton 2000). Pairs of male long-tailed manakins cooperate in complex mating displays for visiting females, but only the dominants or α-males of successful teams actually mate (Foster 1977, 1981, McDonald 1989a, 1993a,b). The β-males, who genetic analyses show are no more related to their α’s than random males in the population (McDonald and Potts 1994), help as song-and-dance partners. The partnership, which remains stable over years, involves singing as a duet the “toledo” call which attracts females to the display site (Trainer and McDonald 1993). Male teams differ in how harmoniously they produce the “toledo,” and the degree of frequency matching by a team is correlated by the rate at which females visited the team’s display site (Trainer and McDonald 1995). Song variability of males declines as males get older, and the “toledos” of teams of older and younger birds become more harmonious as the mating season progresses (Trainer 2000). If a female visits, one male moves toward her along the display perch, then jumps up in a hovering flight moving backwards along the perch while his partner moves along the perch toward the female. This leapfrogging proceeds interspersed with “butterfly flights” in which both males flutter together just above the perch. If the female remains, the β drops out of the display, and the α male mates with the female on the display perch (McDonald 2000). When an α male dies, the β assumes α status at that display site, and acquires a new partner as his β. Females that have mated at a display site tend to return to it in the following year, and have been observed mating with the new α, who had been the β in the prior year (McDonald 2000). Acquisition of α status is slow; the mean age at mating of males is 10 years, although females probably begin

The Montane Cloud Forests of the Volcanic Cordilleras 437

reproducing when one year old (McDonald 1993b). Clearly establishing effective display teams is very important for male long-tailed manakins. Before forming stable α-β teams, males in the first 8 or so years of their lives interact with many other males (McDonald 2007). How well connected young males are is related to the likelihood of their social success improving (McDonald 2007). Mammals

Mammals in the northern highlands of Costa Rica have received relatively little scientific attention (Timm and LaVal 2000a). There has been sufficient collecting to establish the composition of the fauna, and much of the general biology of many mammal is known from studies in other locales, but with few exceptions we know little about the particular lives of mammals in montane forests, or how their lives there compare with their lives in other places. From the central sector of the Cordillera de Tilarán 121 mammal species are known (roughly 60% of the Costa Rican fauna), including two endemics— a harvest mouse and a shrew. The fauna includes at least 58 bats and at least 15 murid rodents. A checklist is provided by Timm and LaVal (2000b). Of note are the eight arboreal species of murid rodents (Langtimm 1992, 2000). These are small and largely nocturnal, and in consequence are seldom seen. They are common, however, and two species, the Vesper Rat and the Slender Harvest Mouse, forage all over trees, having been captured 22 m above the ground (Langtimm 1992). These arboreal rodents may be important frugivores and seed predators (Langtimm 1992, Sargent 1995), a matter that deserves further study. Bats, however, are the best-studied mammals of the Monteverde region (LaVal 1977, LaVal and Fitch 1977, LaVal 2004, Dinerstein 1986). The Monteverde bat fauna is smaller than that of La Selva, which is richer in foliagegleaning and aerially feeding insectivores, but the two sites have similar numbers of frugivorous and flower-visiting species (LaVal and Fitch 1977). At Monteverde fruits of at least 40 species of plants are taken by the eight species of frugivorous bats (Dinerstein 1986). Reproductive activity of frugivorous bats in montane forest coincides with the two peaks in the abundance of the fruits eaten by bats, one of which occurs in May at the transition between dry and wet seasons, and the other in the late rainy season (Dinerstein 1986). The fruits most consumed by bats are mostly water rich (>80% by fresh weight), and higher in nitrogen than many bird-dispersed fruits, but are low in lipids. Consequently, frugivorous bats eat ravenously; individuals

of Artibeus toltecus consume twice their body weight each night. The bat fauna of the Cordillera de Tilarán is changing, apparently as a result of regional climate change, as an increasing number of lowland species settle in montane habitats (Timm and LaVal 2000, LaVal 2004). Of particular interest are the changes in the mammal fauna that have occurred due to hunting and land use changes. Most of these are known anecdotally through conversations with early settlers of the upper Pacific slope of the C. de Tilarán. Many of the changes are quite predictable. Early settlers were of necessity hunters, most mammals bigger than squirrels were hunted for food, and some populations were more susceptible than others. Giant anteaters and white-lipped peccary, common in the San Luis valley until the 1940s, were eliminated from the mountain range early. Otherwise, the mammal fauna of the range is intact, although local ranges and population sizes have been strongly influenced by human settlement of the area. Spider monkeys, paca, tapir, and collared peccary were hunted out of remnant forest stands on the Pacific slope, but persisted in the cloud forest along the crest of the Cordillera and the wet Caribbean slope. Following the establishment of the extensive complex of protected areas in the Cordillera, and the growth of the ecotourism economy, hunting has declined and these species have increased in abundance, and are extending their local ranges into areas that were earlier depopulated. Of the large predators jaguar are now very rare, although footprints continue to be seen in the Peñas Blancas valley, and kills of livestock probably not attributable to mountain lions continue sporadically in remote areas. Signs of mountain lions— footprints and clawed tree trunks— are commonly seen in the forest on the crest of the Cordillera, often just above established farms, and on the Caribbean slope. Some population declines, like that of the forest rabbit, are probably secondarily consequences of human settlement, due to increases in the number of both free-ranging dogs and coyotes.

Species Interactions Studies of species interactions in the montane forests of northern Costa Rica have focused on pollination and seed dispersal in the Monteverde area (Murray et al. 2000). Competitive interactions, predator-prey systems, and mutualisms involved in plant mineral acquisition are undoubtedly important, but have received little attention. Herbivory, aside from a few studies of particular species— for example, the pasture pest Prosapia (Peck 1996), remains almost entirely unexplored, and needs even basic surveys.

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Competitive Interactions

In the tree flora and avifauna there are a number of examples of closely related species, the ranges of which are spatially displaced, with relatively little overlap (e.g., the species of Beilschmiedia and Persea among the canopy trees, or the slate-throated and collared redstarts). Since bird ranges are changing as the regional climate changes (Pounds et al. 1999), and tree seedlings, at least, are amenable to transplant experiments, the opportunities for observational and manipulative studies of competitive interaction would seem abundant. Predator-Prey Interactions

Studies of predation have been limited to those of the pasture pest mentioned above, and scattered observations produced in the course of other studies. Wenny (2000a), for example, found that post-dispersal rodent predation killed 98% of the seeds of Ocotea endresiana, 80% of those of Guarea kunthiana, 50% of those of Eugenia sp., 20% of those of Beilschmiedia pendula, and none of those of Meliosma vernicosa. And Sargent (1995) found that a captive harvest mouse readily ate mistletoe seeds collected from bird feces, perhaps explaining the 60% of dispersed mistletoe seeds that subsequently disappear. Pathogens undoubtedly influence plant and animal populations; according to settlers’ accounts, the Central American yellow fever epidemic in the early 1950s caused dramatic declines in the abundance of the three monkeys in the Cordillera de Tilarán, and more recently Impatiens sultana, an invasive plant becoming alarmingly widespread in the range, suffered almost complete adult mortality, apparently due to an epidemic plant pathogen. But even the most basic surveys remain to be done. Plant secondary chemistry is often related to defense against herbivores or pathogens, but chemical ecology has been explored in only a few cases (Lawton et al. 1993, Murray et al. 1994), although a series of studies exploring the phytomedicinal potential of the montane flora show a remarkable richness in secondary chemistry (Setzer et al. 1992, 1995a,b, 1998, 1999, 2000a,b, 2003, 2005, 2006, Moriarity et al. 1998, Setzer 2000). The richness of the secondary chemistry suggests that much interesting, but unexamined, chemical ecology exists. Mutualisms

Species interactions in pollination and seed dispersal are among the best-studied elements of the biology of the mon-

tane forests in northern Costa Rica. Particular attention has been paid to the complex among the hummingbirds and the plants they pollinate, and to the large, obligately frugivorious birds, such as quetzals, and plants with specialized fruits, like the Lauraceae. Pollination

From floral characteristics the broad outline of which plants are pollinated by what groups of pollinators is now clear (Haber 2000b, Murray et al. 2000). Approximately 9% of the flora, for example, is pollinated by hummingbirds (including 25% of the epiphytes, excluding orchids). Studies of pollination biology in the Monteverde area have been ably summarized by Murray et al. (2000). These studies have focused largely on hummingbird pollination, although several other systems have received attention. These include the pollination biology of Ficus pertusa and its fig wasps, pollination of the heat-generating aroid Xanthosoma robustum by scarab beetles (Goldwasser 2000), buzz-pollination of Saurauia spp. by bumblebees (Cane 1993), deceit pollination of Begonia (Agren and Schemske 1991), alteration of floral sex of Centropogon solanifolius by anther consuming larvae of Zygothrica neolinea, a drosophilid fly (Weiss 1996), and protection of the nectar of the hawkmothpollinated Guettarda poasana from yeasts by floral essential oils containing aromatic alcohols (Lawton et al. 1993). The 30 species of hummingbirds and the plants they visit have been extensively investigated (Feinsinger 1976, 1978, 1987, Feinsinger and Busby 1987, Feinsinger et al. 1986, 1987, 1988a,b, 1991, 1992, Lackie et al. 1986, Linhart et al. 1987a,b, Murray et al. 1987, Feinsinger and Tiebout 1991, Tiebout 1991, Podolsky 1992). There exist two guilds of hummingbirds and flowers they pollinate on the crest and upper Pacific slope of the Cordillera de Tilarán: hummingbirds with long curved bills pollinating flowers with long, curved tubular corollae, and hummingbirds with shorter, straight bills pollinating flowers with shorter, straight tubular corollae (Feinsinger 1976, 1978). Agricultural colonization with large-scale conversion of forest to a patchy landscape of pasture, cropping systems, logged woodlots, early second-growth, and extensive edge habitats produced marked changes in the hummingbird community composition (Feinsinger 1976, 1978). Natural disturbances, however, seem not to cause large changes in hummingbird resource abundance, although a few hummingbird-pollinated plants are more abundant in gaps (Feinsinger et al. 1987, 1988b). Availability and diversity of floral resources, as well as hummingbird visitation and estimated demand on those resources, have been examined to assess diet breadth and among species overlaps in diet. Hummingbird visitation

The Montane Cloud Forests of the Volcanic Cordilleras 439

of flowers of particular species, pollen loads, and pollen deposits were similar in forest, tree fall gaps, and forest clearings cut to resemble small landslides, as, in general, were diet breadths and diet overlaps among hummingbirds (Feinsinger et al. 1988b). The differences in the response of the community of hummingbirds and the plants they pollinate to natural vs. anthropogenic disturbance points out that ecological impacts of human landscape changes may not be predicted by simply scaling up from responses to natural disturbances. Much of this work focused on plant-plant interactions via pollinator sharing. Among the plants pollinated by each guild of hummingbirds most co-occur spatially and overlap in time of blooming, but plant species that share pollinators did not show consistent patterns of competitive interaction (Feinsinger et al. 1986). Aviary experiments did show that pollen loss can occur when hummingbirds feeding at one flower visit a different species before returning to the first (Feinsinger and Busby 1987, Feinsinger et al. 1988b), but in most cases in the field pollination success was uninfluenced by presence or density of neighboring hummingbird pollinated plants. When there were significant interactions some were competitive and others facilitative. Nearly half of the canopy tree species, including the Lauraceae, have inflorescences with many non-descript, small, open, pale flowers, which are visited by a large array of small insects, including bees and wasps, beetles, flies, and butterflies (Haber 2000b, Murray et al. 2000). Given the diverse tree flora, many species of which occur in replacement series of closely related species, each occupying a narrow band along the gradient of moisture on the upper Pacific slope, this assemblage of generalized flowers and pollinators demands careful quantitative study. Seed Dispersal

Most seed dispersal syndromes are present in the montane flora of northern Costa Rica, but some— for example, dispersal by water— are rare. Striking differences in the spectra of dispersal systems exist among major plant life forms: considering just the two dominant dispersal modes for each, ~65% of trees are bird dispersed and about 10% are wind dispersed, ~40% of lianas are bird dispersed and ~10% are wind dispersed, slightly more than half the shrubs are bird dispersed and ~15% are wind dispersed, ~40% of terrestrial herbs are wind dispersed and 27% are gravity dispersed, and ~65% of epiphytes are wind dispersed and a little over 25% are bird dispersed (Haber 2000b, Murray et al. 2000). Bats, arboreal mammals, terrestrial mammals, ants, and explosive dehiscence account for lesser amounts of seed dispersal in most groups.

Seed dispersal by birds has received a great deal of attention in the Monteverde area (Wheelwright 1983, 1985a,b, 1986, 1991, 1993, Wheelwright and Bruneau 1992, Wheelwright et al. 1984, Murray 1986, 1988, Murray et al. 1994, Bronstein and Hoffman 1987, Nadkarni and Matelson 1989, Sargent 2000, Wenny and Levey 1998, Wenny 2000a,b). Tanagers, finches, and thrushes are common opportunistic frugivores, which harvest mainly small, watery, carbohydrate-rich, many-seeded fruits produced by most Melastomataceae, Solanaceae, and Rubiaceae, as well as by members of many other plant families, while quetzals, toucans, and bellbirds are specialized frugivores, which consume mainly large-seeded, lipid- and protein-rich fruits like those of the Lauraceae (Wheelwright et al. 1984, Murray et al. 2000). Fruit consumption and seed dispersal varies greatly, owing to a variety of factors including the nature of the fruit, the frugivores, the crop size, and the location of the plants (Murray et al. 2000). Some fruits have laxative agents that regulate the time the seeds spend in the digestive tract of the dispersing birds (Murray et al. 1994). The size of individual fruits and the size of a tree’s crop can both influence the rate at which lauraceous fruits are removed, but crop size doesn’t seem to influence the length of visits by specialized frugivores (Wheelwright 1991, 1993). Fruits of three common gap-invading pioneer shrubs are taken whole by black-faced solitaires, prong-billed barbets, and black-and-yellow silky flycatchers, which dispersed seeds widely, but fruits of the same plants were mashed by common bush tanagers, spangle-cheeked tanagers, and yellowthighed finches, which dropped most seeds near the parent plant (Murray 1986, 1988). Similar differences have been observed for avian dispersers of Ficus pertusa (Bronstein and Hoffman 1987). Dispersal of Ocotea endresiana (Lauraceae) is remarkably well-directed in some circumstances. Fruits consumed by male three-wattled bellbirds are deposited mainly below the bird’s courtship perches, which are generally on the edges of canopy gaps (Wenny and Levey 1998). Seedlings from seeds dispersed by male bellbirds are thus more likely to survive than seedlings dispersed by other birds. A number of frugivorous birds, including the threewattled bellbird, quetzal, and black-faced solitaire, are altitudinal migrants, but the movements of most of these are not well understood. The relationships among flowering and fruiting phenologies, pollinator and frugivore movement, and plant species ranges deserve more attention as well as broader biogeographic comparisons to determine whether the patterns seen in the Cordillera de Tilarán hold on the isolated massifs of the C. de Guanacaste.

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Mutualisms and Plant Mineral Nutrition

Although nutrient cycling in tall leeward cloud forest has been well studied (Nadkarni et al. 2000; see below, Nutrient Cycling), the extent of nutrient acquisition symbioses remains poorly known. Spores of the vesicular-arbuscular mycorrhizal fungi Glomus, Gigaspora, and Acaulospora are present in terrestrial soils and epiphytic matter (Maffia et al. 2000), and there is vesicular-arbuscular mycorrhizal colonization of roots of terrestrial Piperaceae (Pothomorphe, Sarchorachis, and Piper spp.) and epiphytic Peperomia spp.— but at low rates. Peperomia costaricensis grown in a greenhouse on infertile media had higher rates of internal colonization by the fungi. Either soils in the field are sufficiently fertile that mycorrhizae offer little, at least to members of the Piperaceae, or colonization is poor owing to low fungal spore densities or activities. Clearly, mycorrhizae, particularly those of canopy trees, deserve more attention in these montane settings. Nitrogen-fixing symbioses also remain to be investigated. Plants with well-known nitrogen-fixing symbionts (e.g., Gunnera spp. and Myrica spp.), are common in the regrowth on landslide scars, lichens (Leptogium spp. and Collema spp.) with cyanobacterial symbionts being common in the cloud forest, and free-living cyanobacteria, some with heterocysts, can be found in bryophyte mats, on wet bark, and even in the sheathing stipules of the elfin forest tree, Schefflera rodrigueziana. Protective Mutualisms

The Azteca-Cecropia mutualism is present in the Cecropia spp. of both the Pacific and Caribbean slope (e.g., see Gilbert et al., chapter 12 of this volume), but the cloud forest Cecropia polyphlebia growing on the crest of the cordillera lacks ants (Longino 1989). The reasons for this lack, and the consequences, remain to be discovered. Extrafloral nectaries are conspicuous on many plants. On lowland species of Inga these attract ants, which kill or harass foraging ants, but in montane settings with fewer ants in trees the extrafloral nectaries of Inga attract parasitoids, and a greater proportion of caterpillars are parasitized than in the lowlands (Koptur 1985). Such mutualisms are perhaps widespread; many montane forest insects carry phoretic mites, and mite domatia are conspicuous features of the leaves of many cloud forest plants. Amblyopinine beetles, once thought to be blood-feeding ectoparasites of mammals, are now known to feed instead on the fleas, ticks, and mites on the hosts; the harvest mouse Reithrodontomys creper at Monteverde is the primary host of Amblyopinus tiptoni at Monteverde, while Tome’s rice rat, Oryomys albigularis, hosts A. emarginatus (Ashe and Timm 1987a,b). Modern

genetic techniques might yield interesting insights into the evolution of such symbioses.

Ecosystem Functioning and Dynamics Ecosystem functioning remains poorly known in the mountains of northern Costa Rica (Nadkarni et al. 2000). Most aspects of energy flow remain unstudied. Even basic information on primary productivity is lacking. Although both nutrient cycling and forest dynamics have received considerable attention in some forest types in the Monteverde area, these topics have been little examined in studies comparing different forest types. In short, much remains to be done. Nutrient Cycling

Nutrient cycling, with particular attention to the role of epiphytes and epiphytic organic matter, has been thoroughly examined in the leeward cloud forests of the Monteverde Cloud Forest Reserve in the central Cordillera de Tilarán (Clark et al. 1988, Clark and Nadkarni 1990, Vance and Nadkarni 1990, 1992, Nadkarni and Matelson 1991, 1992a,b, Nadkarni et al. 2000). At 1,480 m elevation 1.5 km to the lee of the continental divide the canopy trees are 18– 25 m tall, basal area is 73.8 m2 ha− 1, there are 555 stems >10 cm diameter at breast height (dbh) per hectare, and the aboveground, terrestrially rooted biomass is estimated to be 490 Mg ha− 1, of which 85% is trunk wood and 12% branch wood (Nadkarni et al. 2000). Belowground root biomass ranges from 1,500 to 7,220 gm m− 2 of which 20 to 40% are fine roots (10 cm dbh die each year— 12.7 trees ha− 1 yr− 1 (Nadkarni et al. 1995). Although

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trunk snapping accounts for 61% of the serious damage to trees in this forest, roughly a third of the trees that snap subsequently sprout. Fewer trees uproot (22% of those damaged), or are knocked down by falling neighbors (7%), and most of these die from the incident. Only 4% of trees die upright (4%). Shade-intolerant, pioneer species (Cecropia polyphlebia, Hampea appendiculata, and Heliocarpus appendiculatus) were roughly twice as likely to die as other species. In the wind-exposed lower montane rain forests along the continental divide treefalls create canopy gaps covering on average 1.3% of the area each year (Nadkarni et al 2000). Most trees (80 to 90%) fall during the severe winter storms known locally as temporales del norte. The number and severity of these winter storms varies from year to year, and so does the number and area of treefall gaps. The percentage of the area opened each year over the decade from 1981 to 1990 varied from 0.6% to 3.8%. Although the turnover time calculated from the long-term geometric mean of the area opened per year is 77 years in this forest, turnover times calculated from 3-year periods range from 51 years to 147 years, emphasizing the importance of long-term studies. Demographic analyses of one of the dominant shade-intolerant trees (Didymopanax pittieri) of the windswept elfin forest on ridge crests suggest that the population is stable, and thus that forest structure at the scale of 1 km2 is stable (Lawton 1980). This in turn suggests that the current disturbance regime has existed for some tree generations. Gaps in the elfin forest vary considerably in many attributes (Lawton and Putz 1988). Most gaps are small; less than 5% are greater than 105 m2. The largest 5%, however, contribute more than one-third of the canopy area opened by disturbance. Of elfin forest gaps 41% formed when trees uprooted, and 39% when trees snapped. The remainder was created by limbfall, the collapse of epiphyte masses, and lightning strikes. Gap area (log-transformed) is correlated with gap aperture (the angular opening to the sky from gap center), gap-maker trunk diameter, nurse log area (also log-transformed), and the area of disturbed mineral soil (Lawton and Putz 1988). Because many gap attributes are related to gap area it is tempting to use it as a simple measure of the overall variation among gaps, but in this forest the first principal component of variation among gap attributes, which contrasts measures of gap size and the height at which the gap maker broke, accounts for only about half of the variation among gaps, and the second principal component, a contrast of gap aperture (“openness”) with position of the gap along the slope, the height of breakage, and gap area, accounts for only an additional one-sixth of the variation in gap attributes (Lawton and

Putz 1988). The size of the tree that fell to create the gap, and the nurse log area in the gap, are both better correlated with the first principal component than is gap area. Elfin forest gaps are rapidly colonized; bare ground and logs are covered within 2– 3 years as a dense thicket of regrowth reaches 1– 4 m in height (Lawton and Putz 1988). In small gaps (10 m2) the leaf area index recovers in 3 years to 50% of mature forest leaf area index (LAI) of 5.1. In large gaps (120 m2) the LAI recovers to 75% within 3 years and 90% within 6 years. Saplings of canopy tree species account for 10% of the regrowing canopy in gaps at 8 months after gap formation, and 50% at 78 months. The rate of absolute height growth is slow by lowland standards, in part because of differences in allocation. The mechanical stresses due to wind in elfin forests are very high, and even shade-intolerant, pioneer trees have dense wood, and thick stems (Lawton 1982, 1984). In relative terms, though, the rate of elfin forest regrowth is similar to that in the lowlands; regrowth of elfin forest pioneers to 50% of canopy height (3– 4 m) takes about 6 years (Lawton and Putz 1988). The density of saplings of canopy tree species is greatest on disturbed mineral soil (8.3 saplings m− 2), owing largely to seeds, such as those of Guettarda poasana, germinating from the soil seed bank, but not much lower (6.4 saplings m− 2) on nurse logs. This is in part due to the very unusual life history of some elfin forest species, such as Didymopanax pittieri, Oreopanax nubigenus, and Cosmibuena valerii, which begin life as epiphytic seedlings and saplings and survive host collapse to reorient as saplings on nurse logs in gaps (Lawton and Putz 1988, Williams-Linera and Lawton 1995). Landslides are conspicuous features of the montane landscape, particularly on the over-steepened walls of quebradas, or gorges, although smaller landslides occur in less precipitous terrain in wet areas in lower montane and premontane rain forest. However, the dynamics of succession on landslides have only begun to be explored (Myster 1993), although it is clear that a distinctive assemblage of species, such as Gunnera insignis, Myrica phanerodonta, and Monochaetum spp., are landslide specialists.

People and Nature People have long occupied the montane forest areas of northern Costa Rica; artifacts from the area around Laguna Arenal have been dated to before 10,000 years BP (Sheets et al. 1991). The Arenal area has been particularly well investigated archeologically, in part due to the correlative dating and preservation made possible by the various eruptions of Volcán Arenal (Sheets et al. 1991, Sheets and McKee

The Montane Cloud Forests of the Volcanic Cordilleras 443

1994). More recently montane areas have been colonized by modern farmers, and this has been followed in some areas, like Monteverde, by the growth of ecotourism. Griffith et al. (2000) discuss the modern agricultural colonization and development of the Cordillera de Tilarán, including the roles of opportunity and economic constraints. History of Land Use

Expansion of Pre-Columbian agricultural societies after 500 BC must have created a mosaic landscape of fields and fallow lands on much of the upper Pacific slopes of the Cordillera de Tilarán and C. de Guanacaste. Pot shards are commonly found between 1,300 and 1,500 m a.s.l. in the area now occupied by Monteverde, Santa Elena, and their surrounding communities. Areas at 1,500 m, particularly the wetter cloud forest habitats, were in general not occupied (Sheets and McKee 1994). The extent to which the modern vegetation of the upper Pacific slope has been influenced by Pre-Columbian agriculture remains unknown. Modern agricultural colonization of the upper Pacific slope of the Cordillera de Tilarán began in the 1920s and 1930s, as homesteaders established small subsistence farms between 1,200 and 1,450 m elevation (Griffith et al. 2000), although commercial beef production occurred at lower elevations. In 1953 the cheese plant at Monteverde was established, and incorporated in 1954 as the Productores de Monteverde, S. A. This led to the conversion of subsistence farms to small dairy farms, and dairy production spread along the upper Pacific slope. By the early 1970s most land on the upper Pacific slope had been occupied, and settlers had cleared patches of cloud forest along the crest of the Cordillera and in premontane rain forest on the Caribbean slope, providing considerable motivation to growing conservation efforts in the area (see below). More recently, coffee production has spread, including a number of organic coffee farms, and vegetable production has increased to serve the growing number of restaurants and hotels in the area. Following the establishment of the Monteverde Cloud Forest Preserve in 1972, ecotourism became a growing sector of the economy, and now dominates the Monteverde– Santa Elena area (Aylward et al. 1996, Chamberlain 2000). Conservation

A detailed history of conservation activity in the Monteverde area of the Cordillera de Tilarán has been provided by Burlingame (2000), while Wheelwright (2000) discussed the problems and prospects for conservation biology in the area. The earliest conservation measures involved the pro-

tection of springs and catchments to ensure water supplies, including the headwaters of the Río Guacimal, set aside by the Quaker settlers of Monteverde, and formally protected as the Bosqueterno, S.A., in 1974. In 1970 George Powell, a graduate student studying foraging by mixed species flocks of birds, alarmed by the growing number of scattered clearings being opened in virgin cloud forest, started looking for ways to preserve critical areas. He established contacts with The Nature Conservancy (TNC), the World Wildlife Fund-U.S. (WWF), and other institutions, and with the Tropical Science Center (TSC, or CCT in Spanish) to hold and manage preserved lands as part of the Monteverde Cloud Forest Preserve, which was formally established in 1972. With land purchases funded by international conservation organizations, the Preserve rapidly grew to over 10,500 ha (Burlingame 2000), and the number of visitors grew to more than 50,000 annually by the early 1990s. By the mid-1980s the Monteverde Cloud Forest Preserve and the Tropical Science Center were focused on land and ecotourism management, and a local group at Monteverde established the Asociación Conservacionista de Monteverde (Monteverde Conservation League, ACM), to pursue funds for land preservation in the Peñas Blancas valley and neighboring regions. Although much of the land of interest lay within the Arenal Forest Reserve established to protect watersheds involved in hydroelectric power generation, disgruntled landowners remained in place. With funds from Barnens Regnskog, a Swedish organization, and The Children’s Rainforest U.S., ACM bought and now administers about 18,000 ha. Currently, there exists a complex of public and private reserves, including Parque Nacional Arenal, cooperating in land preservation under the umbrella of the Área de Conservación Arenal-Tempisque (ACAT), one of Costa Rica’s conservation areas administered through the National System of Conservation Areas (SINAC) of the Ministry of Environment and Energy (MINAE). Ecotourism is not as developed in the Cordillera de Guanacaste, but much of the upper portions of the volcanic massifs are protected in a series of Costa Rican National Parks. The Orosi and Cacao volcanic complex is now included in Parque Nacional Guanacaste, and are included in the ambitious efforts to restore the series of environments from the volcanic summits to the lowland dry forests in their lee. We refer specifically to the chapter by Janzen and Hallwachs (chapter 10 of this volume) for extensive details on this extraordinary conservation and restoration effort (also see Jiménez et al., chapter 9 of this volume). The restoration work in Guanacaste has grown from a recognition that montane systems are inextricably bound up in the fate of adjacent lowlands. Many animals, including large mammals like tapir, birds like quetzals,

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bellbirds, and many hummingbirds, and even butterflies, migrate seasonally from montane areas to lower slopes or lowland plains. The fate of these species depends on coordinated conservation efforts at the large scale. Furthermore, it is now clear that tropical lowland land use affects regional climate (Lawton et al. 2001), and that climatic conditions in Costa Rica’s mountains may depend on careful lowland management. Biologists will need to work with climate scientists, land managers, agricultural specialists, conserva-

tionists, and development agencies to deal with problems at this scale.

Acknowledgments We are grateful for the support of the Monteverde community as well as grants from NASA (IDS/03– 0000– 0371 and NNX06AB68G) administered by Woody Turner.

References Agren, J., and D.W. Schemske. 1991. Pollination by deceit in a neotropical monoecious herb, Begonia involucrata. Biotropica 23: 235– 41. Alvarado, G.E., E. Vega, J. Chaves, and M. Vásquez. 2004. Los grandes deslizamientos (volcánicos y no volcánicos) de tipo debris avalanche en Costa Rica. Revista Geológica de América Central 30: 83– 99. Alvarado, I.G. 1989. Los Volcanes de Costa Rica. San José, Costa Rica: Editorial Universidad Estatal a Distancia. Ashe, J.S., and R.M. Timm. 1987a. Predation by and activity patterns of “parasitic” beetles of the genus Amblyopinus (Coleoptera: Staphylinidae). Journal of Zoology (London) 212: 429– 37. Ashe, J.S., and R.M. Timm. 1987b. Probable mutualistic association between staphylinid beetles (Amblyopinus) and their rodent hosts. Journal of Tropical Ecology 3: 177– 81. Aylward, B., K. Allen, J. Echeverría, and J. Tosi. 1996. Sustainable ecotourism in Costa Rica: the Monteverde Cloud Forest Preserve. Biodiversity and Conservation 5: 315– 43. Bergoeing, J.P., and L.G.Q. Brenes. 1979. Mapa geomorfológico de Costa Rica. San José, Costa Rica: Instituto Geográfico Nacional. Bronstein, J., and K. Hoffman. 1987. Spatial and temporal variation in frugivory at a neotropical fig, Ficus pertusa. Oikos 49: 261– 68. Bruijnzeel, L.A. 2006. Hydrological impacts of converting tropical montane cloud forest to pasture with initial reference to northern Costa Rica. Final Technical Report DFID-FRP Project no. R7991. British Department for International Development Forestry Research Programme. Bruijnzeel, L.A., F.N. Scatena, and L.S. Hamilton, eds. 2010. Mountains in the Mist: Science for Conserving and Managing Tropical Montane Cloud Forests. Cambridge, UK: Cambridge University Press. Burke, K. 1988. Tectonic evolution of the Caribbean. Annual Review of Earth and Planetary Science 16: 201– 30. Burlingame, L.J. 2000. Conservation in the Monteverde zone. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 351– 88. New York: Oxford University Press. Buskirk, W.H. 1976. Social systems in a tropical forest avifauna. American Naturalist 110: 293– 310. Cane, J.H. 1993. Reproductive role of sterile pollen in Saurauia (Actinidiaceae), a cryptically dioecious neotropical tree. Biotropica 25: 493– 95. Carvajal, A. 2003. Distribución de raíces finas en suelos del bosque nuboso y pastos, en Monteverde, Costa Rica. Tesis Bachiller, Instituto

Tecnológico de Costa Rica, Escuela de Ingeniería Forestal. Cartago, Costa Rica. Castillo-Muñoz, R. 1983. Geology. In D.H. Janzen, ed., Costa Rican Natural History, 47– 62. Chicago: University of Chicago Press. Cecchi, E., B. van Wyck de Vries, and J.-M. Lavest. 2005. Flank spreading and collapse of weak-cored volcanoes. Bulletin of Volcanology 67: 72– 91. Chamberlain, F. 2000. Pros and cons of ecotourism. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 376. New York: Oxford University Press. Cháves, R., and R. Sáenz. 1974. Geología de la Cordillera de Tilarán (Proyecto Aguacate, segunda fase). Informas Técnicas y Noticias Geológicas 12: 1– 49. San José, Costa Rica: Dirección Geología, Mineralógia, y Petrológia. Churchill, S.P., H. Balslev, E. Forero, and J.L. Luteyn, eds. 1995. Biodiversity and Conservation of Neotropical Montane Forests. Bronx, NY: New York Botanical Garden. Clark, K.L., R.O. Lawton, and P.R. Butler. 2000. The physical environment. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 15– 38. New York: Oxford University Press. Clark, K.L., and N. Nadkarni. 1990. Nitrate and ammonium ions in precipitation and throughfall of a neotropical cloud forest: implications for epiphyte mineral nutrition. Ecological Bulletin 71: 59. Clark, K.L., and N. Nadkarni. 2000. Microclimate variability. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 33– 34. New York: Oxford University Press. Clark, K.L., N.M. Nadkarni, D. Schaefer, and H.L. Gholz. 1988. Atmospheric deposition and net retention by the canopy in a tropical montane forest, Monteverde, Costa Rica. Journal of Tropical Ecology 14: 27– 45. Coates, A.G., J.B.C. Jackson, L.S. Collins, T.M. Cronin, H.J. Dowsett, L.M. Bybell, P. Jung, and J.A. Obando. 1992. Closure of the Isthmus of Panama: the nearshore marine record of Costa Rica and western Panama. Geological Society of America Bulletin 104: 814– 28. Cole, M.C. 1983. An illustrated guide to the genera of Costa Rican Hepaticae. Brenesia 21: 137– 201. Cole, M.C. 1984. Thallose liverworts and hornworts of Costa Rica. Brenesia 22: 319– 48. Croat, T.B. 1978. Flora of Barro Colorado Island. Palo Alto, CA: Stanford University Press.

The Montane Cloud Forests of the Volcanic Cordilleras 445 Crump, M.L., F.R. Hensley, and K.L. Clark. 1992. Apparent decline of the golden toad: underground or extinct? Copeia 1992: 413– 20. Daniels, J.D. 1998. Establishment and succession of epiphyllic bryophyte assemblages on the fronds of the neotropical understory palm Geonoma seleri. PhD diss., University of North Dakota. Daniels, J., and R.O. Lawton. 1991. Habitat and host preferences of the neotropical strangling fig, Ficus crassiuscula in Lower Montane Rain Forest. Journal of Ecology 79: 129– 41. Dengo, O., and Levy. 1969. Mapa metalogenica de Ámerica Central. Guatemala: ICAITI. Dinerstein, E. 1986. Reproductive ecology of fruit bats and the seasonality of fruit production in a Costa Rican cloud forest. Biotropica 18: 307– 18. Feinsinger, P. 1976. Organization of a tropical guild of nectarivorous birds. Ecological Monographs 46: 257– 91. Feinsinger, P. 1978. Ecological interactions between plants and hummingbirds in a successional tropical community. Ecological Monographs 48: 269– 87. Feinsinger, P. 1987. Effects of plant species on each other’s pollination: is community structure influenced? Trends in Ecology and Evolution 2: 123– 26. Feinsinger, P., J.H. Beach, Y.B. Linhart, W.H. Busby, and K.G. Murray. 1987. Disturbance, pollinator predictability, and pollination success among Costa Rican cloud forest plants. Ecology 68: 1294– 305. Feinsinger, P., and W.H. Busby. 1987. Pollen carryover: experimental comparisons between morphs of Palicourea lasorrachis (Rubiaceae), a distylous, bird-pollinated tropical treelet. Oecologia 73: 231– 35. Feinsinger, P., W.H. Busby, K.G. Murray, J.H. Beach, W.Z. Pounds, and Y.B. Linhart. 1988a. Mixed support for spatial heterogeneity in species interactions: hummingbirds in a tropical disturbance mosaic. American Naturalist 131: 33– 57. Feinsinger, P., W.H. Busby, and H.M. Tiebout. 1988b. Effects of indiscriminate foraging by tropical hummingbirds on pollination and plant reproductive success: experiments with two tropical treelets (Rubiaceae). Oecologia 76: 471– 74. Feinsinger, P., K.G. Murray, S. Kinsman, and W.H. Busby. 1986. Floral neighborhoods and pollination success within four hummingbirdpollinated plant species in a Costa Rican cloud forest. Ecology 67: 449– 64. Feinsinger, P., and H.M. Tiebout. 1991. Competition among plants sharing hummingbird pollinators: laboratory experiments on a mechanism. Ecology 72: 1946– 52. Feinsinger, P., H.M. Tiebout, and B.E. Young. 1991. Do tropical birdpollinated plants exhibit density-dependent interactions? Field experiments. Ecology 72: 1953– 63. Feinsinger, P., H.M. Tiebout, B.E. Young, and K.G. Murray. 1992. New perspectives on neotropical plant-hummingbird interactions. Acta Congressus Internationalis Ornithologici 20: 1605– 10. Finnegan, J.J., and Y. Brunet. 1995. Turbulent airflow in forests on flat and hilly terrain. In M.P. Coutts and J. Grace, eds., Wind and Trees, 3– 40. Cambridge: Cambridge University Press. Fitch, H.S. 1973. A field study of Costa Rican lizards. University of Kansas Science Bulletin 50: 39– 126. Fogden, M.P.L. 2000. Birds of the Monteverde area. Appendix 9. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 541– 52. New York: Oxford University Press.

Foster, M.S. 1977. Odd couples in manakins: a study of social organization and cooperative breeding in Chiroxiphia linearis. American Naturalist 111: 845– 52. Foster, M. S. 1981. Nesting biology of the long tailed manakin. Wilson Bulletin 88: 400– 420. Foster, R.B. 1990. The floristic composition of the Río Manú floodplain forest. In A.H. Gentry, ed., Four Neotropical Rainforests, 99– 111. New Haven, CT: Yale University Press. Gardner, T.W., D. Verdonck, N.M. Pinter, R. Slingerland, K.P. Furlong, T.F. Bullard, and S.G. Wells. 1992. Quaternary uplift astride the aseismic Cocos Ridge, Pacific Coast, Costa Rica. Geological Society of America Bulletin 104: 219– 32. Goldwasser, L. 2000. Scarab beetles, elephant ear ( Xanthosoma robustum) and their associates. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 268– 71. New York: Oxford University Press. Gómez P., L.D. 1986. Vegetación de Costa Rica. San José, Costa Rica: Editorial Universidad Estatal a Distancia. Grieve, T.G.A., J. Proctor, and S.A. Cousins. 1990. Soil variation with altitude on Volcán Barva, Costa Rica. Catena 17: 525– 34. Griffin, D., and M.I. Morales. 1983. Key to the genera of mosses from Costa Rica. Brenesia 21: 299– 323. Griffith, K., D.C. Peck, and J. Stuckey. 2000. Agriculture in Monteverde: moving toward sustainability. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 389– 417. New York: Oxford University Press. Guindon, C.F. 1996. The importance of forest fragments to the maintenance of regional biodiversity in Costa Rica. In J. Schelhas and R. Greenberg, eds., Forest Patches in Tropical Landscapes, 168– 86. Washington, DC: Island Press. Guindon, C.F. 2000. The importance of Pacific slope forest for maintaining regional biodiversity. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 435– 37. New York: Oxford University Press. Guswa, A.J., A.L. Rhodes, and S.E. Newell. 2007. Importance of orographic precipitation to the water resources of Monteverde, Costa Rica. Advances in Water Resources 30: 2098– 112. Haber, W.A. 2000a. Plants and vegetation. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 39– 94. New York: Oxford University Press. Haber, W.A. 2000b. Vascular plants of Monteverde. Appendix 1. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 457– 518. New York: Oxford University Press. Häger, A. 2006. Einfluβ von Klima und Topographie auf Struktur, Zusammensetzung und Dynamik eines tropischen Wolkenwaldes in Monteverde, Costa Rica. PhD diss., Georg August Universitat Gottingen. Häger, A., and A. Dohrenbusch. 2009. Structure and dynamics of tropical montane cloud forests in north-western Costa Rica under contrasting biophysical conditions. In L.A. Bruijnzeel, F.N. Scatena, and L.S. Hamilton, eds., Mountains in the Mist: Science for Conserving and Managing Tropical Montane Cloud Forests, 208– 16. Cambridge, UK: Cambridge University Press. Hale, A.M., D.A. Williams, and K.N. Rabenold. 2003. Territoriality and neighbor assessment in brown jays. Auk 120: 446– 56. Hanson, P. 2000. Insects and spiders. In N. Nadkarni and N. Wheel-

446 Chapter 13 wright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 95– 147. New York: Oxford University Press. Hartshorn, G.S., and B.E. Hammel. 1994. Vegetation types and floristic patterns. In L. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 73– 89. Chicago: University of Chicago Press. Hastenrath, S.L. 1967. Rainfall distribution and regime in Central America. Archiv für Meteorologie, Geophysik und Bioklimatologie, Serie B 15: 201– 41. Hayes, M.P., J.A. Pounds, and W.W. Timmerman. 1989. An annotated list and guide to the amphibians and reptiles of Monteverde, Costa Rica. Herpetological Circulars 17: 1– 67. Jankowski, J. 2004. Patterns of avian diversity and the interspecific abundance-distribution relationship in the Tilarán mountain range, Costa Rica. M.S. thesis, Department of Biological Sciences, Purdue University. Lafayette, IN. Jankowski, J., and K.N. Rabenold. 2007. Endemism and local rarity in birds of neotropical montane rainforest. Biological Conservation 138: 453– 63. Keigwin, L. 1982. Isotopic paleoceanography of the Caribbean and East Pacific: role of Panama uplift in late Neogene time. Science 251: 350– 53. Kempter, K.A., S.G. Benner, and S.N. Williams. 1996. Rincón de la Vieja volcano, Guanacaste province, Costa Rica: geology of the southwestern flank and hazards implications. Journal of Volcanology and Geothermal Research 71: 109– 27. Koptur, S. 1985. Alternative defenses against herbivores in Inga (Fabaceae: Mimosoideae) over an elevational gradient. Ecology 66: 1639– 50. Lackie, P.M., C.D. Thomas, M.J. Brisco, and D.N. Hepper. 1986. On the pollination ecology of Hamelia patens (Rubiaceae) at Monteverde, Costa Rica. Brenesia 25– 26: 203– 13. Langtimm, C.A. 1992. Specialization for vertical habitats within a cloud forest community of mice. PhD diss., University of Florida, Gainesville. Langtimm, C.A. 2000. Arboreal mammals. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 239– 40. New York: Oxford University Press. LaVal, R.K. 1977. Notes on some Costa Rican bat communities. Brenesia 10/11: 77– 83. LaVal, R.K. 2004. Impact of global warming and locally changing climate on tropical cloud forest bats. Journal of Mammalogy 85: 237– 44. LaVal, R.K., and H. S. Fitch. 1977. Structure, movements and reproduction in three Costa Rican bat communities. Occasional Papers of the Museum of Natural History (University of Kansas): 69: 1– 28. Lawton, M.F. 1982. Altruism and sociobiology: a critical look at the critical issue. PhD diss., University of Chicago. Chicago. Lawton, M.F. 1983. Cyanocorax morio. In D.H. Janzen, ed., Costa Rican Natural History. Chicago: University of Chicago Press. Lawton, M.F., and C. Guindon. 1981. Flock composition, breeding success, and learning in the Brown Jay. Condor 83: 27– 33. Lawton, M.F., and R.O. Lawton. 1980. Nestsite selection in the Brown Jay. Auk 97(3): 631– 33. Lawton, M.F., and R.O. Lawton. 1985. The breeding biology of the Brown Jay in Monteverde, Costa Rica. Condor 87: 192– 204. Lawton, M.F., and R.O. Lawton. 1986. Heterochrony and the evolution of social organization in birds. Current Ornithology 3: 187– 224.

Lawton, R.O. 1980. Wind and the ontogeny of elfin stature in a Costa Rican lower montane rain forest. PhD diss., University of Chicago. Chicago. Lawton, R.O. 1982. Wind stress and elfin stature in a montane rain forest tree: an adaptive explanation. American Journal of Botany 69: 1224– 30. Lawton, R.O. 1983. Didymopanax pittieri. In D.H. Janzen, ed., Costa Rican Natural History. Chicago: University of Chicago Press. Lawton, R.O. 1984. Ecological constraints on wood density in a tropical montane rain forest. American Journal of Botany 71: 261– 67. Lawton, R.O. 1986. The evolution of strangling by Ficus crassiuscula. Brenesia 25– 26: 273– 78. Lawton, R.O. 1990. Canopy gaps and light penetration into a windexposed tropical lower montane rain forest. Canadian Journal of Forest Research 20: 659– 67. Lawton, R.O. 1991. More on strangling by Ficus crassiuscula: a reply to Ramírez. Brenesia 32: 119– 20. Lawton, R.O., L.D. Alexander, W.N. Setzer, and K.G. Byler. 1993. Floral essential oil of Guettarda poasana inhibits yeast growth. Biotropica 25(4): 483– 86. Lawton, R.O., and V. Dryer. 1980. Vegetation of the Monteverde Cloud Forest Reserve. Brenesia 18: 101– 16. Lawton, R.O., U.S. Nair, R.A. Pielke Sr., and R.M. Welch. 2001. Climatic impact of tropical lowland deforestation on nearby montane cloud forests. Science 294: 584– 87. Lawton, R.O., U.S. Nair, D. Ray, J.A. Pounds, and R.M. Welch. 2010. Quantitative measures of immersion in cloud and the biogeography of cloud forest. In L.A. Bruijnzeel, F.N. Scatena, and L.S. Hamilton, eds., Mountains in the Mist: Science for Conserving and Managing Tropical Montane Cloud Forests. Cambridge, UK: Cambridge University Press. Lawton, R.O., and F.E. Putz. 1988. Natural disturbance and gapphase regeneration in a windexposed tropical lower montane rain forest. Ecology 69: 764– 77. Linhart, Y.B., W.H. Busby, J.H. Beach, and P. Feinsinger. 1987b. Forager behavior, pollen dispersal, and inbreeding in two species of hummingbird-pollinated plants. Evolution 41: 679– 82. Linhart, Y.B., P. Feinsinger, J.H. Beach, W.H. Busby, K.G. Murray, W.Z. Pounds, S. Kinsman, C.A. Guindon, and M. Kooiman. 1987a. Disturbance and predictability of flowering plants in bird-pollinated cloud forest plants. Ecology 68: 1696– 710. Lips, K.R., F. Brem, R. Brenes, J.D. Reeve, R.A. Alford, J. Voyles, C. Carey, L. Livo, A.P. Pessier, and J.P. Collins. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences 103: 3165– 70. Longino, J.T. 1989. Geographic variation and community structure in an ant-plant mutualism: Azteca and Cecropia in Costa Rica. Biotropica 21: 126– 32. Longino, J.T. 2006. A taxonomic review of the genus Myrmelachista (Hymenoptera: Formicidae) in Costa Rica. Zootaxa 1– 54. Maffia, B., N.M. Nadkarni, and D.P. Janos. 2000. Vesicular-arbuscular mycorrhizae of epiphytic and terrestrial Piperaceae. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 338– 39. New York: Oxford University Press. Marshall, J.S., and R.S. Anderson. 1995. Quaternary uplift and seismic

The Montane Cloud Forests of the Volcanic Cordilleras 447 cycle deformation, Península de Nicoya, Costa Rica. Geological Society of America Bulletin 107: 463– 73. Marshall, L.G., S.D. Webb, J.J. Sepkoski, and D.M. Raup. 1982. Mammalian evolution and the Great American Interchange. Science 251: 1351– 57. McDonald, D.B. 1989a. Cooperation under asexual selection: agegraded changes in a lekking bird. American Naturalist 134: 709– 30. McDonald, D.B. 1989b. Correlates of male mating success in a lekking bird with male-male cooperation. Animal Behaviour 37: 1007– 22. McDonald, D.B. 1993a. Delayed plumage maturation and orderly queues for status: a manakin mannequin experiment. Ethology 94: 31– 45. McDonald, D.B. 1993b. Demographic consequences of sexual selection in the Long-tailed Manakin. Behavioral Ecology 4: 297– 309. McDonald, D.B. 2000. Cooperation between male long-tailed manakins. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 204– 5. New York: Oxford University Press. McDonald, D.B. 2007. Predicting fate from early connectivity in a social network. Proceedings of the National Academy of Sciences (USA) 104: 10910– 14. McDonald, D.B., and W.K. Potts. 1994. Cooperative display and relatedness among males in a lek-mating bird. Science 266: 1030– 32. Melson, W.G. 1994. The eruption of 1968 and tephra stratigraphy of Arenal Volcano. In P.D. Sheets and B.R. McKee, eds., Archaeology, Volcanism, and Remote Sensing in the Arenal Region, Costa Rica, 24– 47. Austin, TX: University of Texas Press. Moriarity, D.M., J. Huang, C.A. Yancey, P. Zhang, W.N. Setzer, R.O. Lawton, R.B. Bates, and S. Caldera. 1998. Lupeol is the cytotoxic principle in the leaf extract of Dendropanax cf. querceti from Monteverde, Costa Rica. Planta Medica 64: 370– 72. Murray, K.G. 1986. Consequences of seed dispersal for gap-dependent plants: relationships between seed shadows, germination requirements, and forest dynamic processes. In A. Estrada and T. H. Fleming, eds., Frugivores and Seed Dispersal, 187– 98. Dordrecht: W. Junk Publishers. Murray, K.G. 1988. Avian seed dispersal of three neotropical gapdependent plants. Ecological Monographs 68: 271– 98. Murray, K.G., P. Feinsinger, W.H. Busby, Y.B. Linhart, J.H. Beach, and S.  Kinsman. 1987. Evaluation of character displacement among plants in two tropical pollination guilds. Ecology 68: 1283– 93. Murray, K.G., S. Kinsman, and J.L. Bronstein. 2000. Plant-animal interactions. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 245– 302. New York: Oxford University Press. Murray, K.G., S. Russell, C.M. Piccone, K. Winnett-Murray, W. Sherwood, and M.L. Kuhlmann. 1994. Fruit laxatives and seed passage rates in frugivores: consequences for plant reproductive success. Ecology 75: 989– 94. Myster, R.W. 1993. Spatial heterogeneity of seedrain, seedpool, and vegetative cover on two Monteverde landslides. Brenesia 39– 40: 137– 45. Nadkarni, N.M. 1981. Canopy roots: convergent evolution in rain forest nutrient cycles. Science 214: 1023– 24. Nadkarni, N.M. 1984. Epiphyte biomass and nutrient capital of a neotropical elfin forest. Biotropica 16: 249– 56. Nadkarni, N.M., R.O. Lawton, K.L. Clark, T.J. Matelson, and D. Schaefer.

2000. Ecosystem ecology and forest dynamics. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 303– 50. New York: Oxford University Press. Nadkarni, N.M., and J.T. Longino. 1990. Invertebrates in canopy and ground organic matter in a neotropical montane forest. Biotropica 22: 286– 89. Nadkarni, N.M., and T.J. Matelson. 1989. Bird use of epiphyte resources in neotropical trees. Condor 91: 891– 907. Nadkarni, N.M., and T.J. Matelson. 1991. Dynamics of fine litterfall within the canopy of a tropical cloud forest, Monteverde. Ecology 72: 2071– 82. Nadkarni, N.M., and T.J. Matelson. 1992a. Biomass and nutrient dynamics of epiphyte litterfall in a neotropical cloud forest, Costa Rica. Biotropica 24: 24– 30. Nadkarni, N.M., and T.J. Matelson. 1992b. Biomass and nutrient dynamics of fine litter of terrestrially rooted material in a neotropical cloud forest, Costa Rica. Biotropica 24: 113– 20. Nadkarni, N.M., T.J. Matelson, and W.A. Haber. 1995. Structural characteristics and floristic composition of a neotropical cloud forest, Costa Rica. Journal of Tropical Ecology 11: 481– 94. Nadkarni, N.M., and N. Wheelwright, eds. 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. New York: Oxford University Press. Nair, U.S., S. Asefi, R.M. Welch, D.K. Ray, R.O. Lawton, V.S. Manoharan, M. Mulligan, T.L. Sever, D. Irwin, and J.A. Pounds. 2008. Biogeography of tropical montane cloud forests, Part II: Mapping of orographic cloud immersion. Journal of Applied Meteorology and Climatology, in press. Nair, U.S., R.O. Lawton, R.M. Welch, and R.A. Pielke Sr. 2003. Impact of land use on tropical montane cloud forests: sensitivity of cumulus cloud field characteristics to lowland deforestation. Journal of Geophysical Research 108(D7): 4206– 18. Nair, U.S., D.K. Ray, R.O. Lawton, R.M. Welch, and R.A. Pielke Sr. 2010. The impact of deforestation on orographic cloud formation in a complex tropical environment. In L.A. Bruijnzeel, F.N. Scatena, and L.S. Hamilton, eds., Mountains in the Mist: Science for Conserving and Managing Tropical Montane Cloud Forests. Cambridge, UK: Cambridge University Press. O’Donnell, S., and A. Kumar. 2006. Microclimatic factors associated with elevational changes in army ant density in tropical montane forest. Ecological Entomology 31: 491– 98. Peck, D.C. 1996. The association of spittlebugs with grasslands: ecology of Prosapia (Homoptera: Cercopidae) in upland dairy pastures of Costa Rica. PhD diss., Cornell University. Podolsky, R.D. 1992. Strange floral attractors: pollinator attraction and the evolution of plant sexual systems. Science 258: 791– 93. Portig, W. 1965. Central American rainfall. Geographical Review 55: 68– 90. Pounds, J.A. 1988. Ecomorphology, locomotion, and microhabitat structure: patterns in a tropical mainland Anolis community. Ecological Monographs 58: 299– 320. Pounds, J.A. 2000. Amphibians and reptiles. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 149– 77. New York: Oxford University Press. Pounds, J.A. 2001. Climate and amphibian declines. Nature 410: 639– 40. Pounds, J.A., M.R. Bustamante, L.A. Coloma, J.A. Consuegra, M.P.L.

448 Chapter 13 Fogden, P.N. Foster, E. La Marca, K.L. Masters, A. Merino-Viteri, R. Puschendorf, S.R. Ron, G.A. Sánchez-Azofeifa, C.J. Still, and B.E. Young. 2005. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439: 161– 67. Pounds, J.A., and M.L. Crump. 1994. Amphibian declines and climate disturbance: the case of the Golden Toad and the Harlequin Frog. Conservation Biology 8: 72– 85. Pounds, J.A., and M.P.L. Fogden. 2000. Amphibians and reptiles of Monteverde. Appendix 8. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 537– 40. New York: Oxford University Press. Pounds, J.A., M.P.L. Fogden, and J.H. Campbell. 1999. Biological response to climate change on a tropical mountain. Nature 389: 611– 14. Pounds, J.A., M.P.L. Fogden, J.M. Savage, and G.C. Gorman. 1997. Tests of null models for amphibian declines on a tropical mountain. Conservation Biology 11: 1307– 22. Pounds, J.A., and R. Puschendorf. 2004. Ecology: clouded futures. Nature 427: 107– 9. Powell, G.V.N. 1979. Structure and dynamics of interspecific flocks in a neotropical mid-elevation forest. Auk 96: 375– 90. Powell, G.V.N. 1980. Migrant participation in neotropical mixed species flocks. In A. Keast and E. S. Morton, eds., Migrant Birds in the Neotropics: Ecology, Behavior, Distribution and Conservation, 477– 83. Washington, DC: Smithsonian Institution Press. Powell, G.V.N. 1985. Sociobiology and adaptive significance of interspecific foraging flocks in the Neotropics. Ornithological Monographs 36: 713– 32. Powell, G.V.N., and R.D. Bjork. 1994. Implications of altitudinal migration for conservation strategies to protect tropical biodiversity: a case study of the Resplendent Quetzal Pharomachrus mocinno at Monteverde, Costa Rica. Bird Conservation International 4: 161– 74. Powell, G.V.N., R.D. Bjork, S. Barrios, and V. Espinoza. 2000. Elevational migrations and habitat linkages: using the resplendent quetzal as an indicator for evaluating the design of the Monteverde reserve complex. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 439– 42. New York: Oxford University Press. Prance, G.T. 1990. The floristic composition of the forests of central Amazonian Brazil. In A. H. Gentry, ed., Four Neotropical Rainforests, 112– 40. New Haven, CT: Yale University Press. Rauscher, S.A., F. Giorgi, N.S. Diffenbaugh, and A. Seth. In press. Extension and intensification of the Meso-American mid-summer drought in the 21st Century. Climate Dynamics. Ray, D.K., U.S. Nair, R.O. Lawton, R.M. Welch, and R.A. Pielke Sr. 2006. Impact of land use on Costa Rican tropical montane cloud forests: sensitivity of orographic cloud formation to deforestation in the plains. Journal of Geophysical Research 111. doi:10.1029/2005JD006096. Rhodes, A.L., A.J. Guswa, and S.E. Newell. 2006. Seasonal variation in the stable isotope composition of precipitation in the tropical montane forests of Monteverde, Costa Rica. Water Resources Research 42: W11402. doi:10.1029/2005WR004535. Riley, C.M. 1986. Observations of the breeding biology of Emerald Toucanets in Costa Rica. Wilson Bulletin 98: 585– 88. Riley, C.M., and K.G. Smith. 1992. Sexual dimorphism and foraging behavior of Emerald Toucanets Aulacorhynchus prasinus in Costa Rica. Ornis Scandinavica 23: 259– 66.

Sargent, S. 1993. Nesting biology of the yellow-throated Euphonia: large clutch size in a neotropical frugivore. Wilson Bulletin 105: 285– 300. Sargent, S. 1995. Seed fate in a tropical mistletoe: the importance of host twig size. Functional Ecology 9: 197– 204. Sargent, S. 2000. Specialized seed dispersal: mistletoes and fruit-eating birds. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 288– 89. New York: Oxford University Press. Schonberg, L.A., J.T. Longino, N.M. Nadkarni, S.P. Yanoviak, and J.C. Gering. 2004. Arboreal ant species richness in primary forest, secondary forest, and pasture habitats of a tropical montane landscape. Biotropica 36: 402– 9. Setzer, M.C., D.M. Moriarity, R.O. Lawton, W.N. Setzer, G.A. Gentry, and W.A. Haber. 2003. Phytomedicinal potential of tropical cloudforest plants from Monteverde, Costa Rica. Revista de Biología Tropical 51(3– 4): 647– 74. Setzer, W.N. 2000. The search for medicines from the plants of Monteverde. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 452– 53. New York: Oxford University Press. Setzer, W.N., M.N. Flair, K.G. Byler, J. Huang, M.A. Thompson, A.F. Setzer, D.M. Moriarity, R.O. Lawton, and D.B. Windham-Carswell. 1992. Antimicrobial and cytotoxic activity of crude extracts of Araliaceae from Monteverde, Costa Rica. Brenesia 38: 123– 30. Setzer, W.N., T.J. Green, R.O. Lawton, D.M. Moriarity, R.B. Bates, S. Caldera, and W.A. Haber. 1995a. Antibacterial activity of a vitamin E derivative from Tovomitopsis psychotrifolia. Planta Medica 61: 275– 76. Setzer, W.N., T.J. Green, K.W. Whitaker, D.M. Moriarity, R.O. Lawton, R.B. Bates, and S. Caldera. 1995b. A cytotoxic diacetylene from Dendropanax arboreus (L.) Decne. & Planchon (Araliaceae). Planta Medica 61: 470– 71. Setzer, W.N., J.A. Noletto, and R.O. Lawton. 2006. Chemical composition of the floral essential oil of Randia matudae from Monteverde, Costa Rica. Flavor and Fragrance Journal 21(2): 244– 46. Setzer, W.N., J.A. Noletto, R.O. Lawton, and W.A. Haber. 2005. Leaf essential oil composition of five Zanthoxylum species from Monteverde, Costa Rica. Molecular Diversity 9: 3– 13. Setzer, W.N., M.C. Setzer, A.L. Hopper, D.M. Moriarity, G.K. Lehrman, K.L. Niekamp, S.M. Moorcomb, R.B. Bates, K.J. McClure, C.C. Stessman, and W.A. Haber. 1998. The cytotoxic activity of a Salacia liana species from Monteverde, Costa Rica is due to a high concentration of tingenone. Planta Medica 64: 583. Setzer, W.N., M.C. Setzer, D.M. Moriarity, R.B. Bates, and W.A. Haber. 1999. Biological activity of the essential oil of Myrcianthes sp. nov. “black fruit” from Monteverde, Costa Rica. Planta Medica 65: 468– 69. Setzer, W.N., M.C. Setzer, J.M. Schmidt, D.M. Moriarity, B. Vogler, S. Reeb, A.M. Holmes, and W.A. Haber. 2000b. Cytotoxic components from the bark of Stauranthus perforatus from Monteverde, Costa Rica. Planta Medica 66: 493– 94. Setzer, W.N., X. Shen, R.B. Bates, J.R. Burns, K.J. McClure, P. Zhang, D.M. Moriarity, and R.O. Lawton. 2000a. A phytochemical investigation of Alchornea latifolia. Fitoterapia 71: 195– 98. Sheets, P.D., J. Hoopes, W. Melson, B. McKee, T. Sever, M. Mueller, M. Chenault, and J. Bradley. 1991. Prehistory and volcanism in the Arenal area, Costa Rica. Journal of Field Archaeology 18: 445– 65.

The Montane Cloud Forests of the Volcanic Cordilleras 449 Sheets, P.D., and B.R. McKee, eds. 1994. Archaeology, Volcanism, and Remote Sensing in the Arenal Region, Costa Rica. Austin, TX: University of Texas Press. Shopland, J. 2000. The cost of social foraging in mixed-species bird flocks. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 206– 7. New York: Oxford University Press. Siebert, L., G.E. Alvarado, J.W. Vallance, and B. van Wyk de Vries. 2006. Large-volume volcanic edifice failures in Central America and associated hazards. In W.I. Rose, G.J.S. Bluth, M.J. Carr, J.W. Ewert, L.C. Patino, and J.W. Vallance, eds., Volcanic Hazards in Central America, Geological Society of America Special Paper 412: 1– 26. Sillet, S.C., S.R. Gradstein, and D. Griffin. 1995. Bryophyte diversity of Ficus tree crowns from intact cloud forest and pasture in Costa Rica. Bryologist 98: 251– 60. Skutch, A.F. 1935. Helpers at the nest. Auk 52: 257– 73. Still, C.J., P.N. Foster, and S.H. Schneider. 1999. Simulating the effects of climate change on tropical montane cloud forests. Nature 389: 608– 10. Tiebout, H.M. 1991. Daytime energy management by tropical hummingbirds: responses to foraging constraint. Ecology 72: 839– 51. Timm, R.M., and R.K. LaVal. 2000a. Mammals. In N. Nadkarni and N.  Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 223– 44. New York: Oxford University Press. Timm, R.M., and R.K. LaVal. 2000b. Mammals of Monteverde. Appendix 10. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 553– 57. New York: Oxford University Press. Tobón-Marín, C., S.A. Bruijnzeel, A. Frumau, and J. Calvo. 2010. Changes in soil hydraulic properties and soil water status after conversion of tropical montane cloud forest to pasture in northern Costa Rica. In L.A. Bruijnzeel, F.N. Scatena, and L.S. Hamilton, eds., Mountains in the Mist: Science for Conserving and Managing Tropical Montane Cloud Forests. Cambridge, UK: Cambridge University Press. Tosi, J.A. 1969. Mapa Ecológico de Costa Rica, Basado en la Clasificación Vegetal Mundial de L.R. Holdridge. Scale 1: 750,000. San Pedro de Montes de Oca, Costa Rica: Tropical Science Center ( TSC). Trainer, J.M. 2000. The roles of long-tailed manakin vocalization in cooperation and courtship. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 215– 16. New York: Oxford University Press. Trainer, J.M., and D.B. McDonald. 1993. Vocal repertoire of the longtailed manakin and its relation to male-male cooperation. Condor 95: 769– 81. Trainer, J.M., and D.B. McDonald. 1995. Singing performance, frequency matching, and courtship success of long-tailed manakins (Chiroxiphia linearis). Behavioral Ecology and Sociobiology 37: 249– 54. Valburg, L.K. 1992. Flocking and frugivory: the effect of social groupings on resource use in the Common Bush-Tanager. Condor 94: 358– 63. Valburg, L.K. 2000. Why join mixed-species flocks?: a frugivore’s perspective. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 205– 6. New York: Oxford University Press. Vance, E., and N.M. Nadkarni. 1990. Microbial biomass and activity in

canopy organic matter and the forest floor of a tropical cloud forest. Soil Biology and Biochemistry 22: 677– 84. Vance, E., and N.M. Nadkarni. 1992. Root biomass distribution in a moist tropical montane forest. Plant and Soil 142: 31– 39. Van Devender, R.W. 1980. Preliminary checklist of the herpetofauna of Monteverde, Puntarenas Province, Costa Rica and vicinity. Brenesia 17: 319– 25. Weiss, M.E. 1996. Pollen-feeding fly alters floral phenotypic gender in Centropogon solanifolius (Campanulaceae). Biotropica 28: 770– 73. Welch, R.M., S. Asefi, U.S. Nair, Q. Han, R.O. Lawton, D.K. Ray, and V.S. Manoharan. 2008. Biogeography of tropical montane cloud forests, Part I: Remote sensing of cloud base heights. Journal of Applied Meteorology and Climatology 47: 960– 75. Wenny, D.G. 2000a. What happens to seeds of vertebrate-dispersed trees after dispersal? In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 286– 87. New York: Oxford University Press. Wenny, D.G. 2000b. Seed dispersal, seed predation, and seedling recruitment of Ocotea endresiana (Lauraceae) in Costa Rica. Ecological Monographs 70: 331– 51. Wenny, D.G., and D.J. Levey. 1998. Directed seed dispersal by bellbirds in a tropical cloud forest. Proceedings of the National Academy of Sciences (USA) 95: 6204– 07. Wheelwright, N.T. 1983. Fruits and the ecology of Resplendent Quetzals. Auk 100: 286– 301. Wheelwright, N.T. 1985a. Competition for dispersers, and the timing of flowering and fruiting in a guild of tropical trees. Oikos 44: 465– 77. Wheelwright, N.T. 1985b. Fruit size, gape width, and the diets of fruiteating birds. Ecology 66: 808– 18. Wheelwright, N.T. 1986. A seven-year study of individual variation in fruit production in tropical bird-dispersed tree species in the family Lauraceae. In A. Estrada and T.H. Fleming, eds., Frugivores and Seed Dispersal, 19– 35. Dordrecht: W. Junk Publishers. Wheelwright, N.T. 1991. How long do fruit eating birds stay in the plants where they feed? Biotropica 23: 29– 40. Wheelwright, N.T. 1993. Fruit size in a tropical tree species: variation, preference by birds, and hereditability. Vegetatio 107/108: 163– 74. Wheelwright, N.T. 2000. Conservation biology. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 419. New York: Oxford University Press. Wheelwright, N.T., and A. Bruneau. 1992. Population sex ratios and spatial distribution of Ocotea tenera (Lauraceae) trees in a tropical forest. Journal of Ecology 80: 425– 32. Wheelwright, N.T., W.A. Haber, K.G. Murray, and C. Guindon. 1984. Tropical fruit-eating birds and their food plants: a survey of a Costa Rican lower montane forest. Biotropica 16: 173– 91. Williams, D.A. 2004. Female control of reproductive skew in cooperatively breeding brown jays (Cyanocorax morio). Behavioral Ecology and Sociobiology 55: 370– 80. Williams, D.A., E.C. Berg, A.M. Hale, and C.R. Hughes. 2004. Characterization of microsatellites for parentage studies of white-throated magpie-jays (Calocitta formosa) and brown jays (Cyanocorax morio). Molecular Ecology Notes 4: 509– 11. Williams, D.A., and A.M. Hale. 2006. Helper effects on offspring production in cooperatively breeding brown jays (Cyanocorax morio). Auk 123: 847– 57. Williams, D.A., and M.F. Lawton. 2000. Brown Jays: complex sociality

450 Chapter 13 in a colonizing species. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 212– 13. New York: Oxford University Press. Williams, D.A., M.F. Lawton, and R.O. Lawton. 1994. Population growth, range expansion, and competition in the cooperatively breeding Brown Jay, Cyanocorax morio. Animal Behavior 48: 309– 22. Williams, D.A., and K.N. Rabenold. 2005. Male-biased dispersal, female philopatry, and routes to fitness in a social corvid. Journal of Animal Ecology 74: 150– 59. Williams-Linera, G., and R.O. Lawton. 1995. The ecology of hemiepiphytes. In M. Lowman and N. Nadkarni, eds., Forest Canopies, 255– 82. Academic Press. Winnett-Murray, K. 2000. Choosiness and productivity in wrens of forests, fragments and farms. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 208– 10. New York: Oxford University Press. Yanoviak, S.P., N.M. Nadkarni, and R. Solano. 2007. Arthropod assemblages in epiphyte mats of Costa Rican cloud forests. Biotropica 39: 202– 10.

Yanoviak, S.P., H. Walker, and N.M. Nadkarni. 2004. Arthropod assemblages in vegetative vs. humic portions of epiphyte mats in a neotropical cloud forest. Pedobiologia 48: 51– 58. Yoshikawa, F., S. Kaizuka, and Y. Ota. 1981. The Landforms of Japan. Tokyo: University of Tokyo Press. Young, B.E. 1993. Effects of the parasitic botfly Philornis carinatus on nestling House Wrens, Troglodytes aedon. Oecologia 93: 256– 62. Young, B.E. 1994a. The effects of food, nest predation and weather on the timing of breeding in tropical House Wrens. Condor 96: 341– 53. Young, B.E. 1994b. Geographic and seasonal patterns of clutch-size variation in House Wrens. Auk 111: 545– 55. Young, B.E. 1996. An experimental analysis of small clutch size in tropical House Wrens. Ecology 77: 472– 88. Young, B.E., and D.B. McDonald. 2000. Birds. In N. Nadkarni and N. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 179– 222. New York: Oxford University Press. Zadroga, F. 1981. The hydrological importance of a montane cloud forest area of Costa Rica. In R. Lal and E.W. Russell, eds., Tropical Agricultural Hydrology, 59– 73. New York: J. Wiley and Sons.

Chapter 14 The Montane Cloud Forests of the Cordillera de Talamanca

Maarten Kappelle1

Dedication I dedicate this chapter to my mother, Mary E. Mohr (b. 1936), and to the memory of my father, Dirk Kappelle (b. 1928– d. 2008), who inspired me to become a biologist. Being a dentist in his professional life, Dirk was a man of many talents and a naturalist in heart and soul. As a nature photographer he earned many prizes and participated in numerous expositions. One of the most remarkable ones was the photo exhibition in St. Andrews Hospital (“Andreas Ziekenhuis”) in Amsterdam, exactly during the week that my wife Marta gave birth to our son Derk (April 1995). During my childhood (1960s and early 1970s) every weekend Dirk and Mary took me and my two brothers out to enjoy the marvels of nature in the Netherlands. We made long hikes through the then-mushroom-laden temperate oak-beech forests and coastal sand dunes with their ever changing skies often painted by seventeenth-century Dutch masters like Vermeer. Numerous times we visited preserves in the brackish estuaries of the River Rhine’s delta— a bird watchers’ paradise and one of the most important European wetlands for thousands of migratory waterfowl that each boreal autumn fly to Africa with the aim to pass the cold winter at warmer latitudes southwards. It was here that my passion for nature was born, and I am still thankful to my parents for showing me all these natural wonders and wildlife spectacles. After his retirement Dirk authored a book on the twentieth-century history of Dutch freshwater fishing in the 1 World Wide Fund for Nature (WWF International), Avenue du MontBlanc 1196, Gland, Switzerland, and Department of Geography, University of Tennessee, Knoxville, TN

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backwaters of the Rhine delta. The work was published in Dutch in 2003 titled “Fishermen from the Inland.” It narrates the personal histories of 31 artisanal fishermen, born around the year 1900, who dedicated their professional lives to traditional inland fishing in the Netherlands. Many of them specialized in capturing fish like eel and salmon that are now extinct or near-extinct in the numerous wide rivers that slowly traverse the Dutch lowlands. His nicely written document humain is perhaps the only account based on personal interviews that is available on this particular topic, since almost no artisanal inland fishermen remain in the country. Being nature lovers pur sang, Dirk and Mary both visited me in Costa Rica on four occasions (1986, 1988– 1989, 1999, and 2000– 2001). During their month-long visits we made multiple trips to get a grasp of the true riches of the country: we traveled from Golfito to Gandoca, from Santa Rosa to San Gerardo de Dota, from Tortuguero to Tucurrique, from Cañas to Corcovado, and from Monteverde to Mansión. It was during these countless trips that I got a good impression of the diversity of the country’s different habitats that made me undertake the endeavor to develop the current volume on Costa Rica’s ecosystems, now in your hands. I am thankful to them for their continual support to my research and writings on the ecological systems of this country that I fell so much in love with back in 1985.

Introduction The tropical evergreen cloud forest of Costa Rica’s southern highlands include both true tropical montane cloud

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Fig. 14.1 Map of the main mountain peaks, towns, indigenous reserves and protected areas located in the Talamancan highland forest region and its adjacent areas. Map prepared by Marco V. Castro.

forest (TMCF) sensu Hamilton et al. (1995) and seasonal cloud forests with less cloud persistence throughout the year (Stadtmüller 1987, Kappelle et al. 1999, Kappelle and Brown 2001). These highland forests occur between 500 and 3,500 meters above sea level (m a.s.l.) and cover both the Pacific and Atlantic slopes of the Cordillera de Talamanca, the tallest and largest mountain range in southern Central America (Fig. 14.1). It runs from the Cerros de

Escazú (Fig. 14.2) in central Costa Rica southwestward into western Panama (Kappelle 1996). Costa Rica’s southern evergreen cloud forest is part of the Talamanca montane forest ecoregion sensu Olson and Dinerstein (2002). It is vital to the country’s society since its many rivers provide drinking and irrigation water to the populations of the main cities in the Valle Central (San José, Alajuela, Heredia, and Cartago), as well as to those

The Montane Cloud Forests of the Cordillera de Talamanca 453

in the valleys of the southern Pacific region (e.g., San Isidro del General, Buenos Aires de Puntarenas, San Vito de Java) and the southern Caribbean zone (e.g., Limón, Cahuita, Bribri, Sixaola) (Kappelle 1996, Valerio 1999). Moreover, the many hydroelectric power plants that have been built in cascade in the river systems of the Cordillera de Talamanca provide much of the country’s hydropower (e.g., the hydro stations of Angostura, Cachí, and Río Macho in the middle and upper sections of the Río Reventazón basin). Levels of species diversity and endemism are extraordinarily high in the Talamancan evergreen cloud forest owing to its relative isolation and geological past as an island archipelago, separated from the South American Andes by the Darién gap in eastern Panama, and disconnected from the Chiapas-Guatemalan mountain complex by the Nicaraguan Depression to the northwest. As a result, a large number of species is restricted to the Cordillera de Talamanca or shared only with Costa Rica’s northern volcanic cordilleras

(see Lawton et al., chapter 13 of this volume), making the Talamanca highlands and its La Amistad Biosphere Reserve of global importance (Kappelle and Brown 2001, 2003).

History of Scientific Exploration Since the early twentieth century the evergreen montane forests of the Cordillera de Talamanca have been explored by a fair number of scientists, though not as much as the cloud forests of the volcanic cordilleras in the north where places like the Monteverde Cloud Forest Preserve have received significant attention from dozens of scientists over the past few decades (Nadkarni and Wheelwright 2000; Lawton et al., chapter 13 of this volume). The first naturalists to study the flora of the Talamancan montane forests were Henri Pittier (1957) and Paul Standley (1937), whose work laid the foundation for today’s botanical knowledge of the

Fig. 14.2 View of a lower montane cloud forest in the disturbed northern sector of the Cordillera de Talamanca at the 2,270 m tall Pico Blanco, Cerros de Escazú. Photograph by Marta Juárez 2006.

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country’s southeastern highland forests (Hammel et al. 2004). Decades later, prominent authors such as Holdridge et al. (1971) contributed with rapid inventories of the country’s forests, including the evergreen oak-dominated cloud forests near Villa Mills (2,500– 3,000 m a.s.l.) just east of Cerro de la Muerte. However, it was not until the early 1980s when more detailed studies on the biodiversity, ecology and sustainable management of the Talamancan montane forests appeared (e.g., see Hartshorn 1983, Gómez 1986, Jiménez et al. 1988, Stadtmüller and Aus der Beek 1992, Chaverri and Hernández 1995, Guariguata and Sáenz 2002, as well as Kappelle 1996, 2006a, 2008, Köhler 2002, Holl and Lulow 1997). These and other authors have contributed considerably to the current knowledge of the patterns and underlying processes that define the composition, structure, and functioning of the montane cloud forests of the Cordillera de Talamanca discussed in this chapter.

The Physical Environment Climate

The evergreen montane cloud forest zone of southern Costa Rica is generally very moist and cool with moderate water deficits (Nuhn 1978, Coen 1983, Herrera 1986 and chapter 2 of this volume). According to the Köppen climate system, the Talamancan cloud forests enjoy a “Cf” climate with a short dry period generally running from midDecember to April (known as verano or “summer”), and a rainy season during the remaining seven to nine months (invierno or “winter”). Cloud formation and persistence is often more intense and severe along the Atlantic slopes of the cordillera owing to the influence of the Trade Winds that blow from the Caribbean lowlands southward (Coen 1983, and see chapter 13 of this volume by Lawton et al. on the cloud forests of the northern volcanic mountains). As a result, the Atlantic or Caribbean slopes receive much more rainfall and fog than the Pacific slopes, with differing implications for the floristic composition of the vegetation along both slopes (Kappelle 1992). Similarly, the valley of the Río Grande de Térraba near Potrero Grande is relatively dry owing to a clear rain shadow effect, which is reflected in the presence of a xeric vegetation type dominated by deciduous trees (e.g., Bursera simarouba). Throughout the year but mostly in the rainy season, condensation belts with fog penetrating the forest canopy develop, often with their cloud base around 2,000 m elevation (Zadroga 1981, Mulligan 2010). As a result, the relative humidity of the air in the forest interior is normally in the

range of 75 to 90%. In oak forests near San Gerardo de Dota along the Pacific slope between 2,500 and 3,000 m, for instance, relative atmospheric humidity levels oscillated between 35– 95% in the 1992 dry season and between 70– 90% in the 1992 rainy season (Van Dunné and Kappelle 1998). Depending on slope orientation and cloud persistence levels the average annual temperature in Talamanca’s highland forests ranges from 5– 11°C at the highest forested peaks and crests over 3,000 m to 13– 16°C at an altitude of 2,300 m, and 20– 25°C at elevations of about 1,000 m (Herrera 1986, Chinchilla 1987, IMN 1988). Yearly mean temperatures of 25°C are common in the mid-elevation watershed of the Río Grande de Térraba, while the annual average temperature at 3,500 m elevation at the Chirripó Massif only reaches 5°C (Mora Carpio 2000). In general, average yearly temperatures decrease about 0.57°C per every 100 m increase in elevation, as has been calculated on the basis of air temperature records taken at breast height in oak forest interiors at different montane altitudes along the Pacific slope of Cerro Chirripó (Kappelle et al. 1995b). Herrera (1986 and chapter 2 of this volume) distinguishes a total of eight climate types in the Cordillera de Talamanca: (i) a very warm, sub-humid to dry climate in, for example, the Valle del Río Grande de Térraba and Reserva Indígena Boruca-Térraba (annual averages: temperature >27°C, rainfall 1,300– 1,700 mm); (ii) a very warm, sub-humid to humid climate in the Río Grande de Térraba watershed (annual averages: temperature 21– 27°C, rainfall 1,550– 2,050 mm); (iii) a very warm, humid climate near Paso Real and Potrero Grande in the Río Grande de Térraba watershed (annual averages: temperature 21– 27°C, rainfall 1,900– 3,100 mm); (iv) a very warm, humid to wet climate in the Río Coto Brus watershed (annual averages: temperature 23– 27°C, rainfall 3,100– 3,400 mm); (v) a warm to cool or cold, humid to wet climate in, for example, the Parque Nacional Tapantí– Macizo de la Muerte, Parque Nacional Chirripó, Parque Internacional La Amistad, and Zona Protectora Las Tablas (annual averages: temperature 6– 26°C, rainfall 1,600– 6,800 mm); (vi) a temperate or cold, wet climate in the northern sector of Parque Nacional Tapantí– Macizo de la Muerte and the northeastern sector of Parque Nacional Chirripó (annual averages: temperature 12– 15°C, rainfall 4,500– 8,000 mm). Although January is normally the coldest month, during which frost may occur occasionally, monthly temperatures do not change a lot throughout the year. However, temperatures do vary significantly during single days— a typical characteristic of diurnal climates— as is shown by weather data collected near Villa Mills at 3,000 m. Here, the yearly mean temperature is 10.9°C, while daily temperatures can

The Montane Cloud Forests of the Cordillera de Talamanca 455

Fig. 14.3 View of the Cordillera de Talamanca between Cerro Urán and Cerro Chirripó, as seen from the Inter-American Highway between Villa Mills and San Isidro del General. Normally, the montane forests just below the treeless páramo belt are bathed in clouds on a daily basis. Photograph by Maarten Kappelle, 2004.

reach minimum values of 6°C during the night and maximum values of 22°C during the day (IMN 1988). Most precipitation in the high Cordillera de Talamanca is purely orographic and results from the formation of condensation belts (Zadroga 1981, Coen 1983, Fig. 14.3). Average rainfall in the montane forests at the Pacific slope of the cordillera ranges from 2,000 to 3,000 mm annually (Reserva Indígena Boruca-Térraba: ca. 2,000 mm; Ojo de Agua: 2,648 mm; Villa Mills: 2,812 mm; Tres de Junio: 3,000 mm; data from IMN 1988). Köhler et al. (2006, 2010) measured incident rainfall (gross precipitation) in montane oak forests at Talamancan Pacific slopes around 2,800 m, and recorded 2,800– 2,900 mm per year. Along the Caribbean slopes in the higher parts of the Atlantic zone of the Cordillera de Talamanca, the average yearly rainfall may reach values up to 5,000 mm. This is the case in the upper watershed of the Río Grande de Orosi, in the Parque

Nacional Tapantí– Macizo de la Muerte at elevations of 1,500 to 2,500 m (Mora Carpio 2000). A large part of the total amount of rainwater available in these forests originates from fog and is scientifically known as “horizontal precipitation” (Bruijnzeel 2001). Epiphytes contribute considerably to total rainfall interception in these mist forests by intercepting cloud water from horizontal precipitation (Hölscher et al. 2004). Geology and Geomorphology

The formation of Costa Rica’s present territory began as a result of tectonic activity in the Mesozoic period (Upper Jurassic) with the appearance of the Western Archipelago— a chain of Mesoamerican islands (Lloyd 1963; Alvarado and Cárdenas, chapter 3 of this volume). Later, in the Upper Miocene, a violent uplifting of the region formed the Me-

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soamerican Isthmus (Lloyd 1963, Seyfried et al. 1987). Whereas the volcanic cordilleras of northern Costa Rica obtained their current form as a result of recent volcanism (Lawton et al., chapter 13 of this volume), the 320 km long Cordillera de Talamanca was formed by the accumulation of Tertiary marine sediments as well as by volcanic activity (Seyfried et al. 1987, Alvarado and Cárdenas, chapter 3 of this volume). The Tertiary oceanic sediments that form the base of the Cordillera de Talamanca are several kilometers thick and are made up of conglomerates, sandstones, marls, limestones, and siliceous shales. Fossils, however, are rather scarce. The intercalated volcanic rocks consist of stratigraphically associated lavas and pyroclastic deposits with intrusive rocks (plutonic rocks from the Miocene) that represent gabbros, granodiorites (basic), monzonites, quartzites, and intermediate aplitic granites (Weyl 1980, Castillo 1984). Today, Paleocene-Eocene sediments are found in the eastern part of Parque Nacional Tapantí– Macizo de la Muerte and in the northern sector of Parque Nacional Chirripó. Oligocene-Miocene sediments, in turn, are characteristic of the western sector of Parque Nacional Chirripó and the area south of San Isidro de El General. MiocenePliocene rocks of volcanic origin dominate the western part of part of Parque Nacional Tapantí– Macizo de la Muerte and the southern sector of Parque Nacional Chirripó, as well as the indigenous reserves of Cabagra, Salitre, and Ujarrás, and Zona Protectora Las Tablas. Finally, Tertiary and Quaternary sediments are predominant in the valleys of the Río General and Río Coto Brus (Tournon and Alvarado 1997). In the Cordillera de Talamanca, the effects that Pleistocene glaciers had on the páramo-covered alpine vegetation belt over 3,200 m altitude are evident (Weyl 1955, Hastenrath 1973, Bergoeing 1977, Kappelle and Horn 2005, and chapter 15 of this volume). Below the alpine páramo zone, the montane forest belt with its (upper) Montane, Lower Montane, and Premontane zones extends down to about 500 m. It is characterized by a very rugged physiography with highly dissected fluvial land forms, a dendritic drainage pattern, narrow crests, steep slopes, and deep, V-shaped valleys (Van Uffelen 1991). Slopes are typically convex, with angles ranging from 20 to 40 degrees (sometimes up to 50 degrees) (Kappelle et al. 1989). Today, the terrain of the Talamancan highlands is dominated by land forms of tectonic and erosive origin. Glacial forms dominate only at the highest peaks, which are covered by páramo vegetation. Alluvial sedimentation is the predominant geomorphology in the valley bottoms of large basins like the Río General and Río Coto Brus. Land forms of volcanic origin are restricted to the area between San

Vito de Java (Coto Brus), Cañas Gordas, and Ciudad Neily (Madrigal and Rojas 1980). The Cordillera de Talamanca is drained by an extensive network of primary and secondary rivers (Pringle et al., chapter 18 of this volume). The main rivers that originate in the Talamancan páramos and montane forests and that drain into the Caribbean Sea are— from north to south— the Río Reventazón, Río Grande de Orosi, Río Pacuare, Río Chirripó Atlántico, Río Telire, Río Estrella, Río Coén, and Río Urén, the latter two of which join to form the Río Sixaola at the border with Panama. In turn, the principal rivers that traverse the Talamancas towards the Pacific coast are the Río Candelaria, Río Parrita, Río Naranjo, Río Savegre, and Río Grande de Térraba or Río Grande de Diquís. The watershed basin of the 160 km long Río Grande de Térraba is the largest in the country and measures up to 507,680 ha (Mora Carpio 2000). It includes two main tributary subsystems: the Río General in the western sector (Valle del General) and the Río Coto Brus in the eastern part of the watershed area. Soils

Talamancan montane forest soils are generally developed in ashes that originate from the volcanoes in the northern cordilleras (Vásquez 1983). These soils are typically dark, deep, and rich in organic material, with medium textures, low levels of fertility, and excessive drainage. Soils that have developed in mountain forest areas are often acid with pH values ranging from 3.7 to 5.5 at depths of 15 cm ( Jiménez and Chaverri 1982, Kappelle 1987, Kappelle et al. 1995b). Inceptisols predominate in the western sector of the Parque Nacional Tapantí— Macizo de la Muerte, south of Buenos Aires de Puntarenas, and around San Vito de Java. Entisols, in turn, are the main soil group in the upper part of the Parque Nacional Chirripó, and in the southern sector of the Fila Costeña. Furthermore, Ultisols are found throughout the Cordillera Talamanca and are widely spread in the eastern sector of the Parque Nacional Tapantí— Macizo de la Muerte, the Valle de El General, the indigenous reserves of Cabagra, Salitre, and Ujarrás, and Zona Protectora Las Tablas (Pérez et al. 1978). At mid and high elevations (>2,000 m) soils may occur that contain yellow-brown to red-brown residual clays: andepts, tropepts, udults, and ustalfs (Otárola and Alvarado 1976, Vásquez 1983, Van Uffelen 1991, Kappelle et al. 1995b, Kappelle and Van Uffelen 2006, Alvarado and Mata, chapter 4 of this volume). In their pioneering soil study, Otárola and Alvarado (1976) described montane forest soils such as Lithic Tropofolists at higher elevations, Tropohumods and Dystrandepts at intermediate

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elevations, and Dystrandepts at lower altitudes. Similarly, Gómez (1986) relates mountain forests of the Cordillera de Talamanca with Typic Dystrandepts, Typic Placandepts, and Andic Humitropepts associated with Entic Dystrandepts and Andic Tropohumults. Soils of mature old-growth oak forests generally have dark brown humus profiles composed of fine organic material, free of litter fragments, and with only little mineral material (Landaeta et al. 1978, Van Uffelen 1991, Hertel et al. 2003). In such volcanic ash– derived soils in the montane zone of the Cordillera de Talamanca (2,000– 3,000 m), sand mineralogy is generally dominated by feldspars, though volcanic glass may occasionally occur in soil profiles at lower elevation; similarly, clay mineralogy is consistently amorphous and mainly allophanic (Landaeta et al. 1978). Humus layers are usually less profound along drier Pacific slopes (2,000 and 3,000 m), where they reach a thickness of only 10 to 20 cm. On the contrary, they are much better developed at similar altitudes along the water-soaked Atlantic slopes where they can reach a thickness of up to 40 cm (Kappelle et al. 1995b, Kappelle and Van Uffelen 2006). Here, soil water saturation, in combination with an anaerobic environment and low temperatures, significantly reduces belowground bioactivity and subsequently slows down decomposition rates. In montane oak forests, the soil carbon pool size ranges from about 500 mol m− 2 in the organic layer to 12.5 mol m− 2 in the mineral topsoil. The molar C/N ratios in both soil layers fluctuate between 25 and 28. Similarly, N concentrations range from 100 to 150 mol m− 3, and P concentrations from 2.5 to 12 mol m− 3 (Hertel et al. 2003 and 2006). Furthermore, these authors observed a very large fine root biomass (>1,300 g m− 2) in the soils of upper montane oldgrowth oak forest, which contrasts with other mature forests in the humid tropics that typically have fine root biomass levels below 1,000 g m− 2.

Plant Geography and Distribution In biogeographical terms Costa Rica and its neighboring countries are part of the Central American Floristic Province as defined by Takhtajan (1986). Costa Rica’s variety of environments created by different seasonal rainfall patterns, the presence of rugged, mountainous zones and gorges, together with lowlands, rich volcanic soils, the proximity of continental areas rich in species, as well as the area’s geological history as an archipelago, all contribute to the country’s high biodiversity, especially in the highlands (Burger 1980, Stehli and Webb 1985). The glacial era influenced Costa Rica’s present-day bio-

diversity considerably and generated a dynamic system of great floristic and faunal heterogeneity (Hooghiemstra et al. 1992). The immigration of plants from mountainous zones in both the north (Mexico, Guatemala) and south (the Andes) played a key role in the development of Costa Rica’s montane forest flora (Gentry 1982, Graham 1989, Kappelle et al. 1992, 2000). Opportunities for species migration between North and South America, formally known as the “Great American Biotic Interchange” (GABI) (Stehli and Webb 1985, Graham 1989), increased significantly once the two subcontinents were connected by the Panamanian Isthmus, which was formed some four to five million years ago (Berry 1918, Keighwin 1982, Donnelly 1989). With regard to modern biogeography there are a few classic studies, such as the pioneering work by Wercklé (1909) and Holdridge et al. (1971) as well as the vegetation synopsis developed by Gómez (1986). More recently, Kappelle et al. (1992) compared the floristic affinity of the highland forests of the Cordillera de Talamanca with similar forests in the Andes, while Islebe and Kappelle (1994) studied similarities between Talamancan and Guatemalan montane forests. A comparison of both studies reveals a higher level of phytogeographic affinity between Costa Rican montane forests and highland forests of the tropical Andes, than between Costa Rican highlands and their equivalents in northern Central America. This is mainly due to two reasons, one of an environmental nature and the other geographic. The first one is that the Guatemalan and Mexican forests receive less rainfall than forests with similar features in Costa Rica and, for example, Colombia; the second is that the Nicaraguan depression and lake basin that separate the mountains of northern Central America (Guatemala) from those in the south (Costa Rica, Panama) act as a barrier to highland species migration between both upland territories (Mexico/ Guatemala vs. Costa Rica/Panama). Around 75% of a total of 253 terrestrial vascular plant genera present in the montane forests of the Cordillera de Talamanca are tropical in distribution (Kappelle et al. 1992). Almost half of these tropical genera are restricted to the Neotropics (46%), with many of them— mostly shrubs and epiphytes— being centered and most diverse in the northern Andes (e.g., Anthurium, Besleria, Burmeistera, Cavendishia, Conostegia, Faramea, Hoffmannia, Philodendron, Phoradendron, and Palicourea) (Kappelle et al. 1992). A smaller number (15%) are pantropical in distribution, including treeferns (Cyatheaceae; see Rojas 1999) and genera belonging to families like Araliaceae, Euphorbiaceae, Lauraceae, Myrsinaceae, and Piperaceae. Ten percent are tropical Asian-American genera and include foremost subcanopy trees such as Cinnamomum, Cleyera, Magnolia, Meliosma, Microtropis, Persea, Styrax, Symplocos, and

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Turpinia. Less common (3%) are genera shared between the American and African tropics (Meliaceae and Urticaceae) (Kappelle et al. 1992). Temperate genera make up almost 18% of the vascular flora and include Holarctic (e.g., Alnus, Quercus, Rhamnus, Vaccinium, and Viburnum), Austral-Antarctic (e.g., Drimys, Escallonia, Fuchsia, Gaiadendron, Gaultheria, Pernettya, and Weinmannia) and wide-temperate genera (e.g., Geranium, Hypericum, Rubus, Salvia, Senecio, and Valeriana). Temperate genera are concentrated in the plant families Asteraceae, Ericaceae, and Rosaceae. Plant genera that can be found everywhere around the world (cosmopolitan genera) are mostly non-woody (e.g., ferns like Asplenium, Blechnum, Dryopteris, Polypodium, and Pteris, and forbs like Gnaphalium, Oxalis, Plantago, Solanum, and Viola) (Kappelle et al. 1992). Holz and Gradstein (2005a) confirm these phytogeographical patterns following a review of floristic affinities of the oak forests’ bryophyte flora. They noted the importance of Andean-centered moss and hepatic species, reflecting the close historical connection between the montane bryophyte floras of Costa Rica and South America. Furthermore, high percentages of Central American endemics in the bryophyte flora of these oak forests suggest the importance of climatic changes associated with Pleistocene glaciations for allopatric speciation (Holz and Gradstein 2005a).

Biodiversity at the Species Level Fungi

The highland forests of the Cordillera de Talamanca are a true storehouse of fungi (Mueller and Mata 2001, Halling and Mueller 2005). Mycological research conducted during the past twenty years has led to a significant increase in our knowledge of mushrooms in these forests, and started with in-depth studies on agarics and boletes by Luis Diego Gómez and Rolf Singer (Halling and Mueller 2005, Mueller et al. 2006). Today, the oak forests of the high Talamancas are considered excellent laboratories for studies on fungi. It is here that mycorrhizal host trees abound (e.g., Quercus, Alnus, and Comarostaphylis; Kappelle 1996). Some species such as Fistulina hepatica are restricted to Quercus (oak) and Alnus (alder) trees (Mueller et al. 2006). Some 22 species of polypore fungi are commonly encountered in Costa Rican oak-dominated forests. The genus Phellinus is richest and represented by at least six species. It is well suited to thrive on decaying oak wood. Other woody or tough macrofungal genera are Ganoderma, Bjerkandera, Coltricia,Coriolopsis, Cyclomyces, Daedalea, Fistulina, Fomes, Fuscocerrena, Laetiporus, Perenniporia, Polyporus,

Tyromyces, and Trametes. Most of the polypore genera occurring in the Talamancan oak forests are cosmopolitan in distribution and seem to have adapted well to strong daily temperature fluctuations, and to high humidity levels throughout the year (Mueller et al. 2006). The Agaricales (mushrooms and boletes) sensu Singer (1986), which include euagaric, bolete, and russuloid clades sensu Monclavo et al. (2002), is the second largest order of Basidiomycetes found in the Talamanca montane forests (Mueller et al. 2006). Greg Mueller and colleagues collected nearly 400 species of Agaricales in these forests, many of which have been identified only at genus level (e.g., Agaricus, Cortinarius, Inocybe, Marasmius sensu lato, Mycena, Psathyrella, and Russula). Roughly half of the 400 agarics are ectomycorrhizal, the other half being putatively saprotrophic. Mueller et al. (2006) estimate that there are perhaps up to 600 agarics that grow in the Talamancan highland forests. Ectomycorrhizal fungal species are a common feature in Costa Rica’s southern highlands. At least forty species occur frequently in the montane oak forests of the Cordillera de Talamanca (Mueller et al. 2006). The most common and diverse genera are Amanita (Fig. 14.4), Boletus, Cantharellus, Hygrocybe, Laccaria, Lactarius, Leccinum, Phylloporus, Russula, and Tylopilus. Many of the species in these genera are considered putative ectomycorrhizal macrofungal endemic to the Neotropical oak forests (Mueller et al. 2006). Less is known about the diversity, distribution, and species composition of saprotrophic fungi. This is mainly due to identification difficulties. Saprotrophic agarics that are most common in the Talamancan highland forests belong to species in genera like Coprinus sensu lato, Crepidotus, Galerina, Gymnopus, Hygropus, Hypholoma, Marasmiellus, Marasmius sensu lato, Mycena sensu lato, Phaeocollybia, Pleurotus, Psathyrella, and Rhodocollybia (Mueller et al. 2006). In another fungal study the diversity of myxomycetes (plasmodial slime molds or myxogastrids; not fungi) was studied in high-elevation oak-dominated forest at 3,100 m near the Cerro de la Muerte Biological Station. In their paper the mycological specialists listed a total of thirtyseven myxomycetic species, including eleven new records for Costa Rica, eight for Central America, and one for the neotropics (Rojas and Stephenson 2007). Lichens

The mountain environment that prevails in the Talamancan oak forests is an ideal home for lichens. Its high precipitation, frequent fog, moderate temperatures, and excellent substrate— slow-growing hardwood oaks— are indeed very

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Fig. 14.4 Fruit bodies of the mushroom Amanita muscaria in the oak forests of San Gerardo de Dota, Costa Rica. Photograph by Carlos Serrano, 2009.

suitable for lichen growth (Sipman 2006). As a result, oaks and other trees often show abundant lichen coverage on the bark of their trunks and branches. As Sipman (2006) states, crown twigs may carry loads of the yellowish, bushy beard lichen (Usnea spp.), whereas older branches are usually covered with whitish patches of leafy lichens belonging to the families Parmeliaceae and Physciaceae, in particular the genera Hypotrachyna, Parmotrema, and Heterodermia. In more shady situations, large individuals of the genera Lobaria and Sticta are conspicuous, and most of the bark not covered by these lichens (or by bryophytes) tends to be covered by greyish crustose lichens (Sipman 2006). In fact, macrolichens constitute a key component of the epiphytic flora of both old-growth and successional oak forests in the Cordillera de Talamanca (Holz 2003). Kappelle and Sipman (1992) presented a first annotated checklist of the lichens that inhabit the old-growth oak forests of the Cordillera de Talamanca. They listed a total of

94 taxa distributed over 66 foliose and 28 fruticose species. The latter become gradually more abundant with increasing elevation, ranging from almost no fruticose lichens at 2,000 m to 50% of all lichen species at 3,400 m altitude. The most species-rich genera were Hypotrachyna (19 species), Cladonia (16), Sticta (10), Lobaria (9), and Usnea (represented by an unknown number of species). Lichen diversity peaks at both 2,500 and 3,200 m elevation. The first altitude corresponds to the transition from lower to upper montane forest, while the second one coincides with the ecotone between upper montane forest and (sub)alpine vegetation. About two-thirds of the Talamancan montane lichens are shared with the highland forests of the Colombian Andes. Lobaria pulmonaria was first reported for Costa Rica by Kappelle and Sipman (1992); the specimens these scholars collected in the Cordillera de Talamanca represent the southernmost distribution of this particular species. More recent research (Holz 2003, Sipman 2006) high-

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lights the importance of dominant genera like the foliose Heterodermia, Hypotrachyna, Leptogium, Parmotrema, and Sticta, and the fruticose Cladonia and Ramalina. Sipman (2006) estimates that the actual epiphytic lichen flora of the neotropical oak forests (Mexico to Colombia) is much larger than the currently known 464 species, and probably close to 1,000 species. This author reports at least 145 species of foliose and fruticose lichens for the montane oak forests of the Cordillera de Talamanca (1,500– 3,500 m). If crustose and foliicolous lichens would be included, the total number of highland lichens in southern Costa Rica could rise considerably (Lücking 1992, Schubert et al. 2003). Plants Trees, Shrubs, Herbs, Ferns, and Vines

Costa Rica’s extraordinary floristic diversity has been the focus of several studies since the beginning of the past century (Wercklé 1909; cf. Gómez and Savage 1983, Gómez 1989). The most important activities carried out by many national and international botanists include the preparation of identification keys and species checklists. With respect to the flora of the montane forests in the Cordillera de Talamanca, specific reference should be made to the works of— in alphabetical order— Alfaro and Gamboa (1999), Blaser (1987), Flores (1990), Gómez (1984, 1986), González (2005), Hartshorn and Poveda (1983), Holdridge et al. (1971), Holz et al. (2002), Kappelle (1987, 1991, 1992, 1995, 1996a, 2001, 2005, 2006b, 2006c, 2008), Kappelle and Horn (2005), Kappelle and Van Omme (1997), Kappelle and Zamora (1995), Kappelle et al. (1989, 1991, 1992, 1994, 1995a, 1995b, 1996, 2000b, 2000c), Oosterhoorn and Kappelle (2000), Orozco (1991), Van Velzen et al. (1993), and Weber (1958, 1959). Oak forests (Quercus spp.)— often with dense Chusquea bamboo stands in the understory— dominate the Talamancan highland vegetation (Kappelle et al. 1989, 1992, Kappelle 1991, 1996). Initial studies report a total of at least 253 terrestrial plant genera in 114 families, distributed over 80 tree genera, 77 shrubs, 44 forbs and grasses, 21 vines, and 31 ferns, commonly seen in these oak forests between 2,000 and 3,200 m elevation (Kappelle et al. 1992). Costa Rica’s Instituto Nacional de Biodiversidad (INBio) reports a total of at least 1,735 plant species in 800+ genera and 200+ families for the Área de Conservación AmistadPacifico (ACLA-P) which includes the national parks of Tapantí– Macizo de la Muerte and Chirripó, as well as the Costa Rican sector of the international park La Amistad, which is shared with Panama (see INBio’s Atta database at www.inbio.ac.cr). These species are spread over some

550 dicot trees, 30 palms, 320+ shrubs, 520 herbs, 170 woody lianas and herbaceous vines, 80 ferns, 10 fern-allies (clubmosses, etc.), 35 epiphytes, and some 20 parasites. If the Talamancan highland sector of the neighboring Área de Conservación Amistad-Caribe (ACLA-C) would be included (e.g., the indigenous reserves Chirripó, Tainy, and Telire, and the Reservas Hitoy Cerere and Barbilla), these numbers should perhaps be multiplied by a factor of 1.5. Kappelle et al. (1991) listed 477 native woody species in 220 genera and 89 families for the highest parts (>2,000 m) of the Cordillera de Talamanca. At lower elevations, in the transition zone from upper montane oak forests down to mixed lower montane and premontane forests in the Amisconde area, Hooftman (1998) recorded a total of 90 genera in 49 plant families in 13,500 m2 plots between 1,150 and 2,300 m altitude. Recent species inventories in the Cordillera de Talamanca estimate that there are at least one thousand species of flowering plants in its montane oak forests, spread over more than 400 genera and at least 140 families (N. Zamora, INBio, pers. comm.). This would include both terrestrial and epiphytic vascular species. On average, each vascular family would be represented by an average of three genera and around seven to eight species. The total of 1,000 vascular species would represent about a ninth of the total vascular flora known from Costa Rica, on the basis of estimates made at the beginning of the twenty-first century (Hammel et al. 2004). However, the total number of vascular plants in the Cordillera de Talamanca is still expected to rise since plant species new to Costa Rica and sometimes new to science are collected, reported, and described every year. This is particularly the case in groups like epiphytic orchids and ferns that blanket the branches of tall canopy trees along the Caribbean slope (Quírico Jiménez, pers. comm., 2010), and in understory shrubs as exemplified by the recent discovery of five new Miconia species by Kriebel and Almeda (2012). If the surveys in the high Talamancas would have included all plant species (that is, flowering and non-flowering vascular species, as well as non-vascular plants like bryophytes) the total number would be over 1,700 species. The great diversity of ferns in the Cordillera de Talamanca, for example, makes up one-third of the known pteridophytic flora in Costa Rica (Lellinger 1989, Alexander Rojas, pers. comm.). Furthermore, 88 out of 188 species of monocots in the mountains of south-eastern Costa Rica are orchids. In the montane oak forests of the Cordillera de Talamanca, the most species-rich woody families are Rubiaceae, Melastomataceae, Lauraceae, Asteraceae, and Ericaceae. They represent about 30% of the total number of recorded species (477) (Kappelle et al. 1991). Several

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woody species are in fact treeferns (Cyatheaceae), and a few are conifers (Gymnospermae: Podocarpaceae: Podocarpus and Prumnopitys). Over 25 correspond to monocots like palms (Geonoma, Chamaedorea, and Prestoea), cyclanths, bamboos (Chusquea spp.), and vines. More than 90% of the 477 species are dicot trees or shrubs. Around 30% of the woody species belong to only five families: Rubiaceae (34 species), Melastomataceae (32), Lauraceae (28), Asteraceae (25), and Ericaceae (25). Other families of major importance are Myrsinaceae (18 species), Araliaceae (17), Solanaceae (16), Poaceae (15), Rosaceae (15), Loranthaceae (14), and Euphorbiaceae (10). The most species-rich genera are Chusquea (15 species), Miconia (14), Ocotea (12), Palicourea (10), Oreopanax (9), Piper (9), Rubus (9), Solanum (9), Ardisia (8), Cavendishia (8), Hypericum (8, but mainly on the upper edges of the oak forests), and Weinmannia (7) (Kappelle and Zamora 1995). When evaluating the distribution of species numbers per family, it turns out there is a large number of speciespoor woody families; really few families are truly speciesrich. Most families (77%) are represented by less than five woody species while only a quarter is present with more than five species. However, this last category comprises twothirds of all woody species. While Fagaceae (Quercus) is the most dominant family in terms of stature, abundance, basal area, and aerial cover, the most diverse woody families that dominate the subcanopy and understory are Lauraceae (Cinnamomum, Nectandra, Ocotea, and Persea), Rubiaceae (Hoffmannia, Palicourea, and Psychotria), Melastomataceae (Miconia and Monochaetum), Asteraceae (Ageratina and Senecio), Ericaceae (Cavendishia, Disterigma, Gaultheria, Macleania, Psammisia, and Vaccinium), Myrsinaceae (Ardisia, Cybianthus, Grammadenia, Myrsine, and Parathesis), Araliaceae (Dendropanax, Oreopanax, and Schefflera) and Solanaceae (Cestrum and Solanum) (Kappelle et al. 1995, 1996). Other frequently observed woody genera are Cecropia, Chusquea, Cordia, Croton, Ficus, Hyptis, Inga, Machaerium, Peperomia, Piper, Psidium, and Vismia (Luis González, pers. comm., 2002). Woody and herbaceous vines (Blakea, Bomarea, Clematis, Dioscorea, Hydrangea, Mikania, Passiflora, Schlegelia, and Smilax) are common at lower altitudes and at mid-elevation, but less frequent in forests above 2,800 m (Kappelle et al. 1995a, Kappelle 1996). Talamanca’s montane forests still contain wild varieties of economically important species, such as the avocado (Persea americana, Lauraceae). Wild individuals of P. americana and its close relative P. schiedeana may abound locally at mid-elevation in these forests. The presence of these and other wild crop relatives (e.g., Phaseolus beans, Solanum

tomatoes, and Vanilla orchids) underscores the importance of conserving in situ the remaining wild genetic reservoirs of agrobiodiversity still found in these highland forests (Smith et al. 1991 and 1992). Finally, according to Chaverri et al. (1997), the Cordillera de Talamanca is one of the four areas with greatest levels of endemism in Costa Rica. Perhaps 30– 40% of the flora is endemic to the region (e.g., see Talamanca-Caribbean Biological Corridor Commission 1993). This is mainly due to the combination of (i) isolated patches of uncommon habitats, (ii) the presence of cloud forests, and (iii) the existence of mountainous areas that are topographically highly dissected (e.g., Gentry 1992). Some examples of vascular plant species endemic to the Área de Conservación Amistad-Pacífico (ACLA-P) are Bursera standleyana, Brunellia costaricensis, Calathea vinosa, Cavendishia talamancensis, Chusquea talamancensis, Conostegia bigibbosa, Dendropanax ravenii, Dichapetalum hammelii, Elaphoglossum adrianae, Eugenia basilaris, Macleania talamancensis, Miconia kappellei, Piper sagittifolium, Prumnopitys standleyi, Roldana scandens, and Solanum longiconicum (see INBio’s Atta database). Vascular Epiphytes

Costa Rica’s montane forests— those in the northern volcanic ranges as well as those in the Cordillera de Talamanca— are characterized by trunks and branches laden with vascular and non-vascular epiphytes that compete with each other for space and light (Lowman and Nadkarni 1995). The abundance of this life form in the tropical montane forest zone is mainly due to an almost continuous presence of clouds and mist (Cavalier et al. 1996, Bruijnzeel and Veneklaas 1998, Bruijnzeel et al. 2010a,b, 2011). Condensation belts, which cause persistently high relative air humidity, supply epiphytes with the water and nutrients they need for their germination, establishment, and growth. In this way, the richness of epiphytes contributes substantially to the overall diversity of tropical highland zones (Henderson et al. 1991, Wolf 1994, Bruijnzeel et al. 2010a,b). Epiphytes occupy a fundamental position in water and nutrient cycles (Nadkarni 1984, 1986, Veneklaas 1990, Hofstede et al. 1993, Tanner et al. 1998, Bruijnzeel et al. 2010a,b). They also inhabit microsites that range from the darkest and wettest places in the understory to the sites most exposed to solar radiation and strong winds in the upper and outer forest canopy (Wolf 1993, 1994). They form mosaics of localized communities that are dominated by particular species that are typical for different microenvironments (Kappelle 2001). During the past decades, more detailed knowledge has

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been generated on the rich epiphyte flora of Costa Rica. Nadkarni (1985) cites more than 120 vascular epiphytes for the Monteverde Cloud Forest Reserve (Cordillera de Tilarán) alone. Many more are expected for the oak forests of the Cordillera de Talamanca. Undoubtedly, the orchids comprise the most diverse group among the epiphytic species present in the Talamancan forests (see Dressler 1993). The genus Epidendrum probably has the greatest diversity of species, accompanied by genera such as Elleanthus, Lepanthes, Maxillaria, Pleurothallis, Scaphyglottis, Stelis, and Telipogon. Another notably diverse monocot family is Bromeliaceae, a strictly Neotropical family (Morales 1998). Tillandsia and Vriesea are particularly characterized by their extraordinary epiphyte diversity. Many species of the genus Vriesea fit the concept of “tank bromeliads,” which accumulate and retain rainwater in a central tank, to sustain themselves during periods of drought (Benzing 1990, Morales 1998). These tanks often house a large fauna of insects and other animals including salamanders (e.g., see the classic study by the Costa Rican scientist Clodomiro Picado Twight [1913]). For Villa Mills (2,800– 3,000 m a.s.l.), a relatively high epiphyte biomass has been calculated (715.16 g/m2 including 49 species), due to the presence of bromeliads of medium and large size, probably belonging to a species of Vriesea, together with shrub species on a 2 m2 area of stems >10 cm DBH and 1 m2 of branches >5 cm thick (Gómez 1986). Köhler et al. (2007) calculated that epiphyte mat weight (epiphyte biomass and canopy humus) at the stand level was 16,215 kg per ha in old-growth montane oak forest near San Gerardo de Dota. Some epiphytic monocots that frequently appear on the branches of Quercus spp. are Tillandsia punctulata and Vriesea orosiensis, in the Bromeliaceae, and Epidendrum platystigma and Maxillaria biolleyi in the Orchidaceae (Kappelle 1996). Araceae are also common, normally represented by (hemi)epiphytes in the genera Anthurium, Monstera, Philodendron, and Syngonium. Less diverse are the Cyclanthaceae (Asplundia and Sphaeradenia), or the Convallariaceae (Maianthemum). Gómez (1986) also mentions Uncinia hamata in the Cyperaceae as a locally important epiphytic monocot. Numerous epiphytic dicot species occur in the Ericaceae: Cavendishia atroviolacea, C. bracteata, Disterigma humboldtii, Macleania rupestris, Psammisia ramiflora, Sphyrospermum cordifolium, and Satyria warszewiczii. The hemiepiphytic genus Clusia sometimes occurs as a terrestrial tree with stilt roots, while at other times it is found as an epiphytic shrub, occupying sites in the higher part of the oak forest (sub)canopy. For its part, the herbaceous genus Peperomia (Piperaceae) has more than 15 epiphytic

species, each restricted to a specific vegetation layer. Other families that are represented by many epiphytic species are Araliaceae (Oreopanax), Asteraceae (Liabum, Senecio), Begoniaceae (Begonia), Campanulaceae (Burmeistera, Centropogon), Gesneriaceae (Alloplectus), Melastomataceae (Blakea, Topobea), Rubiaceae (Hillia, Psychotria, Relbunium), and probably Solanaceae (also, see Benzing 1990). Wagner and Gómez (1983), Lellinger (1989), Kappelle and Gómez (1992), and Mehltreter (1994, 1995) have discussed the presence and abundance of epiphytic and terrestrial pteridophytes in the highlands of the Cordillera de Talamanca. The records of Wagner and Gómez (1983) refer especially to Cerro de la Muerte, which basically includes disturbed páramo vegetation. In his master work on the pteridophyte flora of Costa Rica, Panama, and the Chocó region of Colombia, Lellinger (1989) considered Cerro Chirripó to be a very important site for obtaining knowledge on epiphytic ferns in tropical highland areas. An inventory by Kappelle and Gómez (1992) done at this mountain concluded that the most species-rich epiphytic fern genera at Chirripó are Asplenium, Grammitis, Hymenophyllum, Polypodium sensu lato, and Trichomanes. The genus Vittaria (e.g., V. graminifolia) is frequently observed, but has low levels of diversity. In turn, Elaphoglossum is noteworthy for its incredible wealth of epiphytic ferns (e.g., E. squamipes) as well as terrestrial members (Kappelle et al. 1989, and Alexander Rojas, pers.comm.). The cosmopolitan genus Huperzia— formerly a part of Lycopodium— is a fernally with lots of epiphytic species, commonly found near the forest floor of the oak forests in the high Cordillera de Talamanca. Vascular Parasites

There are also a number of heterotrophic parasites— often epiphytic at the same time— that inhabit these forests— for example, species in the Eremolepidaceae, Loranthaceae, and Viscaceae. A striking example is the shrub Phoradendron tonduzii, which gives a golden color to the crowns of the oaks, such as those found in the valley of San Gerardo de Dota (2,300– 2,900 m). The case of the hemiparasite Gaiadendron punctatum is a particular one, since this species has been observed while infesting other epiphytes without attacking the phorophyte— the host tree that supports the autotrophic as well as the heterotrophic epiphytes (Benzing 1990). Bryophytes

Bryophytes are an important component of Talamancan montane forests in terms of ecosystem functioning, biomass, and biodiversity (Holz et al. 2002). They help minimize soil erosion and occurrence of landslides through their

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sponge effect since they soak up and store water from rain and mist, before releasing it in regular amounts over an extended period of time (Bruijnzeel and Hamilton 2000). Holz et al. (2002) conducted a complete bryophyte inventory of six hectares of oak forest in the Cordillera de Talamanca and identified a total of 206 species: 100 mosses, 105 hepatics, and one hornwort. Tree bases (69 species), rotten logs (70 species), and soil (70 species) are the richest habitats for bryophytes followed by trunks (61 species), branches of the inner canopy (35 species), twigs of the outer canopy (14 species), and leaves in the understory (14 species). Lejeuneaceae (31 species), Plagiochilaceae (13 species), and Lepidoziaceae (nine species) were the most important liverwort families in terms of number of species. Dicranaceae (nine species), Neckeraceae (seven species), Meteoriaceae (seven species), and Orthotrichaceae (seven species) were the most species-rich families among the mosses (Holz et al. 2002). Here, the most speciose and abundant genera of hepatics are Bazzania, Ceratolejeunea, Diplasiolejeunea, Frullania, Herbertus, Heteroscyphus, Lejeunea, Lepidozia, Lophocolea, Plagiochila, Porella, and Radula. Similarly, the most species-rich and common moss genera are Bryum, Campylopus, Dendropogonella, Fissidens, Holomitrium, Hypnum, Leptodontium, Leucobryum, Macromitrium, Meteoridium, Neckera, Pilotrichella, Plagiothecium, Polytrichadelphus, Porotrichum, Prionodon, Pterobryon, Pyrrhobryum, Sematophyllum, Squamidium, Syrrhopodon, Thuidium, and the peat moss Sphagnum. On the basis of similarities in species composition these authors report that bryophyte microhabitats in the studied forests cluster into three main groups: (1) forest floor habitats (including the tree base); (2) phyllosphere (i.e., the leaf environment); and (3) other epiphytic habitats. The distribution of species and life forms in different microhabitats reflects the vertical variation of humidity and light regimes. At the same time they show the impact of the pronounced dry season and the structural characters (tree height, stratification, number of host tree species) of these oak forests on epiphytic bryophytes compared to more humid forests and upper montane forests of lower stature (Holz et al. 2002). The biomass of epiphytic bryophytes growing on small stems (1.8 to 2.8 cm diameter at breast height) of montane Quercus copeyensis trees appears mostly to be made up of mosses (54– 99%), while only 14% of all recorded bryophyte species account for 90% of that “bryomass” (Van Dunné and Kappelle 1998). The most abundant moss and liverwort species that thrive on these small stems are species in the genera Neckera, Pilotrichella (Fig. 14.5), Plagiochila, Porotrichodendron, Prionodon, and Rigodium, which all seem to play a key role in stem flow of understory treelets.

Animals Invertebrates

Very little is known about the invertebrates of the montane forests. Some studies have been conducted on soil invertebrates of cloud forests, such as those of Buskirk and Buskirk (1976), Nadkarni and Longino (1990), and Kappelle (1996, p. 26). The most abundant groups among the Arthropods (insects and spiders) are the Arachnida, Blattarida, Chilopoda, Coleoptera, Dermaptera, Diplopoda, Diplura, Diptera, Hymenoptera, Isopoda, Oligochaeta, Neuroptera, and Orthoptera (Kappelle 1996).Wesselingh et al. (2000) studied pollination by the highland bumblebee (Bombus ephippiatus), one of the most conspicuous insects in the oak woodlands of the Los Santos Forest Reserve. It is hoped that entomologists will increasingly focus their attention on the montane highlands of the Talamanca Mountains as many species new to science are still expected to be revealed in this part of the country. Vertebrates Fishes

The ichthyofauna of the Talamancan mountain rivers between 500 and 1,000 m altitude is not as diverse as in the neighboring Atlantic or Pacific lowlands (Bussing 1998). In fact, above 1,000 m freshwater fish diversity is very limited. More specifically, the Cordillera de Talamanca serves as a barrier to the Central American fish fauna, principally cichlids and poeciliids, which migrated mostly from the great lakes of Nicaragua southward along the broad lowlands of Atlantic Costa Rica (Bussing 1998). At elevations over 2,000 m there aren’t any native fish species that naturally inhabit the streams that traverse the montane oak forests or live in the small lagoons that form in the cores of peat bog areas. Exotic rainbow trout (Oncorhynchus mykiss), however, has been introduced at these altitudes for commercial and recreational purposes (Kappelle 2008). As in the Colombian Andes, its production in artificial ponds has led to important revenues among local small-holders making a living in towns like San Gerardo de Dota, in the western sector of the Cordillera de Talamanca (Kappelle and Juárez 1995, 2000; Fig. 14.6). Amphibians The mountain cloud forests of the Cordillera de Talamanca used to be very rich in amphibians like salamanders, frogs, and toads (Savage 2002). Unfortunately, a skin disease known as chytridiomycosis, first identified in 1998 and caused by a fungus (Batrachochytrium dendrobatidis), has triggered the decline of amphibian populations and ultimately the disappearance of a number of frogs and toads

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Fig. 14.5 Hanging curtains of Pilotrichella flexilis mosses at 2,500 m elevation in the oak forests of San Gerardo de Dota, Costa Rica. Photograph by Carlos Serrano, 2009.

in the Costa Rican mountains (Pounds 2001, Pounds and Crump 1994). Apparently the fungus benefits from modern climate change that includes shifting rainfall patterns in Central America’s mountains (Pounds et al. 2006). Fortunately, populations of some species seem to escape this fate and are doing rather well in the high Talamancas, including the mountain salamander (Bolitoglossa pesrubra, previously known as B. subpalmata), a leptodactilyd quark frog (Eleutherodactylus melanostictus), the mountain tree frog (Hyla picadoi), and the true mountain frog (Rana vibicaria) (Kappelle 2008). The mountain salamander is a small insectivore with moderately webbed hands and feet. Populations prefer boggy sites between 1,500 and 3,500 m elevation. The species is mostly nocturnal and semi-arboreal or terrestrial. Behavioral studies showed that adults tend to hide in tank bromeliads, which often serve as oviposition sites (Vial 1968). The less common leptodactilyd quark frog belongs to the most species-rich vertebrate genus on Earth: Eleutherodactylus has over 500 species (Leenders 2001). It has no toe webs but rather large truncate, emarginated disks on some

of its fingers and toes. This species’ range is between 1,000 and 2,500 m elevation. It is a nocturnal insectivore that serves as prey to many larger vertebrates like bats (Savage 2002). Normally it hides under rocks and logs. The similarly uncommon mountain tree frog (1,900– 2,800 m alt.) is also a nocturnal insectivore, but has clear finger webs (Savage 2002). The more common true mountain frog with its webbed hands and feet, on the contrary, is both insectivorous and carnivorous and preys on arthropods and small mammals (Savage 2002). It prefers dense woods or ponds between 1,500 and 2,700 m, and breeds in shallow ponds or backwaters of very small streams (Kappelle 2008). Reptiles Few studies have focused on the reptiles of Talamanca’s montane forests (Savage and Villa 1986, Savage 2002, Scott and Limerick 1983, Solórzano 2004). What we know is that several dozens of lizards and snakes inhabit these forests. Some common lizards are the green spiny lizard (Sceloporus malachiticus) and the highland alligator lizard (Mesaspis monticola). Snakes that can be frequently observed are

The Montane Cloud Forests of the Cordillera de Talamanca 465

Godman’s montane pit viper (Cerrophidion godmani) and the slender black-speckled palm pit viper (Bothriechis nigroviridis). The green spiny lizard is a small, viviparous insectivore with spine-tipped scales that is preyed upon by birds and snakes (Savage 2002). It takes advantage of solar radiation during the day and is often found on perches such as fence posts, rocks, and dead logs between 600 and 3,800 m. The viviparous highland alligator lizard has yellowish-green or turquoise flecks and lines. It is also active during the day after it warms up by the sunlight. Although it is an insectivore, it may occasionally feed on juvenile Bolitoglossa salamanders. Adults often sit on fallen logs, decaying wood, stumps, loose bark, moss mats, or rocks between 1,800 and 3,800 m altitude (Savage 2002). Godman’s montane pit viper and the black-speckled palm pit viper are both small-sized, viviparous predators that feed on small animals including arthropods, frogs,

Fig. 14.6

lizards, other snakes, small birds, and rodents such as mice. While Godman’s montane pit viper is active during the day and hides on the ground, in low vegetation or near logs, the palm pit viper is mostly arboreal and active during the night. Both species live in the forests between 1,400 and 3,000 m (Savage 2002, Solórzano 2004, Kappelle 2008). Birds The diverse avifauna of the mountain forests of the Cordillera de Talamanca has been the subject of several studies (Stiles et al. 1989, Wilms and Kappelle 2006, Gomes et al. 2008). Results show that Talamanca’s premontane, lower montane, montane and sub-alpine forests are among the richest bird habitats in the country (Stiles et al. 1989). It is believed that at least 560 species of bird live in, or occasionally visit, the forests of the Parque Nacional Chirripó and the Costa Rican sector of Parque Internacional La Amistad (Boza 1984). For example, Chirripó’s montane oak forests

Local villager in San Gerardo de Dota showing a few introduced rainbow trout he has grown in his ponds for commercial purposes.

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serve as key habitat for common species like the band-tailed pigeon (Columba fasciata), the collared redstart (Myioborus torquatus), the flame-throated warbler (Parula gutturalis), the buffy tufted-cheek (Pseudocolaptes lawrencii), and mountain thrush (Turdus plebejus) (Stiles et al. 1989). Some large but now less common birds still living here are the great curassow (Crax rubra), the crested guan (Penelope purpurascens), and the great tinamou (Tinamus major) (Tavares de Almeida 2000). Similarly, Sánchez (2002) estimated at least 415 bird species in the Parque Nacional Tapantí– Macizo de la Muerte alone. An inventory by J. Wilms (2010, pers. comm.) in the upper montane oak forests (2,300– 3,100 m alt.) along the Río Savegre near San Gerardo de Dota, revealed a total of 75 bird species. The most common families were Emberizidae, Parulidae, Thraupidae, Trochilidae, Turdidae, and Tyrannidae, which together account for slightly over 50% of all species recorded. Around 8.0% of the 75 species were obligate frugivores, while obligate insectivores accounted for 29.3%, obligate carnivores 4.0%, and obligate nectarivores 1.3% of all species. Of the 75 species, 11.7% were abundant, while 37.7% were common, 25.3% uncommon, and 25.3% rare. A number of raptors are fairly common in the Talamancan montane forests. For instance, the migratory large-sized American swallow-tailed kite (Elanoides forficatus) arrives in December in the highlands of southeastern Costa Rica, where it feeds on lizards, snakes, nestling birds, and large insects (Kappelle 2008). It nests in tall forest trees or in isolated trees in pastures. Another bird of prey is the red-tailed hawk (Buteo jamaicensis), which consumes a wide variety of species, feeding primarily on rodents, snakes, birds, insects, amphibians, and fish. Sillett (1994) evaluated the foraging ecology and diet of eight species of epiphyte-searching insectivorous birds in the Cordillera de Talamanca near Villa Mills (2,800– 3,100 m) to determine the degree of epiphyte specialization. Four species (approximately 8% of the resident avifauna) turned out to be epiphyte specialists: the buffy tufted-cheek (Pseudocolaptes lawrencii) on arboreal bromeliads, the ruddy treerunner (Margarornis rubiginosus) on bryophytes, the spot-crowned woodcreeper (Lepidocolaptes affinis) on bryophytes and foliose lichens, and the ochraceous wren (Troglodytes ochraceus) on epiphytic root masses. The spectacular and majestic resplendent quetzal (Pharomachrus mocinno costaricensis) is part of an ecological guild of altitudinal migrants (Powell and Bjork 1994) that includes animals that move along continuous forest corridors that stretch over elevational gradients on tropical mountains. Their population viability is often negatively affected by habitat loss and fragmentation (Chaves 2001).

A few examples of fruit-eating and seed-dispersing birds that thrive in Talamancan montane old-growth oak forests are the acorn woodpecker (Melanerpes formicivorus), black guan (Chamaepetes unicolor), black-faced solitaire (Myadestes melanops), black thighed grosbeak (Pheucticus tibialis), brown-capped vireo (Vireo leucophrys), collared trogon (Trogon collaris), emerald toucanet (Aulacorhynchus prasinus), large-footed finch (Pezopetes capitalis), resplendent quetzal (Pharomachrus mocinno costaricensis), ruddy-capped nightingale-thrush (Catharus frantzii), silvery-throated jay (Cyanolyca argentigula), yellow-billed cacique (Amblycercus holosericeus), and yellow-thighed finch (Pselliphorus tibialis) (Stiles et al. 1989, Wilms and Kappelle 2006). The essential relation between these frugivorous, seed-dispersing birds and the plants they feed on is discussed later in this chapter. Mammals Mammals that inhabit the montane cloud forests of the Cordillera de Talamanca have been the subject of very few studies. Most past research has focused on small terrestrial rodents (Lanzewizki 1991, Johnson and Vaughan 1993, Van den Bergh and Kappelle 1998, 2006), tapirs (Tobler 2002, Tobler et al. 2006, González-Maya et al. 2009), and jaguars (Tavares de Almeida 2000), next to observational studies on general mammal presence at specific sites such as along the Savegre River (Mooring et al. 2010). The montane forests of the Parque Nacional Chirripó and Parque Internacional La Amistad are extremely rich in mammals: at least 70 species of mammals are known to live in these forests, including thirty-one rodents, eleven bats, and nine carnivores (Boza 1984, Arias 2001). Similarly, at least 45 mammal species inhabit the forests of the Parque Nacional Tapantí– Macizo de la Muerte and the Zona Protectora Río Navarro y Río Sombrero (Mora Carpio 2000). The most conspicuous non-volant, non-carnivorous mammals observed in these mountain oak forests are the omnivorous white-faced capuchin monkey (Cebus capucinus), which reaches elevations of 2,500 m; the common small red-tailed squirrel (Sciurus granatensis); rats and mice like Heteromys desmarestianus, Oryzomys albigularis, Peromyscus mexicanus, Reithrodontomys creper, Scotinomys xerampelinus, and Tylomys watsoni; the herbivorous prehensile-tailed Mexican hairy porcupine (Sphiggurus mexicanus); the small herbivorous Dice’s cottontail rabbit (Sylvilagus dicei, endemic to Costa Rica and Panama; Carrillo et al. 1999); the widespread coyote (Canis latrans); the slender gray fox (Urocyon cinereoargenteus); and the common northern raccoon (Procyon lotor) and white-nosed coati (Nasua narica), also a member of the raccoons. Mammals that really abound in Talamancan montane

The Montane Cloud Forests of the Cordillera de Talamanca 467

oak forests are rats and mice (Muridae and Heteromyidae)— especially in years following mast seeding in oaks (Van den Bergh and Kappelle 1998). In the Talamancan oak forests Peromyscus mexicanus and Scotinomys xerampelinus are four to five times more common than other species of Muridae. Some of these myomorph species prefer closed, mature oak forest (e.g., Heteromys and Oryzomys), whereas others are more abundant in open, shrubby, or grassy habitats like abandoned pastures (e.g., Reithrodontomys). The population density of rats and mice is normally highest in habitats with intermediate levels of disturbance, stressing the importance of within-habitat microenvironmental heterogeneity for populations of small rodents ( Johnson and Vaughan 1993, Van den Bergh and Kappelle 1998, 2006). Carnivorous mammals that roam this habitat include the long-tailed weasel (Mustela frenata), the tayra or tolomuco (Eira barbara), the spotted skunk (Spilogale putorius), the striped hog-nosed skunk (Conepatus semistriatus), and wild cats like the ocelot (Leopardus pardalis), the margay (Leopardus wiedii), the cougar or mountain lion (Puma concolor), and the jaguar (Panthera onca). Other common species are the omnivorous collared peccary (Pecari tajacu) and the herbivorous red brocket deer (Mazama americana) (Carrillo et al. 1999, Kappelle 2008, Mooring et al. 2010). Because of the cold temperatures bat species become rarer at higher elevations in the montane forests of the Cordillera de Talamanca. However, the highland yellow-shouldered bat (Sturnira ludovici; IUCN Red List category “Least Concern”) has been observed at elevations of 2,000 m in San Gerardo de Dota (David Hille, pers. comm., 2010). The jaguar is still abundant in the Cordillera de Talamanca and can be observed with quite some luck— particularly during the rainy season— in the inner sectors of the Lower Montane Rainforests (sensu Holdridge et al. 1971) of Tapantí-Macizo de la Muerte and Chirripó national parks, as well as in Parque Internacional La Amistad and Zona Protectora Las Tablas (Tavares de Almeida 2000). In these highlands jaguars prey on red brocket deer, collared peccary (Tayassu tajacu), two- and three-toed sloths (Choloepus hoffmanni and Bradypus variegatus), nine-banded armadillo (Dasypus novemcinctus), paca (Agouti paca), and Central American agouti (Dasyprocta punctata). However, they are also known to occasionally cross the forest edge and roam into neighboring pastures where they attack domestic animals like horses, cows, and goats (Tavares de Almeida 2000). The largest mammal that lives in the Talamancan montane oak forests is undoubtfully the endangered Baird’s tapir (Tapirus bairdii) (Naranjo and Vaughan 2000, GonzálezMaya et al. 2009). It prefers undisturbed oak forests over disturbed patches impacted by human activity. In the Cor-

dillera de Talamanca its relative abundance in intact areas is twice as high as in altered forest landscapes (Tobler et al. 2006). Analysis of feces demonstrates the importance of the leaf and stem components in the plant material consumed by tapirs, whereas fruits contribute to less than 10% of its diet. In Costa Rica, remains of oak (Quercus costaricensis) were frequently encountered in tapir fecal samples. Following habitat loss, hunting appears to be the second most important threat to remaining tapir populations in the Cordillera de Talamanca (Tobler et al. 2006).

Biodiversity at the Community and Ecosystem Level Vegetation Zonation

According to the ecological map of Costa Rica’s life zones (Tosi 1969), Gómez’s vegetation studies and cartography (1986; Herrera and Gómez 1993), and the detailed plant zonation studies by Kappelle (1991; Kappelle et al. 1989, 1995b), the Talamanca mountains harbor six altitudinally zoned vegetation belts (elevational formations). From the Pacific and Atlantic coast lines up to the highest mountain peaks of the cordillera (Kappelle 1996), these zones are: a) The tropical moist forest or basal rain forest, with transition to the premontane zone (0– 500 m a.s.l.); b) The tropical premontane moist, rain, or cloud forest (500– 1,500 m a.s.l.); c) The tropical lower montane cloud/rain forest, dominated by Quercus and Lauraceae (1,500– 2,400 m a.s.l.) with many dwarf palms in the understory; d) The tropical upper montane cloud/rain forest, dominated by Quercus (oak) and Myrsinaceae with lots of bamboos (Chusquea) in the understory (2,500– 3,100 m a.s.l.); e) The sub-alpine tropical rain/elfin cloud forest (3,100– 3,300 m a.s.l.), dominated by, for example, Buddleja, Escallonia, and Ericaceae like Comarostaphylis; f) The tropical rain páramo (herbaceous or shrubby) or alpine cloud páramo, dominated by Asteraceae and Poaceae (3,300– 3,819 m a.s.l.). This chapter discusses three of these vegetation zones (b, c, and d), from the lower boundary of the premontane forests at 500 m up to the upper limit of the upper montane oak forests at ca. 3,100 m. The lowland forests of the adjacent coastal zones are dealt with elsewhere in this volume (Pacific lowlands: Gilbert et al., chapter 12 of this volume; Atlantic lowlands: McClearn et al., chapter 16 of this volume). Details on biodiversity zones observed in Parque International La Amistad are discussed by Monro et al. (2009).

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In general, the Talamancan highland forests along the Atlantic slopes have a different structure and composition than the forests that cover the Pacific hillsides (Kappelle 1992; and see Lawton 1980 and chapter 13 of this volume, for similar features at Monteverde in northern Costa Rica). These differences result from the forests’ exposure to Caribbean trade winds, which create a greater atmospheric moisture level (rain, fog) on the Atlantic slopes (Coen 1983; Herrera, chapter 2 of this volume). In a comparison of two forest communities— one occurring on the Atlantic slope and another one on the Pacific slope of the Cordillera de Talamanca— Kappelle (1992) observed the following differences in structure. In the first place, the stature of the Atlantic Quercus costaricensis– Ilex lamprophylla cloud forest community was almost twice as tall as the Pacific Quercus costaricensis– Comarostaphylis arbutoides community. This latter forest had a much more compacted aspect with trees displaying crooked, gnarled trunks. At the same time, the forests of the Pacific slope were denser and richer in thinly stemmed species and shrubs with coriaceous leaves. For their part, the forests of the Atlantic community had lower tree densities but greater tree diameters at breast height. They also contained many hygrophytic species, including ferns. Morales et al. (2007) evaluated mid-elevation (800– 1,500 m.) forest zonation of Parque Internacional La Amistad (PILA) using Al Gentry’s transect method. They sampled ten forest sites— some disturbed and some intact— at 800, 900, 1100, 1300, and 1500 m elevation. Comparisons were made for plant families and genera observed along the elevational gradient, including commercial species. They recorded 2,257 individuals in 235 species and 69 families. Melastomataceae (69 species), Annonaceae (22), Rubiaceae (18), and Arecaceae (palms; 14) were the most species-rich families at 900 m. Next to these families, Cyatheaceae (treeferns) and Celastraceae become abundant around 1,100 m. Even higher, around 1,300 m Chloranthaceae, Euphorbiaceae, Lauraceae, and Clusiaceae are very well represented, while Rubiaceae still abound as well. At an altitude of 1,500 m the most abundant families are Lauraceae (33 species), Rubiaceae (28), Meliaceae (15), Myrsinaceae (14), Moraceae (12), Euphorbiaceae (11), and Monimiaceae (10). A similar study of floristic changes along an elevational gradient (0– 3,491 m) was conducted by Estrada and Zamora (2004) in the Río Savegre watershed. They recorded 2,152 plant species on the basis of existing herbarium collections and complementary fieldwork. The highest plant species richness values were observed between 500 and 2,000 m altitude, while diversity declined continuously

from 2,000 m up to the summit at 3,491 m (Cerro Buenavista). The most diverse plant families were Asteraceae (133 species), Rubiaceae (123), Orchidaceae and Melastomataceae (93 each), while the richest genera were Piper (38 species), Elaphoglossum (36), Miconia (35), and Peperomia (35), respectively. Five species turned out to be endemic to the 590 km2 sized Río Savegre watershed area (Estrada and Zamora 2004). An analysis of the altitudinal zonation of montane Quercus forests along an Atlantic and Pacific transect between 2,000 and 3,200 m in the Chirripó National Park, revealed similarly interesting elevational changes in woody species richness (Kappelle and Zamora 1995). Out of 477 woody species in 223 genera and 90 families, Rubiaceae, Lauraceae, Melastomataceae, and Myrsinaceae abounded in lower montane forests (2,000– 2,300 m) while Ericaceae, Rosaceae, Poaceae, and Asteraceae dominated species diversity in upper montane forests (2,400– 3,200 m). Most diverse genera along this elevational range were Chusquea (16 species), Miconia (13), Ocotea (12), Palicourea (10), Oreopanax (9), Piper (9), Rubus (9), and Solanum (9). In general, woody species diversity declined with increasing altitude (Kappelle and Zamora 1995). Plant Communities

The floristic composition of undisturbed and successional Talamancan montane plant communities in Costa Rica is relatively well known (Weber 1958, Holdridge et al. 1971, Blaser 1987, Kappelle et al. 1989, 1994, 1995b, Orozco 1991, Kappelle and Van Omme 1997, Hooftman 1998, Morales et al. 2007). For instance, the community data analysis of vascular plant species censuses conducted by Kappelle et al. (1995b) in 1,000 m2 (20 × 50 m) plots (excluding epiphytes) at 100 m altitudinal intervals along Chirripó’s 2,000– 3,200 m elevational range showed the presence of at least eight different plant communities grouped into two sets: a set of palmrich, lauraceous-fagaceous, Lower Montane Mollinedia– Quercus Forests (2,000– 2,600 m), and a set of bamboo-rich (3 to 6 m tall Chusquea) myrsinaceous-fagaceous Upper Montane Schefflera– Quercus Forests (2,500– 3,200 m). Here, altitudinal vegetation changes are mostly correlated with temperature changes, and, to a lesser extent, with rainfall differences. On the whole, Chirripó’s Atlantic forests are much wetter with soaked, humus-rich topsoils, as a result of the strong trade winds (see above). In this study, Kappelle et al. (1995b) reported at least 431 vascular plant species spread over 296 dicots, 48 monocots, 86 ferns and fern-allies, and one gymnosperm (a native podocarp). In

The Montane Cloud Forests of the Cordillera de Talamanca 469

terms of structure, canopy height and average stem diameter decreased with increasing altitude, while the canopy surface became more flatted at higher elevations. Further north, in the Los Santos Forest Reserve and Tapantí– Macizo de la Muerte National Park, six Quercus forest communities were identified. Descending from 3,000 down to ca. 2,000 m in valleys like those of the Savegre river, alternating forest communities dominated by the following species can be observed: (a) Myrsine pittieri and Quercus costaricensis; (b) Quercus costaricensis and Q. copeyensis; (c) Geonoma hoffmanniana and Quercus copeyensis; (d) Quercus seemannii and Q. copeyensis; (e) Quercus guglielmi-treleasei and Symplocos austinsmithii; and (f) Quercus seemannii and Miconia lauriformis (Kappelle et al. 1989). In general, 35 to 60 m tall montane oak forest communities are characterized by up to five different structural layers. Their canopies are normally dominated by one or two species in the genus Quercus (Kappelle et al. 1989, 1995b) including Q. costaricensis, Q. copeyensis, Q. seemannii, Q. rapurahuensis, Q. guglielmi-treleasei, and Q. oocarpa. Old-growth oaks may locally reach significant heights and diameters. A good example is the 40 m tall Q. copeyensis tree (with an circumference of 11 m!) observed at San Gerardo de Dota, that received the 2010 Annual Award for Most Exceptional Tree (Vargas 2010; and see Fig. 14.7 for a similarly tall individual of Q. copeyensis in the same area). These oaks are often associated with tree species such as Alfaroa costaricensis, Cinnamomum spp., Clethra gelida, Drimys granadensis, Eugenia spp., Ilex pallida, Guarea tonduzii, Guatteria oliviformis, Ladenbergia brenesii, Lozania mutisiana, Magnolia poasana, M. sororum, Meliosma glabrata, Miconia spp., Microtropis occidentalis, Myrcia oerstediana, Myrcianthes storkii, Myrsine pittieri, Nectandra spp., Ocotea spp., Persea vesticula, Rhamnus oreodendron, Rhus striata, Rondeletia amoena, R. buddleoides, Roupala montana, Schefflera rodriguesiana, Solanum storkii, Symplocos austin-smithii, Trichilia havanensis, Weinmannia pinnata, Xylosma intermedia, and Podocarpaceae (native conifers) such as Prumnopitys standleyi and Podocarpus macrostachyus. The tree Clusia is present as a terrestrial and epiphytic element with stilt roots. The sub-canopy includes trees such as Ardisia spp., Cornus disciflora, Dendropanax querceti, Drimys granadensis, Ilex lamprophylla, Miconia pittieri, Myrsine coriacea, Oreopanax spp., Prunus annularis, Saurauia veraguasensis, Styrax argenteus, Vaccinium consanguineum, Viburnum costaricanum, Weinmannia trianae, Zanthoxylum limoncello, and Z. melanostictum. Different species of bamboo in the genus Chusquea, the palms

Geonoma and Chamaedorea, and several treeferns (Cyatheaceae; Rojas 1999) occupy the rich understory, in combination with shrubs such as Fuchsia, Miconia, Palicourea, Psychotria, and Piper. On the ground, an herbaceous stratum occurs, comprised of many ferns, Anthurium, Acanthaceae, Asteraceae, Bromeliaceae, Campanulaceae, Commelinaceae, Ericaceae, Gesneriaceae, Maianthemum, and Urticaceae. The quantity of vascular epiphytes (Bromeliaceae, Cyclanthaceae, Ericaceae [Cavendishia, Macleania, Psammisia], Orchidaceae, Peperomia, and the parasitic plants of the Loranthaceae) and non-vascular epiphytes (mosses, liverworts and lichens) is spectacular. There are large numbers of commercially important non-vascular epiphytes in the forests of the Cordillera de Talamanca, such as Dendropogonella rufescens, Pilotrichella flexilis (Fig. 14.5), and Phyllogonium viscosum (Romero 1999). The woody vines (lianas) include mainly species from the genera Bomarea, Cissus, Dioscorea, Hydrangea, Muehlenbeckia, Passiflora, and Smilax.

Species Interactions Flowering and Flower Pollination

Montane oak forest subcanopy and shrub layers are often composed of Chusquea bamboos, which flower once every 30 to 35 years (Pohl 1991, Widmer 1998). A reported massive flowering of Chusquea tomentosa occurred between 1988 and 1992 (Pohl 1991, Widmer and Clark 1991) and resulted in a subsequent, massive germination of seeds on a variety of substrates including leaf litter, mosses, and trunks (Grau and Rivera-Ospina, 1996). According to Widmer (1993, 1994) and Edwards-Widmer (1999), the predominance of Chusquea tomentosa and C. talamancensis in the understory of oak forests may eventually have a negative influence on the regeneration of Quercus costaricensis. In the high Talamancas, nectarivorous hummingbirds like Colibri thalassinus, Doryfera ludoviciae, and Panterpe insignis are abundant and essential flower pollinators for a huge number of ornithophilous herbs and shrubs in a variety of genera such as Bomarea, Cavendishia, Centropogon, Fuchsia, Macleania, and Palicourea (Kappelle 2008). Many other plant species, particularly shrubs, are pollinated by insects such as the highland bumblebee, Bombus ephippiatus, a common pollinator in the Cordillera de Talamanca (Wesselingh et al. 2000). In a study on reproduction and pollination of eight shrub species in the Cordillera de Talamanca, Wesselingh and collaborators (Wesselingh 1998, Wesselingh et al. 1999) observed a low reproductive investment in the species,

Fig. 14.7 Tall Quercus copeyensis (white oak) tree at 2,700 m elevation at San Gerardo de Dota, Costa Rica. The upper branches are partly covered by epiphytic bromeliads. Photograph by Maarten Kappelle, 2007.

The Montane Cloud Forests of the Cordillera de Talamanca 471

combining low or moderate reproductive success and a high rate of seed herbivory with factors that cause low production of viable seeds in these woody species. Average flower lifespan for these understory species is 4.4 days, in comparison with longer flower lifespan in arctic and alpine species (Wesselingh et al. 1999). Herbivory, Frugivory, Seed Predation, and Dispersal

Holl and Lulow (1997) studied the effect of the species, type of habitat (open pasture, forest, and beneath isolated trees in pasture), and distance to the forest edge on seed depredation of 10 animal-dispersed species in the southeastern part of the Cordillera de Talamanca, near Las Alturas Biological Station. Additionally, they compared depredation caused by vertebrates and insects and noted that rabbits cut the stems of 64% of the seedlings of four native species that were planted in an abandoned pasture at 1,500 m altitude (Holl and Quirós-Nietzen 1999). Observations by Holl and Lulow (1997) showed that only 26% of the seedlings had survived two years after having been planted. Moreover, the number of seeds dispersed by animals is normally much greater below branches than in open areas such as pastures, Holl states. These results suggest that seed depredation influences regeneration of the montane forest on degraded lands, although the lack of seed dispersal is apparently the most important limiting factor in their recovery (Holl 1998, and 1999). Another study in southern Costa Rica demonstrated that tropical montane tree seeds survive through germination more often in secondary forests, with high levels of mortality occurring in abandoned pastures and forest fragments (Cole 2009). The same study highlights that the majority of seed mortality results from rodent predation in forest fragments, insects and fungal pathogens in secondary forests, and a combination of desiccation, insects, and fungal pathogens in pastures. Plant seeds of Talamancan montane forest trees and shrubs are often dispersed by animals, a species interaction known as zoochory (Wijtzes 1990, Ten Hoopen and Kappelle 2006). Certainly, a large percentage of tropical forest bird species consumes fruits and seeds as part of their diet (Stiles 1985). Probably, frugivorous birds are the most important group of seed dispersers in Talamancan high-elevation oak forests, taking into account the low abundance of monkeys and bats at cool and cold elevations (Kappelle 1996, Wilms and Kappelle 2006, Gomes et al. 2008), although some white-faced capuchin monkeys (Cebus capucinus) have recently been observed at 2,800 m in the Parque Nacional Los Quetzales (Arsenio Agüero, MINAE, pers. comm., 2010). Now, regarding birds, obligate frugivores may represent around or over 10% of the

whole avifauna thriving in these highland forests (Wilms and Kappelle 2006). During field work in 2001– 2002 García-Rojas (2006) evaluated the diet and habitat preference of the frugivorous resplendent quetzal in montane oak-dominated forests between 1,100 and 3,060 m in the Los Santos Forest Reserve. The diet of this subspecies of quetzal includes at least 25 species of fruit trees, thirteen of which are Lauraceae (wild avocados or “aguacatillos”). Other key diet tree species for the quetzal are Cornus disciflora and Symplocos serrulata. García-Rojas hypothesized that a positive relationship would exist between quetzal abundance and the availability and abundance of potential food sources. His field results showed that the largest number of quetzals occurred in Lower Montane Wet Forest (33 individuals) followed by Montane Rain Forest (22). Premontane Wet and Rain Forests had the lowest levels of quetzal abundance (5 and 0, respectively). Census data indicated that quetzals span a large altitudinal gradient but concentrate between 2,000 and 3,000 m elevation— the altitude at which wild avocado trees predominate. Quetzal abundance is highest in Montane Rain Forests during the middle of the dry season (February) and highest in Premontane Forests at the end of the dry season (April). This observation led García-Rojas (2006) to the conclusion that quetzals migrate altitudinally to lower elevations as the dry season advances— a pattern that seems to correlate well with a change in food abundance during the fruiting season (e.g., the ripening of wild avocados) that occurs along the altitudinal gradient as a result of phenological differences among altitudinally restricted tree species (García-Rojas 2006). Next to the resplendant quetzal, dozens of other frugivorous birds play a key role in the dispersal of seeds of an infinite number of ornithochorous trees and shrub genera: Aiouea, Ardisia, Beilschmiedia, Billia, Buddleja, Cinnamomum (= Phoebe), Citharexylum, Cleyera, Conostegia, Cornus, Croton, Ficus, Freziera, Fuchsia, Guatteria, Guettarda, Ilex, Miconia, Monnina, Myrica, Nectandra, Ocotea, Palicourea, Persea, Sapium, Solanum, Symplocos, Vaccinium, and Viburnum (Wilms and Kappelle 2006). Small to medium-sized bird species forage mainly on fruits of fast-growing, light-dependent trees, whereas medium- to large-sized birds prefer the fruits and seeds of slow-growing, mature forest tree species. Tree species like Ilex pallida, Freziera candicans, Fuchsia paniculata, Nectandra cufodontisii, Viburnum costaricanum, and Sapium pachystachys are of particular importance since their fruits are consumed by multiple bird species (Wilms and Kappelle 2006; Fig. 14.8). These are the kind of trees that are of special interest to forest restoration

472 Chapter 14 Fig. 14.8 Number of bird species per diet plant species for a total of twenty frugivorous birds that feed on twenty-two trees and shrubs. A distinction has been made for bird species with preferences for either open or closed forest, and for those without any specific habitat preference. Reproduced from Wilms and Kappelle 2006, with kind permission from Springer.

Fig. 14.9 Resplendent quetzals at San Gerardo de Dota, Costa Rica. Left: Flying towards a native Ocotea pittieri tree with small, ripe avocado fruits; right: Male sitting on a branch in the montane oak forest. Photographs by Carlos Serrano, 2009.

initiatives and organizations, as they attract lots of frugivorous birds and can help speed up recovery of impoverished forest stands and open areas (Gomes et al. 2008, Reid et al. 2014). Trees of Ocotea pittieri and O. pharomachrosorum, for instance, have been observed with lots of resplendent quetzals sitting on their branches and foraging on wild

avocados (Fig. 14.9). This wildlife spectacle has been the reason for naming it the “quetzal-bearing” laurel tree or “pharomachrosorum” in Latin. Small rodents like mice (e.g., Peromyscus spp.) and squirrels (Sciurus granatensis) are also considered key seed predators and dispersers in the forests of the Cordillera de

The Montane Cloud Forests of the Cordillera de Talamanca 473

Talamanca. They prefer the acorns (seeds) of tropical montane Quercus trees (Van den Bergh and Kappelle 1998 and 2006, and Kappelle 2006d, 2008). The huge amounts of acorns available during mast seeding years of mature oak forest stands may considerably affect the size of local rodent populations, as has been demonstrated by studies in the highlands of Chiapas, Mexico (López-Barrera and Manson 2006). As in temperate oak forest, acorns are also fed on and dispersed by jays, which seem to have developed a symbiotic relationship with oaks. In the Talamancan montane oak forests this may be the case for the omnivorous silverythroated jay, Cyanolyca argentigula, which feeds on acorns and fruits of Ericaceae and Melastomataceae, as well as on frogs, salamanders, lizards, and insects (Kappelle 2008). Like birds, mammals are important dispersers of seeds in montane forests of the Cordillera de Talamanca. For instance, the white-faced capuchin monkey (Cebus capucinus) is known to consume and distribute seeds of a number of Miconia and Trichilia trees (Kappelle 2008). Similarly, Baird’s tapir (Tapirus bairdii) disperses seeds of numerous species, which are ingested wholly and dropped as intact seeds (Tobler et al. 2006).

Ecosystem Functioning and Dynamics Ecosystem Structures

eral. Additionally, in a 1,000 m2 oak forest plot at 2,950 m near Jaboncillo de Dota just north of San Gerardo de Dota, Kappelle et al. (1996) calculated a density of 1,820 to 1,970 stems per ha for stems ≥3 cm DBH, while the average basal area for this size class reached almost 65 m2 per ha. The architecture of an oak forest at 3,050 m at Cerro Las Vueltas was studied by Van Leeuwen (1988), who applied Oldeman’s theory of “silvigenesis” to understand spatial and temporal dynamics (Oldeman 1983). Van Leeuwen (1988) observed a mosaic of two dynamic phase sequences (“chronounits”): (i) one dominated by light-loving species (Monnina crepinii and Chusquea spp.) in gaps larger than 500 m2; and (ii) the other dominated by Quercus costaricensis (domination phase or equilibrium phase). Van Leeuwen concluded that Chusquea appears to have had a negative influence on the regeneration of Quercus costaricensis. In a parallel study on Chusquea in the Villa Mills area, Edwards-Widmer (1999) collected data on the size distribution of trees, which also showed an inhibitory effect of bamboo on tree growth in clearings. Certainly, Lawton (1990) emphasized the fact that variability in the light regime (gaps in the canopy vs. closed canopies) is an integral part of disturbance and recovery in montane forests, such as those in Monteverde (see Lawton et al., chapter 13 of this volume), and apparently plays a predominant role in the evolution of tree growth strategies.

Forest Structure

Leaf Characteristics

Many authors have studied the structure of montane oak forests in the Cordillera de Talamanca (e.g., Blaser 1987, Jiménez et al. 1988, Van Leeuwen 1988, Berner 1992, and Kappelle et al. 1996). For instance, in a one-hectare plot of Quercus costaricensis– Q. copeyensis forest at 2,700 m near Villa Mills, Blaser (1987) calculated 5,049 stems ≥1 cm diameter at breast height (DBH), 998 stems ≥5 cm DBH, and 512 stems ≥10 cm DBH. In a pure Quercus copeyensis dominated forest, this author calculated 8,418 stems ≥1 cm DBH, 695 stems ≥5 cm DBH, and 455 stems ≥10 cm DBH (Blaser 1987). At the same time, the basal area for both forests was 50 to 53 m2 per ha for stems ≥1 cm DBH, 48 to 52 m2 per ha for stems ≥10 cm DBH, and 32 to 37 m2 per ha for stems ≥50 cm DBH. Jiménez et al. (1988) found similar numbers for a Q. copeyensis– dominated oak forest at 2,650 m at San Gerardo de Dota (500 stems ≥10 cm DBH per ha), while 80% of the stems and 95% of the total basal area per ha was comprised of oaks. The thickest trees had DBH values of up to 120 cm. On the basis of Jiménez et al. (1988), Helmer and Brown (2000) calculated an aboveground biomass of 388 Mg per ha, which represents a relatively high number for tropical forests in gen-

Leaves in an undisturbed primary oak forest are generally simple, with elliptical shapes and entire leaf margins, pinnate venation, and mucronate or caudate apices— in other words, leaves with “drip tips” and attenuated bases (Leal and Kappelle 1994, Kappelle and Leal 1996). Serrate and dentate leaves are less frequent. Only species such as Oreopanax capitatus and O. nubigenus have true palmate venation. Few species of the montane oak cloud forests have compound or lobulate leaves, in comparison to those of the moist and dry forests of the tropical lowlands. The absence of trees from the family Fabaceae (Leguminosae) at higher elevations is one of the main reasons for the scarcity of species with compound leaves (Holdridge and Poveda 1975). Common tree genera with compound leaves in the highland oak forests are Oreopanax, Schefflera, Weinmannia, and Zanthoxylum. Less common but still often observed tree genera with compound or lobulate leaves are Alfaroa, Billia, Bocconia, Brunellia, Cecropia, Dendropanax, Guarea, Mauria, Prestoea, Rhus, Roupala, Trichilia, and Turpinia. Leaf measurements show an average leaf size of 57.8 cm2 for montane cloud forest species (Leal and Kappelle 1994, Kappelle and Leal 1996). According to the surface size

474 Chapter 14

Fig. 14.10 Schematic lateral profile of three successional stages of tropical montane oak forest at around 2,800 m elevation in the Cordillera de Talamanca. (a) 10-year-old, early successional forest; (b) 32-year-old successional forest; and (c) old-growth oak forest over 250 years of age. Reproduced from Kappelle 2004, with kind permission from Elsevier.

system for leaf blades developed by Raunkiaer and modified by Webb (1959), notophyll and microphyll leaves dominate the foliar spectrum in these oak forests: out of a total of 23 species, 4.3% were nanophylls (0.25– 2.25 cm2), 26.1% microphylls (2.25– 20.25 cm2), 47.8% notophylls (20.25– 45.0 cm2), 13.0% mesophylls (45.0– 182.25 cm2), and 8.7% macrophylls (182.25– 1,640.25 cm2). Quercus copeyensis as well as Q. costaricensis have notophyllous sizes. The same occurs with the species Nectandra cufodontisii, Ocotea praetermissa, Prunus annularis, Rhamnus oreodendron, and Styrax argenteus. The largest leaves (mesophylls) have been found in the species Oreopanax capitatus and O. nubigenus. Comparing successional forests

along a gradient (Fig. 14.10), it turns out that average leaf size is 76.6 cm2 in an early secondary forest (27 species), 34.2 cm2 in a late secondary forest (31), and 57.8 cm2 in a mature, undisturbed oak forest (23), respectively. One notable feature is the presence of very small leaves on species represented by individuals with twisted branches. Among trees of the upper montane belt, Weinmannia pinnata has the smallest leaf surface area (per leaflet) and is the only nanophyll species. Vaccinium consanguineum (Ericaceae) may be considered a “quasi-nanophyll” species for having leaf surface areas of 3.34 to 5.52 cm2. Escallonia myrtilloides has leaf blades of similar sizes to those of the two species mentioned and belongs to habitats located just below the upper limit of the forest, at 3,200– 3,400 m a.s.l. (Gómez 1986, Kappelle et al. 1991, Islebe and Kappelle 1994); there it occupies sites in the sub-alpine elfin forest that borders the páramo vegetation (Gómez 1986). Escallonia myrtilloides is accompanied by many other woody species with nanophyllous leaves restricted to the sub-alpine environment, e.g., Hypericum strictum, Pentacalia firmipes, Pernettya coriacea, Vaccinium floribundum, and Weinmannia trianae (Kappelle et al. 1991). Around 10 km to the east of Jaboncillo de Dota, in the locality of Villa Mills (2,700 m a.s.l.), leaf sizes in the mesophyll class were the most prominent, especially in the sub-canopy of the forest (Dolph and Dilcher 1980). It should be noted, however, that these authors included very few species in their foliar analyses. The average specific leaf weight of 20 forest tree species in a primary oak forest is 160.1 g m− 2 (specific leaf weight = leaf dry weight per leaf area), while the specific leaf water content fluctuates around 222.1 g m− 2. Average levels of leaf nutrients (per unit weight) for 23 species (20 primary and three secondary) are: (i) nitrogen (N/wt): 10.8 mg g− 1; (ii) phosphorus (P/wt): 0.9 mg g− 1; and (iii) potassium (K/ wt): 9.2 mg g− 1. The proportion of N/ P is 12.0. Leaf nitrogen levels remain below 15 mg g− 1. The greatest concentration of phosphorus in leaves occurs in the species Oreopanax capitatus. The levels of potassium varied from low levels in Miconia tonduzii, to relatively high levels in Oreopanax nubigenus (Kappelle and Leal 1996). In general, nutrient concentrations in Costa Rican oak forests are similar to those observed in other tropical montane forests. Forest Light Regime

Camacho and Bellefleur (1996) studied acclimation to two light regimes in leaves of six tree species from the oak forests in the CATIE/COSUDE Experimental Area, in Siberia de Villa Mills (2,700– 2,800 m a.s.l.). These authors shaded groups of seedlings and saplings of the selected species that were growing in light (light and semi-light species sensu

The Montane Cloud Forests of the Cordillera de Talamanca 475

Blaser [1987]: Schefflera rodriguesiana [light] and Quercus copeyensis [semi-light]), prior to expansion of the leaf blade and until their complete development. Simultaneously, selected species that were growing in shade (shade and semi-shade species sensu Blaser [1987]: Vaccinium consanguineum [shade] and Drymis granadensis [semi-shade]) were exposed to light. These authors also studied Quercus costaricensis and Weinmannia pinnata, two species that show characteristics of both groups [semi-light and semishade]. In their study, leaf area, blade thickness, stomatal density, specific density, specific weight, and specific water content were evaluated for individuals under the aforementioned experimental treatment as well as for those under natural conditions (the “light controls” and the “shade controls”; see Camacho and Bellefleur [1996]). The results of this analysis suggest that Quercus copeyensis and Drymis granadensis show a greater potential for acclimation to shade, while Schefflera rodriguesiana seems to acclimate better to brighter surroundings; the species Vaccinium consanguineum, Weinmannia pinnata, and Quercus costaricensis have the potential to acclimatize to both environments (Camacho and Bellefleur 1996). Water and Nutrient Cycling

Talamancan mountain forests often experience an almost diurnal presence of clouds and mist (Kappelle 2006a,d). Although knowledge of the overall effect of clouds through fog or horizontal precipitation on the hydrological input in tropical montane forests is still scanty (Bruijnzeel and Proctor 1995), it has been widely recognized that, compared to other tropical forests, the specific atmospheric humidity regime of these forests represents one of the main factors causing the large array of differences in forest structure and functioning (Bruijnzeel 2001, Bruijnzeel et al. 2010a,b). Köhler et al. (2006) measured incident rainfall (gross precipitation) in Talamancan montane oak forests, and recorded 2,800– 2,900 mm per year, of which 70– 75% corresponded to throughfall, 2– 17% to stemflow, and 10– 25% to canopy interception— depending on the successional age of the forest stands. Their results show that nutrient concentrations in throughfall water exceeded those measured in incident rainfall. In upper canopy trees (Quercus), they recorded a pH of stemflow water ranging from 4.2 to 5.7 and noted significantly higher nutrient concentrations in stemflow in these tall trees, than in lower (sub)canopy trees. Concentrations of NO3−, NH4+, Ca2+, and K+ in cloud water collected in the middle and at the end of the dry season were significantly higher than at the beginning of the dry season (Köhler 2002).Total annual litter production in mature

old-growth oak forest was 12,870 kg ha− 1 per year. Leaves dominated the litter fraction, which contributed to some 56% of total litter (Köhler 2002, Köhler et al. 2006, 2008). In a complementary study, Hölscher et al. (2003) analyzed nutrient fluxes in stemflow and throughfall in three successional stages of Quercus copeyensis dominated upper montane forests in the Cordillera de Talamanca: an oldgrowth forest stand, an early successional (10-year-old) forest stand, and a mid-successional (≥30-year-old) forest stand (Fig. 14.10). Differences in nutrient fluxes among the successional stages were related to structural characteristics of the stands (stem density, leaf area, and epiphyte abundance). No difference in the average stand leaf area index between the old-growth forest and the early successional forest was found. However, a significantly higher leaf area was found in the mid-successional forest. Also, large differences in litterfall from non-vascular epiphytes (mosses, liverworts, and lichens) were noted. These differences reflected changes in epiphyte abundance, with highest values in the old-growth forest. Total nutrient transfer via stemflow and throughfall from the canopy to the soil showed only minor differences among the stands. The stands studied by Hölscher et al. (2003, 2010) differed widely in the ratio of nutrient transport via stemflow to the total nutrient flux by water below the canopy. The K flux with stemflow accounted for 5% of the total in the oldgrowth forest but it accounted for 17% (early successional forest) and 26% (mid-successional forest) in the secondary forests. The authors concluded that differences in canopy structure and epiphyte abundance in old-growth and secondary forests resulted in large differences in the partitioning of nutrient transport into stemflow and throughfall components although total nutrient transfers via water reaching the soil were similar (Hölscher et al. 2003, 2010). Hertel et al. (2006) report that the carbon pool (mol m− 2) of the organic soil layer is often highest in mature oldgrowth forests (533) when compared to early (80) and mid (252) successional stands. Similarly, the organic soil C/ N ratio (mol mol− 1) increases from early (23) and mid (25) successional vegetation to old-growth (27) forests. Concentrations of N and P (mol m− 3) as well as the Ca, Mg, and K pools (mmol m− 2) also rise as forest stands develop from early into mature phases. Acidity levels (pH measured in H2O/KCl), however, decrease from 6.0/5.6 to 4.0/3.4 over successional time (Hertel et al. 2006). Furthermore, the analysis of soil samples from the organic layer and the upper mineral soil (0– 10 cm) showed that the biomass of fine roots (roots 3,000 m) the main resource use concerns moss collection for ornamental purposes (floral arrangements for Christmas rituals), while below 2,000 m coffee plantations dominate the region. Today, ecotourism is the most important activity in the district. Tourism facilities abound, particularly in the Savegre valley. Part of the success of ecotourism can be attributed to the presence of the resplendent quetzal, for which bird watchers from around the world travel long distances to the area to see a glimpse of this magnificent and mythic bird. Of course, when exploring ecotourism opportunities in the Cordillera de Talamanca, it will be essential to assess the carrying capacity of the localities to be developed— particularly when considering the remote

and fragile sectors of this important highland region (Brenes et al. 2007). Reforestation

Until date there have been only a few reforestation activities in the high Talamancas. In general, plantations are small (several hectares) and consist of fast-growing exotic tree species like Cupressus lusitanica (Mexican cypress), Pinus (pine), and Eucalyptus. Sometimes, windbreaks and living fences of Casuarina equisetifolia (casuarina or Australian pine) are observed. Like many other tree plantations that are not being thinned, these plantations produce excessive shade and can even accelerate erosion, since few other species grow succesfully under their canopies (G. Budowski, pers. comm.). For example, Lines and Fournier (1979) demonstrated that C. lusitanica has an allelopathic effect on the germination of some herb seeds. Plantations of promising native species, such as the Andean alder (Alnus acuminata), which fixes nitrogen and helps to restore the soil, are uncommon (Kappelle 1996). Holl and Zahawi (2014)

Fig. 14.11 Landscape mosaic of the oak forest zone along the Río Savegre at about 2,300 m near San Gerardo de Dota. The mosaic is composed of old-growth Quercus copeyensis forest, young successional stands, pastures with isolated oak and Buddleja trees, living fences of cypress, and apple orchards. Photograph by Maarten Kappelle, 1992.

The Montane Cloud Forests of the Cordillera de Talamanca 479 Fig. 14.12 Altitudinal zonation of mountain vegetation, agricultural products, and agroecological belts between 2,000 and 3,500 m elevation in Dota county, Costa Rica. Reproduced from Kappelle and Juárez 2006, with kind permission from Springer.

report that planting trees at mid-elevation in southern highland Costa Rica substantially increases biomass accumulation during the first several years of forest recovery in former agricultural lands.

often by local people in this region. The question is whether the knowledge of medicinal and other useful plants will remain a shared good in the community— or simply will disappear while this rural community quickly modernizes (Kappelle et al. 2000).

Ethnobotany

Numerous native and introduced plant species in the montane cloud forest zone of the Cordillera de Talamanca are used by local peoples. Kappelle et al. (2000) and Kappelle and Juárez (2006) report that of a total of 189 species found in the valley of San Gerardo de Dota, 23.8% are used for medicinal purposes, 39.7% for nutrition, and 24.3% in construction (timber) or as fuel (firewood, charcoal). Other less important uses include dyes, ornamental use (ecotourism), forage, gums, oils, and poisons. Trunks (53%) and fruits (47%) are the plant parts that are most often used, followed by leaves (33%) and branches (30%). More than 27% of all the plants are used on a daily basis, while 34.9% are used occasionally and around 11.6% just rarely. Today, however, native species are used less and less

Emerging Threats Beyond deforestation (clear cutting, land conversion, fragmentation), many other threats are affecting— or soon will affect— the viability of the biodiversity of the montane cloud forests of southern Costa Rica. Climate change, fires, invasive species, hunting, infrastructure, exploitation, illegal Cannabis plantations, etc. are expected to continue to deplete plant and animal populations of this diverse region. Today, many animal species are becoming more and more threatened by fast road traffic. An example is the killing of a female tapir in August 2009 during a road accident, when it crossed the Inter-American Highway at 2,900 m elevation near the northern limit of Parque Nacional Los

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Quetzales at Ojo de Agua. The tapir was pregnant, showed milk production, and died on the spot (Arsenio Agüero, MINAE, pers. comm. 2010; Fig. 14.13). Furthermore, along the Río Savegre near San Gerardo de Dota, palm heart extraction is still occurring in 2010 (Arsenio Agüero, MINAE, pers. comm.). However, the local population is responding swiftly and in an organized manner to this and other incidents, ensuring hunting and extraction are controlled locally by the community. Changes in temperature and precipitation due to increased greenhouse gas (GHG) emissions into the atmosphere are already affecting tropical cloud forests and their species around the globe (e.g., Karmalkar et al. 2008, Bruijnzeel et al. 2010a,b, Laurance et al. 2011, and many sources therein). Regional climate models for Costa Rica clearly show an increase in temperature and decrease in precipitation under the A2 climate change scenario. At high elevations in the country, warming is amplified and future

temperature distribution lies outside the range of presentday distribution. On the Pacific slope, temperature changes seem greater than at the Caribbean, while elevations of cloud formations are expected to increase considerably along the Pacific side (Karmalkar et al. 2008). These modern climate changes (drying of forest stands) together with human intervention may eventually cause an increase in the frequency of forest fires in cloud forests (Asbjornsen and Wickel 2009), which are historically known to occur in the Talamancan highlands (Anchukaitis and Horn 2005).

Public Protected Areas Most areas of the montane cloud forests of the Cordillera de Talamanca have a protected status. Core areas include Parque Nacional Chirripó, Parque International La Amistad (PILA), Parque Nacional Tapantí– Macizo de la Muerte,

Fig. 14.13 A pregnant tapir killed in a 2009 road accident near Ojo de Agua along the Inter-American Highway is being removed by governmental officials. Photograph by Carlos Serrano, 2009.

The Montane Cloud Forests of the Cordillera de Talamanca 481

Fig. 14.14 Group of protected-area managers of the ACLA-P subdivision of the Ministry of Environment, Energy and Technology (MINAET) during a biodiversity training session at Parque Nacional Los Quetzales. Photograph by Maarten Kappelle, 2010.

Parque Nacional Los Quetzales (Fig. 14.14), Reserva Forestal Río Macho, Reserva Biológica Hitoy Cerere, Reserva Biológica Barbilla, Zona Protectora Las Tablas, Zona Protectora Río Navarro y Río Sombrero, and Reserva Forestal Los Santos (Kappelle and Juárez 1994, Kappelle 1996; Fig. 14.1). Most of these areas are part of the Reserva de la Biosfera La Amistad (RBA), a megadiverse area of 612,570 ha (Castro et al. 1995), equivalent to 12% of Costa Rica’s land territory (MIRENEM 1992, Araya and De Marco 2001). It also includes seven indigenous reserves (Cabagra, Chirripó, Salitre, Talamanca, Tayní, Telire, and Ujarrás) that are populated by Bri-Bri, Cabécar, and Naso/Teribe ethnic peoples. Moreover, the RBA includes a number of protected areas in Panama across the border with Costa Rica, such as the Panamanian sector of Parque International La Amistad (PILA) (Aparicio 2006). At a national level, the protected areas belonging to the Costa Rican sector of the RBA have

been administratively distributed over two Conservation Areas: Área de Conservación Amistad-Pacifico (ACLA-P) and Área de Conservation Amistad-Caribe (ACLA-C). The RBA was designated in 1982 through UNESCO’s “Man and the Biosphere Program” (MAB) (Bermúdez and Mena 1992). A year later, these forests and its adjacent páramos were declared a World Heritage Site (Whitmore 1990, Vernes 1992). It has also been recognized as a Center of Plant Diversity (Groombridge 1992, Harcourt et al. 1996, Chaverri et al. 1997), since it may contain even more than 10,000 species of vascular plants (L. D. Gómez, pers. comm. 1989). It is also an Endemic Bird Area (Harcourt et al. 1996) and an integral part of the species-rich Central American Biodiversity Hotspot (Myers et al. 2000). In 2003 the highland peat bogs that are embedded within the montane cloud forest zone of the Cordillera de Talamanca were declared a Ramsar Wetland of International

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Importance known as Turberas de Talamanca (Ramsar site no. 1286; see www.ramsar.org). These peatlands are characterized by Cyperaceae, Juncaceae, Ericaceae, large ferns of the Blechnaceae family, plus Sphagnum and other mosses (for further detail on these peat bogs and related páramo vegetation, see Kappelle and Horn, chapter 15 of this volume). The Talamancan Montane Forests Ecoregion (Dinerstein et al. 1995), to which these protected areas belong, is a key component of the Corredor Biológico Mesoamericano, the CBM (Miller et al. 2001, Obando 2002). This huge contiguous landscape connector that links Central American countries includes one of the oldest formal biocorridors of Costa Rica: the Talamancan-Caribbean Biological Corridor that runs from the Chirripó National Park to the Caribbean coast (see the joint report by the Talamancan-Caribbean Biological Corridor Commission and TNC, 1993). Corridors like the CBM are essential to conserve isolated populations of the Resplendant Quetzal in the fragmented cloud forests of Meso-America (Solórzano et al. 2004, Aparicio 2006). More recently, a proposal has been developed to create a corridor between the Parque Internacional La Amistad and the Península de Osa that includes the Parque Nacional Piedras Blancas and Parque Nacional Corcovado. The proposed corridor has been coined “Amistosa” by the author of this chapter. Plans to develop it are currently under discussion by the government (MINAET) and conservation organizations (e.g., The Nature Conservancy).

IUCN Red Lists, CITES, and National Species Protection The IUCN Red List of Threatened Species (http://www.iucn .org, and see Jiménez 1999) includes at least 27 species of threatened trees known from the Área de Conservación La Amistad– Pacífico (ACLA-P). Listed as “vulnerable” are Caryocar costaricense, Cedrela odorata, Cornus disciflora, Couratari guianensis, Dalbergia retusa, Ilex pallida and I. vulcanica, Oreopanax oerstedianus, Persea schiedeana (wild avocado), Protium pittieri, Quercus costaricensis (oak), Pouteria macrocarpa, Swietenia macrophylla (mahogany), and Tocoyena pittieri. Among the most “endangered” trees are Eugenia salamensis, Lonchocarpus minimiflorus, and Vitex cooperi. Some trees in ACLA-P that have nationally been declared “en veda” and cannot be cut without governmental permission are Copaifera camibar, Myroxylon balsamum, Platymiscium pinnatum, and S. macrophylla (Decreto Ejecutivo 257000-MINAE, La Gaceta No.11, January 16, 1997).

Many amphibians are currently threatened and now appear on the IUCN Red List. For instance, the leptodactilyd quark frog is considered “vulnerable,” while the mountain salamander and mountain tree frog have been ranked as “endangered” and the true mountain frog has been qualified as “critically endangered” (http://www.iucn.org; Kappelle 2008). Because of the loss of its habitat and illegal trade of its adults, chicks, eggs, and feathers throughout its whole distribution range, the resplendent quetzal has been included in CITES Appendix I (http://www.cites.org) as well as in the “vulnerable” category of the IUCN Red List (García-Rojas 2006). At least ten birds known from Parque Internacional La Amistad (PILA) and surrounding areas have been listed on CITES’ Appendix II since they are represented by reduced populations. Another seven species have restricted distributions in the region (Arias 2001). Non-volant mammal species that have the Cordillera de Talamanca as their habitat and have been listed as threatened on the IUCN Red List are Sylvilagus dicei and Tapirus bairdii (both “endangered”), Leopardus tigrinus and Panthera onca (both “near threatened”), Cryptotis gracilis (“vulnerable”), Bassariscus sumichrasti, Bassaricyon gabbii, Heteromys oresterus, and Orthogeomys heterodus (all “low risk” species), and Choloepus hoffmanni, Lontra longicaudis, and Mazama americana (still “data deficient”). Large mammals listed in Appendix I of the CITES convention that are still represented by viable populations in ACLA-P are the puma or cougar, the jaguar, the ocelot, the margay, Baird’s tapir, and Geoffroy’s spider monkey (Ateles geoffroyi) (Carrillo and Vaughan 1994, Carrillo et al. 1999, Kappelle 2008).

Future Perspectives: Looking Ahead It will be necessary to design biodiversity conservation and sustainable development systems for the montane cloud forest zone of southern Costa Rica that work within a context of robust legal frameworks, public-private partnerships (PPPs), engaged participation of civil society organizations (CSOs), and secure, sustainable financing. Indeed, Agenda 21 of the Convention on Biological Diversity (CBD) recognized that mountain ecosystems are fragile and constitute an important source of water, energy, biological diversity, minerals, and forest and agricultural products. It states that 10% of the world’s population depends on resources from mountains. Therefore, the appropriate management of the natural resources that Costa Rica’s cloud forests contain, as well as the development of

The Montane Cloud Forests of the Cordillera de Talamanca 483

sustainable livelihoods of its peoples, should be considered a high priority. In practical terms, this could imply promoting sustainable forest management principles and criteria, boosting reforestation and natural regeneration with native species, development of integrated agroforestry systems (including shaded, bird-friendly coffee plantations instead of non-treed coffee fields), the establishment of biological corridors in ecological networks, and sustainable ecotourism initiatives. If we are to preserve the remaining Talamancan montane cloud forests and its variety of life as expressed in its genes, species, and ecosystem types in the long term, we will need to elaborate a participatory conservation strategy that goes beyond the traditional establishment of networks of protected core areas, buffer zones, and corridors (Kappelle 2004, 2008). We will need the full engagement of civil society— local/regional stakeholders and decision makers alike— to develop a broad-based, consensus-oriented conservation framework that is succesful in the long run. A good example of such an approach is the The Nature Conservancy– led development of a bi-national Site Conservation Plan (SCP) for the Parque Internacional La Amistad (including both the Costa Rican and Panamanian sectors of both the Atlantic and Pacific slopes of the Cordillera). This plan identifies a series of conservation strategies and actions that focuses on long-term benefits for both people and nature (Herrera et al. 2005). Multi-country, multi-scale, and multi-stakeholder initiatives like La Amistad’s SCP can help generate ecosystembased tools and approaches urgently needed to conserve, restore, and sustainably use the threatened, species-rich

highland cloud forests and other ecosystems of Costa Rica’s Cordillera de Talamanca for generations to come.

Acknowledgments I am very grateful to many MSc students from the universities of Amsterdam (UvA), Costa Rica (UCR, UNA), Tennessee (UT), Utrecht (UU), and Wageningen (WUR) who took on specific parts of the research program I have led in the Talamancan montane forests between 1985 and 2005. Also, I owe a particular thank-you to my tutors and peers: Antoine Cleef, Henry Hooghiemstra, Luis Poveda, Nelson Zamora, Quírico Jiménez, and Sally Horn, as well as the late Adelaida Chaverri, Luis Diego Gómez, and Tom van der Hammen. They all supported my work during the past 30 years by providing guidance and helping with plant identification. The Costa Rican Ministry of Environment and Energy (MINAE, previously known as MINAET and MIRENEM, including its predecessors SNP and DGF) graciously allowed me to conduct research in the country’s protected areas. CATIE, INBio, UNA, and UCR provided logistical support during different phases of my research. Funding was kindly provided by INBio, UNA, UvA, and the Netherlands Government (DGIS and NWO). Finally, I would like to thank my wife, Marta E. Juárez Ruiz, my mother, Mary E. Mohr, and my father, the late Dirk Kappelle, who encouraged me continually to conduct ecological studies in Costa Rica and widely publish and share my results with a range of national and foreign audiences during the past three decades.

References Alfaro, E., and B. Gamboa. 1999. Plantas Comunes del Parque Nacional Chirripó. Santo Domingo de Heredia: Instituto Nacional de Biodiversidad (INBio). 283 pp. Anchukaitis, K.J., and S.P. Horn. 2005. A 2000-year reconstruction of forest disturbance from southern Pacific Costa Rica. Palaeogeography, Palaeoclimatology, Palaeoecology 221: 35– 54. Aparicio, K. 2006. Sitio La Amistad Panamá: Conectando Pisos Altitudinales Mediante Corredores Biológicos. Panama: The Nature Conservancy (TNC). 106 pp. Araya, J., and G. de Marco. 2001. Informe sobre el Avance y Desarrollo de la Reserva de la Biosfera de la Amistad— Talamanca, Costa Rica. Technical Report. San José, Costa Rica: MINAE. 81 pp. Arias, E. 2001. Caracterización Biofísica del Parque Internacional La Amistad (PILA). Technical Report. Santo Domingo de Heredia, Costa Rica: INBio and TNC. 73 pp. Asbjornsen, H., and A.J. Wickel. 2009. Changing fire regimes in tropical montane cloud forests: a global synthesis. In M.A. Cochrane,

ed., Fire and Tropical Ecosystems, 607– 22. New York: SpringerVerlag. Aus der Beek, R., and S. Navas. 1993. Técnicas de producción y calidad del carbón vegetal en los robledales de altura de Costa Rica. Colección Silvicultura a Manejo de Bosques Naturales 8: 1– 41. Turrialba, Costa Rica: CATIE. Benzing, D.H. 1990. Vascular Epiphytes: General Biology and Related Biota. Cambridge, UK: Cambridge University Press. xvii + 354 pp. Bergoeing, J.P. 1977. Modelado glaciar en la Cordillera de Talamanca, Costa Rica. Informe Semestral (Julio a Diciembre, 1977): 33– 44. San José, Costa Rica: Instituto Geográfico Nacional (IGN). Bermúdez, F., and Y. Mena. 1992. Parques Nacionales de Costa Rica. San José, Costa Rica: Oficina de Planificación y Servicios Técnicos, Ministerio de Recursos Naturales, Energía y Minas (MIRENEM). Berner, P.O.B. 1992. Effects of slope on the dynamics of a tropical montane oak-bamboo forest in Costa Rica. PhD diss., University of Florida.

484 Chapter 14 Berry, E.W. 1918. The fossil higher plants from the Canal Zone. Bulletin of the United States National Museum 103: 15– 44. Blaser, J. 1987. Standörtliche und waldkundliche Analyse eines Eichenwolkenwaldes (Quercus spp.) der Montanstufe in Costa Rica. PhD thesis, Göttinger Beiträge zur Land- und Forstwirtschaft in den Tropen und Subtropen. Göttingen, Germany. Boza, M.A. 1984. Guía de Parques Nacionales de Costa Rica. Madrid: Fundación de Parques Nacionales (FPN)— INCAFO. 128 pp. Brenes, O., K. Castro del Valle, V. Jiménez, I. Mejía, and A. Mora. 2007. Determinación de la Capacidad de Carga Turística del Parque Internacional La Amistad. Serie Técnica No. 6: Apoyando los Esfuerzos en el Manejo y Protección de la Biodiversidad Tropical. San José, Costa Rica: The Nature Conservancy ( TNC). 27 pp. Bruijnzeel, L.A. 2001. Hydrology of tropical montane cloud forests: a reassessment. Land Use and Water Resource Research 1: 1.1– 1.18. Bruijnzeel, L.A., and L.S. Hamilton. 2000. Decision time for cloud forests. IHP Humid Tropics Programme Series no. 13. Paris, France: UNESCO. 41 pp. Bruijnzeel, L.A., M. Kappelle, M. Mulligan, and F.N. Scatena. 2010a. Tropical montane cloud forests: state of knowledge and sustainability perspectives in a changing world. In L.A. Bruijnzeel, F.N. Scatena, and L. Hamilton, eds., Tropical Montane Cloud Forests: Science for Conservation and Management, chap. 74. Cambridge, UK: Cambridge University Press. Bruijnzeel, L.A., M. Mulligan, and F.N. Scatena. 2011. Hydrometeorology of tropical montane cloud forests: emerging patterns. Hydrological Processes 25(3): 465– 98. Bruijnzeel, L.A., and J. Proctor. 1995. Hydrology and biochemistry of tropical montane cloud forests: what do we really know? In L.S. Hamilton, J.O. Juvik, and F.N. Scatena, eds., Tropical Montane Cloud Forests, Ecological Studies 110: 38– 78. Berlin: Springer. Bruijnzeel, L.A., F.N. Scatena, and L.S. Hamilton, eds. 2010b. Tropical Montane Cloud Forests: Science for Conservation and Management. Cambridge, UK: Cambridge University Press. Bruijnzeel, L.A., and E. Veneklaas. 1998. Climatic conditions and tropical montane forest productivity: the fog has not lifted yet. Ecology 78: 3– 9. Burger, W.C. 1980. Why are there so many kinds of flowering plants in Costa Rica? Brenesia 17: 371– 88. Buskirk, R., and W. Buskirk. 1976. Changes in arthropod abundance in a highland Costa Rican Forest. American Midland Naturalist 95: 288– 98. Bussing, W. 1998. Peces de las Aguas Continentales de Costa Rica. Segunda edición. San José, Costa Rica: Editorial Universidad de Costa Rica (EUCR). 468 pp. Camacho, M., and P. Bellefleur. 1996. Aclimatación morfológica a la luz en seis especies arbóreas de los bosques montanos de Costa Rica. Revista de Biología Tropical 44(1): 71– 79. Carrillo, E., and C. Vaughan. 1994. La Vida Silvestre de Mesoamerica: Diagnóstico y Estrategia para Su Conservacion. Heredia, Costa Rica: EUNA. Carrillo, E., G. Wong, and J.C. Sáenz. 1999. Mamíferos de Costa Rica. Primera edición. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). 248 pp. Castillo, R. 1984. Geología de Costa Rica: Una Sinopsis. San José, Costa Rica: Editorial de la Universidad de Costa Rica (EUCR). 182 pp. Castro, J., M. Ramírez, R. Saunier, and R. Meganck. 1995. The La Amis-

tad Biosphere Reserve. In R. Saunier and R. Meganck, eds., Conservation of Biodiversity in the New Regional Planning, chap.10. Washington, DC: Organization of American States. Cavalier J., D. Solis, and M.A. Jaramillo. 1996. Fog interception in montane forests across the central Cordillera of Panama. Journal of Tropical Ecology 12: 357– 69. Chaverri, A., and O. Hernández. 1995. Ecology and management in montane oak forests: an option for conserving biodiversity. In S.P. Churchill, H. Balslev, E. Forero, and J. Luteyn, eds., Biodiversity and Conservation of Neotropical Montane Forests: Proceedings of the Neotropical Montane Forest Biodiversity and Conservation Symposium, The New York Botanical Garden, 21– 26 June 1993, 609– 17. The New York Botanical Garden. Chaverri, A., B. Herrera, and O. Herrera-MacBryde. 1997. La Amistad Biosphere Reserve: Costa Rica and Panama (Central America: CPD Site MA17). In S.P. Davis, V.H. Heywood, O. Herrera-MacBryde, J. Villalobos, and A.C. Hamilton, eds., Centres of Plant Diversity: A Guide and Strategy for their Conservation, 209– 14. Cambridge, UK: WWF— IUCN, IUCN Publications Unit. Chaves, J. 2001. Movimientos altitudinales de aves frugivoras grandes en la vertiente del Caribe de la Cordillera de Tilarán, Costa Rica: causas y consecuencias para la conservacion. M.Sc. thesis, Escuela de Biologia,Universidad de Costa Rica. Chinchilla, E. 1987. Atlas Cantonal de Costa Rica. San José, Costa Rica: Instituto de Fomento y Asesoría Municipal (IFAM), Imprenta Nacional. 396 pp. Coen, E.J. 1983. Climate. In D.H. Janzen, ed., Costa Rican Natural History, 35– 46. Chicago: University of Chicago Press. Cole, R.J. 2009. Postdispersal seed fate of tropical montane trees in an agricultural landscape, southern Costa Rica. Biotropica 41(3): 319– 27. Daily, G.C., P.R. Ehrlich, and G.A. Sánchez-Azofeifa. 2001. Countryside biogeography: use of human-dominated habitats by the avifauna of southern Costa Rica. Ecological Applications 11: 1– 13. Dinerstein, E., D.M. Olsen, D.J. Graham, A.L. Webster, S.A. Primm, M.P. Bookbinder, and G. Ledec. 1995. A Conservation Assessment of the Terrestrial Ecoregions of Latin America and the Caribbean. Washington, DC: WWF– The World Bank. Dolph, G., and D. Dilcher. 1980. Variation in leaf size with respect to climate in the tropics of the western hemisphere. Bulletin of the Torrey Botanical Club 107: 154– 62. Donnelly, T.W. 1989. Geologic History of the Caribbean and Central America. In Geological Society of the Americas, Decade of North American Geology, vol. A, The Geology of North America: An Overview, 299– 321. Dressler, R.L. 1993. Field Guide to the Orchids of Costa Rica and Panama. Ithaca, NY: Comstock Pub. Associates. 374 pp. Eckardt, N. 1982. Charcoal production in the high altitude oak forest in the Talamanca Mountains, Costa Rica. Undergraduate thesis, Associated Colleges of the Midwest (ACM), Universidad Nacional. Heredia, Costa Rica. Edwards-Widmer, Y. 1999. The ecological role of bamboo (Chusquea spp.) in the old-growth Quercus forests of the Cordillera de Talamanca, Costa Rica. Diss., Naturwissenschaften ETH Zürich, Nr. 13186. DOI: 10.3929/ethz-a-003839772. Estrada, A., and N. Zamora. 2004. Riqueza, cambios y patrones florísticos en un gradiente altitudinal en la cuenca hidrográfica del río Savegre, Costa Rica. Brenesia 61: 1– 52.

The Montane Cloud Forests of the Cordillera de Talamanca 485 Flores, T. 1990. Clave dendrológico para la vegetación arbórea del piso montano de la Cordillera de Talamanca, Costa Rica. Lic. thesis, Universidad Nacional. Heredia, Costa Rica. García-Rojas, M. 2006. Diet and habitat preference of the Resplendent Quetzal (Pharomachrus mocinno costaricensis) in Costa Rican montane oak forest. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, Ecological Studies Series 185: 325– 36. New York: Springer Verlag. Gentry, A.H. 1982. Patterns of neotropical plant species diversity. Evolutionary Biology 15: 1– 84. Gentry, A.H. 1992. Tropical forest biodiversity: distributional patterns and their conservational significance. Oikos 63: 19– 28. Geuze, T. 1989. A Silvicultural Analysis of Secondary Succession in the Mature Oak Forest Belt, Cordillera de Talamanca, Costa Rica. Technical Report. Heredia, Costa Rica: Universidad Nacional. 28 pp. Gomes, L.G.L., V. Oostra, V. Nijman, A.M. Cleef, and M. Kappelle. 2008. Tolerance of frugivorous birds to habitat disturbance in a tropical cloud forest. Biological Conservation 141: 860– 71. Gómez, L.D. 1984. Las Plantas Acuáticas y Anfíbias de Costa Rica y Centroamérica. Vol. I. Liliopsida. San José, Costa Rica: Editorial UNED. 430 pp. Gómez, L.D. 1986. Vegetación de Costa Rica. Vol. 1. In L.D. Gómez, ed., Vegetación y Clima de Costa Rica. Con 10 mapas (escala 1:200.000). San José, Costa Rica: EUNED. Gómez, L.D. 1989. Unidades Naturales: Estado y Uso Actual de los Ecosistemas y Recursos Naturales, Beneficios Potenciales y Riesgos Naturales en la Región de la Reserva de la Biósfera Talamanca— La Amistad. Consultoría. San José, Costa Rica: Organización de Estados Americanos (OAE). 13 pp. Gómez, L.D., and J.M. Savage. 1983. Searchers on that rich coast: Costa Rican field biology, 1400– 1980. In D.H. Janzen, ed., Costa Rican Natural History, 1– 11. Chicago: University of Chicago Press. González, L. 2005. Árboles y Arbustos Comunes del Parque Internacional La Amistad. Santo Domingo de Heredia, Costa Rica: Editorial INBio. 286 pp. González-Maya, J.F., J. Schipper, and K. Rojas-Jiménez. 2009. Elevational distribution and abundance of Baird’s tapir (Tapirus bairdii) at different protection areas in Talamanca region of Costa Rica. Tapir Conservation 18(1): 29– 35 Graham, A. 1989. Late Tertiary paleoaltitudes and vegetational zonation in Mexico and Central America. Acta Botanica Neerlandica 38: 417– 24. Grau, H.R., and D. Rivera-Ospina. 1996. Regeneracion temprana de Chusquea tomentosa (Poaceae, Bambusoideae) en Talamanca, Costa Rica. Revista de Biología Tropical 44: 691– 92. Groombridge, B., ed. 1992. Global Biodiversity: Status of the Earth’s Living Resources. World Conservation Monitoring Centre ( WCMC). New York: Chapman and Hall. 585 pp. Guariguata, M., and G. Sáenz. 2002. Post-logging acorn production and oak regeneration in a tropical montane forest, Costa Rica. Forest Ecology and Management 167: 285– 93. Halling, R.E., and G.M. Mueller. 2005. Common mushrooms of the Talamanca mountains, Costa Rica. Memoirs of the New York Botanical Garden 90: 1– 195. Hamilton, L.S., J.O. Juvik, and F.N. Scatena. 1995. Tropical Montane Cloud Forests. New York: Springer. 407 pp. Hammel, B.E., M.H. Grayum, C. Herrera, and N. Zamora. 2004. Man-

ual de Plantas de Costa Rica. Vol. 1. Introducción. St. Louis, MO: Missouri Botanical Garden, Instituto Nacional de Biodiversidad, and Museo Nacional de Costa Rica. 299 pp. Harcourt, C.S., J.A. Sayer, and C. Billington, eds. 1996. The Conservation Atlas of Tropical Forests: The Americas. IUCN / CIFOR / WCMC / BP. New York: Simon and Schuster. Hartshorn, G.S. 1983. Introduction to Plants. In D.H. Janzen, ed., Costa Rican Natural History, 118– 57. Chicago: University of Chicago Press. Hartshorn, G.S., and L.J. Poveda. 1983. Checklist of trees. In D.H. Janzen, ed., Costa Rican Natural History, 158– 183. Chicago: University of Chicago Press. Hastenrath, S. 1973. On the Pleistocene glaciation of the Cordillera de Talamanca, Costa Rica. Zeitschrift für Gletschertkunde und Glazialgeologie 9: 105– 21. Helmer, E.H., and S. Brown. 2000. Gradient analysis of biomass in Costa Rica and an estimate of total emissions of greenhouse gases from biomass burning. In C.A. Hall, ed., Ecology of Tropical Development: The Myth of Sustainable Development in Costa Rica, 503– 26. San Diego, CA: Academic Press. Henderson, A., S. Churchill, and J. Luteyn. 1991. Neotropical plant diversity. Nature 351: 21– 22. Herrera, W. 1986. Clima de Costa Rica. Vol. 2. En L.D. Gómez, ed., Vegetación y Clima de Costa Rica. Con 10 mapas (escala 1:200.000). San José, Costa Rica: EUNED. Herrera, B., I. Candanedo, and F. Carazo. 2005. Guía de Acciones para la Conservación del Sitio Binacional La Amistad. Serie Técnica No. 1: Apoyando los Esfuerzos en el Manejo y Protección de la Biodiversidad Tropical. San José, Costa Rica: The Nature Conservancy (TNC). 38 pp. Herrera, W., and L.D. Gómez. 1993. Mapa de Unidades Bióticas de Costa Rica. Escala 1:685.000. San José, Costa Rica: US Fish and Wildlife Service / TNC / INCAFO / CBCCR / INBio / Fundación Gómez / Dueñas. Hertel, D., D. Hölscher, L. Köhler, and C. Leuschner. 2006. Changes in fine root system size and structure during secondary succession in a Costa Rican montane oak forest. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, Ecological Studies Series 185: 283– 297. New York: Springer Verlag. Hertel, D., C. Leuschner, and D. Hölscher. 2003. Size and structure of fine root systems in old-growth and secondary tropical montane forests (Costa Rica). Biotropica 35: 143– 53. Hofstede, R.G.M., J.H.D. Wolf, and D.H. Benzing. 1993. Epiphytic biomass and nutrient status of a Colombian upper montane rain forest. Selbyana 14: 37– 45. Holdridge, L.R., W.C. Grenke, W.H. Hatheway, T. Liang, and J.A. Tosi. 1971. Forest Environments in Tropical Life Zones: A Pilot Study. Oxford, UK: Pergamon Press. 735 pp. Holdridge, L.R., and L.J. Poveda. 1975. Arboles de Costa Rica. San José, Costa Rica: Centro Cientifico Tropical (CCT). Holl, K.D. 1998. The role of bird perching structures in accelerating tropical forest recovery. Restoration Ecology 6: 253– 61. Holl, K.D. 1999. Factors limiting tropical moist forest regeneration in agricultural land: seed rain, seed germination, microclimate and soil. Biotropica 31: 229– 42. Holl, K.D., and M.E. Lulow. 1997. Effects of species, habitat, and distance from edge on post-dispersal seed predation in a tropical rainforest. Biotropica 29: 459– 68.

486 Chapter 14 Holl, K.D., and E. Quirós-Nietzen. 1999. The effect of rabbit herbivory on reforestation of an abandoned pasture in southern Costa Rica. Biological Conservation 87: 391– 95. Holl, K.D., and R.A. Zahawi. 2014. Factors explaining variability in woody above-ground biomass accumulation in restored tropical forest. Forest Ecology and Management 319: 36– 43. Hölscher, D., L. Köhler, M. Kappelle, and C. Leuschner. 2010. Ecology and use of old-growth and recovering montane oak forests in the Cordillera de Talamanca, Costa Rica. In L.A. Bruijnzeel, F.N. Scatena, and L.S. Hamilton, eds., Tropical Montane Cloud Forests: Science for Conservation and Management, 610– 17. Cambridge, UK: Cambridge University Press. Hölscher, D., L. Köhler, C. Leuschner, and M. Kappelle. 2003. Nutrient fluxes in stemflow and throughfall in three successional stages of an upper montane rain forest in Costa Rica. Journal of Tropical Ecology 19: 557– 65. Hölscher, D., L. Köhler, A.I.J.M. van Dijk, and L.A. Bruijnzeel. 2004. The importance of epiphytes to total rainfall interception by a tropical montane rainforest in Costa Rica. Journal of Hydrology 292: 308– 22. Holz, I. 2003. Diversity and Ecology of Bryophytes and Macrolichens in Primary and Secondary Montane Quercus forests, Cordillera de Talamanca, Costa Rica. Dissertation zur Erlangung des Doktorgrades der Mathematisch-Naturwissenschaftlichen Fakultäten der GeorgAugust-Universität zu Göttingen. 172 pp. Holz, I., and S.R. Gradstein. 2005a. Phytogeography of the bryophyte floras of oak forests and páramo of the Cordillera de Talamanca, Costa Rica. Journal of Biogeography 32: 1591– 609. Holz, I., and S.R. Gradstein. 2005b. Cryptogamic epiphytes in primary and recovering upper montane oak forests of Costa Rica— species richness, community composition and ecology. Plant Ecology 178: 89– 109. Holz, I., S.R. Gradstein, J. Heinrichs, and M. Kappelle. 2002. Bryophyte diversity, microhabitat differentiation and distribution of life forms in Costa Rican upper montane Quercus forest. Bryologist 105(3): 334– 48. Hooftman, D.A.P. 1998. Generic composition, structure and diversity of secondary forests at Amisconde, the Pacific slope of the Cordillera de Talamanca, Costa Rica. Revista de Biología Tropical 46(4): 1069– 79. Hooghiemstra, H., A.M. Cleef, G. Noldus, and M. Kappelle. 1992. Upper Quaternary vegetation dynamics and palaeoclimatology of the La Chonta bog area (Cordillera de Talamanca, Costa Rica). Journal of Quaternary Science 7(3): 205– 25. Instituto Meterológico Nacional (IMN). 1988. Catastro de las series de precipitationes medidas en Costa Rica. San José, Costa Rica: Instituto Meteorológico Nacional (IMN), Ministerio de Recursos Naturales, Energía y Minas (MIRENEM). Islebe, G.A., and M. Kappelle. 1994. A phytogeographical comparison between subalpine forests of Guatemala and Costa Rica. Feddes Repertorium 105(1– 2): 73– 87. Berlin. Jiménez, Q. 1999. Árboles Maderables en Peligro de Extinción en Costa Rica. Segunda edición, revisada y ampliada. Santo Domingo de Heredia, Costa Rica: INBio. 187 pp. Jiménez, W., and A. Chaverri. 1982. Algunas consideraciones taxonómicas, ecológicas y silviculturales de los robles (Quercus sp.), con énfasis en Costa Rica: una revisión de literatura. Serie Ecología y Manejo

de Vegetación de Altura 1: 1– 24. Universidad Nacional, Heredia, Costa Rica. Jiménez, W., A. Chaverri, R. Miranda, and I. Rojas. 1988. Aproximaciones silviculturales al manejo de un robledal (Quercus spp.) en San Gerardo de Dota, Costa Rica. Turrialba 38(3): 208– 14. Johnson, W., and C. Vaughan. 1993. Habitat use of small terrestrial rodents in the Costa Rican highlands. Revista de Biología Tropical 41(3): 521– 27. Kappelle, M. 1987. A phytosociological analysis of oak forests in the western Talamanca Range, Costa Rica. M.Sc. thesis, Hugo de Vries Laboratorium, University of Amsterdam. Amsterdam, The Netherlands. 217 pp. Kappelle, M. 1991. Distribución altitudinal de la vegetación del Parque Nacional Chirripó, Costa Rica. Brenesia 36: 1– 14. Kappelle, M. 1992. Structural and floristic differences between wet Atlantic and moist Pacific montane Myrsine— Quercus forests in Costa Rica. In H. Balslev and J.L. Luteyn, eds., Páramo: An Andean Ecosystem under Human Influence, 61– 70. London: Academic Press. Kappelle, M. 1993. Recovery following clearing of an upper montane Quercus forest in Costa Rica. Revista de Biología Tropical 41(1): 47– 56. San José, Costa Rica. Kappelle, M. 1995. Ecology of mature and recovering Talamancan montane Quercus forests, Costa Rica. PhD thesis, Hugo de Vries Laboratorium, University of Amsterdam. Amsterdam, The Netherlands. 273 pp. Kappelle, M. 1996. Los Bosques de Roble (Quercus) de la Cordillera de Talamanca, Costa Rica: Biodiversidad, Ecología, Conservación y Desarrollo. Amsterdam / Santo Domingo de Heredia: Universidad de Amsterdam (UvA) / Instituto Nacional de Biodiversidad (INBio). 336 pp. Kappelle, M. 2001. Bosques Nublados de Costa Rica. In M. Kappelle and A.D. Brown, eds., Bosques Nublados del Neotrópico, 301– 70. Instituto Nacional de Biodiversidad (INBio) / Fundación Agroforestal del Noroeste de Argentina (FUA) / World Conservation Union (IUCN) / University of Amsterdam (IBED-UvA) / Laboratorio de Investigaciones Ecológicas los Yungas de Argentina (LIEY). Santo Domingo de Heredia, Costa Rica: Editorial INBio. Kappelle, M. 2004. Tropical montane forests. In J. Burley, J. Evans, and J.A. Youngquist, eds., Encyclopedia of Forest Sciences, vol. 4., Elsevier, 1782– 93. Oxford, UK. Kappelle, M. 2005. Bosques enanos subalpinos de Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 593– 605. Instituto Nacional de Biodiversidad (INBio) / The Nature Conservancy (TNC) / WOTRO Foundation. Santo Domingo de Heredia, Costa Rica: INBio Press. Kappelle, M., ed. 2006a. Ecology and Conservation of Neotropical Montane Oak Forests. Ecological Studies Series, vol. 185. Berlin: Springer Verlag. 483 pp. Kappelle, M. 2006b. Structure and composition of Costa Rican montane oak forests. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 127– 39. Ecological Studies Series, vol. 185. New York: Springer Verlag. Kappelle, M. 2006c. Changes in diversity and structure along a successional gradient in a Costa Rican montane oak forest. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 223– 33. Ecological Studies Series, vol. 185. New York: Springer Verlag.

The Montane Cloud Forests of the Cordillera de Talamanca 487 Kappelle, M. 2006d. Neotropical montane oak forests: overview and outlook. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 449– 67. Ecological Studies Series, vol. 185. New York: Springer Verlag. Kappelle, M. 2008. Biodiversity of the Oak Forests of Tropical America / Biodiversidad de los Bosques de Roble (Encino) de la América Tropical. Bilingual edition. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). 336 pp. Kappelle, M., G. Avertin, M.E. Juárez, and N. Zamora. 2000c. Useful plants within a campesino community in a Costa Rican montane cloud forest. Mountain Research and Development 20(2): 162– 71. Kappelle, M., and A.D. Brown, eds. 2001. Bosques Nublados del Neotrópico. Instituto Nacional de Biodiversidad (INBio) / Fundación Agroforestal del Noroeste de Argentina (FUA) / World Conservation Union (IUCN) / University of Amsterdam (IBED-UvA) / Laboratorio de Investigaciones Ecológicas los Yungas de Argentina (LIEY). Santo Domingo de Heredia, Costa Rica: INBio Press. 698 pp. Kappelle, M., and A.D. Brown. 2003. Mountain biodiversity in neotropical cloud forests: distribution, status and trends. In Status and Trends of, and Threats to, Mountain Biodiversity and Marine, Coastal and Inland Water Ecosystems: Abstracts of Poster Presentations at the Eighth Meeting of the Subsidiary Body on Scientific, Technical and Technological Advice of the Convention on Biological Diversity, CBD Technical Series No. 8, 54– 55. SBSTTA-8 Meeting held in Montreal, March 10– 14, 2003. Montreal, Canada: Secretariat of the Convention on Biological Diversity. Kappelle, M., A.M. Cleef, and A. Chaverri. 1989. Phytosociology of montane Chusquea-Quercus forests, Cordillera de Talamanca, Costa Rica. Brenesia 32: 73– 105. Kappelle, M., A.M. Cleef, and A. Chaverri. 1992. Phytogeography of Talamanca montane Quercus forests, Costa Rica. Journal of Biogeography 19(3): 299– 315. Kappelle, M., T. Geuze, M. Leal, and A.M. Cleef. 1996. Successional age and forest structure in a Costa Rican upper montane Quercus forest. Journal of Tropical Ecology 12: 681– 98. Kappelle, M., and L.D. Gómez. 1992. Distribution and diversity of montane pteridophytes of the Chirripó National Park, Costa Rica. Brenesia 37: 67– 77. Kappelle, M., and S.P. Horn, eds. 2005. Páramos de Costa Rica. Instituto Nacional de Biodiversidad (INBio) / The Nature Conservancy ( TNC) / WOTRO Foundation. Santo Domingo de Heredia, Costa Rica: INBio Press. 767 pp. Kappelle, M., and M.E. Juárez. 1994. The Los Santos Forest Reserve: a bufferzone vital for the Costa Rican La Amistad Biosphere Reserve. Environmental Conservation 21(2): 166– 69. Kappelle, M., and M.E. Juárez. 1995. Agroecological zonation along an altitudinal gradient in the montane belt of the Los Santos Forest Reserve in Costa Rica. Mountain Research and Development 15(1): 19– 37. Kappelle, M., and M.E. Juárez. 1997. Land use changes directed towards sustainable development in the Los Santos Forest Reserve, Costa Rica. George Wright Forum 14(3): 44– 53. Kappelle, M., and M.E. Juárez. 2000. Mountain forests, biodiversity and people in Costa Rica. In M. Price and N. Butt, eds., Forests in Sustainable Mountain Development: A State of Knowledge Report for 2000, 38– 46. IUFRO Research Series 5. Oxon, UK: CABI Publishing.

Kappelle, M., and M.E. Juárez. 2006. Land use, ethnobotany and conservation in Costa Rican montane oak forests. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 393– 406. Ecological Studies Series, vol. 185. New York: Springer Verlag. Kappelle, M., P.A.F. Kennis, and R.A.J. de Vries. 1995a. Changes in diversity along a successional gradient in a Costa Rican upper montane Quercus forest. Biodiversity and Conservation 4: 10– 34. Kappelle, M., and M.E. Leal. 1996. Changes in leaf morphology and foliar nutrient status along a successional gradient in a Costa Rican upper montane Quercus forest. Biotropica 28(2): 331– 44. Kappelle, M., and H.J.M. Sipman. 1992. Foliose and fruticose lichens of Talamanca montane Quercus forests, Costa Rica. Brenesia 37: 51– 58. Kappelle, M., and E. Van Omme. 1997. Lista de las plantas de los bosques nubosos subalpinos de la Cordillera de Talamanca en Costa Rica. Brenesia 47– 48: 55– 71. Kappelle, M., E. Van Omme, and M.E. Juárez. 2000b. Lista de la flora vascular terrestre de la cuenca superior del Río Savegre, San Gerardo de Dota, Costa Rica. Acta Botanica Mexicana 51: 1– 38. Kappelle, M., and J.G. van Uffelen. 2006. Montane oak forest distribution along temperature, humidity and soil gradients in Costa Rica. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 39– 54. Ecological Studies Series, vol. 185. New York: Springer Verlag. Kappelle, M., J.G. van Uffelen, and A.M. Cleef. 1995b. Altitudinal zonation of montane Quercus forests along two transects in the Chirripó National Park, Costa Rica. Vegetatio [Plant Ecology] 119: 119– 53. Kappelle, M., H.P. van Velzen, and W.H. Wijtzes. 1994. Plant communities of montane secondary vegetation in the Cordillera de Talamanca, Costa Rica. Phytocoenologia 22(4): 449– 84. Kappelle, M., M.M.I. van Vuuren, and P. Baas. 1999. Effects of climate change on biodiversity: a review and identification of key research issues. Biodiversity and Conservation 8: 1383– 97. Kappelle, M., and N. Zamora. 1995. Changes in woody species richness along an altitudinal gradient in Talamancan montane Quercus forests, Costa Rica. In S.P. Churchill, H. Balslev, E. Forero, and J.L. Luteyn, eds., Biodiversity and Conservation of Neotropical Montane Forests, 135– 148. Bronx, NY: The New York Botanical Garden. Kappelle, M., N. Zamora, and T. Flores. 1991. Flora leñosa de la zona alta (2000– 3819 m) de la Cordillera de Talamanca, Costa Rica. Brenesia 34: 121– 44. Karmalkar, A.V., R.S. Bradley, and H.F. Diaz. 2008. Climate change scenario for Costa Rican montane forests. Geophysical Research Letters 35: L11702. DOI: 10.1029/2008GL033940. Keighwin, L.D. 1982. Stable isotope stratigraphy and paleoceanography of sites 502 and 503. In W.L. Prell and J.V. Gardner, eds., Initial Reports of the Deep Sea Drilling Project LXVIII: 445– 53. Washington, DC: US Government Printing Office. Köhler, L. 2002. Die Bedeutung der Epiphyten im ökosystemaren Wasser- und Nährstoffumsatz verschiedener Altersstadien eines Bergregenwaldes in Costa Rica. Berichte des Forschungszentrums Waldökosysteme A: 181. Göttingen, Germany: University of Göttingen. Köhler, L., D. Hölscher, L.A. Bruijnzeel, and C. Leuschner. 2010. Epiphyte biomass in Costa Rican old-growth and secondary montane rain forests and its hydrologic significance. In L.A. Bruijnzeel, F.N. Scatena, and L.S. Hamilton, eds., Tropical Montane Cloud Forests:

488 Chapter 14 Science for Conservation and Management, 268– 74. Cambridge, UK: Cambridge University Press. Köhler, L., D. Hölscher, and C. Leuschner. 2006. Above-ground water and nutrient fluxes in three successional stages of montane oak forest with contrasting abundance of epiphytes in Costa Rica. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 271– 82. Ecological Studies Series, vol. 185. New York: Springer Verlag. Köhler, L., D. Hölscher, and C. Leuschner. 2008. High litterfall in oldgrowth and secondary upper montane forest of Costa Rica. Plant Ecology. DOI: 10.1007/s11258– 008– 9421– 2. Köhler, L., C. Tobón, K.F.A. Frumau, and L.A. Bruijnzeel. 2007. Biomass and water storage dynamics of epiphytes in old-growth and secondary montane cloud forest stands in Costa Rica. Plant Ecology 193: 171– 84. Kriebel, R. and F. Almeda. 2012. Five new species of Miconia (Melastomataceae: Miconieae) from Costa Rica and Panama. Harvard Papers in Botany 17(1): 53– 64. Landaeta, A., C.A. López, and A. Alvarado. 1978. Caracterización de la fracción mineral de suelos derivados de cenizas volcánicas de la Cordillera de Talamanca, Costa Rica. Agronomía Costarricense 2(2): 117– 29. Lanzewizki, T. 1991. Populationsökologische Untersuchungen an Kleinsäugern in einem Eichen-Wolkenwald (Quercus spp.) der Montanstufe Costa Ricas. Thesis, Philipps-Universität. Marburg, Germany. Laurance, W.F., D.C. Useche, L.P. Shoo, S.K. Herzog, M. Kessler, F. Escobar, G. Brehm, J.C. Axmacher, I.-C. Chen, L. Arrellano Gámez, P. Hietz, K. Fiedler, T. Pyrcz, J. Wolf, C.L. Merkord, C. Cardelus, A.R. Marshall, C. Ah-Peng, G.H. Aplet, M. del Coro Arizmendi, W.J. Baker, J. Barone, C.A. Brühl, R.W. Bussmann, D. Cicuzza, G. Eilu, M.E. Favila, A. Hemp, C. Hemp, J. Homeier, J. Hurtado, J. Jankowski, G. Kattán, J. Kluge, T. Krömer, D.C. Lees, M. Lehnert, J.T. Longino, J. Lovett, P.H. Martin, B.D. Patterson, R.G. Pearson, K.S.- H. Peh, B. Richardson, M. Richardson, M.J. Samways, F. Senbeta, T.B. Smith, T.M.A. Utteridge, J.E. Watkins, R. Wilson, S.E. Williams, and C.D. Thomas. 2011. Global warming, elevational ranges and the vulnerability of tropical biota. Biological Conservation 144(1): 548– 57. Lawton, R.O. 1980. Wind and the ontogeny of elfin stature in a Costa Rican lower montane rain forest. Ph. D. diss., University of Chicago. Chicago. Lawton, R.O. 1990. Canopy gaps and light penetration into a windexposed tropical lower montane rain forest. Canadian Journal of Forest Research 20: 659– 67. Leal, M.E., and M. Kappelle. 1994. Leaf anatomy of a secondary montane Quercus forest in Costa Rica. Revista de Biología Tropical 42(3): 473– 78. Leenders, T. 2001. A Guide to Amphibians and Reptiles of Costa Rica. Miami, FL: Zona Tropical. 305 pp. Lellinger, D.B. 1989. The Ferns and Fern-Allies of Costa Rica, Panama, and the Choco, Part I: Psilotaceae through Dicksoniaceae. Pteridologia 2A. The American Fern Society. 364 pp. Lines, N., and L.A. Fournier. 1979. Efecto alelopático de Cupressus lusitanica Mill. sobre la germinación de semillas de algunas hierbas. Revista de Biología Tropical 27: 223– 29. Lloyd, J.J. 1963. Tectonic history of the south Central American orogen. Memoir— American Association of Petroleum Geologists 2: 88– 100.

López-Barrera, F., and R.H. Manson. 2006. Ecology of acorn dispersal by small mammals in montane forests of Chiapas, Mexico. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 165– 76. Ecological Studies Series, vol. 185. New York: Springer Verlag. Lowman, M.L., and N.M. Nadkarni. 1995. Forest Canopies. San Diego, CA: Academic Press. Lücking, R. 1992. Foliicolous lichens— a contribution to the knowledge of the lichen flora of Costa Rica, Central America. Beihefte zur Nova Hedwigia 104: 1– 179. Madrigal, R., and E. Rojas. 1980. Manual Descriptivo del Mapa Geomorfológico de Costa Rica. Escala: 1:200,000. Oficina de Planificación Sectorial Agropecuario, Secretaría Ejecutiva de Planificación Sectorial Agropecuaria y de Recursos Naturales Renovables. San José, Costa Rica: IGN / MAG / FAO. Mehltreter, K.V. 1994. Biogeographie und Ökologie der Pteridophyten der Hochgebirge Costa Ricas. Dr. thesis, Universität Ulm. Ulm, Germany. 95 pp. Mehltreter, K.V. 1995. Species richness and geographical distribution of montane pteridophytes of Costa Rica, Central America. Feddes Repertorium 106(5– 8): 563– 84. Merker, C.A., W.R. Barbour, J.A. Scholten, and W.A. Dayton. 1943. The Forests of Costa Rica: A General Report on the Forest Resources of Costa Rica. Washington, DC: USDA Forest Service and Office of the Coordinator of Inter-American Affairs. 84 + 49 pp. Meza, T., and A. Bonilla. 1990. Áreas Naturales Protegidas de Costa Rica. Cartago, Costa Rica: Editorial Tecnológica de Costa Rica (ETCR). 318 pp. Miller, K., E. Chang, and N. Johnson. 2001. Defining Common Ground for the Mesoamerican Biological Corridor. World Resources Institute ( WRI). 45 pp. Monro, A.K., O. Chacón, N. Zamora, N. Brown, F. González, D. Santamaría, and M. Correa. 2009. Zonas de Biodiversidad del Parque Internacional La Amistad (PILA) Costa Rica-Panama. London, UK: The Natural History Museum, Instituto Nacional de Biodiversidad, and Universidad de Panamá. Mooring, M., J. Yee, C. Bryce, W. Taylor, and B. Perry. 2010. Savegre Valley Mammal Study: A Report of Preliminary Results. San Diego, CA: Point Loma Nazarene University. Mora Carpio, J. 2000. Atlas Geográfico del Área de Conservación La Amistad Pacífico ( ACLAP). Proyecto Proarca/Capas. San Isidro de Pérez Zeledón, Costa Rica: Ministerio de Ambiente y Energía (MINAE) / CCAD / USAID / SINAC / MINAE. 66 pp. Morales, J.F. 1998. Bromelias de Costa Rica. Santo Domingo de Heredia, Costa Rica: Editorial INBio. 180 pp. Morales, J.F., N. Zamora, and B. Herrera. 2007. Análisis de la vegetación en la franja altitudinal de 800– 1500 m.s.n.m. en la vertiente pacífica del Parque Internacional La Amistad (PILA), Costa Rica. Brenesia 68: 1– 15. Mueller, G.M., R.E. Halling, J. Carranza, M. Mata, and J.P. Schmit. 2006. Saprotrophic and ectomycorrizal macrofungi of Costa Rican oak forest. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 55– 68. Ecological Studies Series, vol. 185. New York: Springer Verlag. Mueller, G., and M. Mata. 2001. The Costa Rican National Fungal Inventory: A Large Scale Collaborative Project. Inoculum. Supplement to Mycologia 52 (5): 1– 4.

The Montane Cloud Forests of the Cordillera de Talamanca 489 Mulligan, M. 2010. Modelling the tropics-wide extent and distribution of cloud forest and cloud forest loss, with implications for conservation priority. In L.A. Bruijnzeel, F.N. Scatena, and L. S. Hamilton, eds., Tropical Montane Cloud Forests: Science for Conservation and Management. Cambridge, UK: Cambridge University Press. Myers, N., R.A Mittermeier, C.G. Mittermeier, G.A.B. da Fonseca, and J. Kent. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853– 58. Nadkarni, N.M. 1984. Epiphyte biomass and nutrient capital of a neotropical elfin forest. Biotropica 16: 249– 56. Nadkarni, N.M. 1985. Canopy Plants of the Monteverde Cloud Forest Reserve. San José, Costa Rica: Tropical Science Center ( TSC). Nadkarni, N.M. 1986. The effects of epiphytes on precipitation chemistry in a neotropical cloud forest. Selbyana 9: 47– 52. Nadkarni, N.M., and J.T. Longino. 1990. Invertebrates in canopy and ground organic matter in a neotropical montane forest. Biotropica 22: 286– 89. Nadkarni, N.M., and N. Wheelwright, eds. 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. New York: Oxford University Press. Naranjo, E.J., and C. Vaughan. 2000. Ampliación del ámbito altitudinal del tapir centroamericano (Tapirus bairdii ). Revista de Biología Tropical 48: 724. Nuhn, H. 1978. Atlas Preliminar de Costa Rica. Información Geográfica Regional. San José, Costa Rica: Instituto Geográfico Nacional (IGN) and Ofiplan. Obando, V. 2002. Biodiversidad en Costa Rica: Estado del Conocimiento y Gestión. Santo Domingo de Heredia, Costa Rica: INBio / SINAC. 81 pp. Oldeman, R.A.A. 1983. Tropical rain forest, architecture, silvigenesis and diversity. In S.L. Sutton, T.C. Whitmore, and A.C. Chadwick, eds., Tropical Rain Forest Ecology and Management, 139– 50. Oxford, UK: Blackwell. Olson, D.M., and E. Dinerstein. 2002. The Global 200: priority ecoregions for global conservation. Annals of the Missouri Botanical Garden 89: 199– 224. Oosterhoorn, M., and M. Kappelle. 2000. Vegetation structure and composition along an interior-edge-exterior gradient in a Costa Rican montane cloud forest. Forest Ecology and Management 126: 291– 307. Orozco, L. 1991. Estudio ecológico y de estructura horizontal de seis comunidades boscosas de la Cordillera de Talamanca, Costa Rica. Colección Silvicultura y Manejo de Bosques Naturales 2: 1– 34. Turrialba, Costa Rica: CATIE. Otárola, C.E., and A. Alvarado. 1976. Caracterización y clasificación de algunos suelos del Cerro de la Muerte, Talamanca, Costa Rica. Int. Rep. Fac. Agronomía. San Pedro, Costa Rica: Universidad de Costa Rica. 57 pp. Pedroni, L. 1991. Sobre la producción de carbón en los robledales de altura de Costa Rica. Colección Silvicultura y Manejo de Bosques Naturales 3: 1– 27. Turrialba, Costa Rica: CATIE. Pérez, S., A. Alvarado, and E. Ramírez. 1978. Manual Descriptivo del Mapa de Asociaciones de Subgrupos de Suelos de Costa Rica. Escala: 1:200,000. Oficina de Planificación Sectorial Agropecuario. San José, Costa Rica: IGN / MAG / FAO. Picado Twight, C. 1913. Les bromeliacees epiphytes. Bulletin des Sciences de France et Belgique 47: 215– 360.

Pittier, H. 1957. Ensayo Sobre las Plantas Usuales de Costa Rica. Segunda edición revisada. San Pedro de Montes de Oca, Costa Rica: Universidad de Costa Rica. 264 pp. Pohl, R.W. 1991. Blooming history of the Costa Rican bamboos. Revista de Biología Tropical 39(1): 111– 24. Pounds, J.A. 2001. Climate and amphibian declines. Nature 410: 639– 40. Pounds, J.A., M.R. Bustamante, L.A. Coloma, J.A. Consuegra, M.P.L. Fogden, P.N. Foster, E. La Marca, K.L. Masters, A. Merino-Viteri, R. Puschendorf, S.R. Ron, G.A. Sánchez-Azofeifa, C.J. Still, and B.E. Young. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439: 161– 67. DOI: 10.1038 /nature04246. Pounds, J.A., and M.L. Crump. 1994. Amphibian declines and climate disturbance: the case of the Golden Toad and the Harlequin Frog. Conservation Biology 8: 72– 85. Poveda, L.J., and M. Kappelle. 1992. Roldana scandens (Asteraceae), una especie nueva de arbusto escandente para Costa Rica. Brenesia 37: 157– 60. Powell, V.N.G., and R. Bjork. 1994. Implications of altitudinal migration for conservation strategies to protect tropical biodiversity: a case study of the resplendant quetzal Pharomachrus mocinno at Monteverde, Costa Rica. Conservation International 4: 161– 74. Reid, J.L., C.D. Mendenhall, J.A. Rosales, R.A. Zahawi, and K.D. Holl. 2014. Landscape context mediates avian habitat choice in tropical forest restoration. PLOS ONE 9(3): e90573.doi:10.1371/journal .pone.0090573. Rojas, A.F. 1999. Helechos Arborescentes de Costa Rica. Santo Domingo, Heredia, Costa Rica: Editorial INBio. 173 pp. Rojas, C., and S.L. Stephenson. 2007. Distribution and ecology of myxomycetes in the high-elevation oak forests of Cerro Bellavista, Costa Rica. Mycologia 99(4): 534– 43. Romero, C. 1999. Reduced-impact logging effects on commercial nonvascular pendant epiphyte biomass in a tropical montane forest in Costa Rica. Forest Ecology and Management 118: 117– 25. Sánchez, J. 2002. Aves del Parque Nacional Tapantí, Costa Rica. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). 235 pp. Savage, J.M. 2002. The Amphibians and Reptiles of Costa Rica. Chicago: University of Chicago Press. 934 pp. Savage, J.M., and J. Villa. 1986. Introduction to the Herpetofauna of Costa Rica. Contributions to Herpetology, No. 3. Athens, OH: Society for the Study of Amphibians and Reptiles. Schubel, R.J. 1972. A Preliminary Study of Charcoal Making in the Talamanca Mountains of Costa Rica. Technical Report. San Pedro de Montes de Oca, Costa Rica: Organization for Tropical Studies (OTS). 7 pp. Schubel, R.J. 1980. The Human Impact on a Montane Oakforest, Costa Rica. PhD thesis, University of California at Los Angeles (UCLA). Los Angeles, CA. Schubert, R., R. Lücking, and H.T. Lumbsch. 2003. New species of foliicolous lichens from “La Amistad” Biosphere Reserve, Costa Rica. Willdenowia 33: 459– 65. Scott, N.J., and S. Limerick. 1983. Reptiles and amphibians. In D.H. Janzen, ed., Costa Rican Natural History, 351– 74. Chicago: University of Chicago Press. Seyfried, H., A. Astorga, and C. Calvo. 1987. Sequence stratigraphy of

490 Chapter 14 deep and shallow water deposits from an evolving island arc: the upper cretaceous and tertiary of Central America. Facies 17: 203– 14. Siles de Guerrero, G. 1980. Estudio Socioeconómico y Técnico de Productores de Carbón y Recolectores de Mora y Lana en las Reservas de Río Macho y Los Santos. Informe Técnico 10. San José, Costa Rica: Ministerio de Agricultura y Ganadería (MAG). 32 pp. Sillett, T.S. 1994. Foraging ecology of epiphyte-searching insectivorous birds in Costa Rica. Condor 96: 863– 77. Sipman, H.J.M. 2006. Diversity and biogeography of lichens in Neotropical montane oak forests. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 69– 81. Ecological Studies Series, vol. 185. New York: Springer Verlag. Smith, N.J.H., J.T. Williams, and D.L. Plucknett. 1991. Conserving the tropical Cornucopia. Environment 33(6): 7– 9 + 30– 32. Smith, N.J.H., J.T. Williams, D.L. Plucknett, and J.P. Talbot. 1992. Tropical Forests and Their Crops. Ithaca, NY: Comstock Publishing Associates (Cornell University Press). 568 pp. Solórzano, A. 2004. Serpientes de Costa Rica. Santo Domingo de Heredia, Costa Rica: Editorial INBio. 791 pp. Solórzano, S., A.J. Baker, and K. Oyama. 2004. Conservation Priorities for Resplendant Quetzals based on analysis of mitochondrial DNA control-region sequences. Condor 106: 449– 56. Stadtmüller, T. 1987. Los Bosques Nublados en el Trópico Húmedo. Turrialba: University of the United Nations ( Tokyo) and Centro Agronómico Tropical de Investigación y Enseñanza (CATIE). 85 pp. Stadtmüller, T., and R. aus der Beek. 1992. Development of forest management techniques for tropical high mountain primary oakbamboo forest. In F.R. Miller and K.L. Adam, eds., Wise Management of Tropical Forests: Proceedings of the Oxford Conference of Tropical Forests, 245– 59. Oxford, UK: Oxford Forestry Institute, University of Oxford. Standley, P.C. 1937. Flora of Costa Rica. Field Museum of Natural History Botanical Series 18: 1– 1571. Stehli, F.G., and S.D. Webb, eds. 1985. The Great American Biotic Interchange. New York: Plenum Press. Stiles, F.G. 1985. Conservation of forest birds in Costa Rica: problems and perspectives. In A.W. Diamond and T.E. Lovejoy, eds., Conservation of Tropical Forest Birds, 141– 68. Cambridge, UK: International Council for Bird Preservation. Stiles, F.G., A.F. Skutch, and D. Gardner. 1989. A Guide to the Birds of Costa Rica. Ithaca, NY: Cornell University Press. Takhtajan, A.L. 1986. Floristic Regions of the World. Translated by T.J. Crovello and A. Cronquist. Los Angeles, CA: University of California Press. Talamancan-Caribbean Biological Corridor Commission and The Nature Conservancy (TNC). 1993. Work Report Phase 1 of the TalamancanCaribbean Biological Corridor Project. With five annexes. Limón, Costa Rica: Talamancan-Caribbean Biological Corridor Commission / The Nature Conservancy ( TNC). Tanner, E.V.J., P.M. Vitousek, and E. Cuevas. 1998. Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79: 10– 22. Tavares de Almeida, R. 2000. Evaluando y Valorizando las Áreas Silvestres Protegidas para la Conservación del Jaguar en Mesoamérica: Costa Rica, Área de Conservación La Amistad Pacífico. Ministerio de Ambiente y Energía (MINAE) and Instituto Nacional de Biodi-

versidad (INBio). San José, Costa Rica: Universidad Latina de Costa Rica. 63 pp. Ten Hoopen, G.M., and M. Kappelle. 2006. Soil seed bank size and composition in disturbed and old growth montane oak forests in Costa Rica. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 299– 308. Ecological Studies Series, vol. 185. New York: Springer Verlag. Tobler, M.W. 2002. Habitat use and diet of Baird’s tapirs (Tapirus bairdii) in a montane cloud forest of the Cordillera de Talamanca, Costa Rica. Biotropica 34(3): 468– 74. Tobler, M.W., E.J. Naranjo, and I. Lira-Torres. 2006. Habitat preference, feeding habits and conservation of Baird’s Tapir in Neotropical montane oak forests. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 347– 59. Ecological Studies Series, vol. 185. New York: Springer Verlag. Tosi, J.A., Jr. 1969. Mapa Ecológico de Costa Rica, Basado en la Clasificación Vegetal Mundial de L.R. Holdridge. Escala: 1:750,000. San José, Costa Rica: Centro Científico Tropical (CCT). Tournon, J., and G. Alvarado. 1997. Mapa Geológico de Costa Rica. Escala: 1:500,000. Cartago, Costa Rica: Editorial Tecnológico de Costa Rica. Ureña, A. 1990. Reseña Histórica del Cantón de Dota. San José, Costa Rica: Editorial Serrano Elizondo. 379 pp. Ureña, E. 1941. Monografía de Santa María de Dota. Revista del Archivo Nacional de Costa Rica 5(1– 2): 69– 85. Valerio, C.E. 1999. Costa Rica: Ambiente y Biodiversidad. Santo Domingo de Heredia, Costa Rica: Editorial INBio. 139 pp. Van den Bergh, M.B., and M. Kappelle. 1998. Diversity and distribution of small terrestrial rodents along a disturbance gradient in montane Costa Rica. Revista de Biología Tropical 46(2): 331– 38. Van den Bergh, M., and M. Kappelle. 2006. Diversity and distribution of small terrestrial rodents in disturbed and old growth montane oak forests in Costa Rica. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 337– 45. Ecological Studies Series, vol. 185. New York: Springer Verlag. Van Dunné, H.J.F., and M. Kappelle. 1998. Biomass-diversity relations of epiphytic bryophytes on small Quercus copeyensis stems in a Costa Rican montane cloud forest. Revista de Biología Tropical 46(2): 35– 42. Van Leeuwen, E.M.M. 1988. Estudios Preliminares de Estructura y Dinámica de un Bosque Robledal (Quercus costaricensis Liebmann) en las Montanas Altas de la Cordillera de Talamanca, Costa Rica. M.Sc. thesis, Wageningen Agricultural University. Wageningen, Netherlands. 73 pp. Van Omme, E., M. Kappelle, and M.E. Juárez. 1997. Land cover/use changes and deforestation trends over 55 years (1941– 1996) in a Costa Rican montane cloud forest watershed area. In ISSS, AISB, IBG, and ITC, eds., Abstracts of the 1997 Conference on Geo-Information for Sustainable Land Management. Enschede, The Netherlands: ITC. Van Uffelen, J.G. 1991. A geological, geomorphological and soil transect study of the Chirripó Massif and adjacent areas, Cordillera de Talamanca, Costa Rica. M.Sc. thesis, Wageningen Agricultural University. Wageningen, The Netherlands. Van Velzen, H.P., W.H. Wijtzes, and M. Kappelle. 1993. Lista de especies de la vegetación secundaria del piso montano pacífico, Cordillera de Talamanca, Costa Rica. Brenesia 39– 40: 147– 61.

The Montane Cloud Forests of the Cordillera de Talamanca 491 Vargas, A. 2010. Roble de Dota es el Árbol Excepcional del 2010. La Nación, Saturday, June 12, 2010, 18. Vásquez, A. 1983. Soils. In D.H. Janzen, ed., Costa Rican Natural History, 63– 65. Chicago: University of Chicago Press. Veneklaas, E.J. 1990. Rainfall Interception and Above-ground Nutrient Fluxes in Colombian Montane Tropical Rain Forest. PhD thesis, Utrecht University. Utrecht, Netherlands. 109 pp. Vernes, J.R. 1992. Biosphere Reserves: Relations with Natural Heritage Sites. Parks (IUCN) 3(3): 29– 34. Vial, J.L. 1968. The ecology of the tropical salamander Bolitoglossa subpalmata in Costa Rica. Revista de Biología Tropical 15: 13– 115. Wagner, W.H., and L.D. Gómez. 1983. Pteridophytes. In D.H. Janzen, ed., Costa Rican Natural History, 311– 18. Chicago: University of Chicago Press. Webb, L.J. 1959. A physiognomic classification of Australian rain forests. Journal of Ecology 47: 551– 70. Weber, H. 1958. Die Páramos von Costa Rica und Ihre pflanzengeographische Verkettung mit den Hochanden Südamerikas. Akademie der Wissenschaften, Abhandlungen der MathematischNaturwissenschaftlichen Klasse 1956: 120– 94. Weber, H. 1959. Los páramos de Costa Rica y su concatenación fitogeográfica con los Andes Sudamericanos. San José, Costa Rica: Instituto Geográfico Nacional (IGN). Wercklé, C. 1909. La subregión fitogeográfica costarricense. San José, Costa Rica: Sociedad Nacional de Agricultura, Tipografía Nacional. 55 pp. Wesselingh, R.A. 1998. Plant reproduction and pollination in a tropical montane forest in Costa Rica. Acta Botanica Neerlandica 47(1): 155. Wesselingh, R.A., H.C.M. Burgers, and J.C.M. den Nijs. 2000. Bumblebee pollination of understory shrub species in a tropical montane forest in Costa Rica. Journal of Tropical Ecology 16(5): 657– 72. Wesselingh, R.A., M. Witteveldt, J. Morissette, and H.C.M. den Nijs 1999. Reproductive ecology of understory species in a tropical montane forest in Costa Rica. Biotropica 31(4): 637– 45. Weyl, R. 1955. Contribución a la geología de la Cordillera de Talamanca. San José, Costa Rica: Instituto Geográfico Nacional (IGN). 77 pp.

Weyl, R. 1980. Geology of Central America. Stuttgart, Germany: Gebr. Borntraeger. Whitmore, T.C. 1990. An Introduction to Tropical Rain Forests. Oxford, UK: Clarendon. 226 pp. Widmer, Y. 1993. Bamboo and gaps in the oak forests of the Cordillera de Talamanca, Costa Rica. Verhandlungen der Gesellschaft für Ökologie (Freising) 22: 329– 32. Widmer, Y. 1994. Distribution and flowering of six Chusquea bamboos in the Cordillera de Talamanca, Costa Rica. Brenesia 41– 42: 45– 57. Widmer, Y. 1998. Pattern and performance of understory bamboos (Chusquea spp.) under different canopy closures in old-growth oak forests in Costa Rica. Biotropica 30(3): 400– 415. Widmer, Y., and L.G. Clark. 1991. New species of Chusquea (Poaceae: Bambusoideae) from Costa Rica. Annals of the Missouri Botanical Garden 78: 164– 71. Wijtzes, W.H. 1990. Dispersal strategies of upper montane primary forest and secondary vegetation on the Pacific side of the Cordillera de Talamanca, Costa Rica. Technical Report. Amsterdam: Hugo de Vries Laboratory, University of Amsterdam. Wilms, J.J.A.M., and M. Kappelle. 2006. Frugivorous birds and seed dispersal in disturbed and old growth montane oak forests in Costa Rica. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 309– 24. Ecological Studies Series, vol. 185. New York: Springer Verlag. Wolf, J.H.D. 1993. Diversity patterns and biomass of epiphytic bryophytes and lichens along an altitudinal gradient in the Northern Andes. Annals of the Missouri Botanical Garden 80(4): 928– 60. Wolf, J.H.D. 1994. Factors controlling the distribution of vascular and non-vascular epiphytes in the northern Andes. Vegetatio 112: 15– 28. Zadroga, F. 1981. The hydrological importance of a montane cloud forest area of Costa Rica. In R. Lal and E.W. Russell, eds., Tropical Agricultural Hydrology, 59– 73. New York: J. Wiley.

Chapter 15 The Páramo Ecosystem of Costa Rica’s Highlands

Maarten Kappelle1,2,* and Sally P. Horn2

Definition and Global Distribution of Páramos Páramo is a grass- or shrub-dominated ecosystem that occupies the cool and wet upper slopes of tropical mountains, at alpine elevations above the timber or tree line and below the snow limit, if present (Cuatrecasas 1968, Cleef 1981, Monasterio and Vuilleumier 1986, Luteyn 1999, Hofstede et al. 2003). At the global level, páramos belong to the biome or major habitat type known as Tropical Montane Grasslands and Shrublands (Olson et al. 2001, Hoekstra et al. 2005), which, in structure and physiognomy, is similar to the arctic tundra biome, although páramos are characterized by large diurnal, rather than annual, shifts in temperature. Páramos in the broadest sense of the biome are found in Latin America (Cuatrecasas 1958, Cleef 1981, Luteyn 1999), Africa (Hedberg 1964, 1992), and Southeast Asia (Smith and Cleef 1988, Hope et al. 2003). In Africa, the term “afroalpine” is used to refer to the páramo zone (“moorlands”) along the slopes of Mt. Kilimanjaro (5,895 m elevation), Mt. Kenya (5,199 m), Mt. Elgon (4,321 m), Mt. Rwenzori (5,109 m), and the high mountains of Ethiopia (to 4,550 m) (Hedberg 1964, 1992, Beck et al. 1981), while in Asia the term “tropical alpine” is most common, particularly on 4,884 m high Mt. Jaya (Mt. Carstenz), Irian Jaya, Indonesia, and Mt. Wilhelm (4,509 m), Papua New Guinea (Van Royen 1980, Smith and Cleef 1988, Hnatiuk 1994, Rundel et al. 1994a,b, Johns et al. 2006). Though species groups differ by continent, a number of plant families (e.g., Asteraceae and Ericaceae) and plant growth forms (e.g., 1 World Wide Fund for Nature (WWF International), Avenue du MontBlanc 1196, Gland, Switzerland 2 Department of Geography, University of Tennessee, Knoxville, TN, USA * Corresponding author

492

stem rosettes, tussock grasses, and cushion plants) occur in tropical alpine ecosystems around the globe (Smith and Cleef 1988, Luteyn 1992, Hofstede et al. 2003). In Latin America, páramos are mainly restricted to the latitudinal zone between the parallels of 11ºN and 8ºS (Cuatrecasas 1979, Luteyn 1999), where they cover some 35,000 km2 (Hofstede et al. 2003) (Fig. 15.1). In Central America, they occur in Costa Rica (Fig. 15.2) and Panama (Weber 1958, Luteyn 1999, Kappelle 2003, Kappelle and Horn 2005, Samudio and Pino 2006), where they have been termed “Isthmian Páramos” (Vargas and Sánchez 2005) to distinguish them from their Andean equivalents (Luteyn 1999). In the Andean cordilleras of South America páramos occur on high peaks and plateaus in Venezuela (Salgado-Laboriau 1979, 1980, Monasterio 1980, Monasterio and Molinillo 2003, Vareschi 1970, 1992), Colombia (Cuatrecasas 1958, 1968, Cleef 1981, Sturm and Rangel 1985, Rangel 2000), and Ecuador (Mena et al. 2001). Continuing southward, the biome extends to the Huancabamba depression in northern Peru (Brack and Mendiola 2000, Recharte et al. 2002, Mostacero et al. 2007), where páramo takes the form of a drier tussock grass community, the jalca (Sarmiento 2007). Some of the highest Andean peaks with páramo vegetation on their slopes are Mt. Chimborazo (6,310 m), Mt. Cotopaxi (5,896 m), and Mt. Cayambe (5,840 m) in Ecuador, the “twin peaks” of Cristóbal Colón (5,776 m) and Simón Bolívar (5,776 m) in the isolated Santa Marta Mountains in northern Colombia, Mt. Nevado El Ruiz in central Colombia (5,335 m), and Pico Bolivar (5,007 m) in the Venezuelan Cordillera de Mérida. An interesting example of non-Andean páramo or páramo-like vegetation occurs in coastal Brazil, on the mountain summits in the Atlantic Forest region where

The Páramo Ecosystem of Costa Rica’s Highlands 493 Fig. 15.1 The distribution of páramo vegetation in Central America and the northern Andes. The black shading indicates elevations above 3,000 m that are potentially páramo, as originally mapped by Jim Luteyn. Modified from Luteyn 1999 with the permission of the author. Originally published in Horn and Kappelle (2009) and reprinted with the permission of Springer.

Safford (1999a,b) has carried out detailed studies of vegetation dynamics following fires. Full understanding of the affinity of these highland ecosystems with Andean-centered páramos awaits more detailed botanical study (A.M. Cleef, pers. comm.). These Brazilian coastal mountain páramos may potentially show more floristic similarity with nonpáramo vegetation on elevated sandstone plateaus in the Amazon basin of Colombia and Venezuela (Cleef and Duivenvoorden 1994). Neotropical alpine ecosystems that are similar to Andean and Isthmian páramo, though much drier and less species-rich, are found at northern latitudes in Guatemala on the Tajamulco Volcano (at 4,220 m the highest point in Central America), the Tacaná Volcano (4,110 m), and the high peaks of the Altos de Chiantla in the Sierra de los Cuchumatanes (Hastenrath 1968, Islebe and Kappelle 1994, Islebe and Cleef 1995, Steinberg and Taylor 2008), as well as in Mexico along the slopes of the volcanoes Citlaltepetl

(Pico de Orizaba, 5,754 m), Popocatépetl (5,452 m), and Iztaccíhuatl (5,286 m) (Beaman 1959, Hastenrath 1968, Rzedowski 1978, Almeida et al. 1994). These alpine meadows are often dominated by bunch grasses and are locally known as zacatonales (“zacate” means grass in the Aztec language Nahuatl). Steinberg and Taylor (2008) consider the zacatonales in the Sierra de los Cuchumatanes to be páramo grasslands, but most researchers place the northern limit of true páramo in Costa Rica (Kappelle and Horn 2005). Beginning at approximately 8ºS and extending to 30°S, neotropical wet páramo is replaced by arid puna ecosystems characterized by low precipitation, cold temperatures, and sparse, species-poor vegetation of low stature (Cabrera 1968, Quintanilla 1983). The puna stretches over a high plateau (altiplano) and covers the Andean slopes of central and southern Peru, Bolivia, northern Chile, and northwestern Argentina.

494 Chapter 15

Isthmian and Andean páramos have their lowest altitudinal occurrences close to 3,000 m on smaller mountains and around 3,500 m on higher peaks, where— under natural conditions— they border montane (Andean) or subalpine (elfin) closed-canopy forests (Luteyn et al. 1992, Luteyn 1999, Kappelle and Brown 2001, Kappelle 2005d). In Costa Rica the transition from closed-canopy montane forest to alpine, treeless páramo vegetation occurs at around

3,100 m on the Buenavista massif of the Cordillera de Talamanca (informally known as the “Cerro de la Muerte”; Fig. 15.3), and near ca. 3,300 m on the higher Chirripó massif, with variations between windward and leeward slopes (Weber 1959, Kappelle 1991, 1992, Chaverri 2008), and at some sites between burned and unburned mountainsides (Chaverri et al. 1976). On high mountains in the Andes, neotropical páramos

Fig. 15.2 Map showing the main peaks covered by páramo and the location of protected areas that conserve páramo ecosystems in the Costa Rican highlands. Map prepared by Marco V. Castro.

The Páramo Ecosystem of Costa Rica’s Highlands 495

Fig. 15.3 View of the Buenavista massif (Cerro de la Muerte), looking towards the southeast with the town of Quepos visible in the distance. Photograph by Carlos Serrano.

have their upper limits between 4,500 and 5,000 m elevation, where they border the nival belt characterized by snow-capped peaks (Cuatrecasas 1958, Weber 1958, Troll 1959, 1968, Cleef 1981, Sturm and Rangel 1985, Luteyn 1999). On lower neotropical mountains with peaks between 3,000 to 4,500 m, as in Costa Rica and Panama, páramos may lack the fully developed upper páramo belt known as superpáramo (Chaverri and Cleef 1996, 2005, Kappelle et al. 2005b). The páramo landscape in Costa Rica underwent repeated glaciation during the late Quaternary (Weyl 1955a, Hastenrath 1973, Horn 1990a, Orvis and Horn 2000, Lachniet and Seltzer 2002), as did Andean páramos (e.g., Smith et al. 2005). The buildup, advance, and subsequent decay of valley glaciers and small ice caps throughout the highland neotropics shaped páramo landscapes during repeated cycles of cooling and warming. In Costa Rica the effects of past glaciation are particularly evident on the Chirripó massif, where glacial erosion and deposition left behind a picturesque alpine landscape dotted by over 30 glacial lakes (Horn et al. 1999, 2005; Fig. 15.4; see also Horn and

Haberyan in this volume). Páramo lakes in Costa Rica, as throughout the Andes, form the headwaters of major rivers upon which lowland populations depend (Luteyn 1999).

History of Scientific Exploration in Costa Rican Páramos Scientific exploration of Costa Rican páramos by European and North American scholars started at the end of the nineteenth century when a first geological profile of the páramodotted Cordillera de Talamanca was prepared by geologist Robert T. Hill (1898). He based his ideas on observations previously made by paleontologist William M. Gabb (Gabb 1874a,b, 1895) who had visited Costa Rica after being hired in 1873 by entrepreneur Minor C. Keith, who led the construction of the railroad between Puerto Limón and San José (Denyer and Soto 1999). According to Swiss botanist Henri F. Pittier (1891), Costa Rica’s highest peak, Cerro Chirripó, was still completely unexplored at that time. In Guatemala, however, German naturalist Moritz F. Wagner

The Páramo Ecosystem of Costa Rica’s Highlands 497

(1866) had already noted the presence of tropical alpine vegetation on that country’s highest mountains. Costa Rica’s páramo-covered peaks were believed to be sacred by the indigenous peoples of the area, the Cabécar and Bri-Bri tribes (Stone 1961). For that reason, the peaks were still mostly unexplored upon the arrival of the Spanish colonists in the early sixteenth century, although indigenous trails existed across the Talamancan mountain range, and were used by early explorers crossing from the Atlantic to the Pacific slope and vice versa (Gomez 2005a). The first non-indigenous explorer to ascend the summit of Cerro Chirripó was likely the German priest and missionary Agustín Blessing Presinger, who climbed the peak in 1904 (Kohkemper 1968, Gómez 2005a). Five years later, though, the botanist Karl Wercklé (1909) stated that alpine páramo vegetation was absent in Costa Rica. However, Wercklé did report the presence of some alpine plant life forms— samples of which are still stored in Costa Rica’s National Herbarium— in the more accessible northwestern sector of the Cordillera de Talamanca (Gómez 1978). The area Karl Wercklé visited was today’s Dota County, which includes Cerro de las Vueltas, previously known as Páramo del Abejonal, and other peaks of the Buenavista massif (Gómez 2005a). Wercklé stressed the need for further exploration to confirm this assumption (Gómez 1978). Apparently, Wercklé had not met with Blessing or heard about the impressions from his visit to Chirripó’s peak (Gómez 2005a). In 1920, the American mining geologist Wickland and German colleague Ruin made the first geological journey to the Chirripó páramo, for the purpose of collecting rock samples. They were followed by the Swiss botanist Walter Kupper, who ascended the high peaks in 1932 and collected the first plant specimens (Kohkemper 1968, Grayum et al. 2004). These specimens were later identified and described as species new to science by German taxonomist Karl Süssenguth (1942). Only five years later, the US botanist Paul Standley (1937) of Chicago’s Field Museum was the first to note the significant similarity between the flora of Costa Rica’s páramo and the plant species composition of highland Andean South America (Gómez 2005a). Standley was able Fig. 15.4 Photo mosaic of the Chirripo páramo, showing evidence of past glaciation. Clockwise from upper left: Lago Chirripó, a glacial tarn occupying a bedrock basin in the cirque floor at the head of the Valle de los Lagos, and two downstream tarns dammed by rock thresholds; Cerro Chirripó, a glacial horn produced by the headward erosion of glaciers in three cirques; glacial striations in the Valle Talari; Lago de las Morrenas 1, the largest lake in the Valle de las Morrenas, also a tarn quarried into bedrock (see also Figs. 19.7 and 19.8 in chapter 19 of this volume, by Horn and Haberyan); the U-shaped valley carved by the Pirámide glacier, on the eastern flank of Cerro Chirripó; glacially smoothed rock exposure in the upper Valle Talari ( Valle de los Conejos). Photo credits— Lake photographs by Chad Lane, others by Sally Horn. (Photo of U-shaped valley carved by the Pirámide glacier from Lachniet and Seltzer 2002.)

to reject Wercklé’s hypothesis that no páramo was present in Costa Rica. German geologist Richard H. Weyl visited Cerro Chirripó in 1955, accompanied by Hannes Ihrig, and prepared a first map of the Chirripó massif (Gómez 2005a). Together with Costa Rican engineer Féderico Gutiérrez Braun he made a reconnaissance flight and gave names to several high peaks (Gutiérrez-Braun 1955). Weyl (1955a,b, 1956a,b, 1957) was the first to report evidence of past glaciation on the massif; his initial observations of glacial features have been confirmed and extended through field studies by other earth scientists (e.g., Hastenrath 1973, Horn 1990a, Orvis and Horn 2000, 2005, Lachniet and Seltzer 2002, Lachniet et al. 2005). In the same period that Weyl conducted his geological research, German botanist Hans Weber visited Chirripó with Alfonso Jiménez Muñoz, at that time curator at Costa Rica’s National Herbarium (Gómez 2005a). Weber studied Chirripó’s páramo flora in detail (Grayum et al. 2004) and produced an extensive report on his botanical observations (Weber 1958, 1959). In his publications he stressed the striking floristic affinity between Costa Rica’s (isthmian) páramo and its Andean equivalents, reconfirming Paul Standley’s earlier conclusion. Weber’s botanical account marked a change in the study of Costa Rican páramos, catalyzing field trips aimed at the collection and description of flowering plants, ferns, lichens, and fungi (Gómez 2005a). Between 1963 and 1968, Costa Rican botanist Luis Diego Gómez Pignataro— to whom this book is dedicated— organized a series of botanical collection trips to the Buenavista (or Cerro de la Muerte) massif (including the 3,491 m high Cerro Buenavista), Cerro Cuericí (also known as Cerro Chirripocillo), Cerro Urán, and Cerro Chirripó (Kohkemper 1968, Gómez 1986). Luis Gómez was inspired by Warren Herbert Wagner Jr., who in 1967 taught him pteridology on field trips to Cerro de la Muerte, during which Gómez collected, identified, and listed numerous fern species (Gómez 1978, Gómez 1994a,b). On several of his later trips Gómez was accompanied by Australian-based, US-born botanist Arthur S. Weston, who collected several thousand plant specimens in the páramos over repeated visits in the 1970s. Among his collections was a new genus, Westoniella, in the Asteraceae (Cuatrecasas 1977), which has 5 species in Costa Rica (four of which are endemic) and 2 in Panama. Weston is among only a handful of botanists to have visited and collected on the more remote páramo-covered peaks in Southeast Costa Rica, including Mts. (or cerros) Amo, Dúrika, Dudu, and Kámuk, as well as on nearby Panamanian Cerro Fábrega. Weston described his observations of the páramo flora of these previously unexplored mountains in two highly valu-

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able, unpublished reports (Weston 1981a,b). Meanwhile, in 1966, Austrian limnologist Heinz Löffler ascended the Chirripó massif to study its glacial lakes (Löffler 1972). His example was followed by German marine ecologist Klaus Gocke, whose expedition by helicopter to the Chirripó páramo focused on the limnology of the largest glacial lake, Lago Chirripó (Gocke et al. 1981; see Horn and Haberyan, chapter 19 of this volume). On a second series of botanical surveys between 1982 and 1984, Luis Diego Gómez was joined by a botanist from Missouri Botanical Garden, Gerrit Davidse. These expeditions focused on the more remote páramos in the Talamancan range, including the zones around Mts. Dúrika and Fábrega (the latter in Panama). Gómez, Davidse, and colleague Gerardo Herrera discovered dozens of species new to science as part of their field work (Gómez 1986, Grayum et al. 2004). University of Pennsylvania biologist Daniel H. Janzen was the first to report on the impact of fires on Costa Rican páramo vegetation, on the basis of field study of a small

fire on the Buenavista massif (Janzen 1973). In 1976, Costa Rican biologist Adelaida Chaverri Polini and collaborators investigated the immediate aftermath of a very large (>5,000 ha) wildfire that burned nearly the entire Chirripó páramo and large areas of adjacent forest in March 1976 (Chaverri et al. 1976; Fig. 15.5). The burned area had been established as a national park only the year before (Boza 1988), with strategic and technical support from Chaverri and associates (Wallace 1992, Chaverri and Esquivel 2005). Chaverri’s pioneering work in Chirripó National Park and the Buenavista massif in the 1970s (for an overview, see Kappelle and Cleef 2003, 2004a,b) triggered a series of other páramo studies with emphasis on vegetation composition and fire ecology and history, by Williamson et al. (1986) and University of Tennessee geographer Sally Horn (Horn 1988, 1989a,b,c, 1990b, 1991). Since then, Horn and collaborators, including Ken Orvis, Kurt Haberyan, and students, have intensified the study of the páramo’s past and present environment, coupling work on the dynamics and history of fire and vegetation with

Fig. 15.5 Burned páramo vegetation in the Valle de las Morrenas, Parque Nacional Chirripó. Photograph taken in 1976 by the late Adelaida Chaverri (courtesy Catalina Vaughan Chaverri).

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research on limnology, geomorphology, and paleoclimate (Horn 1990a, 1992, 1993, 1997, 1998a,b, 2005, Horn and Haberyan 1993, Horn and League 2005, Horn and Sanford 1992, Horn et al. 1999, 2005, Haberyan and Horn 1999, Haberyan et al. 1995, 1997, 2003, League and Horn 2000, Orvis and Horn 2000, 2005, Kappelle et al. 2005a, Lane et al. 2011, Horn and Lane 2013). In the early 1980s Adelaida Chaverri teamed up with two Dutch ecologists from the University of Amsterdam, Antoine M. Cleef and Maarten Kappelle (Grayum et al. 2004), with whom she carried out a number of investigations on the floristic composition and plant geography of Costa Rican páramos and adjacent oak forests (Chaverri and Cleef 1996, 2005, Cleef and Chaverri 1992, 2005, Kappelle et al. 1989, 1992). Additionally, she collaborated in the preparation of the first management plan for the páramos of the Chirripó National Park (Bravo et al. 1991), and subsequently analyzed its status, strengths, and flaws during the 1990s (Chaverri and Esquivel 2005, Chaverri 2008). During the 1990s, Chaverri, Cleef, and Kappelle, in collaboration with other Costa Rican and Dutch scientists, developed a vibrant high-altitude ecological research program (ECOMA) at the Universidad Nacional (UNA) that generated a body of knowledge on Costa Rican páramo biogeography (Cleef and Chaverri 1992, Islebe and Kappelle 1994), paleoclimate and vegetation history (Hooghiemstra et al. 1992, Islebe 1996, Islebe and Hooghiemstra 1997, Islebe et al. 1995a,b, 1996, 2005), soils (van Uffelen 1991, Kappelle and van Uffelen 2005), plant communities and their distribution (Kappelle 1991, Badilla and Kappelle 1992, Chaverri and Cleef 1996, Kappelle et al. 2005b, Brak et al. 2005), the vascular flora (Kappelle et al. 1991, 2000, Kappelle and Van Omme 1997), bryophytes (Gradstein and Holz 2005), algae (Kappelle et al. 2005a), and lichens (Sipman 1999, 2005). Over the past twenty-five years, other scientists, based at the Universidad de Costa Rica (UCR) and the Instituto Nacional de Biodiversidad (INBio) in Costa Rica and at US and European universities, have contributed considerably to knowledge of páramo ecosystems and environments with studies addressing, for instance, geology and geomorphology (e.g., Calvo 1987, Obando 2004, Lachniet and Seltzer 2002), flowering plants (Vargas 1987, Alfaro and Gamboa 1999), ferns (Barrington 2005), birds (Barrantes 2005), mollusks (Barrientos 2005), and insects (Barrientos and Monge 1995). An important research group around German botanist Focko Weberling assessed in detail the growth forms of a number of páramo plant species belonging to the Apiaceae and Escalloniaceae (Wiedmann and Weberling 1993), Asteraceae and Clusiaceae (Weberling and Weberling 1993), Ericaceae (Schneidt and Weberling 1993,

Schneidt et al. 1996), and Rosaceae and Poaceae (Stein and Weberling 1992). It is hoped that over the next decade a new generation of scientists will arise and conduct multidisciplinary research in the Costa Rican páramos with the aim of informing conservation strategies needed to preserve this unique and highly diverse wet tropical alpine ecosystem in the face of increasing visitation to páramos and population and land use pressure in surrounding forests (Chaverri 2008).

Geographic Distribution and Altitudinal Zonation in Costa Rica The isthmian páramos of Costa Rica and Panama form part of the Mesoamerican biodiversity hotspot, one of the 25 most important such areas on Earth (Myers et al. 2000). Biodiversity hotspots are defined as regions that contain at least 0.5% or 1,500 endemic vascular plant species, and that have lost at least 70% of their primary vegetation (Myers 1988, 1990, 2003). The Mesoamerican Biodiversity Hotspot ranges from central Mexico to the Darién lowlands in eastern Panama, and includes the UNESCOdeclared Amistad Biosphere Reserve, a globally recognized Center of Plant Diversity (Chaverri et al. 1997) and World Heritage Site, which protects most of the isthmian páramos of Costa Rica and Panama (Kappelle 2005b). At the same time, isthmian páramos of Costa Rica and Panama are embedded in the Talamancan Montane Forest ecoregion (Dinerstein et al. 1995, Olson et al. 2001), one of the planet’s 200 biologically most distinct ecoregions identified by WWF-US (Olson and Dinerstein 1998). Ecoregions are large areas of land or water that contain a geographically distinct assemblage of natural communities that share similar environmental conditions and a large majority of their species and ecological dynamics, and that interact ecologically in ways that are critical for their longterm persistence (Dinerstein et al. 1995, Olson et al. 2001). The “Global 200” ecoregions are selected on the basis of features related to their exceptional biodiversity, including species richness, endemic species, unusual higher taxa, unusual ecological or evolutionary phenomena, and the global rarity of habitats (Olson and Dinerstein 2002). Costa Rican páramo has been classified in Holdridge’s Life Zone System as “tropical subalpine rain páramo” (Spanish: páramo pluvial subalpino) (Holdridge 1967). In Holdridge’s system the term “subalpine” implies a mean annual biotemperature of 3 to 6ºC. Similarly, the adjective “rain” or “pluvial” implies an average annual precipitation of 1,000 to 2,000 mm, while the potential evapotranspiration ratio is low (0.125 to 0.25), producing a “superhumid”

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environment (Holdridge 1967). The map of Costa Rican Life Zones shows a presence of subalpine rain páramo on the Chirripó massif and the summit of Cerro Kámuk (Tosi 1969), covering only 0.2% of Costa Rica’s total land area (Holdridge et al. 1971). However, both Holdridge et al.’s analysis and Tosi’s life zone map did not cover all páramo patches that exist in Costa Rica— which actually add up to around 0.3% of the country’s territory (Kappelle and Horn 2005). Isthmian páramos are normally surrounded by tropical montane cloud forests (Kappelle 2001, chapter 14 of this volume), generally dominated by tall oaks in the genus Quercus (Blaser 1987, Kappelle 1995, 1996, 2006). These oaks are of Holarctic origin and migrated southward through North America hundreds of thousands of years ago (Hooghiemstra et al. 1992, Kappelle et al. 1992; Kappelle, chapter 14 of this volume). Today, the isthmian páramos share many plant species with adjacent montane oak forests (Cleef and Chaverri 1992, 2005, Kappelle et al. 1992, Vargas and Sánchez 2005). Some authors consider the isthmian mountains of Costa Rica and Panama (e.g., the Cordillera de Talamanca) to be a disconnected, northwestern extension of the Andean cordilleras of South America (F. Sarmiento, pers. comm.). These isthmian páramos on the summits of Central American mountains can be considered biogeographic “islands in the sky” located in the northwestern part of the Neotropical páramo “archipelago” (Luteyn 1999, Cleef and Chaverri 2005, Vargas and Sánchez 2005). Costa Rica’s northwesternmost páramos occur on the peaks of the Irazú (3,432 m) and Turrialba (3,340 m) volcanoes in the Cordillera Volcánica Central, while the core páramo area is situated further southeast, in the Cordillera de Talamanca, and distributed over three protected areas: Tapantí-Macizo de la Muerte National Park (e.g., Cerro Vueltas, 3,156 m; Cerro Buenavista, 3,491 m), Chirripó National Park (Cerro Cuericí, 3,345 m; Cerro Urán, 3,280 m; Cerro Chirripó, 3,819 m; and another 25 peaks over 3,000 m; for details see map in Kappelle and Horn, 2005, p. 765), and the western sector of the binational La Amistad International Park (e.g., Cerro Kamuk, 3,554 m; Cerro Dúrika, 3,280 m) (Fig. 15.2). The páramos in neighboring Panama are found in the eastern sector of La Amistad International Park (Cerro Fábrega, 3,340 m; Cerro Itamut, 3,279 m; and Cerro Echandi, 3,162) and on the summit of Barú Volcano (3,475 m) (Kappelle and Horn 2005, Samudio and Pino 2006). In Costa Rica, the páramo ecosystem covers a mere 15,205 ha, of which almost 10,000 ha is found on Cerro Chirripó and neighboring peaks (Kappelle 2005a). That is less than 0.3% of Costa Rica’s total land surface

(51,100 km²). These areas of páramo in Costa Rica account for only 0.4% of the total area of 35,000 km2 of páramo estimated for the Neotropics as a whole (Hofstede et al. 2003). About half (52.7%) of the páramo area in Costa Rica occurs in the subalpine belt (3,100– 3,300 m), while the other half (47.3%) is located in the alpine belt (3,300– 3,819 m). In Costa Rica, a clear altitudinal zonation of páramo vegetion types can be observed, especially along the slopes of Cerro Chirripó (Kappelle 1991, Chaverri and Cleef 1996). The lowest páramo zone (ca. 3,100– 3,300 m), known as subpáramo (Chaverri and Cleef 1996, Luteyn 1999), borders the upper montane oak-dominated cloud forests (Kappelle 1996). The subpáramo is a transition zone composed of species from the forest below and grass páramo above, in which shrubs and small trees form mosaics that alternate with shrubby grasslands dominated by bunch grasses or dwarf bamboos (Horn and Kappelle 2009). The subpáramo shrublands (arbustales, matorrales) are 2 to 8 m tall (Fig. 15.6). Here, dwarfish, sparsely-distributed, epiphyteloaded trees (e.g., Buddleja, Comarostaphylis, Escallonia, Myrsine) mix with small-leaved, gnarled shrubs (e.g., Diplostephium, Hypericum, Miconia, Solanum) (Weber 1958, Kappelle 1991, Chaverri and Cleef 1996). Above the subpáramo, the truly alpine belt (>3,300 m) in its strict sense is known as páramo proper— a term coined by Cuatrecasas (1958)— and consists of 0.5 to 2.5 m tall, bamboo-dominated (Chusquea subtessellata) grasslands (chuscales; Fig. 15.7), at drier spots replaced by bunch or tussock grasses (e.g., Calamagrostis, Festuca, Muhlenbergia.) The broomlike Chusquea subtesellata is the most common species in Costa Rican páramos and perhaps covers up to 60% of the total páramo area in the country (Kappelle 1991). Above 3,600 m elevation on the Chirripó massif, scattered occurrences of a type of transitional superpáramo may be observed on rocky and sandy soils. In this vegetation zone on the highest and coldest slopes, patches of small plants capable of enduring low temperatures, high diurnal temperature variation, and strong radiation (e.g., Acaena, Draba, Lupinus, Senecio, Westoniella) grow amidst exposed rocks covered by dense mats of mosses and lichens (Weber 1958, Kappelle 1991, Chaverri and Cleef 1996).

The Physical Environment Climate

As in other tropical mountainous countries, such as Venezuela and Papua New Guinea (Troll 1959, Lauer 1981, Rundel et al. 1994a,b), Costa Rica’s páramo-blanketed high

Fig. 15.6 Schematic lateral profile of a 6 m tall woody subpáramo shrubland in the subalpine belt around 3,100 m elevation at Buenavista massif. The small trees and shrubs depicted include the genera Buddleja, Comarostaphylis, Escallonia, Garrya, Myrsine, Oreopanax, and Schefflera. Drawing by Francisco Quesada and Luis González Arce.

Fig. 15.7 Clumps of Chusquea subtessellata bamboos on the Buenavista massif (Cerro de la Muerte). Photograph by Carlos Serrano.

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crests and summits (>3,100 m a.s.l.) are characterized by large mean diurnal temperature changes, with fluctuations of 7º to 10ºC typical and up to 20ºC possible, and comparably much smaller variation in mean monthly temperature (around 2ºC over the year, with January and February having the lowest monthly means) (Herrera 2005, Chaverri 2008; Herrera, chapter 2 of this volume). This contrasts with temperate alpine environments, which show much higher temperature seasonality due to their high-latitude positions. The Zugspitze mountain in the German Alps, for instance, has a mean diurnal temperature range of about 5ºC, compared with a seasonal range of about 13ºC in mean monthly temperature (Rundel et al. 1994a,b). The aseasonal temperature regime of Neotropical páramos can be described as equatorial, altitude-determined, mensual isothermy (Herrera 2005). Mean annual temperatures in the Costa Rican páramos are relatively low. They range from 11.0°C at ca. 3,065 m elevation (Villa Mills weather station, just below the páramo of Cerro Buenavista ) to 8.5°C. at ca. 3,466 m (Cerro Páramo meteorological station within the Buenavista páramo; Fig. 15.8) and ca. 6.5°C. at 3,670 m (Chirripó National Park weather station) (Herrera 2005, Chaverri 2008, Lane et al. 2011). The lowest daily minima have been measured in the first months of the year. Kohkemper (1983) and Horn et al. (1999) recorded extreme lows of − 9 and − 9.4°C on the Chirripó massif in February 1971 and January 1985, respectively, and Weber (1959) reported an extreme low of − 7°C in February 1956 on the Buenavista massif. On Cerro Chirripó, sheets of ice up to 0.6 cm thick have been observed to form on the surface of small ponds and along the shores of glacial lakes during these times of record overnight lows (Kohkemper 1983, Horn et al. 1999, Chaverri 2008). Temperature measurements made in 1989 and 1990 in the interior of Chirripó’s closed-canopy oak forests at two altitudes (2,000 and 2,700 m) indicate that the average air temperature at breast height (1.3 m above the forest floor) drops 0.57°C per 100 m increase in elevation (Kappelle et al. 1995, Kappelle and van Uffelen 2006). This value is close to the temperature decline of 0.6°C per 100 m elevation calculated for mountain slopes in Venezuela (Walter 1985), and in East Africa, New Guinea, and Hawai’i (Rundel et al. 1994a,b), and to the mean annual surface lapse rate of 0.54°C per 100 m derived by Orvis and Horn (2000) for Costa Rica as a whole, based on a dataset of 188 meteorological stations. Low temperatures together with strong daily fluctuations in temperature and humidity create conditions that combine to produce frost phenomena, water deficits, and even

Fig. 15.8 Walter climate diagram for the páramo ecosystem, based on data from the meteorological station at the 3,466 m high Cerro Páramo on the Buenavista massif, Costa Rica (9°33’41”N, 83°45’18”W). Temperature data are expressed by the more or less “horizontal” line in the lower part of the graph and correspond to the period 1971– 2000. Mean annual temperature during these thirty years was 8.5°C. Precipitation data are expressed by the bimodal curve in the center and upper part of the graph and correspond to the years 1971– 2001. Mean annual rainfall over this period was 2,581 mm, of which 89% fell between May and November. Monthly precipitation in excess of 100 mm is shown at a 10% scale. Diagram prepared by Will Fontanez at the University of Tennessee.

droughts (Herrera 2005). These are environmental stresses to which plant species have adapted over evolutionary time scales— for example, by acquiring small, rounded, leathery leaves, and dense leaf pubescence (Cleef 1981, Körner 1998). As in other tropical high-altitude zones (Troll 1968, Lauer 1981, Luteyn 1999), the páramo-clad peaks in Costa Rica undergo a “freeze and thaw” cycle most days of the year, creating conditions that have been referred to as “summer every day and winter every night” (Hedberg 1964, Körner 1998). Repeated daily freezing and thawing can result in frost-heaving of soils and displacement of saturated soils on slopes (solifluction) (Troll and Lauer 1978). These periglacial (literally, “near ice”) geomorphic processes can create a poor soil environment for woody plant roots, and may function as key selective forces directing the adaptation of plants to survive the harsh conditions of high tropical páramo environments (Körner 1998). In terms of precipitation and humidity, Costa Rican páramos have a wet to pluvial climate with daily abrupt

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changes in cloud cover, rain, fog, and relative atmospheric humidity (Herrera 1986, 2005). Relative humidity levels typically range from 70 to 85%. The daily changes in humidity and rain result from the orographic uplift caused by the country’s main mountain ranges (e.g., Cordillera Volcánica Central and Cordillera de Talamanca), proximity to coastal zones, and the influence of the Intertropical Convergence Zone (ITCZ), the latitudinal zone of of low pressure and converging winds centered near the equator that migrates north and south with the seasons through the latitudinal band in which Costa Rica is located (Coen 1983, and see Herrera, chapter 2 of this volume). Average annual rainfall is usually between 1,000 and 2,000 mm, but may be higher on some exposed slopes facing the Caribbean and locally up to 4,500 mm (Herrera 1986, 2005). Some sites, however, receive much less rainfall, perhaps even less than 1,000 mm per year. Whereas there are no official reports of snowfall in Costa Rica, Pittier (1938) reported that on January 10, 1897, while hiking with fellow explorers and guides through the páramos of Cerro Buenavista (Cerro de la Muerte), he witnessed a true snow storm mixed with rain, though no snow accumulated on the ground surface (Herrera 2005). Daily temperature oscillations in Costa Rica’s páramo are largest during the drier period of the year (December through early April, verano) (Fig. 15.8), when strong northern and northeastern tradewinds prevail. During the wetter part of the year (late April through November, invierno), southwestern winds predominate, causing heavy rains. During this period, it rains almost every day, while cloudy skies predominate and reduce solar radiation receipt at the surface to 42% of its value at the top of the atmosphere, compared to 63% during the dry season (Herrera 2005). However, from the end of June to August, short periods of low precipitation (4 to 6 contiguous days) may occur, known as veranillos (Chaverri 2008). Geology, Geomorphology, and Soils

The Cordillera de Talamanca, site of most Costa Rican páramos (>90% of the total area covered by the biome), is a high mountain range composed of Tertiary sediments with a thickness of probably several km, intercalated with Tertiary volcanic and plutonic rocks (Weyl 1957, 1980, Ballman 1976, Castillo 1984, Calvo 1987, Seyfried et al. 1987, Drummond et al. 1995, Wunsch et al. 1999; Alvarado and Cárdenas, chapter 3 of this volume). Initial uplift took place during the Middle Oligocene and Middle Miocene (Weyl 1956a,b), resulting in the gradual transformation of the Meso-American Island Arc into today’s continental land

bridge or isthmus (Seyfried et al. 1987), which ultimately allowed the great biotic interchange between North and South America (Rich and Rich 1983, Stehli and Webb 1985, Kappelle et al. 1992). Today, the Cordillera de Talamanca is considered an uplifted, inactive segment of the Central American Magmatic arc, composed of intrusive batholiths and plutonic stocks of quartz-diorites and monzonites with subordinate granites and gabbros. Associated sedimentary rocks are predominately volcarenites, breccias, fossiliferous calcarenites (with remains of mollusks and foraminifera), and sandy black shales (Alvarado and Cárdenes, chapter 3 of this volume). Calvo (1987) reported at least five lithological units within the12 km2 core area of Cerro Chirripó: lavas and pyroclastic deposits (both from the Paleocene– Lower Miocene), marine deposits, mainly derived from pyroclastics (most probably, Middle to Lower Pliocene), and intrusive and metamorphic rocks. The Costa Rican páramos experienced marked changes in climate during the Pleistocene, when mountain glaciers, snow, and ice covered the highest portions of the Cordillera de Talamanca (Weyl 1955a,b, 1956a,b, Hastenrath 1973, Bergoeing 1977, Barquero and Ellenberg 1982– 83, Calvo 1987, Horn 1990a, van Uffelen 1991, Shimizu 1992, Orvis and Horn 2000, 2005, Lachniet and Seltzer 2002, Lachniet et al. 2005). Pleistocene glaciation left its traces on the Chirripó and Buenavista massifs and on Cerro Kamuk (Lachniet and Seltzer 2002), shaping the landscape of these peaks at elevations over 3,000 m. Glacial landforms are best developed on the Chirripó massif, where they include, in addition to the glacial lakes already mentioned, cirques, U-shaped valleys, arêtes, roches moutonnées, whalebacks, smoothed and striated rock surfaces, and glacial deposits including glaciofluvial outwash, subglacial till, ablation till, kame terraces, and lateral, medial, and terminal moraines (Lachniet et al. 2005; Alvarado and Cárdenas, chapter 3 of this volume). Cerro Chirripó, at 3,819 m the highest point in Costa Rica, is a glacial horn, formed by the headward erosion of glaciers in three valleys (Fig. 15.4). Outside of the limit of glacial ice, periglacial geomorphological processes produced features such as solifluction fans and blockfields composed of rocks shattered by freeze-thaw cycles (Lachniet et al. 2005). Lachniet and Seltzer (2002) estimated that ice covered about 35 km2 on the Chirripó massif during the last local glacial maximum (Fig. 15. 9), and that ~5 and 2 km2 of ice once existed around Cerros Buenavista and Kamuk, respectively. Small pockets of páramo (10 cm DBH (diameter at breast height) in order to evaluate potential timber resources (Werner 1985, Finegan and Sabogal 1988, Guillén 1993). Guariguata et al. (1997) compiled the first extensive investigation of differences in woody vegetation structure and composition of seedlings, saplings, and trees between and within old growth and post-agricultural secondary forest stands of 16– 18-year-old growth at and around La Selva Biological Station. They demonstrated that stem density and basal area for seedlings, saplings, treelets, and trees were similar between old growth forest and secondary sites. Plant species richness was consistently lower in intermediate-aged secondary stands because of greater dominance by fewer species (Guariguata et al. 1997, Boucher et al. 2001). In later resurveys of the same forest stands, plant species richness was found to attain levels similar to old growth forests within 30 years (Chazdon et al. 1998, Capers et al. 2005, Letcher and Chazdon 2009a). In contrast, species richness of lianas showed no change or a slight decline with forest age, depending on the method of assessment (Letcher and Chazdon 2009b). Aboveground biomass also follows a similar trend, achieving comparable levels with old growth forest after 21– 30 years of abandonment, emphasizing the high conservation value of secondary forests (Letcher and Chazdon 2009a, Norden et al. 2009). In fact, as much as 70% of species found in secondary forest stands in the area were shown to have commercial and medicinal uses (Chazdon and Coe 1999), aside from their value in the provision of ecosystem services. Across secondary forest stands there is a clear and

expected trend of successional change in forest structure and composition, but local site factors result in variations in species composition and rates of changes among stands (Chazdon et al. 2007). Small-scale local variation in soil fertility and compaction has affected tree species distributions in both old growth and secondary forest stands (Clark et al. 1999, Guarigata and Dupuy 1997, Herrera and Finegan 1997), which, owing to species-specific effects, has influenced understory floristic composition and species richness (Finegan and Delgado 2000). Other studies of secondary forests in this region focus on characterizing the structure and composition of these forests (Guariguata et al. 1997, Redondo-Brenes et al. 2001), describing the dynamics of the forest at different ages since abandonment (Vílchez et al. 2004), or determining the economic value of secondary forest as carbon sinks (Ramírez et al. 2002). The small spatial extent of these studies limits our ability to extrapolate their results to the entire region. The presence of several large old growth forests in the region, the remnant trees in secondary forest stands at the time of abandonment (Guariguata et al. 1997), and the abundance of seeds in the soil seed bank— substantially higher than in nearby old growth forest (Dupuy and Chazdon 1998)— as well as the presence of seed dispersers (Slocum and Horvitz 2000, Chazdon et al. 2003), have all contributed to a rapid recovery of tree basal area, woody seedling abundance, and species richness (Chazdon et al. 1998, Nicotra et al. 1999, Chazdon et al. 2005, Capers et al. 2005, Letcher and Chazdon 2009a). Secondary forest reassembly is converging with old growth community composition (Norden et al. 2009), though investigations of community phylogenetic structure during succession have found strong phylogenetic overdispersion at multiple scales (Letcher 2010). After 20– 25 years of development, when these stands reach the point of stem exclusion, aboveground carbon stocks have been calculated to be equivalent to those in primary forests of the region (Clark and Clark 2000). Early findings indicated that species-specific differences in root architecture result in differential nitrogen and phosphorus exploitation. Nutrient use efficiency, productivity, and nutrient residence times also showed species-specific responses (Hiremat et al. 2002). Shifts in nitrogen uptake in bromeliads (using isotope ratio) indicate that 77– 80% of the nitrogen in small individuals originates from the atmospheric sources, whereas in larger individuals as much as 64– 72% was soil-derived (Reich et al. 2003), adding a further layer of complexity to rainforest research. Various combinations of species identity and cutting rotations in monoculture and polyculture plots with native tree and monocot species produced highly variable results in total soil organic

The Caribbean Lowland Evergreen Moist and Wet Forests 545

carbon (TSOC) levels after 10 years. TSOC calculations ranged from loss of 24% (0.9 mg/ha/year) to an increase of 14% (0.6 mg/ha/year) with root C:N ratio and fine-root growth accounting for most of the changes in soil carbon sequestration (Russell et al. 2004). In later investigations using the same plots, Russell et al. (2010) found that after 16 years, species-specific variations were significant for partitioning of net primary production (NPP) among biomass components, tissue turnover rates, aboveground and belowground biomass, and detritus and also in belowground C cycling processes such as soil respiration, heterotrophic respiration, and belowground NPP. Such species-specific trends were also recorded for independent plantation stands at La Selva for litterfall and macronutrient content (Montagnini et al. 1993). Arbuscular mycorrhizae, spore abundance, and host tree species showed species-specific signals (Lovelock and Ewel 2005). Total NPP and soil organic carbon at 1 m depth showed no species effects (Russell et al. 2010). Collectively these findings highlight that at small scales, species-specific signals and plantation diversity richness impact biogeochemical cycling and that predictive models need to incorporate these biotic variations. In terms of carbon sequestration, intermediate-aged plantation plots at La Selva indicate rates of carbon sequestration of 5.2 Mg C ha− 1 yr− 1 over 17 years (Russell et al. 2010). These findings are comparable with results at the same location in younger stands on different soils (Redondo-Brenes and Montagnini 2006) and in older stands of exotic species in Panama (Kraenzel et al. 2003). Remote Sensing

Many of the earliest studies and projects described in the preceding sections were based on landscape-level studies with data from aerial photography and Landsat satellite images. The main problem with the use of data acquired by sensors (cameras and scanners) that measure reflectance from the surface for the Caribbean lowlands is the persistent cloud cover over the Caribbean Lowland region. For this reason many of the images acquired by these surface reflectance measuring satellite sensors for the Caribbean lowlands are not free of clouds, especially in the northwestern portion of the zone. One solution to the cloud problem is the use of Synthetic Aperture Radar (SAR) sensors that measure backscatter at microwave frequencies and are not affected by cloud cover. However, until the recent launch of the Japanese PULSAR, data acquired with other SAR sensors in spacecraft ( JERS-1, Radarsat, SRTM) had very coarse spatial resolution. SAR data acquired in Costa Rica by aircraft (Wu and Joyce 1988, Elizondo and Zamora 1998, Joyce 2006) have been acquired only over scattered selected areas.

Although coverage did not include the northwestern region of the Caribbean Lowlands, where clouds are the most persistent, most coverage included the area around the La Selva property. Since energy transmitted from improved SAR sensors can penetrate the forest vegetation, the measurement of SAR backscatter has the potential to be used to assess forest structure and make estimations of the aboveground biomass. L-Band SAR data were acquired for a portion of the Caribbean Lowlands (January and February 2010) and are posted for downloading. In addition to improvement in the technology of SAR sensors since 2000, there has been significant improvement in the technology for hyperspectral and laser (Lidar) sensors. Both of these technological advances have been used to great effect in analyses of the forests at the La Selva Biological Station and the surrounding areas, including the Sarapiquí watershed and the Caribbean portion of the Mesoamerican Biological Corridor (Arroyo-Mora et al. 2008, Clark et al. 2005, Drake et al. 2002a,b, 2003, Dubayah et al. 2010, Zhang et al. 2006). In summary, remotely sensed data have been analyzed to produce maps of the forest vegetation and for studies of land use change ( Joyce 2006) throughout the Caribbean lowlands. Various other studies with remotely sensed data have provided information on forest parameters and forest function in selected areas in the Caribbean lowlands, especially for the forest on the OTS-administered La Selva Biological Station property and vicinity. New sensor technology and improved analytical techniques, especially for hyperspectral, SAR, and Laser (Lidar) sensors, also hold great potential for providing additional information for assessment of forest structure, biomass, and species composition. Animals— Invertebrates and Vertebrates

Costa Rica has a long and robust tradition of taxon-based animal research. In the Caribbean lowlands, much of the invertebrate work has been of a taxonomic and biogeographic nature, with special attention being paid to ants, butterflies and moths, and beetles. Among the vertebrates, birds, frogs, and bats have been particularly well-studied. In recent years there has been a proliferation of studies of plant– animal interactions in the general areas of herbivory, seed dispersal, pollination, and trophic relations. DNA barcoding has come into its own as a technique used in invertebrate (as well as plant) studies. Genomic and other molecular and biochemical techniques are now routinely paired with field observations to provide an integrated perspective on the lives of these tropical animals. Most of the reviews in the following sections are based on the published literature. The discussion of the Caribbean lowland fishes is derived

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largely from the research and personal observations of one of the coauthors (R.C.C.). Invertebrates

The most comprehensive invertebrate inventory project in the Caribbean lowlands was the 14-year ALAS (Arthropods of La Selva) enterprise led by Rob Colwell and Jack Longino. During this time period (starting in 1991), hundreds of thousands of specimens were collected, processed, and deposited in museums around the world, including at Costa Rica’s INBio (National Biodiversity Institute) (http:// purl.oclc.org/alas). The ALAS project also developed the software programs EstimateS and Biota, used for calculating biodiversity and for managing biodiversity databases, respectively (Colwell 2005, Colwell et al. 2004, Gotelli and Colwell 2001). A long-term tropical butterfly project run by Phil DeVries and Isidro Chacón moved its Costa Rican center of operations from La Selva to the nearby Tirimbina Biological Reserve and continues to provide country-wide information on lepidopteran diversity (Chacón and Montero 2007, DeVries 1979, 1997, DeVries et al. 2012, Walla et al. 2004). Angel Solís from INBio and his colleagues have been monitoring dung beetle populations throughout the country for several decades, with a 35-year record for La Selva (Escobar et al. 2008). Nematode diversity in different soil types at La Selva (including canopy soils) has recently become a noteworthy topic (Powers et al. 2009). Treatments of the more ecological invertebrate projects are to be found in the Plant-Animal Interactions sections below. Fish

Although the species comprising the fish fauna of the Caribbean lowlands of Costa Rica have been identified, most aspects of their biology in the wild are poorly studied (e.g., see Pringle et al., chapter 18 of this volume). The total biodiversity of fishes in the Caribbean lowlands is minute (Bussing 1998; Bussing 1994, Appendix 4 lists 43 species at the La Selva Biological Station) compared to the thousands of species in the Amazon (1300++; Goulding 1980), and the fish fauna is dominated by just a few families— the cichlids (Cichlidae), the characins (Characidae), and the livebearers (Poeciliidae). Even these families are represented by only a handful of species each. The various catfish families that achieve incredible diversity further south (e.g., the pimelodid catfishes, the callichthyids, and the suckermouth catfishes of the family Loricariidae) are represented by just three species of pimelodids. Other families have token representation, including single species of the Carcharhinidae, Elopidae, Gobiesocidae, Rivulidae, Atherinidae, Syngnathidae, Synbranchidae, Haemulidae, Centropomidae,

Eleotridae, and a couple of members of the Mugilidae and Gobiidae (Table 16.1). Despite low biodiversity, the ichthyofauna has many fascinating characteristics. For example, the pipefish Pseudophallus mindii is found near the coast but has also been recorded at least twice at La Selva (Bussing 1998; Coleman, personal observation), a full 75 km from the coast, and certainly a long swim for a small pipefish. The freshwater clingfish (Gobiesox nudus) is from a family, Gobiesocidae, often associated with the intertidal zone of the eastern Pacific Ocean including Washington, British Columbia, and Alaska. Fishes such as the American eel (Anguilla rostrata) and the pike killifish (Belonesox belizanus) are considered distinctly coastal and have wide latitudinal ranges on the Atlantic coast north and south of Costa Rica. The blackbelt cichlid, Theraps maculicauda, always appears to be within sight of the surf line. Other “coastal” fish, such as the tarpon (Megalops atlanticus), penetrate far upstream into the lowlands. The bigmouth sleeper (Gobiomorus dormitor) is usually seen near the coast but can be found far inland at La Selva. It is not known whether individual sleepers move this distance— given their sedentary lifestyle, it seems unlikely. The distribution of species in the region is no doubt a product of the overall river patterns in the region. There appear to be three major assemblages. The large river bounding the north side of the region is the Río San Juan, which flows from Lake Nicaragua into the Caribbean. Because this large river drains Lake Nicaragua, it brings fishes that are not typically found in the rest of the zone into the northern edge of the region. For instance, several cichlids such as the midas cichlid Amphilophus citrinellum and the jaguar cichlid Parachromis managuense are common in the Lake and are also found at the river mouth at the far northeastern corner of the lowlands at Refugio Nacional de Vida Silvestre Barra del Colorado. In fact, it is interesting that these species have not penetrated further south. The bull shark Carcharhinus leucas and the sawfish Pristis pristis are in the Lake and in the Río San Juan, and extremely rarely a bull shark will swim up the Río Sarapiquí to be spotted at La Selva. Gars (Astractosteus tropicus) are found in the Río San Juan and are common in the sluggish waters of Caño Negro. We cannot compare the fishes of the Costa Rican lowlands to the fishes north of the Río San Juan because that portion of Nicaragua is largely unstudied with regard to fishes. The bulk of the northern portion of the lowlands is drained by several large river systems that originate in the volcanic highlands to the west and flow roughly north or northeast to the Río San Juan. These include, from west

Table 16.1. Family

List of Fishes of the Caribbean Lowlands of Costa Rica Ordered per Sector Species

English Name

Spanish Name

Fishes of the Río San Juan sector Carcharinidae Carcharhinus leucas Pristidae Pristis pristis Lepisosteidae Astractosteus tropicus Clupeidae Dorosoma chavesi Characidae Astyanax nasutus Gymnotidae Gymnotus maculosus Pimelodidae Rhamdia nicaraguensis Rivulidae Rivulus isthmensis Poeciliidae Alfaro cultratus Brachyraphis parismina Neoheterandria umbratilis Phallichthys amates Phallichthys tico Poecilia gillii Poecilia mexicana Atherinidae Atherinella hubbsi Synbranchidae Synbranchus marmoratus Cichlidae Amphilophus citrinellus Archocentrus centrarchus Archocentrus nigrofasciatus ?Astatheros alfari Astatheros longimanus Herotilapia multispinosa Parachromis dovii Parachromis managuensis Gerreidae Eugerres plumieri Haemulidae Pomadasys croco Mugilidae Agonostomus monticola Gobiidae Awaous banana

bull shark sawfish gar shad Colcibolca tetra knifefish catfish Isthmian rivulus alfaro olomina olomina merry widow olomina molly shortfin molly silverside marbled swamp eel midas cichlid flier cichlid convict cichlid pastel cichlid redbreast cichlid rainbow cichlid wolf cichlid jaguar cichlid mojarra Atlantic grunt mountain mullet lamearena

tiburón pez sierra gaspar sabalete sardina lagunera madre de barbudo barbudo olomina olomina olomina olomina olomina olomina olomina olomina sardina anguila de pantano mojarra mojarra congo mojarra cholesca mojarrita guapote guapote tigre mojarra prieta roncador tepemechín lamearena

Fishes of the coastal sector Elopidae Megalops atlanticus Anguillidae Anguilla rostrata Poecillidae Belonesox belizanus Poecilia mexicana Atherinidae Atherinella hubbsi Cichlidae ?Amphilophus citrinellus ?Archocentrus centrarchus Theraps maculicauda Centropomidae Centropomus parallelus Centropomus pectinatus Centropomus unidecimalis Carangidae Caranx latus Gerreidae Eugerres plumieri Haemulidae Pomadasys croco Eleotridae Dormitator maculatus Eleotris amblyopsis Eleotris pisonis Gobiomorus dormitor Paralichthyidae Citharichthys spilopterus Citharichthys uhleri Achiridae Trinectes paulistanus

tarpon American eel pike killifish shortfin molly silverside midas cichlid flier cichlid blackbelt cichlid fat snook blackfin snook common snook jack mojarra Atlantic grunt fat sleeper sleeper spiny-cheek sleeper big-mouth sleeper flounder flounder sole

sábalo real anguila pepesca gaspar olomina sardina mojarra mojarra pis pis calva gualaje Atlántico róbalo jurel mojarra prieta roncador guarasapa pez perro pez perro guavina lenguado lenguado lenguado redondo

Fishes of the central sector Characidae Astyanax aenus (= fasciatus) Bramocharax bransfordii Brycon guatemalensis Bryconamericus scleroparius Carlana eigenmanni Hyphessobrycon tortuguerae Roeboides bouchellei Gymnotidae Gymnotus cylindricus Pimelodidae Rhamdia nicaraguensis

banded tetra longjaw tetra machaca creek tetra carlana tetra Tortuguero tetra glass headstander knifefish catfish

sardina sardina picuda machaca sardina de quebrada sardinita sardinita sardinita madre de barbudo barbudo continued

Table 16.1.

Continued

Family

Rivulidae Poeciliidae

Atherinidae Gobiesocidae Syngnathidae Synbranchidae Cichlidae

Mugilidae Gobiidae

Eleotridae

Species

English Name

Spanish Name

Rhamdia guatemalensis Rhamdia rogersi Rivulus isthmensis Alfaro cultratus Brachyraphis holdridgei Brachyraphis olomina Brachyraphis parismina Neoheterandria umbratilis Gambusia nicaraguensis Phallichthys amates Phallichthys quadripunctatus Phallichthys tico Poecilia gillii Priapichthys annectens Atherinella chagresi Atherinella hubbsi Gobiesox nudus Pseudophallus mindii Synbranchus marmoratus Archocentrus nigrofasciatus Archocentrus septemfasciatus Astatheros alfari Astatheros rostratus Herotilapia multispinosa Hypsophrys nicaraguense Neetoplus nematopus Parachromis dovii Parachromis loisellei Tomocichla underwoodi Agonostomus monticola Joturus pichardi Awaous banana Sicydium adelum Sicydium altum Gobiomorus dormitor

catfish catfish Isthmian rivulus alfaro olomina olomina olomina olomina mosquito fish merry widow olomina olomina molly olomina silverside silverside clingfish pipefish marbled swamp eel convict cichlid

bardudo barbudo olomina olomina olomina olomina olomina olomina olomina olomina olomina olomina olomina olomina sardina sardina chupapiedra pez pipa anguila de pantano congo mojarra mojarra

Fishes of the Río Sixaola sector Characidae Astyanax aenus (= A. fasciatus) Astyanax orthodus Gymnotidae Gymnotus cylindricus Rhamphichthyidae Hypopomus occidentalis Pimelodidae Rhamdia guatemalensis Rhamdia rogersi Poeciliidae Alfaro cultratus Brachyraphis parismina Phallichthys amates Poecilia gillii Priapichthys annectens Atherinidae Atherinella chagresi Syngnthidae Pseudophallus mindii Synbranchidae Synbranchus marmoratus Cichlidae Archocentrus myrnae Archocentrus nigrofasciatus Astatheros bussingi Astatheros rhytisma Parachromis loisellei Haemulidae Pomadasys croco Mugilidae Agonostomus monticola Joturus pichardi Gobiidae Awaous banana Sicydium adelum Sicydium altum Eleotridae Gobiomorus dormitor

pastel cichlid rainbow cichlid

wolf cichlid tuba mountain mullet hog mullet lamearena goby goby big-mouth sleeper banded tetra largespot knifefish knifefish catfish catfish alfaro olomina merry widow molly olomina silverside pipefish marbled swamp eel topaz cichlid convict cichlid

Atlantic grunt mountain mullet hog mullet lamearena goby goby big-mouth sleeper

mojarrita moga moga guapote guapotillo vieja tepemechin bobo lamearena chupapiedra chupapiedra guavina sardina sardina blanca madre de barbudo madre de barbudo barbudo barbudo olomina olomina olomina olomina olomina sardina pez pipa anguila de pantano mojarra congo mojarra guapote amarillo roncador tepemechin bobo lamearena chupapiedra chupapiedra guavina

The Caribbean Lowland Evergreen Moist and Wet Forests 549

to east, the Río San Carlos system and the Río SarapiquíChirripó system (Bussing 1998). East of the Chirripó the rivers flow into the Caribbean, possibly an important difference in terms of the movement of fishes because fishes in the latter rivers must pass through intertidal, brackish, or marine waters to connect to other river systems. Interestingly, there do not appear to be significant differences between the fish fauna of these two types of rivers, although there are some. This may be because in the area around the city of Guápiles, numerous tributaries of the Río Chirripó (draining north to the Río San Juan) and the Tortuguero and Parismina systems (draining east into the Caribbean) are found within a few kilometers of each other. It is easy to imagine that one of the regular flooding events common to this area could move fishes between the north-draining systems and those that drain to the Caribbean. To the east of Siquirres, from Matina to the port of Limón, as the topography flattens out into the coastal plain, there is a distinct lack of rivers. The only water now flowing through the seemingly endless banana plantations are tiny silt-filled streams. As one heads south, near Cahuita and down to the Panamanian border, there are smaller rivers that flow into the Caribbean and others that drain into the Sixaola system. This break is significant because there is a notable change in the fish communities between the Sixaola system and the northern part of the lowlands. The Río Sixaola and its tributaries have similar, related, but distinctly different species, than the rest of the region. For example, with regard to cichlids, although Archocentrus septemfasciatus is common throughout the entire northern quadrant, it is replaced in the Sixaola region by Archocentrus myrnae (Tobler 2007). Similarly, Amphilophus alfari is replaced by Amphilophus bussingi. This is not to say that no northern sector fish are found in the Sixaola. For example, although there is a different tetra, namely the largespot tetra, Astyanax orthodus, the banded tetra A. aenus is also there, as is the convict cichlid, which is found over much of northern Costa Rica (Bussing 1998). Other species will be found once someone looks for them. For example, again with regard to cichlids, Bussing does not indicate Neetroplus nematopus in the Río San Juan, yet it is common both in the main part of the Caribbean lowlands and in Nicaragua. Other fishes, such as Tomocichla underwoodi (= T. tuba) are almost certainly not found in the Sixaola region because we have looked extensively for them and not found them there. Finally, there is the possibility that some fishes are located now where they have been introduced by humans. This is a common occurrence around the world both currently and historically and there is little reason to imagine that the Caribbean lowlands have been exempt from this influence.

The second key contrast between the Costa Rican Caribbean lowlands and the Amazon drainage concerns the changes in water volume and depth. The Amazonian flood cycle is present in the Costa Rican lowlands in almost similar magnitude, but is completely different in periodicity and tempo. The rivers of the main part of the Caribbean lowlands (there are no natural lakes as such, except for Lake Nicaragua on the northern boundary) are the product of constantly changing hydrodynamics. If anything, it is the variability that characterizes these habitats. The variation originates in the large-scale patterns of rainfall— heavy rains in late September through early January, the dry season from mid-January through April, the “little wet” season from May through August and then the “little dry” season through August and September. The timing of each of these periods changes from year to year. The important point is that even during the dry season, large storms can drop a substantial amount of water both on the lowlands and on the mountains to the west, which then rapidly moves down the streams and into the rivers. Rivers can swell in a matter of hours to twice their volume or more. For example, the height of the Río Puerto Viejo rose almost ten meters within 24 hrs at the La Selva Biological Station in January of 2006 and then dropped back to its original level over the next couple of days. This variation in water volume can radically alter the physical environment, moving large woody debris tremendous distances and reshaping river substrates in minutes. The water itself also changes in temperature, dropping to near 20°C or lower, or rising up to 27°C or higher. With changes in water depth, areas that were slow-moving become rapids and vice versa. The rivers can flood huge areas of land, then recede, moving fish into places far from the original river. This is important because many of the fishes associate themselves with particular substrates, depths, and temperatures. While the physical conditions change, sometimes daily, so too does the distribution and activity of many of the fishes. In summary, although various species can be nominally placed as being native to the region, the exact location at which a species is found can vary daily. Almost two decades of underwater snorkel studies have revealed that just because a fish is found at a particular location today means little as to whether that species will be found there tomorrow or next week. An open question remains whether the fish move into and out of desirable portions of a river or whether they simply “hunker down” and wait out the bad weather. Clearly at least some fishes are moving large distances because stretches of some rivers will become disconnected or entirely dewatered during certain times of the year, yet have fishes at other times. Although Rivulus (a killifish) can occasionally be spotted “flipping” along the

550 Chapter 16

ground from one body of water to the next, most of the fishes in the region are confined to living and dispersing in water. A final key contrast with other aquatic environments is the almost complete lack of aquatic macrophytes in most of these rivers and streams. There simply are no plants in most places (see also Pringle et al., chapter 18 of this volume). The substrate is rock, gravel, sand, or compacted clay. The exception is during flooding events when terrestrial vegetation becomes inundated. Nor are there large-leaved aquatic or emergent plants on which the fish can lay eggs. Small fishes, such as many livebearers, persist by living along the margins of the rivers. Woody debris is critical for hiding, as well as for creating microclimates of different velocity, substrate, and temperature. The taxonomy of some groups is a major challenge for understanding the fish communities of the Caribbean lowlands. For example, the convict cichlid, Archocentrus nigrofasciatus, has been placed in at least five genera within the last two decades (Herichthys, Heros, Cichlasoma, Cryptoheros, Amatitlania). These name changes reflect ongoing attempts to understand phylogenetic relationships that are not clearly resolved, largely because the biogeographic origins of these fishes are complicated (Chakrabarty and Albert 2011). Certainly some of the fishes are the result of radiations north from South America with the rise of the Isthmus of Panama, but the timing and numbers of these radiations are unclear. Other fishes have likely come from the north. The wolf cichlid (Parachromis dovii), or guapote as it is called locally, comes from a group with origins in the West Indies, yet the West Indian fishes are likely derived from older South American ancestors. No doubt further research will resolve some of these difficulties, particularly concerning closely related cichlid taxa such as Poecilia gillii and P. mexicana. Research on fishes in the Caribbean lowlands has been hampered by several obstacles. The large amount of moving water and the large sediment load also mean that visibility varies from excellent to non-existent. Certain rivers, such as the Río Chirripó, have never had any appreciable visibility, and therefore our knowledge is limited to the results of sampling (fishing, electroshocking). Others, such as the Río Puerto Viejo or the Río San José, can range from almost clear to no visibility from one day to the next. Names of rivers in the region also pose a challenge in that names on maps do not always agree with names on road signs, with GIS systems, or with local names for a river. Also, certain names are used repeatedly for different rivers, even two rivers located relatively close to each other. For instance, Río Toro appears as the name of several rivers in the region and

there are two different rivers named Río Sardinal within 15 kilometers of each other, yet they are entirely unconnected. Similarly, different segments of a river often bear a different name. Finally, river connectedness is complex and may involve stream capture, reticulation, and intermittent flows. This complexity could be important for understanding the evolution and relatedness of populations and subpopulations of fishes. The region and the fishes in it face various threats. Intense agriculture (particularly banana and pineapple) close to the rivers means that pesticides and sedimentation are always potential problems. Fishing by humans is present and likely responsible for local reduction in populations of some species— for example, guapote are increasingly rare and also wary of humans. Tomocichla underwoodi numbers near the town of Río Frio have decreased markedly over the last decade. Spear fishing, though illegal, is increasingly common and brazen and potentially a major threat because it specifically targets the largest individuals. On January 8, 2009, a previously unrecognized threat demolished the Río Sarapiquí when a magnitude 6.1 earthquake on the Caribbean slope of Volcán Poas caused massive landslides of material into the headwaters and tributaries of the Río Sarapiquí. The main river channel became saturated with mud and debris such that it virtually solidified all the way down to the confluence with the Río Puerto Viejo (about 25 km). It appeared that most, possibly all, of the fish in the main river were killed at that time, apparently from oxygen deprivation. How frequently such events occur, and whether their magnitude is amplified by human effects on the terrain, is unknown. On a positive note, the past decade has seen a notable increase in Costa Ricans using donning masks and snorkeling, simply to appreciate the beauty and environment of the lowland rivers. This is a positive development. Amphibians

The lowland forests (below 300 m a.s.l.) of the Caribbean slope of Costa Rica host a diverse amphibian assemblage, with 91 species of frogs in 38 genera, 10 species of salamanders in two genera, and three species of caecilians in two genera (Table 16.2). Frogs are distributed among 14 families, yet salamanders and caecilians are each represented in the region by a single family. Of Costa Rica’s 187 amphibian species, 104 occur in the Caribbean lowlands. There are no amphibian species that are endemic to the Caribbean lowlands of Costa Rica, largely because amphibian species in the lowland tropics generally have large geographic ranges (Savage 2002, Whitfield et al. in press). The amphibian fauna of the lowlands is quite distinct from

The Caribbean Lowland Evergreen Moist and Wet Forests 551 Table 16.2.

(a) Diversity and Habitat Affiliations of Amphibians of the Caribbean Lowlands of Costa Rica

Taxon

Family

Genera

Frogs

Rhinophrynidae Bufonidae Aromobatidae Dendrobatidae Eleutherodactylidae Brachycephalidae Strabomantidae Leiuperidae Leptodactylidae Amphignathodontidae Centrolenidae Hylidae Microhylidae Ranidae Plethodontidae Caeciliidae

1 4 1 5 1 1 1 1 1 1 3 15 2 1 2 2

1 6 1 5 2 17 6 1 4 1 11 30 2 4 10 3

42

104

Salamanders Caecilians Total

Species

Larval habitat

Adult habitat

P P,S S S, Ph D D D P P D S P, Ph, S P P, S D D

F T T T A, T A, Aq, T A, T T F, T A A A F Aq, T A, F, T F

NOTE. Larval habitat indicates pond or pool breeding (P), stream-breeding (S), phytotelm-breeding (Ph), and directdeveloping (D). Adult habitat indicates arboreal (A), aquatic (Aq), fossorial (F), or terrestrial (T). Source: Data derived from Savage 2002 and IUCN 2006.

montane forests, but is rather similar to those amphibian faunas found from moist forests from southern Mexico through central Panama (Savage 2002). The amphibian fauna from the most intensively studied site in the region, La Selva Biological Station, hosts 55 species (52.9% of the Caribbean lowlands assemblage). Three major ecological assemblages of amphibians found in Caribbean lowlands may be distinguished based primarily upon their use of reproductive resources: (1) lotic-breeding species with tadpoles in streams or rivers, (2) lentic-breeding species with larvae in ponds or pools, and (3) species with specialized forms of terrestrial reproduction. The stream-breeding assemblage is much less abundant and diverse in the lowlands than upslope, and in the lowlands glass frogs (Family Centrolenidae) are the most diverse representatives. The assemblage of lentic-breeding species may utilize habitats ranging from small forest pools to large permanent water bodies, and is particularly diverse in temporary wetlands (Donnelly and Guyer 1994). A few lentic-breeding species— including the dendrobatid Oophaga pumilio (previously Dendrobates pumilio) and the hylid Cruziohyla calcarifer— reproduce in phytotelmata. Terrestrial species with direct development (including the species-rich genera Craugastor and Pritimatnis) are particularly diverse and abundant in the Caribbean lowlands, likely because the high rainfall and lack of a severe dry season prevent terrestrial eggs from desiccating (Scott 1976, Whitfield et al. 2007). Fortunately, for the most part, amphibian assemblages

in the lowland tropics have not been as severely affected by the rapid and devastating species loss occurring in montane sites (Lips et al. 2005, 2006, 2008, Whitfield et al. in press). Thirty-three percent of Costa Rican amphibians are listed by the IUCN as threatened with extinction, but only 22.1% of species in the Caribbean lowlands region are threatened, and these are mostly higher-elevation species whose ranges only marginally extend into the lowlands. There are nonetheless many significant threats to lowland amphibian faunas, including widespread land-use change, emerging infectious diseases, and climate change (Butterfield 1994, Bell and Donnelly 2006, Whitfield et al. in press). The apparently non-native amphibian chytrid fungus, Batrachochytrium dendrobatidis, appears to be broadly distributed in this region and the neighboring volcanic cordilleras (Puschendorf et al. 2006, Puschendorf et al. 2009, and see Lawton et al., chapter 13 of this volume), but has not been reported to cause widespread declines here. However, at least one frog species (Craugastor ranoides) seems to have suffered extirpation throughout the region even close to sea level— possibly due to chytridiomycosis (Puschendorf et al. 2005, Puschendorf et al. 2006). Invasive competitors currently appear to represent little threat. Although at least one non-native frog has established small but persistent populations in this region (Osteopilus septentrionalis surrounding Puerto Limón), it is probably restricted to highly disturbed residential areas (Savage 2002). Whitfield et al. (2007) reported assemblage-wide declines for terrestrial frogs at La Selva, but the geographic extent and proximate

552 Chapter 16

causes for these declines remain unclear. The most serious future threats to amphibian populations in addition to continued habitat loss will likely result from anthropogenic climate change, in particular if increases in temperature are accompanied by directional shifts in precipitation regimes (Aguilar et al. 2005, IPCC 2007, Lawler et al. 2009, Whitfield et al. in press). Reptiles

The reptiles of the Caribbean lowlands of Costa Rica encompass a diverse assemblage including 36 species of lizards in 22 genera, 83 species of snakes in 47 genera, 6 species of turtles in 4 genera, and 2 species of crocodilians each in their own genus. In all, 127 of Costa Rica’s 222 reptile species occur in the lowlands of the Caribbean versant. Over half of the diversity in this region belongs to colubrid snakes, but the anoles (Family Polychrotidae) constitute another conspicuously diverse group. Savage (2002) suggested that the reptile fauna of this region is composed of species forming a lowland moist forest assemblage that ranges from eastern Mexico through Panama and is differentiated from other Mesoamerican reptile assemblages occurring in upland or more xeric habitats. The reptile fauna of the most intensively studied site in the Caribbean lowlands, La Selva Biological Station, includes 89 species (70.0% of the regional pool; Guyer and Donnelly 2005). The ecology of the reptiles is extremely variable, both within and among the major groups. The lizards in the region range from the large-bodied and primarily herbivorous Iguana to very small-bodied forest floor arthropodeating lizards (Lepidoblepharis, Norops). A diverse assemblage of leaf-litter lizards includes anoles, geckos, teiids, gymnophthalmids, anguids, and skinks (Lieberman 1986). The anoles sort ecologically along a vertical gradient from leaf-litter to trunk-dwelling and canopy species (Irschick et al. 1997). The boid and viperid snakes are semi-arboreal (Boa), arboreal (Corallus, Bothriechis), or terrestrial (Epicrates, Bothrops, Lachesis, Porthidium) and feed primarily on vertebrates. The elapids feed mostly on other snakes. The highly diverse assemblage of colubrids ranges dramatically in body form and habitat preferences, with many arboreal, terrestrial, and fossorial species but relatively few aquatic species (Guyer and Donnelly 1990, 2005, Savage 2002). The colubrids also vary greatly in diet, preying upon arthropods (Tantilla), mollusks (Dipsas, Sibon), amphibians (Chironius, Leptodeira, Leptophis, Urotheca), lizards (Scaphiodontophis, Imantodes, Oxybelis), snakes (Clelia, Drymarchon, Erythrolamprus), birds (Pseustes), or mammals (Lampropeltis). The non-marine turtle fauna includes stream-dwelling species (Rhinoclemmys funerea, Chelydra, and Trachemys), pond-inhabiting species (two Kinosternon

and Chelydra), and a single terrestrial species (Rhinoclemmys annulata). The crocodilians include the spectacled caiman, Caiman crocodilus, which inhabits swamps, ponds, streams, and rivers, and the American crocodile, Crocodylus acutus, which occurs primarily in larger rivers. The greatest threat to reptiles in the Caribbean lowlands is rampant habitat modification. Although some species of reptiles fare well in lands cleared of forests (especially heliothermic lizards such as Ameiva sp. and Basilicus vittatus), most reptiles prefer intact forests. Turtles (particularly Chelydra and Trachemys) and green iguanas are hunted and consumed by humans. Crocodiles and caiman have been actively hunted by humans for meat and hides; and while crocodiles were extirpated through much of their range, conservation efforts have been extremely effective and crocodile populations have been recovering in the past two decades (Savage 2002). Three non-native species of lizards have established populations in the area (the house geckos Hemidactylus frenatus and Hemidactylus garnotti, and the Caribbean anole Ctenotus cristatellus) but appear to be confined to highly disturbed habitats and currently do not appear to pose a threat to native faunas. Huey et al. (2009) suggested that many forest-dwelling lizards are thermoconformers whose optimal body temperatures are low relative to ambient temperatures, and that human-induced increases in temperature are likely to have particularly adverse effects on these ectotherms in the near future. Birds

The Atlantic lowland evergreen forests (below 300 m a.s.l.) along the Caribbean slope of Costa Rica are home to a highly diverse avifauna. These forests, as discussed earlier, are characterized by high rainfall, limited seasonality, a variety of habitat types, and complex vegetation structure within forests, all of which combine to support high bird species richness (Orians 1969, Slud 1976, Stiles 1983). These biotic and climatic factors ensure the availability of a wide variety of food resources such as fruits, flowers, nectar, and insects throughout the year, and also provide many unique resources for birds, such as army ant swarms (Blake and Loiselle 2000). The close proximity of the Caribbean slope, North America, and the once-continuous Caribbean forest belt connecting the region to the speciesrich South American forests has further contributed to the origin of high species diversity in the Caribbean lowlands of Costa Rica, with species diversifying along elevational (e.g., golden-crowned and white-throated spadebills, Platyrinchus coronatus and P. mystaceus, respectively) and latitudinal (e.g., the northern and southern nightingale-wrens, Microcerculus philometa and M. marginatus, respectively) gradients (Levey and Stiles 1994). Finally, as with the birds

The Caribbean Lowland Evergreen Moist and Wet Forests 553 Table 16.3. (b) Diversity and Habitat Affiliations of Reptiles of the Caribbean Lowlands of Costa Rica Taxon

Family

Genera

Lizards

Corytophanidae Iguanidae Polychrotidae Gekkonidae Teiidae Gymnopthalmidae Anguidae Scincidae Xantusiidae Boidae Ungaliophidae Colubridae Viperidae Elapidae Chelydridae Kinosternidae Emydidae Alligatoridae Crocodylidae

2 2 4 5 1 3 2 2 1 3 1 37 5 1 1 1 2 1 1

3 2 13 7 2 3 3 2 1 3 1 69 7 3 1 2 3 1 1

75

127

Snakes

Turtles

Crocodilians Total

Species

Habitat A, T A, T A, T A, T T T T T T A, T A, T A, Aq, F, T A, T F, T Aq Aq, F Aq, T Aq Aq

NOTE. Habitat indicates arboreal (A), aquatic (Aq), fossorial (F), or terrestrial (T). Source: Data derived from Savage 2002.

of the Osa Peninsula (see Gilbert et al., chapter 12 of this volume), the birds of the Caribbean lowlands tend to have low population densities but high species packing, with cooccurring similar species segregating by prey type, foraging height, and substrate use, among other variables (Terborgh et al. 1990, Chapman and Rosenberg 1991). As a result of these factors, the lowland Caribbean forests have the highest avian diversity in Costa Rica. A total of 484 species in 309 genera and 61 families has been recorded to date (Table 16.4). Of these, 289 are known or strongly suspected to breed in the Caribbean lowlands (Stiles and Skutch 1989, Garrigues and Dean 2007, Sigel et al. 2010). Yet, although the region hosts the highest species diversity, endemism rates are lower than on either the Osa Peninsula or the higher-elevation forests, likely due to the once-continuous extent of lowland forest from Mexico south into South America (Levey and Stiles 1994). The Costa Rican lowland Caribbean region hosts, during part to all of the year, 20 species that are endemic to southern Central America and northern Colombia. Of these, three species are also found in the Pacific lowlands and foothills of both coasts and 14 range into the Caribbean foothills. Four species— snowy cotinga (Carpodectus nitidus), plaincolored tanager (Tangara inornata), sulphur-rumped tanager (Heterospingus rubrifrons), and Nicaraguan seed-finch (Oryzobus nuttingi)— are restricted to the Caribbean lowlands, rarely ranging up to elevations above 700 m. An additional 33 species of elevational migrants traverse

the Caribbean slope, presumably to track the availability of food resources. For example, the three-wattled bellbird (Procnias tricarunculata) and the resplendent quetzal (Pharomachrus mocinno) move downslope in the non-breeding season, following the availability of their preferred Lauraceae (avocado) fruits (Hamilton et al. 2003, Powell and Bjork 1994). However, one species of hummingbird— the violet-crowned woodnymph (Thalurania colombica)— reverses the trend by breeding in the lowlands and migrating upslope (Stiles and Skutch 1989). Elevational migrants are highly dependent upon forested habitat in both their breeding and non-breeding grounds, as well as along their migratory pathway, and perhaps as a consequence of forest loss and fragmentation, 27% of these species (9 of 33) are considered threatened (IUCN 2010). Lowland Caribbean forests and disturbed areas (including secondary forests, open areas, and gardens) provide important overwintering habitat to many species of latitudinal migrants. Most latitudinal migrants breed in North America and either pass through Costa Rica on migration (76 species) or spend the non-breeding (winter) season in the lowland Caribbean area (49 species; Stiles and Skutch 1989, Parker et al. 1996, Garrigues and Dean 2007). These species have broader geographic ranges and are not as forest-dependent (and accordingly are not as threatened) as elevational migrants, with 7% of the species (9 of 125) considered threatened. The avifauna also includes three species of Austral migrants, which move annually between Costa Rica and South America. The streaked flycatcher (Myiodynastes maculatus) breeds in South America and spends the non-breeding season in the Costa Rican lowlands. An additional two species, the piratic flycatcher (Legatus leucophaius) and the yellow-green vireo (Vireo flavoviridis), breed in Costa Rica and migrate to South America during the late wet season (October– April). The greatest avian diversity in the lowland Caribbean region is found in primary forests and older, tall secondary forests, with a total of 166 species. An additional 66 species are generalists, found in forests as well as in other habitats. Open areas, including fields, pastures, young second growth, gardens, and developed areas, have the nexthighest diversity, with a total of 118 species. Edge habitats, between open and forested areas, are used by an additional 52 species. Finally, the region is home to 59 species using aquatic habitats (including lakes, rivers, and marshes), and 23 aerial species (mostly swallows and nightjars that spend the majority of their time on the wing; Sigel et al. 2010). The avifauna takes advantage of the wide variety of food resources available within the lowland Caribbean forests throughout the year. Insectivores numerically dominate the lowland Caribbean region, with 167 species. Omnivores

554 Chapter 16

are the second most-diverse dietary guild with 155 species, followed by carnivores with 97 species. The avifauna also includes 33 species of frugivores, 25 species of nectarivores, and 6 species of granivores. One of the most notable features of tropical lowland avifauna, including that of the lowland Caribbean region of Costa Rica, is the single- and multispecies flocks. Five types of flocks are commonly found in lowland Caribbean forests: single species flocks, understory antwren/antvireo mixed flocks, understory-midstory tanager mixed flocks, canopy mixed flocks, and ant-followers. Thirty-two species of landbirds form single-species flocks, including the great green (Ara ambiguus) and scarlet (A. macao) macaws, chestnutmandibled (Ramphastos swainsonii) and keel-billed (R. sulfuratus) toucans, and dusky-faced (Mitrospingus cassinii) and plain-colored (Tangara inornata) tanagers. Forest understory antwren-antvireo mixed flocks form around several nuclear species, including white-flanked (Myrmotherula axillaris), checker-throated (Epinecrophylla fulviventris), and dot-winged (Microrhopias quixensis) antwrens and streak-crowned antvireos (Dysithamnus striaticeps), which were among the most abundant understory species at La Selva in the 1970s, but are now scarce (Sigel et al. 2006). These flocks are attended by numerous species of wrens, gnatwrens, flycatchers, and woodcreepers, including the sulphur-rumped flycatcher (Myiobius sulphureipygius), buff-throated foliage-gleaner (Automolus ochrolaemus), and plain xenops (Xenops minutus). Tanager flocks form around two nuclear species, tawny-crested (Tachyphonus delattrii) and olive (Chlorothraupis carmioli) tanagers, and are attended by many species of tanagers, finches, flycatchers, and woodcreepers, including the yellow-margined flycatcher (Tolmomyias assimilis), the white-throated shriketanager (Lanio leucothorax), and the orange-billed sparrow (Arremon aurantiirostris). Canopy mixed flocks include cacique flocks formed around the scarlet-rumped cacique (Cacicus uropygialis), greenlet-honeycreeper flocks formed around the lesser greenlet (Hylophilus decurtatus) and the shining honeycreeper (Cyanerpes lucidus), and grosbeak flocks centered around the nuclear species black-faced grosbeak (Caryothraustes poliogaster); the latter two canopy flocks are frequently attended by Nearctic migrant warblers as well as resident species. Finally, ant-following flocks form around three nuclear species: bicolored (Gymnopithys leucaspis), ocellated (Phaenostictus mcleannani), and spotted antbirds (Hylophylax naevioides). These flocks are joined by several obligate and facultative attendant species, including northern barred-woodcreeper (Dendrocolaptes sanctithomae), plain-brown woodcreeper (Dendrocincla fuliginosa), bare-crowned (Gymnocichla nudiceps) and immaculate (Myrmeciza immaculata) antbirds, red-throated

ant-tanagers (Habia fuscicauda), and rarely the rufousvented ground-cuckoo (Neomorphus geoffroyi). The lowland Caribbean avifauna faces a wide variety of threats, including global climate change (Clark et al. 2003, Colwell et al. 2008), pesticides (Matlock et al. 2002), and cascading effects of alterations to other components of the lowland rainforest community (Feeley and Terborgh 2008, Young et al. 2008, Michel 2012). However, the greatest threat is the loss and fragmentation of lowland evergreen forests. Forested land cover in the Caribbean lowlands has decreased from nearly 100% to 70% in 1963 to 35% by 1983, and forest loss has continued since this time (Read et al. 2001). As a result, a total of 55 species are considered near-threatened, threatened, or vulnerable according to the IUCN (2010), and/or of medium, high, or urgent conservation priority (Parker et al. 1996). The majority of these species (36, or 65%) are associated with forest habitats, and another 5 species of generalists spend some time in forested habitats. Fragmentation-associated threats to lowland Caribbean forest birds also disproportionately affect species of various dietary guilds, specifically insectivores. Although the distribution of threatened species amongst dietary guilds of all species in all habitats in the lowland Caribbean is relatively even (8 carnivores, 14 frugivores, 3 granivores, 14 insectivores, 3 nectarivores, and 13 omnivores), understory insectivores have been particularly hard hit at the La Selva Biological Station in the Sarapiquí region. At La Selva, 51 species have experienced moderate or severe declines since 1960, including 8 species that are believed extirpated. Of these, 65% (33 of 51) are insectivores, 41% (21 of 51) are ant-followers or associated with mixed flocks, and 47% (24 of 51) are residents of the forest understory. The nuclear species of both the antwren– antvireo understory mixed flocks (M. axillaris, E. fulviventris, and M. quixensis) and the tanager mixed flocks (T. delattrii and C. carmioli) are among the species that have experienced declines at La Selva, which in turn has apparently led to declines of attendant species, including the sulphur-rumped flycatcher (M. sulphureipygius) and white-throated shrike-tanager (L. leucothorax; Sigel et al. 2006). It has not yet been established with certainty whether the trends seen at La Selva are widespread throughout the Caribbean lowlands. In any case, insectivore declines have important implications for arthropod and plant communities, as insectivorous birds (along with bats) at La Selva protect plants by consuming herbivorous arthropods (Michel et al. 2014). Mammals

Costa Rica is one of the few countries in the Western Hemisphere in which the entire mammalian fauna that was present

The Caribbean Lowland Evergreen Moist and Wet Forests 555 Table 16.4.

Diversity, Migratory Status, Habitat Guilds, Dietary Guilds, and Number of Threatened Species among Birds of the Caribbean Lowlands of Costa Rica

Family

Genera / species

Permanent residentsa

Latitudinal migrantsb

Elevational migrantsc

Visitantsd

Habitat guildse

Dietary guildsf

Threatened speciesg

Tinamidae Anatidae Cracidae Odontophoridae Podicipedidae Phalacrocoracidae Anhingidae Ardeidae Threskiornithidae Ciconiidae Cathartidae Accipitridae Falconidae Rallidae Heliornithidae Eurypygidae Aramidae Charadriidae Recurvirostridae Jacanidae Scolopacidae Columbidae Psittacidae Cuculidae Tytonidae Strigidae Caprimulgidae Nyctibiidae Apodidae Trochilidae Trogonidae Momotidae Alcedinidae Bucconidae Galbulidae Ramphastidae Picidae Furnariidae Thamnophilidae Formicariidae

2/3 5/6 3/3 2/3 2/2 1/1 1/1 11/17 4/4 1/1 3/3 19/33 5/10 8/9 1/1 1/1 1/1 3/3 1/1 1/1 6/13 7/14 8/12 5/8 1/1 6/7 4/7 1/2 4/8 21/26 1/5 3/3 2/6 3/4 2/2 4/5 7/9 11/14 13/18 1/1

3 2 2 2 2 1 1 11 2 0 3 19 6 6 1 1 0 0 0 0 0 11 9 4 1 7 4 2 3 12 3 2 5 4 2 3 8 12 16 1

0 3 0 0 0 0 0 6 0 0 0 11 3 2 0 0 0 2 1 1 13 0 0 3 0 0 3 0 1 1 0 0 1 0 0 0 1 0 0 0

0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 8 2 0 0 0 0 2 0 0 2 0

0 1 1 1 0 0 0 0 2 1 0 2 1 1 0 0 1 1 0 0 0 3 0 1 0 0 0 0 4 5 0 1 0 0 0 0 0 2 0 0

F, O Aq F F Aq Aq Aq Aq, F, O Aq, F Aq F, O Ae, Aq, E, F, G, O E, F, O Aq, F Aq F Aq Aq Aq Aq Aq, O F, O E, F, G, O F, G, O O F, G, O Ae, F, O F, O Ae E, F, G, O F F, G Aq, F E, F, G E, F F, G E, F, G, O F, G, O E, F, O F

O O O O C C C C, I C C C C, I C O O C C I C O C, I E, F, O F C, I, O C C, I I C, I I N O O C I I O I, O I I I

1 0 2 2 0 0 0 1 0 0 0 6 1 1 0 0 0 0 0 0 1 2 6 1 0 0 0 0 1 3 0 0 0 0 0 2 1 1 3 0 continued

at the time of European settlement is still largely extant, at least in well-protected parks. The Caribbean lowland area of Costa Rica has a diverse mammalian fauna that is characteristic of Neotropical lowland rain forests and consists of approximately 125 species representing 10 orders and 30 families. The majority of species found in the lowlands are broadly distributed in the northern Neotropics— lowland tropical mammals tend to be distributed both in latitude and elevation in a manner more widespread than is the case for amphibians, reptiles, and birds. The Costa Rican Caribbean lowland mammal fauna includes 5 marsupials, 71 (possibly more) bats, 3 (possibly 4) primates, 2 armadillos, 3 anteaters, 1 rabbit, 3 squirrels, 10 (possibly more) long-tailed rats and mice, 1 pocket gopher,

1 porcupine, 1 paca, 1 agouti, 4 mustelids, 1 skunk, 4 procyonids, 5 cats, 2 peccaries, 2 deer, and 1 tapir. The West Indian manatee (Trichechus manatus) historically occurred in the rivers and canals along and well inland from the coast and it is still found there now, although in reduced numbers ( Jiménez, chapter 20 of this volume). This species list is likely to be complete with the exception of the orders Chiroptera and Rodentia, where cryptic or difficult-to-capture species may not yet have been observed. All of the species in this historical species list, with the exception of the giant anteater (Myrmecophaga tridactyla), still occur in the lowlands and represent more than half (55%) of Costa Rica’s mammalian fauna. Although Costa Rica’s Caribbean lowlands occupy an

556 Chapter 16 Table 16.4.

Continued Genera / species

Permanent residentsa

Latitudinal migrantsb

Elevational migrantsc

Visitantsd

Habitat guildse

Dietary guildsf

Threatened speciesg

Grallariidae Tyrannidae Cotingidae Pipridae Vireonidae Corvidae Hirundinidae Troglodytidae Sylviidae Turdidae Mimidae Bombycillidae Parulidae Genus Incertae Sedis (Coerebidae) Thraupidae Genus Incertae Sedis (Saltator) Emberizidae Cardinalidae Icteridae Fringilidae Passeridae

1/2 36/54 5/5 3/4 3/10 1/2 6/9 6/10 3/3 4/8 2/2 1/1 13/34 1/1

2 35 2 1 3 2 3 10 3 1 1 0 3 1

0 13 0 0 7 0 6 0 0 4 1 1 31 0

0 3 2 3 0 0 0 0 0 2 0 0 0 0

0 3 1 0 0 0 0 0 0 1 0 0 0 0

E, F E, F, G, O F E, F E, F, G, O G, O Ae, O E, F, O E, F, G F, G, O E, O G E, F, G, O O

I F, I, O F, O F I, O O I I I O O O I, O O

0 3 3 1 0 0 0 1 0 1 0 0 3 0

14/27 1/5

17 5

3 0

3 0

4 0

E, F, G, O E, F, O

I, O O

3 1

8/11 5/7 9/15 1/4 1/1

8 2 12 3 1

2 4 3 0 0

0 1 0 1 0

1 0 0 0 0

F, O F, G, O E, F, G, O G, O O

G, O G, O I, O F O

2 1 0 1 0

Total

309/484

286

128

33

37

Family

55

Permanent residents live in the lowland Caribbean year-round. Latitudinal migrants include passage migrants and breeding and non-breeding part-year residents that spend the remainder of the year in North or South America. c Elevational migrants include breeding and non-breeding part-year residents that spend the remainder of the year at higher elevations. d Visitants occur accidentally or visit occasionally, though not on a seasonal or annual basis. e Habitat guild codes: Ae: Aerial (spend most time on the wing); Aq: Aquatic (associated with lakes, rivers, and marshes); E: edge (associated with forest edge and canopy); F: Forest (associated with primary or tall secondary forest); G: Generalist (associated with multiple habitat types); O: Open (associated with fields, pastures, young secondary forest, suburban, and urban areas). Codes from Sigel et al. 2010. f Dietary guild codes: C: Carnivores (diet primarily or entirely vertebrates, carrion, snails, and large arthropods); F: Frugivores (diet primarily or entirely fruit); G: Granivores (diet primarily or entirely seeds); I: Insectivores (diet primarily or entirely insects and other arthropods); N: nectarivores (diet primarily or entirely floral nectar); O: Omnivore (diet includes food from multiple categories). Codes from Sigel et al. 2010. g Threatened species include species assigned Conservation Priority of Urgent (1), High (2), or Medium (3) by Parker et al. 1996 (per Blake and Loiselle 2000), and/or species assigned an IUCN (2010) Red List Category of Near Threatened or higher. Source: Data derived from Slud 1960, Stiles and Skutch 1989, Ridgely and Gwynne 1992, Parker et al. 1996, Blake and Loiselle 2000, Sigel et al. 2006, 2010, Garrigues and Dean 2007, and IUCN 2010. a

b

extensive area from the Nicaraguan to Panamanian borders, until recently little research has been undertaken on the region’s mammals other than in the La Selva– Parque Nacional Braulio Carrillo region and to a lesser extent in the Maquenque and Tortuguero protected areas. More than 100 scientific papers on various aspects of mammals at La Selva have been published since Slud (1960) first mentioned white-lipped peccaries, monkeys, and tapirs there. As part of the elevational transect that became the La Selva– Parque Nacional Braulio Carrillo biological corridor, Timm et al. (1989) conducted a faunal survey of the elevational transect from 35 m to 2,600 m on Volcán Barva, documenting that at least 141 species of mammals occurred in the protected area. They reviewed the historical and present-day distributions, systematics, and ecology of each species. This

research was the first such elevational transect undertaken in the Neotropics. Three species of primates inhabit the Caribbean lowlands of Costa Rica, the mantled howler monkey, Central American spider monkey, and white-faced capuchin monkey. All three species were widely distributed throughout the Caribbean lowlands historically. During the early 1950s, primate populations throughout Central America were ravaged by an epidemic of mosquito-borne yellow fever (Fishkind and Sussman 1987, Timm 1994). Primates were observed only infrequently at La Selva between the late 1960s and early 1980s. Fortunately, all three species rebounded and they became more abundant than they were in the 1960s and late 1970s. Today capuchin, howler, and spider monkeys can be seen almost daily in protected areas and nearby for-

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est fragments, often in large groups. Capuchin and howler monkeys can occupy quite small fragments, moving along fencerows. Capuchins living in close proximity to banana plantations feed on ripe bananas from the plantations. Historically, howler monkeys were the most abundant primates in the Caribbean lowlands, and this still may be the case today. A sighting of the night monkey (Aotus) at La Selva has never been confirmed or repeated. The order Carnivora deserves special mention, not because there have been many studies on these animals, but because of their critical role in ecosystems (Terborgh 1988) and because they represent some of the animals most sought after by researchers and visitors alike. The most commonly seen species of the Carnivora are actually omnivorous or frugivorous— the white-nosed coati (Nasua narica), kinkajou (Potos flavus), and tayra (Eira barbara). The northern raccoon (Procyon lotor) occurs in low density in this area, which is interesting given its extremely wide distribution from southern Canada to central Panama and its high abundance in other areas of its range. The Neotropical otter (Lontra longicaudis) can be seen along streams and its fecal remains of fish and crustacean debris can be found on rocks. The ocelot (Leopardus pardalis) is the most frequently seen of the cats; it adapts well to disturbed habitats and can be found in small fragments, although little is known about how these populations are affected by fragmentation and the development of roads. Jaguars (Panthera onca) and pumas (Puma concolor) are the two large cats found in the area. The jaguar is now extremely rare, especially in the lowlands, although wandering individuals are occasionally seen. The puma, on the other hand, although not abundant, is more common than the jaguar and is seen regularly at La Selva. Given the number of observations in recent years in many areas of the country, it appears as if puma numbers are increasing. The majority of sightings at La Selva are in areas where collared peccaries are frequently observed. Most of the data collected on felines in the Caribbean lowlands come from camera-trapping efforts by TEAM (the Tropical Ecology Assessment and Monitoring project of Conservation International, CI), a long-term biodiversity monitoring program that has been successful in capturing pictures of elusive animals from the lowlands (Ahumada et al. 2011). The coyote (Canis latrans), a generalist predator, recently expanded its range in Costa Rica to include the Caribbean lowlands. Costa Rica has a rich and diverse bat fauna with all of the families and feeding niches found in the New World represented. There are currently 117 species of bats known from the country, which means that more than 50% of Costa Rica’s terrestrial mammals are bats. The middle and higher elevation slopes have received far less study than

have the lowlands. The Caribbean lowland zone has a fauna of at least 71 bat species that includes all of the Neotropical families and most of the genera, as well as all of the feeding niches. More research has been undertaken on bats in the Caribbean lowlands than has been undertaken on all other Costa Rican mammals combined throughout all of the country. La Selva, with its rich bat fauna and ready access to both mature forest and varying stages of second growth, has been the center of bat research in Costa Rica for nearly five decades. The Tirimbina Biological Reserve has also become an important center of bat research in the past decade. Early studies on bats at La Selva focused primarily on distributions, basic ecology, and systematics, providing a background for in-depth studies of behavior and ecology, as well as for assessing recent changes in distribution and abundance. LaVal (1977) reported on the distribution of several then poorly known species that he found at La Selva, including the first records of the thumbless bat (Furipterus horrens). Inexplicably, this species has never again been detected in Costa Rica despite the intensive netting and acoustical monitoring efforts in the lowlands. Critical to later studies on ecology and conservation of bats has been the presence of voucher specimens that the early researchers deposited in scientific collections and detailed keys for the identification of species, which were based heavily upon studies undertaken at La Selva (Timm and LaVal 1998, Timm et al. 1999). When the white tent-making bat (Ectophylla alba) was discovered at La Selva, it was considered one of the rarest of New World bats and little was known of its biology (Timm 1982). Research has been undertaken on this species over several decades there and at Tirimbina, documenting that it alters the shape of Heliconia leaves by cutting the midrib along the length of the leaf, causing the sides of the leave to collapse down around the bats and forming a roost site that protects the bats from predators as well as acting as a rain shield. Research on the tent-making bat species (including Dermanura phaeotis, D. watsoni, Uroderma bilobatum, Vampyressa thyone) has provided several exciting new insights into bat biology (LaVal and Rodríguez-Herrera 2002, Rodríguez-Herrera et al. 2007, 2008, Rodríguez-Herrera and Tschapka 1999, Timm 1982, 1984, 1985, 1987). Numerous other studies with nectar- feeding bats (Greiner et al. 2013, Sperr et al. 2009, Tschapka 2003, Voigt 2004, 2013), sac-winged bats (Voigt 2005, Voigt et al. 2008), vampire bats (Voigt et al. 2012), and others make this group of lowland Caribbean vertebrates one of the best studied in all of the New World tropics. There have been few ecological studies on rodents in the Caribbean lowlands almost certainly because most species

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are found in low numbers and are difficult to capture. The most recent ecological study was on the vesper mouse, Nyctomys sumichrasti (Rodentia: Cricetidae), a poorly known, arboreal, nocturnal species found throughout much of Central America. Romero and Timm (2013) documented that vesper mice have 1:1 sex ratios, they reproduce year-round, and litters may occur in rapid succession. Litter size is small with a mode of two, and embryos are not evenly distributed across the uterine horns contrary to hypotheses predicting that arboreal species would balance weight distribution. In a recent synthesis of group dynamics, behavior, and current and historical abundances of peccaries in the Caribbean lowlands, Romero et al. (2013) documented that collared peccaries were historically found in quite low numbers, whereas white-lipped peccaries were abundant being found in large herds throughout the region. During the 1960s white-lipped peccaries declined, and are now extirpated from most of the lowlands. On the other hand, beginning in the late 1970s, collared peccaries increased in numbers and are now abundant at La Selva, where they are protected. Collared peccaries do not exhibit a habitat preference between primary and secondary forests, although they may behave differently in the two forest types. Plant– Animal Interactions

Interactions between plants and animals have profound impacts on ecosystem attributes. Here we focus on two particular types of interactions— herbivory and seed dispersal. Herbivory Rates in Caribbean Lowland Forests

Summarizing the complex theoretical framework of plant– herbivore interactions goes beyond the scope of this chapter (for three excellent reviews of this topic see Barone and Coley 2002; Coley and Barone 1996; Marquis and Braker 1994). However, it is important to note that many of the studies conducted in the Caribbean lowlands of Costa Rica represent part of the foundations of current herbivory theories. Most of the biomass in tropical rain forests is concentrated in the canopy (Rinker and Lowman 2001) and, therefore, most of the interactions between plants and their herbivores (in absolute terms) would be expected to occur in the upper strata of the forest (Lowman 1995, Rinker and Lowman 2001). In the canopy, however, leaves fully exposed to the sun suffer significantly lower herbivory rates than do leaves in the shade; research in tropical rain forests in Australia and Panama suggests that herbivory rates are higher in understory plants than in the forest canopy (Lowman 1995). In mature moist tropical forests, it has been estimated

that understory vegetation contains only about 3% of the aboveground biomass (Clark et al. 2001). The available estimates of herbivory rates in the Caribbean lowland forest of Costa Rica, however, are mostly for understory plant species so the comparison between canopy and understory herbivory for these forests cannot be made at this time. Two community-level studies at La Selva (one including 77 plant species and the other covering 45 species) revealed herbivory rates of 12.4% and 8.6%, respectively (Marquis and Braker 1994). These estimates are within the 7.0%– 20.3% average herbivory estimates for other tropical rain forests understories, and are higher than the herbivory rates reported for temperate forests (Marquis and Braker 1994). Herbivory by Vertebrates

A study performed in the Sábalo creek, a fourth-order stream bordering La Selva Biological Station, found that most of the fish species are herbivores. Non-planktonic plant matter represented more than 25% of the diet of 77% of the species (Wooton and Oemke 1992). Fish species including more than 50% of plant matter in their diets include Astyanax fasciatus, Brycon guatemalensis, Bryconamericus scleroparius, Melaneris chagresi (Characidae), Cichlasoma tuba, C. alfari, C. septemfasciatum, C. nigrofasciatum, C. nicaraguense (Cichlidae), and Neoheterandria umbratilis (Poeciliidae) (Wooton and Oemke 1992). In the canopy, the largest and most conspicuous lizard is the green iguana (Iguana iguana). Juvenile green iguanas feed on both leaves and arthropods (Hirth 1963). Adults are mostly herbivorous, feeding on leaves, flowers, and fruits (Guyer and Donnelly 2005). In the understory, two folivorous turtles are present— the brown wood turtle (Rhinoclemmys annulata) and the black wood turtle (Rhinoclemmys funerea). The diets of both species include more than 50% of plant tissue (Guyer and Donnelly 2005). The brown wood turtle feeds on vines, shrubs, and ferns in the forest understory, and the black wood turtle forages terrestrially along river edges, usually at night (Acuña-Mesén 1998, Guyer and Donnelly 2005, and see Pringle et al., chapter 18 of this volume). In tropical rain forests, the biomass of folivorous mammals is 1.5 to 5 times higher in the canopy than in the understory (Leigh 1999). This is not surprising, as most of the annual net production of vegetation in tropical rain forests is concentrated in the forest canopy (Clark et al. 2001, Lowman 1995). Four predominantly folivorous mammal species are found in the canopies of Caribbean lowland forests: the howler monkey (Alouatta palliata), the brown-throated three-toed sloth (Bradypus variegatus), Hoffmann’s twotoed sloth (Choloepus hoffmanni), and the Mexican hairy porcupine (Coendou mexicanus). The diets of these four

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species are composed of more than 50% leaf tissue. Other canopy dwellers are the Central American spider monkey (Ateles geoffroyi) and the white-headed capuchin monkey (Cebus capucinus). These two species are mostly frugivorous; however, they complement their diets with leaves (Marquis and Braker 1994). In the understory, five mammal species are the predominant folivores— the forest rabbit (Sylvilagus brasiliensis), the collared peccary (Pecari tajacu), the white-tailed deer (Odocoileus virginianus), the Central American red brocket (Mazama temama, formerly M. americana), and the locally rare Baird’s tapir (Tapirus bairdii). The white-lipped peccary (Tayassu pecari), a primarily herbivorous mammal that once inhabited the Caribbean lowland of Costa Rica, almost has been extirpated (Romero et al. 2013). Herbivory by Invertebrates

Insects are the most important herbivores in the tropical rain forest. In addition to the outstanding species diversity of this group, insect herbivores contribute to most of the herbivory in both canopy and understory plants (Lowman 1995, Rinker and Lowman 2001). One example of this high diversity is the insect community at La Selva. At least 171 families of phytophagous insects are present in this forest alone (Coley and Barone 1996). Most of these insects have specialized diets, feeding on one or a few plant species (Dyer et al. 2007, García-Robledo and Horvitz 2011, 2012a,b). In this section we discuss some aspects of the natural history for the main insect herbivore guilds, and also some plant– herbivore associations that have been thoroughly studied in the Caribbean lowlands. In Costa Rica’s Caribbean lowland forests, most associations between plants and sap-feeders remain unknown. A study on the distribution of cast nymphal skins of the sundown cicada (Fidicina mannifera, Homoptera: Cicadidae) suggests a potential association between this insect and plants from the family Fabaceae (Young 1980, 1984). Another large homopteran found in the region, the peanuthead bug (Fulgora laternaria, Homoptera: Fulgoridae) feeds on the sap of Simarouba amara (Simaroubaceae) (Orlando Vargas, personal observation). In the Caribbean lowlands, treehoppers are apparently generalists, feeding on a wide range of host plants (Wood 1993). Leaf-miners are endophytic herbivores that feed within the tissue of leaves during larval stages. The orders Coleoptera, Diptera, Hymenoptera, and Lepidoptera include leaf-mining species. Tropical leaf-miners have very restricted diets, with most species being monophagous. At La Selva, 130 species of leaf-mining beetles (71 Buprestidae, 41 Hispinae, 18 Curculionidae) were recorded (Hespenheide 1985, 1991). Most leaf-mining species consume a very

small fraction of the leaf tissue of their host plants, and it is suggested that herbivory by leaf-miners does not represent a significant contribution to the total herbivory in tropical rain forests. Leaf-cutter ants are the predominant herbivores in the neotropics (Perfecto and Vandermeer 1993). It is estimated that leaf-cutting ants consume between 12 and 17% of the total leaf production (Cherrett 1986, Haines 1978, Wirth et al. 1997). In the Caribbean lowlands, the leaf-cutting ant Atta cephalotes is a common herbivore in agricultural areas, secondary forests, and old-growth forests (Perfecto and Vandermeer 1993). During the past years scientists have been working on research topics such as the symbiotic interactions among leaf-cutting ants, basidiomycete fungi, and nitrogen-fixing bacteria (Pinto-Tomas et al. 2009); the chemical ecology of plant– Atta interactions (NicholsOrians 1991a,b,c,d); and foraging strategies, demography, and leaf-cutting ants’ effects on soil changes, seedling recruitment, and forest regeneration (Farji- Brener 2001, 2005, Farji-Brener et al. 2010, Farji-Brener and Illes 2000, Folgarait et al. 1996, Peñaloza and Farji-Brener 2003). The ecology of Neotropical acridid grasshoppers (families Acrididae and Romaleidae) is best known from species in the Caribbean lowlands as the result of extensive research on this group at La Selva (Braker 1986, 1989a,b, 1991, 1993, Rowell 1978, 1983a,b,c,d, 1985a,b). Although most temperate species of acridid grasshoppers are generalists, in neotropical rain forests they can display diet breadths that range from strict specialization to one host plant to generalist diets (Marquis and Braker 1994). For example, at La Selva, one species of grasshopper from the subfamily Copiocerinae feeds only on geonomid and bactroid palms (Marquis and Braker 1994). In contrast, the grasshopper Microtylopteryx hebardi (Subfamily Ommatolampinae) feeds on at least 60 species of plants in 17 monocotyledonous and dicotyledonous families (Braker 1986, 1991). In the Caribbean lowlands, grasshoppers from the subfamily Proctolabinae are mostly specialists, feeding on plants from the families Nyctaginaceae and Solanaceae. Grasshoppers from the subfamily Ommatolampinae and the family Romaleidae usually have broader diets (Marquis and Braker 1994). Lepidopteran larvae are an important component of insect herbivore communities in tropical rain forests. In some forests, caterpillars may account for more than 95% of the total number of species, number of individuals, and biomass of externally feeding holometabolous larvae (Novotný and Basset 2000, Novotný et al. 2002). In the Caribbean lowland forests of Costa Rica, larval lepidopterans are known to have a strong impact on seedling recruitment (Dyer et al. 2010). In the Caribbean lowlands, herbivory rates by Lepidop-

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tera are known for understory shrubs of the genus Piper (Piperaceae). In a study performed in four Caribbean forests (Bijagual, El Bejuco, and Tirimbina Biological Reserve, and Parque Nacional Braulio Carrillo), the average amount of herbivory attributed to lepidopterans on new leaves of Piper shrubs is 82.3% (Dyer et al. 2010). The lepidopteran fauna in the Caribbean lowland forest of Costa Rica has been thoroughly studied in comparison to other Neotropical forests. Two long-term projects have generated comprehensive inventories for adult butterflies at La Selva and in Braulio Carrillo (i.e., the Arthropods of La Selva Project [ALAS] and the Tropical Ecology Assessment and Monitoring Network– Costa Rica [TEAM project– Volcán Barva]). In the Sarapiquí area, the associations of caterpillars and their host plants are known for 3,028 lepidopteran species and morphospecies (Gentry and Dyer 2002). Caterpillars at La Selva are associated with at least 307 host plant species (Dyer and Gentry 2002). The genus Piper (Family Piperaceae) is a diverse pantropical genus of shrubs, vines, and small trees (Dyer and Palmer 2004). One third of the ca. 1,000 described species of Piper are Neotropical in distribution (Dyer and Palmer 2004). In the Caribbean lowlands of Costa Rica, plants in the genus Piper have been the focus of several remarkable studies on plant– herbivore interactions. Studies of plant– herbivore interactions with Piper trigonum (formerly known as Piper arieianum) represent the initial evidence that in a tropical plant, resistance against herbivore attacks has a genetic basis and an impact on life history traits such as growth, seed production, and seed viability (Marquis 1984, 1990, 1992). Current research on Piper-arthropod interactions in the Caribbean lowland forests of Costa Rica includes topics such as the chemical ecology of plant– herbivore interactions and the direct and indirect effects of trophic networks on herbivory rates (Dyer and Palmer 2004). At present, the genus Piper is considered to be an emerging model system to understand evolutionary and ecological processes in plant– animal interactions (Dyer and Palmer 2004). The insect herbivore fauna of Piper in the Caribbean lowland forests of Costa Rica is diverse. Specialist herbivores include geometrid moths (Eois spp. and Epimecis sp.), skippers (e.g., Quadrus cerealis), and stem borer weevils from the genus Ambates. Specialist flea beetles (genus Physimera) feed on leaf tissue. Generalist folivores include apatelodid, limacodid, and saturniid moths. Herbivory by leaf-cutting ants and orthopterans is also common (Dyer and Palmer 2004). The association between plants from the order Zingiberales and beetles from the genus Cephaloleia (Chrysomelidae: Cassidinae) is one of the oldest and most conservative plant-herbivore interactions (García-Robledo and Staines 2008, Wilf et al. 2000). In the literature, Cephaloleia beetles

are frequently included in a non-monophyletic group known as the “rolled leaf” beetles, because adults feed and mate in the scrolls formed by the young leaves of their host plants (García-Robledo and Horvitz 2011, 2012a). In the Caribbean lowlands of Costa Rica, associations between Cephaloleia and their host plants have been investigated over the past three decades (García-Robledo and Horvitz 2012b). Research on the genus Cephaloleia includes the use of plant chemical signals for the location of host plants (García-Robledo and Horvitz 2009), the effects of plant chemical defenses and nutrient contents on insect performance (Auerbach and Strong 1981, Gage and Strong 1981), population dynamics ( Johnson 2004a,b, Johnson 2005, Johnson and Horvitz 2005, Morrison and Strong 1981) and the structure of Cephaloleia species assemblages (Strong 1981, Strong 1982a,b). Cephaloleia species are also model organisms used to understand plant– herbivore evolutionary processes and the diversification of tropical insect herbivores (García-Robledo and Staines 2008, McKenna and Farrell 2005, 2006, Strong and Wang 1977, Wilf et al. 2000). The species composition and diet breadth of Cephaloleia beetles is particularly well known for La Selva (GarcíaRobledo et al. 2013). In this forest, at least 40 species of Cephaloleia are known to associate with at least 43 native plants from the order Zingiberales (García-Robledo 2010, Staines 1996). Diet breadths of Cephaloleia species at La Selva range from strict monophagous, such as Cephaloleia fenestrata which feeds only on Pleiostachya pruinosa (Marantaceae), to generalist species, such as Cephaloleia belti, which feeds on 15 plant species from three families of Zingiberales (García-Robledo and Horvitz 2009, 2011, 2012a). Frugivory and Seed Dispersal

More than 90% of the woody plant species in a Caribbean lowland forest in Costa Rica have seeds adapted for dispersal by animals (Chazdon et al. 2003). Animals disperse seeds via endozoochory (defecation or regurgitation of intact, ingested seeds), ectozoochory (expectoration or dropping of seeds carried externally by a disperser), or hoarding (burial of seeds in subsurface caches). Dispersed seeds can be moved many times (primary dispersal, secondary dispersal) and by multiple animals prior to seed death or seed germination (Van der Wall and Longland 2004). In this section we will summarize the activities of animal seed dispersers that have been studied in the Caribbean lowland forests of Costa Rica: ants, fish, birds, volant mammals, and terrestrial mammals. Numerous species of tropical leaf litter ants act as secondary seed dispersers, removing small seeds from fallen

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fruits or from the feces of frugivores and transporting the seeds into nests (Kaspari 1993, Levey and Byrne 1993). Ants can act as seed predators, eating and killing some seeds they encounter, but a portion of seeds taken by ants may be discarded intact and in viable condition within refuse piles (Levey and Byrne 1993, García-Robledo and Kuprewicz 2009). Ants may enhance seed germination success and seedling growth via seed cleaning, scarification, or deposition in a nutrient-rich microhabitat that is favorable for seedling establishment (Horvitz 1981, Passos and Oliveira 2002, García-Robledo and Kuprewicz 2009). Usually ants remove seeds only short distances (a few meters) from parent plants and thus may not be as effective at seed dispersal as animals that deposit seeds farther from the source (Howe and Smallwood 1982). Lowland rain forests on Costa Rica’s Caribbean slope contain high ant diversity (437 species found at the 1,600 ha La Selva; Longino et al. 2002), including many leaf litter– dwelling species that interact with fruits and seeds (Kaspari 1993). In field trials involving arrillate seeds of Renealmia alpinia, García-Robledo and Kuprewicz (2009) observed that at least four species of leaf-litter ants removed seeds up to 1.8 m from the source. In this study, Ectatomma ruidum removed seeds rapidly from sources and enhanced the germination of seeds brought into nests. Ants of the genus Pheidole, commonly found throughout forests in the Caribbean lowlands, readily remove and cache Miconia nervosa and M. centrodesma seeds in refuse piles, having both positive and negative effects on seed survival (Levey and Byrne 1993). Small seeds from the genus Miconia appear particularly attractive to leaf-litter granivorous ants with at least 22 species from the tribes Attini, Ectatommini, Ochetomyrmicini, Pheidolini, and Solenopsidini noted removing M. affinis seeds from feces of frugivores (Kaspari 1993). Seeds of many Calathea species found throughout the Caribbean lowlands possess eliasomes that attract ant seed dispersers including ants from the genera Odontomachus, Pachycondyla, Ectatomma, and Aphaenogaster (Le Corff and Horvitz 1995 and references therein). Frugivory by fish is an understudied realm of seed dispersal biology on the Caribbean slope of Costa Rica. Seed dispersal by fish has been more extensively studied in the flooded forests of central Amazonia where many tree species have buoyant, hydrochorous seeds (Kubitzki and Ziburski 1994 and references therein). Seed dispersal by fish may contribute to distribution patterns of riparian species. Studies of Brycon guatemalensis, an abundant frugivorous fish found in the rivers throughout La Selva Biological Station, have found that this species acts as a major disperser of Ficus insipida and F. glabrata seeds (Banack et al. 2002). Brycon guatemalensis consume copious amounts of Ficus

seeds and contribute to the upstream dispersal and establishment of this riparian tree species (Horn 1997). Most Neotropical bird species are, to some extent, frugivorous and may serve as effective seed dispersers for a variety of plant species. Avian frugivores can remove many fruits while foraging and usually defecate or regurgitate intact seeds long distances from source plants (Howe 1977, Levey 1987). Seed deposition within bird feces may enhance seed germination or subsequent removal by secondary seed dispersers (e.g., ants, rodents) (Levey and Byrne 1993). Frugivory and seed dispersal by birds in the Caribbean region of Costa Rica have been critically reviewed by Levey et al. (1994)— therefore, we focus here on studies conducted after the publication of the Levey et al. (1994) review. The Caribbean lowland region of Costa Rica is especially speciose with regard to birds, containing at least 411 species of which 256 breed in the region (Levey and Stiles 1994). This area contains one of the highest diversities of birds in Central America (also, see previous sections in this chapter). Some lowland forest frugivorous birds feed exclusively on fruits (e.g., Corapipo altera, Euphonia gouldi, Manacus candei, Pipra mentalis) while others consume fruits to supplement insectivorous diets (Blake et al. 1990). Many resident avian species recorded in La Selva consume fruits and seeds and over 60% of altitudinal migrants are frugivores that track seasonal fruit abundances (Levey and Stiles 1994). Loiselle and Blake (1999) evaluated the seed dispersal effectiveness of six frugivorous birds that are common in the region: Mionectes oleagineus, Pipra mentalis, Corapipo leucorrhoa, Hylocichla mustelina, Chlorothraupis carmioli, and Euphonia gouldi. Bird species differed in their reliabilities as consumers of fruits from four species of Melastomataceae and seed deposition patterns differed by bird and plant species. Overall seed dispersal effectiveness can differ widely, even among fruit-eating bird species with high dietary overlap. A study involving seed dispersal agents in plantations and abandoned pastures in the region found that birds are among the most important seed dispersers in plantation habitats, potentially accelerating forest succession (Zamora and Montagnini 2007). Forests of differing ages contain floristic differences that may also affect frugivory and seed dispersal by birds. Overall sugar concentrations of fruits found in secondary lowland forests are higher than those of fruits in primary forests, which results in faster fruit removal rates by birds in secondary habitats, although proportions of fruit removal do not differ among forests (Lumpkin and Boyle 2009). Though less studied in the Caribbean lowlands, large frugivorous birds such as toucans and aracaris (family Ramphastidae) consume high quantities of fruits and disperse

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both large and small seeds over long distances via endozoochory. Though usually found in the forest canopy, Pteroglossus torquatus, Ramphastos sulfuratus, and R. swainsonii have been observed consuming fruits and seeds of the ginger Renealmia alpinia in the understory (García-Robledo and Kuprewicz 2009). Toucans may also play an integral role in the dispersal and establishment of some large-seeded palms commonly found in the Costa Rican lowlands (e.g., Iriartea deltoidea). Mixed parentage aggregations of I. deltoidea seedlings located beneath adult trees are governed by the seed handling behaviors and movement patterns of these large ramphastids (toucans) (Sezen et al. 2009). Seed dispersal by bats has received much attention in the Neotropics with many studies conducted in the Caribbean lowland forests of Costa Rica. Bats can disperse small seeds (e.g., Ficus spp., Cecropia spp.) via endozoochory, whereas they disperse large seeds (e.g., Dipteryx panamensis, palm seeds) by dropping them during flight or under feeding sites and roosts (Fleming and Heithaus 1981, Kelm et al. 2008, and references therein). Bats may be highly effective seed dispersers owing to their capability for long distance seed dispersal among various habitats (Heithaus and Fleming 1978). Most phyllostomid bats found in Caribbean lowland forests are highly frugivorous. Artibeus, Carollia, and Dermanura consume fruits and seeds from many understory and canopy plants in the region (Levey et al. 1994). Artibeus jamaicensis and Dermanura watsoni have been evaluated as highly effective dispersers of seeds from the fig Ficus insipida (Banack et al. 2002). Within the Sarapiquí Basin of the Caribbean slope, Melo et al. (2009) found 46 species of large (>8 mm) seeds beneath leaf tents constructed by D. watsoni. Their findings had implications on seed and seedling distributions near bat tents within forested habitats— seed densities and seedling abundances were higher under bat tents than in areas away from tents (Melo et al. 2009). Bats, owing to their abilities to forage, feed, and roost in diverse habitats, may serve as effective natural reforestation agents. Artificial roosts constructed throughout a forest– pasture mosaic in the Caribbean lowlands successfully recruited 10 species of bats, including five frugivores/nectarivores (Kelm et al. 2008). These bats transported many seeds from earlysuccessional plants into degraded lands, potentially leading to forest succession within these pasturelands (Kelm et al. 2008). However, further evaluations of seed germination success and seedling growth are needed to evaluate the effectiveness of bats as reforestation agents (Holl 2008). Seed dispersal and frugivory by terrestrial mammals is a common phenomenon in the forests of the Costa Rican Caribbean slope. Numerous terrestrial species are known fruiteaters, including agoutis (Dasyprocta punctata), collared peccaries (Pecari tajacu), armadillos (Dasypus novemcinc-

tus), coatis (Nasua narica), tayras (Eira barbara), kinkajous (Potos flavus), pacas (Cuniculus paca), and numerous species of opossums. Most Carnivora likely also consume fruits and seeds to supplement their diets, though their effectiveness as seed dispersers is virtually unknown in this region. Small rodents, particularly the heteromyid rodent Heteromys desmarestianus, consume and cache small and large seeds, potentially serving as effective seed dispersers for some plants (especially palms) (Fleming 1974). Many terrestrial rodents consume and destroy seeds while foraging, acting as significant seed predators and only incidental seed dispersers (Smythe 1986). The seeds of the palm Socratea exorrhiza that fall to the forest floor are rapidly encountered by small (H. desmarestianus, Proechimys semispinosus) and mid-sized (D. punctata) terrestrial mammals (Kuprewicz 2010, 2013). Predation of seeds by terrestrial mammals tracks fruiting patterns, with lower predation levels during peak fruit set compared to higher levels at the end of the fruiting season (Notman and Villegas 2005). Seed caching, however, does not appear to follow these fruiting patterns (Notman and Villegas 2005), and hoarding events by agoutis at La Selva are relatively rare (Kuprewicz 2010, 2013). In forests protected from human hunting in the Caribbean lowlands (such as La Selva), local populations of collared peccaries have recently increased, likely due to direct effects (fewer peccaries killed by hunters than previously) as well as indirect effects (release from predators [large felids] that remain uncommon in the area despite reduced human hunting). Collared peccaries forage singly or in small groups (Romero et al. 2013) and are seed predators that consume and kill many large seeds (e.g., Dipteryx panamensis, Iriartea deltoidea, Mucuna holtonii, Socratea exorrhiza) (Kuprewicz and García-Robledo 2010, Kuprewicz 2010, 2013). Peccaries may disperse some seeds via endozoochory or expectoration (Beck 2005), but in the Caribbean forest of La Selva, they act primarily as seed predators; this behavior negatively affects seedling recruitment and may have dramatic implications for future tree distributions and plant propagation (Kuprewicz 2010, 2013). A comparison of seed removal and seed fates in two Caribbean lowland forests (Tirimbina Rain Forest Center, a hunted forest, and La Selva, a forest protected from hunting) found that some seed species (Carapa nicaraguensis, Lecythis ampla, Pentaclethra macroloba) had higher seed removal rates in La Selva when compared to Tirimbina. Overall seed dispersal was also higher at La Selva than at Tirimbina (Guariguata et al. 2000). Removal of large terrestrial frugivorous mammals through hunting can have complex effects on the seed dispersal, seed survival, and resultant seedling demography in defaunated regions (Wright et al. 2000).

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People and Nature Human Populations and Demography

As indicated earlier, precontact indigenous populations were substantial but not nearly the size of Maya, Aztec, and Inca populations to the north and south. The Caribbean lowlands constitute part of the Costa Rican archaeological subregion identified as Atlantic Highlands and Watershed. The best-known archaeological site in this area is the Las Mercedes site, uncovered by the railroad construction of Minor C. Keith in the 1870s, and currently located on the campus of EARTH University in Guápiles. Keith removed more than 15,000 items and distributed them among several museums in the United States. In the 1890s the Swedish archaeologist Carl V. Hartman also worked at Las Mercedes and sent many valuable objects to Sweden. This site is dated at about 1,000– 2,000 years old and therefore does not provide insight into the earliest indigenous populations (Snarskis 1976). Many additional archaeologically valuable locations are scattered around the Caribbean lowlands, some of them currently under excavation and others undiscovered or untouched. The human population of Costa Rica’s Caribbean lowlands grew slowly throughout the colonial period after the demographic collapse of the indigenous populations (Augelli 1987). Spanish settlers tended to establish themselves in the Central Valley (Palmer and Molina 2004). The Caribbean coast is known during these years for the exploits of a few colorful English and Dutch pirates— the Nicaraguan Caribbean town of Bluefields, for instance, is named after the Dutch pirate Abraham Blauvelt— and not for any substantial settlements of colonists or indigenous people (Ross and Capelli 2003). After Costa Rica’s independence from Spain in 1821, the Central Valley population centers (San José, Cartago, Alajuela, Heredia) continued to expand— a trend that was enhanced as coffee production became the dominant economic force in the country. The entire human population of Costa Rica is estimated to have been about 19,000 people in 1770, then 52,000 in 1801, then 200,000 in 1900, then 875,000 in 1950 (Augelli 1987). Sixty years later Costa Rica’s population size had been multiplied by a factor of five, reaching a total of 4,564,000 inhabitants (Centro Centroamericano de Población 2011). Significant populations of Europeans and North Americans did not arrive in the Caribbean lowlands until the construction of the railroad between Alajuela and the Caribbean coast in the late nineteenth century. The railroad was built to transport coffee, Costa Rica’s major agricultural export crop, from the central highlands (where it was grown) to the Caribbean port of Limón for export to Europe. The builder and financier of this railroad, US investor Minor C.

Keith, started the Caribbean lowland banana industry to help finance the railroad project. Excellent, extensive treatments of both the coffee and the banana industries of Costa Rica are recommended (Chapman 2007, Chomsky 1996, Koeppel 2008, Paige 1997, Palmer and Molina 2004, Ross and Capelli 2003). West Indian Afro-Caribbean workers were brought to the Costa Rican lowlands to work on the railroad and on the banana plantations. By 1883 there were 902 Jamaicans in Limón Province, and by 1927 there were 18,003. These workers were not granted Costa Rican citizenship until 1948, and they were not allowed to leave Limón Province, even to work on the Pacific banana plantations. Today about one-third of the population of Limón Province is made up of West Indian immigrants and their descendants (Biesanz et al. 1987). The distinctive language and culture of the Limón area are due to the influence of these Afro-Caribbean workers and their descendents. As mentioned previously, Puerto Limón is the largest city in the Caribbean lowlands. Although it is the second largest city in Costa Rica, its population of 63,000 puts it at a distant second to the capital of San José with its population of about 335,000. Other Caribbean-side population centers include Guápiles (~19,000), Siquirres (~18,000), Guácimo (~7,000), and Puerto Viejo de Sarapiquí (~6,000). Human settlement in the Caribbean lowlands increased dramatically during the 1960s, 1970s, 1980s, and 1990s owing to at least three factors: Costa Rica’s extremely high birth rate before 1960 (Coale 1983), a deliberate governmental policy to move people from the Central Valley to the “hinterlands,” and farm labor immigration from other Central American countries (particularly from Nicaragua). The birthrate has fallen in recent years (Coale 1983) but the Caribbean lowlands continue to see increasing populations. Agriculture and Pesticides

The Caribbean lowland area of Costa Rica is threatened by the same dangers that affect other tropical systems— deforestation, loss of biodiversity, genetic fragmentation of plant and animal populations, spread of alien invasive species, climate change, human population increase, and the pressure to value short-term economic gains over long-term sustainability. Some of these subjects are treated in other sections of this chapter. Here we focus on one particular theme, that of agricultural development and pesticide use, because it is a topic that is critically important in its own right and also because it brings many of these other areas into clear focus. A consideration of agriculture and pesticide use is also intimately related to emerging issues such as valuation of ecosystem services, global food security, poverty alleviation, the objectives of the Millennium Eco-

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system Assessment, and the new Sustainable Development Goals (SDGs). Globally, the use of pesticides (insecticides, fungicides, rodenticides, herbicides, and germicides) has increased dramatically in the past seventy years (Carvalho 2006) and every corner of the planet, including Arctic ice, bears traces of these chemicals (Chernyak et al. 1996, Cone 2006, Pelley 2006). Much early use of insecticides was related to mosquito/malaria control ( Jaga and Dharmani 2003, Lubick 2007), but a significant proportion of pesticide application has now been turned toward agricultural food production (Monge et al. 2005, Wesseling et al. 1999). Although the use of pesticides has certainly led to increased food production— the so-called Green Revolution— (Cooper and Dobson 2007), some of these positive effects are being lost through evolving resistance to the chemicals by pests and non-target organisms (Brausch and Smith 2009, Jansen et al. 2011, Nolte 2011, Raymond et al. 2001) or offset by various direct and indirect calculated costs of pesticide use. Pesticides have been shown to have serious human health consequences, both acute (Soares and Porto 2009) and chronic (Abhilash and Singh 2009, Charboneau and Koger 2008, Nag and Raikwar 2011, Yearout et al. 2008), as well as a range of environmental impacts including soil and water contamination (Liess and von der Ohe 2005) and non-target organism toxicity (Berny 2007, Kendall and Smith 2003, Pisani et al. 2008). The role of pesticides in the endocrine and developmental disruption of wildlife and humans (see Buchanan et al. 2009, Casals-Casas and Desvegne 2011, Mnif et al. 2011, Soin and Smagghe 2007 for reviews) is also becoming an increasingly powerful concern. Both the negative and positive aspects of global agricultural development and pesticide use are seen in microcosm with the specific case of the Caribbean lowlands of Costa Rica over the past several decades. DDT was used widely and heavily in Costa Rica from 1957 to 1985 (to the tune of 1,387 total tons during that period) to control mosquito-borne malaria (Pérez-Maldonado et al. 2010, Duszeln 1991). Today DDT and other banned organochloride pesticides (OCPs)— widely known as persistent organic pollutants (POPs)— have a relatively low and uniform distribution in soils across the country (Daly et al. 2007a) but, as recently as 2009, levels of DDT in soil and children’s blood serum were considered above acceptable levels in two rural communities in the Limón area (Pérez-Maldonado et al. 2010). Pesticide use in Central America doubled between 1980 and 2000 (Wesseling et al. 2005). During the 1990s, Costa Rica’s annual use of 4 kg of pesticides per inhabitant and 38 kg per agricultural worker was the highest in all of Central America (Wesseling et al. 2001). In recent years, Costa Rica has been at the top of the world’s coun-

tries in pesticide use (Polidoro et al. 2008, World Resources Institute 2007), on the basis of the number of kg of active ingredients applied annually to each hectare of agricultural land (52 kg a.i. [active ingradients]/ha/yr in 2000). Raw pesticide import data from 1977 to 2009 have been analyzed for Costa Rica (de la Cruz et al. 2014) and indicate increases in the variety of chemicals used, as well as their environmental hazards. Pesticides are used on large volume agricultural crops such as banana, coffee, pineapple, rice, and heart-of-palm (also called palm heart), as well as on non-traditional agricultural export crops (NTAEs) such as plantain, carrot, cassava, squash, and cut flowers. Pesticides are applied to crops for export as well as for local (within Costa Rica) consumption. A third to a half of Costa Rica’s imported pesticides are used in banana production (Castillo et al. 2006) and most of Costa Rica’s banana production today is in the Caribbean lowlands. Bananas are the world’s number one fruit consumed and in the past few years Costa Rica has been among the world’s top three banana-exporting countries, along with Ecuador and the Philippines (Barraza et al. 2011). In 2009 Costa Rica’s banana plantations covered more than 50,000 hectares and employed 35,000 workers (CORBANA 2009). The effects of chemicals used by the United Fruit Company in Costa Rica during the sigatoka (Mycosphaerella musicola) fungus outbreak of the 1930s led to an extended workers’ strike (Marquardt 2002). Decades later, the claims of worker sterility from the use of the nematicide DBCP (marketed under the name Nemagon) led to several class-action lawsuits settled out of court or in favor of the plaintiffs (Ling and Jarocki 2003). DBCP has been linked to several types of cancer among Costa Rica’s banana workers (Wesseling et al. 1996). Chlorothalonil is a pesticide currently in use on Costa Rican banana plantations, with application rates of up to 45 times per year (Chaves et al. 2007). This fungicide is considered to be highly toxic to humans (Caux et al. 1996, Margni et al. 2002, Sherrard et al. 2003) and in Costa Rica has also been shown to be toxic to fish, birds, and aquatic invertebrates (Castillo et al. 2000). Fortunately, unlike DDT, it breaks down rapidly in Costa Rica’s tropical climate (45% degradation after 24 hrs), but some residues are still present after 85 days and toxic metabolites are also persistent (Chaves et al. 2007). In Costa Rica, as has been the case elsewhere, the pesticide industry has changed from using a few broadly acting chemicals to using a wide range of active ingredients with shorter active lives (Galt 2008a). Chemicals from agricultural production find their way into the soils and rivers of the Caribbean lowlands. Sediments from clearing land for plantations also drain into the area’s rivers and modify habitat for local freshwater organ-

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isms and for more distant marine organisms. The streams receiving water from Caribbean lowland banana-processing plants are home to altered macroinvertebrate communities in the presence of pesticide levels that are well below those responsible for acute toxicity (Castillo et al. 2006). A more distant effect is produced by the Río Estrella, which drains a large area of banana plantations and discharges into the Caribbean Sea 10 km north of Parque Nacional Cahuita and the offshore coral reef (Roder et al. 2009). Aerosolized pesticides are carried from their lowland sites of application to higher elevations on the slopes of Volcán Barva, where they precipitate out over “pristine” mid-elevation forests (Daly et al. 2007b). Cassava growers in an indigenous Bribri community near Limón indicated that they had had no training in use of agricultural chemicals and that less than one-third of them used protective clothing during spraying (Polidoro et al. 2008). In this same community, Bribri women who worked with chemically sprayed plantains reported more respiratory problems than women who did not work in agriculture (Fieten et al. 2009). In the face of worrisome data regarding pesticide effects, there is potentially some good news. The most toxic chemicals used in Costa Rican agriculture do have less toxic alternatives (Humbert et al. 2007). An organic treatment for the post-harvest control of banana crown rot has been developed by scientists at EARTH University (Demerutis et al. 2008). Some international banana companies have sought Rainforest Alliance certification, which lends the required stamp of “sustainability” to products sold to segments of the European market. In Costa Rica, education and extension services also effectively reduce the intensity of pesticide use (Galt 2007). For example, on a potato farm near Cartago pesticide use was reduced if there were minors (children) in the household or if the farmer had taken an agricultural course (Galt 2008b). Recent studies indicate that the current standards for pesticide residues in the destination countries are creating pressure for less pesticide use in the producing countries, including Costa Rica (Galt 2008c). Consumer groups around the world indicate a “willingness to pay” more for bread and produce in exchange for less pesticide use (Batte et al. 2007, Boccaletti and Nardella 2000, Chalak et al. 2008, Florax et al. 2005, Foster and Maurato 2000, Kahn 2009). Adherence to “developed country pesticide standards” in developing countries (Okello and Swinton 2010) is one powerful way to break the ominous “circle of poison” of the recent past whereby chemicals banned in developed nations were sold and used in the Third World, only to return to the developed world as residue on imports (Weir and Shapiro 1981). In a study of pesticide use on five vegetables

(carrot, chayote, corn, green bean, and squash) grown in Costa Rica both for national use and for export, pesticide use was less on the produce bound for export to the United States (Galt 2008), reportedly because of EPA guidelines on pesticide residues. Although large-scale completely pesticide-free agriculture is probably not possible, it is entirely possible to imagine a scenario that combines the following: (1) economic incentives for the use of chemicals with lower toxicity and with lower application rates, (2) development of more organically grown and free-trade products, (3) industrial, academic, and extension training to maximize worker knowledge and safety, (4) continued and intensified consumer pressure for healthy products, (5) enforced guidelines on pesticide residues in consumer nations, (6) environmental monitoring of air, soil, and water by government and the scientific community, (7) epidemiological studies on the relation between disease and exposure to chemicals, and (8) creative high technology solutions to food security such as removing pesticides from fruit juices in the final stages of processing. Many of these efforts are currently underway, albeit not universally, in the Caribbean lowlands of Costa Rica. Costa Rica is in a position to attempt a unified approach to intensified but non-destructive agriculture because of its long history of agricultural activity, its worldrecognized conservation efforts, and the well-established multi-institutional and international scientific research being conducted within the country. Conservation

The conservation history of Costa Rica since the 1950s has been well documented and analyzed. Excellent treatments are available regarding the founding of the national park and reserve system (Boza 1993, Evans 1999, Wallace 1992), the proliferation of conservation efforts during the past 60+ years (Calvo-Alvarado 1990, Campbell 2002a, Johnson and Clisby 2009, Powell et al. 2000), and the establishment of specific projects and private reserves (Butterfield 1994, Chornook and Guindon 2008, Nadkarni and Wheelwright 2000, Wheelwright and Nadkarni 2014). Case studies of Costa Rican conservation initiatives such as payment for environmental services (Dick et al. 2010, Morse et al. 2009, Pagiola 2008, Sánchez-Azofeifa et al. 2007, Sierra and Russman 2006, Snider et al. 2003), the Mesoamerican Biological Corridor (Dettman 2006, Sader et al. 2004), the Biodiversity Law of 1998 (Miller 2011), participatory resource management (Sims and Sinclair 2008), and carbon sequestration (Lansing 2011) are also available. For many decades Costa Rica has been held up as an example to the world for the amount of its land under pro-

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tection, its sustainable ecotourism, and the strong environmental ethic among its citizens. Critics and scholars have pointed out some of the discrepancies between this image and stark reality, including illegal logging and harvesting of forest products, underfunding of national parks, negative tourism impacts on protected areas, duplicated or disorganized conservation efforts, and unequal distribution of the economic benefits of conservation initiatives (Campbell 2002a,b, Hoffman 2011, Silva 2003, Sylvester and Avalos 2009, Vivanco 2006). Several unquestionable conservation success stories do exist, however, as does a continuing willingness on the part of interested parties to invent new strategies to cope with problems that arise. The title of an article by one of the founders of Costa Rica’s National Park system, Mario A. Boza, remains as apt today as it was upon its publication— with regard to environmental solutions, “Costa Rica is a laboratory, not Ecotopia” (Boza et al. 1995). More than a dozen national parks, wildlife refuges, and biological corridors have been created in the Caribbean lowlands since 1970, when the Tortuguero area was first protected and then made into a National Park in 1975 (for a map of the region’s protected areas, see Fig. 16.2). As a heuristic exercise, we have chosen to compare the Tortuguero area to the San Juan– La Selva (SJLS) Biological Corridor because of several fascinating similarities and instructive differences in the establishment and current operations of these two areas. Among the similarities in the scenario for the creation of these two entities are (1) the realization that an iconic vertebrate species was about to be lost, (2) rapid legal action to protect the nesting areas of these animals, (3) cooperation among scientists, government officials, and representatives of non-governmental organizations (NGOs) to create and consolidate the protected areas, (4) the large size and ecological diversity of the area under protection, (5) the welcome outcome— a conservation success story— at least in terms of halting the precipitous decline of the iconic vertebrate species, and (6) increasing pressure on the protected areas from other sources in recent years. Notable differences in the two stories are (1) the dominant conservation paradigms at the time of establishment of the protected areas, (2) the funding and management of the areas, (3) the ownership of the land contained within the protected areas, (4) the extent of community income from ecotourism, and (5) the strength of international scientific research conducted in the protected areas. The 35 km stretch of the Caribbean coast between the Tortuguero and Parismina rivers has probably been a nesting ground for the Atlantic population of the green turtle Chelonia mydas and other sea turtles for many hundreds if not thousands of years (Spotila 2004). Early Spanish explor-

ers noted the vast turtle populations in this area and named the zone “Tortuguero” (place of turtles) (Ross and Capelli 2003). Indigenous people and colonial settlers harvested eggs and adult turtles for local consumption and for export (Jackson 1997, Lefever 1992), but large-scale exportation of eggs, meat, and calipee in the mid-twentieth century dramatically increased the pressure on the Costa Rican green turtle population almost to the point of extinction. Dr. Archie Carr, a turtle specialist from the University of Florida, had been monitoring these animals since 1955 and became alarmed at their rapid decline in the early 1970s (Carr 1967, Carr et al. 1978). He spoke urgently with people in the international conservation community and the Costa Rican government and prompted a series of actions over the next several years. First, an executive decree was issued in 1970, prohibiting the harvesting of turtles and their eggs along the beach and protecting a portion of the nesting area. The 19,000 ha Parque Nacional Tortuguero was established as one of the first of Costa Rica’s national parks by Law 5680 in 1975, during the presidency of Daniel Oduber. A contiguous area of 92,000 ha was established in 1985 as the Refugio Nacional de Vida Silvestre Barra del Colorado. In 1994, a 50 ha parcel of land wedged between the two protected areas became the Dr. Archie Carr Wildlife Refuge and the site of the John H. Phipps Biological Station. Two marine turtle laws, 7906 (1999) and 8325 (2002), banned catching the turtles at sea. Owing to these conservation efforts, Tortuguero now has the largest group of nesting green turtles in the entire Atlantic population (see also Cortés, chapter 17 of this volume). From 1971 to 2003, there was a 417% increase in the number of nests, with estimates of 104,000 nests per year and 17,000– 37,000 nesting females per year during the 1999– 2003 period (Troëng and Rankin 2005). A very active international research effort, including a graduate program based at the University of Florida (supported by the Phipps Biological Station in Costa Rica), has contributed important information on the Tortuguero green turtles, including data on genetic diversity of nesting females (Bjorndal et al. 2005), spatial distribution of nests (Tiwari et al. 2005), adult survival (Troëng and Chaloupka 2007), effect of sea surface temperatures on nesting (Solow et al. 2002), hatchling success (Tiwari et al. 2006), levels of bacteria in nests (Santoro et al. 2006), and the genetic composition of juvenile foraging groups (Monzón-Argüello et al. 2010). The green turtle is still considered to be endangered over its entire range (Rieser 2012, Seminoff and Wallace 2012), although some populations are in better shape than others (Broderick et al. 2006, Seminoff and Shanker 2008). The Tortuguero population, although rebounded, is still nowhere near the levels estimated for Precolombian pop-

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ulations ( Jackson 1997, McClenachan et al. 2006, Troëng and Rankin 2005). These turtles take nearly 30 years to reach sexual maturity (Frazer and Ladner 1986) and the overharvesting of juveniles in the open ocean (both intentionally and as bycatch of commercial fishing and shrimping operations) could lead to reduced numbers of mature adults available for breeding in the future (Lahanas et al. 1998, Lagueux 1998, Mortimer 1995). Despite these caveats, the population of green turtles at Tortuguero in recent years appears healthy (Chaloupka et al. 2008). The hope persists that the Tortuguero/Barra del Colorado protected area will also benefit other threatened and endangered vertebrates such as manatees (Smethurst and Nietschmann 1999), hawksbill turtles (Bjorndal et al. 1993, Troëng et al. 2005), and leatherback turtles (Troëng et al. 2007), but the recovery of these species seems less optimistic. Since its inception, the scientific research in the Tortuguero protected area has been combined with ecotourism and revenue generation for the local community (Meletis 2007, Lee and Snepenger 1992). Turtle watching tourism has increased greatly over the years, as have the revenues generated by ecotourism (Ballantyne et al. 2009, Jacobson and Figueroa Lopez 1994). A training program for local tourist guides was developed (Jacobson and Robles 1992) and turtle watching guidelines for sustainable ecotourism have been suggested (Landry and Taggart 2010). Every year scores of volunteers arrive to patrol the beach during the laying season (Campbell and Smith 2006), in order to tag adults, count nests, and watch over hatchlings. The basic tourism package has changed over the years from a “hard” (rugged) to a “soft” (more comfortable) experience (Harrison and Meletis 2010, Place 1991). With tourism has come a certain amount of disturbance for the human community as well as for the turtles (Harrison and Meletis 2010, Jacobson and Figueroa López 1994), such as waste management problems, trampling of beaches, and light from houses distracting hatchlings during their migration to the sea. Adjustments to the tourism offerings are made periodically in an adaptive management paradigm (Meletis and Campbell 2009, Harrison and Meletis 2010). Many segments of society are involved in the turtle conservation enterprise, including scientists, local guides, tourists, volunteers, citizen scientists, donors, funding agencies, government officials, and tourism-dependent business people. Tortuguero turtle conservation has drawn the attention of social scientists nearly to the extent that it has attracted the attention of biologists (Campbell 2002b). Twenty years after the establishment of Parque Nacional Tortuguero, a parallel scenario arose in the Caribbean lowland forest along the Río San Juan with the great green macaws (Ara ambiguus). Where once there had existed

large flocks of these birds in Costa Rica’s Caribbean lowland feeding and nesting areas, their numbers were reduced to about 50 breeding pairs by the early 1990s (Monge et al. 2003). Other populations still existed in reproductively isolated groups from Honduras to Ecuador but the total species population was down to around 5,000 individuals when the species was designated as CITES I, critically endangered in 1985 (Müller 2000) and was then reduced further to about 3,700 individuals over the next ten years (Monge et al. 2009). The decline of this macaw in Costa Rica appeared to be due more to habitat destruction than to direct harvesting of the animals, although illegal collecting of eggs and hatchlings for the pet trade was documented. Land-clearing for cattle pastures and banana plantations resulted in a loss of 80% of suitable habitat for these birds by the 1990s (see Deforestation section, this chapter). Of particular concern was the logging of Dipteryx panamensis trees, a critical food and nesting tree for the great green macaw in Costa Rica (Stiles and Skutch 1989). Because of its extremely dense wood, this tree had been virtually immune to logging pressures until the introduction of a particularly strong carbon steel chainsaw blade. George V.N. Powell, a noted ornithologist who had been working in Monteverde with highland birds, was also working in the Caribbean lowlands with the great green macaw population. He sounded the alarm about the macaws (Powell et al. 1999) in much the same manner that Archie Carr had done with the green turtles at Tortuguero. Starting in the early 1990s, there was much talk of biological corridors as a conservation strategy (Beier and Noss 1998, Newcomer 2002, Sánchez-Azofeifa et al. 2003). The concept of a Paseo Pantera (Path of the Panther), connecting protected areas from Mexico to Colombia, had been proposed by Archie Carr III (son of the Archie Carr who promoted the creation of Parque Nacional Tortuguero) and other scientists from the Wildlife Conservation Society (WCS) and the Caribbean Conservation Corporation (CCC), along with USAID and other funding agencies (Kaiser 2001). The GEF (Global Environmental Facility) was established in 1991 with World Bank funds to support conservation initiatives (Clémençon 2006, Ervine 2007, 2010, Griffiths 2004), including the Mesoamerican Biological Corridor (MBC; a reformulated version of the Paseo Pantera) (Miller et al. 2001, Minc et al. 2001). This concept was formalized in 1992 at the UN Conference on Environment and Development (UNCED) in Río de Janeiro (MBC 2002). In 1997, an official treaty to create the MBC was signed by Central American countries, with Mexico joining later. Each country was tasked with developing its own plans— Costa Rica chose to create a series of smaller corridors, each administered by a user group with the involvement of at

568 Chapter 16

Fig. 16.8 Entrance to the Boca Tapada community in the Refugio Nacional Vida Silvestre Maquenque at the northern end of the San Juan– La Selva Biological Corridor. The community lies along the Río San Carlos near the confluence with the Río San Juan and the border with Nicaragua. This area is the breeding and nesting area of Costa Rica’s remaining population of Great Green Macaws. Photo by Deedra McClearn.

least one representative from MINAE (Ministerio de Ambiente y Energía). The treaty version of the MBC now had two principal aims: physical connectivity of protected areas and sustainable economic development in the communities around the protected areas (Finley-Brook 2007). To return to the plight of the great green macaw, the San Juan– La Selva Biological Corridor (246,608 ha) was defined in 1997, as part of the larger national corridor initiative and also to protect the nesting area of the great green macaw. This is a mixed-use corridor, with private lands and agricultural fields. The northern portion of the corridor was set aside as the Refugio Nacional de Vida Silvestre Maquenque in 2005 after it became clear that the political will and the financing did not exist to make this a fully protected national park. The refuge is contiguous with the Nicaraguan Indio Maíz national park across the Río San Juan, and is the only remaining nesting area of the great green macaw in Costa Rica. The Dipteryx panamensis trees were protected

from logging throughout the entire country in 2008 by executive decree. The management of the SJLS Corridor is handled through the Tropical Science Center (TSC) by Olivier Chassot (who had been a research assistant working for George Powell in 1994) and Guiselle Monge. The establishment of Maquenque and the SJLS Corridor can be considered a conservation success story in the sense that the decline of this population of macaws seems to have been arrested and their numbers may even be increasing after 15 years of protection. There is a modest biological field station at the Lagarto Lodge in Boca Tapada (on the edge of the Maquenque wildlife refuge) (Fig. 16.8) which hosts groups of Costa Rican and international students. Smallscale efforts to combine conservation and ecotourism have met with some success, but revenues from ecotourism have not radically transformed the local economy, which remains based in agriculture, particularly pineapples and yucca (Jackiewicz 2006). Ironically, the sort of development that

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the SJLS corridor communities are expecting and demanding is exactly the sort of development that has caused social and environmental problems in Tortuguero. The publications pertaining to the SJLS Corridor, the Refugio Nacional de Vida Silvestre Maquenque, and the Costa Rican portions of the MBC include technical reports from governments and from NGOs (Lampman 2000, Sader et al. 2004), as well as popular articles about the great green macaw (Chassot and Monge 2002, Chassot et al. 2005, 2009, Monge et al 2005). The scientific literature contains a number of analyses of land use, notably those employing remote sensing (satellite and airplane overflight imagery) to assess forest coverage, forest biomass, and the distribution of particular tree species (Chun 2008, Kalacska et al. 2008, Wang et al. 2008). Every park, wildlife refuge, and private reserve has its unique story, just as every conservation program has its champions and its critics (Fig. 16.9). Parque Nacional Tortuguero was created during the time of the early park system, just after the “closing of the frontier” in the 1960s (Augelli 1987). The SJLS Corridor came into being twenty years later, during an era with a much larger Costa Rican human population, no more freely available, governmentsponsored land for small-holder farming, and the expectation of economic benefits from any and all biological conservation projects. A transfrontier mixed-use biological corridor is a very different beast from a discrete national park. After 20 years of existence and billions of dollars spent on the MBC, the GEF has drawn its share of criticism regarding the practical implementation of conservation programs and the neoliberal agenda that it represents (Clémençon 2006, Ervine 2007, 2010). Nonetheless, at a smaller spatial scale the SJLS Corridor and the Refugio Nacional de Vida Silvestre Maquenque can be credited with protecting critical habitat. The maintenance of forest cover in these areas will have a lasting impact on the conservation of Costa Rica’s biodiversity. The first fifteen years represent a promising start towards the optimal scenario that biodiversity conservationists envision, but agricultural pressure and a local sense of unfulfilled economic expectations pose formidable risks to this vision.

Fig. 16.9 These images of Costa Rican wildlife stamps from the 1980s depict the green turtle and the great green macaw, and represent an increasing environmental awareness by both the Costa Rican government and the public in general.

Perspectives on the Future We began this chapter with the theme of geography but quickly added the theme of time— the deep time of the geological perspective as well as the short time frame of such human enterprises as road building and forest clearing. The coauthors are scientists and conservationists and all are aware of the importance of spatial and temporal scale in our research activities. We also recognize that our own efforts are often limited in both space and time, but that the maintenance of intact ecosystems in today’s world requires planning and implementation activities that are temporally prolonged and spatially extensive. The rapidity of the transformation of the Costa Rican Caribbean lowlands has been astonishing. We wonder whether there is common ground for an ecologist, a hotel owner in Maquenque, a turtle-tagging volunteer at Tortuguero, a local subsistence farmer, a NASA remote sensing expert, a MINAE park ranger, a Bribri landowner with a homegarden and a field of cassava, and a corporate responsibility executive at a banana company all to work together to ensure that ecosystem services and biodiversity are maintained in the long run. We certainly believe there are common ground and a common cause that will trigger our joint attention to address these issues successfully in an integrated manner in the near future.

References Abhilash, P.C., and N. Singh. 2009. Pesticide use and application: an Indian scenario. Journal of Hazardous Materials 165: 1– 12. Acuña-Mesén, R.A. 1998. Las Tortugas Continentales de Costa Rica. San José, Costa Rica: Universidad de Costa Rica. Aguilar, E., T.C. Peterson, P.R. Obando, R. Frutos, J.A. Retana, M. Solera,

J. Soley, I.G. Garcia, R.M. Araujo, A.R. Santos, V.E. Valle, M. Brunet, L. Aguilar, L. Álvarez, M. Bautista, C. Castañon, L. Herrera, E.  Ruano, J.J. Sinay, E. Sánchez, G.I.H. Oviedo, F. Obed, J.E. Salgado, J.L. Vázquez, M. Baca, M. Gutiérrez, C. Centella, J. Espinosa, D. Martínez, B. Olmedo, C.E.O. Espinoza, R. Nuñez, M. Haylock,

570 Chapter 16 H. Benavides, and R. Mayorga. 2005. Changes in precipitation and temperature extremes in Central America and northern South America, 1961– 2003. Journal of Geophysical Research: Atmospheres 110: 1– 15. Ahumada, J.A., C.E.F. Silva, K. Gajapersad, C. Hallam, J. Hurtado, E. Martin, A. McWilliam, B. Mugerwa, T. O’Brien, F. Rovero, D. Sheil, W.R. Spironello, N. Minarni, and S.J. Andelman. 2011. Community structure and diversity of tropical forest mammals: data from a global camera trap network. Philosophical Transactions of the Royal Society B 366: 2703– 11. Alvarado, G. 1990. Características geológicas de la Estación Biológica La Selva, Costa Rica. Tecnología en Marcha 10: 11– 22. Alvarado, G.E., P. Denyer, and E. Gazel. 2009. Endeavor research into evolving paradigms around ophiolites: the case of the oceanic igneous complexes of Costa Rica. Revista Geológica de América Central 40: 49– 73. Ansmann, A., H. Baars, M. Tesche, D. Müller, D. Althausen, R. Engelmann, T. Pauliquevis, and P. Artaxo. 2009. Dust and smoke transport from Africa to South America: Lidar profiling over Cape Verde and the Amazon rainforest. Geophysical Research Letters 36: 2– 6. Arford, M.R., and S.P. Horn. 2004. Pollen evidence of the earliest maize agriculture in Costa Rica. Journal of Latin American Geography 3: 108– 15. Arias, G. 2004. Analisis del impacto económico y social de las plantaciones forestales en Costa Rica. Heredia, Costa Rica: FUNDECOR. Arroyo-Mora, J.P., R.L. Chazdon, M. Kalacska, G. Obando, L. Aguilar, and L.F. Salas. 2009. Development of a forest management GIS for Costa Rica, a case study for the Central Volcanic Cordillera Conservation Area: management trends, lessons and potential uses in ecological research and conservation planning. Proceedings of the XXIII World Forestry Congress, 18– 25 October. Buenos Aires, Argentina. Arroyo-Mora, J.P., M. Kalacska, R. Chazdon, D.L. Civco, G. ObandoVargas, and A.A. Sanchun Hernández. 2008. Assessing recovery following selective logging of lowland tropical forests based on hyperspectral imagery. In M. Kalacska and G.A. Sánchez-Azofeifa, eds., Hyperspectral Remote Sensing of Tropical and Sub-tropical Forests, 193– 212. New York: CRC Press. Arroyo-Mora, J.P., G.A. Sánchez-Azofeifa, B. Rivard, J.C. Calvo, and D.H. Janzen. 2005. Dynamics in landscape structure and composition for the Chorotega region, Costa Rica from 1960 to 2000. Agriculture, Ecosystems and Environment 106: 27– 39. Ascunce, M.S., A. González-Oliver, and C.J. Mulligan. 2008. Ychromosome variability in four Native American populations from Panama. Human Biology 80: 287– 302. Asner, G.P., T.K. Rudel, M. Aide, R. Defries, and R. Emerson. 2009. A contemporary assessment of global humid tropical forest change. Conservation Biology 23: 1386– 95. Auerbach, M.J., and D.R. Strong. 1981. Nutritional ecology of Heliconia herbivores: experiments with plant fertilization and alternative hosts. Ecological Monographs 51: 63– 83. Augelli, J.P. 1987. Costa Rica’s frontier legacy. Geographical Review 77(1): 1– 16. Avnery, S., R.A. Dull, and T.H. Keitt. 2011. Human versus climatic influences on late-Holocene fire regimes in southwestern Nicaragua. Holocene 21: 699– 706. Bacon, C.D., D. Silvestro, C. Jaramillo, B.T. Smith, P. Chakrabarty, and A. Antonelli. 2015. Biological evidence supports an early and com-

plex emergence of the Isthmus of Panama. PNAS Early Edition, www.pnas.org/cgi/doi/10.1073/pnas.1423853112. Ballantyne, R., J. Packer, and K. Hughes. 2009. Tourists’ support for conservation messages and sustainable management practices in wildlife tourism experiences. Tourism Management 30: 658– 64. Banack, S.A., M.H. Horn, and A. Gawlicka. 2002. Disperser- vs. establishment-limited distribution of a riparian fig tree (Ficus insipida) in a Costa Rican tropical rain forest. Biotropica 34: 232– 43. Barnosky, A.D., P.L. Koch, R.S. Feranec, S.L. Wing, and A.B. Shabel. 2004. Assessing the causes of Late Pleistocene extinctions on the continents. Science 306: 70– 75. Barone, J.A., and P.D. Coley. 2002. Herbivorismo y las defensas de las plantas. In M.R. Guariguata-Urbano and G.H. Kattan, eds., Ecología y Conservación de Bosques Neotropicales, 465– 92. Cartago, Costa Rica: Libro Universitario Regional (EULAC-GTZ). Barraza, D., K. Jansen, B. van Wendel de Joode, and C. Wesseling. 2011. Pesticide use in banana and plantain production and risk perception among local actors in Talamanca, Costa Rica. Environmental Research 111: 708– 17. Bartoli, G., M. Sarnthein, M. Weinelt, H. Erlenkeuser, D. GarbeSchönberg, and D.W. Lea. 2005. Final closure of Panama and the onset of northern hemisphere glaciation. Earth and Planetary Science Letters 237: 33– 44. Batte, M.T., N.H. Hooker, T.C. Haab, and J. Beaverson. 2007. Putting their money where their mouths are: consumer willingness to pay for multi-ingredient, processed organic food products. Food Policy 32: 145– 59. Battistini, R., and J.P. Bergoeing. 1984. Geomorfología de la costa Caribe de Costa Rica. Revista Geográfica 99: 167– 88. Bayón, C., T. Manera, G. Politis, and S. Aramayo. 2011. Following the tracks of the first South Americans. Evolution: Education and Outreach 4: 205– 17. Beck, H. 2005. Seed predation and dispersal by peccaries throughout the neotropics and its consequences: a review and synthesis. In P.-M. Forget, J.E. Lambert, P.E. Hulme, and S.B. Van der Wall, eds., Seed Fate: Predation, Dispersal and Seedling Establishment, 77– 115. Wallingford, UK: CAB International. Beer, C., M. Reichstein, E. Tomelleri, P. Ciais, M. Jung, N. Carvalhais, C. Rödenbeck, M.A. Arain, D. Baldocchi, B.G. Bonan, A. Bondeau, A. Cescatti, G. Lasslop, A. Lindroth, M. Lomas, S. Luyssaert, H. Margolis, K.W. Oleson, O. Roupsard, E. Veenendaal, N. Viovy, C. Williams, F.I. Woodward, and D. Papale. 2010. Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329: 834– 38. Beier, P., and R.F. Noss. 1998. Do habitat corridors provide connectivity? Conservation Biology 12: 1241– 52. Bell, K.E., and M.A. Donnelly. 2006. Influence of forest fragmentation on community structure of frogs and lizards in Northeastern Costa Rica. Conservation Biology 20: 1750– 60. Benway, H.M., and A.C. Mix. 2004. Oxygen isotopes, upper-ocean salinity, and precipitation sources in the eastern tropical Pacific. Earth and Planetary Science Letters 224: 493– 507. Berny, P. 2007. Pesticides and the intoxication of wild animals. Journal of Veterinary Pharmacology and Therapeutics 30: 93– 100. Berti, G. 2000. Estado actual de los bosques secundarios en Costa Rica: perspectivas para su manejo productivo. Revista Forestal Centroamericana: 29– 34.

The Caribbean Lowland Evergreen Moist and Wet Forests 571 Biesanz, R., K.Z. Biesanz, and M.H. Biesanz. 1987. The Costa Ricans. San José, Costa Rica: Editorama. Bjorndal, K.A., A.B. Bolten, and C.J. Lagueux. 1993. Decline of the nesting population of hawksbill turtles at Tortuguero, Costa Rica. Conservation Biology 7: 925– 27. Bjorndal, K.A., A.B. Bolten, and S. Troëng. 2005. Population structure and genetic diversity in green turtles nesting at Tortuguero, Costa Rica, based on mitochondrial DNA control region sequences. Marine Biology 147: 1449– 57. Blake, J.G., and B.A. Loiselle. 2000. Diversity of birds along an elevational gradient in the Cordillera Central, Costa Rica. Auk 117: 663– 86. Blake, J.G., F.G. Stiles, and B.A. Loiselle. 1990. Birds of La Selva Biological Station: habitat use, trophic composition, and migrants. In A.H. Gentry, ed., Four Neotropical Rainforests, 161– 82. Binghampton, NY: Vail-Ballou Press. Boccaletti, S., and M. Nardella. 2000. Consumer willingness to pay for pesticide-free fresh fruit and vegetables in Italy. International Food and Agribusiness Management Review 3: 297– 310. Borge, C., and R. Castillo. 1997. Cultura y Conservación en la Talamanca Indígena. San José, Costa Rica: Editorial UNED. Boucher, D.H., J.H. Vandermeer, I.G. de la Cerda, M.A. Mallona, I. Perfecto, and N. Zamora. 2001. Post-agriculture versus post-hurricane succession in southeastern Nicaraguan rain forest. Plant Ecology 156: 131– 37. Bourgeois, S., V. Yotova, S. Wang, S. Bourtoumieu, C. Moreau, R. Michalski, J.-P. Moisan, K. Hill, A.M. Hurtado, A. Ruiz-Linares, and D. Labuda. 2009. X-chromosome lineages and the settlement of the Americas. American Journal of Physical Anthropology 140: 417– 28. Boza, M.A. 1993. Conservation in action: past, present, and future of the national park system of Costa Rica. Conservation Biology 7: 239– 47. Boza, M.A., D. Jukofsky, and C. Wille. 1995. Costa Rica is a laboratory, not Ecotopia. Conservation Biology 9: 684– 85. Braker, E. 1991. Natural history of a neotropical gap-inhabiting grasshopper. Biotropica 23: 41– 50. Braker, E. 1993. Ecological, behavioural, and nutritional factors influencing use of palms as host plants by a neotropical forest grasshopper. Journal of Tropical Ecology 9: 181– 95. Braker, H.E. 1986. Host plant relationsips of the neotropical grasshopper Microtylopteryx hebardi Rehn (Acrididae: Ommatolampinae). PhD diss., University of California, Berkeley. Braker, H.E. 1989a. Evolution and ecology of oviposition on host plants by acridoid grasshoppers. Biological Journal of the Linnean Society 38: 389– 406. Braker, H.E. 1989b. Oviposition on host plants by a tropical forest grasshopper (Microtylopteryx herbardi: Acrididae). Ecological Entomology 14: 141– 48. Brausch, J.M., and P.N. Smith. 2009. Development of resistance to cyfluthrin and naphthalene among Dahnia magna. Ecotoxicology 18: 600– 609. Bristow, C.S., K.A. Hudson-Edwards, and A. Chappell. 2010. Fertilizing the Amazon and equatorial Atlantic with West African dust. Geophysical Research Letters 37: 1– 5. Brockett, C.D., and R.R. Gottfried. 2002. State policies and the preservation of forest cover: lessons from contrasting public-policy regimes in Costa Rica. Latin American Research Review 37: 7– 40.

Broderick, A.C., R. Frauenstein, F. Glen, G.C. Hays, A.L. Jackson, T. Pelembe, G.D. Ruxton, and B.J. Godley. 2006. Are green turtles globally endangered? Global Ecology and Biogeography 15: 21– 26. Brook, B.W., and D.M.J.S. Bowman. 2004. The uncertain blitzkrieg of Pleistocene megafauna. Journal of Biogeography 31: 517– 23. Brown, J.K.M., and M.S. Hovmøller. 2002. Aerial dispersal of pathogens on the global and continental scales and its impact on plant disease. Science 297: 537– 41. Brown, S., and A.E. Lugo. 1990. Tropical secondary forests. Journal of Tropical Ecology 6: 1– 32. Buchanan, I., H.C. Liang, W. Khan, Z. Liu, R. Singh, K. Ikehata, and P. Chelme-Ayala. 2009. Pesticides and herbicides. Water Environment Research 81: 1731– 816. Buchs, D.M., R.J. Arculus, P.O. Baumgartner, C. Baumgartner-Mora, and A. Ulianov. 2010. Late Cretaceous arc development on the SW margin of the Caribbean Plate: insights from the Golfito, Costa Rica, and Azuero, Panama complexes. Geochemistry, Geophysics, Geosystems 11: 1– 35. Bunker, D.E., and W.P. Carson. 2005. Drought stress and tropical forest woody seedlings: effect on community structure and composition. Journal of Ecology 93: 794– 806. Burney, D.A., and T.F. Flannery. 2005. Fifty millennia of catastrophic extinctions after human contact. Trends in Ecology and Evolution 20: 395– 401. Burnham, R.J., and A. Graham. 1999. The history of Neotropical vegetation: new developments and status. Annals of the Missouri Botanical Garden 86: 546– 89. Bussing, W.A. 1994. Ecological aspects of the fish community. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 195– 98. Chicago: University of Chicago Press. Bussing, W.A. 1998. Freshwater Fishes of Costa Rica. 2nd ed. San José, Costa Rica: University of Costa Rica Press. Butterfield, R.P. 1994. The regional context: land colonization and conservation in Sarapiquí. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 299– 306. Chicago: University of Chicago Press. Butterfield, R., and M. Espinoza. 1995. Screening trial of 14 tropical hardwoods with an emphasis on species native to Costa Rica: fourth year results. New Forests 9: 135– 45. Butterfield, R.P., and E. González. 1996. Especies forestales para la reforestación y recuperación de pastizales degradados en las tierras bajas del atlántico húmedo de Costa Rica. Revista Forestal Centroamericana 16: 9– 15. Cadol, D., and E. Wohl. 2010. Wood retention and transport in tropical, headwater streams, La Selva Biological Station, Costa Rica. Geomorphology 123: 61– 73. Cadol, D., E. Wohl, J.R. Goode, and K.L. Jaeger. 2009. Wood distribution in neotropical forested headwater streams of La Selva, Costa Rica. Earth Surface Processes and Landforms 34: 1198– 215. Callegari-Jacques, S.M., F.M. Salzano, J. Constans, and P. Maurieres. 1993. Gm haplotype distribution in Amerindians: relationship with geography and language. American Journal of Physical Anthropology 90: 427– 44. Calvo, J. 2008. Bosque, cobertura y recursos forestales. 2008. Informe Final. In CONARE and La Defensoria de los Habitantes, eds., Dec-

572 Chapter 16 imoquinto informe Estado de la Nación en desarrollo humano sostenible, 1– 26. Calvo, J., V. Jiménez, and J.C. Solano. 2006. Estudio de monitoreo de cobertura forestal de Costa Rica 2005. II. Parte Coberturas de áreas reforestadas, plantadas con café y frutales en Costa Rica para el estudio de cobertura forestal. Proyecto Ecomercados, 114 Fondos GEF— Ecomercados convenio de donación TF FONAFIFO, ITCR, EOSL. San José, Costa Rica. Calvo-Alvarado, J.C. 1990. The Costa Rican national conservation strategy for sustainable development: exploring the possibilities. Environmental Conservation 17: 355– 58. Campbell, L.M. 2002a. Conservation narratives in Costa Rica: conflict and co-existence. Development and Change 33: 29– 56. Campbell, L.M. 2002b. Science and sustainable use: views of marine turtle conservation experts. Ecological Applications 12: 1229– 46. Campbell, L.M., and C. Smith. 2006. What makes them pay? Understanding values of conservation volunteers in Tortuguero, Costa Rica. Environmental Management 38: 84– 98. Cannariato, K.G., and A.C. Ravelo. 1997. Pliocene-Pleistocene evolution of eastern tropical Pacific surface water circulation and thermocline depth. Paleoceanography 12: 805– 20. Capers, R.S., R.L. Chazdon, A. Redondo-Brenes, and A.B. Vílchez. 2005. Successional dynamics of woody seedling communities in wet tropical secondary forests. Journal of Ecology 93: 1071– 84. Caquineau, S., A. Gaudichet, L. Gómes, and M. Legrand. 2002. Mineralogy of Saharan dust transported over northwestern tropical Atlantic Ocean in relation to source regions. Journal of Geophysical Research 107: 1– 14. Cardelús, C.L., M.C. Mack, C. Woods, J. DeMarco, and K.K. Treseder. 2009. The influence of tree species on canopy soil nutrient status in a tropical lowland wet forest in Costa Rica. Plant and Soil 318: 47– 61. Carr, A.F. 1967. So Excellente a Fishe: A Natural History of Sea Turtles. Garden City, New York: Natural History Press. Carr, A., M.H. Carr, and A.B. Meylan. 1978. The ecology and migrations of sea turtles, 7. The west Caribbean green turtle colony. Bulletin of the American Museum of Natural History 162: 1– 46. Carvalho, F. 2006. Agriculture, pesticides, food security and food safety. Environmental Science and Policy 9: 685– 92. Casals-Casas, C., and B. Desvergne. 2011. Endocrine disruptors: from endocrine to metabolic disruption. Annual Review of Physiology 73: 135– 62. Castillo, L.E., E. Martínez, C. Ruepert, C. Savage, M. Gilek, M. Pinnock, and E. Solís. 2006. Water quality and macroinvertebrate community response following pesticide applications in a banana plantation, Limón, Costa Rica. Science of the Total Environment 367: 418– 32. Castillo, L.E., C. Ruepert, and E. Solís. 2000. Pesticide residues in the aquatic environment of banana plantation areas in the North Atlantic zone of Costa Rica. Environmental Toxicology and Chemistry 19: 1942– 50. Caux, P.Y., R.A. Kent, G.T. Fan, and G.L. Stephenson. 1996. Environmental fate and effects of chlorothalonil: a Canadian perspective. Critical Reviews in Environmental Science and Technology 26: 45– 93. Cavelier, J. 1996. Environmental factors and ecophysiological processes along altitudinal gradients in wet tropical mountains. In S.S. Mulkey, R.L. Chazdon, and A.P. Smith, eds., Tropical Forest Plant Ecophysiology, 399– 439. New York: Chapman and Hall.

Cavelier, J., S.J. Wright, and J. Santamaria. 1999. Effects of irrigation on fine root biomass and production, litterfall and trunk growth in a semideciduous lowland forest in Panama. Plant and Soil 211: 207– 13. Centro Centroamericano de Población. 2011. Estimación de la población de Costa Rica. Centro Centroamericano de Población, Instituto Nacional de Estadística y Censos, Universidad de Costa Rica. San José, Costa Rica. Accessed June 21, 2011, http://ccp.ucr.ac.cr. Cernusak, L., K. Winter, C. Martínez, E. Correa, J. Aranda, M. García, C. Jaramillo, and B.L. Turner. 2011. Responses of legume versus nonlegume tropical tree seedlings to elevated CO2 concentration. Plant Physiology 157: 372– 85. Chacón, I.A., and J. Montero. 2007. Mariposas de Costa Rica. Costa Rica: INBio. Chakrabarty, P., and J.S. Albert. 2011. Not so fast: a new take on the Great American Biotic Interchange. In J.S. Albert and R.E. Reis, eds., Historical Biogeography of Neotropical Freshwater Fishes, 293– 305. Berkeley: University of California Press. Chalak, A., K. Balcombe, A. Bailey, and I. Fraser. 2008. Pesticides, preference heterogeneity and environmental taxes. Journal of Agricultural Economics 59: 537– 54. Chaloupka, M., K.A. Bjorndal, G.H. Balazs, and A.B. Bolten. 2008. Encouraging outlook for recovery of a once severely exploited marine megaherbivore. Global Ecology and Biogeography 17: 297– 304. Chapman, A., and K. Rosenberg. 1991. Diets of four sympatric Amazonian woodcreepers (Dendrocolaptidae). Condor 93: 904– 15. Chapman, P. 2007. Bananas: How the United Fruit Company Shaped the World. Edinburgh: Canongate Publishing. Charboneau, J.P., and S.M. Koger. 2008. Plastics, pesticides and PBDEs: endocrine disruption and developmental disabilities. Journal of Developmental and Physical Disabilities 20: 115– 28. Chassot, O., and G. Monge. 2002. La biodiversidad amenazada en el Corredor Biológico San Juan– La Selva. Ambientico 107: 14– 15. Chassot, O., G. Monge, G. Powell, P. Wright, and S. Palminteri. 2005. San Juan– La Selva Biological Corridor, Costa Rica: a project of the Mesoamerican Biological Corridor for the protection of the great green macaw and its environment. San José, Costa Rica: Tropical Science Center. Chassot, O., J.G. Monge, and G. Powell. 2009. Biología de la conservación de la lapa verde (1994– 2009), 15 años de experiencia. San Pedro, Costa Rica: Centro Cientifico Tropical. Chaves, A., D. Shea, and W.G. Cope. 2007. Environmental fate of chlorothalonil in a Costa Rican banana plantation. Chemosphere 69: 1166– 74. Chazdon, R.L., S. Careaga, C. Webb, and O. Vargas. 2003. Community and phylogenetic structure of reproductive traits of woody species in wet tropical forests. Ecological Monographs 73: 331– 48. Chazdon, R.L., and F.G. Coe. 1999. Ethnobotany of woody species in second-growth, old-growth, and selectively logged forests of northeastern Costa Rica. Conservation Biology 13: 1312– 22. Chazdon, R.L., R.K. Colwell, J.S. Denslow, and M.R. Guariguata. 1998. Statistical methods for estimating species richness of woody regeneration in primary and secondary rain forests of NE Costa Rica. In F. Dallmeier and J. Comiskey, eds., Forest Biodiversity Research, Monitoring and Modeling: Conceptual Background and Old World Case Studies, 285– 309. Paris: Parthenon Publishing. Chazdon, R.L., S.G. Letcher, M. van Breughel, M. Martínez-Ramos,

The Caribbean Lowland Evergreen Moist and Wet Forests 573 F. Bongers, and B. Finegan. 2007. Rates of change in tree communities of secondary tropical forests following major disturbances. Philosophical Transactions of the Royal Society B: Biological Sciences 362: 273– 89. Chazdon, R.L., A. Redondo-Brenes, and B.A. Vílchez. 2005. Effects of climate and stand age on annual tree dynamics in tropical secondgrowth rain forests. Ecology 86: 1808– 15. Chernyak, S.M., C.P. Rice, and L.L. McConnel. 1996. Evidence of currently-used pesticides in air, ice, fog, seawater and surface microlayer in the Bering and Chuckchi Seas. Marine Pollution Bulletin 32: 410– 19. Cherrett, J.M. 1986. History of the leaf-cutting ant problem. In C.S. Lofgren and R.K. van der Meer, eds., Fire Ants and Leaf-cutting Ants, Biology and Management, 10– 17. Boulder: Westview Press. Chomsky, A. 1996. West Indian Workers and the United Fruit Company in Costa Rica 1870– 1940. Baton Rouge: Louisiana State University Press. Chornook, K., and W. Guindon. 2008. Walking with Wolf. Hamilton, Ontario: Wandering Words Press. Chou, C., J.D. Neelin, C.-A. Chen, and J.-Y. Tu. 2009. Evaluating the “rich-get-richer” mechanism in tropical precipitation change under global warming. Journal of Climate 22: 1982– 2005. Chun, S.L.M. 2008. The utility of digital aerial surveys in censusing Dipteryx panamensis, the key food and nesting tree of the endangered great green macaw ( Ara ambigua) in Costa Rica. PhD diss., Duke University. Clark, D.A. 2004. Sources or sinks? The response of tropical forests to current and future climate and atmospheric composition. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 359: 477– 91. Clark, D.A., S. Brown, D.W. Kicklighter, J.Q. Chambers, J.R. Thomlinson, and J. Ni. 2001. Measuring net primary production in forests: concepts and field methods. Ecological Applications 11: 356– 70. Clark, D.A., and D.B. Clark. 2011. Assessing tropical forests’ climatic sensitivities with long-term data. Biotropica 43: 31– 40. Clark, D.A., D.B. Clark, R. Sandoval, and M.V. Castro. 1995. Edaphic and human effects on landscape-scale distributions of tropical rain forest palms. Ecology 76: 2581– 94. Clark, D.A., S.C. Piper, C.D. Keeling, and D.B. Clark. 2003. Tropical rain forest tree growth and atmospheric carbon dynamics linked to interannual temperature variation during 1984– 2000. Proceedings of the National Academy of Sciences 100: 5852– 57. Clark, D.B. 1996. Abolishing virginity. Journal of Tropical Ecology 12: 735– 39. Clark, D.B., and D.A. Clark. 2000. Landscape scale variation in forest structure and biomass in a tropical rain forest. Forest Ecology and Management 137: 185– 98. Clark, D.B., D.A. Clark, and S.F. Oberbauer. 2010. Annual wood production in a tropical rain forest in NE Costa Rica linked to climatic variation but not to increasing CO2. Global Change Biology 16: 747– 59. Clark, D.B., M.W. Palmer, and D.A. Clark. 1999. Edaphic factors and the landscape-scale distributions of tropical rain forest trees. Ecology 80: 2662– 75. Clark, M.L., D.A. Roberts, and D.B. Clark. 2005. Hyperspectral discrimination of tropical rain forest tree species at leaf to crown scales. Remote Sensing of Environment 96: 375– 98.

Clémençon, R. 2006. What future for the Global Environment Facility? Journal of Environment Development 15: 50– 74. Clement, C.R., and A.B. Junqueira. 2010. Between a pristine myth and an impoverished future. Biotropica 42: 534– 36. Coale, A.J. 1983. Recent trends in fertility in less developed countries. Science 221: 828– 32. Coates, A.G. 1997. The forging of Central America. In A.G. Coates, ed., Central America: A Natural and Cultural History, 1– 37. New Haven, London: Yale University Press. Cody, S., J.E. Richardson, V. Rull, C. Ellis, and R.T. Pennington. 2010. The Great American Biotic Interchange revisited. Ecography 33: 326– 32. Coley, P.D., and J.A. Barone. 1996. Herbivory and plant defenses in tropical forests. Annual Review of Ecology and Systematics 27: 305– 35. Colwell, R.K. 2005. EstimateS 7.5 User’s Guide. http://viceroy.eeb .uconn.edu/estimates. Colwell, R.K., G. Brehm, C.L. Cardelús, A.C. Gilman, and J.T. Longino. 2008. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science 322: 258– 61. Colwell, R.K., C.X. Mao, and J. Chang. 2004. Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85: 2717– 27. Condit, R., N. Pitman, E.G. Leigh Jr., J. Chave, J. Terborgh, R.B. Foster, V.P. Núñez, S. Aguilar, R. Valencia, G. Villa, H.C. Muller-Landau, E.  Losos, and S.P. Hubbell. 2002. Beta-diversity in tropical forest trees. Science 295: 666– 69. Cone, M. 2006. Silent snow: the slow poisoning of the Arctic. Grove Weidenfeld Publishers. Cooper, J., and H. Dobson. 2007. The benefits of pesticides to mankind and the environment. Crop Protection 26: 1337– 48. CORBANA (Corporación Bananera Nacional CR). 2009. Estadísticas bananeras (online). http://www.corbana.co.cr. Corella, O. 1999. Valoración de la base forestal de las plantaciones forestales y su contribución al abastecimiento de madera en la zona del Atlántico Norte de Costa Rica. M.Sc. thesis, CATIE. Turrialba, Costa Rica. Cox, P.M., P.P. Harris, C. Huntingford, R.A. Betts, M. Collins, C.D. Jones, T.E. Jupp, J.A. Marengo, and C.A. Nobre. 2008. Increasing risk of Amazonian drought due to decreasing aerosol pollution. Nature 453: 212– 15. Cramer, W., A. Bondeau, S. Schaphoff, W. Lucht, B. Smith, and S. Sitch. 2004. Tropical forests and the global carbon cycle: impacts of atmospheric carbon dioxide, climate change and rate of deforestation. Philosophical Transactions of the Royal Society of London, Series B 359: 331– 43. Daly, G.L., Y.D. Lei, C. Teixeira, D.C.G. Muir, L.E. Castillo, L.M.M. Jantunen, and F. Wania. 2007a. Organochlorine pesticides in the soils and atmosphere of Costa Rica. Environmental Science and Technology 41: 1124– 30. Daly, G.L., Y.D. Lei, C. Teixeira, D.C.G. Muir, L.E. Castillo, and F. Wania. 2007b. Accumulation of current-use pesticides in neotropical montane forests. Environmental Science and Technology 41: 1118– 23. De Camino, R., O. Segura, L.G. Arias, and I. Pérez. 2000. Costa Rica: forest strategy and the evolution of land use. Washington, DC: World Bank. De la Cruz, E., V. Bravo-Durán, F. Ramírez, and L.E. Castillo. 2014. Environmental hazards associated with pesticide import into Costa Rica, 1977– 2009. Journal of Environmental Biology 35: 44– 55.

574 Chapter 16 Demerutis, C., L. Quirós, A. Martínez, E. Alvarado, R.N. Williams, and M.A. Ellis. 2008. Evaluation of an organic treatment for post-harvest control of crown rot of banana. Ecological Engineering 34: 324– 27. Denevan, W.M. 1976. The aboriginal population of Amazonia. In W.M. Denevan, ed., The Native Population of the Americas in 1492, 205– 34. Madison, WI: University of Wisconsin Press. Denevan, W.M. 1992. The pristine myth: the landscape of the Americas in 1492. Annals of the Association of American Geographers 82: 369– 85. Denevan, W.M. 2003. The native population of Amazonia in 1492 reconsidered. Revista de Indias 62: 175– 88. Dettman, S. 2006. The Mesoamerican biological corridor in Panama and Costa Rica: integrating bioregional planning and local initiatives. Journal of Sustainable Forestry 22: 15– 34. DeVries, P.J. 1979. Pollen-feeding rainforest Parides and Battus butterflies in Costa Rica. Biotropica 12: 237– 38. DeVries, P.J. 1997. The butterflies of Costa Rica and their natural history. Vol. II. Riodinidae. Princeton, NJ: Princeton University Press. DeVries, P.J., L.G. Alexander, I.A. Chacón, and J.A. Fordyce. 2012. Similarity and difference among rainforest fruit-feeding butterfly communities in Central and South America. Journal of Animal Ecology 81: 472– 82. Dick, J.McP., R.I. Smith, and E.M. Scott. 2010. Ecosystem services and associated concepts. Environmetrics 22: 598– 607. Dickau, R., A.J. Ranere, and R.G. Cooke. 2007. Starch grain evidence for the preceramic dispersals of maize and root crops into tropical dry and humid forests of Panama. Proceedings of the National Academy of Sciences 104: 3651– 56. Diffenbaugh, N., and M. Scherer. 2011. Observational and model evidence of global emergence of permanent, unprecedented heat in the 20th and 21st centuries. Climatic Change 107: 615– 24. Dillehay, T.D. 2009. Probing deeper into first American studies. Proceedings of the National Academy of Sciences 106: 971– 78. Dirzo, R., and P.H. Raven. 2003. Global state of biodiversity and loss. Annual Review of Environment and Resources 28: 137– 67. Dixon, R.K., S.A. Brown, R.A. Houghton, A.M. Solomon, M.C. Trexler, and J. Wisniewski. 1994. Carbon pools and flux of global forest ecosystems. Science 263: 185– 90. Donnelly, M.A., and C. Guyer. 1994. Patterns of reproduction and habitat use in an assemblage of Neotropical hylid frogs. Oecologia 98: 291– 302. Doughty, C.E., and M.L. Goulden. 2008. Are tropical forests near a high temperature threshold? Journal of Geophysical Research 113: 1– 12. Doughty, C.E., A. Wolf, and C.B. Field. 2010. Biophysical feedbacks between the Pleistocene megafauna extinction and climate: the first human-induced global warming? Geophysical Research Letters 37: 5703– 07. Drake, J.B., R.O. Dubayah, D.B. Clark, R.G. Knox, J.B. Blair, M.A. Hofton, R.L. Chazdon, J.F. Weishampel, and S. Prince. 2002a. Estimation of tropical forest structural characteristics using large-footprint lidar. Remote Sensing of Environment 79: 305– 19. Drake, J.B., R.O. Dubayah, R.G. Knox, D.B. Clark, and J.B. Blair. 2002b. Sensitivity of large-footprint lidar to canopy structure and biomass in a neotropical rainforest. Remote Sensing of Environment 81: 378– 92. Drake, J.B., R.G. Knox, R.O. Dubayah, D.B. Clark, R. Condit, J.B. Blair, and M.A. Hofton. 2003. Aboveground biomass estimation in closed

canopy Neotropical forest using lidar remote sensing: factors affecting the generality of relationships. Global Ecology and Biogeography 12: 147– 59. Dubayah, R.O., S.L. Sheldon, D.B. Clark, M.A. Hofton, J.B. Blair, G.C. Hurtt, and R.L. Chazdon. 2010. Estimation of tropical forest height and biomass dynamics using lidar remote sensing at La Selva, Costa Rica. Journal of Geophysical Research 115: 1– 17. Dupuy, J.M., and R.L. Chazdon. 1998. Long-term effects of forest regrowth and selective logging on the seed bank of tropical forests in NE Costa Rica. Biotropica 30: 223– 37. Duszeln, J. 1991. Pesticide contamination and pesticide control in developing countries: Costa Rica, Central America. In M.I. Richardson, ed., Chemistry, Agriculture and the Environment, 410– 28. London: The Royal Society of Chemistry. Dyer, L.A., D.K. Letourneau, G.V. Chavarria, and D.S. Amoretti. 2010. Herbivores on a dominant understory shrub increase local plant diversity in rain forest communities. Ecology 91: 3707– 18. Dyer, L.A., and A.D.N. Palmer. 2004. Piper: a model genus for studies of phytochemistry, ecology, and evolution. New York: Kluwer Academic /Plenum Publishers. Dyer, L.A., M.S. Singer, J.T. Lill, J.O. Stireman, G.L. Gentry, R.J. Marquis, R.E. Ricklefs, H.F. Greeney, D.L. Wagner, H.C. Morais, I.R. Diniz, T.A. Kursar, and P.D. Coley. 2007. Host specificity of Lepidoptera in tropical and temperate forests. Nature 448: 696– 99. Dzierma, Y., W. Rabbel, M.M. Thorwart, E.R. Flueh, D. Kiel, M.M. Mora, and G.E. Alvarado. 2011. The steeply subducting edge of the Cocos Ridge: evidence from receiver functions beneath the northern Talamanca Range, south-central Costa Rica. Geochemistry, Geophysics, Geosystems 12: 1– 25. Eklund, T.J., and C.M. Pringle. 1997. Seasonal variation of tropical precipitation chemistry: La Selva, Costa Rica. Atmospheric Environment 31: 3903– 10. Elizondo, C.L., and L.B. Zamora. 1998. Desarrollo del Proyecto GLOBESAR en Costa Rica. In Conservación del bosque en Costa Rica, 1– 278. Academia Nacional de Ciencias: Programa Centroamericano de Población, Universidad de Costa Rica. Engelbrecht, B.M.J., L.S. Comita, R. Condit, T.A. Kursar, M.T. Tyree, B.L. Turner, and S.P. Hubbell. 2007. Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447: 80– 82. Engelbrecht, B.M.J., and T.A. Kursar. 2003. Comparative droughtresistance of seedlings of 28 species of co-occurring tropical woody plants. Oecologia 136: 383– 93. Enquist, B.J., and C.A.F. Enquist. 2011. Long-term change within a Neotropical forest: assessing differential functional and floristic responses to disturbance and drought. Global Change Biology 17: 1408– 24. Enquist, C.A.F. 2002. Predicted regional impacts of climate change on the geographical distribution and diversity of tropical forests in Costa Rica. Journal of Biogeography 29: 519– 34. Ervine, K. 2007. The greying of green governance: power politics and the Global Environmental Facility. Capitalism Nature Socialism 18: 125– 43. Ervine, K. 2010. Participation denied: the Global Environmental Facility, its universal blueprint, and the Mexico– Mesoamerican Biological Corridor in Chiapas. Third World Quarterly 31: 773– 90. Escobar, F., G. Halffter, A. Solís, V. Halffter, and D. Navarrete. 2008. Temporal shifts in dung beetle community structure within a protected

The Caribbean Lowland Evergreen Moist and Wet Forests 575 area of tropical wet forest: a 35-year study and its implications for long-term conservation. Journal of Applied Ecology 45: 1584– 92. Espeleta, J.P., and D.A. Clark. 2007. Multi-scale variation in fine-root biomass in a tropical rain forest: a seven-year study. Ecological Monographs 77: 377– 404. Evans, S. 1999. The Green Republic: A Conservation History of Costa Rica. Austin, TX: University of Texas Press. Fagundes, N.J.R., R. Kanitz, R. Eckert, A.C.S. Valls, M.R. Bogo, F.M. Salzano, D.G. Smith, W.A. Silva Jr., M.A. Zago, A.K. Ribeiro-dos-Santos, S.E.B. Santos, M.L. Petzl-Erler, and S.L. Bonatto. 2008. Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. American Journal of Human Genetics 82: 583– 92. FAO. 2000. Global forest resource assessment 2000— Main Report, FAO Forestry Paper 140, United Nations Food and Agricultural Organization. FAO. 2007. State of the world’s forests. United Nations Food and Agricultural Organization. Farji-Brener, A.G. 2001. Why are leaf-cutting ants more common in early secondary forests than in old-growth tropical forests? An evaluation of the palatable forage hypothesis. Oikos 92: 169– 77. Farji-Brener, A.G. 2005. The effect of abandoned leaf-cutting ant nests on plant assemblage composition in a tropical rainforest of Costa Rica. Ecoscience 12: 554– 60. Farji-Brener, A.G., S. Amador-Vargas, F. Chinchilla, S. Escobar, S. Cabrera, M.I. Herrera, and C. Sandoval. 2010. Information transfer in head-on encounters between leaf-cutting ant workers: food, trail condition or orientation cues? Animal Behaviour 79: 343– 49. Farji-Brener, A.G., and A.E. Illes. 2000. Do leaf-cutting ant nests make “bottom-up” gaps in neotropical rain forests?: a critical review of the evidence. Ecology Letters 3: 219– 27. Farrera, I., S.P. Harrison, I.C. Prentice, G. Ramstein, J. Guiot, P.J. Bartlein, R. Bonnefille, M. Bush, W. Cramer, U. von Grafenstein, K. Holmgren, H. Hooghiemstra, G. Hope, D. Jolly, S.-E. Lauritzen, Y. Ono, S. Pinot, M. Stute, and G. Yu. 1999. Tropical climates at the Last Glacial Maximum: a new synthesis of terrestrial palaeoclimate data. I. Vegetation, lake-levels and geochemistry. Climate Dynamics 15: 823– 56. Feeley, K.J., S.J. Davies, R. Pérez, S.P. Hubbell, and R.B. Foster. 2011. Directional changes in the species composition of a tropical forest. Ecology 92: 871– 82. Feeley, K.J., and M.R. Silman. 2010. Biotic attrition from tropical forests correcting for truncated temperature niches. Global Change Biology 16: 1830– 36. Feeley, K.J., and J.W. Terborgh. 2008. Direct versus indirect effects of habitat reduction on the loss of avian species from tropical forest fragments. Animal Conservation 11: 353– 60. Fernández-Arce, M. 2009. Seismicity of the Pejibaye– Matina, Costa Rica region: a strike-slip tectonic boundary? Geofísica Internacional 48: 361– 74. Fieten, K.B., H. Kromhout, D. Heederik, and B. van Wendel de Joode. 2009. Pesticide exposure and respiratory health of indigenous women in Costa Rica. American Journal of Epidemiology 169: 1500– 1506. Finegan, B. 1992. The management potential of neotropical secondary lowland rain forest. Forest Ecology and Management 47: 295– 321. Finegan, B. 1996. Pattern and process in neotropical secondary rain

forests: the first hundred years of succession. Trends in Ecology and Evolution 11: 119– 24. Finegan, B., and D. Delgado. 2000. Structural and floristic heterogeneity in a 30-yr-old Costa Rican rain forest restored on pasture through natural secondary succession. Restoration Ecology 8: 380– 93. Finegan, B., and C. Sabogal. 1988. El desarrollo de sistemas de producción sostenible en bosques tropicales húmedos de bajura: un estudio de caso en Costa Rica. Chasqui 17: 3– 24. Finley-Brook, M. 2007. Green neoliberal space: the Mesoamerican Biological Corridor. Journal of Latin American Geography 6: 101– 24. Fishkind, A.S., and R.W. Sussman. 1987. Preliminary survey of the primates of the Zona Protectora and La Selva Biological Station, northeastern Costa Rica. Primate Conservation 8: 63– 66. Fix, A.G. 2002. Colonization models and initial genetic diversity in the Americas. Human Biology 74: 1– 10. Fleming, T.H. 1974. The population ecology of two species of Costa Rican heteromyid rodents. Ecology 55: 493– 510. Fleming, T.H., and E.R. Heithaus. 1981. Frugivorous bats, seed shadows, and the structure of tropical forests. Biotropica 13: 45– 53. Florax, R.J.G.M., C.M. Travisi, and P. Nijkamp. 2005. A meta-analysis of the willingness to pay for reductions in pesticide risk exposure. European Review of Agricultural Economics 32: 441– 67. Flores Rodas, J.G. 1984. Diagnostico del sector industria forestal. Dirección General Forestal, Ministerio de Agricultura y Ganaderia, San José, Costa Rica. Folgarait, P.J., L.A. Dyer, R.J. Marquis, and H.E. Braker. 1996. Leafcutting ant preferences for five native tropical plantation tree species growing under different light conditions. Entomologia Experimentalis et Applicata 80: 521– 30. Foster, V., and S. Mourato. 2000. Valuing the multiple impacts of pesticides use in the UK: a contingent ranking approach. Journal of Agricultural Economics 51: 1– 21. Frankie, G.W., H.G. Baker, and P.A. Opler. 1974. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology 62: 881– 919. Frazer, N.B., and R.C. Ladner. 1986. A growth curve for green sea turtles, Chelonia mydas, in the U.S. Virgin Islands, 1913– 1914. American Society of Ichthyologists and Herpetologists 1986: 798– 802. Gage, D.A., and D.R. Strong. 1981. The chemistry of Heliconia imbricata and Heliconia latispatha and the slow growth of a hispine beetle herbivore. Biochemical Systematics and Ecology 9: 79– 82. Galt, R.E. 2007. Regulatory risk and farmers’ caution with pesticides in Costa Rica. Transactions of the Institute of British Geographers 32: 377– 78. Galt, R.E. 2008a. Beyond the circle of poison: significant shifts in the global pesticide complex, 1976– 2008. Global Environmental Change 18: 786– 99. Galt, R.E. 2008b. Pesticides in export and domestic agriculture: reconsidering market orientation and pesticide use in Costa Rica. Geoforum 39: 1378– 92. Galt, R.E. 2008c. Toward an integrated understanding of pesticide use intensity in Costa Rican vegetable farming. Human Ecology 36: 655– 77. García-Robledo, C. 2010. Ecology and evolution of diet expansions to exotic hosts in generalist and specialist “rolled leaf” beetles (genus Cephaloleia, Coleoptera; Chrysomelidae). PhD diss., University of Miami.

576 Chapter 16 García-Robledo, C., and C.C. Horvitz. 2009. Host plant scents attract rolled-leaf beetles to Neotropical gingers in a Central American tropical rain forest. Entomologia Experimentalis et Applicata 131: 115– 20. García-Robledo, C., and C.C. Horvitz. 2011. Experimental demography and the vital rates of generalist and specialist insect herbivores on novel and native host plants. Journal of Animal Ecology 80: 976– 89. García-Robledo, C., and C.C. Horvitz. 2012a. Jack of all trades masters novel host plants: positive genetic correlations in specialist and generalist insect herbivores expanding their diets to novel hosts. Journal of Evolutionary Biology 25: 38– 53. García-Robledo, C., and C.C. Horvitz. 2012b. Parent-offspring conflicts, “optimal bad motherhood” and the “mother knows best” principles in insect herbivores colonizing novel host plants. Ecology and Evolution 25: 38– 53. García-Robledo, C., and E.K. Kuprewicz. 2009. Vertebrate fruit removal and ant seed dispersal in the Neotropical ginger Renealmia alpinia (Zingiberaceae). Biotropica 41: 209– 14. García-Robledo, C., and C.L. Staines. 2008. Herbivory in gingers from latest Cretaceous to present: is the ichnogenus Cephaloleichnites (Hispinae, Coleoptera) a rolled-leaf beetle? Journal of Paleontology 82: 1035– 37. García-Robledo, C., D.L. Erickson, C.L. Staines, T.L. Erwin, and W. J. Kress. 2013. Tropical plant– herbivore networks: reconstructing species interactions using DNA barcodes. PLOS ONE 8: e52967. doi:52910.51371/journal.pone.0052967. García-Serrano, C.R., and J.P. Del Monte. 2004. The use of tropical forest (agroecosystems and wild plant harvesting) as a source of food in the Bribri and Cabecar cultures in the Caribbean Coast of Costa Rica. Economic Botany 58: 58– 71. Garrigues, R., and R. Dean. 2007. The Birds of Costa Rica: A Field Guide. Ithaca, NY: Cornell University Press. Garrison, V.H., E.A. Shinn, W.T. Foreman, D.W. Griffin, C.W. Holmes, C.A. Kellogg, M.S. Majewski, L.L. Richardson, K.B. Ritchie, and G.W. Smith. 2003. African and Asian dust: from desert soils to coral reefs. BioScience 53: 469– 80. Genereux, D., and C. Pringle. 1997. Chemical mixing model of streamflow generation at La Selva Biological Station, Costa Rica. Journal of Hydrology 199: 319– 30. Gentry, A.H. 1982. Neotropical floristic diversity: phytogeographical connections between Central and South America, Pleistocene climatic fluctuations, or an accident of the Andean Orogeny? Annals of the Missouri Botanical Garden 69: 557– 93. Gentry, G.L., and L.A Dyer. 2002. On the conditional nature of Neotropical caterpillar defenses against their natural enemies. Ecology 83: 3108– 19. Goebel, T., M.R. Waters, and D.H. O’Rourke. 2008. The late Pleistocene dispersal of modern humans in the Americas. Science 319: 1497. Gotelli, N.J., and R.K. Colwell. 2001. Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecology Letters 4: 379– 91. Goulding, M. 1980. The Fishes and the Forest: Explorations in Amazonian Natural History. Berkeley: University of California Press. Graham, A. 1987. Miocene communities and paleoenvironments of Southern Costa Rica. American Journal of Botany 74: 1501– 18. Graham, A. 1992. Utilization of the isthmian land bridge during the Cenozoic: paleobotanical evidence for timing, and the selective in-

fluence of altitudes and climate. Review of Palaeobotany and Palynology 72: 119– 28. Graham, A., and D.L. Dilcher. 1998. Studies in Neotropical paleobotany. XII. A palynoflora from the Pliocene Río Banano formation of Costa Rica and the Neogene vegetation of Mesoamerica. American Journal of Botany 85: 1426– 38. Greiner, S., M. Nagy, M. Knörnschild, H. Hofer, and C.C. Voigt. 2013. Sex-biased senescence in a polygynous bat species. Ethology 119: 1– 9. Griffin, D.W. 2007. Atmospheric movement of microorganisms in clouds of desert dust and implications for human health. Clinical Microbiology Reviews 20: 459– 77. Griffiths, T. 2004. Help or hindrance?: the Global Environmental Facility, biodiversity conservation, and indigenous peoples. Cultural Survival Quarterly 28: 1– 11. Guariguata, M.R., R.L. Chazdon, J.S. Denslow, J.M. Dupuy, and L. Anderson. 1997. Structure and floristics of secondary and old-growth forest stands in lowland Costa Rica. Plant Ecology 132: 107– 20. Guariguata, M.R., and J.M. Dupuy. 1997. Forest regeneration in abandoned logging roads in lowland Costa Rica. Biotropica 29: 15– 28. Guariguata, M.R., J. Rosales, and B. Finegan. 2000. Seed removal and fate in two selectively logged lowland forests with contrasting protection levels. Conservation Biology 14: 1046– 54. Guillén, A.L. 1993. Inventario comercial y análisis silvicultural de bosques húmedos secundarios en la region Huétar Norte de Costa Rica. Thesis, Instituto Tecnológico de Costa Rica. Cartago, Costa Rica. Guyer, C., and M.A. Donnelly. 1990. Length-mass relationships among an assemblage of tropical snakes in Costa Rica. Journal of Tropical Ecology 6: 65– 76. Guyer, C., and M.A. Donnelly. 2005. Amphibians and Reptiles of La Selva, Costa Rica, and the Caribbean Slope. Berkeley: University of California Press. Haines, B.L. 1978. Element and energy flows through colonies of the leaf-cutting ant, Atta colombica, in Panama. Biotropica 10: 270– 77. Hamilton, D., V. Molina, P. Bosques, and G.V.N. Powell. 2003. El estatus del pájaro campana (Procnias tricarunculata): un ave en peligro de extinción. Zeledonia 7: 15– 24. Hammel, B.E., and N.A. Zamora. 1993. Ruptiliocarpon (Lepidobotryaceae): a new arborescent genus and tropical American link to Africa, with a reconsideration of the family. Novon 3: 408– 17. Harris, R.N., G. Spinelli, C.R. Ranero, I. Grevemeyer, H. Villinger, and U. Barckhausen. 2010. Thermal regime of the Costa Rican convergent margin: 2. Thermal models of the shallow Middle America subduction zone offshore Costa Rica. Geochemistry, Geophysics, Geosystems 11: 1– 22. Harrison, E., and Z. Meletis. 2010. Tourists and turtles: searching for a balance in Tortuguero, Costa Rica. Conservation and Society 8: 26– 43. Hartshorn, G.S. 1983. Plants: introduction. In D.H. Janzen, ed., Costa Rican Natural History, 118– 57. Chicago: University of Chicago Press. Hartshorn, G.S. 2006. Understanding tropical forests. BioScience 56: 264– 65. Hartshorn, G.S., and B.E. Hammel. 1994. Vegetation types and floristic patterns. In L.A. McDade, K.S. Bawa, H. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 73– 89. Chicago: University of Chicago Press. Hasbún, C.R., A. Gómez, G. Köhler, and D.H. Lunt. 2005. Mitochon-

The Caribbean Lowland Evergreen Moist and Wet Forests 577 drial DNA phylogeography of the Mesoamerican spiny-tailed lizards (Ctenosaura quinquecarinata complex): historical biogeography, species status and conservation. Molecular Ecology 14: 3095– 3107. Haug, G.H., R. Tiedemann, and L.D. Keigwin. 2004. How the Isthmus of Panama put ice in the Arctic. Oceanus 42: 95– 98. Haug, G.H., R. Tiedemann, R. Zahn, and A.C. Ravelo. 2001. Role of Panama uplift on oceanic freshwater balance. Geology 29: 207– 10. Heckenberger, M.J., A. Kuikuro, U.T. Kuikuro, J.C. Russell, M. Schmidt, C. Fausto, and B. Franchetto. 2003. Amazonia 1492: pristine forest or cultural parkland? Science 301: 1710– 14. Heithaus, E.R., and T.H. Fleming. 1978. Foraging movements of a frugivorous bat, Carollia perspicillata (Phyllostomatidae). Ecological Monographs 48: 127– 43. Herrera, B., and B. Finegan. 1997. Substrate conditions, foliar nutrients and the distributions of two canopy tree species in a Costa Rican secondary rain forest. Plant and Soil 191: 259– 67. Hespenheide, H.A. 1985. The visitor fauna of extrafloral nectaries of Byttneria aculeata (Sterculiaceae): relative importance and roles. Ecological Entomology 10: 191– 204. Hespenheide, H.A. 1991. Bionomics of leaf-mining insects. Annual Review of Entomology 36: 535– 60. Hiremat, A.J., J.J. Ewel, and T.G. Cole. 2002. Nutrient use efficiency in three fast-growing tropical trees. Forest Science 48: 662– 71. Hirth, H.F. 1963. Some aspects of the natural history of Iguana iguana on a tropical strand. Ecology 44: 613– 15. Hoernle, K., D.L. Abt, K.M. Fischer, H. Nichols, F. Hauff, G.A. Abers, P. Bogaard, K. van den Heydolph, G. Alvarado, M. Protti, and W. Strauch. 2008. Arc-parallel flow in the mantle wedge beneath Costa Rica and Nicaragua. Nature 451: 1094– 97. Hoernle, K., P. Bogaard, R. van den Werner, B. Lissinna, F. Hauff, G. Alvarado, and D. Garbe-Schöngberg. 2002. Missing history (16– 71 Ma) of the Galapagos hotspot: implications for the tectonic and biological evolution of the Americas. Geology 30: 795– 98. Hoffman, D.M. 2011. Do global statistics represent local reality and should they guide conservation policy?: examples from Costa Rica. Conservation Society 9: 16– 24. Holl, K.D. 2008. Are there benefits of bat roosts for tropical forest restoration? Conservation Biology 22: 1090– 91. Holtum, J.A.M., and K. Winter. 2010. Elevated CO2 and forest vegetation: more a water issue than a carbon issue? Functional Plant Biology 37: 694– 702. Horn, M.H. 1997. Evidence for dispersal of fig seeds by the fruit-eating characid fish Brycon guatemalensis Regan in a Costa Rican tropical rain forest. Oecologia 109: 259– 64. Horn, S.P. 2006. Pre-Columbian maize agriculture in Costa Rica: pollen and other evidence from lake and swamp sediments. In J. Staller, R. Tykot, and B. Benz, eds., Histories of Maize: Multidisciplinary Approaches to the Prehistory, Biogeography, Domestication, and Evolution of Maize, 367– 80. San Diego, CA: Elsevier Press. Horn, S.P., and L.M. Kennedy. 2001. Pollen evidence of maize cultivation 2700 years ago at La Selva Biological Station, Costa Rica. Biotropica 33: 191– 96. Horn, S.P., and R.L. Sanford. 1992. Holocene fires in Costa Rica. Biotropica 24: 354– 61. Horn, S.P., R.L.J. Sanford, D. Dilcher, T. Lott, P.R. Renne, M.C. Wiemann, D. Cozadd, and O. Vargas. 2003. Pleistocene plant fossils in and near La Selva Biological Station, Costa Rica. Biotropica 35: 434– 41.

Horvitz, C.C. 1981. Analysis of how ant behaviors affect germination in a tropical myrmecochore Calathea microcephala (P and E) Koernicke (Marantaceae). Microsite selection and aril removal by neotropical ants, Odontomachus, Pachycondyla, and Solenopsis (Formicidae). Oecologia 51: 47– 52. Howard, A.F. 1995. Price trends for stumpage and selected agricultural products in Costa Rica. Forest Ecology and Management 75: 101– 10. Howard, A.F., and J. Valerio. 1996. Financial returns from sustainable forest management and selected agricultural land-use options in Costa Rica. Forest Ecology and Management 81: 35– 49. Howe, H.F. 1977. Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58: 539– 50. Howe, H.F., and J. Smallwood. 1982. Ecology of seed dispersal. Annual Review of Ecology and Systematics 13: 201– 28. Huey, R.B., C.A. Deutsch, J.J. Tewksbury, L.J. Vitt, P.E. Hertz, H.J.A. Perez, and T. Garland. 2009. Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society B: Biological Sciences 276: 1939– 48. Hughen, K.A., T.I. Eglinton, L. Xu, and M. Makou. 2004. Abrupt tropical vegetation response to rapid climate changes. Science 304: 1955– 59. Humbert, S., M. Margni, R. Charles, O.M. Torres Salazar, A.L. Quirós, O. Jolliet. 2007. Toxicity assessment of the main pesticides used in Costa Rica. Agriculture, Ecosystems and Environment 118: 183– 90. IPCC. 2007. Summary for policymakers. In S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K.B. Averyt, M. Tignor, and H.L. Miller, eds., Climate Change 2007: The Physical Sciences. Contribution of Working Group 1 to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK: Cambridge University Press. Iriarte, J. 2011. Narrowing the gap: exploring the diversity of early foodproduction economies in the Americas. Current Anthropology 50: 677– 80. Iriarte, J., and E. Alonso. 2009. Phytolith analysis of selected native plants and modern soils from southeastern Uruguay and its implications for paleoenvironmental and archeological reconstruction. Quaternary International 193: 99– 123. Iriarte, J., I. Holst, O. Marozzi, C. Listopad, E. Alonso, A. Rinderknecht, and J. Montaña. 2004. Evidence for cultivar adoption and emerging complexity during the mid-Holocene in the La Plata basin. Nature 432: 614– 17. Irschick, D.J., L.J. Vitt, P.A. Zani, and J.B. Losos. 1997. A comparison of evolutionary radiations in mainland and Caribbean Anolis lizards. Ecology 78: 2191– 203. Islebe, G., H. Hooghiemstra, M. Brenner, J.H. Curtis, and D.A. Hodell. 1996. A Holocene vegetation history from lowland Guatemala. Holocene 6: 265– 71. Islebe, G., and O. Sánchez. 2002. History of Late Holocene vegetation at Quintana Roo, Caribbean coast of Mexico. Plant Ecology 160: 187– 92. IUCN. 2006. The 2006 IUCN Red List of Threatened Species. www .iucnredlist.org. IUCN. 2010. The 2010 IUCN Red List of Threatened Species. www .iucnredlist.org. Jackiewicz, E.L. 2006. Community-centered globalization: moderniza-

578 Chapter 16 tion under control in rural Costa Rica. Latin American Perspectives 33: 136– 46. Jackson, J.B.C. 1997. Reefs since Columbus. Coral Reefs 16(suppl.): S23– S32. Jacobson, S.K., and A. Figueroa López. 1994. Biological impacts of ecotourism: tourists and nesting turtles in Tortuguero National Park, Costa Rica. Wildlife Society Bulletin 22: 414– 19. Jacobson, S.K., and R. Robles. 1992. Ecotourism, sustainable development, and conservation education: development of a tour guide training program in Tortuguero, Costa Rica. Environmental Management 16: 701– 13. Jaga, K., and C. Dharmani. 2003. Global surveillance of DDT and DDE levels in human tissues. International Journal of Occupational Medicine and Environmental Health 16: 7– 20. Jain, S., and L.S. Collins. 2007. Trends in Caribbean paleoproductivity related to the Neogene closure of the Central American Seaway. Marine Micropaleontology 63: 57– 74. Jansen, M., A. Coors, R. Stoks, and L. De Meester. 2011. Evolutionary ecotoxicology of pesticide resistance: a case study in Daphnia. Ecotoxicology 20: 543– 51. Jentsch, A., J. Kreyling, and C. Beierkuhnlein. 2007. A new generation of climate-change experiments: events, not trends. Frontiers in Ecology and the Environment 5: 365– 74. Johnson, C.N. 2002. Determinants of loss of mammal species during the Late Quaternary ‘megafauna’ extinctions: life history and ecology, but not body size. Proceedings of the Royal Society of London, Series B 269: 2221– 27. Johnson, C.N. 2009. Ecological consequences of Late Quaternary extinctions of megafauna. Proceedings of the Royal Society of London, Series B 276: 2509– 19. Johnson, D.M. 2004a. Life history and demography of Cephaloleia fenestrata (Hispinae : Chrysomelidae : Coleoptera). Biotropica 36: 352– 61. Johnson, D.M. 2004b. Source-sink dynamics in a temporally heterogeneous environment. Ecology 85: 2037– 45. Johnson, D.M. 2005. Metapopulation models: an empirical test of model assumptions and evaluation methods. Ecology 86: 3088– 98. Johnson, D.M., and C.C. Horvitz. 2005. Estimating postnatal dispersal: tracking the unseen dispersers. Ecology 86: 1185– 90. Johnson, M., and S. Clisby. 2009. Naturalising distinctions: the contested field of environmental relations in Costa Rica. Landscape Research 34: 171– 87. Joyce, A.T. 2006. Land use change in Costa Rica: 1966– 2006, as influenced by social, economic, political, and environmental factors. San José, Costa Rica: Lil SA. Kahn, M. 2009. Economic evaluation of health cost of pesticide use: willingness to pay method. Pakistan Development Review 48: 459– 70. Kaiser, J. 2001. Bold corridor project confronts political reality. Science 293: 2196– 99. Kalacska, M., G.A. Sánchez-Azofeifa, B. Rivard, J.C. Calvo-Alvarado, and M. Quesada. 2008. Baseline assessment for environmental services payments from satellite imagery: a case study from Costa Rica and Mexico. Journal of Environmental Management 88: 348– 59. Kallos, G., A. Papadopoulos, P. Katsafados, and S. Nickovic. 2006. Transatlantic Saharan dust transport: model simulation and results. Journal of Geophysical Research 111: 1– 11.

Kaspari, M. 1993. Removal of seeds from Neotropical frugivore droppings: ant responses to seed number. Oecologia 95: 81– 88. Keigwin, L. 1982. Isotopic paleoceanography of the Caribbean and East Pacific: role of Panama uplift in Late Neogene time. Science 217: 350– 52. Kelm, D.H., K.R. Wiesner, and O. von Helversen. 2008. Effects of artificial roosts for frugivorous bats on seed dispersal in a Neotropical forest pasture mosaic. Conservation Biology 22: 733– 41. Kendall, R.I., and P.N. Smith. 2003. Wildlife toxicology revisited. Environmental Science and Technology 37: 178A– 183A. Kennedy, L.M., and S.P. Horn. 1997. Prehistoric maize cultivation at the La Selva Biological Station Costa Rica. Biotropica 29: 368– 70. Kennedy, L.M., and S.P. Horn. 2008. A Late Holocene pollen and charcoal record from La Selva Biological Station, Costa Rica. Biotropica 40: 11– 19. Keyeux, G., C. Rodas, N. Gelvez, and D. Carter. 2002. Possible migration routes into South America deduced from mitochondrial DNA studies in Colombian Amerindian populations. Human Biology 74: 211– 33. Kleber, M., L. Schwendenmann, E. Veldkamp, and R. Rößner Jahn. 2007. Halloysite versus gibbsite: silicon cycling as a pedogenetic process in two lowland neotropical rain forest soils of La Selva, Costa Rica. Geoderma 138: 1– 11. Koeppel, D. 2008. Banana: The Fate of the Fruit That Changed the World. New York: Penguin. Körner, C. 2009. Responses of humid tropical trees to rising CO2. Annual Review of Ecology, Evolution, and Systematics 40: 61– 79. Kraenzel, M., A. Castillo, T. Moore, and C. Potvin. 2003. Carbon storge of harvest-age teak (Tectona grandis) plantations in Panama. Forest Ecology and Management 173: 213– 25. Krech, S., III. 1999. The Ecological Indian. New York: W.W. Norton. Kubitzki, K., and A. Ziburski. 1994. Seed dispersal in flood plain forests of Amazonia. Biotropica 26: 30– 43. Kumar, B.M., and P.K.R. Nair. 2010. Tropical Homegardens. The Netherlands: Springer. Kuprewicz, E.K. 2010. The effects of large terrestrial mammals on seed fates, hoarding, and seedling survival in a Costa Rican rain forest. PhD diss., University of Miami. Kuprewicz, E.K. 2013. Mammal abundances and seed traits control the seed dispersal and predation roles of terrestrial mammals in a Costa Rican forest. Biotropica 45: 333– 42. Kuprewicz, E.K., and C. García-Robledo. 2010. Mammal and insect predation of chemically and structurally defended Mucuna holtonii (Fabaceae) seeds in a Costa Rican rain forest. Journal of Tropical Ecology 26: 263– 69. Kürschner, W.M., Z. Kvacek, and D.L. Dilcher. 2008. The impact of Miocene atmospheric fluctuations on climate and the evolution of terrestrial ecosystems. Proceedings of the National Academy of Sciences 105: 449– 53. Lagueux, C. 1998. Marine turtle fishery of Caribbean Nicaragua: human use patterns and harvest trends. Ph.D. diss., University of Florida. Lahanas, P.N., K.A. Bjorndal, A.B. Bolten, S.E. Encalada, M.M. Miyamoto, R.A. Valverde, and B.W. Bowen. 1998. Genetic composition of a green turtle (Chelonia mydas) feeding ground population: evidence for multiple origins. Marine Biology 130: 345– 52. Lampman, S.C. 2000. Environmental change in the Mesoamerican Biological Corridor. Journal of Forestry 98: S3. Landry, M.S., and C.T. Taggart. 2010. “Turtle watching” conservation

The Caribbean Lowland Evergreen Moist and Wet Forests 579 guidelines: green turtle (Chelonia mydas) tourism in nearshore coastal environments. Biodiversity and Conservation 19: 305– 12. Lane, C.S., C.I. Mora, S.P. Horn, K.H. Orvis. 2008. Sensitivity of bulk sedimentary stable carbon isotopes to prehistoric forest clearance and maize agriculture. Journal of Archaeological Science 35: 2119– 32. Lansing, D.M. 2011. Realizing carbon’s value: discourse and calculation in the production of carbon forestry offsets in Costa Rica. Antipode 43: 731– 53. LaVal, R.K. 1977. Notes on some Costa Rican bats. Brenesia 10/11: 77– 83. LaVal, R.K., and B. Rodríguez-Herrera. 2002. Murciélagos de Costa Rica: Bats. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Lavin, M., B.P. Schrire, G. Lewis, R.T. Pennington, A. Delgado-Salinas, M. Thulin, C.E. Hughes, A. Beyra Matos, and M.F. Wojciechowski. 2004. Metacommunity process rather than continental tectonic history better explains geographically structured phylogenies in legumes. Philosophical Transactions of the Royal Society B: Biological Sciences 359: 1509– 22. Lawler, J.J., S.L. Shafer, and A.R. Blaustein. 2009. Projected climate impacts for the amphibians of the Western Hemisphere. Conservation Biology 24: 38– 50. Le, M., and W.P. McCord. 2008. Phylogenetic relationships and biogeographical history of the genus Rhinoclemmys Fitzinger, 1835 and the monophyly of the turtle family Geoemydidae ( Testudines: Testudinoidea). Zoological Journal of the Linnean Society 153: 751– 67. Le Corff, J., and C.C. Horvitz. 1995. Dispersal of seeds from chasmogamous and cleistogamous flowers in an ant-dispersed Neotropical herb. Oikos 73: 59– 64. Lee, D.N.B., and D.J. Snepenger. 1992. An ecotourism assessment of Tortuguero, Costa Rica. Annals of Tourism Research 19: 367– 70. Lefever, H.G. 1992. Turtle bogue: Afro-Caribbean life and culture in a Costa Rican village. Selingsgrove, London. Leigh, E.G. 1999. Tropical Forest Ecology: A View from Barro Colorado Island. Oxford: Oxford University Press. Lessios, H.A. 2008. The Great American Schism: divergence of marine organisms after the rise of the Central American Isthmus. Annual Review of Ecology, Evolution, and Systematics. Letcher, S.G. 2010. Phylogenetic structure of angiosperm communities during tropical forest succession. Proceedings of the Royal Society of London, Series B 277: 97– 104. Letcher, S.G., and R.I. Chazdon. 2009a. Rapid recovery of biomass, species richness, and species composition in a forest chronosequence in northeastern Costa Rica. Biotropica 41: 608– 17. Letcher, S.G., and R.I. Chazdon. 2009b. Lianas and self-supporting plants during tropical forest succession. Forest Ecology and Management 257: 2150– 56. Levey, D.J. 1987. Seed size and fruit-handling techniques of avian frugivores. American Naturalist 129: 471– 85. Levey, D.J., and M.M. Byrne. 1993. Complex ant plant interactions: rainforest ants as secondary dispersers and postdispersal seed predators. Ecology 74: 1802– 12. Levey, D.J., T.C. Moermond, and J.S. Denslow. 1994. Frugivory: an overview. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 282– 94. Chicago: University of Chicago Press. Levey, D.J., and F.G. Stiles. 1994. Birds: ecology, behavior, and taxo-

nomic affinities. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rainforest, 217– 28. Chicago: University of Chicago Press. Lewis, S.L., J. Lloyd, S. Sitch, E.T.A. Mitchard, and W.F. Laurance. 2009. Changing ecology of tropical forests: evidence and drivers. Annual Review of Ecology, Evolution, and Systematics 40: 529– 49. Lieberman, D., M. Lieberman, R. Peralta, and G. Hartshorn. 1996. Tropical forest structure and composition on a large-scale altitudinal gradient in Costa Rica. Journal of Ecology 84: 137– 52. Lieberman, S.S. 1986. Ecology of the leaf litter herpetofauna of a neotropical rain forest: La Selva, Costa Rica. Acta Zoológica Mexicana 15: 1– 72. Liess, M., and P. von der Ohe. 2005. Analyzing effects of pesticides on invertebrate communities in streams. Environmental Toxicology and Chemistry 24: 954– 65. Ling, A., and M.O. Jarocki. 2003. Pesticide justice. Multinational Monitor 24: 6. Lips, K.R., F. Brem, R. Brenes, J.D. Reeve, R.A. Alford, J. Voyles, C. Carey, L. Livo, A.P. Pessier, and J.P. Collins. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences 103: 3165– 70. Lips, K.R., P.A. Burrowes, J.R. Mendelson, and G. Parra-Olea. 2005. Amphibian declines in Latin America: widespread population declines, extinctions, and impacts. Biotropica 37: 163– 65. Lips, K.R., J. Diffendorfer, J.R. Mendelson, and M.W. Sears. 2008. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. PLOS Biology 6: 441– 54. Loiselle, B.A., and J.G. Blake. 1999. Dispersal of melastome seeds by fruit-eating birds of tropical forest understory. Ecology 80: 330– 36. Longino, J.T., J. Coddington, and R.K. Colwell. 2002. The ant fauna of a tropical rain forest: estimating species richness three different ways. Ecology 83: 689– 702. Lonsdale, P. 2005. Creation of the Cocos and Nazca plates by fission of the Farallon Plate. Tectonophysics 404: 237– 64. Lorenz, M.W. 2009. Migration and trans-Atlantic flight of locusts. Quaternary International 196: 4– 12. Lovelock, C.E., and J.J. Ewel. 2005. Links between tree species, symbiotic fungal diversity and ecosystem functioning in simplified tropical ecosystems. New Phytologist 167: 219– 28. Lowman, M.D. 1995. Herbivory as a canopy process in rain forest trees. In M.D. Lowman and N.M. Nadkarni, eds., Forest Canopies. New York: Academic Press. Lozano-García, M.d.S., M. Caballero, B. Ortega, A. Rodriguez, and S. Sosa. 2007. Tracing the effects of the Little Ice Age in the tropical lowlands of eastern Mesoamerica. Proceedings of the National Academy of Sciences 104: 16200– 16203. Lubick, N. 2007. DDT’s resurrection. Environmental Science and Technology (September 15): 6323– 25. Lumpkin, H.A., and W.A. Boyle. 2009. Effects of forest age on fruit composition and removal in tropical bird-dispersed understorey trees. Journal of Tropical Ecology 25: 515– 22. Lutz, E. 1993. Interdisciplinary fact-finding on current deforestation in Costa Rica. The World Bank Environmental Department, Environmental Working Paper No. 61. Lyons, S.K., F.A. Smith, and J.H. Brown. 2004. Of mice, mastodons and

580 Chapter 16 men: human-mediated extinctions on four continents. Evolutionary Ecology Research 6: 339– 58. MacFadden, B.J. 2006. Extinct mammalian biodiversity of the ancient New World tropics. Trends in Ecology and Evolution 21: 157– 65. MacMillan, I., P.B. Gans, and G. Alvarado. 2004. Middle Miocene to present plate tectonic history of the southern Central American Volcanic Arc. Tectonophysics 392: 325– 48. Malhi, Y., L.E.O.C. Aragão, D. Galbraith, C. Huntingford, R. Fisher, P. Zelazowski, S. Sitch, C. McSweeney, and P. Meir. 2009. Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest. Proceedings of the National Academy of Sciences 106: 20610– 15. Malhi, Y., and O.L. Phillips. 2004. Tropical forests and global atmospheric change: a synthesis. Philosophical Transactions of the Royal Society of London, Series B 359: 549– 55. Malhi, Y., O.L. Phillips, J. Lloyd, et al. 2002. An international network to monitor the structure, composition and dynamics of Amazonian forests (RAINFOR). Journal of Vegetation Science 13: 439– 50. Malhi, Y., and J. Wright. 2004. Spatial patterns and recent trends in the climate of tropical rainforest regions. Philosophical Transactions of the Royal Society of London, Series B 359: 311– 29. Mann, C.C. 2005. 1491: New Revelations of the Americas before Columbus. New York: Vintage Books. Marengo, J.A., J. Tomasella, L.M. Alves, W.R. Soares, and D.A. Rodríguez. 2011. The drought of 2010 in the context of historical droughts in the Amazon region. Geophysical Research Letters 38: 12703– 7. Margni, M., D. Rossier, P. Crettaz, and O. Jolliet. 2002. Life cycle impact assessment of pesticides on human health and ecosystems. Agriculture, Ecosystems and Environment 93: 379– 92. Marquardt, S. 2002. Pesticides, parakeets, and unions in the Costa Rican banana industry, 1938– 1962. Latin American Research Review 37: 3– 36. Marques, M.C.M., M.D. Swaine, and D. Liebsch. 2011. Diversity distribution and floristic differentiation of the coastal lowland vegetation: implications for the conservation of the Brazilian Atlantic forest. Biodiversity and Conservation 20: 153– 68. Marquis, R. 1990. Genotypic variation in leaf damage in Piper arieianum (Piperaceae) by a multispecies assemblage of herbivores. Evolution 44: 104– 20. Marquis, R. 1992. A bite is a bite is a bite?: Constraints on response to folivory in Piper arieianum (Piperaceae). Ecology 73: 143– 52. Marquis, R.J. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226: 537– 39. Marquis, R.J., and E. Braker. 1994. Plant– herbivore interactions: diversity, specificity and impact. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 261– 81. Chicago: University of Chicago Press. Martin, P.S. 1967. Prehistoric overkill. In P.S. Martin and H.E. Wright Jr., eds., Pleistocene Extinctions: The Search for a Cause, 75– 120. New Haven: Yale University Press. Martin, P.S. 1984. Prehistoric overkill: the global model. In P.S. Martin and R.G. Klein, eds., Quaternary Extinctions: A Prehistoric Revolution, 354– 403. Tucson, AZ: University of Arizona Press. Matlock, R.B., Jr., D. Rogers, P.J. Edwards, and S.G. Martin. 2002. Avian communities in forest fragments and reforestation areas associated

with banana plantations in Costa Rica. Agriculture, Ecosystems and Environment 91: 199– 215. MBC. 2002. The Mesoamerican Biological Corridor: a platform for sustainable development. Managua, Comisión Centroamericana de Ambiente y Desarrollo (CCAD). United Nations Development Program/Global Environmental Facility. McClenachan, L., J.B.C. Jackson, and M.J.H. Newman. 2006. Conservation implications of historic sea turtle nesting beach loss. Frontiers in Ecology and the Environment 4: 290– 96. McDade, L.A., K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds. 1994. La Selva: Ecology and Natural History of a Neotropical Rainforest. Chicago: University of Chicago Press. McGee, D., F. Marcantonio, and J. Lynch-Stieglitz. 2007. Deglacial changes in dust flux in the eastern equatorial Pacific. Earth and Planetary Science Letters 257: 215– 30. McKenna, D.D., and B.D. Farrell. 2005. Molecular phylogenetics and evolution of host plant use in the Neotropical rolled leaf ‘hispine’ beetle genus Cephaloleia (Chevrolat) (Chrysomelidae: Cassidinae). Molecular Phylogenetics and Evolution 37: 117– 31. McKenna, D.D., and B.D. Farrell. 2006. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proceedings of the National Academy of Sciences 103: 10947– 51. Meletis, Z.A. 2007. Wasted visits?: ecotourism in theory vs. practice at Tortuguero, Costa Rica. Ph.D diss., Duke University. Meletis, Z.A., and L.M. Campbell. 2009. Call it consumption!: (Re)conceptualizing ecotourism as consumption and consumptive. Geography Compass 1: 850– 70. Melillo, J.M., P.A. Steudler, J.D. Aber, K. Newkirk, H. Lux, F.P. Bowles, C.  Catricala, A. Magill, T. Ahrens, and S. Morrisseau. 2002. Soil warming and carbon-cycle feedbacks to the climate system. Science 298: 2173– 76. Melo, F.P.L., B. Rodríguez-Herrera, R.L. Chazdon, R.A. Medellin, and G.G. Ceballos. 2009. Small tent-roosting bats promote dispersal of large-seeded plants in a Neotropical forest. Biotropica 41: 737– 43. Michel, N.L. 2012. Mechanisms and consequences of avian understory insectivore population decline in fragmented Neotropical rainforest. PhD diss., Tulane University. Michel, N.L., T.W. Sherry, and W.P. Carson. 2014. The omnivorous collared peccary negates an insectivore-generated trophic cascade in Costa Rican wet tropical forest understorey. Journal of Tropical Ecology 1: 1– 11. Miller, K., E. Chang, and N. Johnson. 2001. Defining common ground for the Mesoamerican Biological Corridor. Washington, DC: World Resources Institute. Miller, M.J. 2011. Persistent illegal logging in Costa Rica: the role of corruption among forestry regulators. Journal of Environment Development 20: 50– 68. Minc, G., D. Rodríguez, S. Sakai, R. Quiroga, L. Taber, and A. Rodríguez. 2001. The Mesoamerican Biological Corridor as a vector for sustainable development in the region: the role of international financing, preliminary considerations. Washington, DC: Inter-American Development Bank and World Bank. Mnif, W., A.I.H. Hassine, A. Bouaziz, A. Bartegi, O. Thomas, and B. Roig. 2011. Effect of endocrine disruptor pesticides: a review. International Journal of Environmental Research and Public Health 8: 2265– 303. Molina, I., and S. Palmer. 2007. The History of Costa Rica. San José, Costa Rica: Editorial UCR.

The Caribbean Lowland Evergreen Moist and Wet Forests 581 Molnar, P. 2008. Closing of the Central American Seaway and the Ice Age: a critical review. Paleoceanography 23: 1– 15. Monge, G., O. Chassot, G.V.N. Powell, S. Palminteri, U.A. Zelaya, and P. Wright. 2003. Ecología de la lapa verde (Ara ambigua) en Costa Rica. San José, Costa Rica: Centro Cientifico Tropical. Monge, P., T. Partanen, C. Wesseling, V. Bravo, C. Ruepert, and I. Burstyn. 2005. Assessment of pesticide exposure in the agricultural population of Costa Rica. Annals of Occupational Hygiene 49: 375– 84. Montagnini, F. 1994. Agricultural systems in the La Selva region. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 307– 16. Chicago: University of Chicago Press. Montagnini, F., E. González, C. Porras, and R. Rheingans. 1995. Mixed and pure forest plantations in the humid tropics. Commonwealth Forestry Review 74: 306– 14. Montagnini, F., K. Ramstad, and F. Sancho. 1993. Litterfall, litter decomposition and the use of mulch of four indigenous tree species in the Atlantic lowlands of CR. Agroforestry Systems 23: 39– 61. Monzón-Argüello, C., L.F. López-Jurado, C. Rico, A. Marco, P. López, G.C. Hays, and P.L.M. Lee. 2010. Evidence from genetic and Lagrangian drifter data for transatlantic transport of small juvenile green turtles. Journal of Biogeography 37: 1752– 66. Moran, R., and A.R. Smith. 2001. Phytogeographic relationships between neotropical and African-Madagascan pteridophytes. Brittonia 53: 304– 51. Morrison, G., and D.R. Strong. 1981. Spatial variations in egg density and the intensity of parasitism in a Neotropical chrysomelid (Cephaloleia consanguinea). Ecological Entomology 6: 55– 61. Morse, W.C., J.L. Schedlbauer, S.E. Sesnie, B. Finegan, C.A. Harvey, S.J. Hollenhorst, K.L. Kavanagh, D. Stoian, and J.D. Wulfhorst. 2009. Consequences of environmental service payments for forest retention and recruitment in a Costa Rican biological corridor. Ecology and Society 14: 23– 43. Mortimer, J.A. 1995. Teaching critical concepts for the conservation of sea turtles. Marine Turtle Newsletter 71: 1– 4. Muhs, D.R., and J.R. Budahn. 2009. Geochemical evidence for African dust and volcanic ash inputs to terra rossa soils on carbonate reef terraces, northern Jamaica, West Indies. Quaternary International 196: 13– 35. Müller, M. 2000. Review of the in situ status of the great green or Buffon’s macaw Ara ambigua and the European Endangered Species Programme (EEP). International Zoo Yearbook 37: 183– 90. Mundt, C.C., K.E. Sackett, L.D. Wallace, C. Cowger, and J.P. Dudley. 2009. Aerial dispersal and multiple-scale spread of epidemic disease. EcoHealth 6: 546– 52. Nadkarni, N.M., and N.T. Wheelwright. 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. New York: Oxford University Press. Nag, S.K., and M.K. Raikwar. 2011. Persistent organochlorine pesticide residues in animal feed. Environmental Monitoring and Assessment 174: 327– 35. Neelin, J.D., M. Munnich, H. Su, J.E. Meyerson, and C.E. Holloway. 2006. Tropical drying trends in global warming models and observations. Proceedings of the National Academy of Sciences 103: 6110– 15. Newcomer, Q. 2002. Path of the tapir: integrating biological corridors, ecosystem management, and socioeconomic development in Costa Rica. Endangered Species Update 19: 186– 93.

Newson, L. 1993. The demographic collapse of native peoples of the Americas, 1492– 1650. In W. Bray, ed., The Meeting of Two Worlds, 247– 88. British Academy. Nichols-Orians, C.M. 1991a. Condensed tannins, attine ants, and the performance of a symbiotic fungus. Journal of Chemical Ecology 17: 1177– 95. Nichols-Orians, C.M. 1991b. Differential effects of condensed and hydrolyzable tannin on polyphenol oxidase activity of attine symbiotic fungus. Journal of Chemical Ecology 17: 1811– 19. Nichols-Orians, C.M. 1991c. The effects of light on foliar chemistry, growth and susceptibility of seedlings of a canopy tree to an attine ant. Oecologia 86: 552– 60. Nichols-Orians, C.M. 1991d. Environmentally induced differences in plant traits: consequences for susceptibility to a leaf-cutter ant. Ecology 72: 1609– 23. Nicotra, A.B., R.L. Chazdon, and S. Iriarte. 1999. Spatial heterogeneity of light and woody seedling regeneration in tropical wet forests. Ecology 80: 1908– 26. Nieuwenhuyse, A., A.G. Jongmans, and N. van Breemen. 1993. Andisol formation in a Holocene beach ridge plain under the humid tropical climate of the Atlantic coast of Costa Rica. Geoderma 57: 423– 42. Nieuwenhuyse, A., and S.B. Kroonenberg. 1994. Volcanic origin of Holocene beach ridges along the Caribbean coast of Costa Rica. Marine Geology 120: 13– 26. Nof, D., and S. Van Gorder. 2003. Did an open Panama Isthmus correspond to an invasion of Pacific water into the Atlantic? Journal of Physical Oceanography 33: 1324– 36. Nolte, P. 2011. Pesticide resistance: what action will you take? American Vegetable Grower 59: 28. Norden, N., R.L. Chazdon, A. Chao, Y.-H. Jiang, and B.A. Vílchez. 2009. Resilience of tropical rain forests: tree community reassembly in secondary forests. Ecology Letters 12: 385– 94. Notman, E.M., and A.C. Villegas. 2005. Patterns of seed predation by vertebrate versus invertebrate seed predators among different plant species, seasons and spatial distributions. In P.-M. Forget, J.E. Lambert, P.E. Hulme, and S.B. Van der Wall, eds., Seed Fate, Predation, Dispersal and Seedling Establishment, 55– 75. Wallingford: CABI Publishing. Novotný, V., and Y. Basset. 2000. Rare species in communities of tropical insect herbivores: pondering the mystery of singletons. Oikos 89: 564– 72. Novotný, V., S.E. Miller, Y. Basset, L. Cizek, P. Drozd, K. Darrow, and J. Leps. 2002. Predictably simple: assemblages of caterpillars (Lepidoptera) feeding on rainforest trees in Papua New Guinea. Proceedings of the Royal Society B 269: 2337– 44. Okello, J.J., and S.M. Swinton. 2010. From circle of poison to circle of virtue: pesticides, export standards and Kenya’s green bean farmers. Journal of Agricultural Economics 61: 209– 24. Orians, G.H. 1969. The number of birds species in some tropical forests. Ecology 50: 783– 801. Pagiola, S. 2008. Payments for environmental services in Costa Rica. Ecological Economics 65: 712– 24. Paige, J.M. 1997. Coffee and Power: Revolution and the Rise of Democracy in Central America. Cambridge, MA: Harvard University Press. Palmer, S., and I. Molina, eds. 2004. The Costa Rica Reader. Durham: Duke University Press.

582 Chapter 16 Parker, G.G. 1994. Soil fertility, nutrient availability, and nutrient cycling. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 54– 64. Chicago: University of Chicago Press. Parker, T.A., III, D.F. Stotz, and J.W. Fitzpatrick. 1996. Ecological and distributional databases. In D.F. Stotz, J.W. Fitzpatrick, T.A. Parker III, and D.K. Moskovits, eds., Neotropical Birds: Ecology and Conservation, 115– 436. Chicago: University of Chicago Press. Passos, L., and P.S. Oliveira. 2002. Ants affect the distribution and performance of seedlings of Clusia criuva, a primarily bird-dispersed rain forest tree. Journal of Ecology 90: 517– 28. Pelley, J. 2006. DDT’s legacy lasts for many decades. Environmental Science and Technology 40: 4533– 34. Peñaloza, C., and A.G. Farji-Brener. 2003. The importance of treefall gaps as foraging sites for leaf-cutting ants depends on forest age. Journal of Tropical Ecology 19: 603– 5. Pennington, R.T., J.E. Richardson, and M. Lavin. 2006. Insights into the historical construction of species-rich biomes from dated plant phylogenies, neutral ecological theory and phylogenetic community structure. New Phytologist 172: 605– 16. Pérez, S., and F. Protti. 1978. Comportamiento del sector forestal durante el periodo 1950– 1977. DOC-OPSA-15zs Oficina de Planificación Sectorial Agropecuaria, San José, Costa Rica. Pérez-Maldonado, I.N., A. Trejo, C. Ruepert, R.D.C. Jovel, M.P. Méndez, M. Ferrari, E. Saballos-Sobalvarro, C. Alexander, L. Yáñez-Estrada, D. Lopez, S. Henao, E.R. Pinto, and F. Díaz-Barriga. 2010. Assessment of DDT levels in selected environmental media and biological samples from Mexico and Central America. Chemosphere 78: 1244– 49. Perfecto, I., and J. Vandermeer. 1993. Distribution and turnover rate of a population of Atta cephalotes in a tropical rain forest in Costa Rica. Biotropica 25: 316– 21. Perkins, S. 2001. Dust, the thermostat. Science News 160: 200– 202. Pinto-Tomas, A.A., M.A. Anderson, G. Suen, D.M. Stevenson, F.S.T. Chu, W.W. Cleland, P.J. Weimer, and C.R. Currie. 2009. Symbiotic nitrogen fixation in the fungus gardens of leaf-cutter ants. Science 326: 1120– 23. Piperno, D.R., and T.D. Dillehay. 2008. Starch grains on human teeth reveal early broad crop diet in northern Peru. Proceedings of the National Academy of Sciences 105: 19622– 27. Piperno, D.R., and I. Holst. 1998. The presence of starch grains on prehistoric stone tools from the humid Neotropics: indications of early tuber use and agriculture in Panama. Journal of Archaeological Science 25: 765– 76. Piperno, D.R., and D.M. Pearsall. 1998. The Origins of Agriculture in the Lowland Neotropics. San Diego: Academic Press. Piperno, D.R., A.J. Ranere, I. Holst, and P. Hansell. 2000. Starch grains reveal early root crop horticulture in the Panamanian tropical forest. Nature 407: 894– 97. Pisani, J.M., W.E. Grant, and M. Mora. 2008. Simulating the impact of cholinesterase-inhibiting pesticides on non-target wildlife in irrigated crops. Ecological Modelling 210: 179– 92. Place, S.E. 1991. Nature tourism and rural development in Tortuguero. Annals of Tourism Research 18: 186– 201. Polidoro, B.A., R.M. Dahlquist, L.E. Castillo, M.J. Morra, E. Somarriba, and N.A. Bosque-Pérez. 2008. Pesticide application practices, pest knowledge, and cost-benefits of plantain production in the Bribri–

Cabécar Indigenous Territories, Costa Rica. Environmental Research 108: 98– 106. Porder, S., D. Clark, and P.M. Vitousek. 2006. Persistence of rock-derived nutrients in the wet tropical forests of La Selva. Costa Rica. Ecology 87: 594– 602. Poux, C., P. Chevret, D. Huchon, W.W.D.J.E. Jong, P. Douzery, and S. Url. 2006. Arrival and diversification of caviomorph rodents and platyrrhine primates in South America. Systematic Biology 55: 228– 44. Powell, G., and R. Bjork. 1994. Implications of altitudinal migration for conservation strategies to protect tropical biodiversity: a case study of the resplendent quetzal (Pharomachrus mocinno) at Monteverde, Costa Rica. Bird Conservation International 4: 161– 74. Powell, G., P. Wright, C. Guindon, and R. Alemán Bjork. 1999. Resultados y recomendaciones para la conservación de la lapa verde (Ara ambigua) en Costa Rica. San José, Costa Rica: Centro Cientifico Tropical. Powell, G.V.N., J. Barborak, and S.M. Rodriguez. 2000. Assessing representativeness of protected natural areas in Costa Rica for conserving biodiversity: a preliminary gap analysis. Biological Conservation 93: 35– 41. Powers, J.S., M.D. Corre, T.E. Twine, and E. Veldkamp. 2011. Geographic bias of field observations of soil carbon stocks with tropical land-use changes precludes spatial extrapolation. Proceedings of the National Academy of Sciences 108: 6318– 22. Powers, J.S., and W.H. Schlesinger. 2002a. Geographic and vertical patterns of stable carbon isotopes in tropical rain forest soils in Costa Rica. Geoderma 109: 141– 60. Powers, J.S., and W.H. Schlesinger. 2002b. Relationships among soil carbon distributions and biophysical factors at nested spatial scales in rain forests of northeastern Costa Rica. Geoderma 109: 165– 90. Powers, T.O., D.A. Neher, P. Mullin, A. Esquivel, R.M. Giblin-Davis, N. Kanzaki, S.P. Stock, M.M. Mora, and L. Uribe-Lorio. 2009. Tropical nematode diversity: vertical stratification of nematode communities in a Costa Rican humid lowland rainforest. Molecular Ecology 18: 985– 96. Puschendorf, R., F. Bolaños, and G. Chaves. 2006. The amphibian chytrid fungus along an altitudinal transect before the first reported declines in Costa Rica. Biological Conservation 132: 136– 42. Puschendorf, R., A.C. Carnaval, J. van der Wal, H. Zumbado-Ulate, G. Chaves, F. Bolaños, and R.A. Alford. 2009. Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool. Diversity and Distributions 15: 401– 8. Puschendorf, R., G. Chaves, A.J. Crawford, and D.R. Brooks. 2005. Eleutherodactylus ranoides (NCN): dry forest population, refuge from decline? Herpetological Review 36: 53. Pyke, C.R., R. Condit, A. Salomón, and S. Lao. 2001. Floristic composition across a climatic gradient in a neotropical lowland forest. Journal of Vegetation Science 12: 553– 66. Raich, J.W., A.E. Russell, K. Kitayama, W.J. Parton, and P.M. Vitousek. 2006. Temperature influences carbon accumulation in moist tropical forests. Ecology 87: 76– 87. Ramírez, O.A., C.E. Carpio, R. Ortíz, and B. Finegan. 2002. Economic value of carbon sink services of tropical secondary forests and its management implications. Environmental and Resource Economics 21: 23– 46. Raymond, M., C. Berticat, M. Weill, N. Pasteur, and C. Chevillon. 2001.

The Caribbean Lowland Evergreen Moist and Wet Forests 583 Insecticide resistance in the mosquito Culex pipiens: what have we learned about adaptation? Genetica 112: 287– 96. Read, J.M. 1999. Land-cover change detection for the tropics using remote sensing and geographic information systems. PhD diss., Louisiana State University. Read, J.M., J.S. Denslow, and S.M. Guzman. 2001. Documenting land cover history of a humid tropical environment in northeastern Costa Rica using time-series remotely sensed data. In A.C. Millington, S.J. Walsh, and P.E. Osborne, eds., GIS and Remote Sensing Applications in Biogeography and Ecology. Boston, MA: Kluwer Academic Publishers. Redondo-Brenes, A., and F. Montagnini. 2006. Growth, productivity, aboveground biomass, and carbon sequestration of pure and mixed native tree plantations in the Caribbean lowlands of Costa Rica. Forest Ecology and Management 232: 168– 78. Redondo-Brenes, A., A. Vílchez, and R.L. Chazdon. 2001. Estudio de la dinámina y composición de cuatro bosques secundarios en la región Huetar Norte, Sarapiquí, Costa Rica. Revista Forestal Centroamericana 36 (Oct– Dec): 21– 26. Reed, S.C., T.E. Wood, M.A. Cavaleri. 2012. Tropical forests in a warming world. New Phytologist 193: 27– 29. Reguero, M., A.M. Candela, and R.N. Alonso. 2007. Biochronology and biostratigraphy of the Uquía Formation (Pliocene– early Pleistocene, NW Argentina) and its significance in the Great American Biotic Interchange. Journal of South American Earth Sciences 23: 1– 16. Reich, A., J.J. Ewel, N.M. Nadkarni, T. Dawson, and R.D. Evans. 2003. Nitrogen isotope ratios shift with plant size in tropical bromeliads. Oecologia 137: 587– 90. Rieser, A. 2012. The Case of the Green Turtle: An Uncensored History of a Conservation Icon. Baltimore: Johns Hopkins University Press. Renner, S.S. 2004a. Bayesian analyses of combined data partitions, using multiple calibrations, supports recent arrivals of Melastomataceae in Africa and Madagascar. American Journal of Botany 88: 1290– 300. Renner, S.S. 2004b. Plant dispersal across the tropical Atlantic by wind and sea currents. International Journal of Plant Sciences 165(Suppl.): S23– S33. Renner, S.S. 2005. Relaxed molecular clocks for dating historical plant dispersal events. Trends in Plant Science 10: 550– 58. Ridgely, R.S., and J.A. Gwynne. 1992. A Guide to the Birds of Panama: With Costa Rica, Nicaragua, and Honduras. Princeton, NJ: Princeton University Press. 656 pp. Rinker, B.H., and M.D. Lowman. 2001. Canopy herbivory and soil ecology, the top– down impact of forest processes. Selbyana 22: 225– 31. Roder, C., J. Cortés, C. Jiménez, and R. Lara. 2009. Riverine input of particulate material and inorganic nutrients to a coastal reef ecosystem at the Caribbean coast of Costa Rica. Marine Pollution Bulletin 58: 1937– 43. Rodríguez-Herrera, B., R.A. Medellín, and M. Gambia-Ríos. 2008. Roosting requirements of white tent-making bat Ectophylla alba (Chiroptera: Phyllostomidae). Acta Chiropterologica 10: 89– 95. Rodríguez-Herrera, B., R.A. Medellín, and R.M. Timm. 2007. Murciélagos neotropicales que acampan en hojas: neotropical tent-roosting bats. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Rodríguez-Herrera, B., and M. Tschapka. 1999. Tent use by Vampyressa

nymphaea (Chiroptera: Phyllostomidae) in Cecropia insignis (Moraceae) in Costa Rica. Acta Chiropterologica 6: 171– 74. Romero, A., B.J. O’Neill, R.M. Timm, K.G. Gerow, and D. McClearn. 2013. Group dynamics, behavior, and current and historical abundance of peccaries in Costa Rica’s Caribbean lowlands. Journal of Mammalogy 94: 771– 91. Romero, A., and R.M. Timm. 2013. Reproductive strategies and natural history of the arboreal, Neotropical vesper mouse, Nyctomys sumichrasti. Mammalia 77: 363– 70. Rosero-Bixby, L., and A. Palloni. 1998. Population and deforestation in Costa Rica. Population and Environment 20: 149– 85. Ross, Y., and L. Capelli. 2003. Passion for the Caribbean. San José, Costa Rica: Grupo Santillana SA. Rowell, C.H.F. 1985a. The feeding biology of a species-rich genus of rainforest grasshoppers (Rhachicreagra: Orthoptera, Acrididae), I. Foodplant use and foodplant acceptance. Oecologia 68: 87– 98. Rowell, C.H.F. 1985b. The feeding biology of a species-rich genus of rainforest grasshoppers (Rhachicreagra: Orthoptera, Acrididae), II. Foodplant preference and its relation to speciation. Oecologia 68: 99– 104. Rowell, H.F. 1978. Food plant specificity in neotropical rain-forest acridids. Entomologia Experimentalis et Applicata 24: 651– 62. Rowell, H.F. 1983a. Checklist of acridoid grasshoppers. In D.H. Janzen, ed., Costa Rican Natural History, 651– 53. Chicago: University of Chicago Press. Rowell, H.F. 1983b. Drymophilacris bimaculata. In D.H. Janzen, ed., Costa Rican Natural History, 714– 16. Chicago: University of Chicago Press. Rowell, H.F. 1983c. Osmilia flavolineata. In D.H. Janzen, ed., Costa Rican Natural History, 750– 51. Chicago: University of Chicago Press. Rowell, H.F. 1983d. Tropidacris cristata. In D.H. Janzen, ed., Costa Rican Natural History, 772– 73. Chicago: University of Chicago Press. Ruiz-Narváez, E.A., F.R. Santos, D. de Carvalho-Silva, and J. Azofeifa. 2005. Genetic variation of the Y chromosome in Chibcha-speaking Amerindians of Costa Rica and Panama. Human Biology 77: 71– 91. Russell, A.E., C.A. Cambardella, J.J. Ewel, and T.B. Parkin. 2004. Species, rotation, and life-form diversity effects on soil carbon in experimental tropical ecosystems. Ecological Applications 14: 47– 60. Russell, A.E., J.W. Raich, A.R. Bedoya, O. Valverde-Barrantes, and E.  González. 2010. Impacts of individual tree species on carbon dynamics in a moist tropical forest environment. Ecological Applications 20: 1087– 100. Russell, A.E., J.W. Raich, O.J. Valverde-Barrantes, and R.F. Fisher. 2007. Tree species effects on soil properties in experimental plantations in tropical moist forest. Soil Science Society of America Journal 71: 1389– 97. Sader, S.A., and A.T. Joyce. 1988. Deforestation rates and trends in Costa Rica— 1940 to 1983. Biotropica 20: 11– 19. Sader, S.A., T. Sever, D. Irwin, and S. Saatchi. 2004. Monitoring the Mesoamerican Biological Corridor: a NASA/CCAD cooperative research project. Final Report submitted to NASA-ESE (NAG5– 8712). Sader, S.A., R.T. Waide, W.T. Lawrence, and A.T. Joyce. 1989. Tropical forest biomass and successional age class relationships to a vegetation index derived from Landsat TM data. Remote Sensing of Environment 28: 143– 56. Sadofsky, S., K. Hoernle, S. Duggen, F. Hauff, R. Werner, and D. GarbeSchönberg. 2009. Geochemical variations in the Cocos Plate sub-

584 Chapter 16 ducting beneath Central America: implications for the composition of arc volcanism and the extent of the Galápagos Hotspot influence on the Cocos oceanic crust. International Journal of Earth Sciences (Geologische Rundschau) 98: 901– 13. Sak, P.B., D.M. Fisher, T.W. Gardner, J.S. Marshall, and P.C. Lafemina. 2009. Rough crust subduction, forearc kinematics, and Quaternary uplift rates, Costa Rican segment of the Middle American Trench. Geological Society of America Bulletin 121: 992– 1012. Sánchez-Azofeifa, G.A., G.C. Daily, A.S.P. Pfaff, and C. Busch. 2003. Integrity and isolation of Costa Rica’s national parks and biological reserves: examining the dynamics of land-cover change. Biological Conservation 109: 123– 35. Sánchez-Azofeifa, G.A., A. Pfaff, J.A. Robalino, and J.P. Boomhower. 2007. Costa Rica’s payment for environmental services program: intention, implementation, and impact. Conservation Biology 21: 1165– 73. Santoro, M., G. Hernández, M. Caballero, and F. García. 2006. Aerobic bacterial flora of nesting green turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. Journal of Zoo and Wildlife Medicine 37: 549– 52. Saugier, B., J. Roy, and H.A. Mooney. 2001. Estimations of global terrestrial productivity: converging toward a single number? In J. Roy, B. Saugier, and H.A. Mooney, eds., Terrestrial Global Productivity, 543– 57. San Diego, CA: Academic Press. Savage, J.M. 2002. The Amphibians and Reptiles of Costa Rica. Chicago: University of Chicago Press. Schelhas, J., and G.A. Sánchez-Azofeifa. 2006. Post-frontier forest change adjacent to Braulio Carrillo National Park, Costa Rica. Human Ecology 34: 407– 31. Schnitzer, S.A., and F. Bongers. 2002. The ecology of lianas and their role in forests. Trends in Ecology and Evolution 17: 223– 30. Schrago, C.G. 2007. On the time scale of New World primate diversification. American Journal of Physical Anthropology 132: 344– 54. Schwendenmann, L., E. Veldkamp, T. Brenes, J.J. O’Brien, and J. Mackensen. 2003. Spatial and temporal variation in soil CO2 efflux in an old-growth neotropical rain forest, La Selva, Costa Rica. Biogeochemistry 64: 111– 28. Scott, N.J. 1976. The abundance and diversity of the herpetofaunas of tropical forest litter. Biotropica 8: 41– 58. Seminoff, J.A., and K. Shanker. 2008. Marine turtles and IUCN Red Listing: a review of the process, the pitfalls, and novel assessment approaches. Journal of Experimental Marine Biology and Ecology 356: 52– 68. Seminoff, J.A., and B.P. Wallace. 2012. Sea turtles of the eastern Pacific: advances in research and conservation. Tucson: University of Arizona Press. Senna, M.C.A., M. Costa, and Y.E. Shimabukuro. 2005. Fraction of photosynthetically active radiation absorbed by Amazon tropical forest: a comparison of field measurements, modeling, and remote sensing. Journal of Geophysical Research 110: 1– 8. Sezen, U.U., R.L. Chazdon, and K.E. Holsinger. 2009. Proximity is not a proxy for parentage in an animal-dispersed Neotropical canopy palm. Proceedings of the Royal Society B 276: 2037– 44. Sherrard, R., C. Murray-Gulde, J.J. Rodgers, and Y. Shah. 2003. Comparative toxicity of chlorothalonil: Ceriodaphnia dubia and Pimephales promelas. Ecotoxicology and Environmental Safety 56: 327– 33. Sierra, R., and E. Russman. 2006. On the efficiency of environmental

service payments: a forest conservation assessment in the Osa Peninsula, Costa Rica. Ecological Economics 59: 131– 41. Sigel, B.J., D.W. Robinson, and T.W. Sherry. 2010. Comparing bird community responses to forest fragmentation in two lowland Central American reserves. Biological Conservation 143: 340– 50. Sigel, B.J., T.W. Sherry, and B.E. Young. 2006. Avian community response to lowland tropical rainforest isolation: 40 years of change at La Selva Biological Station, Costa Rica. Conservation Biology 20: 111– 21. Silva, E. 2003. Selling sustainable development and shortchanging social ecology in Costa Rican forest policy. Latin American Politics and Society 45: 93– 127. Sims, L., and A.J. Sinclair. 2008. Learning through participatory resource management programs: case studies from Costa Rica. Adult Education Quarterly 58: 151– 69. Slocum, M.G., and C.C. Horvitz. 2000. Seed arrival under different genera of trees in a neotropical pasture. Plant Ecology 149: 51– 62. Slud, P. 1960. The birds of finca “La Selva,” Costa Rica: a tropical wet forest locality. Bulletin of the American Museum of Natural History 121: 55– 148. Slud, P. 1976. Geographical and climatic relationships of avifaunas, with special reference to avian distribution in the Neotropics. Smithsonian Contributions to Zoology 212: 1– 149. Smethurst, D., and B. Nietschmann. 1999. The distribution of manatees (Trichechus manatus) in the coastal waterways of Tortuguero, Costa Rica. Biological Conservation 89: 267– 74. Smythe, N. 1986. Competition and resource partitioning in the guild of Neotropical terrestrial frugivorous mammals. Annual Review of Ecology and Systematics 17: 169– 88. Snarskis, M.J. 1976. Stratigraphic excavations in the eastern lowlands of Costa Rica. American Antiquity 41: 342– 53. Snider, A.G., S.K. Pattanayak, E.O. Sills, and J.L. Schuler. 2003. Policy innovations for private forest management and conservation in Costa Rica. Journal of Forestry (July/August): 17– 23. Soares, E.L., and M. Firpo de Souza Porto. 2009. Estimating the social cost of pesticide use: an assessment from acute poisoning in Brazil. Ecological Economics 68: 2721– 28. Soin, T., and G. Smagghe. 2007. Endocrine disruption in aquatic insects: a review. Ecotoxicology 16: 83– 93. Sol Castillo, R.F. 2000. Asentamientos prehispánicos en la reserva biológica La Selva, Sarapiquí, Costa Rica. Tésis de licenciado no. 339 en antropología, University of Costa Rica. Sollins, P., M.F. Sancho, C.R. Mata, and R.L. Sanford. 1994. Soils and soil process research. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 34– 53. Chicago: University of Chicago Press. Solow, A.R., K.A. Bjorndal, and A.B. Bolten. 2002. Annual variation in nesting numbers of marine turtles: the effect of sea surface temperature on re-migration intervals. Ecology Letters 5: 742– 46. Sperr, E.B., E.A. Fronhofer, and M. Tschapka. 2009. The Mexican mouse opossum (Marmosa mexicana) as a flower visitor at a neotropical palm. Mammalian Biology 74: 76– 80. Spotila, J.R. 2004. Sea Turtles: A Complete Guide to Their Biology, Behavior, and Conservation. Baltimore, MD: Johns Hopkins University Press. Stahl, P.W. 2004. Greater expectations. Nature 432: 561– 63. Staines, C.L. 1996. The genus Cephaloleia (Coleoptera: Chrysomelidae)

The Caribbean Lowland Evergreen Moist and Wet Forests 585 in Central America and the West Indies. Revista de Biología Tropical, Special Publication 3: 3– 87. Steph, S., R. Tiedemann, M. Prange, and J. Groeneveld. 2006. Changes in Caribbean surface hydrography during the Pliocene shoaling of the Central American Seaway. Paleoceanography 21: 1– 25. Stiles, F., and A. Skutch. 1989. A Guide to the Birds of Costa Rica. Ithaca, NY: Cornell University Press. Stiles, F.G. 1983. Birds: introduction. In D.H. Janzen, ed., Costa Rican Natural History, 502– 29. Chicago: University of Chicago Press. Strong, D.R. 1981. The possibility of insect communities without competition: Hispine beetles on Heliconia. In R.F. Denno, ed., Insect Life History Patterns: Habitat and Geographic Variation, 183– 94. New York: Springer. Strong, D.R. 1982a. Harmonious coexistence of hispine beetles on Heliconia in experimental and natural communities. Ecology 63: 1039– 49. Strong, D.R. 1982b. Potential interspecific competition and host specificity: hispine beetles on Heliconia. Ecological Entomology 7: 217– 20. Strong, D.R., and M.D. Wang. 1977. Evolution of insect life histories and host plant chemistry: hispine beetles on Heliconia. Evolution 31: 854– 62. Stuart, A.J., P.A. Kosintsev, T.F.G. Higham, and A.M. Lister. 2004. Pleistocene to Holocene extinction dynamics in giant deer and woolly mammoth. Nature 431: 684– 89. Sun, Y., S. Solomon, A. Dai, and R.W. Portmann. 2007. How often will it rain? Journal of Climate 20: 4801– 18. Surovell, T., N. Waguespack, P.J. Brantingham, and G.C. Frison. 2005. Global archaeological evidence for proboscidean overkill. Proceedings of the National Academy of Sciences 102: 6231– 36. Sylvester, O., and G. Avalos. 2009. Illegal palm heart (Geonoma edulis) harvest in Costa Rican national parks: patterns of consumption and extraction. Economic Botany 63: 179– 89. Tamm, E., T. Kivisild, M. Reidla, M. Metspalu, D.G. Smith, C.J. Mulligan, C.M. Bravi, O. Rickards, C. Martínez-Labarga, E.K. Khusnutdinova, S.A. Fedorova, M.V. Golubenko, V.A. Stepanov, M.A. Gubina, S.I. Zhadanov, L.P. Ossipova, L. Damba, M.I. Voevoda, J.E. Kipierri, R. Villems, and R.S. Malhi. 2007. Beringian standstill and spread of Native American founders. PLOS ONE 9: 1– 6. Terborgh, J., S. Robinson, T. Parker, C. Munn, and N. Pierpont. 1990. Structure and organization of an Amazonian forest bird community. Ecological Monographs 60: 213– 38. Timm, R.M. 1982. Ectophylla alba. Mammalian Species 166: 1– 4. Timm, R.M. 1984. Tent construction by Vampyressa in Costa Rica. Journal of Mammalogy 65: 166– 67. Timm, R.M. 1985. Artibeus phaeotis. Mammalian Species 235: 1– 6. Timm, R.M. 1987. Tent construction by bats of the genera Artibeus and Uroderma. In B.D. Patterson and R.M. Timm, eds., Studies in neotropical mammalogy: essays in honor of Philip Hershkovitz. Fieldiana: Zoology (New Series) 39: viii + 1– 506. Timm, R.M. 1994. The mammal fauna. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 229– 37 + 394– 98. Chicago: University of Chicago Press. Timm, R.M., and R.K. LaVal. 1998. A field key to the bats of Costa Rica. Occasional Publication Series, University of Kansas Center of Latin American Studies 22: 1– 30.

Timm, R.M., R.K. LaVal, and B. Rodríguez-Herrera. 1999. Clave de campo para los murciélagos de Costa Rica. Brenesia (Museo Nacional de Costa Rica) 52: 1– 32. Timm, R.M., D.E. Wilson, B.L. Clauson, R.K. LaVal, and C.S. Vaughan. 1989. Mammals of the La Selva– Braulio Carrillo Complex, Costa Rica. North American Fauna 75: 1– 162. Tiwari, M., K. Bjorndal, A.B. Bolten, and B.M. Bolker. 2005. Intraspecific application of the mid-domain effect model: spatial and temporal nest distributions of green turtles, Chelonia mydas, at Tortuguero, Costa Rica. Ecology Letters 8: 918– 24. Tiwari, M., K. Bjorndal, A. Bolten, and B. Bolker. 2006. Evaluation of density-dependent processes and green turtle Chelonia mydas hatchling production at Tortuguero, Costa Rica. Marine Ecology Progress Series 326: 283– 93. Tobler, M. 2007. Reversed sexual dimorphism and courtship by females in the topaz cichlid Archocentrus myrnae (Chichlidae, Teleostei) from Costa Rica. Southwestern Naturalist 52: 371– 77. Toledo, M., L. Poorter, M. Peña-Claros, A. Alarcón, J. Balcázar, J. Chuviña, C. Leaño, J.C. Licona, H.ter Steege, and F. Bongers. 2011. Patterns and determinants of floristic variation across lowland forests of Bolivia. Biotropica 43: 405– 13. Torroni, A., J.V. Neel, R. Barrantes, T.G. Schurr, and D.C. Wallace. 1994. Mitochondrial DNA “clock” for the Amerinds and its implications for timing their entry into North America. Proceedings of the National Academy of Sciences 91: 1158– 62. Tosi, J.A. 1969. Mapa ecológica de Costa Rica. San José, Costa Rica: Tropical Science Center. Troëng, S., and M. Chaloupka. 2007. Variation in adult annual survival probability and remigration intervals of sea turtles. Marine Biology 151: 1721– 30. Troëng, S., P.H. Dutton, and D. Evans. 2005. Migration of hawksbill turtles Eretmochelys imbricata from Tortuguero, Costa Rica. Ecography 28: 394– 402. Troëng, S., E. Harrison, D. Evans, A. de Haro, and E. Vargas. 2007. Leatherback turtle nesting trends and threats at Tortuguero, Costa Rica. Chelonian Conservation and Biology 6: 117– 22. Troëng, S., and E. Rankin. 2005. Long-term conservation efforts contribute to positive green turtle Chelonia mydas nesting trend at Tortuguero, Costa Rica. Biological Conservation 121: 111– 16. Tschapka, M. 2003. Pollination of the understorey palm Calyptrogyne ghiesbreghtiana by hovering and perching bats. Biological Journal of the Linnean Society 80: 281– 88. Tyree, M.T., B.M.J. Engelbrecht, G. Vargas, and T.A. Kursar. 2003. Desiccation tolerance of five tropical seedlings in Panama: relationship to a field assessment of drought performance. Plant Physiology 132: 1439– 47. USDA– NRCS, Soil Survey Staff. 1999. Soil Taxonomy. Washington, DC: US Government Printing Office. Van Avendonk, H.J.A., W.S. Holbrook, D. Lizarralde, and P. Denyer. 2011. Structure and serpentinization of the subducting Cocos plate offshore Nicaragua and Costa Rica. Geochemistry, Geophysics, Geosystems 12: 1– 23. Van der Wall, S.B., and W.S. Longland. 2004. Diplochory: are two seed dispersers better than one? Trends in Ecology and Evolution 19: 155– 61. Veldkamp, E., A. Becker, L. Schwendenmann, D.H. Clark, and H. SchulteBisping. 2003. Substantial labile carbon stocks and microbial activity

586 Chapter 16 in deeply weathered soils below a tropical wet forest. Global Change Biology 9: 1171– 84. Veldkamp, A., P.H. Verburg, K. Kok, G.H.J. de Koning, J. Priess, and A.R. Bergsma. 2001. The need for scale sensitive approaches in spatially explicit land use change modeling. Environmental Modeling and Assessment 6: 111– 21. Vila, R., C.D. Bell, R. Macniven, B. Goldman-Huertas, R.H. Ree, C.R. Marshall, Z. Bálint, K. Johnson, D. Benyamini, and N.E. Pierce. 2011. Phylogeny and palaeoecology of Polyommatus blue butterflies show Beringia was a climate-regulated gateway to the New World. Proceedings of the Royal Society B: Biological Sciences 278: 2737– 44. Vílchez, A., R.L. Chazdon, and A. Redondo. 2004. Fenología reproductiva de cinco especies forestales del bosque secundario tropical. Kurú: Revista Forestal (Costa Rica) 1: 1– 10. Vivanco, L.A. 2006. Green Encounters: Shaping and Contesting Environmental Relations in Costa Rica. Oxford: Berghahn Books. Voigt, C.C. 2004. The power requirements (Glossophaginae: Phyllostomidae) in nectar-feeding bats for clinging to flowers. Journal of Comparative Physiology B 174: 541– 48. Voigt, C.C. 2005. The evolution of wing sacs and perfume-blending in the emballonurid bats. In R. Mason, M. LeMaster, and D. MüllerSchwarze, eds., Chemical Signals in Vertebrates, vol. X, 93– 100. Springer Verlag. Voigt, C.C. 2013. Sexual selection in neotropical bats. In R.H. Macedo and G. Machado, eds., Sexual Selection– Perspectives and Models from the Neotropics, 409– 32. Amsterdam: Elsevier. Voigt, C.C., O. Behr, B. Caspers, O. von Helversen, M. Knörnschild, F. Mayer, and M. Nagy. 2008. Songs, scents, and senses: sexual selection in the greater sac-winged bat, Saccopteryx bilineata. Journal of Mammalogy 89: 1401– 10. Voigt, C.C., S.L. Voigt-Heucke, and K. Schneeberger. 2012. Isotopic data do not support food sharing within large networks of female vampire bats (Desmodus rotundus). Ethology 118: 260– 68. Walla, T.R., S. Engen, P.J. DeVries, and R. Lande. 2004. Modeling vertical beta-diversity in tropical butterfly communities. Oikos 107: 610– 18. Wallace, D.R. 1992. The Quetzal and the Macaw. San Francisco: Sierra Club Books. Wang, I.J., A.J. Crawford, and E. Bermingham. 2008. Phylogeography of the pygmy rain frog (Pristimantis ridens) across the lowland wet forests of isthmian Central America. Molecular Phylogenetics and Evolution 47: 992– 1004. Washington, R., C. Bouet, G. Cautenet, E. Mackenzie, I. Ashpole, S. Engelstaedter, G. Lizcano, G.M. Henderson, K. Schepanski, and I. Tegen. 2009. Dust as a tipping element: the Bodélé Depression, Chad. Proceedings of the National Academy of Sciences 106: 20564– 71. Webb, S.D. 1991. Ecogeography and the Great American Interchange. Paleobiology 17: 266– 80. Wegner, W., G. Wörner, R.S. Harmon, and B.R. Jicha. 2011. Magmatic history and evolution of the Central American Land Bridge in Panama since Cretaceous times. Geological Society of America Bulletin 123: 724. Weigt, L.A., A.J. Crawford, A.S. Rand, and M.J. Ryan. 2005. Biogeography of the túngara frog, Physalaemus pustulosus: a molecular perspective. Molecular Ecology 14: 3857– 76. Weir, D., and M. Schapiro. 1981. Circle of Poison. Oakland, CA: Institute for Food and Development Policy. Wendt, T. 1993. Composition, floristic affinities and origins of the Mex-

ican Atlantic slope rain forests. In T.P. Ramamoorthy, R. Bye, A. Lot, and J. Fa, eds., Biological Diversity of Mexico: Origins and Distribution, 595– 680. Oxford University Press. Werner, P. 1985. La reconstitution de la forêt tropicale humide au Costa Rica: analyse de croissance et dynamique de la végetation. Diss., University of Lausanne. Switzerland. Werner, R., K. Hoernle, P. van den Bogaard, C. Ranero, and R. von Huene. 1999. Drowned 14-m-y old Galápagos archipelago off the coast of Costa Rica: implications for tectonic and evolutionary models. Geology 27: 499– 502. Wesseling, C., A. Ahlbom, D. Antich, A.C. Rodríguez, and R. Castro. 1996. Cancer in banana plantation workers in Costa Rica. International Journal of Epidemiology 25: 1125– 31. Wesseling, C., D. Antich, C. Hogstedt, A.C. Rodríguez, and A. Ahlbom. 1999. Geographical differences of cancer incidence in Costa Rica in relation to environmental and occupational pesticide exposure. International Journal of Epidemiology 28: 365– 74. Wesseling, C., A. Aragon, L. Castillo, M. Corriols, F. Chaverri, E. de la Cruz, M. Keifer, P. Monge, T.J. Partanen, C. Ruepert, and V. van Wendel de Joode. 2001. Hazardous pesticides in Central America. International Journal of Occupational and Environmental Health 7: 287– 94. Wesseling, C., M. Corriols, and V. Bravo. 2005. Acute pesticide poisoning and pesticide registration in Central America. Toxicology and Applied Pharmacology 207: 697– 705. Wheelwright, N.T., and N.M. Nadkarni, eds. 2014. Monteverde: ecología y conservación de un bosque nuboso tropical. Bowdoin Scholars’ Bookshelf. Book 3. http://digitalcommons.bowdoin.edu /scholars-bookshelf/3 Whitfield, S.M., K.E. Bell, T. Philippi, M. Sasa, F. Bolaños, G. Chaves, J.M. Savage, and M.A. Donnelly. 2007. Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proceedings of the National Academy of Sciences 104: 8352– 56. Whitfield, S.M., K.R. Lips, and M.A. Donnelly. In press. Decline and conservation of amphibians in Central America. In H.H. Heatwole, C. Barrio-Amoros, and J.W. Wilkenson, eds., Status of Conservation and Declines of Amphibians: Western Hemisphere. Sydney: Surrey Beatty and Sonos, Pty. Ltd. Wilf, P., C.C. Labandeira, W.J. Kress, C.L. Staines, D.M. Windsor, A.L. Allen, and K.R. Johnson. 2000. Timing the radiations of leaf beetles: hispines on gingers from latest Cretaceous to recent. Science 289: 291– 94. Willis, K.J., L. Gillson, and T.M. Brncic. 2004. How “virgin” is virgin rainforest? Science 304: 402– 3. Wirth, R., W. Beyschlag, R.J. Ryel, and B. Holldöbler. 1997. Annual foraging of the leaf-cutting ant Atta colombica in a semideciduous rain forest in Panama. Journal of Tropical Ecology 13: 741– 57. Wood, T.E., D. Lawrence, and D.A. Clark. 2005. Variation in leaf litter nutrients of a Costa Rican rain forest is related to precipitation. Biogeochemistry 73: 417– 37. Wood, T.K. 1993. Diversity in the New World Membracidae. Annual Review of Entomology 38: 409– 35. Woodburne, M.O. 2010. The Great American Biotic Interchange: dispersals, tectonics, climate, sea level and holding pens. Journal of Mammalian Evolution 17: 245– 64. Woodburne, M., A.L. Cione, and E.P. Tonni. 2006. Central American provincialism and the Great American Biotic Interchange. In

The Caribbean Lowland Evergreen Moist and Wet Forests 587 O.  Carranza-Castañeda and E.H. Lindsay, eds., Advances in late Tertiary vertebrate paleontology in Mexico and the Great American Biotic Interchange. Publicación Especial del Instituto de Geología y Centro de Geociencias de la Universidad Nacional Autónoma de México, vol. 4, 73– 101. Wooton, J.T., and M.P. Oemke. 1992. Latitudinal differences in fish community trophic structure, and the role of fish herbivory in a Costa Rican stream. Environmental Biology of Fishes 35: 311– 19. World Resources Institute. 2007. http://www.wri.org. Wright, S.J., O. Calderón, A. Hernandéz, and S. Paton. 2004. Are lianas increasing in importance in tropical forests?: a 17-year record from Panama. Ecology 85: 31– 45. Wright, S.J., H. Zeballos, I. Domínguez, M.M. Gallardo, M.C. Moreno, and R. Ibañez. 2000. Poachers alter mammal abundance, seed dispersal, and seed predation in a neotropical forest. Conservation Biology 14: 227– 39. Wu, S.T., and A.T. Joyce. 1988. The application of an integrated knowledge-based Geographic Information System for the study of mountainous tropical forest. In Technical Papers of the 1988 ACSMASPRS Annual Convention 6: 12– 20. Yearout, R., X. Game, K. Krumpe, and C. Mckenzie. 2008. Impacts of DBCP on participants in the agricultural industry in a third world nation (an industrial health and safety case study of a village at risk). International Journal of Industrial Ergonomics 38: 127– 34. You, C.F., P.R. Castillo, J.M. Gieskes, L.H. Chan, and A.J. Spivack. 1996. Trace element behavior in hydrothermal experiments: implications for fluid processes at shallow depths in subduction zones. Earth and Planetary Science Letters 140: 41– 52.

Young, A.M. 1980. Environmental partitioning in lowland tropical rain forest cicadas. Journal of the New York Entomological Society 88: 86– 101. Young, A.M. 1984. On the evolution of cicada × host-tree associations in Central America. Acta Biotheoretica 33: 163– 98. Young, B.E., T.W. Sherry, B.J. Sigel, and S. Woltmann. 2008. Edge and isolation effects nesting success of Costa Rican forest birds. Biotropica 40: 615– 22. Zaldivar, M.E., O.J. Rocha, G. Aguilar, L. Castro, E. Castro, and R. Barrantes. 2004. Genetic variation of cassava (Manihot esculenta Crantz) cultivated by Chibchan Amerindians of Costa Rica. Economic Botany 58: 204– 13. Zaldivar, M.E., O.J. Rocha, E. Castro, and R. Barrantes. 2002. Species diversity of edible plants grown in homegardens of Chibchan Amerindians from Costa Rica. Human Ecology 30: 301– 16. Zamora, C.O., and F. Montagnini. 2007. Seed rain and seed dispersal agents in pure and mixed plantations of native trees and abandoned pastures at La Selva Biological Station, Costa Rica. Restoration Ecology 15: 453– 61. Zamudio, K.R., and H.W. Greene. 1997. Phylogeography of the bushmaster (Lachesis muta: Viperidae) implications for Neotropical biogeography, systematics, and conservation. Biological Journal of the Linnean Society 62: 421– 42. Zhang, J., B. Rivard, A. Sánchez-Azofeifa, and K. Castro-Esau. 2006. Intra- and inter-class spectral variability of tropical tree species at La Selva, Costa Rica: implications for species identification using HYDICE imagery. Remote Sensing of Environment 105: 129– 41.

Chapter 17 The Caribbean Coastal and Marine Ecosystems

Jorge Cortés1

Introduction Background

The Caribbean coast of Costa Rica is bounded on the north by the Río San Juan at the border with Nicaragua, and to the south by the Río Sixaola at the border with Panama (Fig. 17.1). The shoreline is about 212 km long, characterized by relatively straight, high-energy sandy beaches and coastal lagoons in the north; and rocky points with coral reefs and sandy beaches in the south (Cortés and Guzmán 1985a, Parkinson et al. 1998, Cortés and León 2002, Cortés 2007, Cortés and Wehrtmann 2009). The continental platform is relatively narrow, with a total area of 2,310 km2 (M.V. Castro Campos, pers. comm., 2007), and the Exclusive Economic Zone (EEZ) is 24,000 km2 (INCOPESCA 2006). The entire coast has been classified as very sensitive to extremely sensitive to oil pollution (Acuña et al. 1996– 1997, TNC 2008). The coastal and marine ecosystems of the Caribbean coast of Costa Rica consist of coastal lagoons, mangrove forests, beaches, rocky intertidal outcrops, seagrass beds, coral reefs, subtidal hard and soft bottoms, and open waters (Cortés and Wehrtmann 2009). In this chapter I present a historical overview of scientific research in the region, then a brief description of the ecosystems, and conclude with a discussion on threats and conservation initiatives that take place along the Caribbean coast of Costa Rica. Historical Overview

The first publication on coastal and marine organisms of the Caribbean coast of Costa Rica was written by William Randolph Taylor (1933) and dealt with algae, based on a 591

collection at Punta Piuta made by C.W. Dodge, B.W. Dodge, and W.S. Thomas on March 20, 1930. Apparently no further research was carried out in this part of the country until the late 1950s when Archie Carr arrived at Tortuguero and initiated his pioneering work on sea turtles (Carr 1967). Since then a huge number of papers have been published on the sea turtles of Tortuguero, starting with Carr in the early 1960s (e.g., Carr 1962) and followed by more recent papers— for example, Bjorndal et al. (1993), Tiwari et al. (2005), Troëng et al. (2005), Goshe et al. (2010), and Vander Zanden et al. (2013). In 2006, a dissertation on parasites of the green turtle was completed and published (Santoro et al. 2006a, b, 2007, Santoro and Mattiucci 2009). Goshe et al. (2010) estimated an age at maturation of female green turtles (Chelonia mydas) from Costa Rica, using mean size at nesting, as 42.5 years. Elmer Yale Dawson came to Costa Rica to attend the Second Annual Advanced Seminar in Tropical Biology at the Universidad de Costa Rica in 1962. He visited the Caribbean coast to collect algae and published a paper expanding the list of marine algae for Costa Rica to 196 species (Dawson 1962). In 1965, Roy T. Tsuda came in association with the Organization for Tropical Studies (OTS) and collected algae on the Caribbean and Pacific coasts of Costa Rica; he added two more species to Dawson’s list of the Caribbean algae of Costa Rica (Tsuda 1968). William C. Banta and Renate J.M. Carson described 13 species of Bryozoa collected by Banta in 1964 from two environments in Portete: a small coral reef and a reef flat dominated by turtle grass (Banta and Carson 1977). John M. Lawrence collected the 1 Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), and Escuela de Biología, Universidad de Costa Rica (UCR), San Pedro de Montes de Oca, 11501-2060 San José, Costa Rica

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Fig. 17.1 The Caribbean coast of Costa Rica and its Marine Protected Areas (MPAs). Map prepared by Marco V. Castro.

same year, also at Portete, the sea urchins Echinometra lucunter (Linnaeus, 1758), Tripneustes ventricosus (Lamarck, 1816), and Lytechinus variegatus (Lamarck, 1816), to determine lipid reserves in their guts (Lawrence 1967). Joseph Richard Houbrick reported on 229 species of mollusks that he collected in 1966 in Portete and Barra del Colorado. The collection consisted of 181 species of gastropods, 35 pelecypods, 3 scaphopods, 8 chitons, and 2 cephalopods. Fifty-

one species were new records for the western Caribbean (Houbrick 1968). In 1968, a plankton tow was taken offshore as part of a US Navy project, and Michel and Foyo (1976) found species of the following groups: Siphonopora, Heteropoda, Copepoda, Euphausicea, Chaetognatha, and Salpidae. In 1971, Deborah M. Dexter, sponsored by the Organization for Tropical Studies (OTS), collected samples from five sandy beaches between Limón and Cahuita with

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the aim to study the macro-infauna, and reported 52 species, mainly polychaetes and crustaceans (Dexter 1974); the polychaetes were described by Fauchald (1973). As part of the RV Pillsbury Cruise to Central America in 1971, bottom trawls and plankton tows were done at 11 sites along the coast and specimens of sponges, black corals, mollusks, crabs, crinoids, sea stars, holothurians, polychaetes, pennatulids, and nemerteans were collected (Voss 1971). Other than the cruise report by Gilbert L. Voss, only one publication has been found in which specimens collected during that expedition are mentioned: Williams’ (1993) paper on mud shrimps collected east of Limón. The RV Alpha Helix, Scripps Institution of Oceanography, during the Belém to Belize City Expedition, collected one kilometer south of the Port of Limón on July 9, 1977, and a paper was published on four species of pelagic copepods (Ferrari and Bowman 1980). The most important marine ecosystems of the Caribbean, in terms of area, species richness, and economic value, are the coral reefs. The first study was by Gerard M. (Jerry) Wellington while with the Peace Corps in 1970. He described the coral reef at Cahuita and its associated flora and fauna (Wellington 1974a); and he published on the algae of the area (Wellington 1973, 1974b). The next investigation was also carried out at Cahuita by Risk et al. (1980) in 1978, when Michael J. (Mike) Risk came to Costa Rica to teach the first course on coral reefs offered in the country. Both of these studies noted that excessive terrigenous sedimentation was negatively affecting the coral reef at Cahuita. This motivated research on the effect of sediments on corals, and a thesis was done (Cortés 1981), and papers published (Cortés and Risk 1984, 1985). Work on the impact of human activity on the Caribbean coral reefs has continued (Cortés 1994, Fonseca and Cortés 2002, Roder 2005, Roder et al. 2009). After the initial studies at Cahuita, other reef areas of the Caribbean of Costa Rica were described: all the reefs along the coast (Cortés and Guzmán 1985a), at the Refugio Nacional de Vida Silvestre Gandoca-Manzanillo (Cortés 1992a), and at Punta Cocles (Fernández and Alvarado 2004). The largest coral reef is at Parque Nacional Cahuita, followed by the reefs at the Refugio Nacional de Vida Silvestre Gandoca-Manzanillo (Fig. 17.1). In the late 1970s the first thesis on the Caribbean coast related to marine organisms was done by Claudia Charpentier. She studied the seasonal variation in the chemical composition of five species of algae from Cahuita (Charpentier 1980). The early 1980s are marked by several events that significantly transformed the reefs of the Caribbean. The first was the 1982– 83 El Niño Southern Oscillation (ENSO) event, during which the southern Caribbean experienced

doldrums conditions with clear skies resulting in abnormal warming of the waters that led to extensive coral bleaching and death (Cortés et al. 1984). The second event was the mass mortality of the black sea urchin, Diadema antillarum (Philippi, 1845), a very important herbivore (Murillo and Cortés 1984). Finally, around that time, the first observation of massive death of the sea fan, Gorgonia flabellum Linnaeus, 1758, was recorded by Guzmán and Cortés (1984). These disturbances combined with the extreme terrigenous sedimentation resulted in a significant coral reef decline (Cortés 1994). Another bleaching event impacted the reefs in 1995 (Jiménez 2001). The 1991 Limón Earthquake (7.5 Richter Scale), which uplifted the coast as much as 1.9 m in some areas, resulted in the death of intertidal and shallow subtidal organisms (Cortés et al. 1992, 1994). A significant impact was observed on the burrowing sea urchin, E. lucunter. Skeletons of hundreds of this urchin were cast on the rocky areas, and many were collected and measured to determine population structure (R. Soto et al., unpublished data). The 1980s were also marked by an interest in the marine biodiversity of the Caribbean coast, and since then several theses have been written and papers published. A series of papers on algae were published during that decade: Kemperman and Stegenga (1983, 1986), Soto (1983), Stegenga and Kemperman (1983), and Soto and Ballantine (1986); and more recently, a paper by Thomas and Freshwater (2001), an inventory of macroalgal epiphytes on the seagrass Thalassia testudinum in Parque Nacional Cahuita (Samper-Villareal et al. 2008), a species list by Bernecker (2009), and new reports by Bernecker and Wehrtmann (2009). Sponges from Cahuita and Isla Uvita were identified as part of a thesis (Loaiza-Coronado 1989) and later published (Loaiza-Coronado 1991), while Van der Hal (2006) identified and studied the distribution of sponges in seagrass beds. Cortés (1996) published a compilation of reported sponges from the Caribbean coast of Costa Rica, and an update (Cortés et al. 2009). Some groups of cnidarians have been studied and papers published since the 1980s include hydroids (Cortés 1992b, Cortés 1996– 1997, Kelmo and Vargas 2002, Cortés 2009a), octocorals (Guzmán and Cortés 1985, Guzmán and Jiménez 1989, Sánchez 2001, Breedy 2009), stony corals (Cortés and Guzmán 1985b, Cortés 1992c, 2009a), other cnidarians (Cortés 1996– 1997, 2009b), and sea anemones (Acuña et al. 2013). There has been an interest in mollusks for a long time, starting with the pioneering work by Houbrick (1968), followed by the collections done by David G. Robinson while working on his dissertation research: the systematics and

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paleoecology of Pleistocene gastropods (Robinson 1991). Robinson published with Michel Montoya a list of marine mollusks collected between 1982 and 1986, at ten localities of the Caribbean coast of Costa Rica: Barra del Colorado, Río Matina, Moín, Portete, Puerto Limón, Río Banano, Río Estrella, Cahuita, Puerto Viejo, and Manzanillo. Their inventory included 395 species: 288 gastropods, 100 bivalves, five polyplacophorans, and two cephalopods (Robinson and Montoya 1987). José Espinosa from Cuba and Jesús Ortea from Spain, in conjunction with the Instituto Nacional de Biodiversidad (INBio), did extensive collections between Cahuita and Gandoca from 1999 to 2001, and published many papers (e.g., Espinosa and Ortea 1999, 2000, 2001, Ortea et al. 1999, 2001, Ortea 2001, Espinosa et al. 2006). Finally, Rodríguez-Sevilla and coworkers (2003) published a compilation of all known mollusks of the Caribbean coast of Costa Rica. García-Ríos and Álvarez-Ruiz (2011) added five new records of chitons (Polyplacophora) to the list of 8 previously known species. Ornelas-Gatdula et al. (2012) studied the sea slug, Navanax aenigmaticus, and found that it consisted of three species, N. gemmatus being the species found on the Caribbean coast. Yolanda Camacho-García et al. (2014) reported on the diversity and distribution of sea slugs in this area. The crustaceans have also received some attention and lists of species have been published, and new species described. Dora P. Henry and Patsy A. McLaughlin reported four species of barnacles collected from boat hulls in Portete (Henry and McLaughlin 1975). The first thesis on crustaceans from the Caribbean was by Odalisca Breedy on benthic microcrustaceans (Breedy 1986); she later published on the isopods (Breedy and Murillo 1995). The other paper on isopods of the Caribbean was by Regina Wetzer and Niel L. Bruce, in which they described a new genus and species that inhabit the shallow waters of Parque Nacional Cahuita, with specimens collected by Richard C. Brusca and P.M. Delaney (Wetzer and Bruce 1999). Paul S. Young described a new species of coral-inhabiting barnacle found in Brazil and Cahuita (Young 1989). Several papers have been published on copepods, starting with the report of four species from the Caribbean of Costa Rica by Ferrari and Bowman (1980), and another on a calanoid species (Walter 1989). Wolfgang Mielke collected benthic copepods in Costa Rica between August and September 1990, and published a series of papers that report and describe new species and subspecies from the Caribbean (Mielke 1992, 1993, 1994). Álvaro Morales Ramírez in his compilation of copepods of Costa Rica included 13 species from the Caribbean (Morales-Ramírez 2001, Morales-Ramírez et al. 2014). Dennis A. Moran and Ana I. Dittel in their publication on anomuran and brachyuran crabs of Costa Rica

included the known Caribbean species (Moran and Dittel 1993). Austin B. Williams (1993) in his paper on mud shrimps from the western Atlantic included species from Costa Rica. Rita Vargas and Jorge Cortés published a series of compilations on several groups of crustaceans (Vargas and Cortés 1997, 1999, 2006), while Ingo S. Wehrtmann and Rita Vargas reported new records and range extensions of shrimps (Wehrtmann and Vargas 2003). Iorgu Petrescu and Richard W. Heard described a new species of cumacean collected in Parque Nacional Cahuita (Petrescu and Heard 2004). Eduardo Suárez-Morales et al. (2013) reported on a group of planktonic copepods from Cahuita. Other papers published on crustaceans include a study of the coral bioeroder shrimp Alphaeus simus Guérin-Meneville, 1856, at Cahuita (Cortés 1985). Ronald Umaña and Didiher Chacón studied post-larvae of the lobster Panulirus argus (Latreille, 1804) (Umaña and Chacón 1994). Wehrtmann and Albornoz (2002) found differences in the reproductive traits of two species of Alpheus, one from the Caribbean and another from the Pacific. Terossi et al. (2010a), studying populations of the shrimp Hippolyte obliquimanus in Brazil and Costa Rica, found that it has a high plasticity of reproductive features, not only as adults, but also in the larval development (Terossi et al. 2010b). Azofeifa-Solano et al. (2014) reported on the reproductive biology of an anemone shrimp. Three papers have been published on fisheries-related topics; the first was on crustaceans: an assessment of pink shrimp populations, Farfantepenaeus brasiliensis (Latreille, 1817) (reported as Penaeus brasiliensis) (Tabash-Blanco 1995). The second was on mollusks: a comparison of populations of the West Indian topshell, Cittarium pica, in exploited and protected sites (Schmidt et al. 2002), and the third, on post-larval settlement of the spiny lobster, Panulirus argus (Latreille, 1804) in Cahuita National Park (González and Wehrtmann 2011). There have been a few taxonomical studies of echinoderms. Juan José Alvarado and Jorge Cortés published a list of known echinoderms of Costa Rica including Caribbean species (Alvarado and Cortés 2004). Natalie Bolaños and coworkers, with the help of J.J. Alvarado, published on the diversity and abundance of echinoderms in the reef lagoon at Cahuita (Bolaños et al. 2005). Gordon Hendler described a species of ophiuroid that he collected, and dedicated it to the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) of the Universidad de Costa Rica (Hendler 2005). Another study on echinoderms was carried out by Marta F. Valdez and Carlos Villalobos, who determined the spatial distribution, correlation with the substrate, and aggregations of the black sea urchin D. antillarum at Cahuita (Valdez and Villalobos 1978). Papers were

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published on the mass mortality of D. antillarum in 1983 and 1992 (Murillo and Cortés 1984, Cortés 1994), and on its subsequent recovery (Alvarado et al. 2004, Fonseca et al. 2006, Myhre and Acevedo-Gutiérrez 2007). The diversity of echinoderms of the Caribbean coast must be higher than reported, when compared to the species lists of neighboring countries (Alvarado 2011). The first paper published on fishes of the Caribbean coast of Costa Rica was by Gilbert and Kelso (1971), covering the fishes of the Tortuguero area, mainly freshwater species. Another paper from that area was prepared by Winemiller and Leslie (1992), who studied the fish communities in the freshwater-marine ecotone at the river mouths and coastal lagoons. Phillips and Perez-Cruet (1984) compared reef fishes from Cahuita and the Pacific. Didiher Chacón of the non-govermental organization ANAI (National Association for Indigenous Matters) published on the tarpon (Chacón 1993, Chacón and McLarney 1992). This NGO has also published on the leatherback turtle population that nests in Gandoca (Chacón et al. 1996, Chacón 1999). Bussing and López (2009) in their chapter on marine fishes of Costa Rica included a list of species of the Caribbean coast. Salas et al. (2010) found that there is weak genetic connectivity between populations of a damselfish, Stegastes partitus, from Costa Rica-Panamá (CR-PAN) and the Mesoamerican Barrier Reef System. They also noticed strong self-recruitment in CR-PAN. Benavides-Morera and Brenes (2010) reported 13 species of fishes captured at Laguna Gandoca, with 77% of the catch consisting of one species, Centropomus pectinatus. They also found that salinity was important in the temporal and spatial distribution of the icthyofauna of the lagoon. An important contribution to knowledge of the biodiversity of the Caribbean coast of Central America is the Bussing and López (2010) compendium on the coastal and marine fishes of the Caribbean Coast of Lower Central America, which includes all the species known from the Caribbean coast of Costa Rica. Ignacio Jiménez did a thesis on the ecology and conservation of the West Indian manatee Trichechus manatus Linnaeus, 1778, in the northeast of Costa Rica ( Jiménez 1998). He later published two papers, one on the state of conservation, ecology, and popular knowledge of the manatee ( Jiménez 1999), and the other on a predictive model of the distribution of the manatee based on studies along the northern Caribbean coast of Costa Rica (Jiménez 2005). He found that manatees prefer lagoons to other watercourses and indicated the threat of forest clearing to manatee conservation. Previously, Reynolds et al. (1995) found that the population of the manatee has been declining and attributed this to illegal hunting, increases in motorboat traffic, high levels of pollutants, and the ingestion of plastic bags. Ig-

nacio Jiménez has established the Fundación Salvemos al Manatí de Costa Rica (Save the Costa Rican Manatee Foundation). Laura May-Collado and colleagues studied dolphin whistles along the southern Caribbean coast of Costa Rica. May-Collado and Wartzok (2008) determined that the common bottlenose dolphins (Tursiops truncatus) can change their whistle structure depending on local conditions. The Guyana dolphin’s (Sotalia guianensis) whistles have a higher frequency in Costa Rica than in well-studied populations in Brazil (May-Collado and Wartzok 2009). Finally, May-Collado (2010) found changes in the whistle structure of populations in Guyana and bottlenose dolphins when interacting along the Caribbean coast of Costa Rica. Other studies on marine biodiversity include one on sipunculids (Cutler et al. 1992), and a thesis on polychaetes of Parque Nacional Cahuita by Victoria Bogantes Aguilar, increasing the number of species to over 50 (BogantesAguilar 2014). The zooplankton of Parque Nacional Cahuita with emphasis on echinoderm larvae was studied by Álvaro Morales-Ramírez (1987) in his Master thesis and later published (Morales and Murillo 1996). Allan CarrilloBaltodano (2012) re-surveyed 25 years later, the same stations as Morales-Ramírez and found significant differences regarding some but not all groups. Dominici-Arosemena et al. (2000) published a paper on the ichthyoplankton of the Limón area. A compilation on marine biodiversity of the Caribbean coast of Costa Rica was published by Cortés and Wehrtmann (2005). The book “Marine Biodiversity of Costa Rica, Central America” includes numerous chapters with lists of species from the Caribbean (Wehrtmann and Cortés 2009). Other topics studied include primary productivity and biomass of phytoplankton in the coral reef at Parque Nacional Cahuita (Silva-Benavides 1986), mangrove ecology and pollution assessment (Coll et al. 2001, 2004), mangrove monitoring (Fonseca et al. 2007a, Cortés et al. 2010), seagrass bed ecology (Paynter et al. 2001, Krupp 2006, Nielsen-Muñoz 2007, Nielsen-Muñoz and Cortés 2008, Krupp et al. 2009), and seagrass bed monitoring (Fonseca et al. 2007b, Cortés et al. 2010, Van Tussenbroek et al. 2014). Schmidt et al. (2002) published on the population ecology and fishery of the gastropod Cittarium pica (Linnaeus, 1758). Jiménez and Cortés (1993) published on the compressive strength and density of the coral Siderastrea siderea (Ellis and Solander, 1786), while Muller-Parker and Cortés (2001) focused on the distribution of light and nutrients in Cahuita, and Acevedo-Gutiérrez et al. (2005) addressed the social interactions between bottlenose and tucuxis dolphins in the Gandoca-Manzanillo area. Most of the research on marine pollution has been car-

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ried out by CIMAR scientists and students. The first publications were on petroleum pollution as part of CARIPOL, a Caribbean-wide pollution project (Mata et al. 1987). Jenaro Acuña González published on the presence of oil in the Canales de Tortuguero (Acuña et al. 1986), and recently around Limón (Acuña-González et al. 2004); he also prepared a map on coastal sensitivity to oil spills (Acuña et al. 1996– 1997). Dagner Mora and his group from AyA (Instituto Costarricense de Acueductos y Alcantarillados, Costa Rica’s water utility company) published on the sanitary quality of the beach waters in Limón in the early 1980s and considered them “close to being unsafe for swimming” (Mora et al. 1987). García et al. (2006) found that total and fecal coliform densities are very high in Limón and Cahuita. Héctor M. Guzmán of the Smithsonian Tropical Research Institute (STRI) and coworkers determined that heavy metal pollution (Guzmán and Jiménez 1992) and mercury levels (Guzmán and García 2002) in coral reefs in Costa Rica were high. Other studies on metals in sediments were done by García-Céspedes et al. (2004) and Salazar et al. (2004). Heavy metals in animals were determined by Guzmán and Jiménez (1992) in corals, and by Rojas (1990) and Rojas et al. (1998) in a sea cucumber; in the first case the levels were high, in the second case, some metals were high while others low. As part of a pollution project at CIMAR, Alison L. Spongberg (2004) found that PCB contamination in surface sediments was intermediate in Limón compared to other sites in Costa Rica. García et al. (2006) found large amounts of solid wastes and the majority was plastics. Loría et al. (1998) found in corals higher levels of 40K on the Caribbean than on the Pacific coast, high levels of 226Ra on both coasts, and low levels of 134Cs. Finally, two theses have been written, one on metals in the water column at Parque Nacional Cahuita (Sandí 1990), and another one on the nutritional and skeletal characteristics of a reef-building coral as a response to land-based pollution (Roder 2005, Roder et al. 2009). No pollutants were detected in Laguna Gandoca where the largest mangrove forest of Costa Rica’s Caribbean region is located (Coll et al. 2004). The first paper on marine fossils from the Caribbean coast of Costa Rica was published by Thomas Wayland Vaughan (1919), and dealt with coral species from Limón. Afterwards many papers on paleontology were published (Collins and Coates 1999, Fischer and Aguilar 2007, Aguilar 2009 and reference therein). The geology of the coast has been studied extensively (see Geology and Geomorphology section below). Research on coastal geology has been carried out by scientists from the Escuela Centroamerica de Geología at the Universidad de Costa Rica (UCR), the Refinadora Costarricense de Petróleo (RECOPE), and the

Smithsonian Tropical Research Institute (STRI) through their Panama Paleontology Project. Omar G. Lizano of CIMAR has published on simulations and predictions of wave activity at the Caribbean coast of Costa Rica (Lizano and Moya 1990, Lizano 1996). Lizano and Fernández (1996) documented all the tropical storms and hurricanes that passed close to the Caribbean coast of the country, while Alfaro et al. (2010) analyzed the impact of those storms. Finally, O.G. Lizano also described the characteristics of the tides at both coasts of Costa Rica (Lizano 2006) and the wind and wave climatology prevailing at the Caribbean (Lizano 2007) (see below). Current State of Knowledge

More than 165 papers and at least 20 theses on marine sciences of the Caribbean coast of Costa Rica have been published until date. The majority of these publications have a biological focus, and within these, most deal with biodiversity of marine organisms, sea turtles, and coral reef ecology. There are now close to 20 papers on geology, 15 on chemistry (mainly concerned with pollution), about half a dozen on meteorology, and a few on physical oceanography. Beaches and rocky intertidal zones are among the least studied habitats at the Caribbean coast of Costa Rica. Only one paper has been published that identifies invertebrates of sandy beaches (Dexter 1974), and one that covers the endolithic fauna of hard intertidal substrates (Pepe 1985). There are only two mangrove forests at the Caribbean coast, with additional isolated mangrove trees found at several other places (Cortés 1991, Cortés et al. 2001). The mangrove forests are described below. Over 2,300 species have been reported from the country’s Caribbean region, but there are significant gaps in taxonomic knowledge— for example, there are no publications on bacteria or flatworms, and there are gaps in geographic coverage, such as the deep waters (Cortés and Wehrtmann 2005, Wehrtmann et al. 2009). The biodiversity of the Caribbean coast of Costa Rica is among the best known in the Caribbean (Miloslavich et al. 2010). Some ecosystems have been studied in detail— for example, coral reefs, and they are being monitored continuously (Fonseca et al. 2006, Cortés et al. 2010), as well as seagrass beds (Paynter et al. 2001, Krupp 2006, Fonseca et al. 2007a, Nielsen-Muñoz 2007, Krupp et al. 2009, Cortés et al. 2010, Van Tussenbroek et al. 2014). Other ecosystems are badly in need of study— for example, the coastal lagoons, beaches, and the rocky intertidal environment found here. Pollution levels are relatively low along the Caribbean coast of Costa Rica. Exceptions are found around the ports

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of Moín and Limón where the highest levels of pollutants in Costa Rica have been detected which should be closely monitored, although these pollutant levels are considered normal for non-industrial ports. There have been a few publications on geological phenomena but more work is needed regarding sediment origin, composition and movement, fossil coral reefs, and rates of coastal uplift. The physical oceanography of the Caribbean coastal zone has not received any attention from researchers yet, although its understanding is expected to help us get a better insight in sediment and pollutant transport taking place along the coastline.

The Physical Environment Climate

The climate of the Caribbean coast of Costa Rica is hot and humid, and it rains year-round (Herrera, chapter 2 of this volume). There is no discrete dry season since rainfall is nearly homogeneous between January and October, while during the rest of the year there is a marked increase in precipitation (Alfaro 2002, Taylor and Alfaro 2005). Precipitation on the Caribbean coast is lowest in March– April and maximum in November– December (Alfaro 2002). Along the coast the amount of rain decreases from the northwest (6,000 mm) to the southeast (2,500 mm) (Herrera 1985 and chapter 2 of this volume). The main hurricane tract is north of the Caribbean coast of Costa Rica (Alfaro 2007), though a few hurricanes have passed close to the coast while none have directly hit the coast in historical times (Alvarado and Alfaro 2003, Alfaro et al. 2010); only one tropical storm hit the Port of Limón directly, in December 1887 (Lizano and Fernández 1996). Geology and Geomorphology

The geology of the Caribbean coast of Costa Rica is represented in stratigraphy by the Limón Basin (Linkimer and Aguilar 2000, Brandes et al. 2007; Alvarado and Cárdenes, chapter 3 of this volume) and is part of the Chorotega backarc physiographic province (Marshall 2007). The northern section of the coast is composed of extensive low-relief alluvial plains, with high-energy barrier beaches, while the south has a narrow coastal plain with rocky promontories and intervening sandy beaches (Bergoeing 1998, Parkinson et al. 1998, Denyer and Cárdenas 2000, Cortés 2007; Alvarado and Cárdenes, chapter 3 of this volume). Rivers transport high sediment loads from the mountain ranges to the coastal plain and spread them on the coast (Bergoeing 1998, Cortés et al. 1998). At the northern section of

the coast, aided by the waves and currents, sediments form prograding beach ridges parallel to the shore, creating elongated coastal lagoons in a passive margin-like setting (Parkinson et al. 1998). The Tortuguero lowlands are intruded by Neogene-Quaternary backarc volcanoes (Bergoeing 1998, Marshall 2007). Brandes et al. (2007), using data from a grid of seismic lines off-shore parallel and perpendicular to the coast, indicated that the North Limón Basin has the characteristics of a passive continental margin, while on the South Limón Basin compressional tectonic forces predominate, as Parkinson et al. (1998) proposed. The southern section of the Caribbean coast is characterized by mountains close to the shore, rocky promontories made up of fossil coral reefs of Pleistocene or Holocene origin, or beachrock (Budd et al. 1999, McNeill et al. 2000, Cortés and Jiménez 2003), and crescent-shaped sandy beaches (Cortés and Guzmán 1985a, Cortés 2007, Marshall 2007). Some of the fossil reef tracts extend along the coast, while others are found inland (Aguilar and Denyer 1994, Denyer and Cortés in prep). This section of the coast has been uplifted several times. The uplift in the past 2 million years has been related to the rise of the Coco Volcanic Cordillera (Cocos Ridge) subducted with the Cocos Plate on the Pacific margin, under the Caribbean plate (Coates et al. 1992, Collins et al. 1995, McNeill et al. 2000). Denyer (1998) determined uplift rates of 1.8 mm/yr for the Manzanillo area between 27,000 and 5,000 years ago, and of 0.9 mm/yr in the past 5,000 years. Recently, uplift of the coast was witnessed during the 1991 Limón Earthquake (magnitude 7.5) when the entire intertidal zone was uplifted, in some areas up to 1.9 m (Denyer et al. 1994a, b, Denyer 1998). Evidence of previous uplift, similar to the 1991 event, is recorded in notches in the rocks of the Limón area (Denyer et al. 1994b, Denyer 1998, personal observation) (Fig. 17.2). The Limón Basin initiated in the Cretaceous with pelagic carbonates and volcanoclastic sediments (Changuinola Formation), and later was covered by volcanic sediments during the Paleocene-Eocene (Tuis Formation). During the Eocene-Oligocene, two types of rocks were deposited, mudstones (Sensori Formation) and shallow marine carbonates (Animas Formation and Punta Pelada Formation). This was followed by the Uscari Formation (Oligocene-Miocene) that consists of mud-rich shallow water deposits, and grades into the Río Banano Formation (Miocene-Pliocene) consisting of shallow-water deltaic and estuarine deposits. Coates et al. (1992) consider both Uscari and Río Banano as part of the Limón Group, criteria that McNeill et al. (2000) also followed, but Denyer (1998) indicated that more work was needed to map the contact of these two formations. The

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from the reef bottom (Cortés 1981). The tides on the Caribbean coast of Costa Rica are mixed or semidiurnal depending on the moon phase, and have a range of less than 40 cm. The tides are affected by wind direction and force, atmospheric pressure, currents, and waves (Lizano 2006). The main currents along the coast are from the northwest to the southeast, as part of the persistent cyclonic PanamaColombia Gyre, the coastal branch of which is sometimes referred to as the Panama-Colombia Countercurrent (Mooers and Maul 1998, Andrade et al. 2003, Centurioni and Niiler 2003). Strong eddies in the opposite direction— that is, SE to NW, along the coast— have been observed. These currents distribute sediments, nutrients, pollutants, and organisms along the coast. The transport of sediments and pollutants is impacting the coral reefs in a negative manner (Cortés and Risk 1985, Cortés et al. 1998).

Ecosystems Coastal Lagoons

Fig. 17.2 Notches indicating previous sea levels in Punta Portete. The lower one was the level before the Limón Earthquake of 1991. Photograph by Jorge Cortés.

following sequence is the Suretka Formation (PliocenePleistocene) and is made up of volcanic and plutonic blocks and coarse grains. The Late Pleistocene-Holocene deposits known as the Limón Formation are from reef origin, and form the present-day rocky points on the southern Caribbean coast of Costa Rica, where extant coral reefs grow (Taylor 1975, Coates et al. 1992, Fernández et al. 1994, Denyer 1998, Linkimer and Aguilar 2000, McNeill et al. 2000, Denyer et al. 2003, Brandes et al. 2007). For additional details on the geology of this region reference is made to Alvarado and Cárdenes (chapter 3 of this volume). Waves, Tides, and Circulation

Waves are normally from the northeast, but when there are storms or hurricanes in the Caribbean Sea waves may come from other directions as well (Lizano 2007). If they are strong enough, they can break corals and lift sediments

Characteristic of the northern section of the Caribbean coast of Costa Rica are the elongated coastal lagoons parallel to the coastline (Parkinson et al. 1998, Denyer and Cárdenas 2000) (Fig. 17.3). The coastal lagoons, including a few dredged sections, extend from Moín to Barra del Colorado, connecting all the northern section of the Caribbean coast. The flooded lands along the channels are covered by the tree Pterocarpus officinalis Jacq. and the palm Raphia taedigera Mart., 1828. Studies of the fauna and flora of the coastal lagoons have been scarce, although a few papers have been published on the lagoons’ fish (Gilbert and Kelso 1971, Winemiller and Leslie 1992), as well as on the manatees. Two studies have shown that manatee populations are declining mainly owing to human action (Reynolds et al. 1995, Jiménez 1999). Jiménez (2005) found that forest clearings are a threat to manatee conservation because they expose manatees more to human populations. A paper was published on hydrocarbon pollution levels that were higher near the refinery and low at the northern end of the Canales de Tortuguero (Acuña et al. 1986). On the basis of geomorphic, sedimentologic, and stratigraphic data obtained in the Barra de Colorado area, Parkinson et al. (1998) concluded that the north Caribbean region is a wave-dominated delta that has formed along a passive continental margin. This tectonic setting contrasts with the southern section of the Caribbean coast and the Pacific coast that are seismically active continental margins. Much more study is needed in these important coastal lagoons.

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Fig. 17.3 Canales de Tortuguero, a coastal lagoon parallel to the shoreline. Photograph by Jorge Cortés.

Mangrove Forests

The reduced tidal range and the geomorphology of the Caribbean coast of Costa Rica are not propitious for the development of mangrove forests (Coll et al. 2001, Cortés et al. 2001). Only two well-developed mangrove forests exist on the Caribbean coast, while there are isolated trees in several areas (Cortés 1991, Cortés et al. 2001, Sánchez-Vindas 2001, personal observation). One of the mangrove forests is found near the main port of the Caribbean, Moín, and it has been greatly impacted by construction and pollution (Cortés et al. 2001). This mangrove forest was studied in the mid-1970s and was found to be structurally more complex than Pacific stands with the tallest trees belonging to Pterocarpus officinalis, which in fact is not considered a nuclear species of the mangrove forest (Pool et al. 1977). The other mangrove forest of the Caribbean coast of Costa Rica is in much better condition. It is located at

Laguna Gandoca (Figs. 17.1, 17.4) within the Refugio Nacional de Vida Silvestre Gandoca-Manzanillo (Coll et al. 2001) where pollution has been very low (Coll et al. 2004). The mangrove forest in Laguna Gandoca is the largest on the Caribbean coast of Costa Rica (12.5 ha), and this area is three times the area it had in 1976 (Coll et al. 2001). The forest consisted of Rhizophora mangle Linnaeus, 1753, Avicennia germinans (Linnaeus) Stearn, 1958, Laguncularia racemosa (Linnaeus) C.F. Gaertn., 1805, and Conocarpus erectus Linnaeus, 1753. The mangrove forest at Gandoca has been monitored since 1999 following the Caribbean Coastal Marine Productivity or CARICOMP protocol (CARICOMP 1997). The peak in productivity and flowering was in July, the warmest month. Productivity apparently declined during the study period while the mean temperature went up. Biomass (14 kg/m2) and density (9 trees/10 m2) were low compared to other CARICOMP sites, but productivity in

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July (4 g/m2 /day) was similar to most CARICOMP sites (Fonseca et al. 2007a). Beaches

The entire northern section of the Caribbean coast comprises a series of high-energy sandy beaches (Fig. 17.5), which are very important for turtle nesting (Troëng and Rankin 2005), while in the southern section beaches are present between rocky points (Cortés and Guzmán 1985a, Cortés and Jiménez 2003). The color of the beaches ranges from white— consisting almost exclusively of carbonates— to pitch-black beaches made up of magnetite. The presence of pink and golden beach colors depends on the proportions of marine organism fragments, terrigeneous sediments, and weathering (Cortés et al. 1998). Dexter (1974) has published the only paper that addresses sandy-beach fauna. She identified and quantified

invertebrates from five sandy beaches along the southern section of the Caribbean coast (Playa Bonita, Airport Beach, Cahuita North, Cahuita South, Puerto Viejo). The most abundant species was the isopod Excirolana braziliensis Richardson, 1912 (reported as Cirolana salvadorensis) followed by the polychaete Scolelepis (Scolelepis) squamata (Müller, 1806) (reported as Scolelepis agilis) and the bivalve Donax denticulatus Linnaeus, 1758. Other groups found were nematodes, nemerteans, oligochaetes, cumaceans, amphipods, decapods, and gastropods. Four species of marine turtles nest on the beaches of the Caribbean coast: Chelonia mydas (Linné, 1758) (green turtle), Dermochelys coriacea (Vandelli, 1761) (leatherback), Eretmochelys imbricata (Linné, 1766) (hawksbill), and sporadically Caretta caretta (Linné, 1758) (loggerhead) (Savage 2002, Troëng 2005). Some beaches at the Caribbean coast of Costa Rica are considered turtle nesting sites of global importance— for example, Tortuguero for the green (Troëng

Fig. 17.4 Rhizophora mangle, the predominant mangrove tree in the Laguna Gandoca, Refugio Nacional de Vida Silvestre Gandoca-Manzanillo. Photograph by Jorge Cortés.

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Fig. 17.5 A beach within the Parque Nacional Tortuguero, an important nesting site for the green turtle, Chelonia mydas. Photograph by Peter O. Baumgartner.

and Rankin 2005), and Gandoca for the leatherback turtle (Chacón et al. 1996, Chacón 1999, Troëng et al. 2004). Rocky Intertidal Zone

Rocky points are present only in the southern section of the Caribbean coast of Costa Rica and are made up of carbonate rocks, fossil coral reefs, and beachrocks (Fig. 17.6). The assemblages of the rocky intertidal zones have not been studied extensively. There are some reports of mollusks collected here (Houbrick 1968, Robinson and Montoya 1987, Espinosa and Ortea 2001) and there is one paper on the endolithic fauna of carbonate substrates observed in Cahuita (Pepe 1985). Nothing has been published on the geographic distribution or vertical zonation of organisms that inhabit the rocky intertidal zone. Schmidt et al. (2002) studied the West Indian topshell, C. pica, at three locations along the Caribbean coast, two where these snails are collected artisanally for food, and one where it is protected. They found that the average population density at the unexploited site, being 14 ind/m2, was

three times higher than at sites where it was extracted. In the exploited sites the animals were smaller, but growth rates were not significantly different from the non-exploited site. They recommended that the minimum size for extraction should be 40 mm and that the fishery should be closed from July to November, which coincides with the reproductive season. The entire intertidal and shallow subtidal zones were seismically uplifted during the 1991 Limón Earthquake, in some areas as much as 1.9 m (Denyer et al. 1994a,b, Denyer 1998). The subaerial exposure of marine organisms resulted in their massive death (Cortés et al. 1992, 1994). This process of coastal uplift has been going on for a long time as evidenced by notches in the rocks of the Limón area and fossil coral reefs found inland (Denyer 1998, Cortés and Jiménez 2003) (Figs. 17.2, 17.6). Seagrass Beds

Four species of seagrasses have been reported from the Caribbean coast of Costa Rica (Cortés and Salas 2009):

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Thalassia testudinum Banks ex König, 1805 (turtle grass), Syringodium filiformis Kützing, 1860 (manatee grass), Halophila decipiens Ostenfeld, 1902, and Halodule wrightii Ascherson, 1868. The first two species form extensive beds mainly in the reef lagoons (Cortés and Guzmán 1985a, Cortés et al. 1992, Nielsen-Muñoz and Cortés 2008, Krupp et al. 2009). Seagrass beds are shallow, very productive environments (Fig. 17.7). In Cahuita the peak of production was in July (Fonseca et al. 2007b, Cortés et al. 2010), and higher at sites with intermediate environmental conditions and sediment grain size (Paynter et al. 2001). A seagrass bed in Parque Nacional Cahuita has been monitored using the above-mentioned CARICOMP protocol. Average productivity of T. testudinum was 2.7 ± 1.15 g/m2 /day, which is intermediate when compared to other CARICOMP sites. Total biomass of T. testudinum (822.8 ± 391.84 g/m2) was intermediate to high, and shoot density (1,188 ± 335.5 shoots/m2) was higher than other CARICOMP sites (Fonseca et al. 2007b). Flowering of T. testudinum was observed starting in April and continuing until June with a peak in May, while fruit production continued until August. The sex ratio was two males for every female flower in 2004, and four males/female in 2005 and 2006 (Nielsen-Muñoz 2007, Nielsen-Muñoz and Cortés 2008). When compared to other CARICOMP sites the productivity in Costa Rica results to be intermediate although it has been declining (Van Tussenbroek et al. 2014). Seagrass beds, almost exclusively made up of T. testudinum, in the Refugio Nacional de Vida Silvestre GandocaManzanillo covered an area of about 16 ha (Krupp 2006, Krupp et al. 2009). Environmental conditions and especially

depth controlled the average canopy cover and aboveground biomass of T. testudinum, as well as levels of shoot densities, productivity, and leaf sizes (Krupp et al. 2009). Coral Reefs

As indicated above, the southern section of the Caribbean coast of Costa Rica has carbonate promontories, mainly comprised of fossil coral reefs (Pleistocene, Holocene) (Fig. 17.8), and beachrock in some sections (Cahuita, Punta Uva). Present day coral reefs are growing over those rocky outcrops. The coral reefs are distributed in three discrete sections (Cortés and Guzmán 1985a, Cortés and Jiménez 2003) (Fig. 17.1): (1) fringing reefs between Moín and Limón, including Isla Uvita; (2) the largest fringing reef of the coast plus patch reefs and carbonate banks at Cahuita National Park (Fig. 17.9); and (3) fringing and patch reefs, carbonate banks, and an algal ridge between Puerto Viejo and Punta Mona. The two most important economic activities along the southern Caribbean coast of Costa Rica, tourism and fisheries, both depend on these coral reefs. Natural and anthropogenic disturbances have negatively impacted the coral reefs at the Caribbean coast. The main recent threats to the reefs are coral bleaching (Cortés et al. 1984, Jiménez 2001), the massive death of the black sea urchin, D. antillarum (Murillo and Cortés 1984, Alvarado et al. 2004), and the 1991 Limón Earthquake, which uplifted the coast significantly (Cortés et al. 1992), all of which have taken their toll on the reefs. But the most important impacts along the Caribbean coral reefs today are related to human activities: increased terrigenous sediment loads Fig. 17.6 Rocky intertidal zone (fossil reefs) at Isla Uvita. Note the erosional notches that mark the sea level before the 1991 Limón earthquake. Photograph by Jorge Cortés.

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Fig. 17.7 Seagrass beds in the reef lagoon at Parque Nacional Cahuita. Monospecific bed of Thalassia testudinum on the left, and Syringodium filiformis on the right. Photo credits— Left, Ingo S. Wehrtmann; right: Vanessa Nielsen.

Fig. 17.8 Fossil corals at Isla Uvita: Diploria strigosa on the left and piles of Acropora palmata on the right. Photographs by Jorge Cortés.

resulting from deforestation and bad agricultural practices (Cortés and Risk 1985, Cortés 1994), overexploitation of resources ( J. Cortés, personal observation), tourism, and damage by anchoring (unpublished data) (Fig. 17.10). One coral reef in Parque Nacional Cahuita has been monitored using the CARICOMP protocol continously since 1999. Live coral cover increased from 15 to 17% while coralline algal cover decreased from 17 to 5%. Unfortunately, macroalgal cover has increased from 63 to 74% (Fonseca et al. 2006). Other coral reefs along the coast have

also shown signs of recovery (unpublished data) but live coral coverage is still far below what it was or should be for a similar region with lower levels of anthropogenic impact. Isla Uvita

Isla Uvita is the only relatively large island on the Caribbean coast of Costa Rica (Figs. 17.1, 17.11). It is historically important since it was Christopher Columbus’ only landing site in Costa Rica when he visited the coast during his

604 Chapter 17 Fig. 17.9 The largest coral reef on the Caribbean coast of Costa Rica at Parque Nacional Cahuita. Photograph by Jorge Campos.

fourth voyage in 1502. The island is just off the port of Limón. Nevertheless, the strong northwest-southeast current between the island and the port has kept the island relatively free from pollutants (Cortés and Guzmán 1985a). The island is made up of fossil coral reefs (Figs. 17.6, 17.8), and is surrounded by living reefs and seagrass beds. It was briefly described by Cortés and Guzmán (1985a), while its sponges were described by Loaiza-Coronado (1991). Isla Uvita is a natural laboratory; more scientific work is needed to fully understand its ecosystem dynamics. This island represents today’s main conservation gap along the country’s Caribbean coast (Alvarado et al. 2011), as it is threatened by high tourism pressures (BarrantesRojas 2010). Pérez-Reyes (2003) developed an environmental interpretation of the trails of the island and BarrantesRojas (2010) an interpretation program for its marine environment, including a proposal for zonation. PereiraChaves and Sierra-Sierra (2009) proposed a strategy for managing the existing marine resources found at Isla Uvita. Open Waters

Very little is known about the off-shore areas along the Caribbean coast of Costa Rica. The bottom close to shore is either a carbonate-dominated, hard bottom, or sand, and farther off-shore the bottom consists of mud (J. Cortés, personal observation). A few bottom samples as well as plankton samples have been collected off the Caribbean coast in the past (Voss 1971), but there appears to be only one publication on mud shrimps (Williams 1993). One zooplankton tow sample was collected in 1968 by Michel and Foyo (1976), who reported the presence of siphonophorans, heteropods, copepods, euphausids, chaetognaths, and salps. Moreover, Ferrari and Bowman (1980) reported the four species of pelagic copepods collected south of Limón in 1977.

People and Nature Human Population and Demography

The entire Caribbean coast is located within the Province of Limón. Based on the 2000 Census (which is the latest one available) (http://www.inec.go.cr/) the population size of Limón was 339,295 people, or 8.9% of Costa Rica’s national population. Its fecundity rate, 2.4, is one of the highest in the country, while some coastal districts— for example, Colorado— have even higher rates, up to 2.9. Population density is 18.5 per km2, with an urban population of 37.1%. The sex ratio at birth is estimated at 107 boys to 100 girls, and 4.0% of the population is over 65 years old. The indigenous and the Afro-Costa Rican populations are the largest in the country. Average schooling time is 6.1 yr, and the percentage of students attending schools regularly is 60.1%, which are among the lowest in the country. The percentage of illiteracy, 7.7%, is above the national average (4.8%). Unemployment is among the highest in the country: 6.8%. Some of the above-mentioned parameters point to a province with serious social and economic issues that may result in environmental degradation and need to be addressed urgently. Threats Natural and Anthropogenic Impacts

The threats to the marine environments of the Caribbean coast of Costa Rica can be divided into natural and anthropogenic. In most cases the anthropogenic impacts are chronic in nature. During the 1980s three natural events affected organisms and ecosystems of the Caribbean coast (Fig. 17.12). The first was the El Niño– Southern Oscillation (ENSO) warming event of 1982– 1983 (Cortés et al. 1984, and see an earlier section in this chapter). During this event

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corals and other reef organisms died. At around the same time, an infectious disease caused the massive death of the black sea urchin, Diadema antillarum, throughout the Caribbean Sea (Lessios et al. 1984). In fact, D. antillarum is a very important herbivore on coral reefs. Its death on the Caribbean coast, and especially in Cahuita where densities were high (Valdez and Villalobos 1978, Murillo and Cortés 1984), significantly impacted the reefs as herbivory pressure was reduced. The populations of D. antillarum are now recovering slowly (Cortés 1994, Alvarado et al. 2004, Fonseca et al. 2006, Myhre and Acevedo-Gutiérrez 2007). The first report of the massive death of seafans in the genus Gorgonia was provided by Guzmán and Cortés (1984),

many years before it was actually observed in other parts of the Caribbean (Smith et al. 1996, Nagelkerken et al. 1997). ENSO-related warming events again impacted the coral reefs in 1995 (Jiménez, 2001). The magnitude 7.5 Limón Earthquake that happened in 1991 and uplifted the coast had a truly significant impact on the coastal and marine ecosystem as it subaerially exposed marine organisms and lifted others to very shallow waters. This led to mass mortality of intertidal and shallow subtidal organisms, including reef organisms and seagrass beds. Landslides produced by the earthquake generated enormous amounts of sediments that exacerbated the existing sedimentation problem (Cortés et al. 1992, 1994).

Fig. 17.10 Main anthropogenic impacts on the coral reefs of the Caribbean coast of Costa Rica. (A) Sediments killing coral, Siderastrea siderea, at Cahuita National Park. The live coral is on the left side of the photographs, the black section is dead coral tissue, exposed after removing the sediments. (B) Anchor damage on coral; white horizontal stripes across the coral, exposing the skeleton. (C) Tourist walking in the shallow lagoon breaking coralline algae, corals, and snails. Photographs by Jorge Cortés.

606 Chapter 17 Fig. 17.11 Isla Uvita, a natural laboratory just off the Port of Limón. Photograph by Jorge Cortés.

Even today, more than 22 years after the earthquake, there are sections of the mountains that have not recovered completely, and consequently generate sediments during strong storms that are deposited downslope affecting the coast (E. Junier, pers. comm., 2007). Human activity inland, including pollution and sedimentation, does have a significant impact on the coastal area. Acuña et al. (1986) found high levels of pollutants where the Río Parismina— which receives water from towns located inland— meets the Canales de Tortuguero. Other sources of pollution are close to the shoreline, at the ports and refinery (Mata et al. 1987, Acuña-González et al. 2004). High levels of terrigenous sedimentation from deforested mountains inland are found along the Caribbean coast of Costa Rica and are negatively impacting coral reefs (Cortés and Risk 1985, Fonseca and Cortés 2002, Cortés and Jiménez 2003, Mora-Cordero 2005). The impact of those sediments on the reefs is the main anthropogenic disturbance to the coast. In recent years coastal alteration (urban growth, development of tourist facilities) and possibly overexploitation of marine resources have impacted coastal and marine ecosystems along the Caribbean coast, although there are no studies on this issue available yet. Schmidt et al. (2002) have published the only paper that exists on overexploitation of a marine organism at the Caribbean coast. However, the author of this chapter has observed a significant decline in lobster populations and those of commercially important fish. Declines in fish populations have been reported Caribbean-wide by Paddock et al. (2009). Central America,

including the Caribbean coast of Costa Rica, turns out to be the Caribbean subregion that has the highest levels of decline (about 6% per year between 1996 and 2007). Climate Change

The impact of climate change on Costa Rica’s coastal areas has not yet been studied. However, several changes in coastal climates are expected. First, sea level rise will occur and result in greater levels of coastal erosion, which actually is already taking place along the Caribbean coast (Cortés and León 2002). This will result in the generation of more sediment. Also, there will be intrusions of saline water towards the inland. Furthermore, seawater is expected to get warmer while acidity (pH) levels are expected to go down (Kleypas et al. 2006, IPCC 2007). Both processes will have a severe impact on Costa Rica’s Caribbean coral reefs over the coming period. Conservation Marine Protected Areas

There are three Marine Protected Areas (MPAs) at the Caribbean coast that include both terrestrial and marine areas [note: only the size of the marine portion is indicated in parentheses here] (Fig. 17.1): Parque Nacional Tortuguero (52,681 ha), Parque Nacional Cahuita (23,290 ha), and Refugio Nacional de Vida Silvestre Gandoca-Manzanillo (4,983 ha) (Mora et al. 2006). The first protected area is intended to safeguard turtle nesting beaches and fishing

Fig. 17.12 Main natural impacts on the coral reefs of the Caribbean coast of Costa Rica. Top left: Bleached elkhorn coral, Acropora palmata, in 1983; the coral has lost its symbiotic algae (Zooxanthellae) and the white skeleton is visible. Top right: Dead black sea urchin, Diadema antillarum, in Cahuita National Park in 1983. Bottom: Uplifted coral, Siderastrea siderea, five days after the 1991 Limón Earthquake. Photographs by Jorge Cortés.

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grounds (see McClearn et al., chapter 16 in this volume), while the latter two areas are intended to protect coral reefs and seagrass beds. The Refugio Nacional de Vida Silvestre Gandoca-Manzanillo also includes the mangrove forest located at Laguna Gandoca as well as an important leatherback nesting site. Furthermore, there is Reserva Pacuare, a private protected area at the coast where sea turtle nesting beaches are guarded (Dick 2004). The status of Isla Uvita as a Protected Area has been debated for years, but so far no agreement has been reached, even though it is a very valuable place in both biological as well as recreational terms. In close cooperation with Conservation International (CI) and specialists from other conservation and research institutions, The Nature Conservancy (TNC 2008, Alvarado et al. 2011) led a process to evaluate the status of biodiversity and threats that affect the Costa Rican and Panamanian portions of the Southwestern Caribbean ecoregion. One of the key results of this assessment concerned the identification of coastal and marine priority sites of important conservation value. According to Alvarado et al. (2011), the only Costa Rican priority area without a legally recognized conservation status is Isla Uvita. Fortunately, all other TNC-identified sites have already been protected within the framework of Costa Rica’s national system of protected areas, which is administered by the governmental agency SINAC (Sistema Nacional de Áreas de Conservación), under supervision of the Ministry of Environment and Energy (MINAE). Furthermore, the TNC-led study helps to guide conservation strategies and action, in order to abate current and future threats that affect coastal and marine biodiversity along Costa Rica’s Caribbean shoreline. CITES and IUCN Red Lists

Costa Rica is a signatory of CITES, enforced by MINAE. The IUCN Red Lists include all scleractinian corals, all the black corals, all marine turtles, and several species of fish found at the Caribbean coast (www.iucnredlist.org). Conservation Organizations

Two government institutions, MINAE and the Costa Rican Fisheries Institute (INCOPESCA), are involved with marine conservation issues at the Caribbean coast. The first one administers the protected areas and the second one oversees fishing activity. At least seven non-governmental organizations (NGOs) are involved in marine conservation as of 2007. Four of them, the Caribbean Conservation Corporation (CCC), the Tropical Science Center (TSC), Reserva Pacuare, and the National Association for Indigenous Matters (ANAI), are involved with marine turtles, while Fundación KETO and Fundación Delfín Talamanca focus

on the tucuxis dolphins that live along the southern portion of the coast, while Fundación Salvemos al Manatí de Costa Rica helps to conserve the manatees in the area. As mentioned above, TNC was working closely with others to set conservation priorities, develop strategies for action, and evaluate conservation progress in the coastal-marine zone of Costa Rica’s Caribbean region (e.g., TNC 2008). Conservation Strategies and Action Threat Abatement and Restoration

Anthropogenic impacts must be reduced or eliminated to minimize the impact of natural disturbances. The best measure is to efficiently protect the marine and coastal ecosystems. This is being accomplished, with different degrees of success, by MINAE, private reserves, and NGOs. Pressures such as fishing have not been controlled effectively and far from ideal is the lack of control on deforestation happening in the highlands upstream. A water treatment plant has been operating in Limón, possibly reducing the amount of sewage water going into the waters near-shore. Unfortunately, to date there haven’t been any projects focusing on the ecological restoration of coastal and marine ecosystems found along the Caribbean coast. Economic Valuation of Environmental Goods and Services Only Blair et al. (1996) have done an evaluation of the economic benefits that the Cahuita coral reef provides to the local economy. They found that the primary reason why tourists visit the area is the Cahuita National Park, and within the park, the presence of a coral reef. The park’s visitation is generating over a million dollars in revenue per year, serving the community. These authors point out that the degradation of the environment— for example, expressed in the presence of garbage and sewage pollution— makes tourists hesitate to recommend the area to others who might also be interested in visiting Cahuita and its surroundings. Involvement of Local People The experience of co-management of a section of Cahuita National Park by government authorities and the local community as well as the functioning of a regional Council for Refugio Nacional de Vida Silvestre Gandoca-Manzanillo are just two good examples of decentralization and local participation (Valverde 2000, Weitzner 2000). In Cahuita a co-management committee, installed informally in 1997 and then officially in 1998, consists of two representatives of MINAE and three local representatives (two from the local Development Association and one from the Tourist Board). The committee has experienced ups and downs, but

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it has maintained several strengths: the potential for managing conflicts, economic independence, and involvement of community leaders (Weitzner 2000). This type of management scheme has been effective in involving the local community more strongly and raising awareness around the importance of the coral reef and its value to the community in Cahuita (Valverde 2000). Another example concerns the Refugio Nacional de Vida Silvestre Gandoca-Manzanillo, which is co-administrated by MINAE, local organizations, and NGOs. One positive outcome of this co-management scheme has been that the local population now feels that it has a responsibility for protecting and maintaining the refuge. Area management is now better and more efficient than before (Valverde 2000). It is obvious that the local communities are benefiting economically from tourist visitation to these protected areas and that they should contribute significantly to ensure its sustainable use and conservation. Other Strategies The presence of a Private Reserve and the local involvement of several NGOs in the region is fundamental for the protection and conservation of the coastal and marine environments along the Caribbean coast of Costa Rica. International programs have also been important for the study and conservation of the marine habitats of the Caribbean. For example, a Marine Pollution Monitoring Program in the Caribbean (CARIPOL) has been operational since the 1980s, while the previously discussed CARICOMP serves as a Caribbean-wide monitoring network that has been operating since the early 1990s. To date CARICOMP has generated very important information necessary for managing coastal and marine ecosystems in a sound manner. Future Perspectives Scenarios for the Twenty-First Century: Towards Sustainability?

There are signs of recovery or stability over time of some marine organisms and ecosystems from the Caribbean coast of Costa Rica. The coral reefs that have been studied in some detail are recovering in several areas— for example, Cahuita (Fonseca et al. 2006, Cortés et al. 2010)— and relatively stable in other areas (Cortés et al. 2010). The populations of a keystone species like D. antillarum are recovering after their massive mortality (Alvarado et al. 2004, Myhre and Acevedo-Gutiérrez 2007), resulting in an increase in coral cover and a reduction of algal cover. Green turtle populations are also recovering in Tortuguero where effective protection has been put in place (Tröeng and Rankin 2005),

but other species are still declining— for example, the leatherback turtle (Tröeng et al. 2004). One of the two mangrove forests is now suffering destruction, while the other is increasing its extent (Coll et al. 2001). It seems that populations and ecosystems can recover from the negative impact imposed on them if the pressures are reduced or eliminated. However, we have no control over the impact of natural disturbances that affect the region’s coastal and marine biodiversity. Currently, the main threats are anthropogenic in origin and can be prevented or controlled by us. Therefore, the coastal and marine ecosystems of Costa Rica’s Caribbean shores will survive during the twenty-first century only if we succeed in significantly reducing or eliminating the various human-induced threats that negatively affect these vital ecosystems. Importance of Ecosystem Health for Human Survival

There is a clear dependence of a significant number of people along the Caribbean coast on the health of the coastal and marine ecosystems of this region. Directly, commercial and subsistence fishers, as well as tour operators, depend on these ecosystems. Indirectly, many people depend on them, mainly via tourism, and yet more indirectly by the environmental services that these ecosystems provide to society, such as coastal protection, carbon uptake, water purification, and oxygen production. Research Needs

Some ecosystems, such as coral reefs, and groups of organisms, such as mollusks, have been studied in detail. In fact, several coral reefs, the mangrove forest in Laguna Gandoca, and the seagrass beds in Cahuita are currently being monitored (Fonseca et al. 2006, 2007a,b, Cortés et al. 2010). Also, organisms such as sea turtles are monitored at several beaches (Chacón 1999, Troëng and Rankin 2005). On the other hand, some ecosystems, such as deep waters or the coastal area north of Puerto Limón, have not yet been studied. Groups of organisms such as flatworms, tunicates, and others have not been studied along the Caribbean coast until date. Studies are needed on the external, land-based threats and their impacts on the coastal and marine ecosystems of Costa Rica’s Caribbean shores. Better trained scientists, as well as increased and continuously flowing financial resources, are needed to maintain and expand the studies on the marine and coastal ecosystems of the country’s Caribbean coast. Furthermore, fisheries are particularly in need of scientific research to inform sustainable use and sound management of marine resources. On a final note, it is important to recognize that scientific marine research results in a general need to be published and disseminated, in par-

610 Chapter 17

ticular to inform decision-making on policies for resource use and management. Other Needs

The afore-mentioned presence of private reserves and the engagement of NGOs have proven to be important factors that contribute to successful protection, conservation, and sustainable use of the coastal and marine systems and their organisms. A more extensive protected area coverage and stronger stakeholder involvement should be encouraged, though, especially in relation to fisheries. There is also a need for all kinds of educational materials concerning marine ecosystems found at the Caribbean coast. And there should be much more active participation of local communities in fund-raising, managing, and protecting the coastal and marine ecosystems in the area. Also, there is a strong need for field stations that could facilitate the study of Caribbean marine environments in Costa Rica in situ. Isla Uvita and Cahuita seem to be ideal sites for the establishment of such research stations. And finally, better international cooperation is needed in order to advance research on topics for which there is no in-country expertise or equipment available.

Conclusions The Costa Rican Caribbean coastal and marine ecosystems are species rich (Cortés and Wehrtmann 2005, Wehrtmann

et al. 2009), economically important for local communities, and key to sustainable development in the region. However, they are being threatened by natural and anthropogenic factors. Hence, human disturbances must be eliminated or at least minimized, to ensure a healthy future for all coastal and marine ecosystems that thrive along Costa Rica’s Caribbean shores.

Acknowledgments I thank Maarten Kappelle and the late Luis Diego Gómez for the invitation to contribute to this book. Economic support to write this chapter was provided by the Universidad de Costa Rica (UCR) through the Escuela de Biología. Fieldwork was supported by the Vicerrectoría de Investigación and the Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), both at UCR. Juan José Alvarado, Laura May-Collado, and Sebastian Tröeng provided valuable information. Eric Alfaro, Omar Lizano, Percy Denyer, and Teresita Aguilar helped with literature searches and commented on different sections of this chapter. Xochilt Lezama Cáceres helped with the maps. My thanks to Richard Petersen, Harlan Dean, Earl Junier Wade, and José A. Vargas for doing a critical review of the chapter. I appreciate the support over many years of teachers, students, colleagues, assistants, protected areas personnel, and local inhabitants who have helped me get to know the Caribbean region of Costa Rica.

References Acevedo-Gutiérrez, A., A. DiBerardinis, S. Larkin, L. Larkin, and P. Forestell. 2005. Social interactions between tucuxis and bottlenose dolphins in Gandoca-Manzanillo, Costa Rica. Latin American Journal of Aquatic Mammals 4: 49– 54. Acuña, F.H., A. Garese, A.C. Excoffon, and J. Cortés. 2013. New records of sea anemones (Anthozoa: Actiniaria) from Costa Rica. Revista de Biología Marina y Oceanografía 48: 177– 84. Acuña, J., M.M. Murillo, and F. Araya. 1986. Estudio preliminar sobre la presencia de hidrocarburos de petróleo en la zona fluvial Río MoínCanales Tortuguero. Ingeniería y Ciencia Química 10: 59– 60. Acuña, J.A., J. Cortés, and M.M. Murillo. 1996– 1997. Mapa de sensibilidad ambiental para derrames de petróleo en las costas de Costa Rica. Revista de Biología Tropical 44(3)/45(1): 463– 70. Acuña-González, J.A., J.A. Vargas-Zamora, E. Gómez-Ramírez, and J. García-Céspedes. 2004. Hidrocarburos de petróleo, disueltos y dispersos, en cuatro ambientes costeros de Costa Rica. Revista de Biología Tropical 52(Suppl. 2): 43– 50. Aguilar, T. 2009. Marine fossils. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America, 81– 94. Berlin: Springer + Business Media BV.

Aguilar, T., and P. Denyer. 1994. Bioestratigrafía del parche arrecifal de la Quebrada Brazo Seco, Plio-Pleistoceno, Limón, Costa Rica. Revista Geológica de América Central 17: 55– 66. Alfaro, E.J. 2002. Some characteristics of the annual precipitation cycle in Central America and their relationships with its surrounding tropical oceans. Tópicos Meteorológicos y Oceanográficos 9: 88– 103. Alfaro, E.J. 2007. Escenarios climáticos para temporadas con alto y bajo número de huracanes en el Atlántico. Revista de Climatología 7: 1– 13. Alfaro, E.J., A. Quesada, and F. Solano. 2010. Análisis del impacto en Costa Rica de los ciclones tropicales ocurridos en el Mar Caribe desde 1968 al 2007. Diálogos: Revista Electrónica de Historia 11: 22– 38. Alvarado, J.J. 2011. Echinoderm diversity in the Caribbean Sea. Marine Biodiversity 41: 261– 85. Alvarado, J.J., and J. Cortés. 2004. The state of knowledge on echinoderms of Costa Rica and Central America. In T. Heinzeller and J.H. Nebelsick, eds., Echinoderms: Munchen, 149– 55. Leiden: A.A. Balkema Publ. Alvarado, J.J., J. Cortés, and E. Salas. 2004. Status of the sea urchin

The Caribbean Coastal and Marine Ecosystems 611 Diadema antillarum Philippi (Echinodermata: Echinoidea) at Cahuita National Park (1977– 2003), Costa Rica. Caribbean Journal of Science 40: 257– 59. Alvarado, J.J., B. Herrera, L. Corrales, J. Asch, and P. Paaby. 2011. Identificación de las prioridades de conservación de la biodiversidad marina y costera en Costa Rica. Revista de Biología Tropical 59: 829– 42. Alvarado, L., and E.J. Alfaro. 2003. Frecuencia de los ciclones tropicales que afectaron a Costa Rica durante el siglo XX. Tópicos Meteorológicos y Oceanográficos 10: 1– 11. Andrade, C.A., E.D. Barton, and C.N.K. Mooers. 2003. Evidence for an eastward flow along the Central and South American Caribbean Coast. Journal of Geophysical Research 108: 3185– 96. Azofeifa-Solano, J.C., M. Elizondo-Coto, and I.S. Wehrtmann. 2014. Reproductive biology of the sea anemone shrimp Periclimenes rathbunae (Caridea, Palaemonidae, Pontoniinae), from the Caribbean coast of Costa Rica. ZooKeys 457: 211– 25. Banta, W.C., and R.J.M. Carson. 1977. Bryozoa from Costa Rica. Pacific Science 31: 381– 424. Barrantes-Rojas, N. 2010. Programa interpretativo del ecosistema marino de la Isla Quiribrí (Uvita), Limón. Licentiate thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Benavides-Morera, R., and C.L. Brenes. 2010. Análisis hidrográfico e ictiológico de las capturas realizadas con una red de trampa fija en la laguna de Gandoca, Limón, Costa Rica. Revista de Ciencias Marinas y Costeras 2: 9– 26. Bergoeing, J.P. 1998. Geomorfología de Costa Rica. San José, Costa Rica: Instituto Geográfico Nacional. Bernecker, A. 2009. Marine benthic algae. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media BV. Text: pp. 109– 117, Species List: CD pp. 17– 70. Bernecker, A., and I.S. Wehrtmann. 2009. New records of benthic marine algae and Cyanobacteria for Costa Rica, and a comparison with other Central American countries. Helgoland Marine Research 63: 219– 29. Bjorndal, K.A., A.B. Bolten, and C.J. Laguex. 1993. Decline of the nesting population of hawkbill turtles at Tortuguero, Costa Rica. Conservation Biology 7: 925– 27. Blair, N., C. Geraghty, G. Gund, and B. Jones. 1996. An economic evaluation of Cahuita National Park: establishing the economic value of an environmental asset. Unpublished report. Boston: Kellogg Graduate School of Management. Bogantes-Aguilar, V. 2014. Poliquetos (Annelida: Polychaeta) del Parque Nacional Cahuita, Limón, Costa Rica. Licentiate thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Bolaños, N., A. Bourg, J. Gómez, and J.J. Alvarado. 2005. Diversidad y abundancia de equinodermos en la laguna arrecifal del Parque Nacional Cahuita, Caribe de Costa Rica. Revista de Biología Tropical 53(suppl. 3): 285– 90. Brandes, C., A. Astorga, S. Bak, R. Littke, and J. Winsemann. 2007. Fault controls on sediment distribution patterns, Limón Basin, Costa Rica. Journal of Petroleum Geology 30: 25– 40. Breedy, O. 1986. Contribución al estudio de los microcrustáceos bentónicos (Isopoda y Tanaidacea) en el arrecife coralino del Parque Nacional Cahuita, Limón, Costa Rica. Licentiate thesis, Universidad de Costa Rica. San Pedro, Costa Rica.

Breedy, O. 2009. Octocorals. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media BV. Text: pp. 161– 67, Species List: CD pp. 108– 11. Breedy, O., and M.M. Murillo. 1995. Isópodos (Crustacea: Peracarida) de un arrecife del Caribe de Costa Rica. Revista de Biología Tropical 43: 219– 29. Budd, A.F., K.G. Johnson, T.A. Stemann, and B.H. Tompkins. 1999. Pliocene to Pleistocene reef coral assemblages in the Limon Group of Costa Rica. Bulletins of American Paleontology 357: 119– 58. Bussing, W.A., and M. López. 2009. Marine fish. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media BV. Text: pp. 453– 58, Species List: CD pp. 412– 73. Bussing, W.A., and M.I. López. 2010. Peces costeros del Caribe de Centroamérica Meridional/Marine Fishes of the Caribbean Coast of Lower Central America. Revista de Biología Tropical 58(Suppl. 2): 1– 234. Camacho-García, Y.E., M. Pola, L. Carmona, V. Padula, G. Villani, and J.L. Cervera. 2014. Diversity and distribution of the heterobranch sea slug fauna on the Caribbean of Costa Rica. Cahiers de Biologie Marine 55: 109– 27. CARICOMP. 1997. Structure and productivity of mangrove forests in the Greater Caribbean Region. Proceedings of the 8th International Coral Reef Symposium, Panamá 1: 669– 72. Carr, A.F. 1962. Orientation problems in the high seas travel and terrestrial movement of marine turtles. American Scientist 50: 359– 74. Carr, A.F. 1967. So Excellent a Fishe: A Natural History of Sea Turtles. Graden City, NY: Natural History Press. Carrillo-Baltodano, A.M. 2012. Diversidad, abundancia, composición y biomasa del zooplancton de la zona arrecifal del Parque Nacional Cahuita, Limón ¿Cuál es la disponibilidad de larvas de invertebrados bentónicos 25 años después? Licentiate thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Centurioni, L.R., and P.P. Niiler. 2003. On the surface currents of the Caribbean Sea. Geophysical Research Letters 30: 1279– 82. Chacón, D. 1993. Aspectos biométricos de una población de sábalo Megalops atlanticus (Pisces, Megalopidae). Revista de Biología Tropical 41(Suppl. 1): 13– 18. Chacón, D. 1999. Anidación de la tortuga Dermochelys coriacea (Testudines: Dermochelyidae) en Playa Gandoca, Costa Rica (1990 a 1997). Revista de Biología Tropical 47: 225– 36. Chacón, D., and W.O. McLarney. 1992. Desarrollo temprano del sábalo Megalops atlanticus (Pisces, Megalopidae). Revista de Biología Tropical 40: 171– 77. Chacón, D., W. McLarney, C. Ampie, and B. Venegas. 1996. Reproduction and conservation of the leatherback turtle Dermochelys coriacea (Testudines: Dermochelyidae) in Gandoca, Costa Rica. Revista de Biología Tropical 44: 853– 60. Charpentier, C. 1980. Variaciones estacionales en la composición química de cinco algas de la costa Caribe de Costa Rica y su posible utilización. Licentiate Thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Coates, A.G., J.B.C. Jackson, L.S. Collins, T.M. Cronin, H.J. Dowsett, L.M. Bybell, P. Jung, and J.A. Obando. 1992. Closure of the Isthmus of Panama: the near-shore marine records of Costa Rica and western Panama. Geological Society of America Bulletin 104: 14– 28. Coll, M., J. Cortés, and D. Sauma. 2004. Características físico-químicas

612 Chapter 17 y determinación de plaguicidas en el agua de la laguna de Gandoca, Limón, Costa Rica. Revista de Biología Tropical 52(Suppl. 2): 33– 42. Coll, M., A.C. Fonseca, and J. Cortés. 2001. Caracterización del manglar de Laguna Gandoca, Refugio Nacional de Vida Silvestre GandocaManzanillo, Limón, Costa Rica. Revista de Biología Tropical 49(Suppl. 2): 321– 29. Collins, L.S., and A.G. Coates, eds. 1999. A Paleobiotic Survey of Caribbean Faunas from the Neogene of the Isthmus of Panama. Bulletins of American Paleontology 357: 1– 351. Collins, L.S., A.G. Coates, J.B.C. Jackson, and J.A. Obando. 1995. Timing and rates of emergence of the Limón and Bocas del Toro basins: Caribbean effects of Cocos Ridge subduction? In P. Mann, ed., Geologic and Tectonic Development of the Caribbean Plate Boundary in Southern Central America. Geological Society of America Special Papers 295: 291– 307. Cortés, J. 1981. The Coral Reef at Cahuita, Costa Rica, A Reef Under Stress. M.Sc. thesis, McMaster University. Hamilton, Ontario, Canada. Cortés, J. 1985. Preliminary observations of Alphaeus simus GuérinMeneville, 1856 (Crustacea: Alphaeidae) a little known Caribbean bioeroder. Proceedings of the 5th International Coral Reef Congress, Tahiti 5: 351– 53. Cortés, J. 1991. Ambientes y organismos marinos del Refugio Nacional de Vida Silvestre Gandoca-Manzanillo, Limón, Costa Rica. Geoistmo 5: 61– 68. Cortés, J. 1992a. Los arrecifes coralinos del Refugio Nacional de Vida Silvestre Gandoca-Manzanillo, Limón, Costa Rica. Revista de Biología Tropical 40: 325– 33. Cortés, J. 1992b. Organismos de los arrecifes coralinos de Costa Rica: V. Descripción y distribución geográfica de hydrocorales (Cnidaria; Hydrozoa: Milleporina and Stylasterina) de la costa Caribe. Brenesia 38: 45– 50. Cortés, J. 1992c. Nuevos registros de corales (Anthozoa: Scleractinia) para el Caribe de Costa Rica: Rhizosmilia maculata y Meandrina meandrites. Revista de Biología Tropical 40: 243– 44. Cortés, J. 1994. A reef under siltation stress: a decade of degradation. In R.N. Ginsburg, compiler, Proceedings of the Colloquium on Global Aspects of Coral Reefs: Health, Hazards and History, 1993, 240– 46. Miami, FL: RSMAS, University of Miami. Cortés, J. 1996. Biodiversidad marina de Costa Rica: Filo Porifera. Revista de Biología Tropical 44: 911– 14. Cortés, J. 1996– 1997. Biodiversidad marina de Costa Rica: Filo Cnidaria. Revista de Biología Tropical 44(3)/45(1): 323– 34. Cortés, J. 2007. Coastal morphology and coral reefs. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, vol. 1, 185– 200. London: Taylor and Francis. Cortés, J. 2009a. Stony corals. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media BV. Text: pp. 169– 73, Species List: CD pp. 112– 18. Cortés, J. 2009b. Zoanthids, sea anemones, and corallimorpharians. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media BV. Text: pp. 157– 59, Species List: CD pp. 105– 7. Cortés, J., A.C. Fonseca, M. Barrantes, and P. Denyer. 1998. Type, distribution and origin of sediments of the Gandoca-Manzanillo National Wildlife Refuge, Limón, Costa Rica. Revista de Biología Tropical 46(Suppl. 6): 251– 56.

Cortés, J., A.C. Fonseca, and M. Coll. 2001. Descripción del manglar del Refugio de Vida Silvestre Gandoca-Manzanillo, Limón, Costa Rica. In F. Pizarro, C. Gómez-Fuentes, and R. Córdoba- Muñoz, eds., Humedales de Centroamérica, 90– 91. San José, Costa Rica: ORMA-UICN. Cortés, J., A.C. Fonseca, J. Nivia, V. Nielsen-Muñoz, J. Samper-Villareal, E. Salas, S. Martínez, and P. Zamora-Trejos. 2010. Monitoring coral reefs, seagrasses and mangroves in Costa Rica (CARICOMP). Revista de Biología Tropical 58(Suppl. 3): 1– 22. Cortés, J., and H.M. Guzmán. 1985a. Arrecifes coralinos de la costa Atlántica de Costa Rica. Brenesia 23: 275– 92. Cortés, J., and H.M. Guzmán. 1985b. Organismos de los arrecifes coralinos de Costa Rica. III: Descripción y distribución geográfica de corales escleractinios (Cnidaria: Anthozoa: Scleractinia) de la costa Caribe. Brenesia 24: 63– 124. Cortés, J., and C.E. Jiménez. 2003. Corals and coral reefs of the Caribbean of Costa Rica: past, present and future. In J. Cortés, ed., Latin American Coral Reefs, 223– 39. Amsterdam: Elsevier Science. Cortés, J., and A. León. 2002. The Coral Reefs of Costa Rica’s Caribbean Coast. Santo Domingo, Heredia, Costa Rica: Editorial INBio. Cortés, J., M.M. Murillo, H.M. Guzmán, and J. Acuña. 1984. Pérdida de zooxantelas y muerte de corales y otros organismos arrecifales en el Caribe y Pacífico de Costa Rica. Revista de Biología Tropical 32: 227– 32. Cortés, J., and M.J. Risk. 1984. El arrecife coralino del Parque Nacional Cahuita, Costa Rica. Revista de Biología Tropical 32: 109– 21. Cortés, J., and M.J. Risk. 1985. A reef under siltation stress: Cahuita, Costa Rica. Bulletin of Marine Science 36: 339– 56. Cortés, J., and E. Salas. 2009. Seagrasses. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media BV. Text: pp. 119– 22, Species List: CD pp. 71– 72. Cortés, J., R. Soto, and C. Jiménez. 1994. Efectos ecológicos del Terremoto de Limón. Revista Geológica de América Central, Volumen Especial: Terremoto de Limón: 187– 92. Cortés, J., R. Soto, C. Jiménez, and A. Astorga. 1992. Death of intertidal and coral reef organisms as a result of a 7.5 earthquake. Proceedings of the 7th International Coral Reef Symposium, Guam 1: 235– 40. Cortés, J., N. Van der Hal, and R.W.M. Van Soest. 2009. Sponges. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media BV. Text: pp. 137– 42, Species List: CD pp. 83– 93. Cortés, J., and I.S. Wehrtmann. 2005. Costa Rica. In P. Miloslavich and E. Klein, eds., Caribbean Marine Biodiversity: The Known and the Unknown, 169– 79. Lancaster, PA: DEStech Publications. Cortés, J., and I.S. Wehrtmann. 2009. Diversity of marine habitats of the Caribbean and Pacific of Costa Rica. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America, 1– 45. Berlin: Springer + Business Media BV. Cutler, N., E. Cutler, and J.A. Vargas. 1992. Peanut worms (Phylum Sipuncula) from Costa Rica. Revista de Biología Tropical 40: 153– 58. Dawson, E.Y. 1962. Additions to the marine flora of Costa Rica and Nicaragua. Pacific Naturalist 3: 375– 95. Denyer, P. 1998. Historic-prehistoric earthquakes, seismic hazards, and Tertiary and Quaternary geology of the Gandoca-Manzanillo National Wildlife Refuge, Limón, Costa Rica. Revista de Biología Tropical 46(Suppl. 6): 237– 50.

The Caribbean Coastal and Marine Ecosystems 613 Denyer, P., O. Arias, and S. Personius. 1994a. Efectos tectónicos del terremoto de Limón. Revista Geológica de América Central, Volumen Especial: Terremoto de Limón: 39– 52. Denyer, P., and G. Cárdenas. 2000. Costas marinas. In P. Denyer and S. Kussmaul, eds., Geología de Costa Rica, 185– 218. Cartago: Editorial Tecnológica de Costa Rica. Denyer, P., W. Montero, and G.E. Alvarado. 2003. Atlas tectónico de Costa Rica. San Pedro, Costa Rica: Editorial Universidad de Costa Rica. Denyer, P., S. Personius, and O. Arias. 1994b. Generalidades sobre los efectos geológicos del terremoto de Limón. Revista Geológica de América Central, Volumen Especial: Terremoto de Limón: 29– 38. Dexter, D.M. 1974. Sandy-beach fauna of the Pacific and Atlantic coasts of Costa Rica and Colombia. Revista de Biología Tropical 22: 51– 66. Dick, B.M. 2004. Prioridades de conservación en la gestión integrada de los recursos naturales en la zona costera de la Reserva Pacuare, Limón, Costa Rica. M.Sc. thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Dominici-Arosemena, A., E. Brugnoli-Olivera, S. Solano-Ulate, H. MolinaUreña, and A.R. Ramírez-Coghi. 2000. Ictioplancton en la zona portuaria de Limón, Costa Rica. Revista de Biología Tropical 48: 439– 42. Espinosa, J., and J. Ortea. 1999. Descripción de nuevas Marginelas (Mollusca: Neogastropoda: Marginellidae) de Cuba y del Caribe de Costa Rica y Panamá. Avicennia 10/11: 165– 76. Espinosa, J., and J. Ortea. 2000. Descripción de un género y once especies nuevas de Cystiscidae y Marginellidae (Mollusca: Neogastropoda) del Caribe de Costa Rica. Avicennia 12/13: 95– 114. Espinosa, J., and J. Ortea. 2001. Moluscos del mar Caribe de Costa Rica: desde Cahuita hasta Gandoca. Avicennia (Suppl. 4): 1– 76. Espinosa, J., J. Ortea, and J. Magaña. 2006. Nuevas especies de la Familia Eulimidae Philippi, 1853 (Mollusca: Prosobranchia) con caracteres singulares, recolectadas en Costa Rica, Cuba y Bahamas. Revista de la Academia Canaria de Ciencias XVII: 137– 41. Fauchald, K. 1973. Polychaetes from Central American sandy beaches. Bulletin of the Southern California Academy of Sciences 72: 19– 31. Fernández, C., and J.J. Alvarado. 2004. El arrecife coralino de Punta Cocles, costa Caribe de Costa Rica. Revista de Biología Tropical 52(Suppl. 2): 121– 29. Fernández, J.A., G. Bottazi, G. Barboza, and A. Astorga. 1994. Tectónica y estratigrafía de la Cuenca de Limón Sur. Revista Geológica de América Central, Volumen Especial: Terremoto de Limón: 15– 28. Ferrari, F.D., and T.E. Bowman. 1980. Pelagic copepods of the Family Oithonidae (Cyclopoida) from the east coast of Central and South America. Smithsonian Contributions to Zoology 312: 1– 27. Fischer, R., and T. Aguilar. 2007. Invertebrate paleontology. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources and Hazards, vol. 1, 453– 66. London: Taylor and Francis. Fonseca, A.C., and J. Cortés. 2002. Land use in the La Estrella River basin and soil erosion effects on the Cahuita reef system, Costa Rica. In B. Kjerfve, W.J. Wiebe, H.H. Kremer, W. Salomons, and J.I. Marshall, eds., Caribbean Basins: LOICZ Global Change Assessment and Synthesis of River Catchment/Island-Coastal Sea Interaction and Human Dimension. LOICZ Reports & Studies 27: 68– 82 + 114– 18. Texel, Netherlands: LOICZ. Fonseca, A.C., J. Cortés, and P. Zamora. 2007a. Monitoreo del manglar de Gandoca, Costa Rica (Sitio CARICOMP). Revista de Biología Tropical 55: 23– 31.

Fonseca, A.C., V. Nielsen, and J. Cortés. 2007b. Monitoreo de pastos marinos en Perezoso, sitio CARICOMP en Cahuita, Costa Rica. Revista de Biología Tropical 55: 55– 66. Fonseca, A.C., E. Salas, and J. Cortés. 2006. Monitoreo del arrecife coralino Meager Shoal, Parque Nacional Cahuita (sitio CARICOMP). Revista de Biología Tropical 54: 755– 63. García, V., J.A. Acuña-González, J.A. Vargas-Zamora, and J. GarcíaCéspedes. 2006. Calidad bacteriológica y desechos sólidos en cinco ambientes costeros de Costa Rica. Revista de Biología Tropical 54(Suppl. 1): 35– 48. García-Céspedes, J., J.A. Acuña-González, and J.A. Vargas-Zamora. 2004. Metales traza en sedimentos de cuatro ambientes costeros de Costa Rica. Revista de Biología Tropical 52(Suppl. 2): 51– 60. García-Ríos, C.I., and M. Álvarez-Ruiz. 2011. Diversidad y microestructura de quitones (Mollusca: Polyplacophora) del Caribe de Costa Rica. Revista de Biología Tropical 59: 129– 36. Gilbert, C.R., and D.P. Kelso. 1971. Fishes of the Tortuguero area, Caribbean Costa Rica. Bulletin of the Florida State Museum, Biological Sciences 16: 1– 54. González, O., and I.S. Wehrtmann. 2011. Postlarval settlement of spiny lobster, Panulirus argus (Latreille, 1804) (Decapoda: Palinuridae), at the Caribbean coast of Costa Rica. Latin American Journal of Aquatic Research 39: 575– 83. Goshe, L.R., L. Avens, F.S. Scharf, and A.L. Southwood. 2010. Estimation of age at maturation and growth of Atlantic green turtles (Chelonia mydas) using skeletochronology. Marine Biology 157: 1725– 40. Guzmán, H.M., and J. Cortés. 1984. Mortandad de Gorgonia flabellum en la costa Caribe de Costa Rica. Revista de Biología Tropical 32: 305– 8. Guzmán, H.M., and J. Cortés. 1985. Organismos de los arrecifes coralinos de Costa Rica. IV. Descripción y distribución geográfica de octocoralarios de la costa Caribe. Brenesia 24: 125– 74. Guzmán, H.M., and E.M. García. 2002. Mercury levels in coral reefs along the Caribbean coast of Central America. Marine Pollution Bulletin 44: 1415– 20. Guzmán, H.M., and C.E. Jiménez. 1989. Pterogorgia anceps (Pallas) (Octocorallia: Gorgoniidae): nuevo informe para la costa caribeña de Costa Rica. Revista de Biología Tropical 37: 231– 32. Guzmán, H.M., and C.E. Jiménez. 1992. Contamination of coral reefs by heavy metals along the Caribbean coast of Central America (Costa Rica and Panama). Marine Pollution Bulletin 24: 554– 61. Hendler, G. 2005. Two new brittle star species of the genus Ophiothrix (Echinodermata: Ophiuroidea: Ophiotrichidae) from coral reefs in the southern Caribbean Sea, with notes on their biology. Caribbean Journal of Science 41: 583– 99. Henry, D.P., and P.A. McLaughlin. 1975. The barnacles of the Balanus amphitrite complex (Cirripedia, Thoracica). Zoologische Verhandelingen 141: 1– 254. Herrera, W. 1985. Clima de Costa Rica. San José, Costa Rica: Editorial UNED. Houbrick, J.R. 1968. A survey of the litoral marine molluscs of the Caribbean coast of Costa Rica. Veliger 11: 4– 23. INCOPESCA. 2006. Memoria Institucional 2002– 2006: Instituto Costarricense de Pesca y Acuicultura. San José, Costa Rica: Imprenta Nacional. IPCC (Intergovernmental Panel on Climate Change). 2007. Climate Change 2007: The Physical Science Basis. Paris: WMO, UNEP.

614 Chapter 17 Jiménez, C. 2001. Bleaching and mortality of reef organisms during a warming event in 1995 on the Caribbean coast of Costa Rica. Revista de Biología Tropical 49(Suppl. 2): 233– 38. Jiménez, C., and J. Cortés. 1993. Density and compressive strength of the coral Siderastrea siderea (Ellis and Solander, 1786) (Scleractinia: Siderastreidae): intraspecific variability. Revista de Biología Tropical 41(Suppl. 1): 39– 43. Jiménez, I. 1998. Ecología y conservación del manatí (Trichechus manatus, L.) en el noreste de Costa Rica. Base de datos de los humedales del noreste de Costa Rica asociada a un Sistema de Información Geográfica. M.Sc. thesis, Universidad Nacional. Heredia, Costa Rica. Jiménez, I. 1999. Estado de conservación, ecología y conocimiento popular del manatí (Trichechus manatus) en Costa Rica. Vida Silvestre Neotropical 8: 18– 30. Jiménez, I. 2005. Development of predictive models to explain the distribution of the West Indian manatee Trichechus manatus in tropical watercourses. Biological Conservation 125: 491– 503. Kelmo, F., and R. Vargas. 2002. Anthoathecatae and Leptothecatae hydroids from Costa Rica (Cnidaria: Hydrozoa). Revista de Biología Tropical 50: 599– 627. Kemperman, T.C.M., and H. Stegenga. 1983. A new Caulerpa species (Caulerpaceae, Chlorophyta) from the Caribbean side of Costa Rica, Central America. Acta Botanica Neerlandica 32: 271– 75. Kemperman, T.C.M., and H. Stegenga. 1986. The marine bentic algae of the Atlantic side of Costa Rica. Brenesia 25– 26: 99– 122. Kleypas, J.A., R.A. Feely, V.J. Fabry, C. Langdon, C.L. Sabine, and L.L. Robbins. 2006. Impacts of Ocean Acidification on Coral Reefs and Other Marine Calcifiers: A Guide for Future Research. Report of a Workshop. NSF / NOAA / USGS. Krupp, L.S. 2006. Distribution, Ecology and State of the Seagrass Beds in the Gandoca-Manzanillo National Wildlife Refuge, Caribbean Costa Rica. M.Sc. thesis, Universität Bremen. Bremen, Germany. Krupp, L.S., J. Cortés, and M. Wolff. 2009. Growth dynamics and state of the seagrass Thalassia testudinum in the Gandoca-Manzanillo National Wildlife Refuge, Caribbean Costa Rica. Revista de Biología Tropical 57(Suppl. 1): 187– 201. Lawrence, J.M. 1967. Lipid reserves in the gut of three species of tropical sea urchins. Caribbean Journal of Science 7: 65– 68. Lessios, H.A., D.R. Robertson, and J.D. Cubit. 1984. Spread of Diadema mass mortality through the Caribbean. Science 226: 335– 37. Linkimer, L., and T. Aguilar. 2000. Estratigrafía sedimentaria. In P. Denyer and S. Kussmaul, eds., Geología de Costa Rica, 43– 62. Cartago: Editorial Tecnológica de Costa Rica. Lizano, O.G. 1996. Un método gráfico para el pronóstico de oleaje durante huracanes en el Caribe adyacente a Costa Rica. Tópicos Meteorológicos y Oceanográficos 3: 11– 17. Lizano, O.G. 2006. Algunas características de las mareas en las costa Pacífica y Caribe de Centroamérica. Ciencia y Tecnología 24: 51– 64. Lizano, O.G. 2007. Climatología del viento y oleaje frente a las costas de Costa Rica. Ciencia y Tecnología 25: 43– 56. Lizano, O.G., and W. Fernández. 1996. Algunas características de las tormentas tropicales y de los huracanes que atravesaron o se formaron en el Caribe adyacente a Costa Rica durante el período 1886– 1988. Tópicos Meteorológicos y Oceanográficos 3: 3– 10. Lizano, O.G., and R.J. Moya. 1990. Simulación de oleaje durante el huracán Joan (1988) a su paso por el Mar Caribe de Costa Rica. Revista de Geofísica 33: 105– 26.

Loaiza-Coranado, B. 1989. Generalidades del Phylum Porifera y bases para su identificación con sinopsis de algunas de ellas, en Limón, Costa Rica. Licentiate thesis, Universidad Nacional. Heredia, Costa Rica. Loaiza-Coronado, B. 1991. Estudio taxonómico de las esponjas del Parque Nacional Cahuita, sector Puerto Vargas e Isla Uvita, Limón, Costa Rica. Brenesia 36: 21– 62. Loría, L.G., A. Banichevich, and J. Cortés. 1998. Radionucleidos en corales de Costa Rica. Revista de Biología Tropical 46(Suppl. 5): 81– 90. Marshall, J.S. 2007. Geomorphology and physiographic provinces. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources, Hazards, 75– 122. London: Taylor and Francis. Mata, A., J.A. Acuña, M.M. Murillo, and J. Cortés. 1987. La contaminación por petróleo en el Caribe de Costa Rica: 1981– 1985. Caribbean Journal of Science 23: 41– 49. May-Collado, L.J. 2010. Changes in whistle structure of two dolphin species during interspecific associations. Ethology 116: 1– 10. May-Collado, L.J., and D. Wartzok. 2008. A comparison of bottlenose dolphin whistles in the Atlantic Ocean: factors promoting whistle variation. Journal of Mammalogy 89: 1229– 40. May-Collado, L.J., and D. Wartzok. 2009. A characterization of Guyana dolphin (Sotalia guianensis) whistles from Costa Rica: the importance of broadband recording systems. Journal of the Acoustical Society of America 125: 1202– 13. McNeill, D.F., A.G. Coates, A.F. Budd, and P.F. Borne. 2000. Integrated paleontologic and paleomagnetic stratigraphy of the upper Neogene deposits around Limon, Costa Rica: a coastal emergence record of the Central American Isthmus. Geological Society of America Bulletin 112: 963– 81. Michel, H.B., and M. Foyo. 1976. Caribbean Zooplankton. Part I. Siphonophora, Heteropoda, Copepoda, Euphausiacea, Chaetognatha and Salpidae. Washington, DC: Office of Naval Research Department, Navy. Mielke, W. 1992. Six representatives of the Tetragonicipitidae (Copepoda) from Costa Rica. Microfauna Marina 7: 101– 46. Mielke, W. 1993. Species of the taxa Orthopsyllus and Nitroca (Copepoda) from Costa Rica. Microfauna Marina 8: 247– 66. Mielke, W. 1994. Two co-occurring new Karllangia species (Copepoda: Ameriidae) from the Caribbean coast of Costa Rica. Revista de Biología Tropical 42: 141– 53. Miloslavich, P., J.M. Díaz, P.E. Klein, J.J. Alvarado, C. Díaz, J. Gobin, E. Escobar-Briones, J.J. Cruz-Motta, E. Weil, J. Cortés, A.C. Bastidas, R. Robertson, F. Zapata, A. Martín, J. Castillo, A. Kazandjan, and M. Ortiz. 2010. Marine biodiversity in the Caribbean: regional estimates and distribution patterns. PLOS ONE 5(8): e11916. DOI:10.1371/journal.pone. 0011916. Mooers, C.N.K., and G.A. Maul. 1998. Chapter 7. Intra-Americas Sea circulation. In A.R. Robinson and K.H. Brink, eds., The Sea, vol. 11, 183– 208. New York: John Wiley. Mora, A., C. Fernández, and A.G. Guzmán. 2006. Áreas Marinas Protegidas y Áreas Marinas de Uso Múltiple de Costa Rica: Notas para una Discusión. San José, Costa Rica: MarViva. Mora, D.A., J.C. Rojas, A.V. Mata, and M.A. Sequeira. 1987. Calidad sanitaria de las aguas de la playa de Limón en el período 1981– 1984. Tecnología en Marcha 8: 15– 22. Mora-Cordero, C. 2005. Factores que afectan la cuenca del Río La Es-

The Caribbean Coastal and Marine Ecosystems 615 trella y recomendaciones para mejorar la gestión en la zona costera. Limón, Costa Rica. M.Sc. thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Morales, A., and M.M. Murillo. 1996. Distribution, abundance and composition of coral reef zooplankton, Cahuita National Park, Limon, Costa Rica. Revista de Biología Tropical 44: 619– 30. Morales-Ramírez, A. 1987. Caracterización del zooplancton del arrecife en el Parque Nacional Cahuita, Limón, Costa Rica. M.Sc. thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Morales-Ramírez, A. 2001. Biodiversidad marina de Costa Rica: Los microcrustáceos: Subclase Copepoda (Crustacea: Maxillopoda). Revista de Biología Tropical 49(Suppl. 2): 115– 33. Morales-Ramírez, A., E. Suárez-Morales, M. Corrales, and O. EsquivelGarrote. 2014. Diversity of the free-living marine and freshwater Copepoda (Crustacea) in Costa Rica: a review. ZooKeys 457: 15– 33. Moran, D.A., and A.I. Dittel. 1993. Anomura and brachyuran crabs of Costa Rica: annotated list of species. Revista de Biología Tropical 41: 599– 617. Muller-Parker, G., and J. Cortés. 2001. Spatial distribution of light and nutrients in coral reefs of the Pacific and Caribbean coasts of Costa Rica during January 1997. Revista de Biología Tropical 49(Suppl. 2): 251– 63. Murillo, M.M., and J. Cortés. 1984. Alta mortalidad en la población del erizo de mar Diadema antillarum Philippi (Echinodermata: Echinoidea), en el Parque Nacional Cahuita, Limón, Costa Rica. Revista de Biología Tropical 32: 167– 69. Myhre, S., and A. Acevedo-Gutiérrez. 2007. Recovery of sea urchin Diadema antillarum populations is correlated to increased coral cover and reduced macroalgal cover. Marine Ecology Progress Series 329: 205– 10. Nagelkerken, I., K. Buchan, G.W. Smith, et al. 1997. Widespread disease in Caribbean sea fans: I. Spreading and general characteristics. Proceedings of the 8th International Coral Reef Symposium, Panamá 1: 679– 82. Nielsen-Muñoz, V. 2007. Abundancia, biomasa y floración de Thalassia testudinum (Hydrocharitaceae) en el Parque Nacional Cahuita, Caribe de Costa Rica. Thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Nielsen-Muñoz, V., and J. Cortés. 2008. Abundancia, biomasa y floración de Thalassia testudinum (Hydrocharitaceae) en el Caribe de Costa Rica. Revista de Biología Tropical 56(Suppl. 4): 175– 89. Ornelas-Gatdula, E., Y. Camacho-García, M. Schrödl, V. Padula, Y. Hooker, T.M. Gosliner, and A. Valdés. 2012. Molecular systematics of the “Navanax aenigmaticus” species complex (Mollusca, Opisthobranchia): coming full circle. Zoologica Scripta 41: 374– 85. Ortea, J. 2001. El género Doto Oken, 1815 (Mollusca: Nudibranchia) en el mar Caribe: Historia natural y descripción de nuevas especies. Avicennia (Suppl. 3): 1– 46. Ortea, J., J. Espinosa, and Y. Camacho. 1999. Especies del género Polycera Cuvier, 1816 (Mollusca: Nudibranchia) recolectados en la epifauna de algas rojas del Caribe de Costa Rica y Cuba. Avicennia 10/11: 157– 64. Ortea, J., J. Espinosa, and L. Moro. 2001. Descripción de una nueva especie de Philine Ascanius, 1772. Avicennia (Suppl. 4): 38– 40. Paddack, M.J., J.D. Reynolds, C. Aguilar, et al. 2009. Recent region-wide declines in Caribbean reef fish abundance. Current Biology 19: 1– 6. Parkinson, R.W., J. Cortés, and P. Denyer. 1998. Passive margin sedimen-

tation on Costa Rica’s north Caribbean coastal plain, Río Colorado. Revista de Biología Tropical 46(Suppl. 6): 221– 36. Paynter, C.K., J. Cortés, and M. Engels. 2001. Biomass, productivity and density of the seagrass Thalassia testudinum at three sites in Cahuita National Park, Costa Rica. Revista de Biología Tropical 49(Suppl. 2): 265– 72. Pepe, P.J. 1985. Littoral endolithic fauna of the Central American Isthmus. Revista de Biología Tropical 33: 191– 94. Pereira-Chaves, J., and L. Sierra-Sierra. 2009. Estrategia de manejo de los recursos marinos y costeros en Isla Uvita, Limón, Costa Rica. Revista de Ciencias Marinas y Costeras 1: 127– 43. Pérez-Reyes, C.R. 2003. Interpretación ambiental de un sendero autoguiado en Isla Uvita de Puerto Limón, como un aporte al desarrollo turístico de la Región Caribe de Costa Rica. Licentiate thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Petrescu, I., and R.W. Heard. 2004. Three new Cumacea (Crustacea: Peracarida) from Costa Rica. Zootaxa 721: 1– 12. Phillips, P.C., and M.J. Perez-Cruet. 1984. A comparative survey of reef fishes in Caribbean and Pacific Costa Rica. Revista de Biología Tropical 32: 95– 102. Pool, D.J., S.C. Snedaker, and A.E. Lugo. 1977. Structure of mangrove forests in Florida, Puerto Rico, Mexico, and Costa Rica. Biotropica 9: 195– 212. Reynolds, J.E., W.A. Szelistowski, and M.A. León. 1995. Status and conservation of manatees Trichechus manatus manatus in Costa Rica. Biological Conservation 71: 193– 96. Risk, M.J., M.M. Murillo, and J. Cortés. 1980. Observaciones biológicas preliminares sobre el arrecife coralino en el Parque Nacional Cahuita, Costa Rica. Revista de Biología Tropical 28: 361– 82. Robinson, D.G. 1991. The systematics and paleoecology of the prosobranch gastropods of the Pleistocene Moín formation of Costa Rica. PhD diss., Tulane University. New Orleans, LA. Robinson, D.G., and M. Montoya. 1987. Los moluscos marinos de la costa Atlántica de Costa Rica. Revista de Biología Tropical 35: 375– 400. Roder, C. 2005. Land-based pollution on the Caribbean coast of Costa Rica: nutritional and skeletal characteristics of the reef-building coral Siderastrea siderea as a response. M.Sc. thesis, Universität Bremen. Bremen, Germany. Roder, C., J. Cortés, C. Jiménez, and R. Lara. 2009. Riverine input of particulate material and inorganic nutrients to a coastal reef ecosystem at the Caribbean coast of Costa Rica. Marine Pollution Bulletin 58: 1937– 43. Rodríguez-Sevilla, L., R. Vargas, and J. Cortés. 2003. Biodiversidad marina de Costa Rica: Gastrópodos (Mollusca: Gastropoda) de la costa Caribe. Revista de Biología Tropical 51(Suppl. 3): 302– 99. Rojas, M.T. 1990. Determinación del cadmio, cromo, cobre, hierro, manganeso, plomo y zinc en el pepino de mar, Holothuria sp. (Echinodermata) del arrecife coralino del Parque Nacional Cahuita, Costa Caribe, Costa Rica. Licentiate thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Rojas, M.T., J.A. Acuña, and O.M. Rodríguez. 1998. Metales traza en el pepino de mar Holothuria (Halodeima) mexicana del Caribe de Costa Rica. Revista de Biología Tropical 46(Suppl. 6): 215– 20. Salas, E., H. Molina-Ureña, R.P. Walter, and D.D. Heath. 2010. Local and regional genetic connectivity in a Caribbean coral reef fish. Marine Biology 157: 437– 45.

616 Chapter 17 Salazar, A., O.G. Lizano, and E.J. Alfaro. 2004. Composición de sedimentos en las zonas costeras de Costa Rica utilizando Fluorescencia de Rayos-X (FRX). Revista de Biología Tropical 52(Suppl. 2): 61– 75. Samper-Villarreal, J., A. Bernecker, and I.S. Wehrtmann. 2008. Inventory of macroalgal epiphytes on the seagrass Thalassia testudinum (Hydrocharitaceae) in Parque Nacional Cahuita, Caribbean coast of Costa Rica. Revista de Biología Tropical 56(Suppl. 4): 163– 74. Sánchez, J.A. 2001. Systematics of the southwestern Caribbean Muriceopsis Aurivillius (Cnidaria: Octocrallia), with the description of a new species. Bulletin of the Biological Society of Washington 10: 160– 80. Sánchez-Vindas, P.E. 2001. Flórula Arborescente del Parque Nacional Cahuita. San José, Costa Rica: Editorial EUNED. Sandí, G. 1990. Determinación de Zn, Cd, Pb, Cu, Fe, Mn, y Cr en aguas del arrecife coralino del Parque Nacional Cahuita, Costa Rica. Licentiate thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Santoro, M., E.C. Greiner, J.A. Morales, and B. Rodríguez-Ortíz. 2006a. Digenetic trematode community in nesting green sea turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. Journal of Parasitology 92: 1202– 6. Santoro, M., G. Hernández, M. Caballero, and F. García. 2006b. Aerobic bacterial flora of nesting green turtles (Chelonia mydas) from Tortuguero National Park, Costa Rica. Journal of Zoo and Wildlife Medicine 37: 549– 52. Santoro, M., and S. Mattiucci. 2009. Sea turtle parasites. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America. Berlin: Springer + Business Media B.V. Text: pp. 507– 19, Species List: CD pp. 497– 500. Santoro, M., J.A. Morales, B. Stacy, and E.C. Greiner. 2007. Rameshwarotrema uterocrescens trematode parasitism of the oesophageal glands in green sea turtles (Chelonia mydas). Veterinary Record 159: 59– 60. Savage, J.M. 2002. The Amphibians and Reptiles of Costa Rica. Chicago: University of Chicago Press. Schmidt, E., M. Wolff, and J.A. Vargas. 2002. Population ecology and fishery of Cittarium pica (Gastropoda: Trochidae) on the Caribbean coast of Costa Rica. Revista de Biología Tropical 50: 1079– 90. Silva-Benavides, A.M. 1986. Productividad primaria, biomasa del fitoplancton y la relación con parámetros físico-químicos en el arrecife coralino del Parque Nacional Cahuita. M.Sc. thesis, Universidad de Costa Rica. San Pedro, Costa Rica. Smith, G.W., L.D. Ives, I.A. Nagelkerken, and K.B. Ritchie. 1996. Caribbean sea-fan mortalities. Nature 383: 487. Soto, R. 1983. Nuevos informes para la flora bentónica marina de Costa Rica. Brenesia 21: 365– 70. Soto, R., and D.L. Ballentine. 1986. La flora bentónica del Caribe de Costa Rica (Notas preliminares). Brenesia 25/26: 123– 62. Spongberg, A.L. 2004. PCB contamination in surface sediments in the coastal waters of Costa Rica. Revista de Biología Tropical 52(Suppl. 2): 1– 10. Stegenga, H., and T.C.M. Kemperman. 1983. Acrochaetiaceae (Rhodophyta) new to the Costa Rican Atlantic flora. Brenesia 21: 67– 91. Suárez-Morales, E., A. Carrillo, and A. Morales-Ramírez. 2013. Report on some monstrilloids (Crustacea: Copepoda) from a reef area off the Caribbean coast of Costa Rica, Central America with description of two new species. Journal of Natural History 47: 619– 38. Tabash-Blanco, F.A. 1995. An assessment of pink shrimp, Penaeus brasil-

iensis, populations, in three areas of the Caribbean coast of Costa Rica. Revista de Biología Tropical 43: 239– 50. Taylor, G.D. 1975. The Geology of the Limón Area of Costa Rica. PhD diss., Louisiana State University. Baton Rouge, LA. Taylor, M.A., and E.J. Alfaro. 2005. Climate of Central America and the Caribbean. In J.E. Oliver, ed., Encyclopedia of World Climatology, 183– 89. Netherlands: Springer. Taylor, W.R. 1933. Notes on algae from the tropical Atlantic Ocean, II. Papers Mich Acad Sci Arts Lett 17:395– 407. Terossi, M., J.A. Cuesta, I.S. Wehrtmann, and F.L. Mantelatto. 2010b. Revision of the larval morphology (Zoea I) of the family Hippolytidae (Decapoda, Caridea), with a description of the first stage of the shrimp Hippolyte obliquimanus Dana, 1852. Zootaxa 2624: 49– 66. Terossi, M., I.S. Wehrtmann, and F.L. Mantelatto. 2010a. Interpopulation comparison of reproduction of the Atlantic shrimp Hippolyte obliquimanus (Caridea: Hippolytidae). Journal of Crustacean Biology 30: 571– 79. Thomas, D.T., and D.W. Freshwater. 2001. Studies of Costa Rican Gelidiales (Rhodophyta): four Caribbean taxa including Pterocladiella beachii sp. nov. Phycologia 40: 340– 50. Tiwari, M., K.A. Bjorndal, A.B. Bolten, and B.M. Bolker. 2005. Intraspecific application of the mid-domain effect model: spatial and temporal nest distributions of green turtles, Chelonia mydas, at Tortuguero, Costa Rica. Ecology Letters 8: 918– 24. TNC ( The Nature Conservancy). 2008. Evaluación de ecorregiones marinas en Mesoamérica. Sitios prioritarios para la conservación en las ecorregiones Bahía de Panamá, Isla del Coco y Nicoya del Pacífico Tropical Oriental, y en el Caribe Suroccidental de Costa Rica y Panamá. San José, Costa Rica: The Nature Conservancy. Troëng, S. 2005. Migration of sea turtles from Caribbean Costa Rica: implications for management. PhD diss., Lund University. Lund, Sweden. Troëng, S., D. Chacón, and B. Dick. 2004. Possible decline in leatherback turtle Dermochelys coriacea nesting along the coast of Caribbean Central America. Oryx 38: 395– 403. Troëng, S., D. Evans, E. Harrison, and C. Lagueux. 2005. Migration of green turtles Chelonia mydas nesting at Tortuguero, Costa Rica. Marine Biology 148: 435– 47. Troëng, S., and E. Rankin. 2005. Long-term conservation of the green turtle Chelonia mydas nesting population at Tortuguero, Costa Rica. Biological Conservation 121: 111– 16. Tsuda, R.T. 1968. Additional records of marine benthic algae from Costa Rica. Caribbean Journal of Science 8: 103– 4. Umaña, R., and D. Chacón. 1994. Asentamiento en estadios de postlarvales de la langosta Panulirus argus (Decapoda: Palinuridae), en Limón, Costa Rica. Revista de Biología Tropical 42: 585– 94. Valdez, M.F., and C.R. Villalobos. 1978. Distribución espacial, correlación con el substrato y grado de agregación en Diadema antillarum Phillipi (Echinodermata: Echinoidea). Revista de Biología Tropical 26: 237– 45. Valverde, J. 2000. Descentralización y comanejo de recursos en el Caribe Tico. Ciencias Ambientales 19: 45– 59. Vander Zanden, H.B., K.E. Arthur, A.B. Bolten, B.N. Popp, C.J. Lagueux, E. Harrison, C.L. Campbell, and K.A. Bjorndal. 2013. Trophic ecology of a green turtle breeding population. Marine Ecology Progress Series 476: 237– 49. Van der Hal, N. 2006. Presence and Diversity of Sponge Species at the

The Caribbean Coastal and Marine Ecosystems 617 Caribbean coast of Costa Rica. M.Sc. thesis, University of Amsterdam. Netherlands. Van Tussenbroek, B.I., J. Cortés, R. Collins, A.C. Fonseca, P.M.H. Gayle, H.M. Guzmán, G.E. Jácome, R. Juman, K.H. Koltes, H.A. Oxenford, A. Rodríguez-Ramírez, J. Samper-Villareal, S.R. Smith, J.J. Tschirky, and E. Weil. 2014. Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse. PLOS ONE 9(3): e90600. doi:10.1371/journal .pone.0090600 Vargas, R., and J. Cortés. 1997. Biodiversidad marina de Costa Rica: Orden Stomatopoda (Crustacea: Malacostraca: Hoplocarida). Revista de Biología Tropical 45: 1531– 39. Vargas, R., and J. Cortés. 1999. Biodiversidad marina de Costa Rica: Crustacea: Decapoda (Penaeoidea, Sergestoidea, Stenopodidae, Caridea, Thalassinidea, Palinura) del Caribe. Revista de Biología Tropical 47: 877– 85. Vargas, R., and J. Cortés. 2006. Biodiversidad marina de Costa Rica: Crustacea: Infraorden Anomura. Revista de Biología Tropical 54: 461– 88. Vaughan, T.W. 1919. Fossil corals from Central America, Cuba, and Porto Rico, with an account of the American Tertiary, Pleistocene, and Recent coral reefs. United States National Museum Bulletin 103: 189– 524. Voss, G.L. 1971. Narrative of RV John Elliot Pillsbury Cruise P-7101: Central America, January 20– February 5, 1971. Miami, FL: School of Marine and Atmospheric Science, University of Miami. Walter, T.C. 1989. Review of the new world species of Pseudodiaptomus (Copepoda: Calanoida) with a key to the species. Bulletin of Marine Science 45: 590– 628. Wehrtmann, I.S., and L. Albornoz. 2002. Evidence of different reproductive traits in the transisthmian sister species, Alpheus saxidomus and A. simus (Decapoda, Caridea, Alpheidae): description of the first postembryonic stage. Marine Biology 140: 605– 12. Wehrtmann, I.S., and J. Cortés, eds. 2009. Marine Biodiversity of Costa

Rica, Central America. Berlin: Springer + Business Media BV. Text: 538 pp., Species Lists CD: 500 pp. Wehrtmann, I.S., J. Cortés, and S. Echeverría-Sáenz. 2009. Marine biodiversity of Costa Rica: perspectives and conclusions. In I.S. Wehrtmann and J. Cortés, eds., Marine Biodiversity of Costa Rica, Central America, 521– 33. Berlin: Springer + Business Media BV. Wehrtmann, I.S., and R. Vargas. 2003. New records and range extensions of shrimps (Decapoda: Penaeoidea, Caridea) from the Pacific and Caribbean coasts of Costa Rica, Central America. Revista de Biología Tropical 51: 268– 74. Weitzer, V.A. 2000. From conflict to collaboration: the case of Cahuita National Park, Costa Rica. M.Sc. thesis, University of Manitoba. Winnipeg, Manitoba, Canada. Wellington, G.M. 1973. Additions to the Atlantic benthic flora of Costa Rica. Brenesia 2: 17– 20. Wellington, G.M. 1974a. An ecological description of the marine and associated environments at Monumento Nacional Cahuita. San José, Costa Rica: Sub-dirección de Parques Nacionales, MAG. Wellington, G.M. 1974b. The benthic flora of Punta Cahuita: annotated list of species with additions to the Costa Rican Atlantic flora. Brenesia 3: 19– 30. Wetzer, R., and N.L. Bruce. 1999. A new genus and species of sphaeromatid isopod (Crustacea) from Atlantic Costa Rica. Proceedings of the Biological Society of Washington 112: 368– 80. Williams, A.B. 1993. Mud shrimps, Upogebiidae, from the western Atlantic (Crustacea: Decapoda: Thalassinidea). Smithsonian Contributions to Zoology 544: 1– 77. Winemiller, K.O., and M.A. Leslie. 1992. Fish communities across a complex freshwater-marine ecotone. Environmental Biology of Fishes 34: 29– 50. Young, P.S. 1989. Ceratoconcha paucicostata, a new species of coralinhabiting barnacle (Cirripedia, Pyrgomatidae) from the western Atlantic. Crustaceana 56: 193– 99.

Chapter 18 Rivers of Costa Rica

Catherine M. Pringle1,*, Elizabeth P. Anderson2, Marcelo Ardón3, Rebecca J. Bixby4, Scott Connelly1, John H. Duff5, Alan P. Jackman6, Pia Paaby7, Alonso Ramírez8, Gaston E. Small9, Marcia N. Snyder1, Carissa N. Ganong1, and Frank J. Triska5

Introduction Rivers of Costa Rica drain the narrow isthmus between the continents of North and South America, discharging into either the Pacific Ocean or the Caribbean Sea. The country is thus characterized by a high ocean-to-coast ratio and has 34 major watersheds (Fig. 18.1). The orientation of mountain ranges along the longitudinal axis of the country contributes to the high number of smaller watersheds (>100) that are characterized by steep gradients in their headwaters. Most rivers have their headwaters located in volcanic mountains and are characterized by cold clear waters which evolve into turbid and warm waters in the lowlands. The narrow mountainous region of Costa Rica results in multiple parallel river systems with relatively small drainage areas. Most of the rivers that discharge into the Caribbean and Pacific are relatively short, with the exception of the Río San Juan Odum School of Ecology, University of Georgia, Athens, GA 30602, USA Department on Earth & the Environment, Florida International University, MIami, FL, USA 3 Department of Biology, East Carolina University, Greenville, NC, USA 4 Department of Biology, University of New Mexico, Albuquerque, NM, USA 5 US Geological Survey, Menlo Park, CA, USA 6 Department of Chemical Engineering, University of California, Davis, CA, USA 7 Organization for Tropical Studies (OTS), Apartado 676-2050, San Pedro de Montes de Oca, Costa Rica 8 Institute for Tropical Ecosystem Studies, University of Puerto Rico, Río Piedras, Puerto Rico 9 University of St. Thomas, Saint Paul, MN, USA * Corresponding author 1 2

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(37 km). The Río San Juan is the largest (41,600 km2) watershed in Central America, located on the border between Costa Rica (which contains ~30% of the watershed) and Nicaragua (which contains ~70% of the watershed) and discharging into the Caribbean. Much of Costa Rica has relatively young soils due to recent volcanic activity (Alvarado and Mata, chapter 4 of this volume). Moreover (as discussed in detail later in this chapter), ongoing geothermal activity (Alvarado and Cárdenes, chapter 3 of this volume) occurs along the volcanic spine of Costa Rica, creating spatial patterns in stream solute levels that influence the ecology of streams draining volcanic mountainous areas (Fig. 18.2; Pringle and Triska 2000). Rivers of Costa Rica provide a legacy of historical changes in land use since they integrate the watersheds that they drain, reflecting changes in terrestrial ecosystems. Before the arrival of the Spanish, Costa Rica was inhabited by scattered Indian populations that practiced shifting agriculture, and effects on river ecosystems can be assumed to have been minimal relative to subsequent effects associated with expanding human populations. Agricultural settlement began in the Central Valley and in Nicoya (primarily to produce sugar cane, tobacco, and coffee). Coffee exports began in 1825 and permanent crops replaced the forests of the Central Valley by the end of the century. The end of the nineteenth century was also characterized by a wave of colonization towards the coasts, particularly the Pacific Coast. Deforestation increased exponentially in the early 1920s (WRI 1991). Expansion of the cattle-ranching frontier in

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Fig. 18.1 Map displaying the 34 major watersheds of Costa Rica. Figure created by M. Snyder using Digital Atlas of Costa Rica 2004 data.

the 1950s has had many deleterious effects on forests and water resources. Costa Rica lost 50% of its forest cover between 1940 and 1986, resulting in significant problems in soil erosion, river siltation, and water quality. Costa Rican rivers are vulnerable because of the intensity and duration of rainfall (1.5– 6 m yr− 1). Severe erosion is often a consequence of forest removal in highland and mountainous regions: from 20– 200 tons of soil ha− 1 yr− 1 are eroded from deforested slopes (Hartshorn et al. 1982). Sediment loads in rivers have negative effects on fish and other organisms and are ultimately discharged into coastal regions. In the early 1980s Costa Rica had one of the highest annual rates of deforestation in the world, peaking at 100,000 acres per year (e.g., see Sader and Joyce 1988). Current rates of deforestation are relatively low, since much of the remaining primary forest lies within protected areas; however, pressure to exploit timber and water resources in national parks and forest reserves is increasing with human population growth

Fig. 18.2 Map of Central America showing mountainous areas and approximate locations of streams that have names suggesting that they are affected by underlying geothermal activity. Volcanic activity is common throughout Central America as a result of the northeastward subduction of the Cocos ridge beneath the Caribbean plate. Thus, geothermally modified ground waters occur frequently in the landscape. The distribution of these streams is clustered along the central axis of the mountains. Modified from Pringle and Triska 2000.

Rivers of Costa Rica 623 Fig. 18.3 Río Sarapiquí– San Juan drainage on the Caribbean Slope of the Cordillera Central. This is a 2001 Landsat true color satellite image draped over a digital elevation model with the relief exaggerated. The forest in this image is dark green and is mostly contained in the protected areas of Braulio Carrillo National Park, and the Maquenque Wildlife Refuge. Image created by M. Snyder.

(Fig. 18.3). Shortages of potable water for expanding human populations are becoming increasingly problematic, even in wet lowland areas such as Puerto Viejo de Sarapiquí (Vargas 1995), which receive as much rainfall as 4 m yr− 1. For a more detailed history of river development in Costa Rica, see Pringle and Scatena (1999b). Today, the rivers of Costa Rica appear and function very differently than they did just a decade ago and their structural and functional properties are likely to continue to change in response to future anthropogenic influences. Numerous contributions to riverine research in Costa Rica (reviewed in this chapter) have been made by investigators at the Universidad de Costa Rica (UCR) and its Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), the Universidad Nacional (UNA), EARTH College, and the Instituto Costarricense de Electricidad (ICE). The Organization for Tropical Studies (OTS) has also facilitated riverine research at its biological stations throughout the country— with a significant number of riverine studies conducted at La Selva Biological Station on Costa Rica’s Caribbean slope (e.g., La Selva STREAMS Project: http:// www.streamslaselva.net) and an increasing number of studies occurring at OTS’s Palo Verde Biological Station on the Pacific coast. Additionally, studies conducted at Maritza Biological Station (located in Guanacaste on the Pacific slope and developed with the Stroud Water Research Center) have significantly added to our knowledge of Costa Rican rivers. In the sections that follow, we discuss (1) riverine plants

with a focus on algal periphyton (given the conspicuous lack of information on aquatic macrophytes); (2) riverine animals including both vertebrates and invertebrates; (3) species interactions in rivers ranging from mutualism, competition, and predation to frugivory and seed dispersal by fishes; (4) ecosystem functioning and dynamics with emphasis on biogeochemistry, nutrient cycling, primary productivity, and decomposition; (5) people and nature with a focus on environmental effects of hydropower, land use changes, water withdrawals, and invasive species; and finally (6) future perspectives, a section which discusses research needs and the importance of maintaining the biological integrity of rivers for human survival.

Plants In this section we primarily focus on algal periphyton; however, we will first briefly discuss aquatic and semi-aquatic vascular plants. In the Caribbean lowlands, emergent aquatic vegetation is composed of aquatic grasses like Panicum maximum, Oryza latifolia (small rice, arrocillo), Hymenochne amplexicaulis, Brachiaria sp., as well as floating vegetation such as water hyacinth (Eichhornia crassipes; Jiménez et al. 2005, and see Jiménez, chapter 20 of this volume). Three species of Eichhornia occur in Costa Rica with the native species (E. azurea and E. heterosperma) commonly occurring in swamps and ponds. E. crassipes is abundant (especially in Limón and Guanacaste [ Janzen

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1983]) and is a widespread invasive weed in reservoirs such as Lago Arenal. In general, tropical algae are poorly understood (Mann and Droop 1996). This is likely a function of unexplored areas and the prevalence of a cosmopolitan paradigm long held in the phycological community. Algae are often reported as having cosmopolitan distributions, with worldwide occurrences (Finlay et al. 2002); however, research now indicates that diatom species demonstrate biogeographical patterns that reflect endemism and regional distributions based on environmental factors and historical constraints (Kociolek and Spaulding 2000, Kilroy et al. 2007). These biogeographic patterns hold especially true for many tropical regions where very high levels of diatom endemism have been documented (e.g., Metzeltin and Lange-Bertalot 1998, Moser et al. 1998, Metzeltin and Lange-Bertalot 2002). Although algal distributions are poorly documented in Central America including Costa Rica, regional patterns have been reported that are associated with distinct stream solute chemistries resulting from geothermal activity (Pringle et al. 1993). In a broad landscape-scale survey, Pringle et al. (1993) collected algal samples from multiple streams draining the Barva, Poás, and Arenal Volcanoes along the Cordillera Central (Figs. 18.2, 18.3; and see Lawton et al., chapter 13 of this volume, for a detailed account on the forested ecosystem of this volcanic mountain range). These streams receive different types of geothermally modified groundwater inputs. Diatoms were dominant in most samples, except for thermal (hot) springs, very low pH environments (acidic), and streams with mineral precipitation. In hot springs at Tabacón near Arenal and Tucarón near Platanar, cyanobacteria were prevalent, but with low diversity including the genera Phormidium, Lyngbya, Dermocarpa, Oedogonium, and Oscillatoria, and the diatom genus Pinnularia. Green algae (Chlorophyta) were diverse and occurred in many samples, including Microspora in low pH, acid sulfate waters of Río Azufre (pH = 4.6). A more recent taxonomic survey recognized nineteen new diatom taxa described from the acidic Río Agrio that drains Volcán Poás, including taxa from the diatom genera Chamaepinnularia, Eunotia, Frustulia, and Stauroneis (Wydrzycka and Lange-Bertalot 2001). Other habitats and regions of Costa Rica are less studied but research shows diatoms (Bacillariophyceae) to be the dominant group, with red algae (Rhodophyta), green algae (Chlorophyta), and blue greens (Cyanobacteria) as commonly represented algal divisions in rivers. It also should be noted that aerophilic taxa, which grow in moist subaerial habitats (including bromeliads and wet mosses), form a significant algal component in the wet tropical forests of Costa Rica, and can wash into streams secondarily.

Many diatom taxa that occur in rivers in the Caribbean lowland streams (R. Bixby, unpublished data) and Pacific Coast (Silva-Benavides 1996a) are regionally endemic (Navicula incarum Lange-Bert. & Rumrich, N. ingapirca Rumrich & Lange-Bert., N. kohlenbachii Lange-Bert. & Rumrich, and Stenopterobia pumila Lange-Bert. & Rumrich, all described from Ecuador) or pantropical (e.g., Cocconeis feuerbornii Hustedt described from Java and Rhopalodia gibberula var. argentina Brun., collected from South America, the Caribbean, and Japan [Bourrelly and Manguin 1952]). Overall, we expect the number of endemic, Neotropical, and Pantropical distribution records for all algae to increase— as more floristic and taxonomic works are completed in Costa Rica. Very little systematic and phylogenetic research has been completed on Costa Rican algae. One notable exception is the inclusion of freshwater red algae (Rhodophyta) into North/Central American systematics analyses (Sheath et al. 1993a,b, Sherwood and Sheath 1999). Among freshwater red algae, interesting patterns have been documented in tropical areas of Central America. Sheath et al. (1993b) initiated a study to survey the North American specimens in the Order Ceramiales. Parts of this Order belong to a group of freshwater red algae thought to be secondary invaders from marine environments. This survey reported the first definitive Central American records in Costa Rican streams of the freshwater red algae Ballia prieurii Kütz. and Caloglossa ogasawaerensis Okam based on morphological and molecular analyses. Algae are light-limited in lowland tropical streams that drain primary forest (Fig. 18.4). In the Caribbean lowlands (specifically at La Selva Biological Station; see McClearn et al., chapter 16 of this volume), standing crop accrual of algal periphyton has been shown to be significantly higher at sites bordered by pasture, with high light levels (14– 45 mg m− 2 chl a), versus shaded forested watersheds (4 mg m− 2 chl a, P < .001) (Paaby and Goldman 1992). This degree of light limitation and resulting low algal biomass response is similar to that found in streams of temperate regions where light can be a limiting factor even with increased nutrient levels. Periphyton biomass and species assemblages are often affected by stream solute (nutrients and ions) levels. Solutes can occur in naturally elevated conditions or can be in higher concentrations owing to anthropogenic inputs. As previously mentioned in this section and discussed in more detail later (see Geochemistry section), many streams draining volcanic regions of Costa Rica receive groundwater with elevated levels of solutes resulting from underlying geothermal activity (Pringle and Triska 1991, 2000). Detailed taxonomic studies of algae that are ongoing at

Rivers of Costa Rica 625 Fig. 18.4 Quebrada Salto (60 m a.s.l.), a lowland interior forest stream that is heavily shaded by a multi-strata canopy. The Salto drains La Selva Biological Station, which is located at the gradient break between the mountains and foothills on the Caribbean slope. This river is one of the two main drainages of the station and it receives natural inter-basin transfers of geothermally modified groundwaters (of the sodium chloride bicarbonate type) in its lower reaches. Photo by C. Pringle.

La Selva Biological Station (R. Bixby, University of New Mexico) indicate that euryhaline algal taxa are dominant in high-solute streams at La Selva. High-solute streams receive interbasin transfers of geothermally modified groundwater and are classified as a dilute sodium-chloride-bicarbonate geothermal water type. Euryhaline taxa (Fig. 18.5) reflect the presence of salts and chloride in these streams. In contrast, low-solute streams that do not receive groundwater

inputs are poorly buffered and dominated by acidophilic taxa (Bixby et al. 2005; Fig. 18.5). Biotic parameters such as competition, predation, and grazing can also play a role in influencing algal growth and species composition in Costa Rican streams and rivers. These studies are discussed later in this chapter (see Species Interactions section). Because algae function well as indicators of the status of

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farm sewage on periphyton communities in two streams in south-central Costa Rica. The diatom species composition broadly reflected increases in agricultural pollution (i.e., increases in soluble reactive phosphorus [SRP], ammonium, and nitrate, and low dissolved oxygen), although diatom species groups did not correlate well with common diatom indices of pollution developed in Europe. This study demonstrates the need for understanding the ecological requirements for Neotropical diatoms and the development of more regionally based biomonitoring indices. From a species-level perspective, studies looking at organic pollution in Costa Rican streams note that cosmopolitan diatom taxa (Gomphonema parvulum [Kütz.] Kütz., Navicula subminuscula Manguin, Navicula seminulum Grun., and Nitzschia palea [Kütz.] W. Sm.) were indicative of organic pollution in streams (Silva-Benavides 1996b, Michels 1998a). In contrast, pristine stream sites were found to reflect more variability in environmental parameters and were dominated by different and more regionally distributed diatoms (Quebrada La Pita, Michels, 1998a; Río Savegre, Silva-Benavides, 1996b). Michels et al. (2006) examined diatom communities from 23 stream sites with differing riparian land use in Golfo Dulce on the Osa Peninsula. Diatom species distributions were highly correlated with riparian shading, which separated the first-order forested streams from the larger rivers. This shading gradient was associated with decreased canopy cover as a result of deforestation and agriculture. Turbidity and biological oxygen demand also explained much of the variation among species assemblages.

Animals Fig. 18.5 Light micrographs (scale bar = 10 µm) of Neotropical diatoms found in streams draining La Selva Biological Station, Costa Rica. Some of the taxa are good indicators of stream chemistry, as indicated below: (A) Cocconeis feuerbornii Hustedt, raphe valve; (B) pseudoraphe valve; (C) Navicula kohlenbachii Lange-Bert. & Rumrich; (D) Rhopalodia gibberula var. argentina Brun.; (E) Navicula incarum Lange-Bert. & Rumrich; (F) Navicula ingapirca Rumrich & Lange-Bert.; (G) Stenopterobia pumila Lange-Bert. & Rumrich. This taxon is found in solutepoor unbuffered streams at La Selva with low bicarbonates and is an indicator of acidic conditions. Photos by R. Bixby.

their environment and the quality of its waters, they have been used to assess anthropogenic impacts on Costa Rican streams and rivers. Anthropogenic impacts on algal communities include decreased dissolved oxygen levels, organic inputs (including elevated nitrogen compound levels), and increased sediment load (Silva-Benavides 1996b, Michels et al. 2006). Michels (1998a,b) studied the effects of pig

The relatively recent geologic history of Costa Rica contributes to the lower species diversity of these rivers compared to those of South America. The close proximity of the ocean also creates a distinct signature and marine-derived fauna is abundant in lowland rivers. The presence of marine fauna far inland is a good example, such as the sightings of sharks and flounder in the San Juan– Sarapiquí river drainages. If Costa Rica’s river fauna is compared to that of the Caribbean islands, which also have short and steep river drainages, the pattern is different. Rivers in Costa Rica are much more diverse and species-rich than those of the islands, which are more difficult to colonize by freshwater species. Therefore, Costa Rica is somewhat of an intermediate place, having a low diversity relative to continents and a rich fauna when compared to insular systems. The diversity of river types (e.g., steep mountain streams,

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meandering lowland rivers) and sizes provides for a wide array of faunal community structures and compositions. Many lowland river systems are fish- and shrimp-dominated, while insects and amphibians often predominate in mountainous headwater streams. Animals inhabit a wide variety of habitats within a river: cobble-covered riffles; sandy and muddy pools; and the deep stretches of large rivers. Even the vertical walls of waterfalls are the habitat of some insect species and decapods (Calvert 1915). The amount of information available about the diversity and ecology of the different animal groups varies significantly among taxa. Similar to other parts of the tropics, groups with large body sizes are better known than small organisms. As expected, the diversity of vertebrates is well known, with fishes being the most species-rich group and perhaps the most important for the functioning of riverine ecosystems. In contrast, invertebrates are poorly studied: we lack complete species inventories and have little information on invertebrates at the levels of population, community, and ecosystem (Ramírez and Pringle 1998a,b). River fauna differs considerably among and within drainages. Geomorphological characteristics of rivers provide the setting for the establishment of distinct faunal assemblages. The large percentage of mountainous terrain in Costa Rica results in a significant fraction of river drainages characterized by steep slopes, the presence of waterfalls, and many torrentially flowing waters. Areas of coastal lowlands are relatively limited, in particular on the Pacific slope, and few rivers have developed the typical complex series of meanders and floodplains that characterizes coastal rivers. Some animal groups have distributions that clearly reflect changes in river geomorphology. Fish assemblages, for example, are diverse and abundant in lowland areas, but decrease toward headwaters, and completely disappear above ~800 m a.s.l. In addition, waterfalls play a major role defining fish distribution, with a lack of fish upstream of large waterfalls. Marine-related fauna is also abundant in lowland rivers and decrease or disappear toward the mountains. Marine fishes, such as tarpon (Megalops atlanticus) and even some shark species, are known to travel upriver for several kilometers in large lowland rivers (Bussing 1993) and shrimp are more abundant near the coast (Ramírez et al. 1998). Here we focus on the animal fauna that inhabit rivers or that rely on river resources for food. Thus, while birds are included, we touch upon only those that consume aquatic resources. We discuss (1) general species richness of different faunal groups (our purpose is not to provide extensive species checklists); (2) riverine habitats, where habitat refers to the type of river system inhabited by a particular faunal group and the specific locations used within a river

(e.g., riffles, pools, riparian areas); and (3) available information about animal function within the ecosystem, which is rather limited for most taxa and quite variable among species within faunal groups. Fishes

Fishes are perhaps the most important vertebrate group inhabiting river ecosystems. There are 174 fish species reported for Costa Rica’s freshwater ecosystems, including introduced species, distributed in 38 families (see www .fishbase.org). The most diverse families are the Cichlidae, Poeciliidae, and Characidae. Twenty fish species, mainly in the families Poeciliidae and Characidae, are considered endemic to Costa Rica. River fishes of Costa Rica are well documented by Bussing (1998) and information is also available on the web at www.fishbase.org. Ecological aspects of fish communities at La Selva Biological Station are discussed in detail by Burcham (1980) and Bussing (1994). Winemiller (1983) provides an overview of the fish assemblages of Corcovado National Park located in the Osa Peninsula on Costa Rica’s Pacific Coast. For a detailed description of the ecology of this lowland rainforest peninsula, see Gilbert al. (chapter 12 of this volume). Fishes are more diverse in lowland rivers, decline in abundance and diversity with elevation, and completely disappear from most rivers above 800 m a.s.l. Within a river, they use a wide variety of habitats (e.g., pools, undercut banks; Lyons and Schneider 1990) but tend to be more abundant in slow-water areas such as pools. Deep pools with woody debris provide shelter and food resources for many fish species and they tend to be more abundant and diverse in this type of habitat (Fig. 18.6). Fishes play a key role in ecosystem processes such as nutrient cycling, primary production, and decomposition. Predatory fishes can be important controlling populations of invertebrates and other fish species and can have direct or indirect effects on other resources (e.g., detritus, algae; Pringle and Hamazaki 1998). Species that consume algae and fine organic matter from the river bottom are also important influences on primary production and the movement of organic matter within river systems. Wootton and Oemke (1992) discuss the importance of fish herbivory in a lowland tropical stream (draining La Selva Biological Station and adjacent environments) in the context of latitudinal differences in fish community structure. Inputs of terrestrial insects (e.g., ants) support high densities of fishes (3– 14 individuals m− 2) in forested headwater streams (Small et al. 2013a). In a larger, fourth-order stream, the contribution of terrestrial insects to the diet of the omnivorous fish Astyanax

628 Chapter 18 Fig. 18.6 Theraps underwoodi, a common cichlid found in the Río Sarapiquí drainage that is vulnerable to displacement by invasive tilapia. Photo by R. Coleman.

aeneus (Characidae) resulted in this species playing a disproportionally important role in stream nutrient cycling. Astyanax represented 12% of the fish population and 18% of the fish biomass in this stream, but accounted for 90% of phosphorus supplied by fish excretion (Small et al. 2011a). Twelve species of non-native fishes are now established in many rivers throughout Costa Rica. The best known examples are trout and tilapia, both introduced for aquaculture. Trout inhabit cool-water mountain streams and are now well established in many streams that used to lack fishes (e.g., see Kappelle, chapter 14 of this volume). Trout have been responsible for the extirpation of streamdwelling frogs in most of the high-elevation streams where they have become established. The negative environmental consequences of the spread of tilapias in lowland streams of Costa Rica are discussed in detail in the final section of this chapter (People and Nature: Non-native Fish Introductions; and see Jiménez, chapter 20 of this volume). Increased abundance and distribution of tilapia could mean the endangerment and ultimately extinction of native cichlids (Fig. 18.6) in Costa Rica: the Cichlidae family is the most diverse fish family found in inland waters in Costa Rica, with 9 genera

and 24 species (Bussing 1998). Displacement of native cichlids by tilapias will undoubtedly have major effects on the structure and function of river ecosystems. Other invasive species include armored catfish (Pterygoplichthys spp.: Loricariidae), or “peces diablo” (“devilfish”), which have recently been identified in the Reventazón River basin (Solano and Arias 2011). Pterygoplichthys, common aquarium fish native to South America, are invasive in other Central American countries and are phosphorus-rich fish that form large benthic aggregations and alter stream nutrient dynamics (Capps and Flecker 2013). Amphibians

Of the 179 amphibian species reported for Costa Rica, ~15– 20 are aquatic, with larval tadpole stages that dwell in rivers (Young et al. 2004). Stream-dwelling frog taxa are primarily in the genera Atelopus (e.g., Atelopus varius; Fig. 18.7) and Rana (e.g., Rana warszewitschii), and in the families Centrolenidae (glass frogs) and Hylidae (tree frogs), reaching highest levels of speciation and abundance in rivers at higher elevations where predatory fishes are absent.

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Species-specific body and mouthpart morphology allows larval frogs to occupy virtually all stream microhabitats, including riffles, runs, pools, bank-side marginal pools, and anoxic detrital accumulations. Although tadpoles are a ubiquitous component of many upland Costa Rican streams, the larval stages of stream-breeding anurans are relatively under-studied, and many of the species are yet to be formally described. Savage (2002) provides an overview of most amphibians in Costa Rica. Additional information can be found at the website of Costa Rica’s National Biodiversity Institute, INBio (www.inbio.ac.cr). Catastrophic amphibian declines in Costa Rica, like throughout much of the Neotropics, are well documented (Stuart et al. 2004), with perhaps the earliest and bestknown example being the extinction of the golden toad of Monteverde (Bufo periglenes) in 1989 (see Lawton et al., chapter 13 of this volume). While some amphibian declines are considered enigmatic, such as the dramatic decrease in amphibians inhabiting protected old-growth lowland habitat at La Selva Biological Station (Whitfield et al. 2007), the fungal pathogen Batrachochytrium dendrobatidis has been implicated with the extirpations or extinctions of most highland stream-dwelling species (i.e., frogs with larval tadpole stages) in Costa Rica (Lips et al. 2003). Particularly decimated are species of the once common stream-breeding genus Atelopus, many species of which are now believed to be extinct in the wild (La Marca et al. 2005). Although generally sub-lethal to tadpoles, the chytrid fungus kills adult frogs by inhibiting electrolyte transport (Voyles et al. 2009), and is considered to be an emerging infectious disease of amphibians. Additional information on amphibian declines can be found in Lips (1998, 1999), Young et al. (2004), and Whitfield et al. (2007, 2012, 2013).

Until the early to mid-1980s, tadpoles were a conspicuous component of highland river ecosystems above 800 m a.s.l in Costa Rica. They undoubtedly played a key role in stream and riparian foodwebs. Stream-dwelling amphibians create a linkage of energy and nutrients between aquatic and terrestrial habitats, initially due to the eggs that adults deposit into the streams, and again when the young froglets metamorphose and move to the riparian area. However, little is known about the trophic status of most larvae and adults, and how tadpoles affect stream ecosystem structure and function is poorly understood. Unfortunately, there is presently little chance to study their ecological roles within the country of Costa Rica. Realizing that the ongoing spread of chytrid fungus had not yet decimated highland frogs throughout parts of Panama, investigators have consequently pursued studies in Panama on the role of streamdwelling frogs on ecosystem function as part of the Tropical Amphibian Declines in Streams (TADS) Project (Whiles et al. 2006). Tadpoles were found to reduce algae, alter algal community composition, increase biomass-specific primary production, and alter macroinvertebrate functional structure. It has become clear, from TADS’ studies in Panama, that stream-dwelling frogs were undoubtedly once key players in structuring highland streams in Costa Rica and that their loss has significantly affected ecosystem function (see Ranvestel et al. 2004, Whiles et al. 2006, Verburg et al. 2007, Connelly et al. 2008, Colon-Gaud et al. 2009, Whiles et al. 2013). Reptiles

Caimans, crocodiles, and turtles are the main reptilian fauna inhabiting rivers, and their biology is poorly known.

Fig. 18.7 Stream-dwelling frogs (i.e., with larval tadpole stages) have largely disappeared from high elevation streams throughout Costa Rica. (A) Sexually dimorphic harlequin frogs, Atelopus varius, in amphiplexus on the banks of the Río Sardinalito in Braulio Carrillo National Park (~650 m a.s.l.) in 1983 before the taxon was extirpated. This taxon is vulnerable to a fungal pathogen that has since resulted in its extirpation from most high elevation streams throughout Costa Rica. (B) Dying harlequin frog, Atelopus zeteki, at high elevation stream site in El Cope, Panama, 2004. ( A) photograph by C. Pringle; (B) photograph by S. Connelly.

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Caimans (Caiman crocodilus) and crocodiles (Crocodylus acutus) can be found in rivers up to 350 m a.s.l. Caimans are small (up to 2.5 m) and inhabit many interior lowland swamps and slow rivers. The crocodile is a coastal species that was formerly common in mangrove swamps and coastal rivers but it can also be found in rivers up to 50 km inland. The reader is directed to other references for more detailed life history information about caimans and crocodiles in Costa Rica (Dixon and Staton 1983, Scott and Limerick 1983, Allsteadt and Vaughan 1988, 1992, Savage 2002; website of Costa Rica’s National Biodiversity Institute, INBio [www.inbio.ac.cr]; see also Jiménez, chapter 20 of this volume). There are several species of turtles that use rivers as their main habitats, all tending to increase in diversity in lowland rivers. They fall into three families: (1) the snapping turtle Chelydra serpentina (Chelydridae); (2) the aquatic and terrestrial Embydidae; and (3) the semi-aquatic mud turtles (Kinosternidae). Most reptiles favor slow-flowing rivers and streams in lowland areas as their habitats (e.g., see McClearn et al., chapter 16 of this volume, for reptiles thriving in the Caribbean lowlands). Within these they can be observed on wood debris and along the river margins. At least some turtles prefer to inhabit fast-flowing waters. Among them, the whitelipped mud turtle (Kinosternon leucostomum) can be found in fast-flowing streams with clear waters where it feeds on aquatic invertebrates. Most riverine reptiles are predatory; however, some turtles are omnivorous and consume significant quantities of plant material as well as animals. More detailed information about riverine turtles can be found in Savage (2002) and at the website of Costa Rica’s National Biodiversity Institute, INBio (www.inbio.ac.cr). Birds

Birds are a major component of the faunal diversity associated with rivers of Costa Rica. There are 910 species reported for Costa Rica (as of 2014) and ~150 species are associated with aquatic environments— many with rivers. Detailed information about the life histories of specific bird species common in riverine ecosystems can be found in Stiles (1983) and Stiles and Skutch (1989). Birds play important roles in rivers as predators and some have a role in disturbing the bottom in their search for food. Common wading birds include six species of herons, green ibis (Mesembrinibus cayennensis), and tiger herons (Tigrisoma spp.). Costa Rica’s six species of kingfisher (Ceryle and Chloroceryle spp.) dive for fish from riverside trees, and anhingas (Anhinga anhinga) spear fish with their

bills while swimming underwater and are often seen drying their wings in the sun on riverside snags. Many bird species associated with rivers have particular habitat requirements. For example, jacanas (Jacana spinosa) are common in rivers where aquatic and riparian vegetation is abundant, several species of sand pipers (e.g., Actitis macularis) can be found in rivers with sandy or muddy shores, and ducks (e.g., Cairina moschata) can be found even in small streams with low flow. The strikingly patterned sunbittern (Eurypyga helis) prefers forested streams, as does the sungrebe, or finfoot (Heliornis fulica). Mammals

A few species of mammals are closely associated with rivers. The Neotropical river otter (Lontra longicaudus) inhabits riparian habitats from small streams to large rivers in lowland areas of Costa Rica as well as other parts of Central and South America. Otters feed almost exclusively on crustaceans and fish and represent an important predator of larger bodied shrimp (e.g., Macrobrachium; Figs. 18.8, 18.9) and fish (e.g., cichlids, Fig. 18.6). Otters prefer deeper streams with high arboreal and shrub cover and large rocks and logs (Spinola-Parallada and Vaughan-Dickhaut 1995). The otter is considered a threatened species due to habitat loss, but is classified as Data Deficient on the IUCN Red List of Threatened Species. Another important mammal in river ecosystems is the fishing bat or greater bulldog bat, Noctilio leporinus, in the family Noctilionidae. N. leporinus is a relatively large bat with a mass of 60– 90 g and a wingspan of up to 60 cm, with a bulldog-like face, narrow pointed ears, and very small eyes (Brandon 1983). Fishing bats are common in lowland areas of Costa Rica and can be found searching for food over slow-moving rivers and ponds. Their diet consists primarily of fish but also includes insects and crustaceans picked from the water surface and insects caught in the air. They fly close to the water surface, with their greatly enlarged hind feet and claws occasionally dipping into the waters to grab small fish and other organisms that break the water surface. Noctilio albiventris, the lesser bulldog bat, is smaller than N. leporinus, with a mass of 30– 40 g and a wingspan of 40– 45 cm. It primarily feeds on insects caught on the wing or from the river surface (Brandon 1983). Although now at the verge of extinction, manatees (Trichechus manatus) used to inhabit riverine ecosystems near coastal areas in Costa Rica. Reports from the 1800s include the presence of manatees in the Sarapiquí and San Juan River drainages (Ligon 1983). Recent work with predictive

Fig. 18.8 A freshwater migratory shrimp in the genus Macrobrachium, collected from the Sábalo River in the Caribbean lowlands. Macrobrachium spp. can reach sizes of greater than 15 cm. Photo by M. Snyder.

Fig. 18.9 The freshwater shrimp, Macrobrachium carcinus, about to be consumed at a restaurant in La Virgen, Costa Rica. Photo by M. Snyder.

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models shows that manatees prefer waterways with abundant aquatic vegetation, warm clear waters and high forest cover ( Jiménez et al. 2005; and Jiménez, chapter 20 of this volume). Additional information about aquatic mammals can be found in Janzen (1983) and at the website of Costa Rica’s National Biodiversity Institute, INBio (www.inbio. ac.cr). Crabs

Freshwater crabs inhabiting streams of Costa Rica have not received much attention yet. A total of 15 species and four genera in the family Pseudothelphusidae (Brachyura) are reported (Rólier Lara et al. 2013). Most of the work has focused on taxonomy (Magalhães et al. 2010 and references therein), with much less work focusing on the ecological roles of crabs (Villalobos and Burgos 1975). A recent study examined the abundance and diversity of crabs in the Río Grande de Térraba, which is being considered for one of the largest hydroelectric projects in Central America (ICE 2009, Rólier Lara et al. 2013). They found eight different species of Pseudothelphusidae and three genera, mostly at the middle elevations (between 311 and 600 m above sea level; Rólier Lara et al. 2013). The most common species, Ptychophallus paraxanthusi, was found at elevations from 20 to 700 m (Rólier Lara et al. 2013). Future studies should examine the abundance, diversity, and ecosystem role of crabs in streams in other regions of Costa Rica. Shrimps

Freshwater shrimps are diverse and often dominant components of the river fauna in Costa Rica (e.g., see Gilbert et al., chapter 12 of this volume, regarding shrimps found in southern Pacific lowland moist forest rivers). While their taxonomy has received relatively limited attention CedeñoObregón (1986) reports that there are at least sixteen species in three genera: Atya, Palaemon, and Macrobrachium. A. scabra, A. crassa, and A. innocous occur in both the Pacific and Caribbean sides of the country. A. margaritacea, Palaemon gracilis, M. panamense, M. tenellum, M. digueti, M. occidentele, M. hancocki, and M. americanum inhabit only the Pacific side while M. acanthurus, M. heterochirus, M. olfersii, M. amazonicum, and M. carcinus are those found on the Caribbean side (Cedeño Obregon 1986). Atyids are medium-sized shrimps with short legs. In contrast, palaemonids are mostly predators that reach large sizes and have long legs (Figs. 18.8, 18.9). Large adult palaeomonids in the genus Macrobrachium are often harvested from rivers and can be eaten at local restaurants in lowland Costa

Rica (Fig. 18.9) (García-Guerrero et al. 2013, Snyder et al. 2013). Freshwater shrimps are a marine-derived fauna and those species in Costa Rica maintain a marine connection through their amphidromous life cycle (as do the majority of freshwater shrimp species occurring throughout the Americas): larvae released from adult females drift downstream to the estuary, where they spend part of their life cycle (~120 days), and juveniles subsequently migrate back upstream to freshwater environments (Chace and Hobbs 1966). In Costa Rica, freshwater shrimp larvae have been found in streams from sea level to 700 m a.s.l. (Fureder 1994, Ramírez and Pringle 1998a). In streams located 30– 50 m a.s.l., shrimp larvae are more abundant than drifting insects, making up more than half of all drift net captures (Pringle and Ramírez 1998a). Shrimps are vulnerable to losses in riverine connectivity, given their life history requirement of migration to and from the estuary. Few studies have examined effects of dams on shrimp populations in Costa Rica (Snyder et al. 2011); however, studies in Puerto Rico indicate that large dams without spillway discharge can block upstream migrations of shrimp, resulting in their complete upstream extirpation (Holmquist et al. 1998), with consequent effects on stream ecosystem structure and function (Greathouse et al. 2006a). Shrimp populations are consequently good potential indicators of riverine connectivity (Pringle 1997, March et al. 2003, Crook et al 2009, Greathouse et al. 2006b) and the value of monitoring shrimp populations is becoming increasingly clear. Additional discussion of effects of dams on freshwater shrimps in Costa Rica can be found later in this chapter in the People and Nature section. Shrimps are important macroconsumers in tropical streams and have been shown to affect benthic community composition by decreasing the inorganic sediment mass and the densities of larval Chironomidae and other insects (March et al. 2002, Rosemond et al. 1998, Pringle and Hamazaki 1998). Shrimps in lowland Costa Rican streams tend to be nocturnal to avoid predation by fishes and birds (Pringle and Hamazaki 1998). Atyid shrimps inhabit a wide variety of habitats, including fast-flowing riffles. They are omnivorous, consuming algae, detritus, and invertebrates as part of their diets. Palaemonid shrimps can be omnivorous and/or predatory, feeding on other crustaceans, aquatic insects, and their larvae as well as algae, seeds, fruits, and other mollusks (Cedeño-Obregón 1986, Pringle and Hamazaki 1998, Snyder et al. 2014). The distribution of larger palaemonid shrimps (such as adults in some species of Macrobrachium; Fig. 18.9) is influenced by substrate size and shrimps tend to be more abundant

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in larger rivers and deeper pools. Snyder (2012) suggests that streams receiving geothermally modified solute-rich groundwater (sodium chloride bicarbonate type) may be areas of high habitat quality for Macrobrachium olfersii. Aquatic Insects

Among aquatic invertebrates, insects are the most diverse group of animals in rivers. All major orders of aquatic insects are present in Costa Rican rivers and some are highly diverse (Springer 2008). Although information on insect diversity is still limited, aquatic insects are better studied in Costa Rica than in any other Central American country. Recently, Springer et al. (2014) summarized the state of knowledge of aquatic insects and other invertebrates for Costa Rica, with emphasis on biodiversity and biomonitoring. A manual to identify major freshwater invertebrate groups is underway. The first section of the manual, covering immature stages of Ephemeroptera, Odonata, Plecoptera and Trichoptera, was recently published (Springer et al. 2010) and remaining sections will be published in the near future (see http://macrolatinos.ramirezlab.net/manualcr). New developments in aquatic insect biodiversity are supported by the availability of well-curated museum collections. An important resource is the aquatic insect collection at the University of Costa Rica that is curated by Monika Springer and colleagues. This collection houses over 300 genera, representing 93 families and 11 orders of insects (http: //museo.biologia.ucr.ac.cr / Colecciones / Insectos Acuaticos.htm). Some insect groups are better studied than others, such as the Odonata (dragonflies and damselflies), Trichoptera (caddisflies), and Plecoptera (stoneflies). There are currently 271 species of Odonata reported to occur in Costa Rica (Ramírez et al. 2000, Ramírez 2010). While most species are found in streams and rivers, some inhabit swamps and lakes or specialized habitats such as bromeliads. New species continue to be found, such as Leptobasis guanacaste described by Paulson (2009), and the potential total number of species for the country could reach 300. Information on the adult stages of Odonata can be found in Esquivel (2006) and on larvae in Ramírez (2010). The diversity of Trichoptera (caddisflies) in Costa Rica has reached 460 species and was revised by Holzenthal (1988) and Springer (2006, 2010). A major limitation for the study of this order is the lack of information on the larval stages, which are the main ecological players in river ecosystems. Currently only ~10% of the species are known as larvae, and we know little about their ecological roles (Springer et al. 2014).

The order Ephemeroptera (mayflies) is represented by ~80 species and was revised by Flowers (1992) and Flowers and de la Rosa (2010). The order Plecoptera (stoneflies) is represented by 27 species (Stark 1998). Until recently, Plecoptera in Costa Rica was thought to be represented by a single genus, Anacroneuria. However, recent studies reported a second one, Perlesta, from streams in the Central Valley (Gutiérrez-Fonseca and Springer 2011). Three new species of Anacroneuria were also recently described from the country (Stark 2014). Knowledge of aquatic insects in Costa Rica is now allowing their use in outreach and biomonitoring efforts. Monika Springer and colleagues at the University of Costa Rica and EARTH University have recently developed a user-friendly index to determine water quality in Costa Rica on the basis of insect taxa (Springer et al. 2007). In addition, since 2007 Costa Rica has been implementing the use of stream invertebrates as part of the monitoring process for all development projects associated with rivers and other aquatic environments. Government decree Nº 33903-MINAE-S established that freshwater ecosystem condition in the country must be monitored using water physicochemical parameters and benthic macroinvertebrates, mostly insects, using the BMWP-CR index (Springer et al. 2014). Within river ecosystems, insects play a wide variety of ecological roles. Herbivorous insects are important in controlling rates of primary productivity; detritivorous insects are important in processing organic matter that enters streams (e.g., leaves from riparian trees); and predatory insects can be important secondary consumers in riverine foodwebs. Insects that shred leaf material are not very abundant in Costa Rican rivers and leaves seem to be processed more by generalist insects and other organisms (Irons et al. 1994, Ramírez and Pringle 1998a,b, Rosemond et al. 1998; see foodweb in Fig. 18.10). Information on ecological studies with aquatic insects was summarized by Springer (2008) and Springer et al. (2014).

Species Interactions Symbiosis, Mutualism, Competition, and Parasitism

Symbiotic and mutualistic relationships have not received as much attention in riverine systems relative to terrestrial ecosystems in Costa Rica. Lichtwardt (1997) described the prevalence of gut fungi (Trichomycetes) in aquatic insects. The Trichomycetes appear to be mostly harmless during their life time in the larvae’s guts, and can be beneficial at times when food is scarce (Horn and Lichtwardt 1981). Twenty-three species of Trichomycetes were found in the

634 Chapter 18 Fig. 18.10 Generalized stream food web in Río Puerto Viejo at La Selva Biological Station (35 m a.s.l.).

guts of Ephemeroptera and Diptera (Simuliidae, Chironomidae) larvae in 36 streams throughout Costa Rica. The most common species of Trichomycetes, Harpella tica, was found in 95% of Simuliidae larvae sampled (Lichtwardt 1997). In sections of a polluted stream, Simuliidae larvae had a greater number and diversity of gut fungi than in unpolluted sections of the same stream. The role of competition in determining abundance and distribution of riverine species has received more attention than symbiosis. Based on extensive surveys and determination of morphology and habitat use, Winemiller and Leslie (1992) hypothesized that competition was important in determining fish species abundance in lagoons in Tortuguero National Park on the Caribbean coast. In the same lagoon, Winemiller and Ponwith (1998) also inferred interspecific competition between three species of eleotrid (Eleotridae) fishes using studies of population structure, abundance, and feeding strategies. In contrast, Lips (2001) found that variable environmental conditions were more important than competition in determining spatial and temporal variation in reproductive activity of a species of treefrog (Hyla calypsa) in a cloud forest stream on the Pacific coast. Only one study (that we are aware of) has examined hostparasite relationships in Costa Rican streams. Chandler et al. (1995) measured the prevalence and intensity of a clinostomatid (Digenea: Platyhelminthes) parasite in Poecilia gillii in six isolated pools of an intermittent stream in Santa Rosa National Park, Guanacaste. During the dry

season, when the main stream channel dries up, fish populations become isolated in pools that can diverge over time in their physical characteristics, creating spatial heterogeneity that affects host-parasite dynamics. Chandler et al. (1995) found that fish density and fish size in isolated pools were more important than physical characteristics (dissolved oxygen and pH) of the pools in determining parasite prevalence. Herbivory

Omnivorous fish and shrimp assemblages are important in structuring algal assemblages in lowland Costa Rican streams (Pringle and Hamazaki 1997, 1998). Using electric exclosures in the Sábalo stream at La Selva Biological Station, Pringle and Hamazaki (1997) showed that, in the presence of fishes, algal assemblages were dominated by firmly attached filamentous blue-green algae (Lyngbya sp.), while loosely attached diatoms dominated where fishes were excluded. Consequently, in the absence of fishes, algal standing crop was scoured and exported downstream by frequent high discharge events. Fishes were found to play a key role in maintaining stable algal assemblages that were more resistant to storm events (Pringle and Hamazaki 1997). Also using electric exclosures, Pringle and Hamazaki (1998) separated effects of diurnal fish and nocturnal shrimp assemblages on algal and insect communities. Both fishes and shrimps decreased algal biomass (measured as organic

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ash-free dry mass), with the effects of both groups together being stronger than their individual effects. Fishes shifted algal communities from diatoms to green and blue-green algae, while shrimps had no strong effect on algal community composition. Barbee (2005) examined the role of insect grazers on algal biomass in the Tarcolitos River, which drains the Pacific coast of Costa Rica. The Tarcolitos River has few decapods and low fish diversity and abundance, suggesting that herbivorous insects can play an important role in structuring algal assemblages. Barbee (2005) found a 30% increase in algal biomass (measured as chlorophyll a) when insect grazers, mostly Baetidae (Ephemeroptera) and Chironomidae (Diptera), were excluded from tiles. The only epibenthic grazing fish species present, the freshwater goby, Sycidium salvini, did not feed preferentially or decrease algal biomass on tiles with and without insect grazers. Predator-Prey Interactions

Ecological theory predicts that large omnivores (such as fishes and shrimps in lowland Costa Rican streams) can have strong effects on both basal resources (algae) and small primary consumers such as insects (Pringle and Hamazaki 1998). In addition to being important herbivores, omnivorous fishes and shrimps are key predators in stream foodwebs. Fish and shrimp assemblages were found to be important in reducing abundance of Chironomidae and total insects colonizing tiles and leaf packs in the Sábalo stream at La Selva Biological Station in the Caribbean lowlands (Pringle and Hamazaki 1997, 1998, Rosemond et al. 1998). Predatory effects of fishes on insects were shown to be stronger than the effects of shrimps (Pringle and Hamazaki 1998). No evidence of trophic cascades (Power 1990) was found, which agrees with theoretical predictions of the role of large omnivores in stream foodwebs (Pringle and Hamazaki 1998). Fishes and shrimps are also known to affect drift and migration behavior in invertebrates. Invertebrate drift in streams of La Selva Biological Station is strongly nocturnal, which is thought to be primarily driven by the presence of diurnal drift-feeding fishes (Ramírez and Pringle 1998a, Ramírez and Pringle 2001, Boyero and Bosch 2002). In a study of drift periodicity in streams along an altitudinal gradient (30 to 2,700 m above sea level), Pringle and Ramírez (1998) found higher nocturnal than diurnal drift densities only in streams where predatory fish were present. Fish have also been reported to change upstream migration patterns of snails. Schneider and Lyons (1993) studied the upstream migration of two snail species, Neritina latissima and Co-

chlopinia tryoniana, in the Río Claro on the Osa Peninsula. Presence of the molluscivorous pufferfish (Sphoeroides annulatus) decreased the number of migrating snails and caused both species of snails to hide on the underside of rocks. While there is strong evidence for the important role of predation in reducing insect density and behavior (i.e., drift and migration) in streams at La Selva Biological Station, there is also evidence that phosphorus (P) availability in rivers can have a stronger stimulatory effect on insect densities (Rosemond et al. 2001, Ramírez and Pringle 2004). Working in two streams with low P and one stream with naturally high P, Rosemond et al. (2001) and Ramírez and Pringle (2004) found stronger positive effects of high P levels on insect density than negative effects of fish and shrimp predation. In Quebrada Las Pailas, a small second-order stream in Rincón de la Vieja National Park, Duft et al. (2002) examined interactions of macro- and meio-fauna and their effects on algae. Macro-fauna (size ≥500 µm) and meio-fauna (size 5 meters in some areas) has resulted in hundreds of high-gradient streams with sufficient discharge for electricity generation. Costa Rica’s theoretical hydroelectric potential is estimated at 25,500 megawatts (CFIA 2005); practical hydropower potential is estimated at 10,000 megawatts (FAO 2005). Numerous hydropower plants of different types (e.g., storage, water diversion) and both large and small dams currently harness the flow of Costa Rican rivers (Fig. 18.13), with a collective installed generation capacity of approximately 1,300 megawatts (Anderson et al. 2006b). However, the majority of Costa Rica’s hydropower potential remains untapped and more projects are either under construction or proposed to take advantage of this natural potential as a means for meeting the country’s future needs for electricity. The list of large dams currently in operation (or nearing completion) includes the Cachí, Angostura, and Reventazón Dams in the Reventazón River Basin; the Toro I and II,

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Fig. 18.12 Uses of the Sarapiquí River include transportation, hydropower, recreation, and ecotourism (i.e., sightseeing tours and whitewater rafting). Photos by E. Anderson.

Fig. 18.13 Despite restrictions on private companies, the results of electricity sector reform are visible throughout Costa Rica. Hydropower has been a beneficiary of reforms and 28 private dams have been constructed since 1990. In addition, the Costa Rican Instituto Costarricense de Electricidad (ICE) operates 11 dams and nine other hydropower developments as subsidiaries of ICE have also built many dams. This map shows that private dams are concentrated on gradient breaks and many are located on the wet, northern Caribbean slope.

Cariblanco, and General Dams in the Sarapiquí River Basin; the Peñas Blancas Dam in the San Carlos River Basin; and the Arenal Dam complex in northwestern Costa Rica. Perhaps the best known of these is the Arenal Dam Complex, a multipurpose project that generates a large portion of Costa Rica’s electricity, provides irrigation water, and has created new recreational areas. This Complex has changed the face of the landscape in northwestern Costa Rica: an interbasin transfer across the continental divide (from the Caribbean to the Pacific slope) provided additional water to fill a large reservoir (Fig. 18.14) that flooded several towns and required the resettlement of hundreds of people. After being used to generate electricity, water from the dam is diverted

642 Chapter 18 Fig. 18.14 Arenal reservoir, Costa Rica, is one of the largest hydropower projects in Central America and supplies a substantial portion of Costa Rica’s energy supply. Photo by E. Anderson.

to a canal system and used for irrigation by rice and sugarcane farmers in the area near Bagaces, Costa Rica. The Arenal Dam complex also influences the physical, chemical, and biological characteristics of streams and wetlands in the Tempisque River Basin around the area of Palo Verde National Park; these water bodies are the eventual recipients of water from the Arenal reservoir downstream from agricultural operations. The trend of proliferation of small dams for hydropower, which began in the early 1990s, has disrupted riverine connectivity and altered river ecosystems throughout the country. Of the >30 hydropower plants constructed during the 1990s, the majority have dams 300 river kilometers, mostly headwater streams, were located upstream from the dams of eight hydropower plants in operation in 2006 (Anderson et al.

Fig. 18.15 The El Toro dam on the Sarapiquí River. Photo by E. Anderson.

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Fig. 18.16 Stream de-watering by hydropower projects changes the hydrological and thermal regimes directly below the dam in a de-watered reach of the Puerto Viejo River. Photos by E. Anderson.

Fig. 18.17 De-watered reach of the Puerto Viejo River downstream from the Doña Julia dam. Note the small amount of watered area on the stream bottom and the limited habitat for aquatic fauna such as fishes, shrimps, and otters. Photo by E. Anderson.

2007). De-watered reaches also represent breaks in riverine connectivity on the basis of differences in physical conditions between these reaches and upstream and downstream river segments. Again, the Sarapiquí River Basin provides an example, with approximately 31 kilometers of de-watered reaches resulting from the operation of eight hydropower plants in 2006 (Anderson et al. 2007). Although there are more small, water diversion– type hydropower plants proposed for Costa Rican rivers, the government’s development focus since the turn of the twentyfirst century has started to favor larger dam projects. The social and ecological implications of these projects, as with other large dams, are more complex and far-reaching than those of small, water diversion hydropower plants (World Commission on Dams 2000; McCully 2001). The most noteworthy of the large dam projects is the Diquís Hydropower Project currently proposed by the ICE in southern Costa Rica. The original scheme for this project was first proposed in the 1970s (Reisner and McDonald 1986); since then the project has been presented and retracted from national electricity sector plans in multiple forms. Past schemes of the project proposed the location of the dam to be downstream of the confluence of the Coto Brus and

Fig. 18.18 Mountain mullet, Agonostomus monticola, a migratory fish species whose distribution is disrupted by dams. Photo by E. Anderson.

Fig. 18.19 Theraps underwoodi (Chichlidae) has been characterized as an equilibrium species whose presence may be a good indication of whether hydropower plants leave sufficient water for Neotropical stream fishes. From Anderson et al. 2006a; photo by E. Anderson.

646 Chapter 18 Fig. 18.20 Location of the Sarapiquí River Basin on Costa Rica’s Caribbean Slope. This is one of the most developed watersheds in terms of hydropower plants. Inset photo of Sarapaquí taken near La Virgen. Inset photo by E. Anderson.

General Rivers. These plans were criticized on the basis of projected environmental and social impacts: the dam would have flooded a large area of tropical forest and agricultural lands in an area inhabited by native communities and sedimentation behind the proposed dam was likely to affect the long-term utility of the project. The current plan for the Diquís Hydropower Project has taken these considerations into account and has relocated the project site to the General River, near the town of Buenos Aires. If completed as currently envisioned, the project will create a deep reservoir behind a 150 meter-high dam on the General River and will generate approximately 632 megawatts of electricity ( J. Picado, Instituto Costarricense de Electricidad [ICE], pers. comm.). In terms of installed generation capacity, this project will be the largest in Central America. The strong possibility that the Diquís Hydropower Project will be constructed, as well as other current trends, suggests that hydropower will continue to be the primary source of electricity for Costa Rica well into the future. Construction of dams in Costa Rica and throughout Central America is expected to escalate over the next two decades in response to expanding human populations, increased rural electrification, and growing demands for electricity (Scatena 2004). In fact, a report by the Conservation Strategy Fund (2005) documented approximately 400 potential new hydropower projects, in various stages of study from feasibility to investment opportunity (Burgues-Arrea 2005).

In this economic climate, the Diquís Hydropower Project would help reinforce Costa Rica’s role as a regional leader in hydropower development. Land Use Conversion

With much of the country’s original forest having been cleared in the latter half of the twentieth century (e.g., see Janzen and Hallwachs, chapter 10 of this volume), rivers in Costa Rica today drain a mosaic of pastures, croplands, and urban areas, interspersed with patches of remnant natural forest and secondary growth (Fig. 18.21). Based on their position in the landscape, rivers and streams are on the receiving end of the changes in land cover and land use that have occurred (Fig. 18.3). Increasingly, conversion from one agricultural land use to another, or from one crop to another, is a trend that can be observed throughout Costa Rica. For example, on the country’s Caribbean slope, large areas originally covered by tropical forest were cleared for cattle pastures during the period 1960– 1980; these pasturelands were then converted to banana plantations in the 1990s (Vargas 1995) or, more recently, to pineapple plantations (Fagan et al. 2013). The Tempisque River Basin also presents an interesting example of changing land use patterns that have occurred over the past half-century: in the 1950s, natural forest and pasture each covered approximately half of the land area of the

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basin. By the year 2000 croplands, which were almost nonexistent in 1950, comprised a significant area of the basin (roughly 25%), with rice being one of the dominant crops in terms of land area and economic importance to the region. Since then, sugarcane has emerged as a more lucrative crop and many rice fields in the Tempisque River Basin are now being converted to sugarcane (Jiménez et al. 2005; Jiménez, chapter 20 of this volume). What do all of these changes in land cover and land use mean for the structure and function of river ecosystems in Costa Rica? In general, agricultural land uses in Costa Rica have been linked to water pollution from sediment, agricultural chemicals, and animal waste. However, specific effects depend on the type, intensity, and location of the agricultural land use, and the ecological consequences of some land uses pose more of a threat to river ecosystems than others. For example, forest clearing for pasture has been linked not only to increased stream sediment loads, but also

to the increased presence of fecal coliforms in stream waters from cattle. The ecological effects of banana agriculture on river ecosystems may present more cause for concern than pastures (Castillo et al. 2006, Grant et al. 2013). Banana plantations usually involve major modifications to the way in which water moves through the landscape through the construction of canals that channelize runoff; agricultural chemicals, mainly fungicides, are also applied in large quantities to bananas through aerial spraying and ground application (Castillo et al. 1997, 2000). Both of these actions influence the quantity and quality of regional water resources (Vargas 1995, Castillo et al. 2006). Like bananas, rice plantations also usually contain a network of canals that supply the fields with irrigation water. The cocktail of chemicals applied to rice negatively affects the quality of water in rivers adjacent to or downstream from rice plantations (Rizo-Patron 2005). Pineapple and sugarcane are also highly chemically-intensive crops.

Fig. 18.21 Examples of land cover and land use change in Costa Rica: (a) forest; (b) forest clearing; (c) pineapple plantation; (d) cattle grazing; and (e) banana plantation.

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Concessions for Water

Expanding human populations, agriculture, and a growing tourism industry exert increasing pressure on the quantity of surface water resources in Costa Rica. Concessions for surface water are processed by the Departamento de Aguas of the Ministry of Environment and Energy (MINAE). However, demands for water for domestic and commercial uses are not always in line with real needs, nor is the real value of water incorporated in the price typically paid for the concession, though some exceptions exist (Barrantes Moreno 2006). Further, concessions for water often exceed available water supply in some areas or during certain parts of the year. The cases of the Tempisque River Basin and the Monteverde region illustrate how concessions for water are affecting the quantity of surface water resources in Costa Rica and the potential for conflicts in areas where water scarcity is anticipated in the future. The Tempisque River Basin, the largest in Costa Rica in terms of land area, covers more than half of the province of Guanacaste and approximately 10% of Costa Rica’s national territory. The basin drains a mosaic of agricultural, urban, and forested areas with a highly seasonal climate that includes marked differences in precipitation and river discharge between wet and dry periods. Diverse economic activities, such as the cultivation of rice, sugarcane, and tilapia, depend on the basin’s water resources, as does the tourism industry of the northern Pacific coast. These water users draw from both surface and groundwater resources, and water demands for cropland irrigation, aquaculture, and commercial uses (tourism) often exceed natural supply. For example, to date more than 20 m3 /s of water from the Tempisque River has been legally concessioned; this amount is nearly triple the mean discharge during most of the dry season (February– April), estimated at 7 m3 /s (Jiménez et al. 2005). In addition, plans to construct a water supply dam on the upper Tempisque River have been presented as a means for meeting projected water demands of tourismrelated developments on the northern Pacific coast; this project would only exacerbate existing pressures on water resources in the basin (J. Calvo, Instituto Tecnológico de Costa Rica [ITCR], pers. comm.). Scientists concerned about the ecological implications that current and future concessions of water may have on aquatic ecosystems of the basin initiated a process in 2003 to develop environmental flow recommendations for the Tempisque River, based on the needs of two common riverine species: Crocodilus acutus and Parachromis dovii (Jiménez et al. 2005). In the area of Monteverde, local protests erupted in 2004 when a group of local businessmen were granted a con-

cession to draw water from the La Cuecha stream. Water rights were formally solicited for irrigation of crops and grasslands; however, some Monteverde residents claimed that the businessmen were actually planning to use the water for other purposes that might include creation of tilapia farms or development of a hotel or other tourism-related infrastructure. In January 2005, opponents blocked roads and hindered construction of a pipeline that would draw water from the La Cuecha stream, arguing that water withdrawals would threaten the integrity of natural resources in the Monteverde area and that an appropriate environmental impact assessment had not been completed (Tico Times, January 28, 2005). Non-native Fish Introductions

After habitat destruction, non-native species introductions are a principal cause of imperilment and extinction of freshwater fishes worldwide. Exotic fish introductions, in particular tilapiine fishes (generally known as tilapias), have the potential to influence community and population dynamics of freshwater biota in Costa Rican streams. Native to Africa and the southwestern Middle East, tilapias (Family: Cichlidae) are now pan-tropically distributed following intentional and unintentional introductions most often associated with aquaculture projects (Canonico et al. 2005). Two species, Oreochromis mossambicus and Oreochromis aereus, were introduced to Costa Rica in the 1960s for small-scale rural aquaculture; an additional tilapia species, O. niloticus, was introduced in 1979 (Fitzsimmons 2000). Tilapia production surged in Costa Rica (and worldwide) during the 1990s, as aquaculture practices intensified. By 1998, tilapia farms in Costa Rica produced >6,000 metric tons of tilapia annually, and the country was home to one of the single largest tilapia aquaculture operations in the Americas near the city of Cañas (Fitzsimmons 2000). Alongside Honduras and Ecuador, Costa Rica is now among the top exporters in the Americas of tilapia to international markets. In 2002, Costa Rica produced an estimated 17,000 metric tons of farmed tilapia and an increase in production to 21,000 metric tons is projected by 2010 (Fitzsimmons 2000, 2004). Tilapia introductions have been linked to the decline of native species in freshwater systems throughout the tropics. These unintended consequences relate to the fact that the same characteristics that make tilapia good for aquaculture virtually predispose them to success as an invasive species (Canonico et al. 2005). Tilapia are fast growing, and widely tolerant of a range of environmental conditions such as salinity, dissolved oxygen, and temperature. They also have

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the ability to feed at different trophic levels. The reproductive biology of tilapia also gives them an advantage over native cichlid fishes in many places (van Breukelen 2015). Tilapia have short reproductive cycles and spawn year round, and Oreochromis practice parental care through mouthbrooding, which allows them to protect their young and easily colonize new habitats. Genetic effects of introduced tilapia on native cichlids are also a concern, as is habitat alteration and eutrophication caused by waste produced in cage farming. Little information documenting the current range of tilapias in Costa Rica is available. Since 1990 tilapias have been commonly found along the San Juan River drainage from Lake Nicaragua to the Caribbean Sea. These tilapias were presumably escapees following stocking of Lake Nicaragua during the 1980s (McKaye et al. 1995). It is assumed tilapia inhabit major tributaries of the San Juan River (like the Sarapiquí and San Carlos Rivers) and it is highly likely that other drainages harbor tilapia as well, particularly those of the Guanacaste region where many intensive tilapia farms are located. While long-term effects of the presence and spread of tilapia on river ecosystems in Costa Rica remains to be seen, predictions are not good based on experiences from other countries, which have shown that native cichlid populations often decline in the presence of introduced tilapias (McKaye et al. 1995; Canonico et al. 2005).

Future Perspective Importance of Conserving the Biointegrity of Costa Rican Rivers

There is clearly a strong need for integrated management of water resources and concerted efforts to balance human demands for water with the needs of aquatic ecosystems. Very little infrastructure for monitoring basic water quality parameters exists in Costa Rica. It is hoped that the information provided in this chapter will provide a foundation to inspire efforts to ensure riverine biointegrity throughout the country. Monitoring programs, adaptive management, and creative solutions are needed to balance the many demands that humanity is placing on these running water ecosystems. The previous section (People and Nature) exemplifies the types of development issues and conflicts likely to dominate the future agenda of water resources management in many parts of Costa Rica. Issues range from river fragmentation associated with dam construction to land use changes, water withdrawals, and displacement of native biota by exotic species (e.g., see TNC 2009). Tradeoffs between development and environmental effects must be carefully consid-

ered. What are the cumulative effects of dam construction within a river’s drainage on migratory stream biota, fisheries, potable water supply, and ecotourism? How will future changes in land use within specific watersheds affect nonpoint source nutrient and pesticide inputs into rivers— and how will this affect stream biota and human communities? To what extent will excessive water withdrawals from rivers, which are being facilitated by concessions for water (and often granted on the basis of demand rather than supply), reduce river discharge and compromise the ability of rivers to provide key ecosystem goods and services (e.g., waste assimilation, transportation, fish) upon which residents of Costa Rica rely? Conclusions: Research Needs

As this chapter illustrates, while our understanding of Costa Rican river ecosystems is growing there are many gaps in our knowledge, ranging from lack of information at the species level (regarding basic natural history) to population-, community-, and ecosystem-level information. Nonetheless, Costa Rica stands out, given the amount of information on rivers that is available relative to many other tropical countries. It is widely acknowledged among freshwater ecologists that we have a limited understanding of how tropical rivers function relative to our knowledge of temperate streams and rivers (Pringle 2000, Ramírez et al. 2008). Ecological and hydrological characteristics of tropical rivers are wideranging and often very different from temperate streams. It is unwise to extend paradigms generated from temperate stream research to the tropics without ample data— particularly with respect to conservation and management decisions. For example, the applicability of hydropower technology developed for rivers in the temperate zone must be evaluated with respect to differing hydrological and biological features in tropical Costa Rican rivers (Pringle et al.2000). There is clearly a critical need for studies on the ecological consequences of dam construction in Costa Rica although some inroads have been made (see Anderson et al. 2006a,b, 2007). Developing new methods for assessing and monitoring water quality for tropical rivers is also important (but see Springer et al. 2007, Umaña-Villalobos and Springer 2006), since biological and chemical indices of water quality developed for temperate zone systems are often not appropriate. Further discussion on priority research and management needs for tropical rivers in general can be found in Pringle (2000), which provides a comprehensive review of river conservation in Latin America and the Caribbean.

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Acknowledgments The authors gratefully acknowledge the support of the National Science Foundation (NSF), which has almost continually supported the STREAMS project in lowland

Costa Rica since 1987 through the following awards: BSR87– 17746, BSR-91– 07772, DEB9528434, DEB0075339, and DEB0545463. The Organization for Tropical Studies (OTS) has provided continuous strong logistical support, which has made our research in Costa Rica possible.

References Allsteadt, J., and C. Vaughan. 1988. Ecological studies of the Central American caiman (Caiman crocodilus fuscus) in Caño Negro Wildlife Refuge, Costa Rica. Bulletin of the Chicago Herpetological Society 23: 123– 26. Allsteadt, J., and C. Vaughan. 1992. Population status of Caiman crocodilus (Crocodylia: Alligatoridae) in Caño Negro, Costa Rica. Brenesia 38: 57– 64. Anderson, E.P., M.C. Freeman, and C.M. Pringle. 2006a. Ecological consequences of hydropower development in Central America: impacts of small dams and water diversion on neotropical stream fish assemblages. River Research and Applications 22: 397– 411. Anderson, E.P., C.M. Pringle, and M. Rojas. 2006b. Transforming tropical rivers: an environmental perspective on hydropower development in Costa Rica. Aquatic Conservation: Marine and Freshwater Systems 16: 679– 93. Anderson, E.P., C.M. Pringle, and M.C. Freeman. 2008. Quantifying the cumulative extent of river fragmentation by dams in the Sarapiquí River Basin, Costa Rica: a first step towards evaluating environmental tradeoffs. Aquatic Conservation: Marine and Freshwater Systems 18: 408– 17. Ardón, M., and C.M. Pringle. 2007. The quality of organic matter mediates the response of heterotrophic biofilms to phosphorus enrichment of the water column and substratum. Freshwater Biology 52: 1762– 72. Ardón, M., and C.M. Pringle. 2008. Do secondary compounds inhibit microbial- and insect-mediate leaf breakdown in a tropical rainforest stream, Costa Rica? Oecologia 155: 311– 23. Ardón, M., C.M. Pringle, and S.L. Eggert. 2009. Does leaf chemistry differentially affect breakdown in tropical versus temperate streams?: importance of using standardized analytical techniques to measure leaf chemistry. Journal of the North American Benthological Society 28: 440– 53. Ardón, M., L.A. Stallcup, and C.M. Pringle. 2006. Does leaf quality mediate the stimulation of leaf breakdown by phosphorus in Neotropical streams? Freshwater Biology 51: 618– 33. Ardón, M., J.H. Duff, A. Ramírez, G.E. Small, A.P. Jackman, F.J. Triska, and C.M. Pringle. 2013. Experimental acidification of two biogeochemically-distinct neotropical streams: buffering mechanisms and macroinvertebrate drift. Science of the Total Environment 443: 267– 77. Banack, S.A., M.H. Horn, and A. Gawlicka. 2002. Disperser- vs. establishment-limited distribution of a riparian fig tree (Ficus insipida) in a Costa Rican tropical rain forest. Biotropica 34: 232– 43. Barbee, N.C. 2005. Grazing insects reduce algal biomass in a neotropical stream. Hydrobiologia 532: 153– 65. Barrantes Moreno, G. 2006. Economic valuation of water supply as a key environmental service provided by montane oak forest wa-

tershed areas in Costa Rica. In M. Kappelle, ed., Ecology and Conservation of Neotropical Montane Oak Forests, 436– 46. Ecological Studies Series, vol. 185. New York: Springer Verlag. Benstead, J.P. 1996. Macroinvertebrates and the processing of leaf litter in a tropical stream. Biotropica 28: 367– 75. Benstead, J.P., J.G. March, C.M. Pringle, and F.N. Scatena. 1999. Effects of a low-head dam and water abstraction on migratory tropical stream biota. Ecological Applications 9: 656– 68. Bixby, R.J., U. Wydrzycka, and C.M. Pringle. 2005. Diatom assemblages as indicators of solute levels in lowland Neotropical streams. Bulletin of the North American Benthological Society 22: 425– 26. Bourrelly, P., and E. Manguin. 1952. Algues d’Eau Douce de la Guadeloupe et Dépendances. Centre National de la Recherche Scientifique. Paris: Société d’Edition d’Enseignement Supérieur. 281 pp. Boyero, L., and J. Bosch. 2002. Spatial and temporal variation of macroinvertebrate drift in two neotropical streams. Biotropica 34: 567– 74. Brandon, C. 1983. Noctilio leporinus. In D.H. Janzen, Costa Rican Natural History, 480– 81. Chicago: University of Chicago Press. Brookshire, E.N.J., L.O. Hedin, J.D. Newbold, D.M. Sigman, and J.K. Jackson. 2012. Sustained losses of bioavailable nitrogen from montane tropical forests. Nature Geoscience 5: 123– 126. Brookshire, E.N.J., S. Gerber, D.N.L. Menge, and L. Hedin. 2012b. Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation. Ecology Letters 15:9– 16. Burcham, J. 1980. Fish communities and environmental characteristics of two lowland streams in Costa Rica. Revista de Biología Tropical 36: 273– 85. Burgues-Arrea, I. 2005. Inventario de Proyectos de Infraestructura en Mesoamérica. Conservation Strategy Fund, Proyecto: Integración de la Infraestructura y la Conservación de la Biodiversidad en Mesoamérica. Fondo de Alianzas para los Ecosistemas Críticos, The Nature Conservancy ( TNC). Bussing, W.A. 1993. Fish communities and environmental characteristics of a tropical rainforest river in Costa Rica. Revista de Biología Tropical 41: 791– 809. Bussing, W.A. 1994. Ecological aspects of the fish community. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, 195– 98. Chicago: University of Chicago Press. Bussing, W.A. 1998a. Peces de las aguas continentales de Costa Rica. Editorial de la Universidad de Costa Rica. Bussing, W.A. 1998b. Freshwater fishes of Costa Rica. Revista de Biología Tropical 46(Suppl. 2): 1– 458. Butterfield, R.P. 1994. The regional context: land colonization and conservation in Sarapiquí. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural

Rivers of Costa Rica 651 History of a Neotropical Rain Forest, 299– 306. Chicago: University of Chicago Press. Calvert, P.P. 1915. Studies on Costa Rican Odonata, VI— The waterfalldwellers: the transformation, external features, and attached diatoms of Thaumatoneura larva. Entomological News 26: 295– 305. Canonico, G.C., A. Arthington, J.K. McCrary, and M.L. Thieme. 2005. The effects of introduced tilapias on native biodiversity. Aquatic Conservation: Marine and Freshwater Systems 15: 463– 83. Capps, K. A., and A. S. Flecker. 2013. Invasive aquarium fish transform ecosystem nutrient dynamics. Proceedings of the Royal Society B 280: 20131520. Castillo, L.E., E. de la Cruz, and C. Ruepert. 1997. Ecotoxicology and pesticides in tropical aquatic ecosystems of Central America. Environmental Toxicology and Chemistry 16(1): 41– 51. Castillo, L.E., E. Martínez, C. Ruepert, C. Savage, M. Gilek, M. Pinnock, and E. Solís. 2006. Water quality and macroinvertebrate community response following pesticide applications in a banana plantation, Limón, Costa Rica. Science of the Total Environment 367: 418– 32. Castillo, L.E., C. Ruepert, and E. Solis. 2000. Pesticide residues in the aquatic environment of banana plantation areas in the North Atlantic zone of Costa Rica. Environmental Toxicology and Chemistry 19: 1942– 50. Cedeño-Obregón, F. 1986. Contribución al conocimiento de los camarones de agua dulce de Costa Rica. Colección perteneciente al Museo de Zoología de la Escuela de Biología de la Universidad de Costa Rica. Lic. San Pedro de Montes de Oca, Costa Rica: Universidad de Costa Rica. CFIA. 2005. Panorama Nacional y Regional de la Industria Eléctrica. Colegio Federado de Ingenieros y Arquitectos de Costa Rica (CFIA). Accessed December 2005. http://www.cfia.or.cr/informes.htm. Chace, F.A., and H.H. Hobbs. 1966. The freshwater and terrestrial decapod crustaceans of the West Indies with special reference to Dominica. United States National Museum Bulletin 292: 1– 258. Chandler, M., L.J. Chapman, and C.A. Chapman. 1995. Patchiness in the abundance of metacercariae parasitizing Poecilia gilli (Poecilidae) isolated in pools of an intermittent tropical stream. Environmental Biology of Fishes 42: 313– 21. Colon-Gaud, C., M. Whiles, S.S. Kilham, K.R. Lips, C.M. Pringle, S. Connelly, and S. Peterson. 2009. Assessing ecological responses to catastrophic amphibian declines: patterns of macroinvertebrate production and food web structure in upland Panamanian streams. Limnology and Oceanography 54: 331– 43. Connelly, S., C.M. Pringle, R.J. Bixby, R. Brenes, M. Whiles, K.R. Lips, S.S. Kilham, and A.D. Huryn. 2008. Changes in stream primary producer communities resulting from large-scale catastrophic amphibian declines: Can small-scale experiments predict effects of tadpole loss? Ecosystems 8: 1262– 76. Crook, K.E., C.M. Pringle, and M. C. Freeman. 2009. A method to assess longitudinal riverine connectivity in tropical streams dominated by migratory biota. Aquatic Conservation 19: 714– 23. Dixon, J.R., and M.A. Staton. 1983. Caiman crocodilus. In DH. Janzen, ed., Costa Rican Natural History, 387– 88. Chicago: University of Chicago Press. Drewe, K.E., M.H. Horn, K.A. Dickson, and A. Gawlicka. 2004. Insectivore to frugivore: ontogenetic changes in gut morphology and digestive enzyme activity in the characid fish Brycon guatemalensis. Journal of Fish Biology 64: 890– 902.

Duff, J.H., C.M. Pringle, and F.J. Triska. 1996. Nitrate reduction in sediments of lowland tropical streams draining swamp forest in Costa Rica: an ecosystem perspective. Biogeochemistry 33: 179– 96. Duft, M., K. Fittkau, and W. Traunspurger. 2002. Colonization of exclosures in a Costa Rican stream: effects of macrobenthos on meiobenthos and the nematode community. Journal of Freshwater Ecology 17: 531– 41. Fagan, M.E., R.S. DeFries, S.E. Sesnie, J.P. Arroyo, W. Walker, C. Soto, R.L. Chazdon, and A. Sanchun. 2013. Land cover dynamics following a deforestation ban in northern Costa Rica. Environmental Research Letters 8(3): 034017. Finlay, B.J., E.B. Monaghan, and S.C. Maberly. 2002. Hypothesis: the rate and scale of dispersal of freshwater diatom species is a function of their global abundance. Protist 153: 261– 73. Fitzsimmons, K. 2000. Future trends of tilapia aquaculture in the Americas. In B.A. Costa-Pierce and J.E. Rakocy, eds., Tilapia Aquaculture in the Americas, vol. 2, 252– 64. Baton Rouge, LA: The World Aquaculture Society. Fitzsimmons, K. 2004. Development of new products and markets for the global tilapia trade. In R. Bolivar, G. Mair, and K. Fitzsimmons, eds., Proceeding of the Sixth International Symposium on Tilapia in Aquaculture, 624– 33. Manila, Philippines: BFAR. Flowers, R.W. 1992. Review of the genera of mayflies of Panama with a checklist of Panamanian and Costa Rican species (Ephemeroptera). In D. Quintero and A. Aiello, eds., Insects of Panama and Mesoamerica: Selected Studies, 37– 51. Oxford, England: Oxford University Press. Flowers, R.W., and C. De la Rosa. 2010. Ephemeroptera. Revista de Biologia Tropical 58(Suppl. 4): 63– 93. Food and Agriculture Organization (FAO). 2005. Dirección de Fomento de Tierras y Aguas. AQUASTAT, Costa Rica. Accessed December 10, 2005. http://www.fao.org/ag/agl/aglw/aquastat /countries/costa_ rica/indexesp.stm. Fureder, L. 1994. Drift patterns in Costa Rica streams. PhD thesis, Innsbruck University. Austria. Ganong, C.N., G.E. Small, M. Ardón, W.H. McDowell, D.P. Genereux, J.H. Duff, and C.M. Pringle. 2015. Interbasin flow of geothermally modified ground water stabilizes stream exports of biologically important solutes against variation in precipitation. Freshwater Science 34 (1): 276– 86. García-Guerrero, M. U., F. Becerril-Morales, F.Vega-Villasante, and L.D. Espinosa-Chaurand, 2013. Los langostinos del género Macrobrachium con importancia económica y pesquera en América Latina: conocimiento actual, rol ecológico y conservación. Latin American Journal of Aquatic Research 41: 651– 75. Genereux, D.P., S.J. Wood, and C.M. Pringle. 2002. Chemical tracing of interbasin groundwater transfer in the lowland rainforest of Costa Rica. Journal of Hydrology 258: 163– 78. Gómez, L.D. 1984. Las Plantas Acuáticas y Anfíbios de Costa Rica y Centroamérica. I. Liliopsida. San José, Costa Rica: EUNED. 430 pp. Goulding, M. 1980. The Fishes and the Forest: Explorations in Amazonian Natural History. University of California, Berkeley. Grant, P. B., Woudneh, M. B., & Ross, P. S. 2013. Pesticides in blood from spectacled caiman (Caiman crocodilus) downstream of banana plantations in Costa Rica. Environmental Toxicology and Chemistry 32: 2576– 83. Greathouse, E.A., C.M. Pringle, and J.G. Holmquist. 2006a. Conser-

652 Chapter 18 vation and management of migratory fauna and dams in tropical streams of Puerto Rico. Aquatic Conservation 16: 695– 712. Greathouse, E.A., C.M. Pringle, W.H. McDowell, and J.G. Holmquist. 2006b. Indirect upstream effects of dams: consequences of migratory consumer extirpation in Puerto Rico. Ecological Applications 16: 339– 52. Gutiérrez-Fonseca, P.E., and M. Springer. 2011. Description of the final instar nymphs of seven species from Anacroneuria Klapálek (Plecoptera: Perlidae) in Costa Rica, and first record for an additional genus in Central America. Zootaxa 2965: 16– 38. Hartshorn, G., L. Hartshorn, A. Atmella, L.D. Gómez, A. Mata, R. Morales, R. Ocampo, D. Pool, C. Quesada, C. Solera, R. Solorzano, G. Stiles, J. Tosi, A. Umaña, C. Villalobos, and R. Wells. 1982. Costa Rica Country Environmental Profile: A Filed Study. San José, Costa Rica: Tropical Science Center. Henley, R.W., and J. Ellis. 1983. Geothermal systems, ancient and modern. Earth Science Reviews 19: 1– 50. Holmquist, J.G., J.M. Schmidt-Gengenbach, and B.B. Yoshioka. 1998. High dams and marine-freshwater linkages: effects on native and introduced fauna in the Caribbean. Conservation Biology 12: 621– 30. Holzenthal, R.W. 1988. Catálogo sistemático de los Tricópteros de Costa Rica. Brenesia 29: 51– 82. Horn, B.W., and R.W. Lichtwardt. 1981. Studies on the nutritional relationship of larval Aedis aegypti (Diptera: Culicidae) with Smittium culisetae (Trichmycetes). Mycologia 73: 724– 940. Horn, M.H. 1997. Evidence for dispersal of fig seeds by the fruit-eating characid fish Brycon guatemalensis Regan in a Costa Rican tropical rain forest. Oecologia 109: 259– 64. Instituto Costarricense de Electricidad (ICE). 2004. Plan de la Expansión de la Generación Eléctrica. San Jose, Costa Rica: ICE. Instituto Costarricense de Electricidad (ICE). 2009. Déjenos contarle, revista informativa del Proyecto Hidroeléctrico El Diquís. Costa Rica: ICE. 15 pp. Irons, J.G., M.W. Oswood, R.J. Stout, and C.M. Pringle. 1994. Latitudinal patterns in leaf litter breakdown: is temperature really important? Freshwater Biology 32: 401– 11. Jackson, J.K., and B.W. Sweeney. 1995. Egg and larval development times for 35 species of tropical stream insects from Costa Rica. Journal of the North American Benthological Society 14: 115– 30. Janzen, D.H. 1975. Tropical blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6: 69– 103. Janzen, D.H. 1983. Costa Rican Natural History. Chicago: University of Chicago Press. 816 pp. Jiménez, J.A., J. Calvo, F. Pizarro, and E. González. 2005. Conceptualización de caudal ambiental en Costa Rica: Determinación inicial para el Río Tempisque. San José, Costa Rica: UICN-Mesoamerica. 42 pp. Kilroy, C., B.J.F. Biggs, and W. Vyverman. 2007. Rules for macroorganisms applied to micoorganisms: patterns of endemism in benthic freshwater diatoms. Oikos 116: 550– 64. Kociolek, J.P., and S.A. Spaulding. 2000. Freshwater diatom biogeography. Nova Hedwigia 71: 223– 41. Krammer, K., and H. Lange-Bertalot. 1986. Bacillariophyceae 1. Teil: Naviculaceae. In H. Ettl, J. Gerloff, H. Heynig, and D. Mollenhauer, eds., Süsswasserflora von Mitteleuropa 2/1: 1– 876. Jena, Germany: Gustav Fischer Verlag. La Marca, E., K.R. Lips, S. Lotters, R. Puschendorf, R. Ibañez, J.V. Rueda-

Almonacid, R. Schulte, C. Marty, F. Castro, J. Manzanilla-Puppo, J.E. García-Perez, F. Bolaños, G. Cháves, J.A. Pounds, E. Toral, and B.E. Young. 2005. Catastrophic population declines and extinctions in neotropical harlequin frogs (Bufonidae: Atelopus). Biotropica 37: 190– 201. Lara, L.R., I.S. Wehrtmann, C. Magalhães, and F.L. Mantelatto. 2013. Species diversity and distribution of freshwater crabs (Decapoda: Pseudothephusidae) inhabiting the basin of the Río Grande de Térraba, Pacific slope of Costa Rica. Latin American Journal of Aquatic Research 41:685– 95. Lichtwardt, R.W. 1997. Costa Rican gut fungi ( Trichomycetes) infecting lotic insect larvae. Revista de Biología Tropical 45: 1349– 83. Ligon, S. 1983. Trichechus manatus. In D.H. Janzen, ed., Costa Rican Natural History. Chicago: University of Chicago Press. Lips, K.R. 1998. Decline of a tropical montane amphibian fauna. Conservation Biology 12: 106– 17. Lips, K.R. 1999. Mass mortality and population declines of anurans at an upland site in western Panama. Conservation Biology 13: 117– 25. Lips, K.R. 2001. Reproductive trade-offs and bet-hedging in Hyla calypso, a Neotropical treefrog. Oecologia 128:509– 18. Lips, K.R., D.E. Green, and R. Papendick. 2003. Chytridiomycosis in wild frogs from southern Costa Rica. Journal of Herpetology 37: 215– 18. Lyons, J., and D.W. Schneider. 1990. Factors influencing fish distribution and community structure in a small coastal river in southwestern Costa Rica. Hydrobiologia 203: 1– 14. Magalhães, C., L.R. Lara, and I.S. Wehrtmann. 2010. A new species of freshwater crab of the genus Allacanthos (Crustacea, Decapoda, Pseudothelphusidae) from southern Costa Rica, Central America. Zootaxa 2604: 52– 60. Mann, D.G., and S.J.M. Droop. 1996. Biodiversity, biogeography and conservation of diatoms. Hydrobiologia 336: 19– 32. March, J.G., J.P. Benstead, C.M. Pringle, and F.N. Scatena. 2003. Damming tropical island streams: problems, solutions, and alternatives. BioScience 53: 1069– 78. March, J.G., C.M. Pringle, M.J. Townsend, and A.I. Wilson. 2002. Effects of freshwater shrimp assemblages on benthic communities along an altitude gradient of a tropical island stream. Freshwater Biology 47: 1– 14. McCully, P. 2001. Silenced Rivers: The Ecology and Politics of Large Dams. London: Zed Books. 359 pp. McKaye, K.R., J.D. Ryan, J.R. Stauffer, L.J.L. Pérez, G.I. Vega, and E.P. van den Berghe. 1995. African tilapia in Lake Nicaragua: ecosystem in transition. Bioscience 45: 406– 11. Metzeltin, D., and H. Lange-Bertalot. 1998. Tropical diatoms of South America I. Bibliotheca Diatomologica 5: 1– 695. Metzeltin, D., and H. Lange-Bertalot. 2002. Diatoms from the “Island Continent” Madagascar. Iconographia Diatomologica 11: 1– 286. Michels, A. 1998a. Effects of sewage water on diatoms (Bacillariophyceae) and water quality in two tropical streams in Costa Rica. Revista de Biología Tropical 46(Suppl. 6): 153– 75. Michels, A. 1998b. Use of diatoms (Bacillariophyceae) for water quality assessment in two tropical streams in Costa Rica. Revista de Biología Tropical 46(Suppl. 6): 143– 52. Michels, A., G. Umaña, and U. Raeder. 2006. Epilithic diatom assemblages in rivers draining into Golfo Dulce (Costa Rica) and their relationship to water chemistry, habitat characteristics and land use. Archiv für Hydrobiologie 165: 167– 90.

Rivers of Costa Rica 653 Moll, D., and K.P. Jansen. 1995. Evidence for a role in seed dispersal by two tropical herbivorous turtles. Biotropica 27: 121– 27. Moser, G., H. Lange-Bertalot, and D. Metzeltin. 1998. Insel der Endemiten-Geobotanisches Phänomen Neukaledonien. Bibliotheca Diatomologica 38: 1– 464. Newbold, J.D., B.W. Sweeney, J.K. Jackson, and L.A. Kaplan. 1995. Concentrations and export of solutes from six mountain streams in northwestern Costa Rica. Journal of the North American Benthological Society 14: 21– 37. Paaby, P., and C.R. Goldman. 1992. Chlorophyll, primary productivity, and respiration in a lowland Costa Rican stream. Revista de Biología Tropical 40: 185– 88. Power, M.E. 1990. Effects of fish in river food webs. Science 250: 811– 14. Pringle, C.M. 1997. Exploring how disturbance is transmitted upstream: going against the flow. Journal of the North American Benthological Society 16: 425– 38. Pringle, C.M. 2000. Riverine conservation in tropical versus temperate regions: ecological and socioeconomic considerations. In P. J. Boon, B. Davies, and G. Petts, eds., Global Perspectives on River Conservation: Science Policy and Practice, chap. 15, 367– 78. New York: John Wiley and Sons. Pringle, C.M., and T. Hamazaki. 1997. Effects of fishes on algal response to storms in a tropical stream. Ecology 78: 2432– 42. Pringle, C.M., and T. Hamazaki. 1998. The role of omnivory in a neotropical stream: separating diurnal and nocturnal effects. Ecology 79: 269– 80. Pringle, C.M., P. Paaby-Hansen, P.D. Vaux, and C.R. Goldman. 1986. In situ nutrient assays of periphyton growth in a lowland Costa Rican stream. Hydrobiologia 134: 207– 13. Pringle, C.M., and A. Ramírez. 1998. Use of both benthic and drift sampling techniques to assess tropical stream invertebrate communities along an altitudinal gradient, Costa Rica. Freshwater Biology 39: 359– 73. Pringle, C.M., G.L. Rowe, F.J. Triska, J. Fernández, and J. West. 1993. Landscape linkages between geothermal activity and solute composition and ecological response in surface waters draining the Atlantic slope of Costa Rica. Limnology and Oceanography 38: 753– 74. Pringle, C.M., and F.N. Scatena. 1999a. Factors affecting aquatic ecosystem deterioration in Latin America and the Caribbean. In U. Hatch and M.E. Swisher, eds., Tropical Managed Ecosystems: New Perspectives on Sustainability, 104– 13. Oxford: Oxford University Press. Pringle, C.M., and F.N. Scatena. 1999b. Freshwater resource development: case studies from Puerto Rico and Costa Rica. In U. Hatch and M.E. Swisher, eds., Tropical Managed Ecosystems: New Perspectives on Sustainability, 114– 21. Oxford: Oxford University Press. Pringle, C.M., F. Scatena, P. Paaby, and M. Nuñez. 2000. River conservation in Latin America and the Caribbean. In P.J. Boon, B. Davies, and G. Petts, eds., Global Perspectives on River Conservation: Science, Policy and Practice, chap. 2, 39– 75. New York: John Wiley and Sons. Pringle, C.M., and F.J. Triska. 1991. Effects of geothermal groundwater on nutrient dynamics of a lowland Costa Rican stream. Ecology 72: 951– 65. Pringle, C.M., and F.J. Triska. 2000. Emergent biological patterns and surface-subsurface interactions at landscape scales. In J.B. Jones and P.J. Mulholland, eds., Stream and Groundwaters, 167– 93. Academic Press.

Pringle, C.M., F.J. Triska, and G. Browder. 1990. Spatial variation in basic chemistry of streams draining a volcanic landscape on Costa Rica’s Caribbean slope. Hydrobiologia 206: 73– 85. Pringle, C.M., M. Freeman, and B. Freeman. 2000. Regional effects of hydrologic alterations on riverine macrobiota in the New World: Tropical-temperate comparisons. BioScience 50: 807– 23. Ramírez, A. 2010. Odonata. Revista de Biologia Tropical 58(Suppl. 4): 97– 136. Ramírez, A., P. Paaby, C.M. Pringle, and G. Aguero. 1998. Effect of habitat type on benthic macroinvertebrates in two lowland tropical streams, Costa Rica. Revista de Biología Tropical 46: 201– 13. Ramírez, A., D.R. Paulson, and C. Esquivel. 2000. Odonata of Costa Rica: diversity and checklist of species. Revista de Biología Tropical 48: 247– 54. Ramírez, A., and C.M. Pringle. 1998a. Invertebrate drift and benthic community dynamics in a lowland neotropical stream, Costa Rica. Hydrobiologia 386: 19– 26. Ramírez, A., and C.M. Pringle. 1998b. Structure and production of a benthic insect assemblage in a neotropical stream. Journal of the North American Benthological Society 17: 443– 63. Ramírez, A., and C.M. Pringle. 2001. Spatial and temporal patterns of invertebrate drift in streams draining a Neotropical landscape. Freshwater Biology 46: 47– 62. Ramírez, A., and C.M. Pringle. 2004. Do macroconsumers affect insect responses to a natural stream phosphorus gradient? Hydrobiologia 515: 235– 46. Ramírez, A., and C.M. Pringle. 2006. Fast growth and turnover of chironomid assemblages in response to stream phosphorus levels in a tropical lowland landscape. Limnology and Oceanography 51: 189– 96. Ramírez, A., C.M. Pringle, and M. Douglas. 2006. Temporal and spatial patterns in stream physicochemistry and insect assemblages in tropical lowland streams. Journal of the North American Benthological Society 25: 108– 25. Ramírez, A., C.M. Pringle, and L. Molina. 2003. Effects of stream phosphorus levels on microbial respiration. Freshwater Biology 48: 88– 97. Ramirez, A., C.M. Pringle, and K.M. Wantzen 2008. Tropical river conservation. In D. Dudgeon, ed., Tropical Stream Ecology, 285– 304. London: Academic Press, 316 pp. Ranvestel, A.W., K.R. Lips, C.M. Pringle, M.R. Whiles, and R.J. Bixby. 2004. Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshwater Biology 49: 274– 85. Reisner, M., and R.H. McDonald. 1986. The high costs of high dams. In A. Maguire and J.W. Brown, eds., Bordering on Trouble, 270– 307. MD: Adler & Adler for World Resources Institute. Rizo-Patron, F.L.S. 2005. Estudio de los arrozales del Proyecto Tamarindo: agroquimicos y macroinvertebrados bentónicos en relación al Parque Nacional Palo Verde, Guanacaste, Costa Rica. Tesis, Universidad Nacional. Heredia, Costa Rica. Rosemond, A.D., C.M. Pringle, and A. Ramírez. 1998. Macroconsumer effects on insect detritivores and detritus processing in a tropical stream. Freshwater Biology 39: 515– 24. Rosemond, A.D., C.M. Pringle, A. Ramírez, and M.J. Paul. 2001. A test of top-down and bottom-up control in streams. Ecology 82: 2279– 93.

654 Chapter 18 Rosemond, A.D., C.M. Pringle, A. Ramírez, M.J. Paul, and J.L. Meyer. 2002. Landscape variation in phosphorus concentration and effects on detritus-based tropical streams. Limnology and Oceanography 47: 278– 89. Sader, S., and A. Joyce. 1988. Deforestation rates and trends in Costa Rica, 1940– 1983. Biotropica 20: 11– 19. Savage, J.M. 2002. Amphibians and Reptiles of Costa Rica: A Herpetofauna between Two Continents, between Two Seas. Chicago: University of Chicago Press. 954 pp. Scatena, F.N. 2004. A survey of methods for setting the minimum instream flow standards in the Caribbean basin. River Research and Applications 20: 127– 35. Schneider, D.W., and J. Lyons. 1993. Dynamics of upstream migration in 2 species of tropical freshwater snails. Journal of the North American Benthological Society 12: 3– 16. Scott, N.J., and S. Limerick. 1983. Reptiles and amphibians. In D.H. Janzen, ed., Costa Rican Natural History, 351– 73. Chicago: University of Chicago Press. Sheath, R.G., D. Kaczmarczyk, and K.M. Cole. 1993a. Distribution and systematics of freshwater Hildenbrandia (Rhodophyta, Hildenbrandiales) in North America. European Journal of Phycology 28: 115– 21. Sheath, R.G., M.L. Vis, and K.M. Cole. 1993b. Distribution and systematics of freshwater Ceramiales (Rhodophyta) in North America. Journal of Phycology 29: 108– 17. Sherwood, A.R., and R.G. Sheath. 1999. Biogeography and systematics of Hildenbrandia (Rhodophyta, Hildenbrandiales) in North America: inferences from morphometrics, and rbcL and 18S gene sequence analyses. European Journal of Phycology 34: 523– 32. Silva-Benavides, A.M. 1996a. The epilithic diatom flora of a pristine and a polluted river in Costa Rica, Central America. Diatom Research 11: 105– 42. Silva-Benavides, A.M. 1996b. The use of water chemistry and benthic diatom communities for qualification of a polluted tropical river. Revista de Biología Tropical 44: 395– 416. Small, G.E., C.M. Pringle, M. Pyron, and J.H. Duff. 2011a. Role of the fish Astyanax aeneus (Characidae) as a keystone nutrient recycler in low-nutrient Neotropical streams. Ecology 92: 386– 97. Small, G.E., J.P. Wares, and C.M. Pringle. 2011b. Differences in phosphorus demand among detritivorous chironomid larvae reflect intraspecific adaptations to differences in food resource stoichiometry across lowland tropical streams. Limnology & Oceanography 56: 268– 78. Small, G.E., R.J. Bixby, C. Kazanci, and C. M. Pringle. 2011c. Partitioning stoichiometric components of epilithic biofilms using mixing models. Limnology and Oceanography: Methods 9: 185– 93. Small, G.E., P.J. Torres, L.M. Schweizer, J.H. Duff, and C.M. Pringle. 2013a. Importance of terrestrial arthropods as subsidies in lowland Neotropical rain forest stream ecosystems. Biotropica 45: 80– 87. Small, G.E., J.H. Duff, P.J. Torres, and C.M. Pringle. 2013b. Insect emergence as a nitrogen flux in Neotropical streams: comparisons with microbial denitrification across a stream phosphorus gradient. Freshwater Science 32:1178– 87. Snyder, M.N. 2012. Abundance, distribution, nutrient cycling and energy flow of freshwater Palaemonid shrimps in lowland Costa Rica. PhD diss., University of Georgia, Athens, GA. Snyder, M.N., E.A. Anderson, and C.M. Pringle. 2011. A migratory shrimp’s perspective on habitat fragmentation in the neotropics: ex-

tending our knowledge from Puerto Rico. In A. Asakura, ed., New Frontiers in Crustacean Biology: Proceedings of the TCS Summer Meeting, Tokyo, 20– 24 September 2009, pp. 109– 62. Crustaceana Monographs, vol. 15. Boston: Brill. Snyder, M.N., C.M. Pringle, and R.T. Soto-Mayer. 2013. Landscape-scale disturbance and protected areas: long-term dynamics of populations of the shrimp, Macrobrachium olfersii in lowland neotropical streams, Costa Rica. Journal of Tropical Ecology 29:81– 85. Snyder, M.N., G.E. Small, and C.M. Pringle. 2015. Diet-switching by omnivorous freshwater shrimps diminishes differences in nutrient recycling rates and body stoichiometry across a food quality gradient. Freshwater Biology 60: 526– 36. Solano, D.H., and A.M. Arias. 2011. Peces diablo ( Teleósteo: Siluriformes: Loricariidae) en la cuenca del río Reventazón, Costa Rica. Biocenosis 25(1– 2): 79– 86. Spínola-Parallada, R.M., and C. Vaughan-Dickhaut. 1995. Abundancia relativa y actividad de marcaje de la nutria neotropical (Lutra longicaudis) en Costa Rica / Relative abundance and spraint-marking activity of the neotropical river otter (Lutra longicaudis) in Costa Rica. Vida Silvestre Neotropical 4(1): 38– 45. Springer, M. 2006. A taxonomic key to the families of caddisfly larvae (Insecta: Trichoptera) of Costa Rica. Revista de Biología Tropical 54: 273– 86. Springer, M. 2008. Aquatic insect diversity of Costa Rica: state of knowledge. Revista de Biologia Tropical 56(Suppl. 4): 273– 95. Springer, M. 2010. Trichoptera. Revista de Biologia Tropical 58(Suppl. 4): 151– 98. Springer, M., D. Vásquez, A. Castro, and B. Kohlmann. 2007. Bioindicadores de la calidad de agua. Special publication of EARTH University, Costa Rica. Springer, M., A. Ramírez, and P. Hanson. 2010. Macroinvertebrados de Agua Dulce de Costa Rica I. Revista de Biologia Tropical 58(Suppl. 4): 1– 200. Springer, M., S. Echeverría-Sáenz, and P.E. Gutiérrez-Fonseca. 2014. Costa Rica. In: P. Alonso-EguíaLis, J.M. Mora, B. Campbell, and M. Springer, eds. Diversidad, conservación y uso de los macroinvertebrados dulceacuícolas de México, Centroamérica, Colombia, Cuba y Puerto Rico. Instituto Mexicano de Tecnología del Agua, Jiutepec, Morelos, México. 442 pp. Stallcup, L.A., M. Ardón, and C.M. Pringle. 2006. Does nitrogen become limiting under high-P conditions in detritus-based tropical streams? Freshwater Biology 51: 1515– 26. Stark, B.P. 1998. The Anacroneuria of Costa Rica and Panama (Insecta: Plecoptera: Perlidae). Proceedings of the Biological Society of Washington 111: 551– 603. Stiles, F.G. 1983. Birds. In D.H. Janzen, ed., Costa Rican Natural History, 502– 618. Chicago: University of Chicago Press. Stiles, F.G., and A.F. Skutch. 1989. A Guide to the Birds of Costa Rica. Comstock Publishing. 656 pp. Stout, J. 1980. Leaf decomposition rates in Costa Rican lowland tropical rainforest streams. Biotropica 12: 264– 72. Stout, R.J. 1989. Effects of condensed tannins on leaf processing in mid-latitude and tropical streams: a theoretical approach. Canadian Journal of Fisheries and Aquatic Sciences 46: 1097– 106. Stuart, S.N., J.S. Chanson, N.A. Cox, B.E. Young, A.S.L. Rodrigues, D.L. Frishman, and R.W. Waller. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783– 86.

Rivers of Costa Rica 655 TNC (The Nature Conservancy). 2009. Evaluación de Ecorregiones de Agua Dulce de Mesoamérica: Sitios Prioritarios para la Conservación en las Ecorregiones de Chiápas a Darién. San José, Costa Rica: The Nature Conservancy. 515 pp. Triska, F.J., C.M. Pringle, J.H. Duff, R.J. Avanzino, A. Ramírez, M. Ardón, and A.P. Jackman. 2006a. Soluble reactive phosphorus transport and retention in tropical rainforest streams draining a volcanic and geothermally active landscape in Costa Rica: long term concentration patterns, pore water environment and response to ENSO events. Biogeochemistry 81: 131– 43. Triska, F.J., C.M. Pringle, J.H. Duff, R.J. Avanzino, and G. Zellweger. 2006b. Soluble reactive phosphorus (SRP) transport and retention in tropical rain forest streams draining a volcanic and geothermally active landscape in Costa Rica: in situ amendment and laboratory studies. Biogeochemistry 81: 145– 57. Triska, F.J., C.M. Pringle, G.W. Zellweger, J.H. Duff, and R.J. Avinzino. 1993. Dissolved inorganic nitrogen composition, transformation, retention, and transport in naturally phosphate-rich and phosphatepoor tropical streams. Canadian Journal of Fisheries and Aquatic Sciences 50: 665– 75. Umaña-Villalobos, G., and M. Springer. 2006. Environmental variation in the Grande de Térraba River and some of its tributaries, south Pacific of Costa Rica. Revista de Biología Tropical 54: 265– 72. van Breukelen, N. A. 2015. Interactions between native and non-native cichlid species in a Costa Rican river. Environmental Biology of Fishes 98:885– 89. Vargas, R.J. 1995. History of municipal water resources in Puerto Viejo de Sarapiquí, Costa Rica: a socio-political perspective. Master’s thesis, University of Georgia. Athens, GA. Verburg, P., S.S. Kilham, C.M. Pringle, K.R. Lips, and D.L. Drake. 2007. A stable isotope study of a neotropical stream food web prior to the extirpation of its large amphibian community. Journal of Tropical Biology 23: 643– 51. Villalobos, C.R., and E. Burgos. 1975. Potamocarcinus (Potamocarcinus) nicaraguensis (Pseudothelphusidae: Crustacea) en Costa Rica. Revista de Biología Tropical 22(2): 223– 37. Voyles, J., S. Young, L. Berger, C. Campbell, W.F. Voyles, A. Dinudom, D. Cook, R. Webb, R.A. Alford, L.F. Skerratt, and L. Speare. 2009. Pathogenesis of chytriomycosis, a cause of catastrophic amphibian declines. Science 326: 582– 85. Wantzen, K.M., R. Wagner, R. Suetfeld, and W.J. Junk. 2002. How do plant-herbivore interactions of tress influence coarse detritus processing by shredders in aquatic ecosystems of different latitudes? Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie 28: 815– 21. Webster, J.R., and E.F. Benfield. 1986. Vascular plant breakdown in

freshwater ecosystems. Annual Review of Ecology and Systematics 17: 567– 94. Whiles, M., R.O. Hall Jr., W.K. Dodds, P. Verburg, A.D. Huryn, C.M. Pringle, K.R. Lips, S.S. Kilham, C. Colon-Gaud, A.T. Rugenski, S. Peterson, and S. Connelly. 2013. Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16: 146– 57. Whiles, M., K. Lips, C.M. Pringle, S.S. Kilham, R. Bixby, R. Brenes, S. Connelly, J.C. Colon-Gaud, M. Hunte-Brown, A.D. Huryn, C. Montgomery, and S. Peterson. 2006. The effects of amphibian population declines to the structure and function of Neotropical stream ecosystems. Frontiers 4(1): 27– 34. Whitfield, S.M., K.E. Bell, T. Philippi, M. Sasa, F. Bolaños, G. Chaves, J.M. Savage, and M.A. Donnelly. 2007. Amphibian and reptile declines over 35 years at La Selva, Costa Rica. Proceedings of the National Academy of Sciences 104: 8352– 56. Whitfield, S.M., E. Geerdes, I. Chacon, E.B. Rodriguez, R.R. Jiménez, M.A. Donnelly, and J.L. Kerby. 2013. Infection and co-infection by the amphibian chytrid fungus and ranavirus in wild Costa Rican frogs. Diseases of Aquatic Organisms 104: 173– 78. Whitfield, S.M., J. Kerby, L.R.Gentry, and M.A. Donnelly. 2012. Temporal variation in infection prevalence by the amphibian chytrid fungus in three species of frogs at La Selva, Costa Rica. Biotropica 44: 779– 84. Winemiller, K.O. 1983. An introduction to the freshwater fish communities of Corcovado National Park, Costa Rica. Brenesia 21: 47– 66. Winemiller, K.O., and M.A. Leslie. 1992. Fish assemblages across a complex, tropical fresh-water marine ecotone. Environmental Biology of Fishes 34: 29– 50. Winemiller, K.O., and B.J. Ponwith. 1998. Comparative ecology of eleotrid fishes in Central American coastal streams. Environmental Biology of Fishes 53: 373– 84. Wootton, T., and M.P. Oemke. 1992. Latitudinal differences in fish community trophic structure, and the role of fish herbivory in a Costa Rican stream. Environmental Biology of Fishes 35: 311– 19. World Commission on Dams ( WCD). 2000. Dams and development: a framework for decision-making. Accessed February 26, 2007. http:// www.damsreport.org. WRI ( World Resources Institute). 1991. Accounts overdue: natural resource depreciation in Costa Rica. Washington, DC: WRI. Wydrzycka, U., and H. Lange-Bertalot. 2001. Las diatomeas (Bacillariophyceae) acidófilas del Río Agrio y sitios vinculados con su cuenca, Volcán Poás, Costa Rica. Brenesia 55– 56: 1– 68. Young, B.E., S.N. Stuart, J.S. Chanson, N.A. Cox, and T.M. Boucher. 2004. Disappearing Jewels: The Status of New World Amphibians. Washington, DC: NatureServe.

Chapter 19 Lakes of Costa Rica

Sally P. Horn1,* and Kurt A. Haberyan2

Introduction Costa Rica has an abundance of lakes, distributed from sea level to the nation’s highest peaks and within each of the major terrestrial ecosystems. We focus here on permanent, predominantly fresh, water bodies of all sizes, including water bodies that would be “ponds” in the classification of Horne and Goldman (1994). Costa Rica has lakes that exemplify nearly every natural process of lake formation, including volcanic activity, fluvial dynamics, glaciation, and landslides and other forms of mass movement. Humans have also created many lakes, for a variety of reasons: hydroelectric power, water storage, recreation, aquaculture, livestock, and as consequences of road construction and other activities that blocked original drainages. Natural lakes in Costa Rica are popular hiking and tourist destinations today, and had practical and possibly symbolic importance for prehistoric cultures. They contribute to Costa Rica’s high habitat and biological diversity, and their sediments provide key evidence of ecosystem history. High-elevation lakes in Costa Rica, as throughout the world (Messerli 2001), may be harbingers of global climate change (Horn et al. 2005). We begin this chapter with a short history of research on Costa Rican lakes and a consideration of lake distribution in the country as a whole. We then present a regional survey of Costa Rican lakes, following the classification of terrestrial ecosystems used throughout this book (Kappelle, chapters 1 and 21 of this volume). For each of the seven 1 Department of Geography, University of Tennessee, Knoxville, TN 37996, USA 2 Department of Natural Sciences, Northwest Missouri State University, Maryville, MO 64468, USA * Corresponding author

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principal terrestrial ecosystem regions we describe the common mechanisms of lake formation and highlight two to five lakes that are particularly well known. While much of this information is drawn from our published work, we include additional observations by ourselves and others on aquatic biology and other lake characteristics. We also summarize the contributions that paleolimnological studies have made to understanding ecosystem and environmental history in each region.

Research on Costa Rican Lakes Scientific investigations of Costa Rican lakes began in the latter half of the twentieth century, carried out by Costa Rican scientists and students as well as by visiting foreigners (Umaña et al. 1999). The first detailed study was a thesis on the basic limnology and biology of Laguna de Río Cuarto, submitted to the University of Costa Rica by Kohkemper (1954). The Austrian limnologist Löffler (1972) described the limnology and planktonic communities of high-elevation lakes visited in 1966, while Bumby (1982), a student from the United States of America, focused on the chemical characteristics and macrophytes of mainly low- to mid-elevation lakes during fieldwork in 1973. In the late 1970s, Bergoeing (1978) and Bergoeing and Brenes (1978) interpreted the geomorphology and history of several Costa Rican lake basins from aerial photography, and Bolaños (1979) published an early paper on Tilapia aquaculture. Limnological studies within Costa Rica increased dramatically in the 1980s, propelled in part by the establishment of CIMAR (Centro de Investigación en Ciencias de Mar y Limnología), a research center at the University of

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Costa Rica that began activities in 1979 (Umaña et al. 1999, Vargas 2004). Students and faculty at the Universidad Nacional (UNA) in Costa Rica also initiated limnological studies at this time, as did we ourselves and other foreign visitors. Papers on lakes from this decade focused on physical and chemical properties (Gocke et al. 1981, 1987, Baker 1987, Charpentier et al. 1988), sediments (Horn 1989a), phytoplankton (Hargraves and Víquez 1981, Wujek 1984, Camacho 1985, Umaña 1985, 1988, Dickman and Nanne 1987), and zooplankton (Collado 1983, Collado et al. 1984a,b, Ramírez 1985, Dussart and Fernando 1986). A large number of papers on freshwater fish also appeared (see review by Umaña et al. 1999, and Pringle et al., chapter 18 of this volume); most studies concerned fish in streams but Ulloa et al. (1988, 1989) described fish communities in the Arenal Reservoir. Publications on lakes have grown in both number and scope from the 1990s onward. While some investigations have continued to explore the limnology and biology of particular lakes (for example, Gocke et al. 1990, Gocke 1996– 97, Ramírez et al. 1990, Ramírez and Camacho 1991, Umaña 1990, 1993, 1997a,b, 2001, Umaña and Collado 1990, Umaña and Jiménez 1995, Umaña et al. 1997, Jiménez and Springer 1994, 1996, Petersen and Umaña 2003), new efforts have focused on the diversity of lakes and their geographic distribution. One of the first broad surveys was presented in 1993 (Horn and Haberyan 1993), and geographic expansion continues to the present, with the publication of basic limnological data from additional lakes in many regions (e.g., Jones et al. 1993, Horn et al. 1999, 2005, Haberyan et al. 2003, Tassi et al. 2009). The 1990s also saw the publication of regional surveys on plankton in Costa Rican lakes (Haberyan et al. 1995, Wujek et al. 1998) and on diatoms (Haberyan et al. 1997), chrysophyte cysts (Zeeb et al. 1996), and pollen grains (Rodgers and Horn 1996) in surface lake sediments. The documentation of limnological parameters and biological communities continues to be a strong focus, with recent publications exploring microbial diversity in lake waters (Cabassi et al. 2014) and chironomid sub-fossils in surface sediments (Wu et al. 2015). More studies today include repeat measurements to elucidate seasonal and interannual variations (e.g., Umaña 1997b, 2001, 2010a,b, 2014a,b). With basic limnological and ecological information now in hand, a secondary focus of lake research in Costa Rica is developing an understanding of the history of lake basins, biota, and surroundings through paleolimnological studies. Such studies are based on evidence preserved in lake sediments, including diatoms, pollen grains, charcoal fragments, and other biological and geochemical indicators (Cohen 2003). The study of sediment profiles from lakes

and swamps in Costa Rica is a key tool for understanding Quaternary climate change (Horn 2007), especially during the Holocene (past 11,700 years) and late Pleistocene (ca. 126,000 to 11,700 years ago). Sediment records from Costa Rican lakes complement and extend what can be learned from the study of ancient soils (Driese et al. 2007), cave speleothems (Lachniet et al. 2004), tree rings (Anchukaitis et al. 2008), and glacial geomorphology (Orvis and Horn 2000, Lachniet and Seltzer 2002). Lake-sediment records also contain abundant evidence of the activities and impacts of pre-Columbian people (Horn 2006, 2007). The following sections provide a brief introduction to selected lakes of Costa Rica. While we refer to many publications, a detailed review of the literature is beyond the scope of this chapter. For additional information and references see reviews by Umaña et al. (1999) and Haberyan et al. (2003), and the bibliography of CIMAR publications developed by Fuentes et al. (2006).

Distribution and Origins of Costa Rican Lakes Lakes exist where there are topographic depressions and water to fill them (Cohen 2003). Costa Rica’s high rainfall, and wide array of basin-forming geomorphic and human processes, have produced a very large number of natural and artificial lakes. Most of these lakes are too small to appear on maps that show the country as a whole but they are readily apparent on the 1:50,000 scale topographic maps produced by the Instituto Geográfico Nacional (IGN) from aerial photographs. In the 1980s, IGN staff members meticulously compiled information on the location and size of all water bodies over 0.25 ha in area on each of the country’s 139 1:50,000-scale topographic map sheets. The total number of lakes tallied, including seasonal ponds, brackish lagoons, and reservoirs, was 652. Although many of these lakes have since been drained for agriculture, our limnological investigations have revealed some two dozen lakes that were not mapped, either because they are of a more recent origin or because they were obscured by shadows, glare, clouds, or forest cover on the original photographs. Thus, even accounting for the draining of many lakes and the inclusion of seasonal and brackish water bodies in the IGN database, it is likely that several hundred permanent freshwater lakes still exist in Costa Rica. The 652 water bodies included in the IGN database are distributed throughout the country, from both coasts to the crests of the mountain ranges (Fig. 19.1). Most of the lakes are located in the lowlands; 51% are below 40 m in elevation, 86% are below 500 m, and 92% are below 1,000 m. In terms of lake area, 13% of the IGN water bodies are less

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Fig. 19.1 Distribution of lakes in the database of Costa Rican lakes created by the Instituto Geográfico Nacional (IGN), San José, Costa Rica. Map produced by the Cartographic Services Laboratory of the University of Tennessee, Knoxville, TN, USA.

than 1 ha; 66% are between 1 and 10 ha, 17% are between 10 and 100 ha, 4% are between 100 and 1,000 ha, and less than one percent are larger than 1,000 ha. The dominant mechanisms of lake formation vary with elevation, geology, and terrain, with some lake-forming processes limited to small areas of the country, and others relatively widespread. Along both coasts sandbars have created coastal lagoons that are freshened by inflowing streams (Umaña et al. 1999, Haberyan et al. 2003). In the floodplains of large rivers, stream courses have shifted over time, leaving

behind old channels and other depressions that become lakes. Where slopes are steeper at low to mid-elevations, landslides of various types have blocked drainage of former stream valleys, creating lakes. Volcanism has produced lava flows and lahars that have created impoundments at these elevations, in addition to craters of various types found along a wide elevational gradient. Several volcanic craters at high elevations along the crests of the Cordillera de Guanacaste and Cordillera Central hold lakes (Alvarado 2000, and see Alvarado and Cárdenes, chapter 3 of this vol-

Lakes of Costa Rica 659

ume). Even the highest peaks in the country, reaching over 3,800 m in the Cordillera de Talamanca, are surrounded by lakes, here formed by glaciers (Horn et al. 1999, 2005). For some lakes, the origins of the basins they occupy remain uncertain (Alvarado 2000). In more modern times, human activity has created abundant lakes. Farm ponds have been built for aquaculture, agriculture, and livestock. A multitude of small water bodies has been formed as a secondary impact of road or railroad construction, either by grading across a drainage or by excavating fill for roadbeds. Large reservoirs store water for human consumption (e.g., the Orosi Reservoir, which supplies much of San José: Sánchez-Azofeifa et al. 2002), while others also provide hydroelectric power, recreation, and other services, including the Arenal (8000 ha), Cachí (283 ha), and Angostura (220 ha) reservoirs. The environmental impacts of reservoir construction on Costa Rican streams are described by Pringle et al., chapter 18 of this volume; see also Anderson et al. (2006).

Regional Survey of Costa Rican Lakes Lakes of the Pacific Dry Forest

We consider together here lakes in the two sectors of the Pacific dry forest ecosystem: the Northern Pacific lowland deciduous dry forest, and the Nicoya-Tempisque Pacific dry forest (Fig. 19.2). For extensive descriptions of the Pacific Dry Forest ecosystem and its conservation we refer to Jiménez et al. and Janzen and Hallwachs, chapters 9 and 10 of this volume, respectively. Although seasonally arid, the northern Pacific lowlands of Costa Rica support several permanent, natural water bodies in addition to a number of seasonal lakes and artificial ponds maintained by irrigation. Natural lakes in this region occur in two clusters: one on the southern slope of Miravalles volcano, and one near the mouth of the Río Tempisque. These two areas are among a small number of “lake districts” (Horne and Goldman 1994) in Costa Rica in which multiple lakes exist that share a common mode of formation. Such areas provide important settings for limnological research. Although formed by the same processes, often at the same time, and occupying the same general climate setting, individual lakes within particular lake districts are likely to differ somewhat in basin form, size, microclimate, and watershed conditions including land use and disturbance history, making lake districts valuable sites for comparative research in both modern lake biology and paleolimnology. Lakes in the Miravalles lake district occupy depressions between 330 and 570 m in elevation, in an area of undulating topography created by a volcanic debris avalanche from

Miravalles Volcano about 8,300 years ago (Alvarado et al. 2004, Siebert et al. 2006). The eight we have investigated range from less than one hectare to 4.4 ha in size, and are surrounded by cattle pastures and remnant areas of lowland deciduous dry forest. Despite the seasonal rainfall in this part of Costa Rica, these lakes hold water year-round, although water levels may drop significantly during years of exceptionally severe drought, as we observed in March 1998 (Haberyan et al. 2003). The three we highlight here, Laguna San Pablo, Estero Blanco, and Laguna Martínez (Fig. 19.2, Table 19.1), are fairly broad, shallow, and turbid. These lakes vary in many characteristics, but tend to have somewhat elevated levels of calcium (about 18– 28 mg/ L), sodium (~12– 25 mg/L), and silica (~15– 33 mg/L). Aquatic macrophytes are present in all three lakes. Laguna San Pablo (Fig. 19.3) and Estero Blanco (Fig. 19.4) are largely open water, but San Pablo has two large (>50 m2) floating islands of grass and other plants that are pushed across the lake by strong dry season winds, and Estero Blanco has abundant submerged macrophytes. Laguna Martínez, a smaller and more sheltered lake, had open water in 2001 but was covered by water hyacinth at the time of our last visit in June 2003. Lakes in the Tempisque lake district are found near sea level at the head of the Gulf of Nicoya. Depressions here were formed by the natural migration of the Río Tempisque and its tributaries, which leaves behind abandoned channels, and by the build-up of natural levees along the main river that dam the mouths of tributary streams. Although many of these lakes are shown on topographic maps as permanent water bodies, most probably dry down substantially during the dry season. Land managers, biologists, and conservationists generally refer to these sites as seasonal wetlands rather than lakes (Bravo and Ocampo 1993; Jiménez, chapter 20 of this volume). Examples include the “lagunas” of Palo Verde National Park and of the Laguna Mata Redonda Wildlife Refuge, located 10 km to the southwest (Boza and Cevo 1998). It is unknown whether the seasonal desiccation of these floodplain lakes is the natural long-term condition or the result of stream diversions and agricultural development. In both Palo Verde National Park and the Laguna Mata Redonda Wildlife Refuge, the question of the natural hydrological state is further complicated by the recent spread of aquatic macrophytes, particularly cattail (Typha), through areas of formerly open water (Somarribas and Bravo 1999, Horn and Kennedy 2006). Outside these protected reserves, the IGN maps show lakes that no longer exist, having been drained to make way for the cultivation of rice or other crops. Although these former lakes may be impossible to recognize in the field, their faint outlines are evident in recent satellite imagery.

660 Chapter 19

Fig. 19.2 Locations of lakes discussed in the text, with respect to terrestrial ecosystem regions. Lake numbers correspond to numbers in the authors’ database of limnological observations from approximately one hundred Costa Rican lakes. Map produced by Marco V. Castro.

Aside from the Miravalles lakes and the Tempisque lakes, farm ponds are scattered across the Pacific dry forest region. We have sampled two in the Nicoya-Tempisque Pacific dry forest sector: Laguna Palmita, along the InterAmerican highway about 28 km SSE of the town of Cañas (Horn and Haberyan 1993), and Laguna Solimar, 16 km SSW of Cañas, in the lowlands at the head of the Gulf of Nicoya. Laguna Solimar (Table 19.1) is a turbid, eutrophic lake characterized by warm temperatures (32°C), and relatively high alkalinity and conductivity, in keeping

with the lake’s location at low elevation in the driest part of Costa Rica. Haberyan et al. (1995) classified Solimar as a cyanophyte-dominated lake, with Cylindrospermum the most common phytoplankton. The zooplankton community was composed largely of the copepod Mesocylcops thermocyclopoides, with some ostracods. Sediment cores for paleolimnological study have been recovered from the Miravalles lakes and from the Bocana wetland in Palo Verde National Park. Pollen, microscopic charcoal, and sediment characteristics in profiles from La-

Lakes of Costa Rica 661

gunas San Pablo, Estero Blanco, Martínez, and three other lakes in the Miravalles district document initial forest development following the debris avalanche and associated eruptive phenomena that formed the lake basins, and subsequent shifts in moisture availability, vegetation composition, and fire incidence (Arford and Horn 2004; Horn et al., unpublished data). Past fires in these lowland dry forests resulted from natural ignition (from volcanism and lightning) as well as human activity; analyses of macroscopic (>250 µm) charcoal fragments too large to be readily dispersed by wind indicate that many of the fires occurred within lake watersheds. The upper sections of all six lake sediment profiles contain maize pollen and charcoal from agricultural fires. The earliest maize pollen, in the sediment core from Laguna Martínez, is associated with charcoal dated to 5,500 cal yr BP (calibrated years before present) and constitutes the earliest evidence for maize cultivation in all of Costa Rica (Arford and Horn 2004). [Note: cal yr BP ages reported throughout the text are the weighted means of the calibration probability distributions (Telford et al. 2004a), Table 19.1.

derived using the Calib 5.0.1 program (Stuiver and Reimer 1993) and the dataset of Reimer et al. 2004.] Maize is a fully domesticated plant that can persist on the landscape only with human assistance; the distribution of its pollen in the Miravalles sediments thus demonstrates the presence of settled humans within the northern Pacific lowland deciduous dry forest for over five millennia (Horn 2006). Diatom assemblages in the San Pablo core suggest changes in lake level that generally match climate interpretations from pollen and sediment characteristics (Haberyan et al. 2005), but seem not to show any effects of prehistoric agriculture. The dense and sticky sediments of the Bocana wetland have proven difficult to core, and we have recovered and examined only a partial profile from this site 7 km east of the Organization for Tropical Studies field station in Palo Verde National Park. The most important finding is the presence of pollen of cattail (Typha) in two samples adjacent to and below a charcoal fragment dated to 4,500 cal yr BP (Horn and Kennedy 2006). Beginning in the 1980s, areas of formerly open water in the seasonal wetlands of Palo Verde

Selected Data from Lakes of the Pacific Dry Forest of Costa Rica

Lake Name

San Pablo

Estero Blanco

Martínez

Solimar

Lake Number

71

67

88

30

Parameter Latitude (°N) Longitude (°W) Elevation (m a.s.l.) Area (ha) Depth (m) Secchi (m) Temperature (°C) Stratified? Macrophyte cover pH Conductivity (uS/cm) O2 (mg/L) CO2 (mg/L) Alkalinity (mg/L CaCO3) Ca+2 (mg/L) Mg+2 (mg/L) K+ (mg/L) Na+ (mg/L) Si (mg/L) Cl− (mg/L) S total (mg/L)

10.6594 85.1782 450 4.38 2.5 0.5 29.1 yes 0 9.50 176 12.0 nd 95 17.72 2.37 6.46 15.71 28.33 7.24 nd

10.6657 85.2012 430 1.50 2.8 1.6 28.8 yes 4 7.90 214 7.6 6 75 18.10 6.39 4.63 11.69 15.07 4.47 7.88

10.6405 85.1961 340 1.5 3.6 1.3 25.5 nd 9 6.36 nd nd nd nd 28.02 8.87 5.70 24.54 33.32 4.81 nd

10.2724 85.1301 8 4.33 2.5 0.4 32.0 yes 2 7.73 120 13 0 119 11.9 3.54 7.12 6.68 12.7 4.5 0.6

NOTE. Lagunas San Pablo, Estero Blanco, and Martínez of the Miravalles lake district are located in the northern Pacific lowland deciduous dry forest sector, and Laguna Solimar is located in the Nicoya-Tempisque Pacific dry forest sector of the Pacific dry forest ecosystem. Our previous publications reported coordinates based on the Ocotepeque 1935 datum, as used on Costa Rican topographic maps (Orvis 2002), but here we provide coordinates determined using Google Earth, which uses a WGS84 datum. Some limnological data represent a composite of multiple visits, combined so as to represent dry and wet seasons equally. Macrophyte cover is estimated using a linear scale ranging from 0 to 9, reflecting the proportion of lake surface that is covered by or underlain by macrophytes (coverage 0 reflects 0 to 10%, coverage 1 reflects 10 to 19%, etc.). nd = no data are available. See Horn and Haberyan (1993) and Haberyan et al. (2003) for additional data.

Fig. 19.3 Dry-season view of Laguna San Pablo in the northern Pacific lowland deciduous dry forest ecosystem. This lake occupies a depression in undulating topography formed by volcanic debris flows and lahars from Volcán Miravalles, visible in the background. Watershed vegetation consists of cattle pasture with scattered trees. One of the lake’s two floating islands can be seen in the lower left of the image; a portion of the other island is visible on the far right. Photo by Sally Horn.

Fig. 19.4 Laguna Estero Blanco in the northern Pacific lowland deciduous dry forest ecosystem, photographed during the wet season. Photo by Christine Lafrenz.

Lakes of Costa Rica 663

National Park began to be choked with dense stands of cattail, a process that has greatly reduced migratory bird habitat (see also Jiménez, chapter 20 of this volume). The rapid spread of cattail led to its description as an “invasive species” and one report (Cochard and Jackes 2005) that the plant was not native to the area but had been introduced from Eurasia. However, the sediment profile from the Bocana marsh shows that Typha is native and of some antiquity in the park: if regarded as an invasive, it belongs in a special category as a native invasive species (Horn and Kennedy 2006). A third paleolimnological site in the Pacific dry forest ecosystem consists of an ancient lake bed, now dry and exploited for its diatom-rich sediment (diatomite). Chávez and Haberyan (1996) described diatom assemblages in 23 samples taken at various depths within the Camastro Diatomite, located on the lower western slope of the Rincón de la Vieja volcanic complex. The deposit as a whole is likely Pleistocene in age and may span more than 30,000 years. Seven assemblages were recognized, all suggesting that the lake was similar to many modern lakes of the region: shallow, eutrophic, and slightly basic (pH, 7.8 to 8.5), with low to medium concentrations of silica, and low conductivity. Lakes of the Central Pacific Lowland Seasonal Moist Forest

The Central Pacific lowland seasonal moist forest region (Jiménez et al., chapter 11 of this volume) has fewer natural lakes than the dry and moist forest regions of the northern and southern Pacific lowlands, respectively. Both of the lakes we have sampled were formed by fluvial action (Table 19.2). Laguna Carara occupies a meander scar of the Río Tárcoles in the Carara Biological Reserve; it shows the classic oxbow shape of a cut-off meander, but reserve staff indicated that it receives overflow from the Tárcoles during the wet season, functioning as an alternate channel. The muddy appearance of the lake confirms this connection, at least when we visited in July 1997. The abundance of CO2 and paucity of O2 suggest that primary production in the lake itself is low; rather, much carbon probably enters from the surrounding plants. In 1997 we also visited Laguna Madre Vieja, located across the river from L. Carara. This lake also occupied an old meander scar, but other characteristics differed: its waters were not muddy, and water lilies covered the surface. These observations, together with the elevated concentrations of ions, indicated that Madre Vieja was not flushed annually by river overflow in the 1990s. However, satellite images document shifts in the course of the Río

Table 19.2. Selected Data from Lakes of the Central Pacific Lowland Seasonal Moist Forest of Costa Rica Lake Name

Carara

Madre Vieja

Lake Number

57

58

Parameter Latitude (°N) Longitude (°W) Elevation (m a.s.l.) Area (ha) Depth (m) Secchi (m) Temperature (°C) Stratified? Macrophyte cover pH Conductivity (uS/cm) O2 (mg/L) CO2 (mg/L) Alkalinity (mg/L CaCO3) Ca+2 (mg/L) Mg+2 (mg/L) K+ (mg/L) Na+ (mg/L) Si (mg/L) Cl− (mg/L) S total (mg/L)

9.7984 84.5932 16 2.13 3.5 0.6 30.8 no 1 7.99 362 4.4 12 169 35.33 9.24 5.37 18.85 15.05 4.70 3.39

9.8103 84.5949 16 1.60 3.0 0.2 32.9 no 9 7.60 412 0.6 27 202 44.01 15.05 3.17 12.20 18.38 2.00 0.42

NOTE. Our previous publications reported coordinates based on the Ocotepeque 1935 datum, as used on Costa Rican topographic maps (Orvis 2002), but here we provide coordinates determined using Google Earth, which uses a WGS84 datum. Macrophyte cover is estimated using a linear scale ranging from 0 to 9, reflecting the proportion of lake surface that is covered by or underlain by macrophytes (coverage 0 reflects 0 to 10%, coverage 1 reflects 10 to 19%, etc.). See Haberyan et al. (2003) for additional data.

Tárcoles between 2002 and 2013 that led to the stream reoccupying the abandoned channel in which Laguna Madre Vieja had formed. The lake no longer exists in 2015, its creation and destruction both a consequence of natural fluvial processes in this dynamic floodplain environment. We have not collected sediment cores from Laguna Carara or Laguna Madre Vieja. Abandoned channel lakes generally have relatively short life spans (Cohen 2003), but their sediments can provide valuable records of ecosystem history. The likelihood that sediments are flushed from Laguna Carara during flood events suggests that this site may be a poor prospect for coring, but records might be preserved in wetlands and other small depressions within agricultural fields on the floodplain, identifiable from satellite imagery as locations of former stream channels. The presence of large crocodiles here (Herrera 1992) will require special vigilance, as these reptiles have endangered sediment-coring teams in other parts of the world (Richardson and Livingstone 1962, Tyson 2000).

664 Chapter 19

Lakes of the Southern Pacific Lowland Evergreen Moist Forest

Lakes formed by mass movement and fluvial dynamics are numerous in the southern Pacific lowland evergreen moist forest region described by Gilbert et al. (chapter 12 of this volume), as are small artificial lakes. Here we describe two contrasting natural lakes of very different origin (Table 19.3). Laguna Sierpe is located at the southern edge of the Térraba-Sierpe delta, where it abuts the hills that link the Osa Peninsula to the mainland. It comprises a large, shallow (2.2 m depth) expanse of water surrounded by floating mats of grasses and other plants. Despite its flat bottom and the great exposure of the lake, we found evidence of weak temperature stratification in July 1997. The lake may owe its formation to the build-up of sediments and vegetation along the Río Sierpe or along the coast. The composition Table 19.3. Selected Data from Lakes of the Southern Pacific Lowland Evergreen Moist Forest of Costa Rica Lake Name

Sierpe

Vueltas

Lake Number

43

51

Parameter Latitude (°N) Longitude (°W) Elevation (m a.s.l.) Area (ha) Depth (m) Secchi (m) Temperature (°C) Stratified? Macrophyte cover pH Conductivity (uS/cm) O2 (mg/L) CO2 (mg/L) Alkalinity (mg/L CaCO3) Ca+2 (mg/L) Mg+2 (mg/L) K+ (mg/L) Na+ (mg/L) Si (mg/L) Cl− (mg/L) S total (mg/L)

8.7867 83.3265 16 102.7 2.2 1.2 33.0 yes 1 7.09 102 6.6 6 48 8.88 3.50 0.00 4.35 9.90 2.60 0.37

8.9662 83.1757 270 0.30 3.0 0.6 29.9 yes 1 8.72 233 10.1 0 125 21.72 8.43 3.86 7.02 20.95 1.50 1.48

NOTE. Our previous publications reported coordinates based on the Ocotepeque 1935 datum, as used on Costa Rican topographic maps (Orvis 2002), but here we provide coordinates determined using Google Earth, which uses a WGS84 datum. Some limnological data represent a composite of multiple visits, combined so as to represent dry and wet seasons equally. Macrophyte cover is estimated using a linear scale ranging from 0 to 9, reflecting the proportion of lake surface that is covered by or underlain by macrophytes (coverage 0 reflects 0 to 10%, coverage 1 reflects 10 to 19%, etc.). See Umaña et al. (1999) and Haberyan et al. (2003) for additional data.

of its waters reflect inputs from the surrounding vegetation. The modern diatom assemblage in its surface sediments is largely composed of Nitzschia amphibia and Pseudostaurosira brevistriata. Laguna Vueltas overlooks the Río Limón, which joins the Río Térraba below the confluence of the General and Coto Brus rivers. It apparently formed by ponding behind a block slide, and is turbid and warm. Tilapia were added to the lake for sport fishing, and these fish are prey to boatbilled herons whose Spanish name (chocuaco) gives the lake its local name (we use Laguna Vueltas for consistency with the topographic map). The lake is rather shallow; this, plus inputs from the herons and other sources, contributes to the elevated oxygen levels we observed. The most common diatom in its surface sediments is Nitzschia frustulum. A sediment core from Laguna Vueltas documents late Holocene shifts in vegetation and fire incidence resulting from human activities (Horn et al., unpublished data). Sedimentary pollen assemblages and stable carbon isotope signatures document extensive forest clearance and maize cultivation around 1,100 cal yr BP. Charcoal and maize disappear from the record about 450 cal yr BP, indicating site abandonment following the Conquest, which was marked by population decline throughout Costa Rica. At that point in the record, tree pollen sharply rebounds, indicating recovery of the southern Pacific lowland evergreen moist forest. Lakes of the Northern Highland Evergreen Cloud Forest

The northern highlands are dominated by two chains of Quaternary volcanoes, the Cordillera de Guanacaste to the north and the Cordillera Central to the south, with an intervening area of older, Tertiary volcanic rocks in the Cordillera de Tilarán (Lawton et al., chapter 13 of this book). Not surprisingly, crater lakes of various types are best developed in this part of the country. However, the northern highland evergreen cloud forest region is also home to several lakes formed by lava or lahar flows and by landslides (Table 19.4). Permanent, freshwater lakes in craters atop volcanoes in this ecosystem include Lagunas Santa María, Cerro Chato, and Barva, on the volcanoes for which they are named, and Laguna Botos on Volcán Poás. We highlight Laguna Cerro Chato and Laguna Barva, which have been sampled repeatedly. Laguna Cerro Chato at the southern end of the Cordillera de Guanacaste occupies an inactive crater associated with Volcán Arenal (2.5 km to the northwest). The lake is relatively deep (17.9 m) and surrounded by crater walls that rise 60– 120 m above the lake surface (Umaña 2010a). During four visits during the wet season Umaña

Lakes of Costa Rica 665 Table 19.4.

Selected Data from Lakes of the Northern Highland Evergreen Cloud Forest

Lake Name

Cerro Chato

Barva

Hule

La Palma

Poco Sol

Lake Number

39

11

19

31

37

Parameter Latitude (°N) Longitude (°W) Elevation (m a.s.l.) Area (ha) Depth (m) Secchi (m) Temperature (ºC) Stratified? Macrophyte cover pH Conductivity (uS/cm) O2 (mg/L) CO2 (mg/L) Alkalinity (mg/L CaCO3) Ca+2 (mg/L) Mg+2 (mg/L) K+ (mg/L) Na+ (mg/L) Si (mg/L) Cl− (mg/L) S total (mg/L)

10.4428 84.6883 1050 2.75 17.9 2.3 21.2 yes 0 7.24 28 7.0 3 8 0.32 0.12 0.00 1.15 0.27 2.00 0.35

10.1337 84.1053 2840 0.77 7.9 1.7 11.7 no 0 7.45 60 8.0 4 9 0.63 0.32 1.39 7.41 0.84 9.49 2.00

10.2948 84.2100 740 54.71 22.5 3.0 21.1 yes 1 6.55 78 9.2 5 60 7.88 2.48 1.47 3.97 13.47 2.82 0.63

10.4857 84.7137 570 5.00 10.8 1.4 25.7 yes 1 8.16 293 11.3 6 130 21.64 17.21 2.82 15.02 24.53 10.68 5.36

10.3501 84.6699 776 2.88 11.3 2.1 23.7 yes 0 7.26 107 5.9 3 48 11.03 1.67 0.43 4.46 10.19 2.30 1.50

NOTE. Our previous publications reported coordinates based on the Ocotepeque 1935 datum, as used on Costa Rican topographic maps (Orvis 2002), but here we provide coordinates determined using Google Earth, which uses a WGS84 datum. Some limnological data represent a composite of multiple visits, combined so as to represent dry and wet seasons equally. Macrophyte cover is estimated using a linear scale ranging from 0 to 9, reflecting the proportion of lake surface that is covered by or underlain by macrophytes (coverage 0 reflects 0 to 10%, coverage 1 reflects 10 to 19%, etc.). See Horn and Haberyan (1993), Umaña et al. (1999), and Haberyan et al. (2003) for additional data.

et al. (1997) found the lake to be stratified, but hypothesized that it may overturn during the windier dry season, when whitecaps are visible on the lake despite the sheltering provided by the high crater walls. The bottom of the lake is strewn with rocks and boulders, and we were able to retrieve only a bottom sample of leaves and small amounts of mud. Diatoms in this sample consisted largely of Brachysira brachysira. Laguna Cerro Chato’s waters are dilute. Repeated measurements of lake pH by Umaña and Jiménez (1995) revealed strong variation over time and space, from 3.3 to 6.0, a condition influenced by the very low alkalinity of the lake (8 mg L− 1). The Laguna Cerro Chato watershed supports unbroken northern highland cloud forest. The shade cast by the forest, together with the steep slopes, precludes the development of littoral vegetation. Umaña and Jiménez (1995) found the lake’s phytoplankton to be dominated by chlorophytes, especially Arthrodesmus bifidus, Monorhaphidium griffithii, and small coccoid cells. Zooplankton was dominated by the copepod Tropocyclops prasinus prasinus (85% of all zooplankters observed), and also included four species of cladocerans. The mesh size used for sampling zooplankton

probably prevented the collection of rotifers, but even accounting for that, zooplankton diversity was very low. The lake lacks fish, but tadpoles were observed to be abundant in the open water of the lake. Umaña and Jiménez (1995) examined the stomach content of one tadpole and suggested that zooplankton was not a large part of the diet. Jiménez and Springer (1994, 1996) examined benthic macrofauna in Laguna Cerro Chato. Chironomids were the most abundant organisms, followed by oligochaetes and nematodes. Samples from deeper locations in the lake had lower species diversity and evenness. Overall patterns of abundance and diversity correlated with the oxygen content of the water and the organic content of surface and nearsurface sediments. Laguna Barva lies atop the higher Volcán Barva in the Cordillera Central, also in an old crater with well-developed cloud forest on both the inner and outer crater walls. The lake is much smaller and shallower than Laguna Cerro Chato, and given its high elevation (2,860 m) might be expected to follow the pattern of frequent mixing characteristic of other tropical lakes in cool, cloudy highlands (Löffler 1964). However, Umaña (1990, 1997b, 2010a,b) observed temperature stratification during some visits, especially be-

666 Chapter 19

tween May and August. Abundant allochthonous organic matter contributed by the surrounding forest results in low hypolimnetic oxygen levels and releases humic compounds that stain the water brown. In general, Barva’s waters are poor in dissolved minerals, but high ammonium values have been detected. As in Laguna Cerro Chato, pH values show considerable variability, from 5.5 to 7.5 (Umaña et al. 1999). Phytoplankton dominance has been found to vary over time between small cryptophytes (Cryptochrisis minor, Chroomonas sp.), desmids (Cosmarium sphaerosporum, Staurastrum paradoxum), cyanobacteria (Gloeocapsa sp.), and chlorophytes (Eutetramorus tetrasporus). Over 70 species have been documented in repeated sampling of Barva’s phytoplankton (Umaña et al. 1999), including three species of silica-scaled Chrysophyceae and Synurophyceae (Wujek et al. 1998). Interestingly, the phytoplankton community does not seem to follow an annual pattern, perhaps due to the varying influence of Caribbean and Pacific weather systems (Umaña 2010b). Surface sediment contains abundant diatoms of Brachysira brachysira, accompanied by Gomphonema gracile, along with a diversity of chryosphyte cyst morphotypes (Zeeb et al. 1996). The zooplankton of Laguna Barva consists mainly of the copepods Tropocyclops prasinus and Thermocyclops tunuis, and the cladoceran Ceriodaphnia cornuta. Water boatmen (Notonecta sp.) are also common in open water. The biota of the benthos and littoral zones include representatives of at least six groups: the amphipod Hyalella azteca, the copepod Paracyclops chiltonii, the hydrocarinid orbatid Trimalaconothus novus, the odonates Libellula sp. and Anax sp., the trichoptera Oxyethira sp. and Limnephilus sp., and chironomids (Umaña et al. 1999). Fish are absent. Laguna Hule (Fig. 19.5) is the largest of three natural lakes in a large maar, or volcanic explosion crater, located 11 km north of Volcán Poás. The maar that contains Laguna Hule is over 1.5 km in diameter, so qualifies as a caldera (Alvarado 2000); it is known as the Hule or Bosque Alegre Caldera or Crater (Gocke 1996– 97), and has protected status as the Bosque Alegre National Wildlife Refuge. Unlike the several crater lakes atop volcanoes along the crests of the NW-SE trending Cordillera de Guanacaste and Cordillera Central, the floor of the Hule Crater is lower in elevation than much of the terrain beyond the crater rim. This is the typical configuration of maars, which result from the violent degassing of magma or the interaction of groundwater and magma. Recent investigations indicate that the explosion that formed the Hule maar occurred about 6,200 cal yr BP (Salani and Alvarado 2010, Alvarado et al. 2011). A secondary pyroclastic cone and lava flow in the middle of the Hule caldera separates Laguna Hule (c. 55 ha) from

Fig. 19.5 Laguna Hule, one of three lakes in a volcanic explosion crater in the northern highland evergreen cloud forest ecosystem. The forest on the interior crater walls is little modified by human activity. Photo by Kurt Haberyan.

Laguna Congo (15 ha), and the much smaller Laguna Bosque Alegre (2.0 29.7 no 0 7.47 383 1.0 18 188 56.24 6.04 1.34 7.28 10.65 5.60 2.93

NOTE. Our previous publications reported coordinates based on the Ocotepeque 1935 datum, as used on Costa Rican topographic maps (Orvis 2002), but here we provide coordinates determined using Google Earth, which uses a WGS84 datum. Some limnological data represent a composite of multiple visits, combined so as to represent dry and wet seasons equally. Macrophyte cover is estimated using a linear scale ranging from 0 to 9, reflecting the proportion of lake surface that is covered by or underlain by macrophytes (coverage 0 reflects 0 to 10%, coverage 1 reflects 10 to 19%, etc.). nd = no data are available. See Horn and Haberyan (1993), Umaña et al. (1999), and Haberyan et al. (2003) for additional observations.

et al. 1987, Charpentier et al. 1988). Such a turnover, which may have been nearly complete, occurred prior to our visit in July 1997. At this time, the water was turbid (Secchi depth, 0.8 m, compared to 6.1 m in July 1991) and flecked with plate-like mineral crystals of unknown composition. Also in 1997, the thermocline was slightly weaker (1.7 vs. 2.8°C) and shallower (4.0 vs. 13.3 m), and most ions were more evenly distributed than in 1991. Finally, local residents reported a fish kill and rotten-egg smell in January of 1997. Although we did notice a build-up of deep water CO2 in 1991 (29 mg/L), it did not reach the levels we recorded at that time in Laguna Hule (65 mg/L). Further comparisons are in Umaña et al. (1999) and Cabassi et al. (2014). Gocke et al. (1990) studied the annual cycle of primary productivity in Laguna de Río Cuarto. Based on light/dark bottle studies, they reported that net primary productivity was 163 gC/m2 /y, with maxima in March– April and September– October and minima in July and December– February. Because net annual photosynthesis was insufficient to account for total lake respiration, it appears that much respiration (some 20%) in the lake is of terrestrial carbon.

Fish are present in Laguna de Río Cuarto (Haberyan et al. 1995), but communities have not been described in detail. Men fishing on the shore of the lake in March 2005 reported the presence of guapote (Parachromis dovii) and machaca (possibly Brycon guatemalensis), some very large (scientific names are from www.fishbase.org). Ramírez et al. (1990) carried out repeated sampling of zooplankton between February 1984 and March 1985, and found rotifers to be the most abundant group. They reported the presence of Keratella americana, Polyarthra vulgaris, Pompholix complanata, Hexarthra intermedia, Euchlanis dilatata, and Lecane sp., along with the cladocerans Diaphanosoma spinulosum and Bosmina longirostris and the copepod Microcyclops varicans. In July 1991 we sampled zooplankton with a 160 µm net, too coarse to catch rotifers, and found the cladocerans Ceriodaphnia cornuta, D. spinulosum, and Bosmina hagmanni to dominate the zooplankton (Haberyan et al. 1995). The phytoplankton in July 1991 was dominated by the cyanobacteria Merismopedia along with the chlorophytes Dactylococcopsis and Scenedesmus (Haberyan et al. 1995); a separate analysis of silica-scaled

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Fig. 19.9 Laguna Bonillita in the Caribbean lowland evergreen moist forest ecosystem. Photo by Sally Horn.

chrysophytes in the sample (Wujek et al. 1998) documented the presence of Mallomonas acaroides, M. crassisquama, and Paraphysomonas vestita. Analyses of surface sediments collected from near the center of the lake in 1991 revealed a modern diatom assemblage dominated by Fragilaria tenera with Nitzschia cf. vitrea and Navicula cf. laevissima (Haberyan et al. 1997), and a diversity of chrysophycean cysts (Zeeb et al. 1996). Lagunas Bonilla and Bonillita (Fig. 19.9) are located on a terrace of the Río Reventazón, where it cuts across the lower southeast slope of Volcán Turrialba. Their formation may have involved landslides and lahars (volcanic mudflows) as well as stream dynamics. On the basis of radiocarbon dating of plant fragments at the base of a lakesediment core, Laguna Bonillita, the smaller and higher of the two lakes, formed about 2,500 cal yr BP; the formation of Laguna Bonilla has not been reliably dated (Northrop and Horn 1996). Both lakes are relatively deep (Bonilla, 27 m, and Bonillita, 20 m), and are stratified, at least seasonally (Horn and Haberyan 1993). Neither of the lakes has permanent surface inlets, and only Bonilla has a stream

outlet. Of the two, Laguna Bonilla has been studied in more detail. Umaña (1997a) determined that the lake is oligomictic, mixing sometime between November and February, during the coolest and windiest time of the year. The lake is mildly eutrophic, with abundant cyanobacteria, low Secchi disk transparency (1.5– 1.9 m), and almost permanent anoxia in the deepest portion. Umaña (1997a) measured N to P ratios and on the basis of observed patterns suggested that the lake shifted between phosphorous limitation in the wet season and nitrogen limitation in the dry season. Further study (Petersen and Umaña 2003) revealed that nitrogen limitation becomes more important months after the onset of stratification in the late dry season. The phytoplankton of Laguna Bonilla is co-dominated by chlorophytes and cyanobacteria, while that of Bonillita is dominated by pyrrophytes and chlorophytes (Haberyan et al. 1995, Umaña 1997a). Silica-scaled chrysophytes in the Synurophyceae and Chrysophyceae have also been documented in Bonillita (Wujek et al. 1998). The zooplankton community in both lakes includes the cladocerans Bosmina hagmanni and Ceriodaphnia cornuta, but B. hagmanni

Lakes of Costa Rica 677

dominates in Bonilla and C. cornuta in Bonillita, and copepods were found only in Bonilla (Haberyan et al. 1995, Umaña 1997a). Modern diatom assemblages in surface sediments are also distinct in the two lakes (Fragilaria tenera and F. exigua in Bonilla, versus Encyonema silesiacum and Rhapalodia gibba in Bonillita), despite their proximity and similar watershed conditions (Haberyan et al. 1997). Fish are present in both lakes, but have not been studied scientifically. Laguna Gandoca is a sinuous lake located at sea level along the Caribbean coast near the border with Panama, in the Gandoca-Manzanillo National Wildlife Refuge. The lake occupies a former channel of the Río Sixaola (Denyer 1998), now occupied by the much smaller Río Gandoca. Laguna Gandoca is separated from the Caribbean by a narrow sandbar that impounds the lake, but allows seawater to percolate through. River water, being less dense, forms a stable layer on top. Consequently, stratification is very strong and deep waters are quite distinct from surface waters, being especially saline, oxygen-free, and sulfide-rich (Haberyan et al. 2003; additional data in Umaña et al. 1999). Surprisingly, the several grab samples we took of surface sediment were nearly devoid of fine organic matter. We found no diatoms in the sediments, likely due to the corrosive nature of sea water. At its seaward end, Laguna Gandoca is surrounded by Caribbean mangrove forest, but inland of the mangrove area where we sampled the lake, it is surrounded by agricultural fields and remnant areas of Caribbean lowland evergreen moist forest. The intensive banana cultivation near the lake involves significant ground and aerial spraying of pesticides, a situation that prompted Coll et al. (2004) to analyze water samples from the lake for the presence of these chemicals. They tested for the presence of 20 organochlorated and organophosphorated pesticides in six samples from each of three sampling sites in the lake and found none whatsoever. They interpreted this result in a positive light as potentially indicating that these chemicals were not reaching the lake; however, they cautioned that sampling at other times is necessary to confirm this and that the high rainfall and flooding during their sampling period could have flushed contaminants from the lake. Although preliminary analyses of Laguna Gandoca detected no pesticides, our observations at another lake in the region suggest that pesticides are influencing lake biota. Laguna Zent is an oxbow of the Río Chirripó Atlántico, positioned just downstream from the river’s emergence onto the coastal plain; like Laguna Gandoca, it is in an area of banana cultivation— actually within a plantation. Trees along the banks provide shade, but at least at our sampling site there were few aquatic macrophytes, and even consider-

ing the shade, the lake was surprisingly clear (Secchi depth, greater than the lake depth of 2.0 m). Leaf litter in the lake displayed a fine white coating, and leaves were hardly decomposed. We attribute this to the effects of pesticide runoff on aquatic decomposers, though we did not test our water sample for pesticide residues. Lake waters were very low in oxygen but enriched in carbon dioxide and sulfur. Recent diatoms in the lake are also unusual, being mainly represented by species of Navicula (N. radiosa and N. cryptocephala) and the greatest abundance (13%) of Gyrosigma spenceri we have found in Costa Rica. Sediment cores from Lagunas Bonilla and Bonillita and from swamps at the La Selva Biological Station provide evidence of the late Holocene history of the Caribbean lowland evergreen moist forest (Northrop and Horn 1996, Horn and Kennedy 2001, Kennedy and Horn 2008). As in the Pacific lowlands, pollen and charcoal in cores reveal forest clearance, maize cultivation, and agricultural burning. Stable carbon isotope signatures provide additional evidence of maize agriculture, and a means for gauging the extent of prehistoric cultivation within the watersheds (Lane et al. 2004, 2009). The continuous presence of Pentaclethra pollen in the 3,200-year record from the Cantarrana swamp at La Selva Biological Station puts a constraint on the extent of possible changes in late Holocene moisture in the region. Past drought intervals evident in paleolimnological and other records from the circum-Caribbean could not have been so intense or so long-lasting in the Caribbean lowland evergreen moist forest as to have eliminated mature Pentaclethra trees from the Cantarrana watershed.

Conclusions Modern lakes in Costa Rica range in age from a few decades or less, for most formed by human activity, to over 10,000 years, in the case of the glacial lakes atop Cerro Chirripó. Lakes are ephemeral features over geological time scales, and lakes that predate Costa Rica’s modern glacial lakes have been changed or buried by time and by geomorphic processes. A few old lakes have been filled in to become bogs; the existence of others is marked by the presence of ancient lake sediments in areas now too dry to support lakes or wetlands of any kind. We can expect that nearly every lake in Costa Rica has been affected, to a greater or lesser degree, by changes in its watershed, whether due to climate change or to humans. From the study of lake sediments we are developing a nationwide chronology of such changes, and from this it is clear that prehistoric humans had major influences, beginning by at least 5,500 years ago in northwestern Costa Rica, where lake sediments document the

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first cultivation of maize and associated forest clearance and agricultural burning, and extending to the Panamanian border and across the Central Highlands to the Caribbean lowlands. It is equally clear that human impacts will continue, and will become increasingly widespread and of great potential threat to aquatic environments and biota, whether due to sewage, pesticides, eutrophication, aquaculture, erosion, the introduction of alien species, or resource depletion (e.g., see TNC 2009). Such localized threats can, we hope, be managed in part through community-based efforts to protect resources, and through improved land use policies and enforcement. In contrast, the larger, more subtle threats of global warming will be more difficult to mitigate; even now, the high-altitude lakes on Cerro Chirripó may be already responding. Both sets of threats require much more detailed, and more frequent, scientific observations, because sound responses must be based on ecological knowledge. The challenge for Costa Rica’s freshwater resources is, as in many

nations, the balancing of water quality and aquatic biodiversity in the long term with human needs in the short term.

Acknowledgments Our research on Costa Rican lakes and their sediments has been supported by grants from the National Geographic Society, the National Science Foundation (SES-9111588, BCS-0242286, DGE-0538420), The A.W. Mellon Foundation, the Association of American Geographers, the University of Tennessee, Northwest Missouri State University, and Troy State University. We thank the many people who co-authored or otherwise contributed to the work we reviewed here, most especially Gerardo Umaña, Maureen Sánchez, and Ken Orvis, without whose collaboration our work would have been vastly more difficult, and much less fun. We also thank the government of Costa Rica and many private landowners for granting permission for our studies.

References Alvarado, G.E. 1989. Los Volcanes de Costa Rica: Geología, Historia y Riqueza Natural. 1st ed. San José, Costa Rica: Editorial Universidad Estatal y Distancia. Alvarado, G.E. 2000. Los Volcanes de Costa Rica: Geología, Historia y Riqueza Natural. 2nd ed. San José, Costa Rica: Editorial Universidad Estatal y Distancia. Alvarado, G.E., R. Mora, and G. Peraldo. 2003. The June 2000 Arancibia debris avalanche and block slide. Landslide News 14/15: 29– 32. Alvarado, G.E., G.J. Soto, F.M. Salani, P. Ruiz, and L. Hurtado de Mendoza. 2011. The formation and evolution of Hule and Río Cuarto maars, Costa Rica. Journal of Volcanology and Geothermal Research 201: 342– 56. Alvarado, G.E., E. Vega, J. Chaves, and M. Vásquez. 2004. Los grandes deslizamientos (volcánicos y novolcánicos) de tipo debris avalanche en Costa Rica. Revista Geológica de América Central 30: 83– 99. Anchukaitis, K.J., M.N. Evans, N.T. Wheelwright, and D.P. Schrag. 2008. Stable isotope chronology and climate signal calibration in neotropical montane cloud forest trees. Journal of Geophysical Research 113: G03030. DOI: 10.1029/2007JG000613. Anchukaitis, K.J., and S.P. Horn. 2005. A 2000-year reconstruction of forest disturbance from southern Pacific Costa Rica. Palaeogeography Palaeoclimatology Palaeoecology 221(1– 2): 35– 54. Anderson, E.P., C.M. Pringle, and M. Roja. 2006. Transforming tropical rivers: an environmental perspective on hydropower development in Costa Rica. Aquatic Conservation: Marine and Freshwater Ecosystems 16: 679– 73. Arford, M.R. 2001. Late Holocene environmental history and tephrostratigraphy in northwestern Costa Rica: a 4000 year record from Lago Cote. M.S. thesis, University of Tennessee. Knoxville, TN.

Arford, M.R., and S.P. Horn. 2004. Pollen evidence of the earliest maize agriculture in Costa Rica. Journal of Latin American Geography 3(1): 108– 15. Armoudlian, A., and C. De Moraes. 1994. Preliminary limnological study of Lake Pocosol. In B. Young and S. Sargent, eds., Coursebook for Tropical Biology: An Ecological Approach, 99– 103. San José, Costa Rica: Organization for Tropical Studies. Baker, R.G.E. 1987. Notes on the high altitude freshwater lakes of Volcán Rincón de la Vieja National Park, northern Costa Rica. Brenesia 27: 47– 54. Bart, D. 1999. Report on the reference conditions for the restoration of the marshes near the Las Cruces Biological Field Station, Costa Rica. Unpublished report submitted to the Las Cruces Biological Station, Organization for Tropical Studies, Costa Rica. Bergoeing, J.P. 1978. La Fotografía Aérea y su Aplicación a la Geomorfología de Costa Rica. San José, Costa Rica: Instituto Geográfico Nacional. Bergoeing, J.P., and L.G. Brenes. 1978. Laguna de Hule, una caldera volcánica. Informe Semestral, Instituto Geográfico Nacional de Costa Rica (Jul.– Dec.): 59– 63. Bolaños, B.J. 1979. Estudio preliminar sobre el cultivo de híbridos de Tilapia (Tilapia hornorum x T. mossambica) con gallinaza y superfosfato triple, en Costa Rica. Revista Lationamericana de Acuicultura 2: 22– 28. Boza, M.A., and J.H. Cevo. 1998. Parques Nacionales y Otras Áreas Protegidas de Costa Rica / Costa Rican National Parks and Other Protected Areas. San José, Costa Rica: INCAFO Costa Rica. Bravo, J., and L. Ocampo. 1993. Humedales de Costa Rica. Heredia, Costa Rica: Universidad Nacional de Costa Rica.

Lakes of Costa Rica 679 Bumby, M.J. 1982. A survey of aquatic macrophytes and chemical qualities of nineteen localities in Costa Rica. Brenesia 19/20: 487– 535. Cabassi, J., F. Tassi, F. Mapelli, S. Borin, S. Calabrese, D. Rouwet, G. Chiodini, R. Marasco, B. Chouaia, R. Avino, O. Vaselli, G. Pecoraino, F. Capecchiacci, G. Bicocchi, S. Caliro, C. Ramírez, and R. MoraAmador. 2014. Geosphere-biosphere interactions in bio-activity volcanic lakes: evidences from Hule and Río Cuarto (Costa Rica). PLOS ONE 9(7): e102456. Camacho, L. 1985. Variación estacional de las algas planctónicas del Lago de Río Cuarto, Alajuela, Costa Rica. Lic. thesis, University of Costa Rica. San José, Costa Rica. Charpentier, C., F.A. Tabash, I.A. Fallas, J.C. Zumbado, L. Camacho, and E. Ramírez. 1988. Variación estacional en el lago de Río Cuarto, provincia de Alajuela, Costa Rica. I. Limnología físico-química. Uniciencia 5(1/2): 77– 85. Chaverri, A., and A.M. Cleef. 2005. Comunidades vegetales de los páramos de los macizos de Chirripó y Buenavista, Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 577– 92. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad. Chávez, L., and K.A. Haberyan. 1996. Diatom assemblages from the Camastro diatomite, Costa Rica. Revista de Biología Tropical 44(2): 899– 902. Clark, K.L., R.O. Lawton, and P.R. Butler. 2000. The physical environment. In N.M. Nadkarni and N.T. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 15– 38. New York: Oxford University Press. Clement, R.M., and S.P. Horn. 2001. Pre-Columbian land use history in Costa Rica: a 3000-year record of forest clearance, agriculture, and fires from Laguna Zoncho. Holocene 11: 419– 26. Cochard, R., and B.R. Jackes. 2005. Seed ecology of the invasive tropical tree Parkinsonia aculeata. Plant Ecology 180: 13– 31. Cohen, A.S. 2003. Paleolimnology: The History and Evolution of Lake Systems. New York: Oxford University Press. Coll, M., J. Cortés, and D. Sauma. 2004. Características físicos-químicas y determinación de plaguicidas en el agua de la laguna de Gandoca, Limón, Costa Rica. Revista de Biología Tropical 52(suppl. 2): 33– 42. Collado, C.M. 1983. Costa Rican freshwater zooplankton and zooplankton distribution in Central America and the Caribbean. M.S. thesis, University of Waterloo. Ontario, Canada. Collado, C.M., D. Defaye, B.H. Dussart, and C.H. Fernando. 1984a. The freshwater copepoda (Crustacea) of Costa Rica with notes on some species. Hydrobiologia 119: 89– 99. Collado, C.M., C.H. Fernando, and D. Sephton. 1984b. The freshwater zooplankton of Central America and the Caribbean. Hydrobiologia 113: 105– 19. Denyer, P. 1998. Historic-prehistoric earthquakes, seismic hazards, and Tertiary and Quaternary geology of the Gandoca-Manzanilla National Wildlife Refuge, Limón, Costa Rica. Revista de Biología Tropical 46(suppl. 6): 237– 50. Dickman, M., and H. Nanne. 1987. Impacts of tilapia grazing on plankton composition in artificial ponds in Guanacaste province, Costa Rica. Journal of Freshwater Ecology 4(1): 93. Driese, S.G., K.H. Orvis, S.P. Horn, Z.H. Li, and D.S. Jennings. 2007. Paleosol evidence for Quaternary uplift and for climate and ecosystem changes in the Cordillera de Talamanca, Costa Rica. Palaeogeography, Palaeoclimatology, Palaeoecology 248(1– 2): 1– 23. Dussart, B.H., and C.H. Fernando. 1986. Remarks on two species of

copepods in Costa Rica, including a description of a new species of Tropocyclops. Crustaceana 50(1): 39– 44. Filippelli, G., C. Souch, S.P. Horn, and D. Newkirk. 2010. The preColumbian footprint on terrestrial nutrient cycling in Costa Rica: insights from phosphorous in a lake sediment record. Journal of Paleolimnology 43: 843– 56. Fuentes, G., A.B. Azofeifa, and S. Aguilar. 2006. Bibliografía sobre la producción científica del Centro de Investigación en Ciencias del Mar y Limnología— CIMAR de la Universidad de Costa Rica. Costa Rica: Organization for Tropical Studies, Ciudad de la Investigación. Gocke, K. 1996– 97. Basic morphometric and limnological properties of Laguna Hule, a caldera lake in Costa Rica. Revista de Biología Tropical 44(3)/45(1): 537– 48. Gocke, K., W. Bussing, and J. Cortés. 1987. Morphometric and basic limnological properties of the Laguna de Río Cuarto, Costa Rica. Revista de Biología Tropical 35(2): 277– 85. Gocke, K., W. Bussing, and J. Cortés. 1990. The annual cycle of primary productivity in Laguna de Río Cuarto, Costa Rica. Revista de Biología Tropical 38(2B): 387– 94. Gocke, K., E. Lahman, G. Rojas, and J. Romero. 1981. Morphometric and basic limnological data of Laguna Grande de Chirripó, Costa Rica. Revista de Biología Tropical 29(1): 165– 74. Haberyan, K.A. 1998. The effect of volcanic ash influx on the diatom community of Lake Tanganyika, East Africa. Transactions of the Missouri Academy of Science 32: 102– 5. Haberyan, K.A., and S.P. Horn. 1999. A 10,000-year diatom record from a glacial lake in Costa Rica. Mountain Research and Development 19(1): 63– 70. Haberyan, K.A., and S.P. Horn. 2005. Diatom paleoecology of Laguna Zoncho, Costa Rica. Journal of Paleolimnology 33(3): 361– 69. Haberyan, K.A., S.P. Horn, and M.R. Arford. 2005. Diatom shifts at Laguna San Pablo, Costa Rica, over the last 8000 years. Poster presented at the 18th North American Diatom Symposium, Mobile, Alabama. Haberyan, K.A., S.P. Horn, and B.F. Cumming. 1997. Diatom assemblages from Costa Rican lakes: an initial ecological assessment. Journal of Paleolimnology 17: 263– 74. Haberyan, K.A., S.P. Horn, and G. Umaña. 2003. Basic limnology of fiftyone lakes in Costa Rica. Revista de Biología Tropical 51(1): 107– 22. Haberyan, K.A., G. Umaña, C. Collado, and S.P. Horn. 1995. Observations on the plankton of some Costa Rican lakes. Hydrobiologia 312: 75– 85. Hairston, N.G., Jr. 1979. The adaptive significance of color polymorphism in two species of Diaptomus (Copepoda). Limnology and Oceanography 24: 15– 37. Hargraves, P.E., and R. Víquez. 1981. Dinoflagellate abundance in the Laguna Botos, Poás Volcano, Costa Rica. Revista de Biología Tropical 29(2): 257– 64. Herrera, W. 1992. Mapa-Guía de la Naturaleza Costa Rica / Costa Rican Nature Atlas-Guidebook. San José, Costa Rica: INCAFO Costa Rica. Hodell, D.A., M. Brenner, and J.H. Curtis. 2000. Climate change in the northern American tropics and subtropics since the last ice age. In D.L. Lentz, ed., Landscape Transformations in the Pre-Columbian Americas, 13– 38. New York: Columbia University Press. Hodell, D.A., M. Brenner, J.H. Curtis, and T.P. Guilderson. 2001. Solar forcing of drought frequency in the Maya lowlands. Science 292: 1367– 70.

680 Chapter 19 Hooghiemstra, H., A.M. Cleef, G.W. Noldus, and M. Kappelle. 1992. Upper Quaternary vegetation dynamics and palaeoclimatogy of the La Chonta bog area (Cordillera de Talamanca, Costa Rica). Journal of Quaternary Science 7(3): 205– 25. Horn, S.P. 1989a. Prehistoric fires in the Chirripó highlands of Costa Rica: sedimentary charcoal evidence. Revista de Biología Tropical 37(2): 139– 48. Horn, S.P. 1989b. The Inter-American Highway and human disturbance of páramo vegetation in Costa Rica. Yearbook of the Conference of Latin Americanist Geographers 15: 13– 22. Horn, S.P. 1993. Postglacial vegetation and fire history in the Chirripó páramo of Costa Rica. Quaternary Research 20: 107– 16. Horn, S.P. 2001. The age of the Hule explosion crater, Costa Rica, and the timing of subsequent tephra eruptions: evidence from lake sediments. Revista Geológica de América Central 24: 57– 66. Horn, S.P. 2006. Pre-Columbian maize agriculture in Costa Rica: pollen and other evidence from lake and swamp sediments. In J. Staller, R. Tykot, and B. Benz, eds., Histories of Maize: Multidisciplinary Approaches to the Prehistory, Biogeography, Domestication, and Evolution of Maize, 367– 80. San Diego: Elsevier Press. Horn, S.P. 2007. Late Quaternary lake and swamp sediments: recorders of climate and environment. In J. Bundschuh and G.E. Alvarado, eds., Central America: Geology, Resources, Hazards, vol. 1. Leiden, Netherlands: Taylor & Francis/Balkema. Horn, S.P., and K.A. Haberyan. 1993. Physical and chemical properties of Costa Rican Lakes. National Geographic Research and Exploration 9(1): 86– 103. Horn, S.P., and L.M. Kennedy. 2001. Pollen evidence of maize cultivation 2700 B.P. at La Selva Biological Station, Costa Rica. Biotropica 33(1): 191– 96. Horn, S.P., and L.M. Kennedy. 2006. Pollen evidence of the prehistoric presence of cattail ( Typhaceeae: Typha) in Palo Verde National Park, Costa Rica. Brenesia 66: 85– 87. Horn, S.P., and B.L. League. 2005. Registros de sedimentos lacustres de la vegetación del Holoceno e historia del fuego en el páramo de Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 253– 73. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad. Horn, S.P., K.H. Orvis, and K.A. Haberyan. 1999. Investigación limnológica y geomorfológica de lagos glaciares del Parque Nacional Chirripó, Costa Rica. Revista Informe Semestral (Instituto Geográfico Nacional de Costa Rica) 35: 95– 106. Horn, S.P., K.H. Orvis, and K.A. Haberyan. 2005. Limnología de las lagunas glaciales en el páramo del Chirripó, Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 161– 81. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad. Horn, S.P., and R.L. Sanford. 1992. Holocene fires in Costa Rica. Biotropica 24: 354– 61. Horne, A.J., and C.R. Goldman. 1994. Limnology. 2nd ed. New York: McGraw Hill. Islebe, G.A., and H. Hooghiemstra. 1997. Vegetation and climate history of montane Costa Rica since the last glacial. Quaternary Science Reviews 16(6): 589– 604. Jiménez, C.E., and M. Springer. 1994. Vertical distribution of benthic macrofauna in a Costa Rican crater lake. Revista de Biología Tropical 42(1/2): 175– 79. Jiménez, C.E., and M. Springer. 1996. Depth related distribution of ben-

thic macrofauna in a Costa Rican crater lake. Revista de Biología Tropical 44(2): 673– 78. Jones, J.R., K. Lohman, and G. Umaña. 1993. Water chemistry and trophic state of eight lakes in Costa Rica. Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 25(2): 899– 905. Kennedy, L.M., and S.P. Horn. 2008. A late Holocene pollen and charcoal record from La Selva Biological Station, Costa Rica. Biotropica 40(1): 11– 19. Kling, G.W., M.A. Clark, H.R. Compton, J.D. Devine, W.C. Evans, A.M. Humphrey, E.J. Koenigsberg, J.P. Lockwood, M.L. Tuttle, and G.N. Wagner. 1987. The 1986 Lake Nyos gas disasters in Cameroon, West Africa. Science 236: 169– 75. Kohkemper, J. 1954. Bosquejo limnológico de la laguna “Del Misterio.” Ing. thesis, University of Costa Rica. San José, Costa Rica. Lachniet, M.S., Y. Asmerom, S.J. Burns, W.P. Patterson, V.J. Polyak, and J.O. Seltzer. 2004. Tropical response to the 8200 yr B.P. cold event? Speleothem isotopes indicate a weakened early Holocene monsoon in Costa Rica. Geology 32(11): 957– 60. Lachniet, M.S., and G.O. Seltzer. 2002. Late Quaternary glaciation of Costa Rica. Geological Society of America Bulletin 114(5): 547– 58. Lane, C.S., and S.P. Horn. 2013. Terrestrially derived n-alkane δD evidence of shifting Holocene paleohydrology in highland Costa Rica. Arctic, Antarctic, and Alpine Research 45(3): 342– 49. Lane, C.S., S.P. Horn, and M.T. Kerr. 2014. Beyond the Mayan lowlands: impacts of the Terminal Classic Drought in the Caribbean Antilles. Quaternary Science Reviews 86: 89– 98. Lane, C.S., S.P. Horn, and C.I. Mora. 2004. Stable carbon isotope ratios in lake and swamp sediments as a proxy for prehistoric forest clearance and crop cultivation in the neotropics. Journal of Paleolimnology 32(4): 375– 81. Lane, C.S., S.P. Horn, C.I. Mora, K.H. Orvis, and D.B. Finkelstein. 2011. Sedimentary stable carbon isotope evidence of late Quaternary vegetation and climate change in highland Costa Rica. Journal of Paleolimnology 45(3): 323– 38. Lane, C.S., S.P. Horn, Z.P. Taylor, and C.I. Mora. 2009. Assessing the scale of prehistoric human impact in the neotropics using stable carbon isotope analyses of lake sediments: a test case from Costa Rica. Latin American Antiquity 20(1): 120– 33. Lawton, R.O., U.S. Nair, R.A. Pielke Sr., and R.M. Welch. 2001. Climatic impact of tropical lowland deforestation on nearby montane cloud forests. Science 294: 584– 87. League, B.L., and S.P. Horn. 2000. A 10,000 year record of páramo fires in Costa Rica. Journal of Tropical Ecology 16: 747– 52. Löffler, H. 1964. The limnology of tropical high-mountain lakes. Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 15: 176– 93. Löffler, H. 1972. Contribution to the limnology of high mountain lakes in Central America. Internationale Revue der Gesamten Hydrobiologie 57(3): 397– 408. Martin, P.S. 1964. Paleoclimatology and a tropical pollen profile. In Report on the VI International Congress on the Quaternary (Warsaw 1961) 2: 319– 23. Messerli, B. 2001. Editorial: The International Year of Mountains (IYM), the Mountain Research Initiative (MRI) and PAGES. PAGES (Past Global Changes) News 9(3): 2. Nadkarni, N.M., and N.T. Wheelwright. 2000a. Introduction. In N.M.

Lakes of Costa Rica 681 Nadkarni and N.T. Wheelwright, eds., Monteverde: Ecology and Conservation of a Tropical Cloud Forest, 3– 13. New York: Oxford University Press. Nadkarni, N.M., and N.T. Wheelwright, eds. 2000b. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. New York: Oxford University Press. Nicholson, R.A., P.D. Roberts, and P.J. Baxter. 1996. Preliminary studies of acid and gas contamination at Poás volcano, Costa Rica. In A.J. Appleton, R. Fuge, and G.J.H. McCall, eds., Environmental Geochemistry and Health, 239– 40. Geological Society of America Special Publication 113. Northrop, L.A., and S.P. Horn. 1996. PreColumbian agriculture and forest disturbance in Costa Rica: palaeoecological evidence from two lowland rainforest lakes. Holocene 6(3): 289– 99. Orvis, K.H. 2002. GPS Locations and Costa Rican Topo Maps. Unpublished report. Knoxville, Tennessee: University of Tennessee. 23 pp. http://trace.tennessee.edu/utk_geogpubs/5/ Orvis, K.H., and S.P. Horn. 2000. Quaternary glaciers and climate on Cerro Chirripó, Costa Rica. Quaternary Research 54: 24– 37. Petersen, R.R., and G. Umaña. 2003. Nitrogen and phosphorous limitation in lakes Bonilla and Bonillita, Costa Rica. Verhandlungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 28(3): 1520– 25. Pounds, J.A., M.P.L. Fogden, and J.H. Campbell. 1999. Biological response to climate change on a tropical mountain. Nature 398: 611– 15. Ramírez, E. 1985. Variaciones estacionales de la comunidad zooplanctónica del Lago de Río Cuarto, Alajuela, Costa Rica. Lic., informe de trabajo dirigida, University of Costa Rica. San José, Costa Rica. Ramírez, E., and E. Camacho. 1991. Estudio limnológico preliminar de la Laguna Hule, Costa Rica. Uniciencia 8(1– 2): 17– 25. Ramírez, E., F. Tabash, and C. Charpentier. 1990. Variación estacional en el lago de Río Cuarto, provincia de Alajuela, Costa Rica. Uniciencia 7(1/2): 19– 25. Reimer, P.J., M.G.L. Baillie, E. Bard, A. Bayliss, J.W. Beck, C.J.H. Bertrand, P.G. Blackwell, C.E. Buck, G.S. Burr, K.B. Culter, P.E. Damon, R.L. Edwards, R.G. Fairbanks, M. Friedrich, T.P. Guilderson, A.G. Hogg, K.A. Hughen, B. Kromer, F.G. McCormac, S.W. Manning, C.B. Ramsey, R.W. Reimer, S. Remmele, J.R. Southon, M. Stuiver, S. Talamo, F.W. Taylor, J.J. van der Plicht, and C.E. Weyhenmeyer. 2004. IntCal04 terrestrial radiocarbon age calibration, 26– 0 ka BP. Radiocarbon 46: 1029– 58. Richardson, J.L., and D. Livingstone. 1962. An attack by a Nile crocodile on a small boat. Copeia 1962(1): 203– 4. Rodgers, J.C., III, and S.P. Horn. 1996. Modern pollen spectra from Costa Rica. Palaeogeography, Palaeoclimatology, Palaeoecology 124(1– 2): 53– 71. Salani, F.M., and G.E. Alvarado. 2010. El maar poligenético de Hule (Costa Rica). Revisión de su estratigrafía y edades. Revista Geológica de América Central 43: 97– 118. Sánchez-Azofeifa, G.A., R.C. Harriss, A.L. Storrier, and T. Camino-Beck. 2002. Water resources and regional land cover change in Costa Rica: impacts and economics. Water Resources Development 18(3): 409– 24. Siebert, L., G.E. Alvarado, J.W. Vallance, and B. van Wyk de Vries. 2006. Large-volume volcanic edifice failures in Central America and asso-

ciated hazards. In W.I. Rose, G.J.S. Bluth, M.J. Carr, J.W. Ewert, L.C. Patino, and J.W. Vallance, eds., Volcanic Hazards in Central America, 1– 26. Geological Society of America Special Paper 412. Somarribas, G., and J. Bravo. 1999. Una propuesta metodológica participativa para la protección y conservación de humedales. Avance del Proyecto: “Refugio de Vida Silvestre ‘Laguna’ Mata Redonda, Guanacaste, Costa Rica.” Standley, P.C. 1936– 37. Flora of Costa Rica. Field Museum of Natural History Botany Series 18(1– 4): 1– 1571. Stuiver, M., and P.J. Reimer. 1993. Extended C-14 database and revised Calib 3.0 C-14 age calibration program. Radiocarbon 35: 215– 30. Tabash, F.A., and E. Guadamuz. 2000. A management plan for the sport fishery of Parachromis dovii (Pisces: Cichlidae) in Hule lake, Costa Rica. Revista de Biología Tropical 48(2/3): 473– 85. Tassi, F., O. Vaselli, E. Fernández, E. Duarte, M. Martínez, A. Delgado Huertas, and F. Bergamaschi. 2009. Morphological and geochemical features of crater lakes in Costa Rica: an overview. Journal of Limnology 68(2): 193– 205. Taylor, Z.P., S.P. Horn, and D.B. Finkelstein. 2013. Pre-Hispanic agricultural decline prior to the Spanish Conquest in southern Central America. Quaternary Science Reviews 73: 196– 200. Telford, R.J., P. Barker, S. Metcalfe, and A. Newton. 2004a. Lacustrine responses to tephra deposition: examples from Mexico. Quaternary Science Reviews 23: 2337– 53. Telford, R.J., E. Heegaard, and H.J.B. Birks. 2004b. The intercept is a poor estimate of a calibrated radiocarbon age. Holocene 14(2): 296– 98. TNC ( The Nature Conservancy). 2009. Evaluación de Ecorregiones de Agua Dulce de Mesoamérica: Sitios Prioritarios para la Conservación en las Ecorregiones de Chiápas a Darién. San José, Costa Rica: The Nature Conservancy. 515 pp. Tyson, P. 2000. The Eighth Continent: Life, Death, and Discovery in the Lost World of Madagascar. New York: William Morrow. Ulloa, J., O. Alpírez, and J. Cabrera. 1988. Presencia de Bryconamericus acleroparius, Peociliopsis turrubarensis y Cichlasoma nicaraguense en el Embalse Arenal, Costa Rica. Revista de Biología Tropical 36: 171– 72. Ulloa, J., P. Cabrera, and M. Mora. 1989. Composición, diversidad y abundancia de peces en el Embalse Arenal, Guanacaste, Costa Rica. Revista de Biología Tropical 37: 127– 32. Umaña, G. 1985. Phytoplankton species diversity of 27 lakes and ponds of Costa Rica (Central America). M.S. thesis, Brock University. Ontario, Canada. Umaña, G. 1988. Fitoplancton de las lagunas Barba, Fraijanes y San Joaquín, Costa Rica. Revista de Biología Tropical 36(2B): 471– 77. Umaña, G. 1990. Limnología básica de la Laguna del Barva. Revista de Biología Tropical 38(2B): 431– 35. Umaña, G. 1993. The planktonic community of Laguna Hule, Costa Rica. Revista de Biología Tropical 41(3A): 499– 507. Umaña, G. 1997a. Basic limnology of Lago Bonilla, a tropical lowland lake. Revista de Biología Tropical 45(4): 1429– 37. Umaña, G. 1997b. Variabilidad temporal en tres lagos volcánicos. In Memoria, Jornadas de Investigación 1997. San José, Costa Rica: Universidad de Costa Rica. 25 pp. Umaña, G. 2001. Limnology of Botos lake, a tropical crater lake in Costa Rica. Revista de Biología Tropical 49(suppl. 2): 1– 10. Umaña, G. 2010a. Comparison of basic limnological aspects of some

682 Chapter 19 crater lakes in the Cordillera Volcánica Central, Costa Rica. Revista Geológica de America Central 43: 137– 46. Umaña, G. 2010b. Temporal variation of phytoplankton in a small tropical crater lake. Revista de Biología Tropical 58(4): 1405– 19. Umaña, G. 2014a. Phytoplankton variability in Lake Fraijanes, Costa Rica, in response to local weather variation. Revista de Biología Tropical 62(2): 483– 94. Umaña, G. 2014b. Ten years of limnological monitoring of a modified natural lake in the tropics: Cote Lake, Costa Rica. Revista de Biología Tropical 62(2): 567– 78. Umaña, G., and C. Collado. 1990. Asociación planctónica en el Embalse Arenal, Costa Rica. Revista de Biología Tropical 38(2A): 311– 21. Umaña, G., K.A. Haberyan, and S.P. Horn. 1999. Limnology in Costa Rica. In B. Gopal and R.W. Wetzel, eds., Limnology in Developing Countries, vol. 2, 33– 62. New Delhi: New Delhi International Scientific Publications. Umaña, G., and C.E. Jiménez. 1995. The basic limnology of a low altitude tropical crater lake: Cerro Chato, Costa Rica. Revista de Biología Tropical 43(1– 3): 131– 38. Umaña, G., F. Villalobos, and B. Bofill. 1997. Distribución vertical de zooplancton en el Embalse Arenal, Costa Rica. Revista de Biología Tropical 45(2): 923– 26. Vargas, J.A. 2004. Preface: aquatic ecosystems of Costa Rica III. Revista de Biología Tropical 52(suppl. 2): xi– xiii. Weber, H. 1959. Los Páramos de Costa Rica y su Concatenación Fitogeográfico con los Andes Suramericanos. San José, Costa Rica: Instituto Geográfico Nacional.

Woodruff, S.D. 2001. COADS updates including newly digitized data and the blend with the UK Meteorological Office marine data bank and quality control in recent COADS updates. In Proceedings of Workshop on Preparation, Processing and Use of Historical Marine Meteorological Data, Tokyo (November 28– 29, 2000), 9– 13 & 49– 53. Japan Meteorological Agency and the Ship & Ocean Foundation, Tokyo. Woodruff, S.D., H.F. Díaz, J.D. Elms, and S.J. Worley. 1998. COADS release 2 data and metadata enhancements for improvements of marine surface flux fields. Physics and Chemistry of the Earth 23: 517– 27. Wu, J., D.F. Porinchu, S.P. Horn, and K.A. Haberyan. 2015. The modern distribution of chironomid sub-fossils (Insecta: Diptera) in Costa Rica and the development of a regional chironomid-based temperature inference model. Hydrobiologia 742: 107– 27. Wujek, D.E. 1984. Scale bearing Chrysophyceae (Mallomonadaceae) from north-central Costa Rica. Brenesia 22: 309– 13. Wujek, D.E., R.E. Clancy Jr., and S.P. Horn. 1998. Silica-scaled Chrysophyceae and Synurophyceae from Costa Rica. Brenesia 49– 50: 1– 19. Wydrzycka, U.M. 1996. Las especies de Trachelomonas (Algas: Euglenophyta) en tres lagunas volcánicas de Costa Rica. Revista de Biología Tropical 44(2): 477– 84. Zeeb, B.A., J.P. Smol, and S.P. Horn. 1996. Chrysophycean stomatocysts from Costa Rican tropical lake sediments. Nova Hedwigia 63(3– 4): 279– 99.

Chapter 20 Bogs, Marshes, and Swamps of Costa Rica

Jorge A. Jiménez1

Introduction Costa Rica has a high diversity of freshwater wetlands, ranging from the highland peat bogs in the mountainous Talamancas and the marshes of the Pacific lowlands to the often-seasonal swamps dominated by palms and other forest trees thriving along the coasts (Fig. 20.1). Most of the available information regarding bogs, marshes, and swamps in Costa Rica is restricted to descriptive studies where lists of plant species and studies on forest structure abound. Close to 400 plant species have been listed for these ecosystems (Crow 2002, Córdoba et al. 1998, Gómez 1984, Soto and Arias 1994). Studies on their ecological or functional aspects are, however, mostly absent. Fauna is listed in a few studies but most fauna cited is not restricted to marsh or swamp ecosystems. Even knowledge on the total extent of these ecosystems in the country is highly fragmentary and controversial. Bogs, restricted mostly to the Talamanca mountains, cover around 235 ha according to estimations based on satellite imagery and information provided by organizations such as INBio, SINAC/MINAE, OTS, and IUCN. Estimates for other types of freshwater wetlands coverage are highly variable (Rodríguez 2004, Bravo et al. 1996, Córdoba et al. 1998, Sylvander 1978, Ellison 2004). Back in the mid-seventies, close to 300,000 ha were reported: about 139,000 ha of these as forest swamps, close to 96,200 ha as marshes and nearly 60,000 ha as palm swamps (Sylvander 1978). More recent estimates using satellite image analysis indicate a total of around 222,000 ha, where forest swamps comprised 79,650 ha, palm swamps about 92,800 ha, and 1

Fundación MarViva, Apartado 020-6151, Santa Ana, Costa Rica

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marshes around 49,650 ha. Serrano-Sandí et al. (2013) estimated that palm swamps in Costa Rica totaled 53,931 ha, which they reported to be 16.2% of the total wetland area in the country (332,000 ha). Most of these data are, however, lacking field verification and they are likely to be overestimations. Present total coverage of freshwater wetlands is most likely in the order of 140,000 ha for the whole country (Programa Estado de la Nación 2003), with forested wetlands comprising about half of this area and marshes covering close to 30,000 ha. Estimations of vegetation cover have always been a challenge: while different wetland types are distinguished in such estimations, in reality they do not always form clear and distinct units in the field. Many marshes as well as palm and forest swamps are found growing together in a single area with considerable overlapping areas. Even very small changes in topographic elevation and sedimentation may result in structural and functional changes within such wetlands. Geo-morphological processes trigger those changes and fluctuations in water flow quantity and quality and may also interact in determining the dominant type of wetland vegetation. Excluding bogs that are found between 1,200– 3,100 m a.s.l, most freshwater wetlands are found below 200 m a.s.l., and in the coastal and northern plains. Here, wetlands have been giving way to agriculture and pasturelands at very rapid rates. Particularly marshes under seasonal climates have shown a significant decrease in area, during the past three decades. In the Tempisque watershed, for instance, seasonal marshes in 1975 amounted to around 33,000 ha. By the year 2000 only 7,500 ha (22%) remained. Drainage for sugar cane and rice plantations, as well as for pasture-

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lands, has been the main cause for the loss of the Tempisque wetlands. It is, therefore, not surprising that existing cover estimations are highly controversial depending on the methods used, year of analysis, and extent of field verification done.

Highland Bogs Highland bogs, also known as “raised ombrothermic bogs” (Gómez 1986) or “turberas de altura,” are found between 1,200– 3,100 m a.s.l., along the continental divide of the Cordillera de Talamanca (Brak et al. 2005). These peatforming bogs are restricted to small and poorly drained depressions subject to seasonal flooding. With an area just over 235 ha, this ecosystem is very restricted in the country. The largest patches are found in the Dúrika sabanas (Fig. 20.2) and the Cerro Utyum area (Weston 1981, cited

by Brak et al. 2005, and information available at INBio’s website, www.inbio.ac.cr, and maps prepared by the IUCN). Flooding in these bogs is closely related to the seasonal precipitation patterns but is also dependent on vegetation coverage in the surrounding areas (Islebe et al. 2005). Water table levels determine the intensity and duration of floodings, which cause an accumulation of peat under anoxic conditions. Acid waters typify these bogs (Horn and Haberyan, chapter 19 of this volume). The low acidity (pH) levels of the bogs’ waters usually affect embryonic and larval development of anuran amphibians (Saber and Dunson 1978) as well as the development of tall vegetation (Brak et al. 2005). Most bog areas in the country are found at the headwaters of the Lari, Volcán, Telire, Ceibo, Orosi, and Savegre rivers. However, the limited extension of these bogs result in a relatively low impact on the overall hydrology of these watersheds.

Fig. 20.1 Map of the main wetlands in Costa Rica. Map prepared by Marco V. Castro.

Bogs, Marshes, and Swamps of Costa Rica 685

Fig. 20.2 Highland peat bog in the Sabana de Dúrika, La Amistad International Park (PILA), Costa Rica. Two arborescent Blechnum buchtieni ferns with erect living and pendant decaying fronds dominate in the front. Photo by Luis González Arce.

Palynological and paleoecological studies in these ecosystems are available from bogs adjacent to the InterAmerican Highway (Hooghiemstra et al. 1992, Islebe et al. 1996, Rodgers and Horn 1996). These studies indicate that changes in hydrological conditions have resulted in vegetational changes. Fire events that took place during the Holocene have been connected to climatic variability in that period (Horn 1989, 1993). Repeated fire in the surrounding páramos can affect these bogs by affecting their water retention properties in the soil. Although Horn and Haberyan (chapter 19 of this volume) present limnological data for some pond-like bogs (e.g., the Tres de Junio pond, along the Inter-American Highway south of Cartago; see Fig. 20.3), no detailed hydrological studies are available for these ecosystems yet. While the highland bogs share a large amount of structural

and floristic elements with the páramo vegetation surrounding them, they can be differentiated, however (Kappelle and Horn, chapter 15 of this volume). Over 100 species of forbs, grasses, and sedges have been reported from the high-elevation bogs of Costa Rica (Gómez 1984). These species are typically distributed in a zonal pattern that relates to the bog’s water depth. Brak et al. (2005), Kappelle (1996), Hooghiemstra et al. (1992), and Gómez (1984) have described in detail this zonal pattern: at the bog edges, there is a zone containing species such as the bamboo Chusquea subtessellata, the grass Cortaderia nitida, the shrubs Myrsine coriacea, Escallonia myrtillioides, and Hesperomeles heterophylla, and ericads such as Macleania rupestris and Vaccinium consanguineum, which occur together with the hepatic Frullania and the lichen Usnea.

686 Chapter 20 Fig. 20.3 Highland peat bog at Tres de Junio in the Tapantí-Macizo de la Muerte National Park, Costa Rica. The terrestrial bromeliad Puya dasylirioides dominates the aspect of this vegetation type. Photo by Anouk Paulissen.

In the neighboring zone, closer to the center of the bog, large, cycad-like ferns in the Blechnaceae dominate (Blechnum buchtieni, B. loxense) as well as the endemic bromelia Puya dasylirioides together with the small (sub)shrubs Pernettya prostrata, Hypericum strictum, and the fern Elaphoglossum, which is found together with the yelloweyed grasses Xyris nigrescens and X. subulata. At the center of the bog one can observe Hypericum strictum, Paepalanthus costaricensis, Hieracium irasuense, Utricularia aff. subulata, Isoetes storkii, and Pernettya prostrata, which occur in association with mosses such as Campylopus sp., Sphagnum magellanicum, S. recurvum, and Breutelia subarcuata. Sedges such as Carex donnellsmithii, C. jamesonii, C. bonplandii, and Rhynchospora schaffneri, together with Juncaceae (Juncus sp.), thrive together with the lichen Cladina confusa (Brak et al. 2005, Kappelle 1996, Gómez 1986). Endemic species reported from this ecosystem are largely shared with the páramo and other nearby ecosystems. The salamander Bolitoglossa pesrubra (formerly known as P. subpalmata) has been recorded from the bogs, although thriving mostly in adjacent ecosystems (Kappelle and Savage 2005). This amphibian is usually found among the leaves of another endemic, the bromeliad Puya dasylirioides, also found in adjacent páramo (Vial 1966, 1968). The demography of these bromeliad populations has been studied by Augspurger (1985). Other endemics shared with the páramo and highlands in general are the orchid

Gomphichis adnata, the lichens Lobariella pallida, Menegazzia neotropica, Nephroma helveticum, and the thrush Turdus nigrescens. Very recently, even a new species of dink frog (Anura: Eleutherodactylidae: Diasporus ventrimaculatus) was discovered in the bog area of the Valle del Silencio (La Amistad International Park, PILA) along the Caribbean slope of the Cordillera de Talamanca (Chaves et al. 2009). While bogs have suffered human disturbance as early as ca. 4,900 years ago (Islebe et al. 2005), the total area of these ecoystems has remained relatively constant in recent times. Their conservation has benefited from the inclusion of most sites within the National System of Conservation Areas (SINAC). The 2003 Ramsar declaration of the Costa Rican Talamanca Peatlands (Turberas de Talamanca) at elevations of 700– 3,819 m and intermingled with oak-bamboo forests (Kappelle 1996) as a Wetland Site of International Importance (Ramsar Site no. 1286, Costa Rica’s eleventh Ramsar Site), further contributes to the conservation of this fragile ecosystem (see: www.ramsar.org/wn/w.n.costarica_ talamanca.htm). Fortunately, this Ramsar site covers areas where the Central American tapir Tapirus bairdii, the ocelot Felis pardalis, and the red brocket deer Mazama americana are still found today. According to studies on past changes, modern anthropogenic fire events (Horn 1988 and 2005) and climate change (Islebe et al. 2005) might, however, threat the long-term health of these fragile highland bog ecosystems. Some important sites, such as La Chonta, are not part of the pro-

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tected area system and should be incorporated as soon as possible, since current land-use changes are affecting its hydrological conditions that maintain the integrity of this ecosystem and may ultimately cause eutrophication of the bog waters and loss of its fragile species (M. Kappelle, personal observation).

Marshes The Flora of the Marshes

Marshes are confined to basins and depressions where rainfall and run-off water accumulate. Herbs, grasses, and sedges dominate these ecosystems. Their non-woody vegetation composition reflects climatic, hydrological, and geomorphological variations as they change from site to site. Under rainy climates affecting the Caribbean coastal plains (Herrera 1986, and chapter 2 of this volume), marshes are dominated by herbs such as Calathea lagunae, Calathea lutea, Thalia geniculata, and Montrichardia arborescens, sedges like Cyperus giganteus and Lasciacis procerruna, grass genera such as Panicum and Scleria, and vines like Ipomoea and Solanum lancefolia. In the Sarapiquí region Calathea lutea and Spathiphyllum friedrichstallii and shrubs such as Acalypha diversifolia dominate

the more open, marshy areas. The Corcovado marsh in the core of the Osa peninsula (Gilbert et al., chapter 12 of this volume), is dominated by the grass Pennisetum and herbs like Jussiaea, Polygonum, and Aeschynomene. Other species occurring in marshes under rainy climates are Hymenachne amplexicaulis and Oryza latifolia (Hartshorn 1983, Hartshorn and Hammel 1994, Myers 1990). The headwaters of the Sierpe River along the southwestern Pacific coast harbor about 2,500 ha of marshes (Fig. 20.4), dominated by Thalia geniculata, Cyperus papyrus, C. gigantus, Fimbristylis spadicea, Paspalidium germinatum, and Gynerium sagittatum that occur together with floating herbs such as Nymphaea blanda and the leather fern Acrostichum aureum (Figs. 20.5 and 20.6) (Álvarez et al. 1999, Kappelle et al. 2003). The largest extensions of marshes under seasonal climates (Herrera 1986, and chapter 2 of this volume) are mainly concentrated in just two areas: the Lower Tempisque region that harbors over 7,000 ha, and the Caño Negro– Río Frío– Guatuso Plains that house some 16,000 ha of seasonal marshes. Functional aspects in these marshes are highly seasonal. Most of the information available on seasonal marshes comes from the two best studied marsh regions of the country: Caño Negro and Palo Verde. In the core of the

Fig. 20.4 Freshwater marsh with floating vegetation at Laguna Sierpe. Photo by Luis González Arce.

Fig. 20.5 Freshwater marsh dominated by the leather fern Acrostichum aureum at Estero Caballo in the Sierpe-Térraba wetland. Photo by Luis González Arce.

Fig. 20.6 Detail of the vegetation dominated by the leather fern Acrostichum aureum at Estero Caballo in the Sierpe-Térraba wetland. Photo by Luis González Arce.

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Fig. 20.7 View of the open waters of Lago Caño Negro, Costa Rica. Photo by Garret Crow.

9,969 ha Refugio Nacional de Vida Silvestre Caño Negro, the 800 ha-sized Lago Caño Negro is located (Fig. 20.7). Its open waters have a depth of up to 3 m in the rainy season and may disappear almost completely at the end of the dry season. While there is some similarity in species composition between the marshes of Caño Negro and Palo Verde (Fig. 20.8), there are also important differences regarding the species that (co)dominate each area. Preliminary analyses of the Caño Negro wetlands reported close to 80 species of aquatic plants (Zamora and Bravo 1992, Castillo and March 1993). Vegetation in the Caño Negro ponds is highly seasonal with Nymphaea ampla, Nymphaea blanda, Neptunia plena, Pistia stratiotes, Polygonum hispidium, and Salvinia sprucei dominating during the rainy season. Salvinia auriculata may locally dominate in the more open waters (Fig. 20.9). Ludwigia sedioides, L. peploides, and Pontederia rotundifolia grow in the pond’s shallower areas. At the edges of the ponds clumps of Ambrosia cumanensis coexist with a number of grasses: Hymenachne amplexicaulis, Echinochloa

polystachya, Paspalum repens, Eragrostis hypnoides, and Panicum parvifolium, as well as other species like Luziola subintegra and the rice plant Oryza latifolia (Castillo and March 1993, Zamora and Bravo 1992). Mixed with these grasses occurs a series of sedges: Cyperus papyrus, C. imbricatus, C. holoschoenoides, Oxycarium cubense, Rhynchospora corymbosa, Fuirena umbellata, and Scleria macrophylla. The edges dominated by tall grasses and sedges appear to be highly dependent on geomorphological processes such as erosion and accretion. Changes in their total coverage happen from year to year. During the dry season, when water levels are lower, conditions allow the growth of a large variety of herbs. Among them, Polygonum segetum, P. punctatum, Aeschynomene virginica, and Justicia comata grow on more exposed soil. In deeper areas, Polygonum hispidum and P. acuminatum form rather dense mats. Hydrolea spinosa, Solanum campechiense, Ceratopteris richardii, Echinodorus subalatus subsp. andrieuxii, and Tonina fluviatilis have also been found here. Noteworthy, Zamora and Bravo (1992)

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Fig. 20.8 Overview of the marshes in Parque Nacional Palo Verde, Costa Rica. In the back at the left, the Río Tempisque. Photo by Garret Crow.

reported that the Caño Negro wetlands serve as the southernmost habitat of the palm Acoelorraphe wrightii. Phytoplankton in the marshes’ ponds is composed of around 240 species. Chlorophyta are the most diverse group with 98 species, followed by Euglenophyta, which is represented by 44 species. Plant diversity decreases considerably during the dry season. Apparently the Cyanophyta group, while less diverse in terms of species, is the most abundant and dominating group (Umaña 1991). The Lower Tempisque area harbors the second largest concentration of marshes in Costa Rica. An extensive mix of interconnected flatlands and ponds dominates the floodplains of the Tempisque River, from which over 130 species of aquatic plants have been reported (Crow 2002). Topographical variations in these marshes are minimal. In the Palo Verde Lagoon, for example, ground elevation varies within a 60 cm range along the 8 km length of the lagoon. In spite of these small variations, changes in vegetation types become evident over a depth gradient. The Palo Verde treelet (Parkinsonia aculeata)— which gives its name to the lagoon and the national park— , Echinodorus

paniculatus, and the sedges Eleocharis mutata, E. interstincta, Cyperus digitatus, and C. giganteus are found at higher grounds where the water is usually less than 30 to 40 cm deep (Fig. 20.10). In the deeper parts of the lagoons (40– 80 cm) emergents like Thalia geniculata, Canna glauca, Paspalum repens, Paspalidium germinatum, Ludwigia inclinata, and Typha dominguensis are found. In areas with more open water one observes species such as Nymphaea pulchella, N. amazonum, Eichhornia crassipes, E. heterosperma, Neptunia natans, Sagittaria guyanensis, Pistia stratiotes, Limnobium laevigatum, Salvinia auriculata, Azolla microphylla, Nymphoides humboldtianum, Rynchospora corymbosa, Oxicrym cubense, Ludwigia pepliodes, and Pontederia rotundifolia (Crow 2002, Guzmán 2007). Most of the vegetation cover has a seasonal appearance. Reduced soil cover (60– 63%) is mostly observed during the peak of the dry season (April– May), while highest cover percentages are found in November, at the end of the rainy season (Hernández 1990). The marshes’ water depth, geomorphological processes, human disturbance history, and seasonal hydrology jointly

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define locally which specific emergent species will dominate which marsh. At some sites the herb Mimosa pigra may dominate while in other, more elevated places species such as Thalia geniculata and Typha dominguensis often compose a mixture with isolated Parkinsonia aculeata trees. In other areas, Thalia geniculata and some species of Canna can be found, which co-dominate with Typha. Variations in species assemblages may result from anthropogenic changes in the area. Typha dominguensis, for example, is a native weed that has been observed in the palynological record available from the Palo Verde marsh (1,200 ha). It appeared already at least some 4,500 years ago (Horn and Kennedy 2006). During the past few decades, it has responded very aggressively to human-induced changes in hydrological conditions and fire regimes. Over the past century local people periodically used fire to modify the marsh, as part of their cattle-ranching practices. These fires favored the occurrence of areas with open water in which floating species started to dominate during the rainy season.

These open waters have served as habitats of great importance to at least 60 species of waterfowl (Trama 2005). For instance, they have been heavily used by anatidae ducks (Hernández 1993) with Dendrocygna autumnalis being the most abundant species in the area. Also, the endangered bird Jabiru mycteria is considered highly dependent on these marshes (Villarreal-Orias 1997). This large stork often visits several marshes in a single day (Gamboa 2003). The Fauna of the Marshes

Marshes harbor an interesting fauna that is worthwhile mentioning though often not endemic to wetland areas. For instance, the common caiman (Caiman crocodylus) constitutes an important component of the dynamics of the Caño Negro marshes. In the early 1990s its total population was estimated at about 3,000 individuals (Allsteadt and Vaughan 1992). Caiman density is high during the dry season when 83 to 166 individuals are observed per ha, concentrated in ponds and watercourses that maintain high water levels.

Fig. 20.9 The eared watermoss (Salvinia auriculata), a small, free-floating, aquatic fern-ally that forms extensive carpets on still waters at Caño Negro, Costa Rica. Reproduction is often vegetative and rapid. Photo by Garret Crow.

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During the rainy season, as flooding expands, they expand their range into the adjacent marshes and channels. In the Tempisque marshes similar patterns are observed among American crocodile (Cocodrylus acutus) populations. These display one of the highest densities ever reported for Costa Rica (between 15.8 and 21.9 individuals per km of shoreline). This high density represents a fourfold increase in the crocodile population of this area that happened during the past two decades (Sánchez 2001). In the Caño Negro marshes, fish communities in seasonal ponds are composed of some 21 species dominated by Poecilia gillii, Astyanax aeneus, and Rhamdia nicaraguensis. Less abundant is Ophisternon aenigmaticum. During the rainy season when flooding occurs and ponds become deeper and more extended, levels of fish diversity become higher and fish species abundance gets lower (Sáenz et al. 2006). One of the distinct and endangered fish species in the marshes of Caño Negro is Atractosteus tropicus (Lepisosteidae, gaspar), a large, 50– 60 cm long carnivorous fish that feeds on other fishes (Poeciliidae, Characidae, Pimelodidae,

Gymnotidae) as well as on crustaceans (Mora et al. 1997). Exotic, invasive fish species such as Oreochromis niloticus (Nile tilapia), a cichlid fish of African origin, has already been found in this marsh. It has been introduced for aquaculture purposes in the early 1960s and is now reported as abundant in these marshes (Cabrera et al. 1992). Exotic tilapias (Oreochromis sp.) have been reported from other marshes, including those in the Lower Tempisque basin (Pizarro and Rojas 1993). Its impact on the foodweb and other fish populations in those habitats is still unknown. Close to 307 species of birds (aquatic and terrestrial), including the endangered jabiru stork (Jabiru mycteria) and the great white egret (Egretta alba, Fig. 20.11), are associated with the marshes of Caño Negro. A total of 101 of them are migratory (Hidalgo 1993a). Over 60 species of waterfowl (including some 23 migrants) have been reported for the marshes of the Lower Tempisque region, including the green heron (Butorides virescens, Fig. 20.12). Anatidae ducks heavily use these marshes. Dendrocygna autumnalis is the most abundant species here (Hernández 1993).

Fig. 20.10 Marshes in Parque Nacional Palo Verde with aquatic emergent Echinodorus paniculatus plants and a few palo verde trees (Parkinsonia aculeata), Costa Rica. Photo by Garret Crow.

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Fig. 20.11 A great white egret (Egretta alba) at Caño Negro, Costa Rica. Photo by Garret Crow.

In the Caño Negro marshes, a population of around 47 individuals of the endangered jabiru has been reported (Villarreal-Orias 2000). The jabiru stork feeds on local fish species such as Synbranchus marmoratus, Cichlasoma sp., and Ariopsis seemanni and snails (Pomacea costaricana). Jabirus foraging in groups achieve higher fish capture frequencies and appear to be more succesful (Villarreal-Orias 1997). Rare avian components such as Anas clypeata, Rynchops niger and Bartramia longicauda are also observed in these marshes (Villarreal-Orias 1997). One of the most important Costa Rican centers of mollusk diversity and endemism concerns the Tempisque river basin and its marshes (Barrientos 2003). Here, the endemic bivalve Nephronias tempisquensis has been observed in the Mata Redonda marsh adjacent to the Tempisque River (Scott and Carbonell 1986). These marshes also harbor a high diversity of macro-invertebrates. Over a hundred species of benthic invertebrates have been reported from the Palo Verde Marshes so far (Trama et al. 2009).

Fig. 20.12 Close-up of the green heron (Butorides virescens) along the Río Tempisque at Parque Nacional Palo Verde, Costa Rica. Photo by Pablo Elizondo.

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Swamps Palm Swamps

Palm swamps are a dominant element of lowland wetlands, representing mature steady-state wetlands with at least 2,800 years of presence in the region (Urquhart 1997, 1999). Studies on this particular ecosystem are still rather scarce. Most of the palm swamps reported from Costa Rica are located in and around the Barro Colorado Wildlife Refuge and the Tortuguero National Park. Other palm swamps are known from smaller areas around the Caño Negro Wildlife Refuge, and in the Sierpe-Osa region. Over half (55%) of Costa Rica’s existing palm swamps are conserved within protected areas today (Serrano-Sandi et al. 2013). Because

palm and forest swamps grow together, significant overlap between these two ecosystems is to be expected when estimations of their coverage are done. Which species dominate and how the overall structure of a palm swamp appears will depend on the seasonality and the hydrological regime of a particular site under study. In general, the better drained a swamp is, the greater its plant diversity is. Also, non-constant flooding conditions favor higher plant species diversity than permanent flooding does. There is a tendency for palm species to lose dominance over hardwood species as flooding depth and flood prolongation decrease (Myers 1990). Dominant palm species in such swamps are Raphia taedigera (locally known as yolillo, Figs. 20.13 and 20.14) and Manicaria saccifera (royal palm, napa or cabecinegro).

Fig. 20.13 Palm swamp dominated by raffia or yolillo (Raphia taedigera) at Quebrada Taboga in the Sierpe-Térraba wetland. Photo by Luis González Arce.

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Fig. 20.14 Close-up of the Raphia taedigera– dominated palm swamp at Quebrada Taboga in the Sierpe-Térraba wetland. Photo by Luis González Arce.

In M. saccifera and R. taedigera palm swamps, the maximum level of flooding can be close to 1 m above ground level, with short dry spells throughout the year. Soils are flooded during 53 to 92% of the year but water tables are very close to soil level during most of the year (Myers 1990). Plant diversity tends to be low, with 3– 27 species with stems over 10 cm diameter at breast height (dbh) per ha (Anderson and Mori 1967, Devall and Kiester 1987, Myers 1990, Chavarría and Valverde 2000). Structural development varies significantly: Raphia-dominated swamps exhibit stem densities from 527 to 640 stems/ha and basal areas from 224 to 338 m2 /ha (Myers 1990); Manicariadominated swamps exhibit higher stem densities (715– 910 stems/ha) but lower basal areas (47– 94 m2 /ha (Myers 1990, Holdridge et al. 1971). In Manicaria palm swamps

a large part of the stems belong to hardwood species (stem densities around 230 stems per ha) while in Raphia swamps stem abundance is mostly dominated by palms (Myers 1990). In Raphia-dominated swamps, Raphia is accompanied by disperse trees belonging to species such as Amanoa potamophila, Andira inermis, Annona glabra, Ardisia compressa, Calophyllum brasiliense, Campnosperma panamensis, Carapa guianensis, Cassipourea guianensis, Crataeva tapia, Crudia acuminata, Grias fendleri, Guatteria amphifolia, Homalium racemosum, Inga sp., Ixora nicaraguensis, Luehea seemannii, Ocotea sp., Pentaclethra macroloba, Pithecellobium latifolium, Posoqueria latifolia, Prioria copaifera, Pterocarpus officinalis, Rauvolfia sp., Sickingia maxonii, Sloanea picapica, Spondias mombim,

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Symphonia globulifera, and Trichilia tuberculata (e.g., see Kappelle et al. 2003, for details on the flora of the Raphia swamps found in the Osa Conservation Area). The understory is relatively open and dominated by sedges together with Becquerelia cymosa, Calyptrocarya glomerulata, Scleria microcarpa, Thalia geniculata, the shrub Psychotria chagrensis, small trees such as Alchornea costaricense, Casearia sp., Mabuetia guatemalensis, Posoqueria grandiflora, Senna reticulata, Urera caracasana, the ginger Renealmia aromatica, the herbs Palicourea fastigiata, Jussiaea latifolia, Calathea lagunae, Calathea lutea, Calathea foliosa, Cyclanthus bipartitus, the ferns Adiantum latifolium and Acrostichum aureum, as well as Tabernaemontana chrysocarpa, the palms Calyptrogyne glauca, Asterogyne martiana, the aroids Montrichardia arborescens, Dieffenbachia davidsei, and Spathiphyllum friedrichsthalii and the floating Pistia stratiotes (Myers 1990, Chavarria and Valverde 2000, Hartshorn 1983, Kappelle et al. 2003). In Manicaria-dominated swamps along the Caribbean coastal plains, this palm is found associated with other palms such as Astrocaryum alatum and Euterpe sp., and mixed with tree species such as Calophyllum brasiliense, Symphonia globulifera, Carapa guianensis, and Dialium guianensis (Gómez 1985). In the Sierpe and Golfo Dulce areas, at the Pacific coast, Raphia grows in small patches together with Symphonia globulifera (cerillo) and other palm species such as Elaeis oleifera and Scheelea rostrata together with the non-palm tree Pterocarpus officinalis (Allen 1977, Kappelle et al. 2003). Both Elaeis oleifera and Scheelea rostrata are found dominating swamps of much smaller extension. E. oleifera is found in small patches behind mangroves in the wet areas of both coastal plains while Scheelea rostrata stands are found in the meanders of the Tempisque and Palma rivers in the Lower Tempisque Basin. The small stands dominated by these two species are rapidly disappearing owing to drainage and fire events. While fauna restricted to these environments is scarce and little studied, the occurrence of manatees in the channels associated with Raphia and Manicaria swamps along the Caribbean coast is worthwhile mentioning. In these channels small populations of the manatee (Trichechus manatus) are reported. They feed on many types of plants including the benthic Ludwigia and Hydrilla herbs (Jiménez 2000). Tapirs and peccaries feed on Raphia fruits in the Osa Peninsula (Janzen 1983) and seasonal migrations of these mammals between Raphia swamps and adjacent rain forests have been reported. In Raphia-dominated swamps total numbers of amphibian and reptile species are around 14 and 17, respec-

tively (Bonilla-Murillo et al. 2013). All these species are also found in adjacent non-wetland habitats but seem to be well adapted to the harsh conditions of the palm-dominated wetlands. Forest Swamps

Forest swamps not dominated by palms are characterized by low levels of plant diversity, compared with adjacent dryland forests. Species dominance varies from site to site in response to differences in hydrological regimes and geomorphological settings. Among the most common forest swamps in the country are those dominated by Pterocarpus officinalis (Fabaceae). In such sangrillo swamps, P. officinalis exhibits stem densities of about 57 trees/ha and basal areas of 10.6 m2 /ha. This tree species shares the canopy layer with other tallgrowing species such as Carapa guianensis (Meliaceae) and Astrocaryum alatum, which display similar densities (57 and 143 stems/ha) and basal areas (9.7 and 1.6 m2 / ha, respectively). Other minor elements in those stands are Pentaclethra macroloba and Virola multiflora. Close to the coastline P. officinalis– dominated swamps grow, even containing mangrove forest elements. At Moín, at the Caribbean coast, P. officinalis density was 212 stems/ha with basal areas of 7 m2 /ha. The two other main woody constituents (Avicennia germinans and Rhizophora mangle) showed densities of 84 and 118 stems/ha and basal areas of 13.4 and 3.3 m2 /ha, respectively ( Jiménez 1981). The understory at the site is dominated by Crinum erubescens, with herbs such as Rustia occidentalis, Pavonia spicata, Hymenocalis litoralis, and the fern Acrostichum aureum (Jiménez 1981). Along the Pacific coast, within the Corcovado National Park, Pterocarpus swamps exhibit total densities of 660 saplings and adult trees per ha. In transitional zones where Mora oleifera and P. officinalis grow together, tree densities ranged from 400 stems per ha for Pterocarpus to 155 for Mora. At the same site seedlings of P. officinalis exhibit densities of 72/m2 ( Janzen 1978). At those sites where Mora oleifera dominates over P. officinalis the tidal influence seems to be more prominent. Here, Mora oleifera clearly dominates over other species, including Amphitecna latifolia, Avicennia germinans, Tabebuia rosea, and Luehea seemannii (Hartshorn 1983, 1988). The structural development of these forests exhibits stem densities of 235/ha and basal areas of 35 m2 /ha (Holdridge et al. 1971). At locations deeper into the inland, forest swamps are composed of a mixture of Carapa guianensis, Cryosophila guagara, Erythrina lanceolata, Grias fendleri, Mouriri sp., Prestoea decurrens, Pterocarpus officinalis, and Virola koschnyi (Hartshorn 1983, Kappelle et al. 2003)

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Fig. 20.15 Forest swamp dominated by Symphonia globulifera along a tributary of the Sierpe River. Photo by Luis González Arce.

In the Sierpe-Térraba wetland area, some forest swamps are dominated by Symphonia globulifera (Figs. 20.15 and 20.16) though they thrive at places mixed with other important woody species including Anacardium excelsum, Caryocar costarricense, Terminalia oblonga, Calophyllum brasiliense, Pterocarpus officinalis, Erythrina lanceolata, Inga vera, Carapa guianensis, Hernandia didymantha, and herbs such as Montrichardia arborescens and the floating Pistia stratiotes (Bravo et al. 2000, Kappelle et al. 2003). Cecropia sp. occurs in gaps and is quite abundant in these forest swamps, while Pachira aquatica is found growing along the margins of the river channels and lagoons. At the Osa Peninsula itself, some small isolated patches of forest swamps are dominated by Prioria copaifera trees (Holdridge et al. 1971). In these Prioria swamps, the endemic herb Calathea longiflora has been observed (Gómez 1984).

Prioria copaifera (cativo) is also flourishing along the Caribbean coast, where it forms extensive swamps called “cativales.” These are usually growing behind the narrow mangrove belts that occur on the coastal plains. Here, on loamy soils that accumulate large amounts of detritus, or on seasonally flooded riverbanks, Prioria copaifera individuals can reach significant sizes and basal area values. Trees with a dbh of 160 cm have been reported here. While P. copaifera dominates, stand composition may vary from site to site. Along the Río Colorado, Prioria copaifera exhibits significant dominance over other arboreal components such as Stemmadenia donnell-smithii, Pithecellobium latifolium, Grias fendleri, and Ixora finlaysoniana (Hartshorn 1983, 1988). At other sites, P. copaifera is found growing in association with Pentaclethra macroloba, Iriartea deltoidea, and Eschweilera calyculata (Chavarria and Valverde 2000).

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Fig. 20.16 Detail of the Symphonia-dominated forest swamp in the Sierpe River watershed. Photo by Luis González Arce.

Structural attributes also fluctuate among sites. At the Río Colorado P. copaifera densities were high (290/ha) with basal areas close to 55 m2 /ha (Holdridge et al. 1971). Southward sites exhibit P. copaifera densities of 79 trees/ha (21% of the total) and 29 m2 /ha (63% of the basal area of the forest) (Chavarria and Valverde 2000). Carapa guianensis represents 16% of the stems thicker than 10 cm dbh and about 10% (4.9 m2 /ha) of the total basal area, while Pentaclethra macroloba has some 44 stems/ha and is responsible for a basal area of 4.2 m2 /ha (Chavarria and Valverde 2000). Whereas it is usually a sub-dominant tree of the forest swamps in northeastern Costa Rica, C. guianensis shows a highly synchronous phenology, with flowering happening from September onwards and fruiting occurring during the following May (McHargue and Hartshorn 1983). From 750 to 3,950 seeds are produced by each individual tree,

many of which (54– 98%) are removed by rodents such as agoutis (Agouti paca) (McHargue and Hartshorn 1983). As a light-demanding species, growth of C. guianensis is significantly faster in light gaps (Webb 1999). Campnosperma panamensis (orey) is a swamp tree usually restricted to better-drained swamps usually in the most elevated portions of the swamps, indicating intolerance to strong inundation (Phillips 1995). Orey swamps occur in small patches at the GandocaManzanillo Wildlife Refuge and at the mouth of the Sixaola River. Gómez (1985) reports orey growing in association with Dialyanthera otoba, Symphonia globulifera, Calophyllum brasiliense, Carapa guianensis, Grias fendleri, and Saccoglotis thrichogyna. In those sections of the forest swamps where C. panamensis dominates, this species shows densities of

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203 stems/ ha (37% of trees above 10 cm dbh) and basal areas of 13.8 m2 ha (45% of the total basal area). Other components like the palm Euterpe precatoria and Cassipourea aff. killipii have stem densities of 120 and 140 per ha, and basal areas of 3.9 and 4.4 m2 /ha, respectively. Locally less important elements, such as Symphonia globulifera and Pentaclethra macroloba account for 26 and 20 trees per ha, with basal areas of 3.5 and 2.9 m2 /ha, respectively (Chavarria and Valverde 2000). In this forest type, the undergrowth is dominated by Psychotria poeppigiana, Voyria sp., Tococa guianensis, and the shrub Ourartea sp. (Chavarria and Valverde 2000). Pentaclethra macroloba is a tree that may become very important in some forest swamps. While not exclusive to forest swamps this species becomes the dominant element in many swamps in the Caribbean lowlands. In the Sarapiquí region in northern Costa Rica, for instance, many swamps are dominated by P. macroloba, which grows together with Carapa nicaraguensis, Luehea seemannii, Otoba novogranatensis, Pachira aquatica, and Pterocarpus officinalis (Hartshorn and Hammel 1994). The subcanopy is composed of trees such as Grias cauliflora, Pithecellobium valerioi, and palms like Iriartea deltoidea, and Welfia georgii. At the same time, the understory is dominated by Adelia triloba, Astrocaryum alatum, Bactris longiseta, Chione costaricensis, and Psychotria chagrensis (Hartshorn 1983, 1988). In such Pentaclethra swamps a total of 115 species have been observed (Hartshorn 1983) though just 10 of them account for more than 75% of the basal area. Here, P. macroloba accounts for 30% of the total basal area (31 m2 /ha) and densities of 265 stems per ha. Furthermore, Carapa nicaraguensis exhibits basal area values of 13 m2 /ha and stem densities of 69/ha, while the palm species Iriartea deltoidea is present with high stem densities (133/ha), but its basal area is only 3.38 m2 /ha (Hartshorn and Hammel 1994). It appears that these P. macroloba swamps are highly dynamic and demonstrate fast growth and regeneration rates, with a half-life of about 34 years (Liebermann et al. 1985). The economic value of some of these forest swamps— especially those dominated by Prioria copaifera and Carapa guianensis— has attracted interest of foresters and catalyzed research, particularly on the wood extraction potential of these swamps (Webb 1998, 1999).

Conservation Wetland Protection

During the past few decades the seasonally flooded wetlands in Costa Rica have been significantly degraded owing

to factors such as seasonal fires, artificial drainage, and water diversion. Moreover, illegal fishing and crocodile hunting have been reported periodically (e.g., in March– April 2010; M. Kappelle, pers. comm.); seasonal fires have considerably affected the distribution and coverage of wetland vegetation types; heavy sedimentation, resulting from the degradation of associated watersheds, has caused significant habitat change; and other threats including pollution with pesticides, eutrophication with fertilizers, and the introduction of alien species such as Tilapia have significantly degraded Costa Rica’s freshwater ecosystems, including its bogs, marshes, and swamps (e.g., see TNC 2009). Changes in the Río Frío watershed, associated with the Caño Negro marshes, have promoted the reduction of open water areas that are now being occupied by grasses that colonize recently created mud flats (Castillo and March 1993, Brenes et al. 2001). With channel siltation and losses in wetland coverage, the interconnectivity previously found among Caño Negro, Río Frío, and the Guatuso floodplains is gradually being lost. The exchange of fauna, water, and nutrients among these systems is therefore disappearing. Similarly, in the Tempisque River the severe extraction of water for irrigation purposes has dramatically reduced the connectivity between this river and the adjacent marshes, particularly during the dry season. Drainage and widening of the riverbed, for flood control purposes, have impacted riparian communities, crocodile nesting, and riverine vegetation in most lowland areas. The development of agriculture at the expense of wetland areas is generating significant agrochemical contamination. Pesticides have been reported in eggs of the woodstork (Mycteria americana) common in the seasonal marshes of the lower Tempisque River. High correlations of p,p’-DDE (dichlorodiphenyldichloroethylene), a persistent organic pollutant (POP), have been related to reductions in eggshell thickness (Hidalgo 1993b). Similarly, accumulation of lead, cadmium, selenium, and manganese in woodstork adults was reported for the same locality (Burger et al. 1993). About 60% of freshwater wetlands in the country are located within protected areas, including 11 Ramsar Sites: Palo Verde (1991), Caño Negro (1991), Tamarindo (1993), Térraba-Sierpe (1995), Gandoca-Manzanillo (1995), Humedal Caribe Noreste (1996), Isla del Coco (1998), Manglar de Potrero Grande (1999), Laguna Respringue (1999), Cuenca Embalse Arenal (2000), and Turberas de Talamanca (2003). However, even these protected wetlands are affected by changes in water flow and quality, originated outside the protected areas. Many marshes in the lower Tempisque Basin, for example, are closely interconnected hydrologically. Within the Palo Verde National Park, water flows downwards, starting at Poza Verde, through Varillall, then

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via Piedra Blanca and Palo Verde, in order to finally reach the Nicaragua marshes. This cascade-like connection makes “downstream” marshes highly dependent on alterations in “upstream” marshes. Unfortunately, the marsh that is most upstream (Poza Verde) is located partially outside the Park and receives large amounts of waters flowing in from upstream sugar cane and rice fields. Water quality in all “downstream” marshes, even within a National Park like Palo Verde, is likely to be affected by agriculture-derived contaminants, including pesticides and fertilizers, as well as sediments originating from soil erosion. Interconnectivity among the various Tempisque marshes is also observed in the movements of animals. It is known that birds and fishes migrate seasonally and annually from one marsh to another. When open areas in some of the marshes disappear, duck populations leave for other, more open marshes in the region (McCoy and Rodríguez 1993), underlining the vital connection among marshes and their species populations at regional scales. With the onset of the rainy season gaspar fish (Atractosteus tropicus) migrate upstream to reproduce in the marshes and ponds of the Caño Negro refuge. Similarly, at the onset of the dry season large populations of sardine (Astyanax fasciatus) migrate between the large wetland areas of the lower Tempisque River and the headwaters of its tributaries (López, 1978). Most of these connections have now disappeared or are significantly degraded. Waterfowl that used to visit different marshes in the Lower Tempisque region now fly between wetlands and adjacent rice fields, so as to deal with the loss of some of the marshes. In a recent case study, over 50 species of waterfowl were recorded in a rice field, while only 31 species were observed in a natural marsh (Hurtado-Astaiza 2003). Not only was the diversity higher in the rice field but also over 70% of the common species turned out to be more abundant in rice fields than in adjacent marshes (HurtadoAstaiza 2003). Clearly, farming-related activities enhance foraging opportunities for waterfowl while providing the birds with shallow open-water sites. To some extent, the rice fields have mitigated marsh habitat loss in the Lower Tempisque River. They are, however, being replaced by sugarcane fields, a habitat not very suitable for waterfowl. By the year 2000, around 45% of the cropland in the Tempisque-Bebedero watershed areas was covered by sugarcane, while by 2007 sugarcane fields occupied a total of 70% of the available cropland in that area. In 2008, price increments in imported rice triggered the establishment of new rice fields in the area but in 2009 restrictions in credit access reduced again the amount of cropland covered by rice. The dramatic losses in wetland areas observed in Costa

Fig. 20.17 Dredging at rivers and construction of levies are disconnecting wetlands from the riverine systems in most watersheds of the country. Photo by Jorge Jiménez.

Rica and the related loss of interconnectivity among the remaining sites (Fig. 20.17) underline the need to strengthen the management of protected wetland areas. A watershed approach is urgently needed to safeguard the remaining wetlands and maintain healthy ecological flows between those wetlands (Jiménez et al. 2005). Habitat losses are negatively affecting many of the ecological services normally provided by marshes. Water quality enhancement, a key regional function of marshes, is rapidly being lost. Large tracts of marshes, historically associated with the main watersheds in Costa Rica, have disappeared to give room to croplands. Dikes built along riverbanks have isolated remaining patches of marsh from the main river channels. All these transformations have reduced the capacity of marshes to trap sediments, pesticides, and persistent organic pollutants (POPs). Likely, economically important activities such as the artisanal fisheries in the Térraba-Sierpe Delta and the artisanal green clam (Polymesoda radiata) fisheries in the Tempisque River have already been impacted negatively by those changes. The legal framework for protection of freshwater wetland resources in Costa Rica is very recent. It includes the adherence to the Ramsar Convention in 1991 and several articles in the national Wildlife Law (law nr. 7317) and Environmental Law (law nr. 7554), both established in 1995,

Bogs, Marshes, and Swamps of Costa Rica 701

as well as in the Forest Law (law nr. 7575) approved in 1996, and the Biodiversity Law (law nr. 7788) created in 1999. Since wetland ecosystems have been declared as being of Public Interest (Environmental Law, article 41), one would expect freshwater wetlands to be better conserved. However, for decades legal voids have allowed freshwater wetland reclamation in the country. The definition of wetlands, for example, created over decades substantial vagueness around wetland conservation. In Costa Rica wetlands are legally considered to be “areas of marsh, fen, peatland or water, whether natural or artificial, permanent or temporary, with water that is static or flowing, fresh, brackish or salt, including areas of marine water, the depth of which at low tide does not exceed six metres” (Ramsar Convention 2009). This definition is identical to the one provided by the Convention on Wetlands (Ramsar, Iran 1971). Such an ample concept resulted in a ministerial requirement to delimit and declare any specific wetland, before it will be considered as a legally recognized wetland (Wildlife Law, article 7). Thus, under this interpretation, wetlands were not receiving any protected area status until a delimination and declaration process had been completed. Therefore, wetland areas within private lands— that is, not stateowned— were part of the national system of protected areas only after they were legally expropriated and the private owner had received the corresponding compensation (Res 2005– 0461, Tribunal de Casación Penal). It was only recently (2011) that the Constitutional Court granted full protection to wetlands by declaring all of them part of the State’s Natural Heritage, requiring those occuring in private properties to be protected.1 A study conducted by The Nature Conservancy in close collaboration with its partners (TNC 2009), clearly identifies key freshwater sites of important conservation value, including the Tempisque delta, the Caño Negro wetlands, the Tárcoles river mouth, the Osa swamps, and the Sixaola and San Juan River deltas, among others. It is in these areas that we will need to focus our attention in order to be able to protect the remaining marshes and swamps that still contain so much biodiversity. Degradation and Restoration: The Case of the Palo Verde Marshes

Complementary to the protection of still-existing though threatened wetlands in Costa Rica, the restoration of degraded bogs, marshes, and swamps will become more and more important in the coming decades. Here, a case study 1

Constitutional Court Vote # 2011-016938.

on the ecological restoration of the main marshes of the Palo Verde National Park is presented. It discusses a series of steps that were undertaken to recover the original extent of open water, vegetation communities, and faunal assemblages that once characterized this important lowland wetland along the Pacific coast. During the mid-1970s open water areas were the dominating habitat in the marshes of the Palo Verde National Park. After decades of periodic fires about 85% of its surface was dominated by open water, floating vegetation, and grasses. The elimination of periodic fires and the diversion of surface run-off water from the lagoon (meant to build roads inside the park) coincided with the elimination of the marsh’s grazing and an eight-year dry-weather spell. These factors fostered the subsequent colonization of the marsh by Typha dominguensis. By 1986 most open-water areas had disappeared and Typha occupied around 57% of the marsh while the shrub Parkinsonia aculeata covered about 6%. Six years later Typha occupied 53% of the marsh and P. aculeata 18%. By the early 1990s, most of the openwater areas had disappeared (Castillo and Guzmán 2004). Marsh degradation was further accelerated by the high evapotranspiration rates of Typha that further altered the hydrological regimes and ultimately affected the marsh considerably. During the rainy season evapotranspiration rates in Typha-dominated areas were 57– 80% higher than in open waters, while these numbers were even higher during the dry season (90 to 128%) (Calvo and Arias 2006). Average actual evapotranspiration for this species has been calculated at 3.2 to 4.8 mm per day, one of the highest in vegetated areas in the region (Guzmán 2007). Reduced run-off and rainfall in combination with higher evapotranspiration rates have reduced water depth and the number of months that the marsh is flooded. These conditions favored the expansion of Parkinsonia aculeata, which covered less than 2% of the marsh in the 1970s, to almost 20% by 2002 (Solano 2004). In Parkinsonia-covered areas around 15% of the annual rainfall was intercepted by the shrubs’ crowns (Calvo and Arias 2006). This amount of water represents about 8% of the total volume required to filll the marsh (Calvo and Arias 2004). Rainfall interception further reduced the lagoon’s water levels and enhanced invasion by the bulrush or cattail Typha. The rapid reduction in areas with open water resulted in a decrease of waterfowl species and floating aquatic plant diversity. By 1988 only 3,000 ducks and 500 teals were found where previously over 35,000 ducks and 25,000 teals were observed (McCoy and Rodríguez 1994). Highest waterfowl density occurred during December– February when migratory populations arrived from higher latitudes. Ultimately, the reduction of flooded areas in the wider wa-

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tershed area promotes congregations of both migratory and local waterfowl populations, resulting in extraordinary concentrations of waterfowl in marshes with remaining open waters. These dramatic reductions in open-water areas and the consequent decrease in waterfowl concentrations have raised important concerns in the conservation sector. Rehabilitation attempts of the Palo Verde marsh started in 1986, when creeks were dragged to increase drainage towards the lagoon. Cattle were partially reintroduced to the lagoon’s area in the assumption that grazing pressure would open up the marsh (McCoy 1994, Burnidge 2000). Removal of Typha stands was also attempted in small areas of the marsh using mechanical crushing, a method that proved to be cheap and effective (McCoy and Rodríguez 1994). These efforts brought partial recovery of the waterfowl populations but lost ground to the re-expansion of Typha and Parkinsonia in the following years. Additional efforts were started to eradicate Typha and Parkinsonia from the Palo Verde marsh at the start of this century. Restoration of the hydrological flows that feed into the marsh was the first step in this effort ( Jiménez et al. 2003). Restoring the flow discharge (about 1,350,000 m3 per year in rainy years) of the Huertón Creek back into the marsh resulted in a significant hydrological improvement. This creek had been previously diverted as a result of road construction back in the early eighties. Rebuilding the creek bed and constructing culverts at the road allowed the seasonal flows of this creek to discharge back into the Palo Verde marsh. Furthermore, the Chamorro Creek, which also had discharged water from the Piedra Blanca Marsh into the Palo Verde Marsh, had beeen diverted by the same road. The Chamorro Creek introduced significant amounts of water (between 2.3 and 9.4 million m3 per year in rainy years) into the Palo Verde Marsh. Improving the existent culverts and cleaning the creek bed allowed the flows to reach the Palo Verde marsh again. As a consequence of flow restoration, high water levels in

the lagoon were reached earlier in the year and maintained for a period at least one month longer— a pattern most likely similar to that observed before the divertions. Once the hydrological flows were restored Typha and P. aculeata stands that had invaded the marsh and eliminated other types of vegetation were removed. By applying mechanical crushing and fire it was possible to remove dense mats of Typha in about 370 ha of marsh. Large open-water areas occurred after these interventions. The response of waterfowl was immediate. The next dry season over 25,000 ducks, 6,000 teals, and more than 3,500 woodstork (Mycteria americana) were observed in the marsh with hundreds of individuals belonging to some 60 other species of waterfowl (Trama 2004). Aquatic plant diversity also increased dramatically. Both floating and emergent species colonized the open water areas. Close to 80 species of floating and emergent aquatic plants colonized areas previously occupied exclusively by Typha. While Typha dominance was eliminated, the long-term maintenance of wide open-water areas is still an open question. It is necessary to define whether those open-water areas depend in the long term on habitat disturbance. The existence of large seasonal concentrations of waterfowl in this marsh was the main reason for the establishment of this protected area. We need to ask if these seasonal concentrations were the result of periodic disturbances such as fire and grazing generated by previous cattle ranching operations. Or are they the result of crushing and fire as generated by the rehabilitation project? During the three years following the removal of the emergent vegetation significant open-water areas could naturally persist. It might, however, still be too soon to answer this question fully. This particular case of wetland restoration highlights the need to restore the seasonal, hydrological, and fire regimes and at the same time recover the system’s flora and fauna, in order to ensure bogs, marshes, and swamps are ecologically healthy and continue to provide much-needed environmental services for human well-being.

References Allen, P.H. 1977. The Rainforest of Golfo Dulce. Redwood City, CA: Stanford University Press. 417 pp. Allsteadt, J., and C. Vaughan. 1992. Population status of Caiman crocodylus (Crocodylia: Alligatoridae) in Caño Negro, Costa Rica. Brenesia 38: 57– 64. Álvarez, J., C. Asch, G. Oconitrillo, and S. Vargas. 1999. Plan de ordenamiento territorial para la gestión ambiental del humedal Sierpe de Osa, Costa Rica. San José, Costa Rica: Instituto Geográfico Nacional (IGN). 155 pp.

Anderson, R., and S.A. Mori. 1967. A preliminary investigation of Raphia palm swamps, Puerto Viejo, Costa Rica. Turrialba (2): 221– 24. Augspurger, C.K. 1985. Demography and life history variation of Puya dasylirioides, a long-lived rosette in tropical subalpine bogs. Oikos 45: 341– 52. Barrientos, Z. 2003. Estado actual del conocimiento y la conservación de los moluscos continentales de Costa Rica. Revista de Biología Tropical 51(suppl. 3): 285– 92. Bonilla-Murillo, F., D. Beneyto, M. Sasa. 2013. Amphibians and reptiles

Bogs, Marshes, and Swamps of Costa Rica 703 in the swamps dominated by the palm Raphia taedigera (Arecaceae) in northeastern Costa Rica. Revista de Biología Tropical 61(suppl. 1): 143– 61. Brak, B., M. Vroklage, M. Kappelle, and A.M. Cleef. 2005. Comunidades vegetales de la turbera de altura “La Chonta” en Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 607– 30. Costa Rica: Editorial INBio. Bravo, J., J. González, G. Quiros, M. Alvarado, J. Sandí, and L. Piedra. 2000. Inventario de los bosques inundables de cerillo (Symphonia globulifera) en el humedal Térraba Sierpe, Costa Rica. Boletín de humedales y zonas costeras 2(5). San José. Costa Rica: IUCN, Oficina para Mesoaméica. Bravo, J., M. Romero, A.J. Sánchez, and J. Reynolds. 1996. Inventario y evaluación de los humedales de la cuenca baja del río Tempisque, Guanacaste, Costa Rica. In Workshop on the Utilization and Sustainable Management of the Hidric Resources (November 28– December 1, 1996), 237. Heredia, Costa Rica: EUNA. Brenes, L.G., F.J. Solano, and D.M. Salas. 2001. Degradación del systema lagunar Caño Negro (norte costarricense) por sedimentación. Ciencias Ambientales 21: 36– 41. Burger, J., J.A. Rodgers, and M. Gochfeld. 1993. Heavy metal and selenium levels in endangered wood storks, Mycteria americana, from nesting colonies in Florida and Costa Rica. Archives of Environmental Contamination and Toxicology 24(4): 417– 20. Burnidge, W.S. 2000. Cattle and management of freshwater neotropical wetlands in the Palo Verde National Park, Guanacaste, Costa Rica. M.Sc. thesis, The University of Michigan, School of Natural Resources and Environment. Ann Arbor, MI. 89 pp. Cabrera, J., C.L. Ampie, and G. Galeano. 1992. Presencia de Oreochromis niloticus (Pisces: Cichlidae) en lagunas estacionales del Refugio Nacional de Vida Silvestre Caño Negro, Costa Rica. Brenesia 38: 169– 70. Calvo, J.C., and O. Arias. 2004. Restauración hidrológica del humedal Palo Verde. Ambientico 129: 7– 8. Calvo, J.C., and O. Arias. 2006. Estudio de evapotranspiración de la tifa (Typha dominguensis) en el Parque Nacional Palo Verde, Guanacaste, Costa Rica. Research Report. San José, Costa Rica: Organization for Tropical Studies (OTS). 14 pp. Castillo, M., and J.A. Guzmán. 2004. Cambios en la cobertura vegetal en el Humedal Palo Verde según SIG. Ambientico 129: 4– 6. Castillo, R., and J. March. 1993. Cambios en los habitats ecológicos del Refugio Nacional de Vida Silvestre de Caño Negro 1961– 1992. Revista de Ciencias Sociales de la Universidad de Costa Rica 62: 51– 67. Chavarría, C.R., and O. Valverde. 2000. Delimitación y muestreo florístico del humedal de Punta Mona, Gandoca-Manzanillo, Costa Rica. Boletin de Humedales y Zonas Costeras 2(5). San José, Costa Rica: IUCN. Chaves, G., A. García-Rodríguez, A. Mora, and A. Leal. 2009. A new species of dink frog (Anura: Eleutherodactylidae: Diasporus) from Cordillera de Talamanca, Costa Rica. Zootaxa 2088: 1– 14. Córdoba, R., J.C. Romero, and N.J. Windevoxhel. 1998. Inventario de los Humedales de Costa Rica. San José, Costa Rica: IUCN. 380 pp. Crow, G.E. 2002. Plantas Acuáticas del Parque Nacional Palo Verde y el Valle del Río Tempisque. Santo Domingo de Heredia, Costa Rica: INBio. 300 pp. Devall, M., and R. Kiester. 1987. Notes on Raphia at Corcovado. Brenesia 28: 89– 96.

Ellison, A.M. 2004. Wetlands of Central America. Wetlands Ecology and Management 12: 3– 55. Gamboa, M.E. 2003. El comportamiento de Jabiru mycteria durante la época reproductiva en humedales de la zona norte de Costa Rica. Zeledonia 7(1): 25– 32. Gómez, L.D. 1984. Las plantas acuáticas y anfibias de Costa Rica y Centroamérica. 1. Liliopsida. San José, Costa Rica: Editorial Universidad Estatal a Distancia (EUNED). 430 pp. Gómez, L.D. 1986. Vegetación de Costa Rica. San José, Costa Rica: Editorial Universidad Estatal a Distancia (EUNED). Guzmán, J.A. 2007. Effects of land cover changes on the water balance of the Palo Verde Wetland, Costa Rica. Enschede, the Netherlands: International Institute for Geo-Information Science and Earth Observation. 85 pp. Hartshorn, G. 1983. Introduction: Plants. In D.H. Janzen, ed., Costa Rican Natural History, 118– 83. Chicago: University of Chicago Press. Hartshorn, G. 1988. Tropical and subtropical vegetation of Mesoamerica. In M.G. Barbour and W.D. Billing, eds., North American Terrestrial Vegetation, 365– 90. Cambridge, UK: Cambridge University Press. Hartshorn, G.S., and B.E. Hammel. 1994. Vegetation types and floristic patterns. In L.A. McDade, K.S. Bawa, H.A. Hespenheide, and G.S. Hartshorn, eds., La Selva: Ecology and Natural History of a Neotropical Rain Forest, p. 73– 89. Chicago: University of Chicago Press. Hernández, D. 1990. Cambios anuales en la composición y distribución de la vegetación acuática en el humedal estacional de Palo Verde, Costa Rica. Master’s thesis, Programa Regional en Manejo de Vida Silvestre, Universidad Nacional. Heredia, Costa Rica. 25 pp. Hernández, D. 1993. Uso de habitat por patos Anatidae en un humedal estactional de Costa Rica. In Proceedings of the Ornithological Congress of Costa Rica, 10. San José, Costa Rica: CIPA / MNCR / PRMVS / UNA. Herrera, W. 1986. Clima de Costa Rica. San José, Costa Rica: Editorial Universidad Estatal a Distancia (EUNED). Hidalgo, C. 1993a. Avifauna del Refugio Nacional de Vida Silvestre Caño Negro. In Proceedings of the Ornithological Congress of Costa Rica, 29. San José, Costa Rica: CIPA / MNCR / PRMVS / UNA / UCR. Hidalgo, C. 1993b. Residuos de plaguicidas organoclorados en huevos de Mycteria americana. In Proceedings of the Ornithological Congress of Costa Rica, 22. San José, Costa Rica: CIPA / MNCR / PRMVS / UNA. Holdridge, L.R., W.C. Grenke, W.H. Hatheway, T. Liang, and J.A. Tosi. 1971. Forest Environments in Tropical Life Zones: A Pilot Study. Oxford: Pergamon Press. 746 pp. Hooghiemstra, H., A.M. Cleef, G.W. Noldus, and M. Kappelle. 1992. Upper Quaternary vegetation dynamics and paleoclimatology of the La Chonta bog area. Journal of Quaternary Science 7(3): 205– 25. Horn, S.P. 1988. Effect of burning on a montane mire in the Cordillera de Talamanca, Costa Rica. Brenesia 30: 81– 92. Horn, S.P. 1989. Prehistoric fires in the Chirripó páramo of Costa Rica: sedimentary charcoal evidence. Revista de Biología Tropical 37: 139– 48. Horn, S.P. 1993. Postglacial vegetation and fire history of the Chirripó páramo of Costa Rica. Quaternary Research 40: 107– 16. Horn, S.P. 2005. Dinámica de la vegetación después de fuegos recientes en los páramos de Buenavista y Chirripó, Costa Rica. In M. Kappelle

704 Chapter 20 and S.P. Horn, eds., Páramos de Costa Rica, 631– 55. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Horn, S.P., and L.M. Kennedy. 2006. Pollen evidence of the prehistoric presence of cattail (Typha sp.) in Palo Verde National Park, Costa Rica. Brenesia 66: 85– 87. Horn, S.P., K.H. Orvis, and K.A. Haberyan. 2005. Limnología de las lagunas glaciales en el páramo del Chirripó, Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 161– 81. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Hurtado-Astaiza, J. 2003. Abundancia, diversidad, riqueza, uso de hábitat y comportamiento de aves acuáticas: una comparación entre un humedal seminatural y un arrozal con riego en Costa Rica. M.Sc. thesis, Wildlife Management Regional Program (PRMVS), Universidad Nacional (UNA). Heredia, Costa Rica. 108 pp. Islebe, G., H. Hooghiemstra, and R. van’t Veer. 1996. Holocene vegetation and water level history in two bogs of the Cordillera de Talamanca, Costa Rica. Vegetatio 124:155– 71. Islebe, G., H. Hooghiemstra, and R. van’t Veer. 2005. Historia holocénica de la vegetación y el nivel de agua en dos turberas de la Cordillera de Talamanca, Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 237– 52. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Janzen, D.H. 1978. Description of a Pterocarpus officinalis monoculture in Corcovado National Park. Brenesia 14– 15: 305– 9. Janzen, D.H., ed. 1983. Costa Rican Natural History. Chicago: University of Chicago Press. 816 pp. Jiménez, I. 2000. Los manatíes del río San Juan y los canales de Tortuguero: ecología y conservación. San José, Costa Rica: Amigos de la Tierra. 120 pp. Jiménez, J.A. 1981. The mangroves of Costa Rica: a physiognomic characterization. M.Sc. thesis, University of Miami. Miami, FL. 130 pp. Jiménez, J.A., J.C. Calvo, E. González, and F. Pizarro. 2005. Conceptualización de caudal ambiental en Costa Rica: determinación inicial para el río Tempisque. San José, Costa Rica: IUCN. Jiménez, J.A., E. González, and J. Calvo. 2003. Recomendaciones técnicas para la restauración hidrológica del Parque Nacional Palo Verde. San Pedro, Costa Rica: Organización para Estudios Tropicales (OTS). 11 pp. Kappelle, M. 1996. Los Bosques de Roble (Quercus) de la Cordillera de Talamanca, Costa Rica: Biodiversidad, Ecología, Conservación y Desarrollo. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). 336 pp. Kappelle, M., M. Castro, H. Acevedo, L. González, and H. Monge. 2003. Ecosystems of the Osa Conservation Area, Costa Rica. Bilingual edition (English-Spanish). Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). 496 pp. Kappelle, M., and J. Savage. 2005. Anfíbios y reptiles de los páramos de Costa Rica. In M. Kappelle and S.P. Horn, eds., Páramos de Costa Rica, 513– 19. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). Lieberman, D., M. Lieberman, R. Peralta, and G.S. Hartshorn. 1985. Mortality patterns and stand turnover rates in a wet tropical forest in Costa Rica. Journal of Ecology 73: 915– 24. López, M.I. 1978. Migración de la sardina Astyanax fasciatus (Characidae) en el río Tempisque, Guanacaste, Costa Rica. Revista de Biología Tropical 26(1): 261– 75. McCoy, M. 1994. Seasonal, freshwater marshes in the tropics: a case

where cattle grazing is not bad. In G. Meffe, C.R. Carroll, and M.A. Sunderland, eds., Principles of Conservation Biology, 352– 53. Sunderland, MA: Sinauer. McCoy, M.B., and J.M. Rodríguez. 1993. Números mensuales de patos silvestres en los pantanos de la cuenca baja del Río Tempisque, Guanacaste, durante las estaciones secas de 1986– 1990. In Proceedings of the Orthnitological Congress of Costa Rica, 9. San José, Costa Rica: CIPA / MNCR / PRMVS / UNA. McCoy, M.B., and J.M. Rodríguez. 1994. Cattail (Typha dominguensis) eradication methods in the restoration of a tropical seasonal, freshwater marsh. In W.J. Mitsch, ed., Global Wetlands: Old World and New, 469– 82. Dordrecht, Netherlands: Elsevier Science. McHargue, L.A., and G.S. Hartshorn. 1983. Seed and seedling ecology of Carapa guianensis. Turrialba 33(4): 399– 404. Mora, M., J. Cabrera, and G. Galeano. 1997. Reproducción y alimentación del gaspar Atractosteus tropicus (Pisces: Lepisosteidae) en el Refugio Nacional de Vida Silvestre Caño Negro, Costa Rica. Revista de Biología Tropical 45(2): 861– 66. Myers, R.L. 1990. Palm Swamps. In A.E. Lugo, M. Brinson, and S. Brown, eds., Forested Wetlands, 267– 86. Amsterdam: Elsevier Science Publishers. 527 pp. Phillips, S. 1995. Holocene evolution of the Changuinola Peat Deposit, Panama: Sedimentology of a marine-influenced tropical peat deposit on a tectonically active coast. PhD diss., University of British Columbia. British Columbia, Canada. Pizarro, J.F., and J.R. Rojas. 1993. Presencia de tilapia, Oreochromis (Pisces: Cichlidae) en la desembocadura del río Bebedero, Golfo de Nicoya, Costa Rica. Revista de Biología Tropical 41(3b): 921– 24. Programa Estado de la Nación. 2003. Noveno Informe del Estado de la Nación en Desarrollo Humano Sostenible. San José, Costa Rica: Programa Estado de la Nación. Ramsar Convention. 2009. The Ramsar Convention definition of “wetland” and classification system for wetland type. http://www .ramsar.org. Rodgers, J.C., and S.P. Horn. 1996. Modern pollen spectra from Costa Rica. Palaeogeography, Palaeoclimatology, Palaeoecology 124: 53– 71. Rodríguez, G. 2004. Importancia de los Humedales en Costa Rica: Investigadores relacionados con el tema de Humedales. San José, Costa Rica: Asamblea Legislativa. 14 pp. Saber, P.A., and W.A. Dunson. 1978. Toxicity of bog water to embryonic and larval anuran amphibians. Journal of Experimental Zoology 204(1): 33– 42. Sáenz, I., M. Protti, and J. Cabrera. 2006. Composición de especies y diversidad de peces en un cuerpo de agua temporal en el Refugio Nacional de Vida Silvestre Caño Negro, Costa Rica. Revista de Biología Tropical 54(2): 639– 45. Sánchez, J. 2001. Estado de la población de Cocodrilos (Cocrodylus acutus) en el río Tempisque, Guanacaste. Santo Domingo de Heredia, Costa Rica: Instituto Nacional de Biodiversidad (INBio). 49 pp. Scott, D.A., and M. Carbonell, eds. 1986. A Directory of Neotropical Wetlands. Cambridge, UK: IUCN. 684 pp. Serrano-Sandí, J., F. Bonilla-Murillo, and M. Sasa. 2013. Distribution, surface and protected area of palm swamps in Costa Rica and Nicaragua. Revista de Biología Tropical 61(suppl. 1): 25– 33. Solano, J. 2004. Estudio de la distribucion y abundacia de Parkinsonia aculata y Typha dominguensis en el Humedal Palo Verde. Research

Bogs, Marshes, and Swamps of Costa Rica 705 Report for the B.Sc. Degree, Instituto Tecnológico de Costa Rica (ITCR). Cartago, Costa Rica. 97 pp. Soto, R., and E. Arias. 1994. Informe de humedales de la Península de Osa. Agua Buena de Rincón de Osa, Costa Rica: Fundación Neotrópica, Proyecto Boscosa. 29 pp. Sylvander, R.B. 1978. Los bosques del país y su distribución por provincia. Desarrollo integral de los recursos forestales. PNUD/FAOCOS/72/013. Dirección General Forestal, San José, Costa Rica: Working Paper No. 15. 64 pp. TNC (The Nature Conservancy). 2009. Evaluación de Ecorregiones de Agua Dulce de Mesoamérica: Sitios Prioritarios para la Conservación en las Ecorregiones de Chiápas a Darién. San José, Costa Rica: The Nature Conservancy. 515 pp. Trama, F. 2004. Restauración del Humedal Palo Verde para aves. Ambientico 129: 11– 12. Trama, F. 2005. Manejo Activo y Restauración del Humedal Palo Verde: Cambios en las coberturas de vegetación y respuesta de las aves acuáticas. M.Sc. thesis, Universidad Nacional, Heredia, Costa Rica: International Institute on Wildlife Management and Conservation (ICOMVIS). 154 pp. Trama, F., F.L. Rizo-Patrón, and M. Springer. 2009. Macroinvertebrados bentónicos del Humedal de Palo Verde, Costa Rica. Revista de Biología Tropical 57(suppl. 1): 275– 84. Umaña, G. 1991. Fitoplancton de Caño Negro: un llano de inundación tropical, Costa Rica, América Central. Proceedings of the III National Congress on Biology. San Pedro, Costa Rica: University of Costa Rica. 31 pp. Urquhart, G.R. 1997. Paleoecological evidence of Raphia in the precolumbian Neotropics. Journal of Tropical Ecology 13(6): 783– 92.

Urquhart, G.R. 1999. Long-term persistence of Raphia taedigera Mart. swamps in Nicaragua. Biotropica 31(4): 565– 69. Vial, J.L. 1966. Variation in altitudinal populations of the salamander, Bolitoglossa subpalmata, on the Cerro de la Muerte, Costa Rica. Revista de Biología Tropical 14: 111– 21. Vial, J.L. 1968. The ecology of the tropical salamander Bolitoglossa subpalmata in Costa Rica. Revista de Biología Tropical 15: 13– 115. Villarreal-Orias, J.A. 1997. Estado actual, presas y uso del hábitat del jabirú (Jabirú mycteria) en la cuenca baja del río Tempisque, Costa Rica. M.Sc. thesis, Regional Wildlife Management Program (PRMVS), Universidad Nacional. Heredia, Costa Rica. Villarreal-Orias, J.A. 2000. Tamaño poblacional, reproducción y habitat del jabirú (Jabiru mycteria) en el Área de Conservación Tempisque, Costa Rica. Regional Wildlife Management Program (PRMVS), Universidad Nacional. Heredia, Costa Rica. 24 pp. Webb, E.L. 1998. Gap-phase regeneration in selectively-logged lowland swamp forest, northeastern Costa Rica. Journal of Tropical Ecology 14(2): 247– 60. Webb, E.L. 1999. Growth ecology of Carapa nicaraguensis Aublet (Meliaceae): implications for natural forest management. Biotropica 31(1): 102– 10. Weston, A.S. 1981. Páramos, Ciénagas and Subpáramo Forest in the Eastern Part of the Cordillera de Talamanca. San José, Costa Rica: Tropical Science Center ( TSC). 15 pp. Zamora, N., and J. Bravo. 1992. Caracterización de la Vegetación del Refugio Nacional de Vida Silvestre Caño Negro, Alajuela, Costa Rica. Revista de Ciencias Ambientales 9: 4– 21.

Chapter 21 Costa Rican Ecosystems: A Brief Summary

Maarten Kappelle1,2

Introduction The present volume, Costa Rican Ecosystems, offers an extensive panorama of the main terrestrial, freshwater, coastal, and marine ecosystems that inhabit the small tropical country of Costa Rica. Actually, all key ecosystems that occur in the tropics— with exception of arid deserts and snowy mountain caps— are found in this tiny piece of land and sea along the Central American Isthmus— probably the most species-dense country on Earth (Kappelle, chapter 1 of this volume). In this closing chapter, a summary of Costa Rica’s main ecosystems is given, using the preceding chapters as its foundation. It tries to offer the reader a synopsis of Costa Rica’s overwhelming diversity of life at the highest organizational level: the ecosystem. Hence, this chapter touches briefly upon alpha, beta, and gamma levels of biodiversity, and points out some of the main ecological processes that act at the interface of species and their environment. However, the chapter is not meant to give a full overview of each individual ecosystem; to better understand the ins and outs of each ecological system, the reader is referred to the corresponding chapter for further reading.

Oceanic and Coastal-Marine Ecosystems Costa Rica’s marine and coastal ecosystems include a wealth of plant and animal associations, from the deep sea bottom up to the Pacific and Caribbean shores. These ecosystems contain almost 7,000 species of vertebrates, invertebrates, plants, and microorganisms; almost 75% of all species occur in the Pacific salty waters. Invertebrates are 709

most abundant with nearly 4,000 species at the Pacific coast and Ocean (Cortés, chapter 5 of this volume). At sea level the mean annual temperature is approximately 27°C (Herrera, chapter 2 of this volume). Rocky intertidal shores make up for more than half of the Pacific coast and offer a home to both carnivorous and herbivorous gastropods. At Cahuita on the Caribbean coast a kind of endolithic fauna on top of carbonate substrates is observed (Cortés, chapter 17 of this volume). At Isla del Coco the rocky intertidal environment colors pink and black owing to incrusting algae that grow over barnacles on rock outcrops; here, caves abound along the island’s steep rocky cliffs (Cortés, chapter 7 of this volume). Intertidal barnacles like Tetraclita rubescens and T. stalactifera as well as the porcellanid crab, Petrolisthes armatus, have been observed at rocky outcrops along the Golfo de Nicoya (Vargas, chapter 6 of this volume). Sandy beaches occur widely along both coasts and include some of the last, globally significant nesting sites of marine turtles. Four species nest along the Caribbean shores: Chelonia mydas (green turtle), Dermochelys coriacea (leatherback), Eretmochelys imbricata (hawksbill), and sporadically Caretta caretta (loggerhead) (Cortés, chapter 17 of this volume). At Ostional along the Pacific coast (Península de Nicoya) a significant portion of the world’s population of olive ridley turtles (Lepidochelys olivacea) nests. In the northern sector of the Caribbean shores, between Barra del Colorado and Moín, a number of elongated 1 World Wide Fund for Nature (WWF International), Avenue du MontBlanc 1196, Gland, Switzerland 2 Department of Geography, University of Tennessee, Knoxville, TN 37996, USA

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coastal lagoons occur parallel to the coastline. They form part of a wave-dominated delta that has formed along a passive continental margin. The northern lagoons are home to manatees and fish species alike. Sadly, their manatee populations are declining because of human action. The lagoons include a few dredged sections and are all interconnected. On the flooded lands along the channels Pterocarpus officinalis trees and Raphia taedigera palms dominate the vegetation structure. The southern section of the Caribbean coast lacks these typical lagoons and has— just like the Pacific coast— seismically active continental margins (Alvarado and Cárdenes, chapter 3, and Cortés, chapter 17, of this volume). At the ecotone of the river mouths of the Río Tempisque and Río Grande de Térraba occur large swaths of mangrove forests with a variety of salt-tolerant trees such as Avicennia germinans and Rhizophora mangle. They represent some of the best developed, most diverse, and largest mangroves in Central America. These cradles of biodiversity act as filters between river watersheds and marine systems and serve as nurseries for numerous prawn, bivalves, and fishes (Cortés, chapter 5 of this volume). At the same time, seasonality of the mangrove-rich Golfo de Nicoya seems to be determined by salinity changes as a result of rainfall differences, rather than by changes in water temperature (Vargas, chapter 6 of this volume). Here, primary production is among the highest reported for tropical estuaries. On the other hand, mangrove forests along the Caribbean coast are less well developed and less productive. The small patch of mangroves found close to Moín, the main port at the Caribbean close to Puerto Limón, has been negatively impacted by construction and pollution. Fortunately, the largest mangrove forest on the Caribbean coast— the one at Laguna Gandoca— is rather well preserved. Next to the previously mentioned mangrove species, two other mangrove species are found at Gandoca, Laguncularia racemosa and Conocarpus erectus (Cortés, chapter 17 of this volume). At other places, like in the upper Golfo de Nicoya, intertidal sand and mud flats exist, which form essential habitat to tropical tidal flat benthos and a variety of migratory shorebirds (e.g, waders). Subtidal sediments— those that are permanently submerged— abound in the Golfo de Nicoya and provide a home to infaunal communities of polychaete worms, crustaceans, and mollusks. The flats near the port of Punta Morales are dominated by deposit-feeding polychaete worms. Nematoda, Foraminifera, Copepoda, and Ostracoda have been reported from this site (Vargas, chapter 6 of this volume). Highly productive seagrass beds dominated by marine

flowering plants are relatively rare in Costa Rica but do occur along the Pacific coast— for instance, along the mouth of the Sierpe river (Cortés, chapter 5 of this volume). At the Caribbean coast seagrass species Thalassia testudinum and Syringodium filiformis form extensive beds, mainly in reef lagoons. In Cahuita, average productivity of T. testudinum was 2.7 ± 1.15 g/m2 /day (Fonseca et al. 2007, cited by Cortés, chapter 17 of this volume). Coral reefs occur along both the Pacific and Caribbean shores. Coral community patches and isolated coral colonies cover only a few hectares, have a low coral diversity, and are discontinuous (Cortés, chapter 5 of this volume). Pacific coastal reefs may be constructed and dominated by coral species such as Pavona gigantea, P. clavus, and Pocillopora eydouxi. Unfortunately, several reefs such as those found at places between Cabo Blanco and Golfo de Nicoya are mostly dead, while recovery is slow. Isla del Caño off the west coast of Península de Osa has some of the most extensive coral reefs of the country. Here, pocilloporids dominate reef associations, although twenty species of octocorals, two black corals, seventeen reef-building corals, and four ahermatypic coral species have been identified from this island (Cortés, chapter 5 of this volume). Along the Caribbean coast, fringing reefs are found between Moín and Limón, including Isla Uvita. However, the largest Caribbean fringing reef plus patch reefs and carbonate banks are observed inside Parque Nacional Cahuita. Additionally, smaller patches are located between Puerto Viejo and Punta Mona. Unfortunately, the 1991 Limón Earthquake, which uplifted the coast, together with coral bleaching and the massive dying of sea urchins have taken their toll on the Caribbean reefs, as Cortés explains (Cortés, chapter 17 of this volume). In turn, Isla del Coco has extensive coral reefs and coral communities made up of eighteen species of zooxanthellate corals and fifteen azooxanthelate species. The main reef builder is Porites lobata. Isla del Coco’s reefs are partially eroded biologically by corallivores that feed on them, like the crown-of-thorns starfish Acanthaster planci and the pufferfish Arothron meleagris. Unfortunately, thirty years ago the island’s coral reefs were severely impacted by the 1982– 1983 El Niño Southern Oscillation (ENSO) event, from which the reefs still recover (Cortés, chapter 7 of this volume). Rhodolith beds composed of coralline red macroalgae are found at Isla del Coco. Costa Rica’s pelagic ecosystem— which includes the neritic or coastal zone and the oceanic zone— is rich in plankton, fish, whales, and dolphins (e.g., the spotted coastal dolphin, Stenella attenuata; Cortés, chapter 7 of this volume). In the Golfo de Nicoya some

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dinoflagellates that are part of the local phytoplankton community, like Cochlodinium catenatum, may occasionally cause harmful red tides (marea roja, a kind of toxic algal bloom) that lead to increased fish mortality (Vargas, chapter 6 of this volume). Little is known about the deep benthos of Costa Rica. However, bacterial mats and specific bivalves have been observed in some deep, low-oxygen waters in the Pacific Ocean (Cortés, chapter 5 of this volume). The deep Golfo Dulce serves as a low-oxygen tropical fjord. The Golfo de Nicoya is rich in commercial fish species such as corvina (Sciaenidae), red snapper (Lutjanidae), sea catfishes (Ariidae), and flatfishes (several families). Other common groups include sharks (e.g., Mustelus dorsalis, M. lunulatus), rays (e.g., Urotrygon cimar), flounders, gobies, morays, and congers (Vargas, chapter 6 of this volume). At Isla del Coco there is no gradual change from a shallow (5 cm is around 500 stems per hectare at 2,700 m, while 2,500 stems per hectare are recorded in young (20 to 30 yr old) successional cloud oak forests (Kappelle, chapter 14 of this volume). At an altitude of about 1,500 m in the 18– 25 m tall cloud forests of Monteverde there are approximately 555 stems >10 cm dbh per hectare, responsible for a basal area of almost 75 m2 and an aboveground, terrestrially rooted biomass of almost 500 Mg (Lawton et al., chapter 13 of this volume, and references therein). As a general rule, however, cloud forest structure may differ significantly between slopes depending on slope orientation (windward vs. leeward), rainfall (rainy vs. rain shadow), elevation (temperature variations), and soil (nutrient rich vs. leached horizons). Species diversity in Costa Rican cloud forests is tremen-

dous. Together with the Andean montane forests, Costa Rican (and Panamanian) cloud forests are among the richest in the world and serve as a center of speciation from which many species originated and radiated into northern Meso-America, the Caribbean, and southern South America. Hence, endemism is locally low at the genus level but high at species level. Plant genera such as Epidendrum (an orchid), Elaphoglossum (a fern), Peperomia, Senecio sensu lato, and Anthurium (herbs), Psychotria, Miconia, and Solanum (shrubs), and Chusquea (a bamboo) are particularly rich in endemic species (Kappelle, chapter 14 of this volume). In the Monteverde region (area: 350 km2) over 3,000 plant species have been recorded, which is about a quarter of all plant species known from Costa Rica. Here, above 700 m elevation more than 750 plant species in some 100 genera are trees, of which at least 10% are fruiting or flowering in any given month, while around a hundred bloom especially during the drier months of March, April, and May. Orchid diversity (e.g., Elleanthus, Epidendrum, Lepanthes, Maxillaria, Pleurothallis, Scaphyglottis, Stelis, and Telipogon) is extraordinary with over 30 species known from Monteverde alone (Lawton et al., chapter 13 of this volume). Further south, in the Cordillera de Talamanca, plant species diversity is even higher and possibly up to 5,000 species have their home in Talamanca’s rain and cloud forests at elevations over 500 m above sea level. Around 250 ground-rooted vascular plant genera dominate the Talamancan montane oak forests between 2,000 and 3,200 m elevation. It is here that fungal and lichen diversity is greatest, with some 400 species of Agaricales and over a hundred known foliose and fruticose lichens (Kappelle, chapter 14 of this volume). The average Costa Rican cloud forest flora is composed of many canopy and subcanopy tree genera including Alchornea, Alnus, Brunellia, Buddleja, Clethra, Cleyera, Clusia, Drymis, Escallonia, Ficus (some figs like the hemi-epiphytic Ficus crassiuscula show a strangling behavior), Guarea, Inga, Magnolia, Meliosma, Myrcianthes, Myrsine, Ocotea, Oreopanax, Persea, Prunus, Quercus, Rhamnus, Schefflera, Symplocos, Trichilia, Weinmannia, Zanthoxylum, and the gymnosperm Podocarpus. In the Cordillera de Talamanca, mountain forests between 2,000 and 3,200 m elevation are mostly dominated by species of Quercus (oak), often with understories characterized by Chusquea bamboos (Kappelle, chapter 14 of this volume). One particular endemic cloud forest tree species is the 20– 30 m tall Ticodendron incognitum, a remnant of the Tertiary Laurasian flora. Being the only species in the new family Ticodendraceae it was discovered in 1989 and resembles alder (Alnus). In general, seeds of a third of all tree species are bird-dispersed while seeds of around a tenth are dispersed by wind. Cloud forest

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trees are accompanied in the understory by shrubs (Ardisia, Ilex, Macleania, Miconia, Palicourea, Psychotria, Rubus, Senecio, Solanum, and Vaccinium) and dwarf palms (Chamaedorea, Geonoma, Prestoea) as well as by numerous pteridophytes including tree ferns (Culcita, Cyathea, Dicksonia, Lophosoria). The most species-rich woody families are Rubiaceae, Melastomataceae, Lauraceae, Asteraceae, and Ericaceae, which together represent about 30% of the total number of known woody species in Talamancan montane oak forests. Seeds of Melastomataceae, Solanaceae, and Rubiaceae found at Monteverde are mostly dispersed by opportunistic frugivorous tanagers, finches, and thrushes (Lawton et al., chapter 13 of this volume). Lianas are less common (Hydrangea, Passiflora). Hundreds of mosses and liverworts thrive here and may form impressive curtains in the forest interior (Dendropogon, Pilotrichella) or cover large sections of the bark of trees (e.g., Frullania, Plagiochila) (Kappelle, chapter 14 of this volume). Rodents predate on seeds of many of these cloud forest trees and shrubs including species in the genera Ocotea, Guarea, Eugenia, and Beilschmiedia (Lawton et al., chapter 13 of this volume). Arthropod diversity in Costa Rica’s mountain forests is immense, with thousands of insects known from Monteverde, for instance. However, there is no clear insight in species numbers owing to the lack of extensive sampling at mid- and high elevation. Arboreal arthropod communities are particularly rich in species, some of which have been studied in detail (e.g., species in the ant genus Myrmelachista). Another ant genus (Azteca) forms mutualistic relations with Cecropia trees, similar to the protective cooperation that happens between ants and acacia-like species in Costa Rica’s dry lowlands (Jiménez et al., chapter 9 of this volume). A large amount of insects including numerous bees, beetles, butterflies, flies, and wasps pollinate the flowers of nearly half of the cloud forest canopy tree species, including the Lauraceae, at Monteverde (Lawton et al., chapter 13 of this volume). The highland bumblebee (Bombus ephippiatus) is a key pollinator in the Talamancan montane oak woodlands. Fish diversity is extremely low in Costa Rican highland forest streams over 2,000 m elevation. The only common species is the exotic rainbow trout (Oncorhynchus mykiss) that has been introduced for commercial and recreational purposes. On the contrary, native amphibians and reptiles form an essential component of Costa Rica’s montane cloud forests. Lawton et al. (chapter 13 of this volume) mention the presence of sixty amphibians in the Cordillera de Tilarán, of which over fifty are anurans (frogs, toads) and a hundred are reptiles (70% of which are snakes [e.g., vipers] and the remainder lizards). The green spiny lizard (Sceloporus malachiticus) and the highland alligator lizard

(Mesaspis monticola) are commonly observed in the Talamancan oak forests. Eleutherodactylus is one of the most species-rich genera of frogs on Costa Rica’s mountains. Populations of other anurans such as the golden toad, Bufo periglenes, and the harlequin frog, Atelopus varius, seem to have collapsed over the past decades, probably owing to an emergent, climate-change– related epidemic caused by a chytrid fungus. The golden toad, which used to be endemic to the Monteverde Cloud Forest Reserve, is now considered extinct and consequently has become the symbol of cloud forest destruction globally. In Monteverde alone 425 species of bird have been spotted including the spectacular resplendent quetzal (Pharomachrus mocinno), the three-wattled bellbird (Procnias tricarunculata), the well-studied brown jay (Cyanocorax morio), and some 30 species of hummingbirds (Trochilidae). A large number of these birds play roles as flower pollinators or seed dispersers. At least 560 species of bird have been recorded in Parque Nacional Chirripó and Parque Internacional La Amistad. Common bird families are Emberizidae, Parulidae, Thraupidae, Trochilidae, Turdidae, and Tyrannidae. Over the past three decades the quetzal, an altitudinal migrant, has become the flagship bird species in conserving remnant cloud forest fragments in Costa Rica. Cloud forest mammal diversity is equally spectacular with over 120 species living in the central Cordillera de Tilarán, including 58 bats, 15 murid rodents, and two endemic mammals (a harvest mouse and a shrew). Eight of the bat species (e.g., Artibeus toltecus) are frugivorous and feed on fruits of some forty plant species, while about 10% of the Monteverde’s plant species are pollinated by bats. Large cats such as pumas, ocelots, and margays thrive here, as well as brocket deer, sloths, pacas, coyotes, squirrels, collared peccaries, and Baird’s tapirs. Monkeys are a common feature in these mountains (e.g., capuchin, howler, and spider monkeys). Rodents like Muridae and Heteromyidae may abound during years following mast seeding of oak trees in the upper valley of the Río Savegre (Kappelle, chapter 14 of this volume). At (sub)alpine elevations above the timber or treeline at 3,000 to 3,400 m elevation cloud forest is replaced by treeless grasslands and shrublands, often dominated by clump-forming Chusquea subtessellata bamboos. This is the so-called páramo, a tropical alpine, tundra-like, cool and wet ecosystem (in fact, it is a biome in its own!), composed of bamboos, shrubs, herbs, grasses, ferns, mosses, liverworts, and lichens (Kappelle and Horn, chapter 15 of this volume). The presence of the ericad shrub Comarostaphylis arbutoides marks the border between cloud forest and páramo. During the late Quaternary the Costa Rican páramo landscape underwent repeated glacial cycles of cool-

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ing and warming that left their traces on the rocky outcrops and formed U-shaped valleys and glacial lakes (Alvarado and Cárdenes, chapter 3 of this volume). Today, páramo is found at the summits of the Irazú and Turrialba volcanoes and at the higher mountain peaks along the Cordillera de Talamanca, including the cerros of Vueltas, Muerte, Cuericí, Urán, Chirripó, Amo, Dúrika, Dudu, and Kámuk. Two-thirds of Costa Rica’s 15,000 hectares of páramo vegetation is found in the heart of Parque Nacional Chirripó, which is dominated by the 3,819 m high Cerro Chirripó. The climate is characterized by strong daily fluctuations in temperature and cloud cover (Herrera, chapter 2 of this volume). The average annual páramo temperature ranges from 11.0°C at 3,000 m to about 6°C at 3,800 m. Rainfall may vary significantly among mountain slopes. Depending on slope orientation the yearly mean rainfall is somewhere between 1,000 and 4,000 mm (Kappelle and Horn, chapter 15 of this volume). Páramo soils belong mostly to Histisols, Entisols, Inceptisols, and Andisols (Alvarado and Mata, chapter 4 of this volume). Páramo species diversity is extraordinary if we take into account the small surface that this ecosystem occupies in Costa Rica. Eukaryotic algae (41 genera) abound in the páramo lakes and ponds, while true fungi (272 species) are extremely diverse as well. The same applies to lichens (204 páramo species), mosses (117 species), liverworts (113 species), and ferns (80 species including fern-allies). To date 416 flowering plants have been recorded, out of which 146 are endemic to Costa Rica and Panama. At the genus level several plant taxa are endemic to these páramos: Iltisia, Jessea, Laestadia, Talamancalia, and Westoniella. The endemic Westoniella is represented by six species. Other vascular plant genera that are true páramo inhabitants are Alchemilla, Azorella, Castilleja, Draba, Gnaphalium, Lewisia, Lysipomia, Poa, Ranunculus, Senecio, Stevia, and Uncinia. Most of the flowering páramo plants have special adaptations (e.g., short stems, hairy leaves) to withstand the harsh climate. A number of plant species also display adaptations to cope successfully with páramo fires that occur naturally at regular intervals. Unfortunately, páramo fire frequency has increased over the past decades owing to human activity. This has negatively impacted páramo recovery in a number of places. Fortunately, the bamboo Chusquea subtessellata seems to recover quickly after a fire has taken place (Kappelle and Horn, chapter 15 of this volume). In terms of animal diversity a total of 71 insects have been reported, as well as 27 mollusks. Nineteen species of amphibians and reptiles are known, including the mushroom-tongue salamander, the montane alligator lizard, and the green spiny lizard. Birds are omnipresent and

include seventy species, twelve of which are considered true páramo species. Most páramo birds are carnivorous (e.g., the red-tailed hawk), nectarivorous (for instance, the volcano hummingbird), or frugivorous (such as the sooty robin). Birds are responsible for the pollination of 8% of all páramo plant species and for seed dispersal of 20% of all plants. Mammals, in turn, are represented by 32 species, many of which are abundant in Costa Rican páramo. Shrews, rabbits, tapirs, ocelots, margays, and even pumas can be observed in remote areas (Kappelle and Horn, chapter 15 of this volume).

The Wetlands Wetlands (“humedales”) are areas in which water covers the soil, or is present either at or near the surface of the soil, year-round or for varying periods of time. Costa Rica’s wide variety of natural wetlands includes rivulets, rivers, lagoons, ponds, lakes, coastal channels, seasonal swamps dominated by forest trees or palms, marshes, water-logged peat bogs, and hot springs. A separate category of Costa Rican wetlands concerns the artificial reservoirs that result from river damming for the generation of hydroelectric power, as is the case for Lago Arenal (Costa Rica’s biggest water body), Lago de Cachí, and Lago Angostura. Some of these wetlands are determined by freshwater (the inland or non-tidal wetlands) while others are characterized by brackish or more saline waters (coastal or tidal wetlands). The latter include mangrove forests which have been dealt with earlier in this chapter (see under “Oceanic and Coastal-Marine Ecosystems”). They are spread over 34 major watersheds (Pringle et al., chapter 18 of this volume) and drain into the Caribbean Sea or Pacific Ocean. Costa Rica’s limnology is characterized by multiple parallel river systems with relatively small drainage areas. They run from the highest peaks to the coastal zones. An exception to this rule is the Río San Juan watershed, which is the largest watershed in Central America and shared with Nicaragua. Hundreds of permanent water bodies are found in these watershed basins. Horn and Haberyan (chapter 19 of this volume) report a total of 652 lakes in Costa Rica, including seasonal ponds and brackish lagoons. They originate from volcanic activity, fluvial dynamics, past glaciations, or landslides. Many streams and lakes have a geochemical solute composition which is determined by the input from acid-sulfate and sodium-chloride-bicarbonate springs that originate along volcano slopes. Algal groups like Cyanobacteria (blue greens), which include the genera Phormidium, Lyngbya, Dermocarpa, Oe-

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dogonium, and Oscillatoria, inhabit hot springs at Tabacón at Lago Arenal. Laguna Solimar, a turbid eutrophic lake near Cañas north of the Golfo de Nicoya, is cyanophytedominated, with Cylindrospermum as the most common phytoplankton and the copepod Mesocyclops thermocyclopoides as the principal zooplankton species (Horn and Haberyan, chapter 19 of this volume). At the southern tip of the Cordillera de Guanacaste, phytoplankton of Laguna Cerro Chato is dominated by chlorophytes, especially Arthrodesmus bifidus and Monorhaphidium griffithii. The lake’s zooplankton is determined by the copepod Tropocyclops prasinus prasinus (Horn and Haberyan, chapter 19 of this volume, and references therein). Diatom genera, on the other hand, such as Chamaepinnularia, Eunotia, Frustulia, and Stauroneis thrive particularly in acidic rivers like the Río Agrio, which drains Volcán Poás (Pringle et al., chapter 18 of this volume). Laguna Barva at the summit of the volcano of the same name is dominated by small cryptophytes, desmids, cyanobacteria, and chlorophytes. Glacial lakes in the páramo of Parque Nacional Chirripó harbor phytoplankton that includes cyanobacteria, chlorophytes, pyrrhophytes, and diatoms such as Aulacoseira sp. Some diatom species in the genus Navicula are indicative of organic pollution in Costa Rican streams. Costa Rican highland bogs cover only 235 ha and are distributed from 1,200 to 3,100 m elevation. A good example is the series of bogs at the Sabanas de Dúrika in the Cordillera de Talamanca. Here, repeated fire in the neighboring páramo vegetation may negatively affect water retention properties at ground level and consequently impact the aquatic bog vegetation. High-elevation bogs in the Talamanca mountains harbor up to a hundred species of aquatic and semi-aquatic forbs, grasses, and sedges. Normally, these peaty bogs show a clear zonation of plants from the semi-aquatic edge to the wetter core of the bog. At the bog edge grows a plant community that includes the páramo bamboo Chusquea subtessellata, the bunch grass Cortaderia nitida, and shrubs like Myrsine coriacea, Escallonia myrtillioides, and Hesperomeles heterophylla. Halfway, closer to the bog’s center, one observes the large, cycad-like fern Blechnum buchtieni, the endemic bromeliad Puya dasylirioides, shrubs like Pernettya prostrata and Hypericum strictum, and yellow-eyed grasses in the genus Xyris. In the core of the bog one may observe Hypericum together with Paepalanthus, Hieracium, Utricularia, Isoetes, and Pernettya. Here, Carex sedges, Juncus rushes, mosses like Campylopus, Sphagnum, and Breutelia, and Cladina lichens abound. The acidic and tannin-stained Tres de Junio pond and its bog vegetation at 2,670 m elevation in the Cordillera

de Talamanca (close to Cerro de la Muerte) is less than 1 m deep and inhabited by abundant Sphagnum mosses on hummocks and edges. Further south is the largest glacial lake of Costa Rica, the 22 m deep Lago Chirripó. Sitting at the base of Cerro Chirripó’s páramo vegetation it harbors abundant quillworts (Isoetes storkii) that grow along the edge of the lake (Horn and Haberyan, chapter 19 of this volume). The bog salamander Bolitoglossa pesrubra thrives among the wet leaves of Puya dasylirioides bromeliads. This bog environment is shared with a dink frog (Diasporus ventrimaculatus) as well as with the sooty thrush or robin (Turdus nigrescens) ( Jiménez, chapter 20 of this volume, and references therein). Marshes are more widespread in the country than bogs and reach a total surface of 30,000 ha. They occur in basins and depressions where rainfall and run-off water accumulate. Palm-dominated swamps and seasonally flooded forest swamps together cover about 140,000 ha of land in the country. The marshes of the Caribbean coastal lowlands are dominated by large Calathea, Montrichardia, and Thalia forbs in combination with Cyperus and Lasciacis sedges, Panicum and Scleria grasses, and Ipomoea and Solanum vines. More-open marshes in the Sarapiquí region provide a niche for Spathiphyllum friedrichstallii and Acalypha diversifolia plants. Caribbean wetlands also provide a home to aquatic grasses like Brachiaria and Panicum and to floating water hyacinths (three species of Eichhornia). Similar species assemblages are found in the marshes of Caño Negro and Palo Verde in the north, and at the headwaters of Río Sierpe in the southern part of the country. Open waters at Caño Negro are seasonally covered by Nymphaea water lilies, the water lettuce Pistia stratiotes, and species in the genera Neptunia, Polygonum, and Salvinia. In turn, at the borders of the 1,200 ha Palo Verde marsh one may observe the palo verde treelet (Parkinsonia aculeata), the Amazon sword plant Echinodorus paniculatus, and Cyperus or Eleocharis sedges. Here, at deeper sites, Nymphaea and Eichhornia species co-dominate the floating vegetation (Jiménez, chapter 20 of this volume). Aggressive cattails (Typha dominguensis) show invasive behavior in the freshwater marshes of Parque Nacional Palo Verde (Horn and Haberyan, chapter 19 of this volume). Costa Rican palm swamps are mostly found in the wildlife refuges of Barro Colorado and Caño Negro, as well as in Parque Nacional Tortuguero and the Sierpe-Osa region. They are seasonally flooded and dominated by the palm species Raphia taedigera (“yolillo”) and Manicaria saccifera. In palm swamps plant species diversity is normally low, with less than thirty species found at a single spot. True forest tree– dominated swamps are often characterized by

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Pterocarpus officinalis, Carapa guianensis, Astrocaryum alatum, Pentaclethra macroloba, or Symphonia globulifera trees. All in all, these bogs, marshes, and swamps house up to 400 different species of plant ( Jiménez, chapter 20 of this volume). Costa Rica’s river fauna is locally diverse and may differ considerably among and within drainages. Pringle et al. (chapter 18 of this volume) state that freshwater fish assemblages in Costa Rica are diverse and abundant in lowland areas, but decrease toward headwaters, and completely disappear above ~800 m above sea level. So far, a total of 174 fish species have been reported for the country’s freshwater ecosystems, with Cichlidae, Poeciliidae, and Characidae being the most speciose families. They play essential roles in nutrient cycling, primary production, and decomposition in Costa Rican wetlands. Poecilia gillii, for instance, is a diatom-feeding specialist, affecting the structure and composition of algal communities of Laguna Hule. In the latter lake the cichlid Parachromis dovii (“guapote”) and the banded tetra Astyanax aeneus are also observed. An important number of fish species feed on fruits that fall in the water; these fish serve as seed dispersers of many riparian shrubs and trees such as figs. The alien fish Oreochromis niloticus (Nile tilapia) has been introduced in a number of lakes, including Laguna Chocuaco— which is also known as Laguna Vueltas— close to the Río Grande de Térraba (Horn and Haberyan, chapter 19 of this volume). Furthermore, the seasonal ponds of Caño Negro house ichtyofaunal communities that may be composed of at least 21 different fish species, including the endangered, 50– 60 cm long, carnivorous Atractosteus tropicus, which is locally known as gaspar ( Jiménez, chapter 20 of this volume). Big, marine-derived freshwater shrimps in the genus Macrobrachium, a macroconsumer, are abundant at a number of places and serve as prey for other species. Algal assemblages in lowland streams are highly influenced by such omnivorous shrimp assemblages. Other freshwater invertebrates include all major orders of aquatic insects (e.g., dragonflies, caddisflies, stoneflies, and mayflies), which may be highly diverse at many places (Pringle et al., chapter 18 of this volume). Of all known amphibians in Costa Rica, 15– 20 are truly aquatic. Examples are the stream-dwelling frogs Atelopus varius and Rana warszewitschii (Pringle et al., chapter 18 of this volume). The most conspicuous freshwater reptiles are the caimans (Caiman crocodilus), American crocodiles (Crocodylus acutus), and aquatic turtles (Chelydridae, Embydidae, and Kinosternidae), which can be found in riv-

ers up to 350 m elevation. Caimans are still abundant in the Caño Negro marshes where about 3,000 individuals were recorded in the early 1990s. Crocodiles inhabit the Tempisque marshes and mouth of the Río Grande de Tárcoles. River turtles in the genus Rhinoclemmys inhabiting Parque Nacional Tortuguero have been observed feeding on fruits from Dieffenbachia and Ficus, for which they appear to serve as seed dispersers (Pringle et al., chapter 18, and Jiménez, chapter 20, of this volume). A total of 150 bird species are associated with rivers and other freshwater environments. Good examples are the kingfishers, jacanas, ducks (Cairina moschata), and sand pipers (Actitis macularis). The Palo Verde marsh provides a home to sixty species of waterfowl, including Dendrocygna autumnalis ducks and the endangered stork Jabiru mycteria. The marshes of Caño Negro are even richer in terms of avifauna and provide habitat to over 300 species including the jabiru stork and the great white egret (Egretta alba). The green heron (Butorides virescens) is a common feature in the marshes of the Lower Tempisque region ( Jiménez, chapter 20 of this volume). Freshwater mammals in Costa Rican lowland areas are few. Some of the most conspicuous ones are the river otter (Lutra longicaudus), the large fishing bat (Noctilio leporinus), and the manatee (Trichechus manatus) that used to live in rivers and channels near coastal areas, such as found in the Tortuguero region and near Gandoca-Manzanillo (Pringle et al., chapter 18 of this volume). Unfortunately, manatees have been decimated in the country over the past fifty years and are rarely observed today.

Closing Remarks A lot remains to be done to fully understand the diversity and complexity of the structure and functioning of Costa Rican ecosystems. The present book just highlights the main features of the patterns and processes that characterize the ecosystems of this incredible tropical country— and the current chapter only touches quickly upon the most important aspects of those features. It is hoped that future generations will further investigate the ecological systems of this Rich Coast, this immensely rich country, which is arguably the most diverse spot on Earth. It will be in-depth ecological knowledge that is ultimately needed to successfully raise awareness amongst peoples to conserve and where necessary restore these ecological systems on which humans, and particularly Costa Rica’s society, depend so greatly for future survival.

Acronyms

AAAS American Association for the Advancement of Science AC Área de Conservación ACAHN Área de Conservación Arenal Huetar Norte ACAT Área de Conservación Arenal-Tempisque ACCVC Área de Conservación Cordillera Volcánica Central ACE abundance-based cover estimation ACG Área de Conservación Guanacaste ACLAC Área de Conservación La Amistad-Caribe ACLAP Área de Conservación La Amistad-Pacífico ACM Asociación Conservacionista de Monteverde ACMIC Área de Conservación Marina Isla del Coco ACOPAC Área de Conservación Pacífico Central ACOSA Área de Conservación Osa ACT Área de Conservación Tempisque ACTo Área de Conservación Tortuguero AD Anno Domini AECO Asociación Ecologista Costarricense AICA Área Importante para la Conservación de Aves ANAI Asociación Nacional de Asuntos Indígenas ALAS Arthropods of La Selva ASCONA Asociación Costarricense para la Conservación de la Naturaleza ASEDER Asociación de Emprendedores para el Desarrollo Responsable, Osa ASOMOTI Asociación Mono Tití ATBI All-Taxa Biodiversity Inventory AyA Instituto Costarricense de Acueductos y Alcantarillados BCI Barro Colorado Island, Panama BINGO Big International Non-Governmental Organization BP Before Present CARICOMP Caribbean Coastal Marine Productivity Program CARIPOL Marine Pollution Monitoring Program in the Caribbean CAS Central American Seaway CATIE Centro Agronómico Tropical de Investigación y Enseñanza CBD Convention on Biological Diversity CBM Corredor Biológico Mesoamericano CCAD Comisión Centroamericana de Ambiente y Desarrollo CCC Caribbean Conservation Corporation CCT Centro Científico Tropical CCW counterclockwise CEC cation exchange capacity CENAT Centro Nacional de Alta Tecnología CI Conservation International CIMAR Centro de Investigación en Ciencias del Mar y Limnología CITES Convention on International Trade of Endangered Species CLIP Caribbean Large Igneous Province 723

CONARE Consejo Nacional de Rectores CONICIT Consejo Nacional para Investigaciones Científicas y Tecnológicas CORBANA Corporación Bananera Nacional CORENA Conservación de Recursos Naturales Renovables COSUDE Agencia Suiza para el Desarrollo y la Cooperación CRCC Costa Rican Coastal Current CRD Costa Rican Dome CSO civil society organization CSR corporate social responsibility DBCP dibromochloropropane DBH diameter at breast height DCR Domo de Costa Rica DDE dichlorodiphenyldichloroethylene DDT dichlorodiphenyltrichloroethane DGF Dirección General Forestal DGIS Directorate-General for International Cooperation, Netherlands DGVS Dirección General de Vida Silvestre DIVERSITAS International Programme of Biodiversity Science DNA deoxyribonucleic acid DOC dissolved organic carbon DOM dissolved organic matter EARTH Escuela de la Agricultura de la Región Tropical Húmeda EBA Endemic Bird Area ECEC effective cation exchange capacity ECOMA Programa Ecología y Manejo de Tierras Altas, UNA ECOMAPAS Proyecto de Mapeo de Ecosistemas, INBio-SINAC EDU ecological drainage unit EEZ Exclusive Economic Zone ELA equilibrium line altitude ENSO El Niño Southern Oscillation EPA Environmental Protection Agency ESPH Empresa de Servicios Públicos de Heredia ETP Eastern Tropical Pacific EUC Equatorial Undercurrent FAICO Fundación Amigos de la Isla del Coco FAO United Nations Food and Agriculture Organization FFEM Fonds Français pour l’Environnement Mondial FONAFIFO Fondo de Financiamiento Forestal de Costa Rica FPN Fundación de Parques Nacionales FUNDECOR Fundación para el Desarrollo de la Cordillera Volcánica Central GABI Great American Biotic Interchange GDFCF Guanacaste Dry Forest Conservation Fund GEF Global Environmental Facility GHG greenhouse gases GIS geographic information system GOES Geostationary Operational Environmental Satellite GSA Geological Society of America HAB harmful algal bloom HLDG Herbario Luis Diego Gómez HMS His Majesty’s Ship

724 Acronyms ICE Instituto Costarricence de Electricidad ICOMVIS Instituto Internacional de Conservación y Manejo de Vida Silvestre ICRAF World Agroforestry Centre ICT Instituto Costarricense de Turismo IDA Instituto de Desarrollo Agrario IFGN Instituto Físico-Geográfico Nacional IGN Instituto Geográfico Nacional IICA Instituto Interamericano de Cooperación para la Agricultura IMN Instituto Meteorológico Nacional INBio Instituto Nacional de Biodiversidad INCOP Instituto Costarricense de Puertos del Pacífico INCOPESCA Instituto Costarricense de Pesca y Acuicultura INEC Instituto Nacional de Estadísticas y Censos IPCC Intergovernmental Panel on Climate Change ITCO Instituto de Tierras y Colonización ITCR Instituto Tecnológico de Costa Rica ITCZ Intertropical Convergence Zone IUBS International Union of Biological Sciences IUCN International Union for Conservation of Nature IUFRO International Union of Forest Research Organizations LAI leaf area index LOICZ Land-Ocean Interactions in the Coastal Zone LSFR Los Santos Forest Reserve MA Millennium Ecosystem Assessment MAB Man and the Biosphere Program MAG Ministerio de Agricultura y Ganadería MAT Middle American Trench MBC Mesoamerican Biological Corridor MBRS Mesoamerican Barrier Reef System MCFP Monteverde Cloud Forest Preserve MCL Monteverde Conservation League MINAE Ministerio del Ambiente y Energía MINAET Ministerio del Ambiente, Energía y Telecomunicaciones MIRENEM Ministerio de Recursos Naturales, Energía y Minas MNCR Museo Nacional de Costa Rica MODIS Moderate Resolution Imaging Spectroradiometer MPA Marine Protected Area MSS Multi-Spectral Scanner MSY Maximum Sustainable Yield MY Motor Yacht NASA National Aeronautics and Space Administration NEC North Equatorial Current NECC North Equatorial Counter Current NFMP natural forest management plan NGO non-governmental organization NGS National Geographic Society NOAA National Oceanic and Atmospheric Administration NPA Natural Protected Area NPK nitrogen, phosphorus, and potassium NPP net primary production NRC National Research Council NRCS Natural Resources Conservation Service NSF National Science Foundation NTAE non-traditional agricultural export crop NWO Nederlandse Organisatie voor Wetenschappelijk Onderzoek OAS Organization of American States OCPs organochloride pesticides OET Organización para Estudios Tropicales

OMZ Oxygen-Minimum Zone OSPAR Convention for the Protection of the Marine Environment of the North-East Atlantic OTS Organization for Tropical Studies PAR photosynthetically active radiation PBDE polybrominated diphenyl ether PCB polychlorinated biphenyl PdO Península de Osa PES payment for environmental services PET potential evapotranspiration ratio PILA Parque Internacional La Amistad PNC Parque Nacional Corcovado PNG Parque Nacional Guanacaste PNSR Parque Nacional Santa Rosa POPs persistent organic pollutants PPCPs pharmaceutical and personal care products PPFD photosynthetic photon flux density PPNG Proyecto Parque Nacional Guanacaste PPP public-private partnership PSA pago por servicios ambientales RAMSAR Convention on Wetlands of International Importance, especially as Waterfowl Habitat RARE Rare Animal Relief Effort RBA Reserva de la Biósfera La Amistad RBT Revista de Biología Tropical REA Rapid Ecological Assessment RECOPE Refinadora Costarricense de Petróleo REDD Reduced Emissions from Deforestation and forest Degradation RV Research Vessel SAR synthetic aperture radar SCP Site Conservation Plan SDGs Sustainable Development Goals SEC South Equatorial Current SEPSA Servicios Electricos Potosi S.A. SGS spatial genetic structure SI Smithsonian Institution SICA Sistema de la Integración Centroamericana SINAC Sistema Nacional de Áreas de Conservación SJLS San Juan - La Selva biological corridor SOC soil organic content SOM soil organic matter SPOT Satellite Pour l’Observation de la Terre SPN Servicio de Parques Nacionales SRP soluble reactive phosphorus SRTM Shuttle Radar Topography Mission SSC Species Survival Commission, IUCN STRI Smithsonian Tropical Research Institute TADS Tropical Amphibian Declines in Streams TEAM Tropical Ecology Assessment and Monitoring TM Thematic Mapper, Landsat TMCF Tropical Montane Cloud Forest TNC The Nature Conservancy TRF Tropical Rain Forest TSC Tropical Science Center TSOC total soil organic carbon UCP University of Chicago Press UCR Universidad de Costa Rica UFCO United Fruit Company UICN Unión Internacional para la Conservación de la Naturaleza UN United Nations UNA Universidad Nacional

Acronyms 725 UNAM Universidad Nacional Autónoma de México UNCED United Nations Conference on Environment and Development UNCLOS United Nations Convention on the Law of the Sea UNCSD United Nations Conference on Sustainable Development UNDP United Nations Development Programme UNED Universidad Estatal a Distancia UNEP United Nations Environment Programme UNESCO United Nations Educational, Scientific and Cultural Organization UNFCCC United Nations Framework Convention on Climate Change

USAID USDA USGS UT UTK UvA WCD WCS WMO WRI WUR WWF

United States Agency for International Development United States Department of Agriculture United States Geological Survey University of Texas University of Tennessee at Knoxville Universiteit van Amsterdam World Commission on Dams Wildlife Conservation Society World Meteorological Organization World Resources Institute Wageningen University and Research Centre World Wide Fund for Nature or World Wildlife Fund

Subject Index

Page numbers in italics refer to figures and tables. ACAT. See Área de Conservación ArenalTempisque (ACAT) Acevedo, H., 353 Acevedo-Gutiérrez, A., 169– 70, 223, 595 ACG. See Área de Conservación Guanacaste (ACG) ACLA-C. See Área de Conservation Amistad-Caribe (ACLA-C) ACLA-P. See Área de Conservación AmistadPacífico (ACLA-P) ACMIC. See Área de Conservación Marina Isla del Coco (ACMIC) ACOPAC. See Área de Conservación Pacífico Central (ACOPAC) ACOSA. See Área de Conservación Osa (ACOSA) Acosta, L., 352 Acueductos y Alcantarrillados, 639 Acuña, F. H., 606 Acuña-González, Jenaro, 596 Adams, P. A., 231 Adelson, G. S., 266 Agassiz, Alexander, 165, 177 Agrarian Development Institute (IDA), 365 agriculture agrarian reform and, 365, 370 alley cropping and, 85– 86 in cloud forests of volcanic Cordilleras, 443 crop insurance and, 68 deforestation and, 541, 541 in dry forest areas, 276, 277 fertilizer and, 68, 70– 71, 85 Green Revolution in, 564 land use conversion and, 646– 47, 647 new practices in, 87 nitrogen fixing and, 70– 71 organic inputs and, 85– 86 pesticides and, 563– 65 pollution and, 563– 65, 647, 677 sediment loads and, 602– 3 slash-and-burn, 68, 73, 84, 276 soils’ organic content and, 85 sustainability labeling and, 565 wetlands and, 699, 700 See also banana industry; soils of Costa Rica Aguado, M. T., 118 Agüero, J. M., 81, 86 Aguilar, G., 273 Aguilar, Reynaldo, 370 Albatross expeditions, 99, 116, 165, 167, 177, 231 727

Albornoz, L., 594 ALCOA (company), 371 Alfaro, Anastasio, 166, 195 Alfaro, E., 142, 596 Alfaro, J. P., 78 Alfaro, R., 249 Allan Hancock Foundation, 100, 123, 168 Allen, Paul, 7, 365, 373– 74 Almeda, F., 460 Almeida, R., 396 Altrichter, M., 197, 396 Alvarado, A., 68– 71, 78, 81, 86 Alvarado, G., 32, 201, 355, 456, 667 Alvarado, J. J., 102, 122, 123, 594, 608 Alvarado García, Joaquín, 180, 184 Álvarez, M. D., 271 Álvarez-Ruiz, M., 594 AMBICOR (NGO), 403 Anderson, James J., 100 Anderson, R. C., 223 Anderson, R. S., 231 Angulo, A., 171 Apsit, V. J., 272– 73 Arauz, Randall, 170 Araya, L. M., 78 Ardón, Marcelo, 638, 639 Área de Conservación Amistad-Pacífico (ACLA-P), 9, 460, 461 Área de Conservación Arenal-Tempisque (ACAT), 443 Área de Conservación Guanacaste (ACG), 297– 98, 299, 301, 306, 308, 315– 16, 323– 24 academic study of, 339 agriculture in, 303, 304 All Taxa Biodiversity Inventory (ATBI) for, 250 biodiversity in, 250, 292– 93, 297– 98, 304, 319– 22, 331, 335– 36, 711 birds of, 265 climate change and, 293– 94, 320– 22, 320– 21 climate in, 311, 313– 15, 317, 319– 322, 329 conservation fund for, 281 creation of national park in, 305– 6 deforestation in, 298, 300, 303, 305 disappearance of megafauna in, 293– 94 distorted population dynamics in, 337– 38 ecological succession in, 337– 39 environmental education and, 336

Europeans’ arrival in, 294, 296– 97 even-aged forest in, 296 expropriation of land for, 335 fire control as conservation strategy in, 332, 334 first humans and their impact in, 293– 95 floristic composition in the Península de Nicoya and, 277, 279 forest and grassland fires in, 296, 299, 300, 303, 307, 308, 312– 14 four primary ecosystems of, 292 geology of, 251, 290– 93, 320 growth of, 281 human impact on, 331, 335, 337– 38 hurricanes and, 314– 15 indigenous people’s use of fire in, 300 insect species composition in, 315 invasive species in, 335– 36 jaguars in, 262 landscape-level restoration in, 297– 98 life zones of, 252 livestock raising in, 300, 302, 304 mammals in, 277 maps of, 291, 292, 294– 95, 326 meteor impact in, 293 as model for Área de Conservación Osa (ACOSA), 369 moving threatened species to new locations and, 322 as national monument and national park, 311 national parks and protected areas within, 279, 280 old-growth forest in, 297 Oliver North’s airstrip in, 297 parasitism in, 275 pasture in, 309– 10 petroglyphs in, 298 plant-animal interactions and, 328– 31 plant community distribution and, 254 plant reproduction seasonality in, 328– 31 Pleistocene anachronisms in, 293 poor soils in, 331, 334, 335 prehistoric megafauna in, 305, 333, 337 proposals for expansion of, 322 protection and restoration of marine portion of, 335 purchase of land for inclusion in, 336– 37 reasons for creation of predecessor park and, 331 reforestation in, 303, 305 research sites and, xix

728 Subject Index Área de Conservación Guanacaste (continued) social proximity to centers of power and, 304, 331 species surviving meteor hit and, 290 thermal equator and, 311 tourism and, 304 trade winds and, 293 travel routes through, 304, 305 tree species composition in, 315 wood harvesting in, 296 as World Heritage site, 280 See also dry forests; Proyecto Parque Nacional Guanacaste (PPNG) Área de Conservación Marina Isla del Coco (ACMIC), 162, 182, 193, 237 Área de Conservación Osa (ACOSA) biodiversity in, 374 climate types in, 372 community involvement in master plan for, 371 configuration and agenda of, 369– 70 conservation work in, 395, 402 endemism in, 388, 391 funding for research in, 369 geology of, 372– 73 herpetofauna of, 391 human impact on, 361 landforms in, 373 mapping of, 9 mapping of ecosystems in, 376 Osa community and, 370 park fees in, 402– 3 protected areas in, 403, 713 scarlet macaws in, 393, 401– 2 soils of, 373 study of tent-making bats in, 394– 95 tourism in, 403 Área de Conservación Pacífico Central (ACOPAC), 9, 347, 402, 712 Área de Conservación Tempisque (ACT), 264, 277, 280, 281 Área de Conservation Amistad-Caribe (ACLA-C), 481 Área de Conservation Amistad-Pacífico (ACLA-P), 481, 482 Arias, C., 148 Arias Sánchez, Oscar, 4 Arroyo Mora, J. P., 279, 542– 43 Arroyo Mora, P., 277 ASEDER. See Entrepreneur Association for Responsible Development (ASEDER) Asociación MarViva, 180 Asociación Mono Tití (ASOMOTI), 403 Atkin, L., 77 Atlantic lowlands biodiversity in, 387 fauna of, 387, 389– 90, 390, 392, 394– 400 vegetation of, 347, 390 AVINA Foundation, 371 Azofeifa-Solano, J. C., 594 Baert, L., 231 Bakus, G. J., 107, 169, 173– 74

Ball, B., 153 banana industry in Caribbean lowlands, 563 habitat destruction and, 567 in Osa region, 364– 65, 371 pesticide use and, 564– 65, 677 Banks, N., 231 Banta, William C., 100, 591 Barbee, N. C., 635 Barclay, George W., 209 Barnens Regnskog, 443 Barrantes, G., 224, 363 Barrantes-Rojas, N., 604 Barrientos, Z., 511 Barry, R., 20 Bartels, C., 148, 149 Bartsch, P., 168 Bawa, K. S., 271, 272 Beard, J. S., 8 Beaudette Foundation, 100 Beebe, William, 100, 123, 168 Belcher, Edward, 194, 209 Bellamy, C. L., 231 Bellefleur, P., 474– 75 Benavides-Morera, R., 595 Bennett, H. H., 64 Bentham, G., 209 Benumof, B. J., 206 Bergoeing, J. P., 202, 656 Bernecker, A., 208, 211 Berry, William, 52 Bertsch, F., 86 Bianchi, G., 118 Bickel, D. J., 231 Bigelow, H. B., 168 biodiversity All Taxa Biodiversity Inventory (ATBI) and, 250 alpha, beta, and gamma levels of, 6– 7, 709 in Área de Conservación Guanacaste (ACG), 292– 93, 304, 319– 22, 331, 335– 36, 711 in Área de Conservación Osa (ACOSA), 374 in Área de Conservación Pacífico Central (ACOPAC), 712 in Atlantic versus Pacific lowlands, 387, 387 biased collection efforts and, 539 biological corridors and, 567 Caribbean coastal and marine ecosystems and, 595 Central American land bridge and, 5 in Central Pacific region, 346, 347, 352– 56 climate change and, 28 in cloud forests, 428– 29, 433– 35, 453, 457– 69, 718– 19 Convention on Biological Diversity (CBD) and, 482 Costa Rica’s innovations in preservation of, 4 definitions of, 7 deforestation and, 3

degree of in Costa Rica, 5– 6 in dry forests, 250, 276– 77, 309, 711, 712– 13 at ecosystem level, 6– 7 endemism and, 6 of fish in Caribbean lowlands, 546 Great American Biotic Interchange (GABI) and, 5, 457, 531 in growth forms, 431– 32 habitat loss and, 467 hours of sunlight and solar radiation and, 21 human impact on coral reefs and, 178– 79 illegal fishing and, 236 improving inventories of, 5, 8– 9 information about large versus small organisms and, 627 invasive species and, 336 Isla del Coco and, 169, 171– 72, 194– 95, 200, 236– 38 livestock raising and, 302, 303 mangrove ecosystems and, 108 in marshes, 692– 93 megadiverse countries and, 6 Mesoamerican biodiversity hotspot and, 499, 716 1999 Biodiversity Law and, 701 of oceanic and costal-marine ecosystems, 709, 710 of oceanic islands, 192– 93 in Osa region, 361, 373– 75, 387, 392, 394 in Oxygen-Minimum Zones, 118 on Pacific coast, 119 in palm swamps, 694– 95 in the páramos, 509– 14, 510, 720 in Parque Nacional Santa Rosa, 254 political and legal frameworks supporting, xvii as priceless, 3 progress on in Costa Rica, xvii in rain forests, 714– 16 of rivers of Costa Rica, 626– 27, 630, 633 software programs for study of, 546 Sørenson Index and, 387 in South Pacific region, 347 Stockholm Environment Institute on, xv Sustainable Development Goals (SDGs) and, xv– xvi Taxonomic Impediment and, 5 threats to, 6 in wet forests of the Caribbean lowlands, 539– 40, 550– 53, 555– 56, 561 in wetlands, 692– 93, 694– 95, 721– 22 Biodiversity Support Program, 193 biofuels, 336– 37 Biolley, Paul, 167 Birkeland, Charles, 100 Bishop Museum, 169, 227 Bjarte, H. J., 229 Blair, N., 608 Blake, J. G., 561 Blanco, M. A., 211 Blaser, H., 81

Subject Index 729 Blaser, J., 475 Blauvelt, Abraham, 563 Blessing Presinger, Augustín, 497 Bogantes-Aguilar, Victoria, 595 Bogarín, D., 211 bogs, marshes, and swamps agriculture and, 699 biodiversity in, 692– 93, 694– 95, 721– 22 conservation efforts and, 699– 701 definition of wetlands and, 701 degradation and restoration of, 701– 2 disconnection of from watersheds and, 700 ecological services provided by, 700 endangered and threatened species in, 692– 93 extent of, 683 fauna of the marshes and, 691– 93, 693 fire and, 721 fish communities in, 692 flora of the marshes and, 687, 687– 692, 689– 691 forest swamps and, 696– 99, 697– 98 highland bogs and, 684– 87, 685– 86 human disturbance of, 686, 690– 91, 700 interconnectivity of, 699– 700 invasive species in, 692 loss of wetlands and, 683– 84 map of, 684 in Osa region, 376, 377 palm swamps and, 694– 96, 694– 95 Palo Verde marshes and, 701– 2 Ramsar Convention on Wetlands of International Importance and, 686 research on, 683 rice cultivation and, 700 sugarcane cultivation and, 700 threats to, 686– 87, 699– 701 topographical variations in, 690 water flow and quality and, 699– 700 wetlands ecosystems and, 720– 22 Boinski, S., 399 Bolaños, F., 356 Bolaños, J., 79 Bolaños, Natalie, 594 Bolaños, Rafael Angel, 8 Bonito, Benito “Bloody Sword,” 162 Boone, Lee, 168 Bosque Nacional Diriá, 267, 280 Bosque Puerto Carrillo, 279 Bourillon, Roger, 247 Bowman, T. E., 604 Boza, Mario, 305, 367, 566 Brak, B., 513, 685 Brandes, C., 597 Braun-Blanquet, J., 8, 9, 512 Breedy, O., 102, 118 Breedy, Odalisca, 594 Brenes, C., 207– 8, 595 Brenes, L. G., 656 Bright, D. E., 231 Brinkman, M., 52 Broadbent, E. N., 358 Broenkow, W. W., 100

Brölemann, E. W., 235 Brooks, D. R., 269 Browman, H. L., 156 Brown, J. W., 230, 231 Brown, S., 473 Bruce, Niel L., 594 Brugnoli-Oliveira, E., 148 Bruijnzeel, L. A., 422– 23 Brusca, Richard C., 594 Bumby, M. J., 656 Bundschuh, J., 32 Burcham, J., 627 Burkenroad, M. D., 168 Burlingame, L. J., 443 Burnham, R. J., 254 Buskirk, R., 463 Buskirk, W., 463 Bussing, W. A. on fish communities at La Selva Biological Station, 627 fish of Caribbean coast and, 595 fish of Caribbean lowlands and, 549 Isla del Coco and, 169, 171, 219– 20 specimen collection and, 116 Buurman, P., 83 Byers, G. W., 231 Cabalceta, G., 83 Cabeças de Grado, Joan, 162 Cahoon, L. B., 143 Cajiao-Jiménez, M. V., 122 Calderón, R., 10 California Academy of Sciences, 100, 167– 68 California Current, 200 California Gold Rush (1848), 298 Calvert, Amelia, 360 Calvert, Philip, 360 Calvo, J., 543 Camacho, M., 81, 474– 75 Camacho-García, Yolanda, 594 Campos, J., 149, 151– 52, 153, 154 Carazo Odio, Rodrigo, 164 carbon cycle. See climate change carbon sequestration, 81, 85, 109 Caribbean coastal and marine ecosystems beaches and, 600– 601, 601 biodiversity in, 595 bottom profile of, 103 climate and weather and, 596, 597 climate change and, 606 coastal lagoons and, 598, 599 conservation efforts in, 606, 608– 9, 610 coral reefs of, 593, 602– 3 crustaceans and, 594 current state of knowledge on, 596– 97 declining fish populations and, 606 dolphin studies and, 595 echinoderms of, 594 Economic Exclusive Zone (EEZ) of, 591 El Niño– Southern Oscillation (ENSO) warming events and, 604– 5 fish studies and, 595 future of, 609– 10

geography of, 591 geology and geomorphology of, 596, 597– 98, 598, 601 history of, 591– 96 human population and demography and, 604 Isla Uvita and, 603– 4, 606, 608 Limón earthquake (1991) and, 593 manatee studies and, 595 mangrove forests and, 599– 600 maps of, 592 mass mortality of organisms in, 593, 595, 601, 602, 604– 5 open waters and, 604 versus Pacific coast, 97 pollution and, 595– 97, 606 protected areas and, 593, 606, 608 research expeditions and, 592– 93 research needs in, 609– 10 rocky intertidal zone and, 601, 602 seagrass beds in, 111, 601– 2 summary of oceanic and coastal-marine ecosystems and, 709– 10 threats to, 602– 3, 604– 6, 605, 607 waves, tides, and water circulation in, 598 See also wet forests of Caribbean lowlands Caribbean Coastal Marine Productivity (CARICOMP) protocol, 599– 600, 602, 603, 609 Caribbean Conservation Corporation (CCC), 567, 608 Caribbean lowlands. See wet forests of Caribbean lowlands Caribbean region, as Biodiversity Superpower, xvi CARICOMP protocol. See Caribbean Coastal Marine Productivity (CARICOMP) protocol CARIPOL. See Marine Pollution Monitoring Program in the Caribbean (CARIPOL) Carr, Archie, 566, 591 Carr, Archie, III, 567 Carrillo, Eduardo, 395, 396, 398– 99 Carrillo-Baltodano, Allan, 595 Carson, Renate J. M., 591 CARTA Project, 257 Cascante, A., 350 Castillo, M., 352 Castillo, P., 172, 201, 203, 205 Castro, R., 28 Castro Campos, Marco V., 8 CATIE (Centro Agronómico Tropical de Investigación y Enseñanza). See Tropical Agricultural Research and Higher Education Center (CATIE) Celis, R., 345 CENAT, 257 Central America biogeographic history of, 5 Central American Floristic Province and, 457 closing of the isthmus and, 5, 55, 97, 290– 91, 391, 416, 529– 32

730 Subject Index Central America (continued) Great American Biotic Interchange (GABI) and, 5, 457 isthmian and Andean mountain ranges and, 500 routes across the isthmus and, 298, 300 transisthmian sister species and, 97 Central Pacific region aquatic habitats in, 349, 349, 354 biodiversity in, 346, 347, 352, 353, 354– 56 birds in, 355– 56 climate of, 345 closing of the isthmus and, 503 conservation efforts in, 357– 58 deforestation in, 351, 357 endangered and newly discovered tree species in, 353 endangered species in, 355 endemism in, 345– 46, 348, 350, 355, 356 extent of Central Valley in, 351 fungal diversity in, 354 geography of, 345– 46 geology of, 351 herpetofauna in, 356– 57 human impact on, 357– 58 mammals in, 354– 55 northern distribution limit for some trees in, 349 property development in, 357– 58 protected areas in, 345, 346 river gorge in, 352 savannahs in, 350, 351 species new to science in, 349, 350 tourism in, 357– 58 vegetation of, 347– 353 Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) contributions to riverine research and, 623 development of marine science in Costa Rica and, 100– 101 echinoderm studies and, 594 ecoregional assessment and, 181 Isla del Coco studies and, 171, 172, 175– 76 limnological studies and, 656– 57 marine pollution studies and, 595– 96 Chacón, Didiher, 594, 595 Chacón, Isidro, 546 Chandler, M., 634 Charpentier, Claudia, 593 Chassot, Olivier, 568 Chavarría, U., 257 Chaverri, A., 247, 461, 498– 99, 508, 513, 515 Chávez, L., 663 Cheek, A. O., 155 Chemsak, J. A., 231 Chevalier-Skolnikoff, S., 263– 64 Child, Allan, 100 Choe, J. C., 231 Chorley, R., 20 Choudhury, A., 269 Chubb, L. J., 206

CIMAR. See Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) CITES. See Convention on International Trade of Endangered Species (CITES) Clark, K. L., 422, 668 Clark, L. G., 512 classification systems biotic units and, 8 climate and, 25, 26 Costa Rican ecoregions and, 10 DNA barcoding and, 270 for Isla del Coco vegetation, 211, 213 Luis Diego Gómez’s work and, 8, 9 taxonomy of fish communities and, 550 UNESCO’s vegetation classification system and, 9, 377 volume editor’s choice of, 10 World Wildlife Fund (WWF) and, 250 Cleef, A. M., 499, 508, 512, 513 Cleveland, C. C., 84 climate and weather altitudinal variable and, 536 in Área de Conservación Guanacaste (ACG), 317, 319– 322, 320– 21, 329 on Caribbean coast, 596, 597 climate regions and, 23– 27 in cloud forests, 420– 24, 421– 22, 454– 55, 716 in dry forests, 311, 313– 15, 711 in dry lowlands, 267 El Niño effect and, 102, 104 Föhn effect and, 27 Gulf Stream and, 529 Hadley Cell and, 197 hours of sunlight and solar radiation and, 21, 22 hydric balance and, 23, 23– 27 Intertropical Convergence Zone (ITCZ) and, 173, 197– 99, 198, 420, 503, 535 Isla del Coco and, 197– 99 lake temperatures and, 672– 73, 674– 75 lake turnover and, 667, 674– 75 latitudinal position and, 19– 20 meteorological monitoring and, 422– 23, 425– 26, 535– 36 orography and, 19 of Osa region, 372 of Pacific coast, 104 in páramos, 500, 502– 3 in Pleistocene and Holocene Eras, 529– 30, 532, 533 precipitation and, 21– 22, 22 production of higher trophic levels and, 639 relative humidity and, 22– 23, 23 rivers of Costa Rica and, 622 temperature and, 21, 21 temporal and spatial variations in, 21– 23 temporales del norte and, 442 tourism and, 182 wet forests of Caribbean lowlands and, 534– 37, 535 See also climate change; El Niño events

climate change altitudinal distributions of arthropods and, 433– 34 Área de Conservación Guanacaste (ACG) and, 293, 320– 22, 336 biodiversity and, 28 carbon dioxide neutrality and, 4 Caribbean coastal and marine ecosystems and, 606 changing equilibrium states and, 334 cloud forests of the Talamanca and, 480 Costa Rican ecosystems and, 27– 29 dormancy of moths and butterflies and, 314 effects of on dry forests, 310 fossil evidence of past change and, 27– 28 on geological time scale, 536 highland bogs and, 686 interruption and calendar-shifting of seasonal events and, 330– 31 Isla del Coco and, 178, 199 lake ecosystems and, 678 mangrove ecosystems and, 109 mitigation of, 28– 29 Pacific coastal waters and, 121 on Pacific versus Atlantic slope, 480 páramos and, 506, 515 plant reproductive seasonality and, 328 during Pleistocene and Holocene, 53 rain forest restoration and, 335 seagrass beds ecosystems and, 111 stabilization of greenhouse gas concentrations and, 8 Stockholm Environment Institute on, xv Sustainable Development Goals (SDGs) and, xv– xvi thermoconforming animals and, 552 wet forests of Caribbean lowlands and, 536– 37 See also climate and weather Cline, Joel D., 100 Cloern, J. E., 142 cloud forests, 717 biodiversity in, 718– 19 comparative study of, 457 deforestation and restoration in, 717– 18 forest invasion and restoration and, 334 lakes in, 664– 70 in Osa region, 376, 377 seed dispersal in, 718 summary of ecosystem, 716– 19 See also cloud forests of the Talamanca; cloud forests of the volcanic Cordilleras cloud forests of the Talamanca, 453, 455 agro-ecological zonation in, 477– 78, 479 altitudinal zonation in, 479 amphibians in, 463– 64 biodiversity in, 453, 457– 467 biological corridors in, 482– 83 birds in, 465– 66 bryophytes in oak forests and, 462– 63 climate of, 454– 55

Subject Index 731 ecosystem functioning and dynamics in, 473– 77 emerging environmental threats in, 479– 80 endangered and threatened species in, 482 endemism in, 453, 461 environmental recovery in, 475– 77 epiphytes in, 461– 62 ethnobotany in, 479 fishes in, 463 forest structure in, 473 forest succession in, 474, 475, 476– 77 fungi in, 458 future of, 482– 83 geology and geomorphology of, 453, 455– 56 history of scientific exploration in, 453– 54 human settlement in, 477– 78 Inter-American Highway and, 477, 479– 80, 480 leaf characteristics in, 473– 74 lichens in, 458– 60 mammals in, 466– 67 map of, 452 plants of, 457– 58, 460– 63, 468– 69 public protected areas in, 480– 82 rainfall, mist, and clouds in, 475 Ramsar Wetland of International Importance in, 481– 82 reforestation in, 478– 79 reptiles in, 464– 65 rivers of, 456 seed predation in, 471, 472– 73 societal uses of water from, 452– 53 soils of, 456– 57 species interactions and, 469, 471– 73 successional stages of, 474 tourism in, 477, 478 vascular parasites in, 462 vegetation zones in, 467– 68 water and nutrient cycles and, 475– 76 See also cloud forests; cloud forests of the volcanic Cordilleras cloud forests of the volcanic Cordilleras above-canopy photosynthetic photon flux densities in, 426 above-canopy shortwave radiation in, 426 amphibians and reptiles in, 434– 35 arthropods in, 433 biodiversity in, 428, 429, 431– 32, 433, 434, 435 birds in, 435– 37 canopy structure and treefall gaps in, 424, 429, 442 climate of, 420– 24, 421 conservation in, 443– 44 distinctive habitats in, 428– 29 endemism in, 437 forest light regime in, 474– 75 forest profiles of, 430– 31 growth form diversity in, 431– 32 history of land use in, 443 Holdridge Life Zones in, 428 hunting and land use changes in, 437

hydrology of, 424– 26, 425– 27, 428 landslides in, 442 light in, 424 versus lowland forests, 433 mammals in, 437 map of, 416 modern geography of, 418– 19 Monteverde Flora Project in, 429, 431 nutrient cycling in, 440– 41, 441 people and nature in, 442– 44 phenology of vegetation in, 432– 33 physiography of, 419 plants and vegetation of, 428– 433 protected areas in, 416 rainfall, mist, and clouds in, 422– 24, 424, 425, 425– 26, 440– 41, 441 research and conservation in, 415 satellite image of canopy in, 429 soils in, 419– 20 species interactions in, 437– 40 tectonic history of, 415– 18 temperature changes and, 434 trophic structure and energy flow in, 441 water cycle in, 420– 21 wind in, 421– 23, 421– 22, 425 See also cloud forests; cloud forests of the Talamanca Coan, E. V., 168 Coates, A. G., 5 Cocos Anticyclonic Eddy, 200 coffee industry, 621 Cole, M. C., 431 Colnett, James, 194, 225, 226 Colombia Current, 200 Columbus, Christopher, 3, 534, 603– 4 Colwell, Rob, 546 CONARE. See Consejo Nacional de Rectores (CONARE) Conquest, L., 156 Consejo Nacional de Rectores (CONARE), 171, 172, 182 conservation biofuels as threat to, 336 biological corridors and, 357, 400, 482– 83, 537, 545, 556, 566– 69 in bogs, marshes, and swamps, 699– 701 Caribbean coastal and marine ecosystems and, 606, 608– 9 in cloud forests of volcanic Cordilleros, 443– 44 conflict over, 400– 404 conservation organizations and, 122, 180 Costa Rica’s innovations in, 4 crocodile populations and, 552 debt for nature swaps and, 279 definition of wetlands and, 701 versus development, 281 dry forests and, 279, 331– 33, 334 Eastern Pacific Marine Corridor Initiative and, 181 ecological restoration and, 122 ecosystem approach and, 322 elevational transects and, 556

endangered species and support for, 395, 398 environmental laws and, 700– 701 factors motivating conservation efforts and, 566 funding for, 402– 4 gap analysis and, 8, 9 green turtles and, 566– 67 highland bogs and, 686 image versus reality of in Costa Rica, 565– 66 importance of nonthreatened plants and animals in, 332 Important Areas for Bird Conservation and, 218 Isla del Coco and, 180– 82, 236– 38 laboratory cultivation and, 152– 53 legislation and, 122 lists of endangered and threatened species and, 482 local interventions to strengthen, 281 local people’s involvement in, 608– 9, 610 management of, 608– 9, 610, 649 mangrove ecosystems and, 109 Marine Protected Areas (MPAs) and, 122, 123, 156 NGOs and, 402– 4 Noah’s Ark efforts and, 322, 336 no-take versus protected areas and, 179 paper parks and, 122 protected areas and, 4, 8, 9, 121– 22, 180 protests against water concessions and, 648 radio collars and, 398 Ramsar Convention on Wetlands of International Importance and, 686 scarlet macaws and, 401– 2 status assessment and, 400 structural drivers of, 280 sustainable forestry and, 370– 71 threat abatement and, 122 tourism and, 402– 4, 568– 69 UN conventions on, 122 valuation of and payment for ecological services and, 122– 23, 182, 277, 280, 542– 43, 608 in wet forests of the Caribbean lowlands, 565– 69 wetland protection and, 699– 701 white-lipped peccaries and, 400– 401 Conservation International (CI), 181, 608 Conservation Strategy Fund, 646 Convention for the Protection of the Marine Environment of the North-East Atlantic (OSPAR Convention), 116 Convention on Biological Diversity (CBD), 10, 482 Convention on International Trade of Endangered Species (CITES), 276, 482, 567, 608 Coolidge, K. R., 231 Córdoba-Muñoz, R., 142 corporate social responsibility (CSR), xvii

732 Subject Index Corrales, A., 149 Corredor Biológico Mesoamericano (CBM), 482 Cortés, J. coral reef ecosystems and, 111– 12 Costa Rica’s coastal-marine ecosystems and, 10, 98 crustacean studies and, 594 Isla del Coco ecosystems and, 174 Isla Uvita and, 604, 605 lists of mollusks and, 153 on mangrove systems, 143 marine biodiversity studies and, 595 rocky intertidal ecosystems and, 107 synthesis of marine research and, 102 Costa Rica beaches of, 41 biogeographic history of, 5 biological richness of, 3 biotic units of, 8, 19 cattle boom and end of cattle industry in, 304– 5 climate and latitudinal position of, 19– 20 climate and orography of, 19, 30 climate regions of, 23– 27, 30 deforestation rates throughout, 541, 542 degree of biodiversity in, 5– 6 Economic Exclusive Zones (EEZ) of, 98, 121, 170, 178 ecosystems of, 6– 11, 27– 29 endemicity of species in, 6 environmental publications on, xix– xx as first carbon dioxide– neutral country, 4 five terrestrial ecoregions of, 10 geographical coordinates of, 19 government departments responsible for environmental management in, 4 as Green Republic, xv growing environmental awareness in, 569 image versus reality of conservation in, 565– 66 increasing impact on ecosystems in, xvii independence from Spain, 162 indigenous people of, 532– 33, 534 integrated environmental management in, xvii– xviii as laboratory, 30 land area of, 19 life zones of, 7– 8 marine versus land territory of, 6 as most species-dense country on Earth, 709 name of, 3 National Herbarium of, 497 Pacific versus Caribbean coast of, 6 paleographic reconstruction of, 54 political history of, 300 population of, 563 progress in conservation in, xvii as regional leader in hydropower, 640 tectonics of, 31– 32 temporal and spatial climate variations in, 21– 23 threats to environment of, 3– 4, 6

three terrestrial biomes of, 10 wetland systems in, 9– 10 Costa Rican Coastal Current, 199– 200 Costa Rican Dome, 199 Costa Rican Electricity Institute (ICE), 21 Costa Rican Fisheries Institute (INCOPESCA), 608 Costa Rican Institute of Tourism (ICT), 156 Costa Rican port authority, 156 Cousteau, Jean Jacques, 164 Cousteau, Philippe, 164 Cowardin, L. M., 9 Crisp, D. J., 107 Crocker, Templeton, 100 Cromwell Current, 199 Crossland, Cyril, 168 Crow, G. E., 257 Cuming, Hugh, 98 Cutler, N., 146 Cwikla, P. S., 231 Dall, W. H., 177 Dampier, William, 162 Daniels, J. D., 431 Darwin, Charles, 112, 222, 224, 226, 230 Dauphin, G., 211, 256 Davidse, Gerrit, 498 Davies, Edward, 162 Davis, D. R., 231 Dawson, C. E., 100 Dawson, Elmer Yale, 100, 101, 102, 591 Dean, H. K., 110, 144, 146 deforestation for agriculture, 303– 4, 354, 541, 541 in Área de Conservación Guanacaste (ACG), 298, 300, 303– 4, 305 biodiversity loss and, 3 birds and, 265 for cattle ranching, 354 in Central Pacific region, 357 in Central Valley, 351 cloud forests and, 717– 18 Costa Rica’s Grand Contradiction and, 4 degree of in Costa Rica, 4 dry forests and, 248, 276– 77, 300, 711 end of northern migration of herpetofauna and, 392 extinctions and, 718 Gulf of Nicoya ecosystem and, 139 historical land use and, 622 howler monkeys and, 264 human settlement in the cloud forests of the Talamancas and, 477 Isla del Coco and, 196, 218 for livestock raising, 300 loss of ecological services and, 718 measurement of forest loss and, 541– 42 migrating birds and, 435 multiple causes of, 308, 309 in Parque Nacional Santa Rosa, 307 rate of in Costa Rica, 345, 541, 542, 622– 23 reversal of, 4– 5

sediment loads and, 602– 3 selective logging and, 542 slash-and-burn practices and, 276 small- versus large-scale, 541 soil erosion and, 622 soil organic content and, 84 timber industry and, 305 in wet forests of the Caribbean lowlands, 541– 42 de Goeris, Luis, 226 Delaney, P. M., 594 Denevan, W. M., 534 Denyer, P., 39– 40, 597 Desliens, Nicolas, 162 DeVries, P., 270, 386, 546 Dexter, D. M., 100, 105, 145, 592, 601 Díaz-Fergusson, E., 105, 146 Dinerstein, E., 452– 53 Dittel, A. I., 146, 147, 594 Dittmann, S., 110, 145 Dodge, B. W., 591 Dodge, C. W., 591 Dohrenbusch, A., 422 Dominici-Arosemena, A., 595 Drewe, K. E., 635– 36 dry forests, 251, 253, 255 abandonment of agricultural lands and, 267 apparently evergreen trees in, 333 in Área de Conservación Guanacaste (ACG), 300, 303, 308– 11, 315– 16, 322 bees, wasps, and ants in, 271 biodiversity in, 250, 276– 77, 309, 711, 712– 13 biological corridors and, 280– 81 birds of, 265– 67 burning of pastures in, 255 climate and weather and, 250, 267, 271, 311, 313– 15 climate change and, 310 conservation, management, and sustainability in, 279 defining, 308– 11 defoliation by insects in, 273, 330– 31 deforestation and, 248, 276– 77, 711 disappearance of, 247– 48, 249– 250 dry season in, 267 as ecoregion, 10 edge effect with rain forests and, 319– 20 environmental stresses and, 276 epiphytism in, 275 floristic composition of, 254– 56, 260, 277, 279 flowering, pollination, and breeding patterns in, 271– 73 forest cover in, 277, 278, 279 forest fires and, 248– 49, 273, 276 forest islands and, 309, 310 forest structure and, 252– 54 fragmentation and restoration of, 331– 37 freshwater fishes in, 268– 69 freshwater shrimps in, 271

Subject Index 733 geology, geomorphology, and soils of, 250– 52 herbivory and frugivory in, 273– 74 human impact on, 337– 38 hunting in, 276– 77 insects in, 269– 71 invasion of pastures by, 332– 33, 334 lakes of, 659– 61, 663 land use history of, 276, 277 life zones of, 252 mammals in, 262 versus moist forests, 250 old-growth ecosystems and, 337 parasitism in, 275– 76 in Parque Nacional Palo Verde, 252 pasture and, 248 plant-animal mutualism in, 274 poor scientific understanding of, 309– 10 property development and, 276, 279 protected areas and, 249 protected areas of dry lowlands and, 249 versus rain forests, 311 reforestation in, 248, 277, 279– 80 reptiles and amphibians in, 267– 68 restoration of, 309– 10, 712– 13 seasonality in, 267, 310– 11, 322– 31, 323– 24 secondary forest and, 261 seed dispersal in, 273– 74, 471 soils and, 252, 254 spatial genetic structure of trees in, 273 species interactions in, 271– 76 summary of ecosystem, 711– 13 threats to, 712 types of trees and, 252– 53 vegetation and flora and, 252 vigor of seedlings in, 273 vulnerability of versus cloud and rain forests, 309 of the Western Hemisphere, 247 Dudzik, K. J., 223 Duff, J. M., 637 Duran, F., 355 Durham, J. W., 168 Dutch Agency for International Cooperation (DGIS), 513 Earle, Sylvia, 123 EARTH College, 623 earthquakes coastal subsidence and, 364 frequency of in Osa region, 372 1991 Limón Earthquake and, 49, 593, 597, 598, 601, 602, 605– 6, 710 recent treefalls and landslips in Osa region and, 379 routes across Central America and, 298 sea levels and, 598 2009 earthquake in Caribbean lowlands and, 550 Earth Summit (United Nations Conference on Environment and Development, Rio de Janeiro, 1992), xv

EARTH University, 563, 565 Eastern Pacific Marine Corridor Initiative, 181 Eberhard, G. W., 231 Echeverría-Sáenz, S., 153– 54 ecological services bogs, marshes, and swamps and, 700 deforestation and, 718 ecosystem management and, 156 mangrove forests and, 108– 9 marshes and, 700 valuation of and payment for, 122– 23, 182, 277, 280, 542– 43, 608 ecology, fundamentals of, 10 ECOMAPAS Project, 9 Economic Exclusive Zones, 98, 121, 170, 178, 591 ecosystems anthropic biomes and, 13 benthic, 145 biodiversity at ecosystem level and, 6– 7 classifications of in Costa Rica, 7– 10 climate change and, 27– 29 communities within, 143 definitions of, 10, 143 ecosystem concept in this volume and, 10, 13 ecosystem goods and services and, 156 life zones and, 7– 8 mapping of, 9 need for ecosystem-based management and, 156 oceanic and coastal-marine, 709– 11 in organization of this volume, 13 photographs of, 12 structure of this volume and, 11, 13 See also specific ecosystems Edgar, G. J., 179 Edwards-Widmer, Y., 469, 473 Elizondo, L. H., 345– 46, 350 Ellenberg, H., 9 El Niño events climate change and, 121 coral reefs and, 113, 114, 120, 171, 593, 604– 5, 710 crustaceans and, 111 drought and, 23, 26, 27 Gulf of Nicoya ecosystem and, 148 Isla del Coco and, 199– 200 lake water temperatures and, 672– 73 ocean temperatures and, 2, 104, 219 species composition and, 102 stream phosphorus levels and, 637 threats to Pacific coast environment and, 120– 21 treefall activity and, 379– 80 tree flowering in 1998 and, 271 Emery, C., 228 endangered and threatened species coral reefs and, 109 deforestation and, 718 lists of, 396, 482, 608 mangrove forests and, 109

in marshes, 692– 93 moving up and out of sight, 333 support for conservation work and, 395, 398 threats to cichlids and, 628 Enquist, C. A. F., 27– 28 Enrique II, 162 Entrepreneur Association for Responsible Development (ASEDER), 371 environmental education, 336 environmental laws, 4, 9, 700, 701 Epifanio, C. E., 142, 147 Epler, B. C., 194 equator, thermal, 311, 313, 314, 319 Equatorial Current of the South, 199– 200 Espinosa, José, 594 Espinoza Mendiola, M., 149 Esquivel, A., 78 Esquivel, O., 515 Estero Real– Tempisque Freshwater Ecoregion, 268 Estrada, A., 260, 348, 350, 353– 54, 468 estuaries, 150– 51, 151 Ewel, J., 77, 366– 67, 371 FAICO. See Foundation of Friends of Isla del Coco (FAICO) Faxon, W., 177 Fernández, C., 116 Fernández, Juan Mercedes, 363 Fernández, W., 596 Fernández-Alamo, M. A., 100 Fernández de Oviedo, Gonzalo, 101, 151 Ferrari, F. D., 604 Fertilizantes de Centroamérica (Costa Rica) S.A. (FERTICA), 64 Feutry, O., 102, 109 FFEM. See French Fund for the World Environment (FFEM) fire. See forest and grassland fires Fischer, S., 146 Fisher, A. K., 168 Fisheries and Aquaculture Institute, 156 fishing and fisheries, 182 along rivers, 451, 640 artisanal, 152 ban on catching turtles and, 566 commons and, 139 fishery potential and, 153 fish farms and, 648– 49 fishing lines collected by national park personnel and, 183 human impact on Isla del Coco and, 178 illegal, 182, 236, 699 management strategies and, 152– 53, 156 Maximum Sustainable Yield and, 153 modified circle hooks and, 116 no-take versus protected areas and, 179 overfishing and, 148– 49, 151– 54, 151, 171 Pacific coast’s human population and, 120 restriction of access to fishing boats and, 180– 81, 182

734 Subject Index fishing and fisheries (continued) restriction of in Área de Conservación Guanacaste (ACG), 335 war’s displacement of, 335 in wet forests of the Caribbean lowlands, 550 wetland habitat loss and, 700 Foerster, C., 395, 398 Fogden, M. P. L., 434 Föhn effect, 27 Fonseca, A. C., 103 Forel, A., 228 forest and grassland fires, 312 in Área de Conservación Guanacaste (ACG), 296, 299, 300, 303, 307, 308, 312– 14 clearing for agriculture and, 303 in consecutive years, 334 in dry forest areas, 276 fire control and, 280, 306, 307, 332– 34, 713 natural versus anthropogenic, 334 in páramos, 498– 99, 498, 508, 514, 721 pastures and, 300, 302, 303, 307, 309– 10 payment for ecological services and, 542, 543 recovery from, 514 wetlands and, 686, 691, 699, 701, 702, 721 forestry and forest management, 542– 45, 569 Forestry Law of 1996, 542, 543 Forsythe, W., 86 fossils, 50– 52, 51 Foundation of Friends of Isla del Coco (FAICO), 180, 237 Fournier, L. A., 77, 211, 478 Fournier, M. L., 151– 52 Foyo, M., 592, 604 FPN. See Fundación de Parques Nacionales (FPN) Fraile, J., 77, 79 Frankie, G. W., 247, 254, 271– 72 Freer, E., 154 French Fund for the World Environment (FFEM), 171– 72, 175– 76, 182, 211, 237 Freytag, P. H., 231 Fuller, C. C., 155 Fundación Delfín Talamanca, 608 Fundación de Parques Nacionales (FPN), 402, 403 Fundación KETO, 608 Fundación Salvemos al Manatí de Costa Rica, 595, 608 Furchheim-Weberling, B., 512 Gabb, William More, 3, 495 Gage, Thomas, 152 Gámez Lobo, Rodrigo, xviii García, V., 596 García-Méndez, K., 102, 108 García-Rios, C. I., 594 García-Robledo, C., 561

García-Rojas, M., 471 Garita, J., 154 Garrison, G., 169, 219– 20 Garvin, T., 281 Gasca, R., 100 GEF. See Global Environmental Facility (GEF) Genereux, D. P., 636 Gentry, Al, 468 geological regions of Costa Rica, 31 Abyssal Plain and, 32, 33, 34 Arenal depression and, 48 back-arc region and, 49– 50 Baja Talamanca and, 49 Barranca estuarine system and, 39– 40, 39 coastal geomorphology and, 42– 43 Cordillera Central and, 46 Cordillera Costeña range and, 49 Cordillera de Guanacaste and, 45 Cordillera del Coco and, 34 Cordillera de Talamanca and, 46– 48 Cordillera de Tilarán and, 45– 46 Coto Brus valley and, 48 Fila Bustamente range and, 49 forearc ophiolitic promontories and, 35– 37 General Valley and, 48 geological glossary and, 61– 63 Golfo Dulce Basin and, 45 intra-magmatic axis basins and, 48 literature on, 32 Magmatic Arc and, 45– 48 Middle America Subduction Trench and, 32, 33, 34, 36– 37 Montes del Aguacate, 45– 46 Nicoya Basin and, 37– 40 Nicoya Peninsula and, 35 North Limón basin and, 50 Orotina Basin and, 37– 40 Osa Peninsula and, 36– 37, 37 Parrita Basin and, 40, 43, 45 Parrita-Quepos area and, 40, 40 Punta Burica and, 36– 37, 37 Punta Judas erosive platform and, 41 Puntarenas sand bar and, 38, 39– 40 Quepos Promontory and, 36 San Carlos– Caño Negro– Tortuguero plain and low hills and, 49– 50 Santa Elena Peninsula and, 35 Santa Rosa Ignimbrite Plateau and, 45 South Limón basin and, 50 summary of geological history and, 53– 56 Tempisque Basin and, 37– 40 Térraba Basin and, 40, 43, 45 thrust-fold deformation belts and, 48– 49 Turrubares Block and, 36 Valle Central and, 48 Gichuru, M. P., 84 Gilbert, C. R., 595 Gilbert, Lawrence, 368– 69, 370 Gillespie, T. W., 254 Gissler, August, 162, 164, 196 Gladstone, D. E., 275 Glasstetter, M., 175

Global Environmental Facility (GEF), 9, 211, 237, 369, 567, 569 Gocke, K. exploration of páramos and, 498 Gulf of Nicoya and, 142, 143 lake studies of, 666– 67, 672, 675 on red tides, 154 Goffredi, S. K., 118 Goldman, C. R., 656 Golfo Dulce ecosystem, 143, 154 Gomes, L. G., 476 Gómez, J. R., 225 Gómez, L. D. biogeography of cloud forests and, 457 classification of vegetation macrotypes by, 8, 9, 10 classification schemes for Isla del Coco vegetation and, 211 on epiphytes in cloud forests of the Talamanca, 462 exploration of páramos and, 497– 98 on fungi in cloud forests of the Talamanca, 458 on fungi in the páramos, 509 geomorphology of Costa Rica’s dry forests and, 251 illness and death of, xix– xx influences on, 497 Isla del Coco crabs and, 232 paleobotanical research and, 52 publications on Costa Rica and, xix on vegetation in dry forests, 252, 253, 254, 256 on vegetation of Central Pacific region, 350 vegetation studies in the cloud forests of the Talamanca and, 467 on zonal pattern in highland bogs, 685 Gonyea, Wilford, 364 Gonzales, E., 273 González, C., 207– 8 González, E., 156 González, M. A., 83 González, W., 107 González D’Ávila, Gil, 3 Goodnight, J. C., 231 Goodnight, M. L., 231 Goshe, L. R., 591 Gradstein, S. R., 458, 509– 10 Grant, P. R., 223 Grant, R., 223 Grayum, M., 256, 348, 349 Great American Biotic Interchange (GABI), 5, 457, 532 greenhouse gases. See climate change Griffin, D., 431 GRUAS I and II projects, 8, 9 Grubb, P. J., 8 Guadamuz, E., 667 Guanacaste Dry Forest Conservation Fund, 281 Guariguata, M. R., 544 Guayamí de Osa, 362 Gueydon, Henri Louis de, 194

Subject Index 735 Guillén, C., 77 Gulf of Nicoya ecosystem boundaries of, 139– 41 as commons, 139 comparable environments in Australia and, 145 concentration of sediments in, 141– 42 development of coastline and, 139 eutrophy in, 142 expeditions and, 147, 148, 155 fish communities in, 148– 49 fishing in, 153 history of, 150– 52 hypertrophy in, 142 intertidal sediments in, 144– 45 loss of suspension feeders in, 151– 52 mangrove community in, 143 maps of, 140, 141, 151 need for ecosystem-based management in, 156 overfishing and, 154 photographs of, 139– 41, 140 physical characteristics of, 141– 42 phytoplankton in, 146– 47 pollution in, 155– 56 red tides in, 146, 154– 55 research needs and, 149 rocky intertidal substrates and, 146 salinity of, 141– 42, 141 sardine migration and, 140– 41 seasonality and, 142, 148, 149 shipping in, 139– 40 shrimp trawling and bottom damage in, 153– 54 as single ecosystem, 143 steady state in, 149 subtidal sediments in, 145– 46 tidal levels in, 147 toxic algal blooms and, 155 trophic modeling and, 149– 50, 150, 154 tropho-dynamics of, 148 vertical stratification in, 141 water chemistry and primary productivity of, 142– 43, 143, 149– 50, 151 water currents in, 142 worldwide estuarine trends and, 150– 56 zooplankton in, 147– 48 Gutiérrez Braun, Féderico, 497 Guzman, H. M., 102, 604, 605 Guzmán, Héctor, 596 Haber, W. A., 428, 429 Haberyan, K. A., 663, 685 Haberyan, Kurt, 498– 99 habitat fragmentation, 264 Häger, A., 422 Haggar, J. P., 77 Halffter-Salas, G., 231 Hallwachs, W., 252, 270, 274, 275, 279, 315 Halstead, B. W., 168 Hamazaki, T., 634– 35 Hamilton, L. S., 452

Hammel, B. E., 8 Hamrick, J. L., 272 Hancock, Allan, 100 Hansa-Luftbild (German company), 9 Hansen, K. L., 153 Hanson, P., 433 Harbor Branch Oceanographic Institution, 169 Hargraves, P., 146, 154 Harmon, P., 353 Hartman, Carl V., 563 Hartman, O., 168 Hartshorn, G., 65, 254, 345, 347, 374– 75, 541 Hass, Hans, 168 Hayes, M. P., 434 Heal, O. W., 83 Heard, Richard W., 594 Hedgpeth, J. W., 156 Heithaus, E. R., 273 Helmer, E. H., 473 Hendler, Gordon, 594 Henry, Dora P., 594 Heppner, J. B., 231 Hernáez-Bové, Patricio P., 118 Herrera, Gerardo, 498 Herrera, M. E., 77 Herrera, W., 8, 198, 345, 372 Herrick, J. E., 81 Hertel, D., 475– 76 Hertlein, L. G., 168, 171, 235 Hill, Robert T., 495 Hine, Walter, 305 Hoffman, R. L., 235 Hoffmann, Karl, 3, 7 Hogue, C. L., 227, 231, 386 Holdridge, Leslie R., 8 biogeography of cloud forests and, 457 classification system of, 10 crops planted at La Selva Biological station by, 541 on forests of Osa region, 365, 374 foundational wet forest studies by, 366 land use recommendations of, 65 1960 National Academy of Sciences (US) conference and, 366 predictive power of Holdridge model and, 8 publications on Costa Rica and, xix Tropical Science Center (TSC) and, xv See also Holdridge Life Zones Holdridge Life Zones in Área de Conservación Guanacaste (ACG), 252, 256, 262, 322, 326 in Central Pacific region, 349, 352 classic field study introducing, 7– 8 in cloud forests of volcanic Cordilleros, 428, 435 in Nicoya Peninsula, 260 páramo ecosystem and, 499– 500 soil organic matter and, 82 Holl, K. D., 471, 478– 79 Hölscher, D., 475

Holz, I., 458, 463, 509– 10 Hooftman, D. A. P., 460 Hooghiemstra, H., 27, 515, 685 Hopkins, Timothy, 166 Hopkins Stanford Galapagos Expedition (1898– 1899), 99, 166 Horn, M. H., 635, 685 Horn, S. P., 502, 506– 7, 512 Horn, Sally, 498– 99 Horne, A. J., 656 Hossfeld, B., 148 Houbrick, Joseph, 592, 593– 94 Huber, B., 231 Huertas, J. A., 224 Huey, R. B., 552 Humbert, S., 155 Humboldt Current, 199– 200 Humedal Nacional Térraba-Sierpe, 99, 362 hunting antihunting efforts and, 401, 404 in cloud forests of volcanic Cordilleras, 437 cultural and historical reasons for, 401 in dry forest areas, 276– 77 extinction of New World megafauna and, 293– 94 illegal, 358, 699 in and near national parks, 400– 401 Pleistocene Era extinctions and, 532 of reptiles, 552 seed dispersal and, 562 threats to páramos and, 515 threat to tapir populations and, 467 hurricanes, 314– 15, 321, 324 hydroelectric power, 632, 639– 646, 641– 46, 649 Ibarra, E., 122 IDA. See Agrarian Development Institute (IDA) Iltis, Hugh, 674 INBio. See Instituto Nacional de Biodiversidad (INBio) INCOPESCA. See Costa Rican Fisheries Institute (INCOPESCA) Instituto Costarricense de Electricidad (ICE), 623, 641 Instituto Físico-Geográfico Nacional, 166– 67 Instituto Meteorológico Nacional (IMN), 535, 535 Instituto Nacional de Biodiversidad (INBio) ALAS (Arthropods of La Selva) research and, 546 on cloud forest biodiversity, 460 ECOMAPAS Project and, 9, 513 growth of ecosystems knowledge and, xv, 8– 9 INBioparque and, xv, 13 inventories in Parque Nacional Palo Verde and, 257 Osa region research and, 361, 369, 377 páramo research and, 499, 511 plant species lists from, 539

736 Subject Index Instituto Nacional de Biodiversidad (continued) specimen collection on Caribbean coast and, 594 Inter-American Highway, 321 Área de Conservación Osa (ACOSA) and, 366 commercial exploitation of cloud forests and, 477 construction of human settlements and, 477, 514 Cordillera de Talamanca and, 455, 507 extension of, 366 lakes and ponds along, 660, 668– 69, 670, 674, 685 Mesa Santa Rosa and, 291, 301 páramos along, 514, 670, 673 Parque Nacional Santa Rosa and, 305 peat deposits along, 82, 506 protected forest along, 4 ranching and, 331 tapir killed in road accident and, 479, 480 through Área de Conservación Guanacaste (ACG), 304 Inter American Institute of Agricultural Sciences (IICA), 64 International Union of Biological Sciences (IUBS), 5 Intertropical Convergence Zone (ITCZ), 20– 21, 104, 173, 197, 198, 372, 420, 503 invasive species in Área de Conservación Guanacaste (ACG), 335– 36 biodiversity and, 336 cattail as, 659, 663 Isla del Coco ecosystems and, 211 tilapia as, 628, 628, 640, 648– 49, 692 Irons, J. G., 637– 38 Isla del Coco and its ecosystems, 164, 166– 67, 204, 206, 207 age of the island and, 201 ants and, 228 arachnids and, 231, 232 arthropods and, 235 bay communities of, 214– 15, 218 beaches and, 173, 174 beetles and, 228 biodiversity and, 171– 72, 193– 95, 200– 211, 236– 38 birds of, 221– 24, 224, 225 butterflies and, 230 caves, tunnels, and arches and, 175, 176, 177, 178, 206 climate and weather and, 162, 172– 73, 197– 99 coastal cliff communities of, 215– 16, 218, 218 coconut groves on, 214– 15 conservation and, 180– 82 coral reefs and, 175, 178– 79, 179, 181, 710 Costa Rican government presence on, 236 current state of knowledge about, 171– 72, 196– 97 deforestation and, 196, 218

disharmonious floras and, 209 El Niño Southern Oscillation (ENSO) and, 178, 199, 200, 219 endemicity of species and, 172, 193, 208– 11, 219 expeditions and, 165– 68, 171, 177, 194– 96, 197, 209, 226, 228, 231 fishes of, 219– 20 fishing near, 182, 182 freshwater invertebrates and, 233– 35 fungi, Myxomycetes, and lichens on, 208– 9 future sustainability and, 236 geographical coordinates of, 162, 172, 197 geology and geomorphology of, 172, 192, 200– 201, 201, 205– 6 history of, 162, 164, 165– 71, 193– 96 human impact on, 178– 79, 196, 214– 15, 219, 235– 36 hydroelectric power plant and, 196 importance of for research, 193, 211 as Important Area for Bird Conservation, 218 Indo-Pacific species and, 165, 184, 193 insects and other terrestrial invertebrates on, 227– 32, 229 as internationally important wetland, 165, 193, 236, 238 Intertropical Convergence Zone (ITCZ) and, 173, 197– 98, 199 introduced vertebrates as threat to, 224– 25, 226– 27 invasive species and, 211 Isla del Coco Bioregion and, 193 land cover percentages and, 218 landslide vegetation and, 217, 218, 218 mammals and, 224– 27, 228, 236 maps of, 162, 163, 164, 195, 203 as Marine Conservation Area, 236 national exploration and tourism and, 196 national park and, 164– 65, 236 need for environmental management on, 236– 38 North Equatorial Countercurrent and, 165, 173, 173 as oceanic island, 192– 93, 199– 200, 209, 211 open ocean and deep waters and, 177– 78 origins of plants on, 210– 11 penal and agricultural colonies and, 196, 226 rain forests and, 713– 14 reptiles of, 220– 21, 221, 222 research needs and, 182– 83, 237– 38 riparian communities and, 216– 17, 218 rocky intertidal zones and, 173, 175– 76 sedimentary deposits from the Holocene in, 201– 3, 202 shallow and deep sea fauna and, 711 soils of, 207– 8 sources of species on, 229 species introduced to, 196 sphingids or hawk moths and, 229– 31

terrestrial crustaceans and, 231– 33, 233, 234, 235 threats to, 178– 79 topography and hydrology of, 205– 7 tourism and, 236 treasure hunting and, 195– 96 Treasure Island and, 162 tropical cloud forest on, 213– 14, 214, 215, 218 tropical rain forest on, 213, 213, 216, 218 vegetation and plant communities of, 209– 11, 217– 18, 217, 219 vertebrates on, 218– 19 volcanic rocks and, 203– 5 waste from human residents and visitors and, 236 water circulation around, 173, 173 as World Heritage Site, 165, 184, 193, 236, 238 See also Pacific coast of Costa Rica Isla del Coco Marine Conservation Area (ACMIC). See Área de Conservación Marina Isla del Coco (ACMIC) Islebe, G. A., 27, 457, 508 ITCO. See Lands and Colonization Institute (ITCO) IUCN Red List, 482, 608 Jackson, J. B., 150 Janss Foundation, 169 Janzen, D. H. All Taxa Biodiversity Inventory (ATBI) and, 250 beetle studies and, 269, 273 conservation advocacy of, 280 dry forest studies and, 248, 252, 270, 274 growth of ecosystems knowledge and, xv Guanacaste studies and, 252, 260, 711 natural history of Costa Rica and, xix, xx, 270 páramos studies and, 498, 512 plant-animal mutualism and, 274 reforestation projects and, 279 J. Craig Venter Institute, 169 Jennings, S., 156 Jiménez, C., 113, 123, 175– 76, 595– 96, 665 Jiménez, Ignacio, 595 Jiménez, J., 9, 143, 156, 349 Jiménez, Q., 260, 348, 350– 53 Jiménez, W., 473 John A. Phipps Biological Station, 566 Johnson, N. C., 85, 231 Jordal, B. H., 231 Joyce, A., 345, 542 Juárez, M. E., 477– 78, 479 Kalácska, M., 277, 279 Kappelle, Dirk, 451 Kappelle, M., xx, 8 on birds in forest recovery, 476 cloud forest studies and, 457, 460, 462– 63, 467– 69, 473, 476– 79 on lichens in oak forests, 459

Subject Index 737 mapping of marine ecosystems and, 9 páramo studies and, 499, 508 on tree plantations in Osa region, 377 on zonal pattern in highland bogs, 685 Kass, D. L., 78 Kasteleijn, H. W., 194 Keith, Minor C., 495, 563 Kelso, D. P., 595 Kennedy, John F., 505 Kernan, Kit, 370 Kimble, J. M., 83 Kirkendall, L. R., 229 Kohkemper, J., 656 Kohkemper, M., 502 Köhler, L., 462, 475 Kramp, P. L., 168 Kriebel, R., 460 Kroodsma, D. E., 223– 24 Kumar, A., 433 Kupper, Walter, 497 Kuprewicz, E. K., 561 Kury, A. B., 231 Kyoto Protocol, 8 Lachniet, M. S., 503, 504, 506– 7 Lafond, Gabriel, 363 Lahmann, E. J., 107 lakes of Costa Rica Asunción Pond and, 674 Caribbean lowland moist forest and, 674– 77 Central Pacific moist forest and, 663 Chirripó lake district and, 671 climate change and, 678 diatom assemblages in, 663, 668, 669– 70, 676 distribution and origins of, 657– 59, 658 El Niño– Southern Oscillation (ENSO) warming events and, 672– 73 Estero Blanco and, 659, 660– 61, 662 fish kills and, 666, 675 formation of, 656, 663– 64, 666– 68, 666, 674– 77 geological history of, 657, 663– 64, 670, 674, 677– 78 human impact on, 678 Lago Asunción and, 672 Lago Chirripó and, 670, 672, 674 Lago de las Morrenas and, 672, 673, 674 Laguna Arancibia and, 668 Laguna Barva and, 664, 665– 66 Laguna Bonilla and, 676– 77 Laguna Bonillita and, 675, 676– 77, 676 Laguna Bosque Alegre and, 666 Laguna Botos and, 674 Laguna Carara and, 663 Laguna Cerro Chato and, 664– 65, 668, 674 Laguna Congo and, 666 Laguna Cote and, 667 Laguna de Río Cuarto and, 667, 674– 76 Laguna Gamboa and, 668– 69 Laguna Gandoca and, 675, 677

Laguna Hule and, 665, 666– 68, 666, 674 Laguna La Palma and, 665, 667 Laguna Madre Vieja and, 663 Laguna María Aguilar and, 667 Laguna Martínez and, 659, 660– 61 Laguna Palmita and, 660 Laguna Poco Sol and, 665, 667– 68 Laguna San Pablo and, 659, 660– 61, 662 Laguna Santa Elena and, 668– 69 Laguna Sierpe and, 664 Laguna Solimar and, 660, 661 Laguna Vueltas and, 664 Laguna Zent and, 675, 677 Laguna Zoncho and, 668, 669– 70 lake temperatures and, 674– 75 lake turnover and, 674– 75 maps of, 658, 660 northern highland evergreen cloud forest and, 664– 68 of the Pacific dry forest, 659– 61, 663 páramo grasslands and, 670, 672– 74 pollen records in study of, 668, 669– 70, 674 presence versus absence of fish in, 672 Quebrador Pond and, 673– 74 research on, 656– 57 sediment cores and, 661, 663– 64, 667– 70, 674, 677 Southern Highland cloud forest and, 668– 70 Southern Pacific moist forest, 664 Tres de Junio Pond and, 669– 70, 674 turnover in, 666– 67 water pollution and, 677 water temperatures and, 672– 73 wetlands ecosystems and, 720– 22 wet versus dry season and, 662 Lal, R., 81, 83 Lamont-Doherty Earth Observatory, 168 Lands and Colonization Institute (ITCO), 365 Lang, S. B., 86 Lanteri, A. A., 231 Lapied, E., 79 Las Cruces Biological Station, 477, 668 La Selva Biological Station, 568 ALAS (Arthropods of La Selva) research at, 433, 546 archaeological artifacts at, 532 Arthropods of La Selva (ALAS) Project in, 560 bats at, 437, 557 biodiversity at, 429, 431, 434 butterfly inventories at, 560 contributions to riverine research and, 623, 624– 25 as control forest site, 541 decline in amphibians of, 629 decline of terrestrial frogs in, 551 fish communities at, 627 food web in streams of, 634 forest studies in and around, 543– 45 fossils at, 532

frugivory and seed dispersal at, 561, 635– 36 herbivory at, 558, 634– 35 hydrodynamics at, 549 insect community at, 558 invertebrate studies at, 546, 635 lakes of, 677 microbial respiration studies at, 638 organic matter processing at, 637– 39 patterns of vegetation at, 540– 41 plant species lists from, 539 predator-prey interactions at, 635 primate studies at, 400, 557 production of higher trophic levels at, 639 as renowned research site, 369, 372, 404, 714 reptiles of, 552 research needs and, 556 rivers and streams of, 625 San Juan– La Selva Biological Corridor and, 566, 568– 69, 568 seed dispersal at, 562 soils at, 77, 80, 86, 538– 39 species collection at, 386– 87, 539 stream chemistry at, 636 stream nutrient dynamics at, 637 terminus of Pleistocene lava flows at, 636 travel to, xv, 528 view from research tower at, 537 weather at, 535– 37, 538 Laurencio, D., 268 Laurito, C., 52 LaVal, R. K., 272, 437, 557 Lavelle, P., 79 Lavenberg, R., 219– 20 Law of the Sea of the United Nations (UNCLOS), 164– 65 Lawrence, John M., 591– 92 Lawton, M. F., 423, 473 Layton, W. E., 224 Leenders, T., 356 Leiva, J. A., 85 Lellinger, D. B., 462 León, P., 148, 149, 305 León, S., 79 Leslie, M., 390, 595, 634 Lessios, H. A., 165 Levi, H. W., 231 Levin, L. A., 118 Liesner, R., 252, 260, 273 Lièvre, D., 165, 193 Lines, N., 478 Link, J. S., 156 Linsley, E. G., 231 Lips, K. R., 634 livestock raising abandonment of ranching lands and, 279 in Área de Conservación Guanacaste (ACG), 302 cattle slaughter industry and, 300 clearing land for, 300 cross-isthmus transport and, 331 decline in ranching and, 277

738 Subject Index livestock raising (continued) deforestation and, 541 economic viability of, 302– 3 environmental damage caused by, 315 fire and, 302, 315, 691 grasses chosen for, 302 habitat destruction and, 567 historical land use and, 276, 621– 22 land use conversion and, 646– 47, 647 reduction of biodiversity and, 302, 303 Lizano, O., 142, 155, 171, 596 Lobo, L. A., 272 Lockwood, J. P., 206 Löffler, H., 498, 656 Lohmann, W., 52 Loiselle, B. A., 561 Longino, J., 433, 463, 546 López, F. L., 78 López, M., 116, 148, 171, 219, 397, 595 López Pozuelo, F., 218 Loría-Naranjo, M., 109 Los Angeles County Museum of Natural History, 169 Lourenço, W. R., 231 Lovejoy, Thomas Eugene, xv, 4 Lücking, A., 208, 211, 224 Lücking, R., 208, 211, 224 Lugo, A. E., 248 Luke, Spencer R., 100 Lulow, M. E., 471 Luteyn, J. L., 510 Lyons, J., 635 Macintyre, I. G., 175 Madrigal, R., 32 Madrigal-Castro, E., 102 MAG. See Ministerio de Agricultura y Ganadería (MAG) Malavassi, E., 205 Maldonado, T., 256 Manning, R. B., 100, 102, 165, 168 maps and mapping Área de Conservación Guanacaste (ACG) and, 291, 292, 294– 95, 326 Área de Conservación Osa (ACOSA) and, 377 bogs, marshes, and swamps and, 684 Caribbean coast and, 592 Caribbean lowlands and, 528 Chirripó lake district and, 671 climate zones of Caribbean lowlands and, 535 cloud forests of the Talamanca and, 452 cloud forests of the volcanic Cordilleras and, 416 of Costa Rica, 11, 31 of currents in Eastern Tropical Pacific, 173 distribution of lakes and, 658, 660 distribution of páramo vegetation and, 493 ECOMAPAS Project and, 513 of Economic Exclusive Zones (EEZ), 98 forest cover in Chorotega region and, 278 funding for, 9

geological, 31– 32, 504 Gulf of Nicoya and, 140, 141, 151 hydropower plants and, 641, 646 Isla del Coco and, 162, 163, 164, 171, 195, 203 locations of plant collections in Caribbean lowlands and, 540 of marine ecosystems, 9, 103 of marine protected areas, 592 mega-mammal localities and, 50 methodology for, 9 northern Costa Rica and, 416, 417 Osa region vegetation and, 375, 376, 377 of Pacific coast, 99 paleographic reconstruction of Costa Rica and, 54 páramo ecosystem of Costa Rican highlands and, 494, 497 of páramo plant communities, 513 phytogeographic units and, 9 of potential land use, 64 of protected areas of Caribbean moist forest, 530 of protected areas of montane cloud forest zone, 416 of protected areas of Northwestern dry lowlands, 249 of protected areas of Pacific moist lowland forests, 362 of protected areas of Pacific seasonal forest zone, 346 of protected areas of Talamancan high forest region, 452 of protected areas on Pacific coast, 99 of protected areas that conserve páramo ecosystem, 494 soil maps and, 64, 65, 66– 67, 69, 72, 74– 75 Southern Pacific region and Osa peninsula and, 362 Tosi’s life zone map and, 500 variable place names and, 550 watersheds of Costa Rica and, 622 world maps and atlases and, 162 Marine Pollution Monitoring Program in the Caribbean (CARIPOL), 596, 609 Maritza Biological Station, 623 Marr, Wilhelm, 154 marshes. See bogs, marshes, and swamps Martin, J. W., 171– 72 Martin, P. S., 532 Martínez, A., 20, 116 MarViva Foundation, 237 Mata, A., 101, 156 Mata Jiménez, Alfonso, 247 Mather, J. R., 23, 25, 26 Mathis, W. N., 231 Mattiucci, S., 106 May-Collado, L., 116, 595 McGlynn, T. P., 77 McLaughlin, Patsy A., 594 McLennan, B., 281 McNeill, D. F., 597

Mediterranean Red Book of threatened habitats, 116 Mehltreter, K. V., 462 Mesoamerican Biological Corridor, 545, 565, 567– 68 Michel, H. B. marine research and, 592 on open waters off the Caribbean coast, 604 Mielke, W. crustacean studies and, 594 Gulf of Nicoya ecosystem and, 144 migration of species altitudinal, 355, 507 Great American Biotic Interchange (GABI), 457 of invertebrates, 635 latitudinal, 553 migration potential and, 508– 9 oceanic islands and, 192, 197, 208 sardines and, 141 sea-level rise and, 109 seasonal, 323– 28, 696 sharks and, 183 of shrimp, 632 of turtles, 567 weather events as cues for, 322 Mikheyev, A. S., 228 Millennium Development Goals (MDGs), 563– 64 Millennium Ecosystem Assessment (MA, 2006), xvii Miller, Kenton, 305– 6 Miller, S. E., 227, 231 MINAE. See Ministerio de Ambiente y Energía (MINAE) mining, 639– 40 Ministerio de Agricultura y Ganadería (MAG), 65 Ministerio de Ambiente y Energía (MINAE) administration of protected areas by, 608, 609 anti-hunting efforts of, 401 ECOMAPAS Project and, 9, 513 ecosystem management and, 156 freshwater ecosystem monitoring and, 633 mapping of ecosystems in Área de Conservación Osa (ACOSA) and, 377 marine issues and, 123 natural forest management and, 542– 43 water concessions and, 648 Missouri Botanical Garden, plant species lists from, 539 Mohr, Mary E., 451 moist forests. See cloud forests; dry forests; rain forests Molina-Ureña, H., 148 Monge, Guiselle, 568 Monge, J., 78, 79– 80, 511 Montes, C., 97 Monteverde Cloud Forest Preserve, 443, 462 Montoya, M., 165, 169– 70, 211, 218– 19, 223– 24, 230, 594

Subject Index 739 Monumento Nacional Santa Rosa, 298 Mora, A., 114, 178– 79 Mora, Dagner, 596 Mora, J. M., 224 Mora, José Joaquín, 300 Mora, S., 32 Morales, A., 147 Morales, J. F., 275, 352, 468 Morales, M. I., 431 Morales-Ramírez, A., 102, 116, 147, 148, 594, 595 Moran, Dennis A., 594 Moreno-Díaz, Mary Luz, 182 Motta, P. J., 170 Moya, Jorge, 247 Mueller, Greg, 458 Mueller-Dombois, D., 9 Mug, M., 6, 9– 10 Muller-Parker, G., 595 Murphy, P. G., 248 Murray, K. G., 438 Museo Nacional of Costa Rica, 166 Myers, N., 348 Nadkarni, N., 422, 433, 441, 462, 463 NASA, 257 Nason, J. D., 272 National Academy of Sciences (US), 366 National Aqueduct and Sewerage System (AyA), 21 National Association for Indigenous Matters (ANAI), 595, 608 National Geographic Society, 171 National Institute of Biodiversity (INBio). See Instituto Nacional de Biodiversidad (INBio) National Meteorological Institute (IMN), 21 national park system administration of protected areas by, 608 ECOMAPAS Project and, 9 founding of, 360 funding and, 402 Isla del Coco and, 236, 237 NGOs and, 402 Osa region research facilities and, 369 overvisiting in, 515 removal of vestiges of human residence in, 306 See also protected areas; and specific parks National System of Conservation Areas (SINAC). See national park system; protected areas Nature Conservancy, The acquisition and donation of land by, 403 Caribbean coast conservation efforts and, 608 cloud forest conservation and, 443 Costa Rican– Panamanian site conservation plan and, 483 Costa Rican wetland systems and, 9– 10 ecoregional assessment and, 181 Isla del Coco Bioregion and, 193 Parque Nacional Corcovado and, 367

sustainable economic development and, 371 wetland conservation and, 701 NECC. See North Equatorial Countercurrent (NECC) Newbold, J. D., 636 Newsom, L., 534 New York Zoological Society, 168 New Zealand Threat Classification System, 116 Nickle, D. A., 231 nitrogen cycle, xv– xvi Nixon, S. W., 142 NOAA Southwest Fisheries Science Center, 170 Norrbom, A. L., 231 North, Oliver, 297, 299 North Equatorial Countercurrent (NECC), 165, 173, 199– 200 Nova-Bustos, N., 107 Obando, J. A., 5, 6, 9 Obando-Calderón, G., 224 oceanic and coastal-marine ecosystems, summary of, 709– 11 O’Donnell, S., 433 Oduber, Daniel, 305, 566 Odum, Eugene P., 10 Oelbermann, M., 85 Oemke, M. P., 627 Oldeman, R. A. A., 473 Olsgard, F., 155 Olson, D. M., 10, 452– 53 Opresko, D. M., 118 Organization for Tropical Studies (OTS) contributions to riverine research and, 623 dry forest conservation and, 280 lake studies and, 661, 667 land use assessments and, 64– 65 marine algae research and, 591 North American students and, xv origins of researchers at, 366 research facilities of, 404 research reserves and, 366 specimen collection and, 592– 93 See also La Selva Biological Station Ornelas-Gatdula, E., 103, 594 Ørsted, Anders Sandøe, 3, 7 Ortea, Jesús, 594 Ortega, S., 107 Orvis, K., 498– 99, 502, 506– 7, 672 Osa Forestal (Osa Productos Forestales), 364– 68, 371 Osa region ants in, 386– 88 biodiversity in, 361, 373– 75, 387, 392, 394 birds of, 392– 94 butterflies in, 386 climate of, 372 commerce in, 364– 65, 371 conservation efforts in, 365– 72

early scientific activity in, 364– 65 El Niño Southern Oscillation (ENSO) and, 379– 80 endemism in, 388, 391– 92 fate of Golfo Dulce and, 371 fishes of, 388– 91 forest gap dynamics and, 378– 85 forest swamps in, 697 geomorphology of Costa Rica and, 373 gold mining in, 363, 364, 365 herpetofauna in, 391– 92 human impact on, 361– 64, 371, 389 importance of for science, 361, 404– 5 insects in, 386– 88 land crabs in, 385– 86 land use policies in, 362– 63, 365, 366 land use types in forests of, 382– 83 limited exploration of, 360– 61 mammals in, 394– 400 maps of, 362, 375, 376, 377 Osa Peninsula and, 367 padlocking of research station in, 368 palm swamps in, 694 pastureland in, 378 pre-Columbian artifacts in, 363 primates in, 399 rain forests in, 714 rancho in, 363 small- and large-scale disturbances in, 379– 80, 382 soils of, 373 stature of trees in, 375 streams and rivers of, 389 threatened tree species in, 374 timber industry in, 364– 66 tourism and local economies in, 371 treefalls in, 379– 81, 380, 382 Tropical Science Center (TSC) station in, 363 vegetation of, 368– 69, 373– 75, 377– 78 See also Área de Conservación Osa (ACOSA) OSPAR Convention. See Convention for the Protection of the Marine Environment of the North-East Atlantic (OSPAR Convention) Otárola, C. E., 456, 505 OTS. See Organization for Tropical Studies (OTS) Pacific coast of Costa Rica area of coastal waters and, 97, 165 Bahía Culebra and, 102, 103, 105, 111, 113, 120, 123 beach ecosystems and, 105– 6, 105, 106 bottom profile of, 103 versus Caribbean coast, 97 circulation, tides, and waves and, 104– 5 climate and, 97, 104 climate change and, 121 cold seeps and, 117, 118 conservation efforts and, 122– 23 coral reef ecosystems and, 111– 13

740 Subject Index Pacific coast of Costa Rica (continued) Costa Rican Thermal Dome and, 100, 104, 116, 119 Costa Rica’s inability to patrol waters and, 121, 122 current state of knowledge about, 101– 3 deep benthos zone and, 116– 19 deep water fisheries and, 118 early research on, 101 ecosystem health and human survival and, 123 environmental threats along, 120– 21 expeditions along, 99– 101, 102, 116– 17, 118, 123 geology and geomorphology of, 103– 4 Golfo de Nicoya and, 101, 103, 104, 109, 110, 110, 112 Golfo Dulce and, 102, 104, 111, 112, 118, 123 historical overview of marine research and, 98– 101 human population and demography of, 120 hydrography of, 104 intertidal flats ecosystems and, 109– 11, 110 Intertropical Convergence Zone (ITCZ) and, 104 Isla del Caño and, 102– 3 Isla del Coco expeditions and, 169 islands and islets of, 118, 119 mangrove forests and, 108– 9 marine biodiversity of, 119 marine protected areas and, 121– 22 offshore islands and, 112 Oxygen-Minimum Zones and, 104, 117– 18 pelagic ecosystem and, 116 protected areas of, 99 real-estate development along, 371 research needs and, 123 rhodolith beds in, 114, 115, 116 rocky intertidal ecosystems and, 106– 7, 107 seagrass beds ecosystems and, 111 species diversity and, 119 summary of oceanic and coastal-marine ecosystems and, 709 sustainability and, 123 upwelling and, 105, 107, 111, 113 weather and, 104, 111 See also Gulf of Nicoya ecosystem Pacific Equatorial Undercurrent, 199 Paddack, M. J., 606 Paine, R. T., 146 Palo Verde Biological Station, 623 Palter, J., 142 páramo ecosystem of Costa Rican highlands, 495, 496, 506 algae in, 509 altitudinal zonation and, 455, 467, 479, 494– 95, 499– 500 animals in, 511 biodiversity in, 509– 14, 510, 720 bogs of, 685, 686

bryophytes in, 509– 10 climate change and, 506 climate in, 500, 502– 3, 502 conservation and sustainable use in, 514– 15 definition of páramos and, 492 effects of fire in, 498– 99, 498 endemism in, 508– 9 ferns and fern-allies in, 509, 510 as fire-dependent ecosystem, 508 fire in, 508, 514 flowering plants in, 510, 510 forest succession and, 474, 476 fungi and lichens in, 509 geographical distribution of in Central America, 500 geology and geomorphology of, 495, 497, 503, 504, 505– 8 global distribution of páramos and, 492– 95, 493 history of scientific exploration in, 495, 497– 99 Holdridge Life Zones in, 499– 500 inland waters of, 505– 6 as islands in the sky, 500 lakes of, 670, 672– 74 land use history in, 514 lateral profile of, 501 limnology of, 505– 6 mapping of, 497 Mesoamerican biodiversity hotspot and, 499 montane cloud forests surrounding, 500 paramillo communities and, 513 plant specimen collection and, 497– 98 protected areas in, 494 quarternary history of, 506– 9 Ramsar Wetland of International Importance in, 515 rivers originating in, 456 sacred sites of indigenous people and, 497 soils of Costa Rica, 505 summary of, 719– 20 Talamancan Montane Forest ecoregion and, 499 threats to, 515 vegetation of, 508– 9, 512– 14, 513 World Heritage Site and, 481, 499 Parker, N., 170 Parkinson, R. W., 598 Parque Internacional La Amistad Amistosa corridor initiative and, 9 biodiversity in, 460 biological corridors and, 482 birds in, 465 climate in, 454 conservation and, 514– 15 as core protected area, 480 forest zonation of, 468 highland peat bog in, 685 location of, 452, 494 mammals in, 466, 467 Man and Biosphere Reserve and, 515

The Nature Conservancy’s site conservation plan for, 483 Panama and, 481 páramos in, 500 plant communities in, 513 visitation levels in, 515 World Heritage Sites and, 515 Parque Nacional Arenal, 416, 443 Parque Nacional Barbilla, 530 Parque Nacional Barra Honda, 249, 251, 280 Parque Nacional Bosque Diriá, 249 Parque Nacional Braulio Carrillo, 416, 530, 556, 560, 623 Parque Nacional Cahuita conservation efforts in, 606, 608– 9 coral reefs in, 593, 603, 604, 608 crustacean studies in, 594 location of, 530, 592 marine biodiversity studies and, 595 marine pollution studies in, 596 protected areas and, 4 seagrass beds in, 602, 603 size of, 606 Parque Nacional Carara biological corridors and, 357 birds in, 355 dry and moist forest in, 711 floristic composition of, 347 forest layers in, 348– 49 location of, 346, 403 oxbow lake in, 349 primary forest in, 348 scarlet macaws and, 355 as transition zone, 348 tree species in, 260 Parque Nacional Chirripó biodiversity in, 460 birds in, 465– 66 conservation and, 514– 15 as core protected area, 480 elevational changes in woody species richness in, 468 establishment of, 247 fires in, 498, 498 glacier morphology in, 47 lakes of, 670 location of, 452, 494 mammals in, 466, 467 management planning for, 499 páramos in, 500 protected areas and, 4 Talamancan-Caribbean Biological Corridor and, 482 visitation levels in, 515 Parque Nacional Corcovado Baird’s tapir in, 397– 98 biological corridors and, 400, 482 birds in, 392, 393 BOSCOSA project in, 370 butterfly-hostplant relationship and, 383– 85, 383– 84 canopy gap densities in, 382

Subject Index 741 cessation of agricultural disturbance in, 378 conditions before creation of, 389 conservation work in, 402 creation of, 361, 367– 68, 400 difficulty of accessing, 361 ecosystems in, 375 ecotourism in, 369, 370 environmental activism in, 371 environmental education and, 370– 71 expansion of needed, 397 fishes of, 390, 390, 627 forest swamps in, 696 funding and, 367, 370– 71, 403– 4 gold mining in, 368– 69, 370, 389, 400 human impact in, 361 human pressures on wildlife in, 400– 401 importance of for science, 404– 5 jaguars in, 398– 99 land crabs in, 385– 86 location of, 99, 362 mammals in, 394– 95, 716 Man and Biosphere Reserve and, 515 mapping of vegetation types and, 376 moist tropical forest in, 347 park fees and, 402– 3 patch dynamics in, 383 poaching crisis in, 403, 404 primate studies in, 399 protectability of, 371 protected areas and, 4 public engagement and, 370 relocation of settlers and, 367, 380– 81 research hindered at, 368 research projects in, 368– 70 research stations in, 380, 381, 382 research trails in, 378– 79 size of, 403 sustainable forestry in, 371 treefall events in, 382 white-lipped peccaries in, 396 Parque Nacional Guanacaste biological corridors and, 281 forest fires and, 249 insects in, 269 location of, 249, 416 rattlesnakes in, 268 reforestation and, 279 turtles in, 268 volcanic complexes in, 443 See also Área de Conservación Guanacaste (ACG) Parque Nacional Isla del Coco administration station in, 307 before and after aerial photos of, 381 biodiversity in, 171– 72 biomass of fish in, 171 buffer zone around, 180 conservation and, 180– 82 Costa Rica’s claim of sea around, 164– 65 creation of, 164, 180, 193 deforestation in, 307 discovery of new species and, 171 fish diversity studies at, 169– 70

fishing lines retrieved at, 183 importance of for research, 183– 84 maps and, 171 new species found at, 169 personnel of, 184 removal of cattle and horses from, 306– 7 secondary forest in, 350 shark tagging and, 170 threats to, 360 valuation of environmental goods and services and, 182 as World Heritage site, 165, 184, 193 See also Isla del Coco and its ecosystems Parque Nacional Juan Castro Blanco, 416 Parque Nacional La Cangreja, 346, 352, 355, 357, 711 Parque Nacional Los Quetzales, 357, 452, 471, 481, 494 Parque Nacional Manuel Antonio ants in, 387 dry and moist forest in, 711 Eastern Tropical Pacific Marine Corridor and, 165 gastropods at, 107 justification for creation of, 368 location of, 99, 346, 403 as paper park, 122 primate studies in, 399 property development around, 358 squirrel monkeys in, 354, 403, 716 vegetation of, 353 Parque Nacional Maquenque, 8 Parque Nacional Marino Ballena, 99, 113, 403 Parque Nacional Marino Las Baulas, 99, 106, 106 Parque Nacional Palo Verde Arenal Dam complex and, 642 biological corridors and, 281 birds of, 265 cactus in, 252 climate of, 250 dry forest conservation and, 280 fires in, 249, 255, 701, 702 freshwater avifauna in, 266 geomorphology and, 251– 52 location of, 249 marshes in, 690 natural hydrological state in, 659 plant genera with largest number of species in, 257 pollination systems in, 273 restoration of marshes in, 701– 2 species inventories in, 257 water flow and quality in, 699– 700 wetlands in, 258, 259, 660, 661, 663 Parque Nacional Piedras Blancas, 99, 362, 403, 482 Parque Nacional Rincón de la Vieja, 249, 249, 416, 635 Parque Nacional Santa Rosa Área de Conservación Guanacaste (ACG) and, 281, 331

beetles in, 269 biodiversity in, 254 butterflies in, 270 creation and growth of, 305– 6 dry forest conservation and, 280 fire control in, 307 focus of guards’ efforts in, 306 insects of, 269 justification for creation of, 368 landscape-level restoration and, 298 lianas in, 256 location of, 99, 249 monkeys and capuchins in, 264 moths in, 270 protected areas and, 4 reptile and amphibian species in, 267 restoration efforts in, 713 as right-now act of conservation, 331– 37 seed dispersal and, 274 sphingids in, 270 turtles in, 268 white-faced capuchins in, 263– 64 Parque Nacional Tapantí– Macizo de la Muerte biodiversity in, 460 birds in, 466 climate in, 454 as core protected area, 480 forest communities of, 469 highland peat bog in, 686 location of, 452, 494 mammals in, 466, 467 Man and Biosphere Reserve, 515 páramos in, 500 soils in, 455, 456 Parque Nacional Tortuguero, 601 ants in, 387 conservation efforts in, 606, 608 creation of, 566, 567, 569 fishes of, 390, 390 frugivory and seed dispersal in, 636 as isolated island of forest, 542 as key protected area, 4 location of, 530, 592 palm swamps in, 694 size of, 606 Parque Nacional Volcán Irazú, 4, 416, 494 Parque Nacional Volcán Poás, 402, 416 Parque Nacional Volcán Tenorio, 416 Parque Nacional Volcán Turrialba, 4, 416, 494 Pascal, M., 218– 19 Paseo Pantera, 567 Pearse, John S., 169 Pedroni, L., 477 Pereira, A. I., 145 Pereira-Chaves, J., 604 Pérez, E. A., 52 Pérez-Cruet, M. J., 595 Pérez-Reyes, C. R., 604 Peruvian Current, 199– 200 pesticides, 564– 65 Petren, K., 224

742 Subject Index Petrescu, Iorgu, 594 pharmaceuticals, 169 Phillips, P., 148– 49, 375, 376, 377, 595 Pilsbry, Henry A., 168 Pinchot, Gifford, 168 Piperno, D. R., 533 Pittier, Henri cloud forests of the Talamanca and, 453– 54 expeditions of, 3, 166, 167, 195, 195, 364, 495, 503 on Isla del Coco climate, 172 Pizarro, Francisco, 296 plant reproduction in cloud forests of the Talamanca, 469, 471– 73 cloud forest species interactions and, 437– 39 crown-to-crown vegetative competition and, 330 dry forest seed dispersal and, 332, 333 endozoochory versus ectozoochory and, 560 frugivory and, 560– 62 nonreproductive juveniles and, 333– 34 pollination by birds and, 435 pollination systems and, 439, 469, 471, 719 prehistoric dispersal agents and, 329 seasonality of migration of, 328– 31 seed dispersal and, 397, 435, 439, 471– 73, 560– 62, 635– 36, 718 seed predation and, 471, 472– 73 Platnick, N. I., 231 pollution, 150– 51, 155, 608, 647 Ponwith, B. J., 634 Porsch, Otto, 7 Pounds, J. A., 434 Powell, George, 443, 567 Powers, J. S., 82, 84, 85, 279 PPNG. See Proyecto Parque Nacional Guanacaste (PPNG) Prescott, S. C., 64 PRETOMA, 116, 170 Pringle, C. M., 634– 35, 636, 639 Pritzker family, 364 Proctor, J., 77 Programa Cooperativo Oficina de CaféMAG, 64 Programa Estado de la Nación en Desarrollo Humano Sostenible, xvii protected areas administration of, 608 as biogeographical islands, 347 bogs, marshes, and swamps and, 686– 87, 694 of Caribbean coast, 592 of Caribbean moist and wet forests, 530 in Central Pacific region, 346 in cloud forests of the Talamanca, 481 indigenous reserves and, 481 of northwestern dry lowlands, 249 of the Pacific coast, 99

páramo ecosystem of Costa Rican highlands and, 494 rain forests and, 714 in Southern Pacific region, 362 wetland areas within private lands and, 701 Protti, E., 172 Proyecto Parque Nacional Guanacaste (PPNG), 331 Puente de Piedra, 47 Punta Río Claro Wildlife Refuge, 399 Quesada, A. J., 107– 8 Quesada-Alpízar, M. A., 102 Quiros Herrera, R., 279 Radulovich, P., 86 Raich, J. W., 85 railroads, 563 Rainforest Alliance, 565 rain forests biodiversity of, 714– 16 challenges of primate studies in, 399 climate change and, 335 disturbances and restoration in, 715 versus dry forests, 311 edge effects and, 319– 20 forest gap dynamics and, 378– 85 forest invasion and restoration and, 334, 335 land-use types in, 382– 83 large mammals in, 716 low population densities of birds in, 392– 94 in Osa region, 376, 377, 714 patch dynamics in, 382– 83 protected areas and, 714 similarities in Osa region and elsewhere, 374 small- and large-scale disturbances in, 379– 80, 382 summary of lowland rain forest ecosystems and, 713– 16 treefalls in, 378, 379– 81, 380 Ramírez, A., 635, 639 Ramírez, A. L., 77 Ramírez, A. R., 148 Ramírez, C., 77 Ramsar Convention on Wetlands of International Importance, 165, 193, 236, 686, 699– 701 ranching. See livestock raising Rare Animal Relief Effort (RARE), 367 Raunkiær, C., 473– 74 Reaka, Marjorie, 100, 102 RECOPE. See Refinadora Costarricense de Petróleo (RECOPE) Refinadora Costarricense de Petróleo (RECOPE), 596 reforestation in Área de Conservación Guanacaste (ACG), 303, 305 butterfly-hostplant relationship and, 383– 85, 383– 84

canopy dynamics and, 380– 82 cattle and, 81 cloud forests and, 478– 79, 717– 18 versus creating a tree plantation, 309 dry forests and, 248, 277, 279– 80, 309– 10 research on regenerating tropical forests and, 380 soil organic content and, 84– 85 in wet forests of the Caribbean lowlands, 543– 45 young forest ecosystem and, 13 Refugio de Fauna Silvestre Rafael Lucas Rodríguez Caballero, 280 Refugio de Vida Silvestre Bosque Alegre, 666 Refugio de Vida Silvestre Corredor Fronterizo, 530 Refugio de Vida Silvestre Curú, 249, 262, 281 Refugio de Vida Silvestre Junquillal, 249 Refugio de Vida Silvestre Laguna Mata, 659 Refugio de Vida Silvestre Limoncito, 530 Refugio Nacional de Fauna Silvestre Golfito, 362 Refugio Nacional de Vida Silvestre Barra del Colorado, 530, 592, 694 Refugio Nacional de Vida Silvestre Bosque Nacional Diriá, 265 Refugio Nacional de Vida Silvestre Caño Negro, 530, 689, 694, 700 Refugio Nacional de Vida Silvestre GandocaManzanillo, 530, 592 conservation efforts in, 606, 608– 9 coral reefs and, 593 forest swamps in, 698 lakes in, 677 mangrove forests and, 599, 600 seagrass beds in, 602 size of, 606 Refugio Nacional de Vida Silvestre Maquenque, 530, 568– 69, 568, 623 Refugio Nacional de Vida Silvestre Ostional, 106, 249, 280 Rehder, H. A., 168 Reid, F. A., 79 Reserva Biológica Barbilla, 481 Reserva Biológica Carara, 387, 663 Reserva Biológica Cerro Las Vueltas, 452 Reserva Biológica Hitoy Cerere, 387, 452, 481, 494, 530 Reserva Biológica Isla del Caño, 99, 362, 403 Reserva Biológica Lomas de Barbudal, 249, 255, 280 Reserva Biológica Tirimbina, 546, 557, 560 Reserva de la Biosfera La Amistad, 481 Reserva Forestal Arenal, 443 Reserva Forestal Cordillera Volcánica Central, 416 Reserva Forestal Golfo Dulce, 362 Reserva Forestal Los Santos as core protected area, 481 floristic diversity of, 353 forest communities of, 469

Subject Index 743 human settlements in, 477 insects in, 463 location of, 346, 452, 494 Reserva Forestal Pacuare-Matina, 530, 592 Reserva Forestal Río Macho, 452, 481 Reserva Forestal Río Pacuare, 530, 608 Reserva Natural Absoluta Cabo Blanco biodiversity loss in, 153, 277 biological corridors and, 281 dry forest conservation and, 280 evergreen trees in, 262 location of, 99, 249 mammals in, 265 as protected area, 4 survey of amphibians and reptiles in, 268 Reserva Privada Páramo, 452, 494 Reyes-Castillo, P., 231 Reynolds, J. E., 595 Riba-Hernández, P., 399 Richards, Francis A., 100 Richardson, R., 206 Riehl, C., 266 Rio+20. See United Nations Conference on Sustainable Development (UNCSD, Rio de Janeiro, 2012) Ríos Tropicales (tourism company), 640 Rio Summit. See Earth Summit (United Nations Conference on Environment and Development, Rio de Janeiro, 1992) Risk, Michael J. (Mike), 593 Rivera, D. I., 257 rivers of Costa Rica algae and, 624– 26 amphibians of, 628– 29 animals of, 626– 33 aquatic insects of, 633 biodiversity of, 626– 27, 630, 633 biointegrity of, 649 birds of, 630 changing appearance and function of, 623 climate and weather and, 622 conservation efforts and, 648, 649 contributions to riverine research and, 623 crabs of, 632 cyanobacteria and, 624 dams on, 632, 640– 45, 641, 643– 45, 648 descriptive river names and, 636 diatoms and, 624, 626, 626 diversity of river types and, 626– 27 ecosystem processes in, 627– 28, 633, 634– 35, 636– 39 endemism and, 624 extinctions of river species and, 629 extractive and nonextractive human uses of, 639– 40 fish of, 627– 28, 628 food web in, 634 frugivory and seed dispersal in, 635– 36 geochemistry of, 636 geothermally modified groundwaters and, 622 herbivory in, 634– 35 historical land use and, 621– 22

hot springs and, 624 hydroelectric power and, 632, 639, 640– 44, 641– 46, 646, 649 invasive species in, 628, 648– 49 invertebrate drift in, 635 land use conversion around, 646– 47, 647 mammals of, 630 marine fauna far inland and, 626 organic matter processing in, 637– 39 people and nature around, 639– 44, 646– 49 plants and, 623– 26 pollution in, 626 predator-prey interactions in, 635 primary production in, 637 production of higher trophic levels in, 639 reptiles of, 629– 30 research needs and, 649 riverine connectivity and, 632, 642– 44 shortages of potable water and, 623 shrimps of, 632– 33 species interactions in, 633– 36 springs in, 636 stream nutrient cycling and, 628 stream nutrient dynamics in, 637 stream solute and, 624– 25 threatened species in, 629, 629, 630, 632 tourism and recreation and, 639, 640, 641 transportation on, 640, 641 upstream versus downstream fauna and, 627 waste assimilation and, 640 water concessions and, 648 water pollution and, 647 watersheds of Costa Rica and, 621, 622 wetlands ecosystems and, 720– 22 Robinson, David G., 593– 94 Rocha, O. J., 273 Rodríguez, A., 260 Rodríguez, B., 354 Rodríguez, J. M., 80 Rodríguez-Fonseca, J., 154 Rodríguez-Sevilla, L., 594 Rojas, C., 208 Rojas, E., 32, 154 Rojas, J., 149 Rojas, M. T., 596 Rojas-Acuña, O. W., 172 Rojas-Figueroa, 110 Rolim, G., 23 Romero, A., 558 Roosevelt, Franklin D., 168 Rostad, T., 153 Roth, B., 168 Rouse, G. W., 118 Ruiz-Boyer, A., 354 Russell, A. E., 545 Ryther, J. M., 142 Sader, S., 345, 542 Safford, H. D., 493 Salas, E., 595 Salazar, A., 155

Samper-Villareal, J., 102 Sánchez, J., 355 Sánchez, P. A., 81 Sánchez-Azofeifa, G. A., 345 Sánchez-Navas, 100 Sandoval, L., 224 Santoro, M., 106 Sapper, Karl, 3, 64 Sargent, S., 438 Sasa, M., 267, 356 Sato, A., 224 Sauerbeck, D. R., 83 Savage, J. M., 356, 391, 552 savannahs, 350, 351 Savitsky, B., 8 Sayre, R., 9 Schall, E. W., 168 Scheer, Georg, 168 Schlesinger, W. H., 82, 83, 84 Schmidt, E., 595, 601, 606 Schmitt, Waldo L., 168 Schneider, D. W., 635 Schneidt, J., 512 Schonberg, L. A., 433 Scripps Institution of Oceanography, 100 Segura-Puertas, L., 100 Seltzer, G. O., 503, 504, 506– 7 Senn, D. G., 175 Serafino, A., 77 Servicio de Parques Nacionales (SPN), 306– 7 Servicios Eléctricos Potosí S.A. (SEPSA), 65 Shannon-Wiener diversity function H, 144, 145 Sherry, T. W., 224 Sibaja-Cordero, J. A. beach ecosystems and, 106 Gulf of Nicoya ecosystem and, 144, 146 intertidal flats ecosystems and, 110 on intertidal gastropods, 107– 8 Isla del Coco ecosystems and, 173– 74, 206– 7 Pacific coast studies and, 102 red tides and, 155 Sierra, C., 225 Sierra-Sierra, L., 604 Sillet, S. C., 431 Sillett, T. S., 466 SINAC (Sistema Nacional de Áreas de Conservación). See national park system Sinclair, B. J., 231 Singer, Rolf, 458 Sipman, H. J. M., 459, 509 Sirot, L., 399 Sistema Nacional de Áreas de Conservación (SINAC). See national park system Sixth International Botanical Congress (1935), 8 Skutch, A. F., 224, 265 Slater, J. A., 231 Slud, P., 223, 265, 556 Small, G. E., 637 Smith, J. N. M., 224 Smith, M. A., 275

744 Subject Index Smithsonian Institution, 168 Smithsonian Tropical Research Institute (STRI), 169, 181, 404, 596 Soil Science Society of Costa Rica, 65 soils of Costa Rica Alfisols and, 73– 74, 75– 76, 207 Andisols and, 68– 71, 69, 76, 78, 83, 419, 420, 505, 717 ants and termites and, 77– 78 Aquepts and, 67– 68 arthropods and, 77 bacteria and fungi and, 75– 76 carbon sequestration and, 85, 544– 45 cattle and, 80– 81, 81 in Central Valley, 351 cloud forests and, 419– 20, 426, 456– 57, 716– 17 crabs and, 79, 373 dating of, 538 decomposition and, 83– 84 deforestation and, 345, 622 density of litter fauna and, 77 dry forests and, 251, 252, 254 Dystrandepts and, 419, 505 Dystrudands and, 81 ecosystem management and, 84– 85 ecotourism and, 87 Entisols and, 65– 66, 66, 83, 85, 207, 373, 505, 713 erosion and, 86– 87 fertilizer and, 68, 70– 71, 80– 81 Histisols and, 82– 83, 505, 717 history of soil science in Costa Rica and, 64– 66 Humitropepts, 505 Inceptisols and, 66– 68, 67, 79, 83, 85, 207, 373, 419, 456– 57, 505, 713, 717 international soil science meetings and, 65 Isla del Coco and, 207– 8 Life Zone approach and, 83 Mollisols and, 71, 373, 713 nematodes and, 76– 77 new agricultural practices and, 87 nutrient availability and, 86 Orthents and, 65, 66 in the Osa region, 373 Oxisols and, 538 Placandepts and, 505 in páramos, 505 parent material of, 67 Placudands and, 81 poor soils of Área de Conservación Guanacaste (ACG) and, 331, 334, 335 in rain forests, 713 rodents and, 79– 80 soil as a habitat and, 74– 75 soil compaction and, 80– 81, 86– 87 soil orders and, 83 soil organic matter (SOM) and, 82– 85, 82, 83 Sphagnofibrist and, 505 springtails and, 77 types of soil orders and, 65

Udepts and, 67 Ultisols and, 73– 74, 74, 83, 373, 391, 456– 57, 538, 713, 717 Ustepts and, 67 variability of, 87 vegetation and, 81 Vertisols and, 71– 73, 72 volcanic activity and, 621 in wet forests of the Caribbean lowlands, 537– 39 worms and, 78 Solano, S., 110, 144 Solís, Angel, 546 Sollins, P., 86 Solomon, S. E., 228 Solórzano, A., 267, 356 Somoza, Anastasio, 305 Soto, F., 77 Soto, R., 143– 44 South Asian tsunami (2004), 109 South Equatorial Current, 199– 200 Southern Pacific region, 347, 362, 664. See also Osa region Sowerby, George, 99 Special Areas of Conservation, 114 Spight, Tom M., 100, 107, 123 Spongberg, A. L., 155, 156, 596 Springer, M., 77, 633, 665 Standley, P. C., 3, 351, 453– 54, 497 Stanford Oceanographic Expeditions, 100, 168– 69 Steinberg, M., 493 Stergiou, K. I., 156 Stern-Pirlot, A., 153 Stetson, Warren, 364 Stevens, G. C., 256 Stevenson, Robert Louis, 162 Stiles, F. G., 224, 265, 354 Still, C. J., 423 Stockholm Environment Institute, xv Stoner, K. E., 272, 273 Ston Forestal, 371 Stroud Water Research Center, 623 Suárez, E., 100 Suárez-Morales, Eduardo, 594 Süssenguth, Karl, 497 Sustainable Development Goals (SDGs), xv– xvi swamps. See bogs, marshes, and swamps Sweatman, H. P. A., 224 Swimmer, Y., 116 Szelistowski, W. A., 154 Tabash, F. A., 667 Tabash-Blanco, F., 142, 150 Tafur, N., 86 Takhtajan, A. L., 457 Talamancan-Caribbean Biological Corridor, 482 Talamancan Montane Forests Ecoregion, 10, 482. See also cloud forests of the Talamanca Taylor, M., 493

Taylor, William Randolf, 591 tectonics, 31– 32, 32, 43, 44. See also earthquakes; geological regions of Costa Rica Ten Hoopen, G. M., 476 Térraba-Sierpe National Wetland, 120 Terrosi, M., 594 Thiollay, J., 392 Thomas, D. B., 231 Thomas, W. S., 591 Thompson, William, 162 Thornthwaite, C. W., 23, 25, 26 Thrupp, L. A., 345 Thurber, A. R., 118 Tiffer-Sotomayor, R., 355, 356 timber industry, 364– 65, 370– 71, 374, 542, 568 Timber Products Company, 364 Timm, R. M., 272, 273, 437, 558 Tivives Protection Zone, 350 Tokioka, T., 100 Tomlin, J. R. le B., 168 Tonduz, Adolfo, 364 Tosi, Joseph, xv, 8, 65, 365– 68, 375, 500 tourism benefits of, xvii biodiversity loss and, 277 in Central Pacific region, 357– 58 challenges for conservationists and, 403 climate and, 182 in cloud forests of the Talamanca, 477, 478, 483 in cloud forests of the volcanic Cordilleras, 443 conservation and, 568– 69 deforestation and, 308 environmental impact of, 567 fish and, 122 importance of rivers for, 640 Isla del Coco and, 236 local economies in Osa region and, 371 mangroves and, 108 Pacific coast’s human population and, 120 in Parque Nacional Corcovado, 369, 370 pollution and, 608 property development and, 280, 357– 58 sediment loads and, 602– 3 soil health and, 87 turtle watching and, 567 water demands for, 639, 648 Transnational Trust Co., Ltd., 364– 65 Trevithick, Richard, 151 Troll, C., 9 trophic modeling, 149– 50, 150 Tropical Agricultural Research and Higher Education Center (CATIE), xv, 64, 474– 75 Tropical Amphibian Declines in Streams Project (TADS), 629 Tropical Ecology Assessment and Monitoring Network (TEAM), 560 Tropical Science Center (TSC) Caribbean coast conservation efforts and, 608

Subject Index 745 cloud forest conservation and, 443 erosion and, 87 growth of ecosystems knowledge and, xv land use assessments and, 64– 65 in Osa region, 363, 365– 66 San Juan– La Selva Biological Corridor and, 568 Trusty, J., 211, 213– 17 Tsuchiya, M., 197 Tsuda, Roy T., 591 Ugalde, Álvaro, 305, 360, 367, 395 UK Biodiversity Action Plan, 114, 116 Ulate, Vargas, 254 Umaña, G., 665, 667 Umaña, Ronald, 594, 676 UNA. See Universidad Nacional (UNA) UNCLOS. See Law of the Sea of the United Nations (UNCLOS) UNDP. See United Nations Development Programme (UNDP) UNEP. See United Nations Environment Programme (UNEP) UNESCO. See United Nations Educational, Scientific, and Cultural Organization (UNESCO) United Fruit Company, 364, 365, 371, 564 United Nations Conference on Environment and Development (UNCED), 567 United Nations Conference on Sustainable Development (UNCSD, Rio de Janeiro, 2012), xv, 13 United Nations Development Programme (UNDP), xvi, 182, 211 United Nations Educational, Scientific, and Cultural Organization (UNESCO) Amistad Biosphere Reserve and, 499 Man and Biosphere Reserves and, 515 Reserva de la Biosfera La Amistad and, 481 vegetation classification system and, 9, 377 World Heritage Programme of, 165, 181, 184, 193, 236– 38, 280 World Heritage Sites and, 481, 499, 515 United Nations Environment Programme (UNEP), 4– 5 United States, military action in Central America by, 300 Universidad de Costa Rica, 64, 499, 594, 596, 623, 633. See also Centro de Investigación en Ciencias del Mar y Limnología (CIMAR) Universidad Nacional (UNA), xix, 499, 623, 657 Universidad Nacional Autónoma de México (UNAM), 100 University of California, Santa Barbara, 169 University of Delaware, 101 University of Southern California, 168 University of Texas at Austin, 368– 69, 370 USAID (Agency for International Development), 370 US Civil War, 300

US Department of Defense, 366 US Environmental Protection Agency (EPA), 565 US Fish Commission, 231 US Navy Galápagos Expedition, 168 Valdez, Marta F., 594 Vancouver, George, 194 Van Dam, D., 84 Vanderbilt, William K., 99– 100, 168 Van Devender, R. W., 434 Van Leewen, E. M. M., 473 Van Uffelen, J. G., 505 Vargas, J. A., 101, 110, 142, 144– 47, 156 Vargas, R., 169, 594 Vargas-Castillo, R., 102, 169 Vargas-Montero, M., 154 Vargas-Zamora, J. A., 105, 110– 11, 144, 146, 155 Vaughan, C., 80, 247, 345, 375 Vaughan, Thomas Wayland, 596 Veldkamp, E., 84 Verrill, Addison, 99 Vicencio-Aguilar, M. E., 100 Villa, J., 356, 391 Villalobos, A. F., 235 Villalobos, C., 106, 146, 267, 594 Villarreal Orias, J., 265 Vinson, S. B., 247, 271 Víquez, C., 231 Víquez, R., 146, 154 volcanoes, 44 archaeological preservation and, 442 Caribbean lowland soils and, 538 geochemistry of streams and, 636 geological history of Área de Conservación Guanacaste (ACG) and, 291– 93, 294– 95, 320 geological history of Isla del Coco and, 172, 192, 200– 201, 203– 5 geology of Caribbean coast and, 597– 98 lake formation and, 658, 664, 666, 666, 667, 674, 676 national parks and, 443 recent eruptions of, 46, 56, 296, 505 soils of Costa Rica and, 621 techtonic activity and, 622 volcanic edifices and, 37 Volcán Orosí and, 297– 98 See also cloud forests of the volcanic Cordilleras Von Frantzius, Alexander, 3 Von Humboldt, Alexander, 7 Von Wangelin, M., 147 Voss, Gilbert L., 593 Wagner, Moritz F., 495, 497 Wagner, W. H., 462, 497 Walker, William, 300 Wallace, Alfred Russell, 5 Wartzok, D., 595 weather. See climate and weather Webb, L. J., 473– 74

Weber, H., 497, 502 Weber, W. A., 209 Weberling, F., 499, 512 Wedin, D. A., 85 Wehrtmann, I., 10, 106, 118, 149, 153, 594 Wellington, Gerard M. ( Jerry), 593 Wenny, D. G., 438 Wercklé, C., 351 Wercklé, Karl, 3, 7, 457, 497 Werner, T. K., 224 Wescott, David, 370 Wesselingh, R. A., 463 Weston, Arthur S., 497– 98 Weston, J. C., 165 wet forests of Caribbean lowlands African dust clouds, 531 agriculture and pesticide use in, 565 altitudinal and latitudinal migration and, 553, 555, 556 amphibians and, 550– 52 animals of, 545– 58 archaeological sites in, 563 biodiversity in, 539– 40, 550– 53, 555– 56, 561 birds of, 552– 54 changes in forest cover in, 541– 42 climate and weather in, 534– 37, 549 climate change and, 536– 37 climate zones of, 535 coastal beaches and, 537– 38 colonial and postcolonial development in, 534 conservation efforts in, 552, 565– 69 decline of insectivores in, 554 deforestation in, 541– 42 DNA barcoding in research in, 545 fishing in, 550 fish of, 546– 50 frugivory and seed dispersal in, 560– 62 future of, 569 geographic extent of, 527– 29 geography as destiny in, 527 geological history of, 529– 32 geomorphological units of, 539 habitat modification in, 552 herbivory in, 558– 60 historical overview of, 529– 34 Holdridge Life Zones in, 540 human populations and demography of, 532– 34, 563 hunting in, 552 hydrodynamics of, 549– 50 invertebrates of, 546 lack of plants in rivers and streams of, 550 lakes of, 663, 674– 77 Lepidoptera studies in, 560 locations of plant collections in, 540 locust swarm in, 531 mammals of, 554– 58 precipitation in, 538 primates of, 556– 57 protected areas and indigenous reserves in, 530

746 Subject Index wet forests of Caribbean lowlands (continued) recent land use history of, 534 remote sensing for forest studies in, 545, 569 reptiles of, 552 secondary forests and, 543– 45 snorkeling in, 550 soils in, 537– 39 sources of biomass in, 558 transoceanic winds and, 531 variable place names and, 550 vegetation of, 539– 41 water pollution in, 550 See also cloud forests; rain forests wetlands. See bogs, marshes, and swamps; lakes of Costa Rica; rivers of Costa Rica Wetzer, Regina, 594 Weyl, R., 32, 497 Wheeler, W. M., 228 Wheelwright, N., 433, 443 Whitfield, S. M., 551 Whitney, N. M., 170 Whoriskey, S., 116 Wicksten, M. K., 169 Widmer, Y., 469 Wilder, D. D., 231 Wildlife Conservation Society (WCS), 567 Wille, Alvaro, 404 Williams, A. B., 593, 594 Williamson, G. B., 498 Wilms, J., 466, 476 Wilson, D. E., 354 Wilson, Edward O., 3, 7 Wilson, H. V., 177 Winemiller, K., 390, 595, 627, 634 Wirth, W. W., 231

Witter, J., 155 Wolff, M., 146, 147, 148, 150, 153, 154 Woodley, N. E., 231 Woodrow G. Krieger Expedition, 168 Woods Hole Oceanographic Institutions, 100 Wootton, T., 627 World Bank, 567 World Resources Institute (WRI), 193 World War II, 100 World Wide Fund for Nature. See World Wildlife Fund (WWF) World Wildlife Fund (WWF) Biodiversity Support Program and, 193 classification of ecosystems by, 250 cloud forest conservation and, 443 ecosystems recognized by, 499 Isla del Coco and, 193 Parque Nacional Corcovado and, 367 Wright, Alvin, 365, 366 Writki, Klaus, 100 Wujek, D. E., 672 Würsig, B., 170 WWF. See World Wildlife Fund (WWF) Yanoviak, S. P., 433, 434 Yeaton, R. I., 275 York, T. R., 231 Young, B. E., 170 Young, Paul S., 594 Zahawi, R. A., 478– 79 Zamora, Jesús Jiménez, 162 Zamora, N., 8– 10, 254, 260, 347– 49, 351– 54, 468 Zamparo, D., 275

Zimmerman, T. L., 171– 72 Zona Protectora Acuífero Guácimo y Pococí, 530 Zona Protectora Alberto Manuel Brenes, 416 Zona Protectora Arenal-Monteverde, 416 Zona Protectora Cerro Nara, 346, 353, 357 Zona Protectora Cerros de Escazú, 346 Zona Protectora Cerros de Turrubares, 346, 349, 355, 357 Zona Protectora Cuenca del Río Abangares, 416 Zona Protectora Cuenca del Río Banano, 452, 530 Zona Protectora Cuenca del Río Siquirres, 530 Zona Protectora Cuenca del Río Tuis, 452 Zona Protectora El Rodeo, 346, 350, 355, 711 Zona Protectora La Selva, 530 Zona Protectora Las Tablas, 452, 454, 456, 467, 481, 494 Zona Protectora Nara, 711 Zona Protectora Península de Nicoya, 281 Zona Protectora Río Toro, 416 Zona Protectora R. Navarro y R. Sombrero, 452, 466, 481 Zona Protectora Tortuguero, 530 Zona Protectora Turrubares, 711 Zona Protectora Volcán Miravalles, 416 Zonneveld, I. S., 9 Zoological Society of New York, 100. See also Wildlife Conservation Society (WCS)

Systematic Index of Common Names

Page numbers in italics refer to figures and tables. English Common Names acacia, 274. See also specific species of acacia acacia ant, 338 acorn woodpecker, 466 acridid, 559 African grass, 300, 302, 303, 307, 332, 334, 713 Africanized honeybee, 335– 36 African oil palm, 354, 401 agaric, 458 agariciid, 175 agave, 429 agouti. See Central American agouti ahermatypic coral, 710 alder, 75, 458, 506, 718. See also specific species of alder alga, 100, 101, 102, 105, 107, 111, 121, 147, 150, 154, 155, 168, 173, 175, 218, 509, 591, 593, 605, 624– 26, 627, 629, 632, 634– 35, 636, 709, 711, 720– 21, 722. See also specific species of alga Allen’s salamander, 391 almond, 196. See also specific species of almond Amazon sword plant, 721 amblyopinine beetle, 440 ambrosia beetle, 228– 229 ameiva, 392. See also specific species of ameiva American crocodile, 354, 356, 552, 722 American eel, 546, 547 American oil palm, 377 amphibian, 434– 35, 463, 550– 52, 627, 628– 29, 684, 686, 696, 712, 715, 719, 720, 722 amphioxus, 153 amphipod, 105, 167, 168, 170, 600, 672. See also specific species of amphipod anchovy, 148 Andean alder, 478 angiosperm, 111, 531 anglerfish, 148, 149. See also specific species of anglerfish anguid, 552 anhinga, 267, 354, 630 annelid, 119 anole, 552, 715. See also specific species of anole anole lizard, 267, 435 anoline lizard. See anole lizard 747

anomuran crab, 594 ant, 75, 77– 78, 228, 271, 321, 361, 386– 88, 387, 388, 389, 433, 439, 440, 545, 561, 712, 713, 715, 719. See also specific species of ant ant acacia, 338, 387 antbird, 392, 715. See also specific species of antbird anteater, 555, 715 ant-follower, 554 ant-tanager, 392, 394, 554, 715. See also specific species of ant-tanager ant-thrush, 394. See also specific species of ant-thrush antvireo, 554 antwren, 393, 554. See also specific species of antwren anuran, 719 apatelodid, 560 aphid, 269 apple, 477, 478, 479 aquatic bird, 266, 354, 355 aquatic grass, 623, 721 aracari, 561– 62 arachnid, 232 arbuscular mycorrhiza, 76, 440, 545 Arenal rivulus, 268 ark clam, 151, 151, 152– 53 armadillo, 277, 532, 555, 562, 715. See also specific species of armadillo army ant, 321, 327, 328, 394, 433 aroid, 216, 696, 718 arrow worm, 147, 148 arthropod, 153, 227, 235, 266, 433– 34, 465, 552, 558, 719 artiodactyl, 262, 712 ascidian, 100, 107 Atlantic grunt, 547, 548 atyid, 632. See also specific species of atyid Australian pine, 478 avocado, 68, 73, 461, 471– 72, 472, 482, 553 azooxanthelate, 175, 710 bacteria, 596, 711. See also specific species of bacteria bactroid, 559 Baird’s tapir, 262, 263, 277, 279, 337, 395, 397– 98, 467, 473, 482, 511, 559, 712, 719

balsa, 380 bamboo, 461, 468, 469, 500, 500, 511– 12, 514, 515, 672, 685, 686, 718, 719, 720, 721 banana, 65, 66, 68, 77, 79, 83, 85, 196, 303, 347, 354, 364, 377– 78, 379, 379, 401, 541, 542, 543, 549, 557, 563, 564– 65, 567, 646, 647, 647, 677, 716. See also specific species of banana banded peacock, 270 banded tetra, 268, 269, 276, 547, 548, 549, 722 band-tailed pigeon, 466 barbet, 439. See also specific species of barbet bare-crowned antbird, 554 bark beetle, 228– 29 barnacle, 106, 107, 143, 146, 147, 173, 594, 709 barred cat-eyed snake, 392 basidiomycete, 559 basidiomycotic fungus, 209 bass, 269. See also specific species of bass bat, 262, 264– 65, 271, 272, 273, 329, 330, 332, 338, 354, 384, 437, 439, 464, 466, 467, 471, 545, 555, 557, 562, 712, 713, 715, 719, 722. See also specific species of bat bay-headed tanager, 394 bean, 66, 75, 78, 85– 86, 196, 303, 361, 461, 477, 533. See also specific species of bean bear, 5 beard lichen, 459 bee, 271– 72, 311, 384, 439, 712, 713, 719. See also specific species of bee beet, 477, 479 beetle, 228, 269– 70, 272, 273, 323, 384, 439, 440, 545, 560, 712, 713, 719. See also specific species of beetle bellbird, 439, 443– 44. See also specific species of bellbird benthic alga, 143, 637 benthic fauna, 100, 153, 505, 672 benthic macroalga, 172 benthos, 110, 116– 19, 142, 143, 145, 153, 177, 183, 666, 710, 711 bicolored antbird, 394, 554 bigeye thresher shark, 170 bigmouth sleeper, 389, 546, 547, 548

748 Systematic Index of Common Names bird, 231, 332, 355– 56, 392– 94, 435– 37, 439, 443– 44, 465– 66, 471– 73, 476– 77, 483, 531, 545, 552– 54, 630, 632, 663, 691, 692, 700, 712, 715– 16, 718, 719, 720, 722. See also specific species of bird bivalve, 108, 117, 145, 147, 151, 153, 594, 600, 710, 711. See also specific species of bivalve black-and-yellow silky flycatcher, 439 black-bellied whistling duck, 266– 67 blackbelt cichlid, 546, 547 blackberry, 477, 479 black-billed nightingale-thrush, 511 black cambute, 153 black-cheeked ant-tanager, 392, 394, 715– 16 black-cheeked warbler, 511 black coral, 118, 593, 608, 710 black-faced ant-thrush, 394 black-faced grosbeak, 554 black-faced solitaire, 439, 466 blackfin snook, 547 black guan, 466, 476 black-handed spider monkey, 399, 716 black hawk, 386 black-headed bushmaster, 357, 391, 392, 712, 715 black-headed trogon, 266 black iguana, 268 black mangrove, 108, 143– 44 black noddy, 222 black rat, 193– 94, 224 black river turtle, 636 black sea turtle, 106, 220 black sea urchin, 593, 594, 607 black-speckled palm pit viper, 465 black-striped woodcreeper, 393 black-thighed grosbeak, 466 black vulture, 266 black wood turtle, 558 blue crabs, 147, 153, 232, 235 blue-crowned manakin, 393 blue green (alga), 624, 634, 720– 21 blue-winged teal, 266 boa, 392. See also specific species of boa boat-billed heron, 664 boatman. See specific species of boatman boat-tailed grackle, 303 boid, 552 bolete, 458 booby, 170. See also specific species of booby bottlenose dolphin, 169, 595 bovid, 51 brachiopod, 145 brachyuran crab, 147, 169, 594 bregmacerotid, 148 brittle star, 110 brocket deer, 719 bromeliad, 213, 216, 257, 275, 466, 470, 633, 686, 686, 713– 14, 717, 718, 721. See also specific species of bromeliad brown booby, 222 brown-capped vireo, 466

brown cattle, 303 brown jay, 435– 36, 719 brown noddy, 222, 225 brown rat, 224, 225 brown seabird, 170 brown shrimp, 153 brown-throated three-toed sloth, 277, 558 brown wood turtle, 558, 636 bruchid, 269 brush-footed butterfly, 270 bryophyte, 211, 212, 256, 431, 458, 462– 63, 466, 509– 10, 511, 512– 13 bryozoan, 100, 168 buff-throated foliage-gleaner, 554 buffy tufted-cheek, 466 bug, 269, 313, 559, 712. See also specific species of bug bull, 302 bullet ant, 387– 88, 388 bull horn acacia, 713 bull rain frog, 392 bull shark, 389, 546, 547 bulrush, 257, 701 bumblebee, 463, 469, 511, 719 bunch grass, 721 burrowing sea urchin, 593 bushmaster, 392. See also specific species of bushmaster bush tanager, 439 butterfly, 227– 28, 229– 30, 269, 270, 272, 314, 323, 326– 27, 379, 383– 85, 383– 84, 386, 433– 34, 439, 443– 44, 531, 545, 546, 560, 712, 719 cabbage, 477, 479 cacao, 78, 534, 541 cacique, 554. See also specific species of cacique cactus, 252, 256, 259, 275, 712 caddisfly, 633, 722 caecilian. See cecilian caesalpinoid, 273 caiman, 552, 629– 30, 634, 691– 92, 722. See also specific species of caiman calabash, 274, 275 calanoid, 148, 594 callichthyid, 546 camel, 532 camelid, 51 canid, 51, 262, 712 cantaloupe, 68 cantil snake, 267, 267 capuchin. See white-faced capuchin monkey carangid, 148, 149 Caribbean anole, 552 carnivore, 106, 107, 147, 149, 171, 265, 269, 293, 354, 466, 532, 554, 556, 636 carrot, 477, 479, 564, 565 cashew, 73, 196, 377 cassava, 303, 533, 534, 564 cat, 196, 220, 226, 262, 364, 394, 555, 712, 715. See also specific species of cat caterpillar, 275, 559

catfish, 148, 149, 268, 389, 546, 547, 548, 628. See also specific species of catfish cattail, 257, 280, 659, 661, 701, 721 cattle, 73, 80– 81, 81, 86, 255, 257, 262, 274, 276, 279, 280, 300, 302, 303, 303, 304– 5, 306– 7, 311, 331, 332– 33, 338, 347, 354, 364, 443, 477, 514, 541, 567, 621– 22, 646, 647, 647, 659, 662, 663, 666, 702. See also specific species of cattle cattle egret, 220, 267 cauliflower, 477, 479 Cauque River prawn, 233– 34 cebus monkey, 264 cecilian, 392, 434, 550, 715 celery, 479 Central American agouti, 79–80, 80, 260, 265, 274, 329– 30, 400, 467, 555, 562, 698 Central American spider monkey, 559 Central American squirrel monkey, 265, 354, 379, 394, 395, 399, 400, 403, 712, 716 centrolenid, 715 cephalochordate, 101, 110 cephalopod, 154, 168, 592, 594 cervid, 51 cetacean, 102, 116, 154 Chacoan peccary, 395 chaetognath, 102, 148, 604, 711 characid, 268, 390 characin, 268, 546 charadriiform bird, 145 chayote, 565 checker-throated antwren, 393, 554 chestnut-backed antbird, 393 chestnut-capped brushfinch, 476 chestnut-mandibled toucan, 355, 554 chestnut-sided warbler, 394 chicken, 196 chili pepper, 71, 361 chilopod, 235 chimaeroid, 103 chironomid, 657, 665, 666, 672 chiton, 107, 153, 592 chlorophyte, 665, 667, 672, 675, 676, 690, 721 chrysophyte, 672, 676 chytrid, 434, 551, 629, 719 cicada, 269. See also specific species of cicada cichlid, 268, 389, 390, 463, 546, 547, 548, 549, 550, 628, 628, 630, 649, 667, 692, 722. See also specific species of cichlid citrus, 73 cladoceran, 665, 666, 667, 675, 676– 77 clam, 33, 117, 118, 151, 153, 364. See also specific species of clam Clark’s coral snake, 392 clingfish, 546, 548. See also specific species of clingfish clinostomatid, 634 clubmoss, 211, 213, 509 cnidarian, 100, 149, 593 coati, 264, 332, 386, 400, 562. See also specific species of coati

Systematic Index of Common Names 749 cocoa, 66, 68, 196 cocoa woodcreeper, 394 coconut, 194, 196, 214, 215, 273, 364, 377, 714 coconut palm, 194, 196, 214– 15, 364, 714 Cocos atyid, 235 Cocos clingfish, 220 Cocos cuckoo, 222, 223 Cocos finch, 222– 23, 224, 226 Cocos flycatcher, 222, 224 Cocos gecko, 220, 222, 226 Cocos goby, 220 Cocos lizard, 220, 221, 226 Cocos orange land crab, 233 Cocos prawn, 234– 35 Cocos sleeper, 220 cod, 148 coelenterate, 168 coffee, 64, 68, 71, 77, 78, 150, 196, 303– 4, 351, 352, 358, 377, 443, 477, 478, 479, 483, 563, 564, 621 coliform bacteria, 155 collared peccary, 264, 264, 277, 332, 395, 400, 401, 437, 467, 558, 559, 562, 719 collared redstart, 438, 466 collared trogon, 466 colubrid, 715 common noddy, 222, 225 common northern raccoon, 466 conger, 148, 149, 711 conifer, 461, 469 convict cichlid, 268, 547, 548, 549, 550 copepod, 110, 144, 147, 593, 594, 604, 660, 666, 667, 672, 675, 677, 711, 721 coral, 100, 102– 3, 104, 109, 111– 14, 112, 120– 21, 120, 123, 165, 168, 169, 171, 172, 175– 76, 178– 79, 179, 180, 181, 591, 593, 595, 596, 597, 598, 601, 602– 3, 603, 604, 604, 605, 605, 606, 607, 608– 9, 710. See also specific species of coral coralline alga, 100, 113, 603, 605 corallivore, 102, 114, 176, 710 coreid, 384 corn, 86, 196, 303, 361, 477, 533, 565 corvid, 435 cotinga, 355, 553 cotton, 71, 276, 303, 361 cotton boll weevil, 329 cotton rat, 277 cotton-tail rabbit, 264, 277 cougar, 467, 482 cow, 467 coyote, 264, 277, 332, 333, 437, 466, 557, 719 crab, 75, 79, 80, 105, 144, 146, 149, 174, 215, 232, 395, 593, 632, 634. See also specific species of crab crab-eating raccoon, 355, 355 crab hawk, 386 creek tetra, 269, 276, 547 crested eagle, 355, 394 crested guan, 265, 393, 466

crinoid, 593 croaker, 154 crocodile, 268, 356– 57, 357, 388, 552, 629– 30, 634, 663, 692, 699, 712, 715, 722. See also specific species of crocodile crown-of-thorns starfish, 176, 710 crustacean, 100, 101, 102, 103, 110– 11, 118, 144– 45, 146, 147, 149, 153, 154, 155, 168, 171, 177, 233, 388, 593, 594, 630, 632, 710, 712– 13 crustose lichen, 459 cryptogamic epiphyte, 476 cryptophyte, 666, 721 ctenosaur, 268, 303, 332, 531 cuckoo, 222, 223, 394, 554. See also specific species of cuckoo cumacean, 110, 594, 600 curassow, 466. See also specific species of curassow cutlass fish, 148 Cuvier’s beaked whale, 169 cyanobacterium, 119, 154, 440, 624, 666, 667, 672, 675, 676, 721 cyanophyte, 660, 721 cyclanth, 461 cyclopoid, 667 cypress, 478. See also specific species of cypress damselfish, 114, 595 damselfly, 633 dark-eyed leaf frog, 392 Darwin’s finch. See Cocos finch dasypodid, 51 decapod, 116– 17, 146, 153, 154, 600 decapod crustacean, 144, 145 deer, 75, 260, 555, 715. See also specific species of deer dendrobatid, 551 desmid, 666, 721 detritivore, 144, 639 devilfish, 168, 628 diatom, 142– 43, 146, 147, 154, 506, 509, 624, 626, 626, 637, 657, 663, 664, 666, 668, 669, 670, 672, 674, 676, 677, 721, 722 Dice’s cottontail rabbit, 466 dicot, 460, 461, 462, 468, 509, 510, 668 dink frog, 686, 721 dinoflagellate, 146, 150, 154, 509, 711 dinosaur, 290 diplopod, 235 dipterocarp, 374, 714 dismorphiine butterfly, 386 diurnal butterfly, 227, 230 dog, 196, 437 dolphin, 170, 710. See also specific species of dolphin domestic cat, 224 domestic pigeon, 221 donkey, 151 dotted-winged antwren, 393, 554 dragonfly, 269, 633, 712, 722

drosophilid, 438 drum, 154 duck, 265, 691, 692, 700, 701, 722. See also specific species of duck dung beetle, 546 dusk-faced tanager, 554 dwarf palm, 467, 719 eagle, 355, 393, 394, 716. See also specific species of eagle eared seal, 219 eared watermoss, 691 earless lizard, 392 earthworm, 75, 78– 79, 79 echinoderm, 100, 101, 116– 17, 145, 146, 149, 165, 168, 169, 171, 594, 595 echnoid, 177 ectomycorrhizal fungus, 257 ectosymbiont bacteria, 118 edentate, 262, 712 eel, 451. See also specific species of eel egret, 265, 266. See also specific species of egret eleotrid, 390, 634 elephant ear tree, 274 elephantid, 51 elkhorn coral, 607 emerald toucanet, 435, 466, 476 engraulid, 148 entomofauna, 227, 231 epibenthos, 149 epiphyllic lichen, 208– 9 epiphyllous bryophyte, 211, 428, 431 epiphyte, 275, 377, 429, 431– 32, 433, 438, 439, 440– 41, 441, 442, 455, 457, 459, 460, 461– 62, 463, 466, 468, 469, 470, 475, 476, 500, 539, 593, 712, 717, 718. See also specific species of epiphyte equid, 51 ericad, 513, 685, 718 euagaric, 458 euglenophyte, 667 euglossine bee, 271 eukariotic, 509 euphausid, 604, 711 euryhaline alga, 625 eyelash pit viper, 392 falcon, 355. See also specific species of falcon false killer whale, 169, 170 false vampire, 264– 65 fat sleeper, 269, 389, 547 felid, 51 feline, 354 feral pig, 224, 227 fer-de-lance, 357, 712 fern, 9, 68, 210, 211, 213, 215, 216, 275, 347– 48, 377, 431, 460, 462, 468, 469, 509, 510, 513, 531, 539, 685, 686, 718, 719, 720, 721. See also specific species of fern fern-ally, 509, 510 fiddler crab, 145

750 Systematic Index of Common Names fiery-billed aracari, 355 fig, 722. See also specific species of fig fig wasps, 272, 438 filmy fern, 428, 432, 718 finch, 222, 224, 226, 230, 439, 554, 719. See also specific species of finch finescale sleeper, 268 finfoot, 630 firefly, 269 fish, 149, 183, 388– 91, 390, 463, 546– 50, 558, 561, 595, 606, 627– 28, 630, 632, 634– 35, 634, 637, 639, 642– 43, 644– 45, 657, 664, 665, 666, 667, 672, 692, 693, 700, 710, 711, 712, 715, 719, 722. See also specific species of fish fishing bat, 630 flagellate, 147, 155 flamboyant, 273 flame-throated warbler, 466, 511 flame tree, 273 flatfish, 148, 149, 389 flatworm, 119, 268, 275, 596, 609 flea, 384, 440 flea beetle, 560 flounder, 148, 149, 547, 626, 711 fly, 232, 275, 323, 384, 438, 439, 719. See also specific species of fly flycatcher, 554. See also specific species of flycatcher foliicolous lichen, 460 foliose lichen, 466 foraminifer, 110, 147 forb, 721 forest rabbit, 437, 559 four-footed butterfly, 270 fowl, 196, 451, 691, 692, 700, 701, 702, 722. See also specific species of fowl fox, 265, 277, 466. See also specific species of fox freshwater prawn. See freshwater shrimp freshwater shrimp, 271 frigatebird, 170. See also specific species of frigatebird frog, 463, 465, 473, 545, 550, 551, 628, 629, 629, 715, 719, 722. See also specific species of frog frog lung fluke, 275 fruticose lichen, 459, 460, 718 fungus, 208– 9, 209, 509, 634, 638– 39, 713, 718, 720. See also specific species of fungus fur seal, 101, 219 Galápagos sea lion, 169 gar, 547 gastropod, 101, 106, 107, 123, 168, 173, 233, 592, 594, 595, 600 gecarcinid, 385– 86 gecko, 552. See also specific species of gecko Geoffroy’s spider monkey, 262, 277, 399– 400, 437, 482, 556– 57, 712, 716, 719 geometrid, 560 geonomid, 559 ghost crab, 232

giant anteater, 5, 262, 265, 277, 331, 437, 555 ginger, 696 gladiator frog, 391, 392 glass frog, 551, 628, 715 glass headstander, 268, 547 glass sponge, 169, 172 glyptodont, 50, 51, 293 glyptodontid, 51 gmelina, 334– 35, 402 gnatwren, 554 goat, 194, 196, 224, 225– 26, 467 gobiid, 148 goby, 148, 149, 389, 548, 711. See also specific species of goby Godman’s montane pit viper, 465 golden alga, 509 golden-crowned spadebill, 552 golden-hooded tanager, 394 golden toad, 6, 434, 629, 719 Golfo Dulce poison dart frog, 391 gomphoteriid, 51 gomphothere, 274, 293, 532 gopher, 555. See also specific species of gopher gourd, 361 grackle, 303. See also specific species of grackle granulated poison dart frog, 391 grass, 71, 196, 211, 218, 249, 255, 269, 276, 296, 299, 300, 301– 2, 302– 3, 306, 306, 307, 308, 311, 314, 332– 35, 460, 492– 93, 500, 507, 512– 15, 531, 591, 602, 623, 659, 664, 668, 685– 87, 689, 699, 701, 713, 719, 721. See also specific species of grass grasshopper, 433, 559 gray fox, 265, 277 great ape, 263– 64 great curassow, 265, 355, 393, 400 great egret, 267. See also great white egret greater bulldog bat, 630 great frigatebird, 222 great green macaw, 8, 554, 567, 568– 69, 568, 569 great tinamou, 466 great white egret, 692, 693, 722. See also great egret green alga, 113, 173– 74, 509, 624 green bean, 565 green-black poison dart frog, 392 green clam, 700 green frog eaters, 434– 35 green heron, 692, 693, 722 green ibis, 630 green iguana, 268, 552, 558, 712 green keelback, 435 greenlet, 393, 554. See also specific species of greenlet greenlet-honeycreeper, 554 green spiny lizard, 464, 465, 511, 719, 720 green tree, 257 green turtle, 122, 566– 67, 591, 600– 601, 601, 609, 709 grey-headed tanager, 394 grey teak, 377

grosbeak, 554. See also specific species of grosbeak ground sloth, 50, 274, 293, 532, 533 grunt, 389 guan, 400. See also specific species of guan guapote, 390, 667, 675 guinea fowl, 196 gull, 170. See also specific species of gull Guyana dolphin, 595 gymnophthalmid, 552 gymnosperm, 468 hammerhead shark, 170 harlequin frog, 629, 719 harlequin toad, 356 harpy eagle, 393, 394, 716 harvestman, 231 harvest mouse, 262, 437, 438, 440, 719 hawk, 386, 466, 511, 720. See also specific species of hawk hawk moth, 229– 31, 270, 272 hawksbill sea turtle, 106, 220, 600, 709 headstander, 268, 547. See also specific species of headstander helminth, 275 hemichordate, 145 hemiepiphyte, 429, 431, 432, 462, 718 hemiparasite, 462 hepatic, 211, 256, 458, 463, 685 herb, 539, 687, 691, 696, 718, 719 herbaceous vine, 374, 460 hermatypic coral, 114 hermit, 232– 33, 393. See also specific species of hermit hermit crab, 232– 33 heron, 265, 266. See also specific species of heron herpetofauna, 391– 92, 434 hesperiid, 270 heterokont alga, 509 heteromyid, 562 heteropod, 604, 711 heterotrophic parasite, 462 highland alligator lizard, 464, 465, 719 highland yellow-shouldered bat, 467 hispid cotton rat, 300 Hoffmann’s two-toed sloth, 277, 558– 59 hog mullet, 548 hognose pit viper, 392 hogplum, 377 holothurian, 169, 593 honeybee, 271 honeycreeper, 554. See also specific species of honeycreeper hornworm, 270 hornwort, 463 horse, 51, 274, 293, 300, 303, 304, 305, 306, 333, 338, 467, 514, 532 house gecko, 552 howler monkey. See mantled howler monkey hummingbird, 230, 266, 272, 275, 384, 438– 39, 443– 44, 469, 553, 719. See also specific species of hummingbird

Systematic Index of Common Names 751 humpback whale, 169, 170 hyacinth, 249, 257, 258, 623, 659, 721. See also specific species of hyacinth hydrochoerid, 51 hydroid, 593 hylid, 551 hyperiid amphipod, 170 hyperparasitoid wasp, 275 ibis, 265. See also specific species of ibis ichthyoplankton, 220, 595 ichtyofauna, 722 iguana, 268, 552, 558, 712. See also specific species of iguana iguanian lizard, 276 immaculate antbird, 554 infauna, 105, 145, 593, 710 insect, 269– 71, 315, 323– 28, 384, 386– 88, 439, 462, 463, 469, 471, 473, 511, 627, 632, 633, 634, 634, 635, 637– 39, 667, 712, 713, 719, 720, 722. See also specific species of insect insect grazer, 635 insectivorous bat, 265 invertebrate, 77, 100, 102, 106– 7, 110– 11, 114, 117, 119, 143, 145, 147– 48, 153– 55, 169, 227– 35, 269– 71, 385– 86, 389, 396, 463, 511, 545– 46, 559– 60, 565, 596, 600, 623, 627, 629– 30, 632– 33, 635, 636, 638– 39, 693, 709, 722 iron stick tree, 194 isopod, 143, 145, 594, 600 Isthmian alligator lizard, 391, 392 Isthmian rivulus, 547, 548 ithomiine butterfly, 386 jabiru stork, 692, 693, 712, 722 jacana, 265, 630, 722 jaguar, 262, 277, 305, 354, 366, 395, 396, 398– 99, 401, 404, 437, 467, 482, 557, 712, 715, 716 jaguar cichlid, 546, 547 jaguarundi, 262 jay, 473. See also specific species of jay junco, 511. See also specific species of junco kapok, 374 keelback, 435. See also specific species of keelback keel-billed toucan, 554 Kentucky warbler, 394 kikuyu grass, 71, 86 killifish, 549– 50. See also specific species of killifish kingfisher, 266, 630, 722 king vulture, 355 kinkajou, 557, 562 kinorhynch, 117, 144 kite, 466. See also specific species of kite knifefish, 268, 547, 548 lancelet, 144 land crab, 231, 232, 373, 385– 86, 715

large-footed finch, 466, 511 large-spot tetra, 548, 549 leaf beetle, 269 leaf-cutter ant, 78, 78, 271, 273, 559, 713 leafhopper, 231 leaf-miner, 559 leaf-mining beetle, 559 leatherback sea turtle, 106, 106, 220, 268, 567, 595, 600, 608, 709 leather fern, 688 legume, 272 lemon, 196 leporid, 51 leptodactilyd quark frog, 464, 482 lesser bulldog bat, 630 lesser greenlet, 554 lettuce, 721. See also specific species of lettuce liana, 213, 253, 256, 257, 272, 275, 383, 431, 432, 439, 469, 715, 719 lichen, 208– 9, 218, 440, 458– 60, 466, 476, 500, 509, 511, 512, 513, 685, 686, 718, 719, 720, 721. See also specific species of lichen lightning beetle, 269 lightning bug, 313 lily, 663, 721. See also specific species of lily limacodid, 560 limpet, 107, 634 lithodid crab, 118 little tinamou, 355 littorinid gastropod, 147 littorinid snail, 144 livebearer, 268, 546, 550 liverwort, 209, 211, 463, 476, 509– 10, 512, 513, 718, 719, 720. See also specific species of liverwort lizard, 264, 465, 473, 552, 715, 719. See also specific species of lizard lizardfish, 148 lobster, 146, 594. See also specific species of lobster locust, 531 loggerhead turtle, 600, 709 longhorn beetle, 269 long-tailed hermit, 393 long-tailed manakin, 265, 435, 436– 37 long-tailed weasel, 467 louse, 174. See also specific species of louse lycaenid, 270 lycophyte, 531 macaw, 8, 266– 67, 355, 356, 371, 393, 401– 2, 554, 567– 69, 568, 569, 716. See also specific species of macaw machaca, 547, 635, 675 macroalga, 114, 115, 119, 172, 593, 603, 710 macrobacteria, 117, 118 macrofauna, 102, 110, 144– 45, 635, 665 macroinvertebrate, 117, 271, 565, 629, 633, 636 macrolichen, 459

macrophyte, 623, 659, 661, 663, 665, 669, 672, 675 maërl, 114, 116 magpie jay, 303, 338 mahi-mahi, 116 mahogany, 259, 276, 305, 482 maize, 85– 86, 276, 533, 661, 664, 669, 677, 678 mammal, 394– 400, 437, 439, 443– 44, 466– 67, 473, 531, 630, 632, 696, 712, 715, 719, 720 mammutid, 51 manakin, 266, 393, 435, 436– 37. See also specific species of manakin manatee, 265, 567, 608, 696, 710, 716, 722. See also specific species of manatee manatee grass, 602 manefish, 171 mango, 68, 73, 534 mangrove, 9, 10, 12, 66, 67, 97, 101, 102, 103, 108– 9, 108, 112, 113, 120, 139, 142, 143– 44, 147, 148, 149, 151, 153, 215, 252, 256, 265, 299, 308, 354, 355, 373, 375, 376, 377, 394, 531, 595, 596, 599– 600, 600, 608, 609, 696, 697, 710. See also specific species of mangrove manioc, 196, 533 manta ray, 178 mantis shrimp, 146 mantled howler monkey, 260, 264, 265, 279, 399, 556– 57, 558, 716, 719 many-scaled anole, 392 marbled swamp eel, 268, 547, 548 margay, 262, 467, 482, 511, 719, 720 marine mammal, 6, 169, 219 marine Pacific snake, 221 marine turtle, 268, 608, 709 marlin, 178 marsupial, 262, 555, 712, 715 masked booby, 222 masked tree frog, 392 mastodon, 51, 55, 533 mayfly, 633, 722 mealy amazon, 355 mealy parrot, 393 medusa, 100, 167, 168 megafauna, 274, 293– 95, 297, 304, 305, 329, 337– 38, 361, 532– 34, 713 megalonychid, 51 megatheriid, 50, 51, 51 meiofauna, 101, 102, 110, 144– 45, 635 melastome, 216 melon, 71, 276, 336 merry widow, 547, 548 metalmark, 270 Mexican cypress, 478 Mexican hairy porcupine, 466, 558– 59 Mexican tree frog, 392 mice, 79– 80, 265, 466, 467, 472– 73, 555, 715. See also specific species of mice microalga, 142, 146 microarthropod, 77, 432 microcrustacean, 667

752 Systematic Index of Common Names microdinosaur, 290 midas cichlid, 546, 547 mimosoid, 253, 272 mistletoe, 438 mite, 440 mold, 458. See also specific species of mold mollusk, 100, 101, 102, 103, 107, 110, 116– 17, 120, 145– 46, 149, 151, 152, 153, 155, 165, 167, 168, 169, 170, 275, 305, 388, 511, 552, 592, 593, 594, 609, 632, 693, 710, 715, 720 molly, 268, 547, 548 monarch butterfly, 327 mongoose, 336 monkey, 438, 471, 556, 719. See also specific species of monkey monocot, 460– 62, 468, 509, 510, 544 montane alligator lizard, 511, 720 moray, 148, 149, 711 mosquito, 231, 556 mosquito fish, 548 moss, 209, 211, 218, 431, 463, 464, 469, 476, 479, 500, 506, 509– 10, 512, 513, 515, 686, 718, 719, 720, 721. See also specific species of moss moth, 231, 265, 269, 270, 271, 272, 314, 323– 26, 330, 384, 545, 712, 713. See also specific species of moth motmot. See specific species of motmot mountain lion, 437, 467, 511 mountain mullet, 220, 269, 389, 547, 548, 645 mountain salamander, 464, 482 mountain thrush, 466 mountain tree frog, 464, 482 mourning warbler, 394 mouse. See mice; and specific species of mouse mud shrimp, 594, 604 mule, 331 mullet, 220, 269, 389, 547, 548, 645. See also specific species of mullet murex, 152, 152, 153 muricid snail, 152 murid, 437 Muscovy duck, 267, 276, 355 mushroom, 257, 458, 459 mushroom-tongue salamander, 511, 720 mussel, 117 mustelid, 555 mycorrhizal fungus, 75, 76, 334, 713 myctophid, 148 mylodontid, 50, 51, 51 myriapod, 235 mysid, 147 mytilid bivalve, 33, 117 myxogastrid, 458 Nearctic migrant warbler, 554 nematode, 110, 223, 276, 511, 546, 600, 665 nemertean, 119, 593, 600 Neotropical otter, 557 neritid, 389 neuston, 169

Nicaraguan seed-finch, 553 nightingale-wren, 552 night monkey, 557 Nile tilapia, 692 nine-banded armadillo, 467 noddy. See specific species of noddy Northern barred woodcreeper, 394, 554 northern jacana, 276, 354 Northern raccoon, 557 Northern waterthrush, 394 nudibranch, 103 nymphalid, 270 oak, 81, 257, 293, 377, 429, 458– 61, 462– 64, 464, 465– 67, 469, 471– 75, 474, 478, 482, 500, 506, 515, 686, 718, 719. See also specific species of oak ocellated antbird, 394, 554 ocelot, 262, 263, 467, 482, 511, 557, 686, 719, 720 ochraceous wren, 466 ochre-bellied flycatcher, 393 ochrophyte, 509 octocoral, 102, 103, 171, 172, 593, 710 odonate, 666 oil palm, 66, 68, 358, 364, 377– 78, 379 oligochaete, 155, 600, 665 olive ridley sea turtle, 106, 220, 268, 280, 709 olive tanager, 554 olomina, 268, 547, 548 omnivore, 149, 389, 553– 54, 556, 635 onion, 477, 479 onuphid polychaete, 156 onychophoran, 78 ophiidid, 148 ophiuroid, 116, 149, 153 opossum, 262, 265, 277, 332, 386, 532, 562. See also specific species of opossum orange, 196, 336, 534 orange-billed sparrow, 554 orbatid, 666 orchid, 211, 213, 275, 335, 438, 460, 461, 462, 515, 686, 718 oriole, 222, 265. See also specific species of oriole orthopteran, 560 Osa cecilian, 391 ostracod, 110, 147, 660 otariid, 170, 219 otariid seal, 194 otter, 630, 644. See also specific species of otter owl, 311 oyster, 151– 52 paca, 196, 265, 400, 437, 467, 555, 562, 719 Pacific fat sleeper, 269 palaemonid, 632 palm, 9, 12, 68, 73, 211, 213, 260, 315, 336, 368– 69, 377, 398, 429, 461, 477, 479– 480, 515, 533, 534, 539, 559, 562, 564, 598, 690, 694– 696, 694– 95, 699,

710, 713, 715, 719, 721. See also specific species of palm palm weevil, 379 palo verde, 690, 692 pampathere, 50 Panamanian fiddler crab, 232 pandalid shrimp, 153 panther, 567 papaya, 76, 303 paper wasp, 271 papilionid, 270 parasite, 269, 462. See also specific species of parasite pargo, 390 parrot, 392, 715. See also specific species of parrot passerine, 276 passion-vine butterfly, 383 pastel cichlid, 268, 547, 548 peach, 534 peach palm, 83, 377, 477, 479 peanut, 303, 533 peanut-head bug, 559 peanut worms, 146 peat moss, 463, 505, 514 peccary, 262, 263, 555, 558, 562, 696, 712, 715, 716. See also specific species of peccary pectinidid bivalve, 168 pelagic thresher shark, 170 pelecypod, 592 penaid shrimp, 144, 146, 150, 153, 154 pennatulid, 593 pepper, 68. See also specific species of pepper peregrine falcon, 355 phorophyte, 462 phyllostomid, 273 phytobenthos, 143, 149 phytoplankton, 103, 104, 113, 114, 120, 121, 142, 143, 146– 47, 148, 149, 509, 595, 660, 665, 666, 672, 675, 676, 690, 711, 721 pierid, 270, 327 pig, 194, 196, 207– 8, 221, 225, 226, 364, 477, 514. See also specific species of pig pigeon, 221, 466. See also specific species of pigeon pike killifish, 546, 547 pimelodid, 546 pine, 478. See also specific species of pine pineapple, 73, 303, 347, 541, 542, 543, 564, 568, 646, 647, 647 pink shrimp, 153, 594 pinniped, 219 pipefish, 268, 389, 546, 548 piper, 630 piratic flycatcher, 553 pit viper, 357, 712 plain-brown woodcreeper, 554 plain-colored tanager, 553, 554 plain xenops, 554 plankton, 100, 101, 102, 104, 116, 149, 169, 199, 592– 93, 656, 657, 667, 672, 710

Systematic Index of Common Names 753 planktonic microalga, 146 plantain, 534, 564 plum, 477, 479 pocilloporid, 710 pocket gopher, 79– 80, 354 podocarp, 468 poeciliid, 268, 269, 390, 463 pogonophoran, 117 poison dart frog, 392 polychaete, 101, 102, 103, 105, 110, 110, 116, 118, 144– 45, 146, 147, 149, 153, 155, 156, 168, 593, 595, 600, 710. See also specific species of polychaete polyplacophoran, 594 porcellanid crab, 106, 146, 709 porcupine, 79, 264, 555. See also specific species of porcupine portunid crab, 146 potato, 71, 477, 478, 479 poultry, 364 prawn, 108, 233– 34, 235, 389, 710, 713, 715. See also specific species of prawn primate, 262, 354, 394, 399, 400, 532, 555, 556, 712, 715 proboscidean, 50 procyonid, 555 prong-billed barbet, 439 prothonotary warbler, 394 pteridophyte, 462 pufferfish, 144, 148, 176, 389, 635 pugnose tree frog, 391– 92 puma, 262, 263, 263, 482, 511, 557, 712, 719, 720 purple (murex), 152 purple crab, 234 pygmy rain frog, 531 pyrrhophyte, 672, 676, 721 quetzal. See resplendent quetzal quillwort, 672, 721 rabbit, 196, 262, 471, 511, 532, 555, 712, 720. See also specific species of rabbit raccoon, 262, 264, 265, 355, 712. See also specific species of raccoon radish, 479 raffia, 694 rainbow bass, 269 rainbow cichlid, 547, 548 rainbow trout, 463, 465, 719 rain frog, 392 ramphastid, 562 raptor, 392, 715 rat, 79– 80, 219, 221, 224, 225, 231, 236, 265, 466, 467, 555, 715. See also specific species of rat rattlesnake, 268 ray, 145, 149, 154, 711 razor clam, 153 red alga, 174, 509, 624 red banana, 541 red-breast cichlid, 268, 547 red brocket deer, 277, 467, 559, 686

red-capped manakin, 393 red ceiba, 377 red-eyed tree frog, 392 red-eyed tree snake, 392 red-eyed vireo, 394 red-footed booby, 222 red-footed seabird, 170 red-furred cattle, 300 red macroalga, 710 red mangrove, 108, 143 red snapper, 148, 711 redstart, 438, 466. See also specific species of redstart red-tailed hawk, 466, 511, 720 red-tailed squirrel, 466 red-throated ant-tanager, 554 reef-building coral, 171, 710 reptile, 434– 35, 552, 629– 30, 696, 712, 715, 719, 720, 722 resplendent quetzal, 435, 438, 439, 443– 44, 466, 471– 72, 472, 476, 478, 482, 553, 719 resurrection plant, 429 reticulated ameiva, 392 rhino, 532 rhodolith, 114, 115, 116, 121 rice, 68, 71, 76, 196, 276, 303, 336, 377, 379, 642, 647, 648, 659, 683, 689, 700 riodinid, 270 river otter, 634, 722 river sardine, 268 robin, 148, 394, 511, 720, 721. See also specific species of robin rock louse, 174 rodent, 79– 80, 262, 265, 273, 354, 386, 465, 466, 471, 472– 73, 532, 557– 58, 698, 712, 719 roseate spoonbill, 266, 266, 267, 354 rotifer, 665, 667, 675 royal palm, 694 ruddy-capped nightingale-thrush, 466 ruddy treerunner, 466 rufous-collared sparrow, 511 rufous piha, 393 rufous-vented ground-cuckoo, 394, 554 rush, 216, 721. See also specific species of rush russuloid, 458 sabellariid polychaete, 147 saber-tooth cat, 55 salamander, 462, 463, 464, 465, 473, 550, 551, 686, 715, 721. See also specific species of salamander sally lightfoot crab, 233 salp, 604, 711 Salvin’s spiny pocket mouse, 262, 265 sand crab, 145 sand dollar, 110 sand piper, 722 sardine, 140– 41. See also specific species of sardine saturniid, 270, 560

sawfish, 268, 546, 547 scaphopod, 592 scarab beetle, 438 scarlet macaw, 266, 267, 355, 356, 393, 393, 401– 2, 554, 716 scarlet-rumped cacique, 554 sciaenid, 148, 149, 155 scleractinian coral, 608 scorpion, 227, 229, 231 scorpion fish, 148 scorpion mud turtle, 268 sea anemone, 107– 8 sea bird, 711 sea catfish, 148, 711 sea cucumber, 596 sea fan, 593, 605 seagrass, 102, 103, 111, 120, 593, 595, 596, 601– 2, 603, 604, 608, 609, 710 seal, 101, 194, 219. See also specific species of seal sea lion, 170, 219. See also specific species of sea lion sea robin, 148 sea slug, 103, 594 sea spider, 100 sea star, 593. See also specific species of sea star sea turtle, 105, 106, 106, 123, 305, 395, 398, 566, 591, 596, 608, 609, 716. See also specific species of sea turtle sea urchin, 105, 113, 165, 176, 592, 710 sea weed, 114 sedge, 686, 687, 689, 696, 721 seed beetle, 269 serranid, 148 shark, 116, 148, 149, 154, 168, 170, 171, 178, 183, 626, 627, 711. See also specific species of shark shellfish, 121, 151, 151, 156 shield bug, 269 shining honeycreeper, 554 ship rat, 224 short-tailed hawk, 265 shrew, 437, 511, 719, 720 shrimp, 68, 118, 148, 149, 153– 54, 156, 169, 233, 234, 594, 626, 630, 631, 632– 33, 634– 35, 634, 639, 642, 644, 722. See also specific species of shrimp siboglinid tubeworm, 117 silky anteater, 265 silky shark, 170 silverside, 547, 548 silvery-throated jay, 466 siphonophore, 100, 167, 168, 171, 604, 711 sipunculid, 146, 153, 155, 595 skink, 552 skipper, 560 skipper butterfly, 270, 275 skunk, 262, 555. See also specific species of skunk slate-throated redstart, 438 slaty-backed nightingale thrush, 476 slaty flowerpiercer, 511

754 Systematic Index of Common Names sleeper, 269, 389, 547. See also specific species of sleeper slender black-speckled palm pit viper, 465 slender gray fox, 466 slender harvest mouse, 437 slime mold, 458 sloth, 719. See also specific species of sloth slug, 103, 594. See also specific species of slug small rice, 623 snail, 75, 76, 145, 153, 155, 165, 232, 389, 605, 634, 635. See also specific species of snail snake, 75, 76, 363, 465, 552, 715, 719. See also specific species of snake snapper, 148, 154, 389, 390. See also specific species of snapper snapping turtle, 630 snook, 389, 547 snout beetle, 269 snowy cotinga, 553 social wasp, 327– 28, 328 sole, 547 solemyid, 33 solifugid, 231 solitaire, 439, 466. See also specific species of solitaire sooty-capped bush-tanager, 511 sooty robin, 511, 720, 721 sooty tern, 222 sooty thrush, 721 Southern river otter, 277 soybean, 71 spadebill, 552. See also specific species of spadebill spangle-cheeked tanager, 439 spermatophyte, 210 sperm whale, 194 sphingid, 229– 31, 270 spider, 231, 712. See also specific species of spider spider monkey. See Geoffroy’s spider monkey spiny-cheek sleeper, 389, 547 spiny lobster, 594 spiny pocket mouse, 274 spiny-tailed iguana, 268 spirochaete, 117 sponge, 166, 177, 593. See also specific species of sponge spoonbill, 266– 67, 266, 354. See also specific species of spoonbill spot-breasted oriole, 222, 265 spot-crowned woodcreeper, 466 spotted antbird, 554 spotted dolphin, 102, 116, 710 spotted skunk, 467 spotted sleeper, 220 springtail, 77 squash, 533, 564, 565 squat lobster, 118 squid, 149 squirrel, 79, 264, 273, 472– 73, 555, 715, 719

squirrel monkey. See Central American squirrel monkey starfish, 176, 710. See also specific species of starfish star grass, 255 stem borer, 560 stingray, 148, 149 stomatopod, 100, 153, 154, 165, 168 stonefly, 633, 722 stony coral, 103, 172, 593 stork, 265, 691, 722. See also specific species of stork strangler fig, 375, 431, 432 strawberry, 68 streak-crowned antvireo, 554 streaked flycatcher, 553 striped foliage-gleaner, 393 striped hog-nosed skunk, 467 stylaster, 169 succulent, 429 suckermouth catfish, 546 sugar cane, 64, 68, 71, 73, 196, 276, 303, 336, 541, 543, 642, 647, 648, 683, 700 sulphur (butterfly), 270 sulphur-rumped flycatcher, 554 sulphur-rumped tanager, 553 sunbittern, 630 sundown cicada, 559 sungrebe, 630 Swainson’s thrush, 476 swallowtail butterfly, 270 swallow-tailed gull, 170 swallow-tailed kite, 466 sweet potato, 86 swollen-thorn acacia, 274 tachinid, 275 tamarind, 73 tanager, 393– 94, 439, 554, 719. See also specific species of tanager tank bromeliad, 462, 464 tapir, 262, 263, 318, 354, 366, 378, 388, 443– 44, 467, 479– 80, 480, 555, 556, 696, 712, 715, 716, 720. See also specific species of tapir tapirid, 51 tardigrade, 511 tarpon, 546, 547, 595, 627 tawny-crested tanager, 554 tawny-crowned greenlet, 393 tawny-winged woodcreeper, 394 tayassuid, 51 tayra, 265, 467, 557, 562 teak, 76, 279, 543. See also specific species of teak teal, 701. See also specific species of teal teiid, 552 teleost, 149 Tennessee warbler, 394 tent-making bat, 395, 557, 715 termite, 75, 77– 78, 78 tern, 222. See also specific species of tern tetra, 547. See also specific species of tetra

thallose liverwort, 431 thicket tinamou, 276 threadfin anglerfish, 118 three-toed sloth, 467 three-wattled bellbird, 355, 394, 435, 439, 553, 712, 719 thrush, 439, 686, 719. See also specific species of thrush thumbless bat, 557 tick, 440 tiger heron, 630 tilapia, 336, 628, 628, 640, 648– 49, 692. See also specific species of tilapia timberline wren, 511 tinamou, 266, 466. See also specific species of tinamou toad, 463, 719. See also specific species of toad tobacco, 196, 361 tomato, 71, 461 Tome’s rice rat, 440 tongue fern, 509 tortoise beetle, 269 tortoise shell. See specific species of shell toucan, 439, 561– 62. See also specific species of toucan toxodont, 51 toxodontid, 51 tree boa, 392 tree frog, 628, 634 treefern, 211, 214, 215, 377, 457, 461, 468, 469, 509, 513, 513, 719 trematode, 275– 76 trichiurid, 148 trogon, 266, 466. See also specific species of trogon tropical almond, 273 trout, 336, 477, 479, 628. See also specific species of trout true bug, 712 true mountain frog, 464, 482 true spider, 231 tuba, 548 tuber, 361 tubeworm, 117. See also specific species of tubeworm tucuxis dolphin, 595 tuna, 100, 102, 178 tungara frog, 531 tunicate, 609 turkey, 267. See also specific species of turkey turkey vulture, 266 turquoise-browed motmot, 266 turtle, 103, 116, 153, 168, 178, 531, 552, 600, 606, 629, 630, 715, 722. See also specific species of turtle tussock grass, 492, 500, 512 two-toed sloth, 467 ungulate, 5, 385, 395, 532 urchin, 105, 113, 165, 176, 592, 593, 594, 602, 605, 607, 710. See also specific species of urchin urostigmoid fig, 432

Systematic Index of Common Names 755 Vaillant’s frog, 268 vampire bat, 264, 557 variegated squirrel, 273 vascular epiphyte, 428, 461– 62, 469, 718 vascular parasite, 462 velvet worm, 78 vertebrate, xix, 55, 119, 143, 166, 168, 218– 19, 224, 226, 262– 65, 269, 273, 275, 315, 332, 333, 336, 399, 404, 463– 67, 471, 511, 545, 552, 556, 557, 558, 566– 67, 623, 627, 709, 712, 713 vesicomyid, 33 vesicular-arbuscular mycorrhiza, 440 vesper mouse, 558 vesper rat, 437 vine, 211, 253, 254, 257, 269, 332, 333, 338, 347, 348, 374, 383, 392, 432, 460– 61, 469, 713, 721 violet-crowned woodnymph, 553 viper, 531. See also specific species of viper viperid, 552 vireo, 394. See also specific species of vireo Virginia opossum, 262, 265 vocal rain frog, 391 volcano hummingbird, 511, 720 volcano junco, 511 vulture, 306– 7. See also specific species of vulture wading bird, 715 warbler, 222, 224, 394, 466, 511, 554. See also specific species of warbler wasp, 269, 271, 272, 275, 323, 327– 28, 384, 439, 712, 719. See also specific species of wasp water anole, 392 water boatman, 666 waterfowl, 700, 701– 2, 722 water hyacinth, 257, 258, 349, 623, 659, 721 water lettuce, 721 water lily, 663, 721

water lizard, 392 water opossum, 277 water turkey, 267 weasel, 262, 712. See also specific species of weasel wedge-billed woodcreeper, 392– 93 weed, 81, 114, 196, 211, 335, 515, 624, 691. See also specific species of weed weevil, 269– 70, 273– 74, 329, 330. See also specific species of weevil West Indian manatee, 555, 595 West Indian topshell, 594 whale, 154, 162, 168, 194, 710. See also specific species of whale whip spider, 231 white-capped noddy, 222 white clover, 71 white-faced capuchin monkey, 260, 263– 64, 328, 399, 466, 471, 473, 556– 57, 716, 719 white-flanked antvireo, 554 white-flanked antwren, 393 white-headed capuchin, 559, 716. See also white-faced capuchin monkey white ibis, 267 white-lipped mud turtle, 630 white-lipped peccary, 277, 354, 395– 97, 395, 400– 401, 404, 437, 556, 558, 559, 715, 716 white-nosed coati, 466, 557 white oak, 81, 470 white-tailed deer, 196, 224, 226, 228, 265, 277, 332, 559 white-tailed hognose snake, 392 white tent-making bat, 557 white tern, 222 white-throated capuchin monkey. See whitefaced capuchin monkey white-throated magpie-jay, 266 white-throated robin, 394 white-throated shrike-tanager, 393, 554 white-throated spadebill, 552

white-tip reef shark, 170, 171 wide-head sea catfish, 268 wild sweet potato, 230 wolf cichlid, 547, 548, 550 wood borer, 227 woodcreeper, 266, 392, 554, 715. See also specific species of woodcreeper woodnymph, 553. See also specific species of woodnymph woodpecker, 392, 715. See also specific species of woodpecker woodstork, 266, 267, 276, 699 woodthrush, 394 worm, 78, 153. See also specific species of worm wren, 435, 554. See also specific species of wren wrenthrush, 511

arrayán, 513 arrocillo, 623

caimito, 73 calva, 547 cambute, 153 cangrejero, 386 caoba, 259, 276 caro caro, 274 cascabel, 268 casco de burro, 107 castellana, 267, 267 cativo, 66 cebu, 302, 303 cedro, 276 cerillo, 696 chachalaca, 400 chile, 361 chocuaco, 361 choreja, 257 chucheca, 151, 151, 152

yam, 533 yellow-billed cacique, 466 yellow-billed cotinga, 355 yellow-eyed grass, 686, 721 yellow-margined flycatcher, 554 yellow-naped parrot, 266 yellow-olive flycatcher, 275 yellow-shouldered bat, 467, 553 yellow-thighed finch, 439, 466 yellow-throated brush-finch, 476 yellow-throated euphonia, 435 yellow toad, 267 yellow warbler, 222, 224, 394 Yeti crab, 118 yucca, 303, 568 Zaca’s fiddler crab, 232 zooplankton, 100, 102, 103, 104, 147– 48, 169, 595, 604, 660, 665, 666, 667, 672, 675, 676, 721 zooxanthellate coral, 165, 175, 710

Spanish Common Names agave, 429 agouti, 79– 80, 80, 260, 265, 274, 329– 30, 400, 467, 555, 562, 698 aguacatillo, 471 alfaro, 547, 548 alga, 100, 101, 102, 105, 107, 111, 121, 147, 150, 154, 155, 168, 173, 175, 218, 509, 591, 593, 605, 624– 26, 627, 629, 632, 634– 35, 636, 709, 711, 720– 21, 722 almeja blanca, 151 almendro, 273 anguila, 547 anguila de pantano, 268, 547, 548 anhinga, 267, 354, 630 aracari, 561– 62 árbol de la llama, 273 armadillo, 277, 532, 555, 562, 715

bagre cuatete, 268 bala, 387– 88 bala de cañon, 260 balsa, 380 banana, 65, 66, 68, 77, 79, 83, 85, 196, 303, 347, 354, 364, 377– 78, 379, 379, 401, 541, 542, 543, 549, 557, 563, 564– 65, 567, 646, 647, 647, 677, 716 barbudo, 268, 547, 548 batamba, 512 bobo, 548 bromelia, 213, 216, 257, 275, 466, 470, 633, 686, 686, 713– 14, 717, 718, 721 burro, 300

756 Systematic Index of Common Names chupapiedra, 548 cicada, 269 cigueñón, 266 coati, 264, 332, 386, 400, 562 coco, 273 cocobolo, 276 cocotero, 273, 377 congo, 268, 547, 548 copey, 215 coral, 100, 102– 3, 104, 111– 14, 112, 120– 21, 120, 123, 165, 168, 169, 171, 172, 175– 76, 178– 79, 179, 180, 181, 591, 595, 596, 597, 601, 602– 3, 603, 604, 604, 605, 605, 606, 607, 608– 9, 710 corvina, 148, 154, 711 coyote, 264, 277, 332, 333, 437, 466, 557, 719 cristóbal, 259, 262, 276 curculio, 269 danta, 319 dormilón, 269 encino, 313, 315, 325 encino negro, 272 enea, 257 espatula rosada, 266 espavel, 315 frijol, 66 ganado, 300 garceta grande, 267 garcilla bueyera, 267 garrobo, 268 gaspar, 547, 700, 722 gavilán colicorto, 266 gmelina. See melina grisón, 277 guacamayo rojo, 266 guacimo, 334, 338 gualaje Atlántico, 547 guanábana, 230 guanacaste, 259, 265, 274, 279, 333, 334 guapinol, 273– 74, 328– 29 guapote, 269, 547, 548, 550 guapotillo, 548 guarasapa, 547 guarumo, 215, 217, 228, 230 guatusa, 79 guavina, 269, 389, 547, 548 guayacán real, 259, 276 gumbo limbo, 256 hormiga bala. See bala hormiga del cornizuelo, 274, 338 ibis blanco, 267 indigofera, 300 indio desnudo, 256 jabirú, 266– 67 jacana, 265, 630, 722

jaguar, 262, 277, 305, 354, 366, 395, 396, 398– 99, 401, 404, 437, 467, 482, 557, 712, 715, 716 jaguarundi, 262 jaragua, 255, 276, 300, 301, 302, 302, 306, 306, 308, 311, 312– 14, 335, 713 javelina, 395 jícaro, 274, 304, 315 jurel, 547 lagartija, 267 lamearena, 547, 548 lapa roja, 401 laurel negro, 276 lechuga, 257 lengua de vaca, 710 lenguado, 547 lenguado redondo, 547 liana, 213, 253, 256, 257, 272, 275, 383, 431, 432, 439, 469, 715, 719 lirio de agua, 257 llama del bosque, 273 luciernaga, 313 machaca, 547 madre de barbudo, 268, 547 majagua, 214, 217 majagual, 225 mapache, 264 marañon, 377 madre de barbudo, 547, 548 medusa, 100, 167, 168 melina, 334– 35, 402 mocasín, 267, 712 moga, 548 mojarra, 268, 269, 547, 548 mojarrita, 547, 548 mono araña, 399 mono aullador, 264, 399 mono cariblanca, 263– 64, 399 mono congo, 264, 399 mono tití, 399 mucuna, 78 murex, 152, 152, 153 napa, 694 ocelote, 262 ojoche, 292 olomina, 268, 547, 548 orey, 698 paca, 196, 265, 400, 437, 467, 555, 562, 719 palmito, 73 palo de hierro, 194, 213 palo verde, 257, 258, 690, 692, 721 papaya, 76, 303 pargo, 390 pato aguja, 267 pato real, 267 pava moñuda, 266 pecho rojo, 268

pejibaye, 377 pez diablo, 628 pez perro, 547 pez pipa, 268, 548 pez sierra, 268, 547 piangua, 151, 153 picaculo, 389 pie de burro, 151 pijije común, 266 pis pis, 547 pitahaya, 275 pochote, 254, 279, 377 pocoyo, 389 poró, 75 puma, 262, 263, 263, 482, 511, 557, 712, 719, 720 púrpura, 152 quetzal, 435, 438, 439, 443– 44, 466, 471– 72, 472, 476, 478, 482, 553, 719 quira, 352 róbalo, 389, 547 roble negro, 272 roncador, 547, 548 ron-ron, 276 sabalete, 547 sábalo real, 547 saltarín colilargo, 266 sangrillo, 696 sapo amarillo, 267 sardina, 268, 389, 547, 548 sardina blanca, 548 sardina de quebrada, 547 sardina lagunera, 547 sardina picuda, 547 sardinita, 268, 547 serpiente mocasín, 267 tachinid, 275 taltuza, 79 tayra, 265, 467, 557, 562 tempisque, 276 tepemechín, 269, 389, 547, 548 tepezcuintle, 79, 265, 277 tiburón, 547 tigrillo, 262 tolomuco, 467 tortuga baula, 106, 268 tortuga lora, 106, 268 tucuxi, 595, 608 túngara, 531 vampiro falso, 264– 65 vieja, 548 yayo, 315 yolillo, 66, 377, 694, 694 yucca, 303, 568 zacate, 568

Systematic Index of Scientific Names

Page numbers in italics refer to figures. Acacia, 257, 271, 274, 713 Acacia allenii, 374 Acacia collinsii, 338 Acacia farnesiana, 256 Acacia villosa, 255 See also Vachellia Acaena, 500, 512 Acaena cylindristachya, 512 Acalypha Acalypha diversifolia, 687, 721 Acalypha pittieri, 211 Acanthaceae, 254, 469 Acanthaster planci, 176, 710 Acanthobotrium nicoyaense, 149 Acanthocereus tetragonus, 256 Acarina, 77 Acartia lilljenborgii, 147 Acaulospora, 440 Accipitridae, 555 Achiridae, 547 Acnanthidium catenata, 667 Acnistus arborescens, 351, 352 Acoelorraphe wrightii, 690 Acosmium panamense, 256, 350 Acrididae, 559 Acrocomia aculeata, 335 Acromyrmex volcanus, 387 Acropora palmata, 603, 607 Acrostichum aureum, 9, 215, 377, 687, 688, 696 Actinella, 669 Actinella brasiliensis, 669 Actinella punctata, 669 Actitis macularis, 630, 722 Acuariidae, 276 Adelanthus, 510 Adelia triloba, 699 Adiantum Adiantum amplum, 348 Adiantum concinnum, 275, 348 Adiantum latifolium, 696 Adiantum trapeziforme, 275 Aechmea, 275 Aechmea magdalena, 368 Aellopos fadus, 325 Aequidens, 391 Aeschynomene, 255, 377, 687 Aeschynomene virginica, 689 Agalychnis Agalychnis callidyias, 392 Agalychnis helenae, 392 Agalychnis spurrelli, 392 Agaricales, 458, 718 757

Agaricus, 458 Agave seemanniana, 255 Ageratina, 461, 509, 510 Agkistrodon bilineatus, 267, 267, 712 Agonostomus monticola, 220, 269, 389, 547, 548, 640, 645 Agoutidae, 79 Agouti paca, 79, 80, 196, 265, 467, 698 Agrius cingulatus, 230 Agrostis Agrostis bacillata, 512 Agrostis tolucensis, 513 Aguna asander, 270 Aiouea, 471 Ajaia ajaja, 266, 266, 354 Albizia Albizia adinocephala, 351 Albizia carbonaria, 352 Albizia caribaea, 272 Alcedinidae, 555 Alchemilla, 720 Alchornea, 52, 718 Alchornea costaricense, 696 Alcyonacea, 181 Alcyoniidae, 181 Alfaroa, 473 Alfaroa costaricensis, 469 Alfaroa guanacastensis, 377 Alfaroa williamsi, 349 Alfaro cultratus, 547, 548 Alligatoridae, 553 Alloplectus, 462 Allosanthus trifoliatus, 349 Alnus, 52, 458, 507, 718 Alnus acuminata, 75, 76, 76, 478 Alophia silvestris, 255 Alopias Alopias pelagicus, 170 Alopias superciliosus, 170 Alouatta palliata, 264, 399, 558 Alpheus, 594 Alpheus simus, 594 Alsophila notabilis, 211 Amanita, 458 Amanita muscaria, 458 Amanoa potamophila, 695 Amatitlania, 550 Amauroderma schomburgkii, 354 Amazilia saucerrottei, 275– 76 Amazona Amazona auropalliata, 266 Amazona farinosa, 355, 393 Ambates, 560

Amblycercus holosericeus, 466 Amblycerus spondiae, 273 Amblyopinus Amblyopinus emarginatus, 440 Amblyopinus tiptoni, 440 Amblypygi, 231 Ambrosia cumanensis, 689 Ameiva, 552 Ameiva leptophrys, 392 Americonuphis reesei, 110, 156 Ammotrecha solitaria, 231 Amphignathodontidae, 551 Amphilophus Amphilophus alfari, 549 Amphilophus bussingi, 549 Amphilophus citrinellus, 546, 547 Amphipholis geminata, 110 Amphitecna latifolia, 696 Anacardium, 369, 711 Anacardium excelsum, 260, 262, 315, 350, 368, 378, 697 Anacardium occidentalis, 377 Anacroneuria, 633 Anadara, 153 Anadara tuberculosa, 151, 153 Anamura, 232 Ananthacorus angustifolius, 348 Anartia fatima, 270 Anas Anas clypeata, 693 Anas discors, 266 Anatidae, 555 Anax, 666 Anchoa, 154 Andira inermis, 260, 377, 695, 713 Anguidae, 553 Anguilla rostrata, 546, 547 Anguillidae, 547 Anhinga anhinga, 267, 354, 630 Anhingidae, 555 Ankistrodesmus braunii, 667 Annelida, 119 Annona Annona costaricana, 52 Annona glabra, 214, 215, 217, 230, 695 Annona muricata, 230 Annona reticulata, 254 Annonaceae, 348, 468 Anolis biporcaus, 339 Anomocora carinata, 179 Anous Anous minutus, 222 Anous stolidus, 222, 225

758 Systematic Index of Scientific Names Anteos Anteos clorinde, 327 Anteos maerula, 327 Anthoceros, 431 Anthodiscus, 374 Anthodiscus chococense, 353 Anthonomus, 329, 330 Anthophoridae, 271 Anthophorinae, 271 Anthopleura nigrescens, 107– 8 Anthurium, 347, 457, 462, 469, 539, 715, 718 Anthurium bakeri, 539 Antillesoma antillarum, 146 Anura, 686 Anyphaenoides cocos, 231 Aotus, 556 Apeiba tibourbou, 254, 257, 353 Aphaenogaster, 561 Aphaenogaster araneoides, 387 Aphaenogaster phalangium, 387 Aphelandra scabra, 257, 262 Aphrissa statira, 327 Apiaceae, 52, 499, 510 Apidae, 271 Apis mellifera, 335– 36 Apocynaceae, 230, 254, 348 Apodidae, 555 Ara Ara ambigua, 8, 554, 567 Ara macao, 266, 355, 356, 393, 400, 554, 716 Araceae, 347, 396, 462, 539, 540 Arachis pintoi, 85 Arachnida, 463 Araliaceae, 52, 457, 461, 462 Aramidae, 555 Araneae, 231 Archaeatya, 233 Archaeatya chacei, 235 Archaeolithophyllum, 52 Archaeoprepona, 270 Archaeoprepona demophon, 325 Archocentrus Archocentrus centrarchus, 547 Archocentrus myrnae, 548, 549 Archocentrus nigrofasciatus, 268, 547, 548, 550 Archocentrus septemfasciatus, 548, 549 Arctocephalus galapagoensis, 219 Arcytophyllum, 512 Arcytophyllum lavarum, 512, 513 Ardeidae, 555 Ardisia, 269, 461, 469, 471, 719 Ardisia compressa, 695 Ardisia cuspidata, 217 Ardisia cutteri, 374, 715 Ardisia glandulosa-marginata, 81 Arecaceae, 349, 396, 468, 539 Arenaria, 512 Ariidae, 148, 268, 711 Ariopsis seemanni, 693 Arius guatemalensis, 268

Aromobatidae, 551 Arothron meleagris, 176, 710 Arrabidaea, 257 Arremon aurantiirostris, 554 Arsenura arianae, 323 Arthoniales, 509 Arthrodesmus Arthrodesmus bifidus, 665, 721 Arthrodesmus phinus, 667 Arthropoda, 119 Artibeus Artibeus jamaicensis, 265 Artibeus toltecus, 437, 719 Artiodactyla, 354, 511 Asclepias, 255 Asclepias woodsoniana, 255 Ascomycetes, 208 Ascomycota, 6, 509 Aspidosperma Aspidosperma megalocarpon, 260, 374, 715 Aspidosperma myristicifolium, 349 Asplenium, 347, 458, 462 Asplenium cuspidatum var. triculum, 347 Asplenium salicifolium var. aequilaterale, 347– 48 Asplundia, 462 Astatheros Astatheros alfari, 268, 547, 548 Astatheros bussingi, 548 Astatheros diquis, 389 Astatheros longimanus, 268, 547 Astatheros rhytisma, 548 Astatheros rostratus, 548 Asteraceae, 52, 62, 254, 347, 354, 458, 460, 461, 462, 467, 468, 469, 476, 492, 497, 499, 509, 510, 539, 719 See also Compositae Asterogyne martiana, 696 Astractosteus tropicus, 546, 547, 722 Astrangia dentata, 179 Astrocaryum alatum, 696, 699, 722 Astronium graveolens, 257, 259, 260, 276, 353 Astyanax, 628 Astyanax aeneus, 269, 276, 389, 547, 548, 549, 627– 28, 692, 722 Astyanax aeneus costaricensis, 268 Astyanax fasciatus, 140– 41, 268, 547, 548, 558, 700 Astyanax nasutus, 547 Astyanax orthodus, 548, 549 Ateles geoffroyi, 262, 399, 482, 559, 712 Atelopus, 628, 629 Atelopus varius, 356, 434, 628, 629, 719, 722 Atelopus zeteki, 629 Atherinella Atherinella chagresi, 548 Atherinella hubbsi, 547, 548 Atherinidae, 546, 547, 548 Atlapetes Atlapetes brunneinucha, 476 Atlapetes gutturalis, 476

Atractosteus tropicus, 692, 700 Atta, 273, 559, 713 Atta cephalotes, 78, 559 Atta colombica, 271 Attalea rostrata, 315, 349, 353 Attini, 561 Atya, 632, 634 Atya crassa, 632 Atya innocous, 632 Atya margaritacea, 632 Atya scabra, 632 Atyia, 235 Atyidae, 233, 235 Aulacorhynchus prasinus, 466 Aulacoseira, 507, 668, 670, 672, 674, 721 Aulacoseira alpigena, 507, 674 Aulacoseira italica, 668 Aulacoseira lirata, 507, 674 Auricularia Auricularia auricula, 257 Auricularia delicata, 257 Auricularia fuscosuccinea, 257 Automeris Automeris tridens, 323 Automeris zozimanaguana, 323 Automeris zugana, 323 Automolus ochrolaemus, 554 Avicennia Avicennia bicolor, 109, 143 Avicennia germinans, 108, 109, 143– 44, 377, 599, 696, 710 Awaous Awaous banana, 547, 548 Awaous transandeanus, 389 Axonopus aureus, 255 Ayenia mastatalensis, 352 Azolla microphylla, 690 Azorella, 512, 720 Azorella biloba, 510, 513 Azteca, 440, 719 Azteca alfari, 387 Azteca chartifex, 388, 388 Azteca coeruleipennis, 387 Azteca constructor, 387 Azteca forelii, 387 Azteca instabilis, 387 Azteca ovaticeps, 387 Azteca pittieri, 387 Azteca sericeasur, 387 Azteca xanthochroa, 387 Bachia blairi, 392 Bacillariophyceae, 624 Bacillariophyta, 509 Bactris Bactris gasipaes, 377 Bactris hondurensis, 539 Bactris longiseta, 699 Bactris major, 377 Baetidae, 635 Balaenoptera Balaenoptera edeni, 154 Balaenoptera musculus, 154

Systematic Index of Scientific Names 759 Balaenopteridae, 116 Balanus, 143 Ballia prieurii, 624 Banara guianensis, 339 Bartramia, 510 Bartramia longicauda, 693 Basidiomycetes, 208, 458, 509 Basileuterus melanogenys, 511 Basilicus vittatus, 552 Bassaricyon gabbii, 482 Bassariscus sumichrasti, 482 Bathymodiolus, 117 Batocarpus, 374 Batocarpus costaricensis, 353, 374 Batrachochytrium dendrobatidis, 434, 463, 551, 629 Bauhinia Bauhinia glabra, 259 Bauhinia paulettia, 260 Bauhinia ungulata, 270, 338 Bazzania, 463 Becquerelia cymosa, 696 Begonia, 438, 462 Begonia estrellensis, 432 Begoniaceae, 462 Beilschmiedia, 438, 471, 719 Beilschmiedia pendula, 438 Belonesox belizanus, 546, 547 Bernoullia flammea, 260, 261 Bertiera angustifolia, 230 Besleria, 457 Biblis hyperia, 339 Bignoniaceae, 254 Billia, 471, 473 Billia hippocastanum, 472 Bjerkandera, 458 Blakea, 461, 462 Blattarida, 463 Blechnaceae, 482, 686 Blechnum, 12, 458, 510, 512, 514 Blechnum buchtieni, 513, 685, 686, 721 Blechnum loxense, 686 Blechnum occidentale, 215 Boa, 552 Bocconia, 473 Boidae, 553 Bolbitis portoricensis, 348 Boletus, 458 Bolitoglossa, 465 Bolitoglossa pesrubra, 464, 511, 686, 721 Bolitoglossa subpalmata, 464, 686 Bomarea, 461, 469 Bombacopsis Bombacopsis quinata, 73, 254, 259, 272, 348, 377, 712 Bombacopsis sessilis, 350, 353 See also Pachira; Pochota quinata Bombus ephippiatus, 463, 469, 511 Bombycillidae, 556 Boraginaceae, 254 Borreria Borreria ocymoides, 230 Borreria prostrata, 230

Bos Bos indicus, 300, 303 Bos taurus, 300, 303 Bosmina Bosmina hagmanni, 667, 675, 676– 77 Bosmina longirostris, 667, 675 Bothriechis, 552 Bothriechis nigroviridis, 465 Bothriechis schlegelii, 392 Bothriechis supraciliaris, 392 Bothrops, 552 Bothrops asper, 357, 712 Botryococcus, 509 Botryococcus braunii, 672 Brachiaria, 623, 721 Brachycephalidae, 551 Brachymenium spirifolium, 256 Brachyrhaphis, 389 Brachyrhaphis holdridgei, 548 Brachyrhaphis olomina, 268, 548 Brachyrhaphis parismina, 547, 548 Brachyrhaphis rhabdophora, 389 Brachysira brachysira, 665, 666, 670 Brachyura, 232, 632 Braconidae, 275 Bradypus variegates, 177, 354, 467, 558 Bramocharax bransfordii, 547 Branchiostoma, 144 Branchiostoma californiense, 110, 144 Brassavola nodosa, 275 Bravaisia integerrima, 349 Breutelia, 721 Breutelia subarcuata, 686 Bromelia, 275 Bromeliaceae, 52, 260, 462, 469, 540 Bromus, 512 Brosimum, 213, 292, 294, 369, 374, 711, 713 Brosimum alicastrum, 254, 260, 350, 712 Brosimum costaricanum, 260, 374 Brosimum utile, 348, 349, 353, 374, 715 Bruchidae, 269, 273 Brunellia, 473, 718 Brunellia costaricensis, 461 Brunellia hygrotermica, 377 Brunellia standleyana, 350 Bryconamericus, 634 Bryconamericus scleroparius, 269, 276, 547, 558 Brycon guatemalensis, 547, 558, 561, 635– 36, 640, 675 Bryum, 463, 510 Bubulcus ibis, 220, 267 Bucconidae, 555 Buchenavia costaricensis, 353 Buchnera pusilla, 255 Buddleja, 467, 471, 478, 500, 512, 514, 718 Buddleja cordata, 472 Bufo, 391 Bufo aucoinae, 392 Bufo luetkenii, 267 Bufo melanochloris, 391, 392 Bufo periglenes, 6, 434, 629, 719

Bufonidae, 551 Bulbostylis paradoxa, 255 Buprestidae, 231, 559 Burmeistera, 457, 462 Bursera, 257 Bursera graveolens, 255 Bursera schlechtendalii, 260 Bursera simarouba, 256, 257, 259, 260, 261, 262, 353, 454, 711 Bursera standleyana, 461 Buteo Buteo brachyurus, 266 Buteo jamaicensis, 466, 511 Butorides virescens, 692, 693, 722 Byrsonima, 52 Byrsonima crassifolia, 254, 255, 338, 350, 377 Cacicus uropygialis, 554 Caeciliidae, 551 Caenobita compressus, 215 Caesalpinia, 294 Caesalpinia eriostachys, 254, 261, 712 Caiman, 634 Caiman crocodilus, 552, 630, 722, 691 Cairina moschata, 267, 276, 355, 630, 722 Calamagrostis, 500, 512 Calandrina, 512 Calathea, 539, 561, 715, 721 Calathea foliosa, 696 Calathea inocephala, 261 Calathea lagunae, 687, 696 Calathea longiflora, 697 Calathea lutea, 687, 696 Calathea vinosa, 461 Calatola costaricensis, 292 Caligo memnon, 270 Calliandra tergemina, 255 Callichlamys latifolia, 327 Callicore pitheas, 325 Callinectes, 146 Callinectes arcuatus, 146, 147 Callinectes sapidus, 146, 153 Calocitta formosa, 266, 338 Caloglossa ogasawaerensis, 624 Calophyllum Calophyllum brasiliense, 348, 350, 377, 695, 696, 697, 698 Calophyllum longifolium, 353 Calvatia rugosa, 257 Calycophyllum candidissimum, 254, 257, 259, 348, 353, 712 Calyptogena, 33, 117 Calyptogena costaricana, 117 Calyptrocarya glomerulata, 216, 696 Calyptrogyne glauca, 696 Camaridium micracanthum, 211 Campanulaceae, 462, 469 Campnosperma panamensis, 695, 698– 99 Camponotus Camponotus biolleyi, 228 Camponotus sericeiventris, 387– 88 Campylopus, 463, 510, 512, 686, 721

760 Systematic Index of Scientific Names Canacidae, 231 Canavalia maritima, 214 Canis Canis familiaris, 196 Canis latrans, 51, 264, 333, 466, 557 Canna, 691 Canna glauca, 690 Cannabis, 479 Cantharellus, 458 Capitellidae, 110 Capparaceae, 254 Capparis, 257 Capparis incana, 255 Capra aegagrus hircus, 194, 224 Caprimulgidae, 555 Carangidae, 547 Caranx, 154 Caranx latus, 547 Carapa Carapa guianensis, 80, 374, 377, 378, 695, 696, 697, 698, 699, 715, 722 Carapa nicaraguensis, 699 Carcharhinidae, 546, 547 Carcharhinus Carcharhinus falciformis, 170 Carcharhinus leucas, 389, 546, 547 Carcharhinus melanopterus, 170 Cardinalidae, 556 Cardisoma, 385, 386 Cardisoma crassum, 215, 232, 235, 385 Caretta caretta, 600, 709 Carex, 512, 721 Carex bonplandii, 686 Carex donnellsmithii, 686 Carex jamesonii, 686 Carex lehmanniana, 513 Cariniana, 374 Carlana eigenmanni, 547 Carludovica drudei, 261 Carnivora, 511, 557, 562 Carollia Carollia perspicillata, 265 Carollia subrufa, 265 Carpodectes Carpodectes antoniae, 355 Carpodectes nitidus, 553 Caryocar, 374 Caryocar costaricense, 348, 349, 353, 374, 402, 482, 697, 712, 715 Caryodaphnopsis burgeri, 352, 353 Caryophyllia Caryophyllia diomedeae, 179 Caryophyllia perculta, 179 Caryothruastes poliogaster, 554 Casearia, 696 Casearia corymbosa, 338 Casearia nitida, 338 Casmerodius albus, 267 Cassia Cassia biflora, 338 Cassia grandis, 335, 338 Cassidinae, 269, 560 Cassimiroa edulis, 351

Cassipourea Cassipourea aff. killipii, 699 Cassipourea guianensis, 695 Castilla tunu, 378 Castilleja, 720 Castilleja irazuensis, 512 Castilleja quirosii, 510 Casuarina equisetifolia, 478 Catagonus wagneri, 395 Cathartes aura, 266 Cathartidae, 555 Catharus Catharus frantzii, 466 Catharus fuscater, 476 Catharus gracilirostris, 511 Catharus ustulatus, 476 Catopsis, 275 Cattleya, 275 Caulerpa sertularioides, 113 Cavendishia, 457, 461, 469 Cavendishia atroviolacea, 462 Cavendishia bracteata, 462 Cavendishia talamancensis, 461 Cayaponia racemosa, 338 Ceanothus caeruleus, 513 Cebus Cebus capucinus, 264, 399, 466, 471, 473, 559 Cebus capucinus ssp. imitator, 263 Cecropia, 381, 387, 440, 461, 473, 667– 68, 697, 715, 719 Cecropia obtusifolia, 339 Cecropia peltata, 353 Cecropia pittieri, 215, 217, 228, 230 Cecropia polyphlebia, 440, 442 Cedrela Cedrela odorata, 86, 273, 276, 350, 351, 482 Cedrela salvadorensis, 276, 351 Cedrela tonduzii, 374 Ceiba pentandra, 262, 265, 272, 339, 353, 374, 402, 540, 715 Celastraceae, 468 Centris, 271, 713 Centris aethyctera, 271 Centris bicornuta, 271 Centris flavifrons, 271 Centris flavofasciata, 271 Centrolenidae, 551, 628 Centropogon, 462, 469 Centropogon solanifolius, 438 Centropomidae, 268, 546, 547 Centropomus, 389 Centropomus nigrescens, 389 Centropomus parallelus, 547 Centropomus pectinatus, 547, 595 Centropomus undecimalis, 547, 640 Cephalochordates, 153 Cephaloleia, 560 Cephaloleia belti, 560 Cephaloleia fenestrata, 560 Cephalotes Cephalotes minutus, 387

Cephalotes setulifer, 387 Cephalotes umbraculatus, 387 Cephaloziella subtilis, 256 Cerambycidae, 231, 269, 273 Cerapachys neotropicus, 388 Ceratium Ceratium dens, 154 Ceratium furca, 146 Ceratium fusca, 154 Ceratium fusus, 154 Ceratolejeunea, 463 Ceratopteris richardii, 689 Ceriodaphnia cornuta, 666, 667, 675, 676– 77 Cerrophidion godmani, 465 Cervidae, 5 Ceryle, 630 Cestrum, 461 Chaetocalyx, 256 Chaetoceros, 146, 147 Chaetognatha, 119, 147, 148, 592 Chamaedorea, 349, 461, 469, 719 Chamaepetes unicolor, 466 Chamaepinnularia, 624, 721 Characidae, 268, 269, 389, 546, 547, 548, 558, 627, 628, 692, 712, 715, 722 Charadriidae, 555 Charidotella tuberculata, 269 Chaunochiton, 374 Cheilanthes brachypus, 275 Chelonia Chelonia agassizii, 106, 220 Chelonia mydas, 566, 591, 600, 601, 709 Chelonia mydas ssp. agassizii, 268 Chelydra, 552 Chelydra serpentina, 630 Chelydridae, 553, 630, 722 Chichlidae, 645 Chilopoda, 463 Chiococca semipilosa, 256 Chione costaricensis, 699 Chironectes minimus, 277 Chironius, 552 Chironius exoletus, 435 Chironomidae, 634, 635, 639 Chiroptera, 265, 272, 511, 555 Chiroxiphia linearis, 266, 435 Chloranthaceae, 214, 468 Chloris Chloris paniculata, 218, 219 Chloroceryle, 630 Chlorophyta, 119, 147, 509, 624, 690 Chlorospingus pileatus, 511 Chlorothraupis carmioli, 554, 561 Choloepus hoffmanni, 277, 467, 482, 558 Chordata, 119 Choreutidae, 231 Chroborus, 667 Chromacris colorata, 339 Chroomonas, 666 Chrysobalanus icaco, 353 Chrysochromulina polylepis, 155 Chrysoclamys allenii, 429

Systematic Index of Scientific Names 761 Chrysomelidae, 269, 560 Chrysophyceae, 666, 676 Chrysophyta, 199, 509 Chthamalus, 106 Chthamalus fissus, 107 Chusquea, 12, 460, 461, 467, 468, 469, 473, 512, 718 Chusquea subtessellata, 500, 501, 512, 513, 514, 685, 719, 720, 721 Chusquea talamancensis, 81, 461, 469 Chusquea tomentosa, 81, 469 Chusquea tonduzii, 512 Cicadellidae, 231 Cicadidae, 269, 559 Cichlasoma, 550, 693 Cichlasoma alfari, 558 Cichlasoma nicaraguense, 558 Cichlasoma nigrofasciatum, 558 Cichlasoma septemfasciatum, 558 Cichlasoma tuba, 558 Cichlidae, 268, 269, 389, 546, 547, 548, 558, 627, 628, 648, 712, 715, 722 Ciconiidae, 555 Cimaria vargasi, 153 Cinnamomum, 457, 461, 469, 471 Cinnamomum cinnamomifolium, 350, 351 Cipura campanulata, 255 Cirolana salvadorensis, 145, 600 Cirripedia, 147 Cirsium, 508 Cissus, 469 Citharexylum, 471 Citharichthys Citharichthys gilberti, 389 Citharichthys spilopterus, 547 Citharichthys uhleri, 547 Citrus, 335 Cittarium pica, 594, 595, 601 Cladina, 513, 721 Cladina confusa, 686 Cladocora Cladocora debilis, 179 Cladocora pacifica, 179 Cladonia, 459, 460, 509, 513 Cladonia corymbosula, 512 Clarisia racemosa, 350 Clelia, 552 Clematis, 461 Clethra, 514, 718 Clethra gelida, 469 Cleyera, 457, 471, 718 Cleyera theaeoides, 472 Clupeidae, 547 Clusia, 429, 432, 462, 469, 718 Clusia rosea, 213, 215, 216, 217, 219, 353, 713 Clusiaceae, 399, 468, 499 Clytostoma pterocalyx, 349 Cnemidaria choricarpa, 348 Cnidaria, 119 Coccoidea, 77 Coccoloba caracasana, 260 Cocconeis feuerbornii, 624, 626

Coccyzus ferrugineus, 222, 223 Cochlodinium Cochlodinium catenatum, 146, 154, 711 Cochlodinium catenatum cf. polykrikoides, 154 Cochlopinia tryoniana, 635 Cochlospermum vitifolium, 254, 255, 338, 350 Cocodrylus acutus, 692 Cocos nucifera, 214, 273, 377, 714 Cocytius anteus, 230 Coelosphaerium, 667 Coendou mexicanus, 79, 558 Coenobita compressus, 232– 33 Coenobitidae, 232 Coenocyathus bowersi, 179 Coerebidae, 556 Coffea, 377 Coleoptera, 86, 231, 269– 70, 273, 463, 511, 559 Colibri thalassinus, 469 Collema, 440 Collembola, 77 Coloptychon rhombifer, 391, 392 Coltricia, 458 Colubridae, 553 Colubrina arborescens, 256 Columba Columba fasciata, 466 Columba livia, 221 Columbidae, 555 Comarostaphylis, 458, 467, 500, 508, 511, 512 Comarostaphylis arbutoides, 468, 501, 512, 513– 14, 719 Combretum decandrum, 259 Commelinaceae, 469 Compositae, 509 See also Asteraceae Conepatus semistriatus, 467 Conocarpus erectus, 109, 215, 377, 599, 710 Conostegia, 457, 471 Conostegia bigibbosa, 461 Convallariaceae, 462 Convolvulaceae, 230, 254, 257, 273 Cookeina Cookeina speciosa, 257 Cookeina tricholoma, 257 Copaifera Copaifera aromatica, 262, 353 Copaifera camibar, 374, 482 Copepoda, 144, 592, 710 Copiocerinae, 559 Coprinus, 458 Coptocycla Coptocycla dorsoplagiata, 269 Coptocycla rufonotata, 269 Coragyps atratus, 266 Corallus, 552 Corallus ruschenbergeri, 392 Corapipo Corapipo altera, 561 Corapipo leucorrhoa, 561

Cordia, 257, 461 Cordia alliodora, 254, 387, 543 Cordia eriostigma, 351 Cordia gerascanthus, 255, 276 Coriaria, 512 Coricuma nicoyensis, 110 Coriolaceae, 354 Coriolopsis, 458 Coriolopsis byrsina, 354 Coriolopsis floccosa, 354 Coriolopsis polyzoma, 354 Cornus, 471 Cornus disciflora, 469, 471, 472, 482 Corollia perspicillata, 338 Cortaderia, 512 Cortaderia bifida, 513 Cortaderia nitida, 514, 685, 721 Cortinarius, 458 Corvidae, 556 Corytophanidae, 553 Cosmarium sphaerosporum, 666 Cosmibuena valerii, 429, 432, 442 Cotingidae, 556 Couratari, 374 Couratari guianensis, 349, 374, 482 Couropita nicaraguensis, 260 Coursetia elliptica, 255 Cracidae, 555 Crassostrea prismatica, 151 Crataeva tapia, 377, 695 Craugastor, 551 Craugastor ranoides, 551 Crax rubra, 266, 355, 393, 466 Crematogaster Crematogaster cruces, 388 Crematogaster erecta, 388 Crematogaster evallans, 388 Crematogaster longispina, 387 Crematogaster rochai, 387 Crematogaster tenuicula, 388 Crematosperma, 374 Crepidotus, 458 Crescentia alata, 256, 274, 275, 304, 315, 335, 338 Cricetidae, 558 Criconemella palustris, 76 Crinum erubescens, 696 Crocodylidae, 553 Crocodylus, 634 Crocodylus acutus, 268, 354, 356, 552, 630, 648, 712, 722 Crossopetalum tonduzii, 351 Crotalus durissus, 268 Croton, 461, 471 Croton axillaris, 257 Croton draco, 260, 350, 352, 712 Croton xalapensis, 472 Crotophaga ani, 222 Crudia acuminata, 695 Crustacea, 100, 144, 166, 271, 389 Cruziohyla calcarifer, 551 Cryptoheros, 550 Cryptoheros sajica, 389

762 Systematic Index of Scientific Names Cryptonemiales, 52 Cryptothallus hirsutus, 509 Cryptotis, 511 Cryptotis gracilis, 482 Cryptotis nigrescens, 354 Crypturellus Crypturellus cinnamomeus, 276 Crypturellus soui, 356 Crysophila, 260 Crysophila guagara, 349, 377, 696 Crysopidae, 231 Crytochrisis minor, 666 Ctenophora, 119 Ctenosaura similis, 268 Ctenotus cristatellus, 552 Cuculidae, 555 Culcita, 719 Culicia stellata, 179 Cuniculus paca, 562 Cupressus lusitanica, 478 Curatella americana, 254, 255, 350, 377 Curculionidae, 86, 228– 29, 269, 273, 329, 559 Cuvieronius, 53 Cuvieronius hyodon, 50 Cyanerpes lucidus, 554 Cyanobacteria, 119, 624, 720– 21 Cyanocompsa pallerina, 222, 223 Cyanocorax morio, 435, 719 Cyanolyca argentigula, 466, 472 Cyathea, 13, 210, 215, 719 Cyathea alfonsiana, 210, 213, 214, 713 Cyathea nesiotica, 210, 216 Cyathea notabilis, 210, 211, 213, 713 Cyatheaceae, 52, 377, 457, 461, 468, 459 Cyathus striatus, 257 Cybianthus, 461 Cyclanthaceae, 462, 469 Cyclanthus bipartitus, 696 Cyclomyces, 458 Cyclomyces iodinus, 354 Cyclopeltis semicordata, 275, 348 Cyclopes didactylus, 265 Cydista Cydista diversifolia, 257 Cydista lilacina, 349 Cylindrospermum, 660, 721 Cylindrotheca closterium, 146 Cynometra hemitomophylla, 353 Cynoscion, 154 Cynoscion squamipinnis, 155 Cyperaceae, 254, 462, 482, 510 Cyperus, 257, 721 Cyperus digitatus, 690 Cyperus giganteus, 687, 690 Cyperus holoschoenoides, 689 Cyperus imbricatus, 689 Cyperus papyrus, 687, 689 Cyphomyrmex cornutus, 387 Cyprideis pacifica, 110 Dactylococcopsis, 675 Daedalea, 458

Dahlia imperialis, 351 Dalbergia retusa, 256, 257, 276, 332, 353, 482 Daltania, 510 Danaea nodosa, 216 Danaus plexippus, 327 Daphnia laevis, 667 Dasyprocta punctata, 79– 80, 265, 274, 329, 467 Dasyproctidae, 79 Dasypus novemcinctus, 277, 339, 354, 467 Decapoda, 118, 389 Declieuxia fruticosa, 255 Delonix regia, 273 Delphinidae, 116 Dendrobates Dendrobates auratus, 392 Dendrobates granuliferus, 391 Dendrobates pumilio, 551 Dendrobatidae, 551 Dendrocincla Dendrocincla anabatina, 394 Dendrocincla fuliginosa, 554 Dendrocolaptes sanctithomae, 394, 554 Dendrocygna autumnalis, 266, 691, 692, 722 Dendroica Dendroica pensylvanica, 394 Dendroica petechia, 394 Dendroica petechia ssp. aureola, 222, 224 Dendropanax, 461, 473 Dendropanax arboreus, 348 Dendropanax querceti, 469 Dendropanax ravenii, 374, 461 Dendrophyllia oldroydae, 179 Dendropogon, 719 Dendropogonella, 463 Dendropogonella rufescens, 469 Dermanura Dermanura phaeotis, 557 Dermanura watsoni, 557 Dermaptera, 463 Dermocarpa, 624, 720 Dermochelys coriacea, 106, 220, 268, 600, 709 Desmodium, 257 Desmodus rotundus, 264 Desmophyllum dianthus, 179 Diadema Diadema antillarum, 593, 594– 95, 602, 605, 607, 609 Diadema mexicanum, 113, 169, 171, 176 Dialium guianensis, 696 Dialyanthera otoba, 698 Diaphanosoma spinulosum, 675 Diasporus ventrimaculatus, 686, 721 Dichapetalum hammelii, 461 Dichogaster, 79 Dicksonia, 719 Dicranaceae, 463 Dicranopteris Dicranopteris flexuosa, 217 Dicranopteris pectinata, 217

Dictyosphaerium ehrenbergianum, 667 Didelphimorphia, 265, 354 Didelphis Didelphis marsupialis, 354 Didelphis virginiana, 262, 339 Didymopanax pittieri, 432, 442 Dieffenbachia, 722 Dieffenbachia davidsei, 696 Dieffenbachia longispatha, 636 Digenea, 275, 634 Diglossa plumbea, 511 Dilleniaceae, 269 Dilodendron costaricense, 254, 712 Dinophyta, 119, 509 Dioscorea, 461, 469 Diospyros salicifolia, 256 Diphysa Diphysa americana, 351 Diphysa humilis, 255 Diplasiolejeunea, 463 Diplazium turubalense, 348 Diplopoda, 77, 463 Diploria strigosa, 603 Diplostephium, 500, 512 Diplura, 463 Dipsas, 552 Diptera, 231, 232, 275, 463, 511, 559, 634, 635, 639 Dipteryx panamensis, 540, 567, 568, 715 Disocactus amazonicus, 275 Disterigma, 461, 512 Disterigma humboldtii, 462, 514 Dolichoderus Dolichoderus curvilobus, 387 Dolichoderus lamellosus, 387 Dolichoderus laminatus, 387 Dolichoderus validus, 387 Donax Donax denticulatus, 600 Donax panamensis, 145 Dormitator Dormitator latifrons, 269, 389 Dormitator maculatus, 547 Dorosoma chavesi, 547 Doryfera ludoviciae, 469 Dorymyrmex, 387 Draba, 500, 512, 720 Draba jorullensis, 510 Drimys, 52, 458, 718 Drimys granadensis, 469, 475, 514 Drymarchon, 552 Drymobius melanotropis, 434 Dryopteris, 458 Dysithammus striaticeps, 554 Dysodia speculifera, 323 Echeverria australis, 429 Echimyidae, 79 Echiniscus Echiniscus arctomys, 511 Echiniscus bigranulatus, 511 Echinochloa polystachya, 689

Systematic Index of Scientific Names 763 Echinodorus Echinodorus paniculatus, 690, 692, 721 Echinodorus subalatus ssp. andrieuxii, 256, 689 Echinometra lucunter, 592, 593 Echinopepon paniculatus, 257 Echinothrix diadema, 165 Eciton, 327, 328 Eciton burchelli, 321, 394 Ecitoninae, 433 Ectatomma Ectatomma edentatum, 388 Ectatomma ruidum, 561 Ectatommini, 561 Ectophylla alba, 557 Egretta alba, 692, 692, 722 Ehretia latifolia, 351 Eichhornia, 721 Eichhornia azurea, 623 Eichhornia crassipes, 257, 258, 349, 349, 377, 623, 690 Eichhornia heterosperma, 623, 690 Eira barbara, 265, 467, 557 Elaeis Elaeis guianensis, 377 Elaeis oleifera, 377, 696 Elanoides forficatus, 466 Elaphoglossum, 347, 462, 468, 510, 686, 718 Elaphoglossum adrianae, 461 Elaphoglossum reptans, 214 Elaphoglossum squamipes, 462 Elapidae, 553 Eleocharis, 721 Eleocharis acicularis, 514 Eleocharis interstincta, 690 Eleocharis mutata, 257, 690 Eleotridae, 269, 389, 546, 547, 548, 634 Eleotris, 220 Eleotris amblyopsis, 547 Eleotris picta, 220, 389 Eleotris pisonis, 547 Eleotris tubularis, 220 Eleutherodactylidae, 551, 686 Eleutherodactylus, 356, 434, 464, 719 Eleutherodactylus melanostictus, 464 Eleutherodactylus taurus, 392 Eleutherodactylus vocator, 391 Elleanthus, 275, 462, 718 Elodea canadensis, 668 Elopidae, 546, 547 Emberizidae, 196, 466, 556, 719 Embydidae, 630, 722 Emerita rathbunae, 145 Emydidae, 553 Encyclia, 275 Encyclia cordigera, 275 Encyonema Encyonema lunatum, 674 Encyonema silesiacum, 677 Endopachys grayi, 179 Engraulis, 154 Entada gigas, 213

Enterolobium Enterolobium cyclocarpium, 81, 259, 261, 265, 272, 274, 319, 333, 335, 338, 348, 712, 713 Enterolobium schomburkgii, 319 Enyo ocypete, 325 Eois, 560 Ephemeroptera, 633, 634, 635 Epicharis, 271, 713 Epicrates, 552 Epidendrum, 275, 347, 462, 718 Epidendrum cocoense, 211, 213 Epidendrum insularum, 211, 213 Epidendrum jimenezii, 211 Epidendrum platystigma, 462 Epimecis, 560 Epinannolene pittieri, 235 Epinecrophyla fulviventris, 554 Epiperipatus biolleyi, 78 Equisetum aff. giganteum, 52 Equus, 53 Equus conversidens, 51 Eragrostis hypnoides, 689 Erebidae, 324 Eremolepidaceae, 462 Eremotherium, 50 Erethizontidae, 79 Eretmochelys imbricata, 106, 152, 220, 600, 709 Ericaceae, 52, 432, 458, 460, 461, 462, 467, 468, 469, 473, 474, 482, 492, 499, 510, 719 Erinnyis obscura, 230 Erioderma, 509 Eryngium scaposum, 512 Erythrina, 75– 76, 78 Erythrina costaricensis, 351 Erythrina fusca, 214 Erythrina lanceolata, 696, 697 Erythrina poeppigiana, 85, 352 Erythrochiton gymnanthus, 349 Erythrolamprus, 552 Erythroxylum havanense, 257, 259, 260 Escallonia, 458, 467, 500, 512, 514, 718 Escallonia myrtilioides, 474, 501, 685, 721 Escalloniaceae, 499 Eschweilera calyculata, 697 Esenbeckia berlandieri, 256 Eucalanus Eucalanus attenuatus, 147 Eucalanus elongatus, 147 Eucalyptus, 478 Euchlanis dilatata, 675 Eucometis penicillata, 394 Eucynorta insularis, 231 Eudocimus albus, 267 Eugenia, 213, 438, 469, 719 Eugenia basilaris, 461 Eugenia cocosensis, 213, 217, 713 Eugenia hiraefolia, 353 Eugenia salamensis, 482 Eugerres plumieri, 547 Euglenophyta, 690

Euglossinae, 271 Eulepidotis, 232 Eumomota superciliosa, 266 Eumycota, 509 Eunica monima, 270, 325 Eunotia, 624, 669, 721 Eunotia guyanense, 670 Eunotia intermedia, 668 Eunotia minor, 668 Euphausicea, 592 Euphonia gouldi, 561 Euphorbiaceae, 254, 347, 348, 457, 461, 468, 539 Euphorbia schlechtendalii, 255, 260, 429 Eurema daira, 270, 325 Eurypyga helis, 630 Eurypygidae, 555 Eurytides, 270 Eurytides epidaus, 270 Eurytides philolaus, 270 Euscirrhopterus poeyi, 323 Eutelia furcata, 323 Euterpe, 696 Euterpe precatoria, 699 Euterpe precatoria var. longevaginata, 211, 213, 713 Eutetramorus tetrasporus, 666, 672 Everniastrum, 509 Evolvulus alsinoides, 255 Excirolana braziliensis, 600 Fabaceae, 254, 257, 259, 270, 276, 300, 328, 347, 348, 349, 350, 374, 473, 539, 559, 696, 712 See also Leguminosae Fagaceae, 461 Falconidae, 555 Falco peregrinus, 355 Faramea, 349, 457 Farfantepenaeus, 154 Farfantepenaeus brasiliensis, 594 Farfantepenaeus brevirostris, 153 Farfantepenaeus californiense, 153 Felis Felis onca, 398, 715 Felis pardalis, 686 Felis silvestris, 224, 226 Festuca, 500, 510, 512 Festuca dolichophylla, 512 Ficus, 230, 254, 347, 374, 397, 402, 461, 471, 561, 712, 718, 722 Ficus costaricana, 351, 352, 712 Ficus crassiuscula, 431, 432, 718 Ficus glabrata, 561 Ficus insipida, 349, 561, 635– 36 Ficus jimenezi, 350, 351 Ficus obtusifolia, 350 Ficus padifolia, 52 Ficus pertusa, 213, 230, 438, 439, 713 Ficus talamanca, 52 Ficus tuerckheimii, 431 Ficus velutina, 351 Fidicina mannifera, 559

764 Systematic Index of Scientific Names Fimbristylis spadicea, 687 Fissidens, 463 Fissidens juruensis var. juruensis, 256 Fissidens radicans, 256 Fissidens yucatanensis, 256 Fistulina, 458 Fistulina hepatica, 458 Flacourtiaceae, 348 Fomes, 458 Fomes fasciatus, 354 Fomitopsis Fomitopsis cupreorosea, 354 Fomitopsis feei, 354 Foraminifera, 61, 119, 144, 710 Formicariidae, 555 Formicarius analis, 394 Formicidae, 228, 271, 274 Fragilaria Fragilaria exigua, 677 Fragilaria tenera, 676, 677 Frankia, 76 Frankia acuminata, 75, 76, 76 Fregata minor, 170, 222 Freziera, 471 Freziera calophylla, 214 Freziera candicans, 350, 471, 472 Freziera grisebachi, 377 Fringilidae, 556 Frullania, 463, 510, 685, 719 Frustulia, 624, 721 Frustulia saxonica, 669, 670 Fuchsia, 458, 469, 471 Fuchsia paniculata, 471, 472 Fuirena umbellata, 689 Fulgora laternaria, 559 Fulgoridae, 559 Fungi, 119 Fungia Fungia curvata, 113, 179 Fungia distorta, 179 Furcraea cabuya, 429 Furipterus horrens, 557 Furnariidae, 555 Fuscocerrena, 458 Gaiadendron, 458 Gaiadendron punctatum, 462 Galbulidae, 555 Galerina, 458 Galictis vittata, 277 Gallus gallus, 196 Gambusia nicaraguensis, 548 Ganoderma, 458 Garcinia intermedia, 256, 351, 353 Gardineroseris planulata, 113, 175, 179 Garrya, 508, 514 Garrya laurifolia, 501 Gaultheria, 458, 461, 512 Geastrum Geastrum javanicum, 257 Geastrum saccatum, 257 Gecarcinidae, 79, 232, 385, 715 Gecarcinus quadratus, 79, 234, 373, 385, 394

Gekkonidae, 553 Gentiana, 508 Gentianaceae, 52, 216 Geometridae, 231 Geomyidae, 79 Geonoma, 260, 461, 469, 719 Geonoma hoffmanniana, 469 Geonoma surtuba, 431 Geranium, 458 Gerreidae, 547 Gesneriaceae, 462, 469 Gigaspora, 440 Gliricidia sepium, 255 Gloeocapsa, 666 Glomus, 440 Glossophaga, 329 Glossophaga leachii, 265 Glossophaga soricina, 265, 272, 338 Glossotherium aff. tropicorum, 50 Glottidia audebarti, 145 Glycine max, 75 Glyphorynchus spirurus, 392– 93 Glyptotherium Glyptotherium aff. texanum, 50 Glyptotherium cf. arizonae, 50 Glyricidia sepium, 85 Gmelina arborea, 73, 334– 35, 377, 402, 543 Gnaphalium, 476, 720 Gnaphalium americanum, 512 Gobiesocidae, 546, 548 Gobiesox Gobiesox fulvus, 220 Gobiesox nudus, 546, 548 Gobiidae, 389, 546, 547, 548 Gobiomorus Gobiomorus dormitor, 546, 547, 548 Gobiomorus maculatus, 269, 389 Gobiomorus polylepis, 268 Goethalsia meiantha, 353 Gomphichis adnata, 686 Gomphonema Gomphonema gracile, 666, 672 Gomphonema parvulum, 626 Gomphrena, 256 Goniolithon, 52 Gonocalyx costaricensis, 432 Gonodonta pyrgo, 511 Gonyaulax digitale, 146 Gordonia frutiscosa, 350, 377 Gorgonia, 605 Gorgonia flabellum, 593 Grallariidae, 556 Grammadenia, 461 Grammadenia myricoides, 81 Grammitis, 52, 432, 462 Grandiarca grandis, 151, 151, 152, 153 Graphidales, 509 Grapsus grapsus, 174, 233 Grias Grias cauliflora, 699 Grias fendleri, 377, 695, 696, 697, 698 Guadua paniculata, 256

Guaiacum sanctum, 259, 260, 276 Guarea, 432, 473, 711, 718, 719 Guarea glabra, 272 Guarea kunthiana, 432, 438 Guarea tonduzii, 469 Guatteria, 471 Guatteria amphifolia, 695 Guatteria oliviformis, 469 Guazuma, 294 Guazuma ulmifolia, 254, 261, 303, 334, 338, 350, 712 Guettarda, 471 Guettarda macrosperma, 353 Guettarda poasana, 438, 442 Gunnera, 440, 718 Gunnera insignis, 442 Guzmania sanguinea, 213, 216 Gygis alba, 222, 226 Gymnocichla nudiceps, 554 Gymnophthalmidae, 553 Gymnopithys leucaspis, 394, 554 Gymnopus, 458 Gymnospermae, 461 Gymnostomiella vernicosa, 256 Gymnotidae, 268, 547, 548, 692 Gymnotus Gymnotus cylindricus, 547, 548 Gymnotus maculosus, 268, 547 Gynerium sagittatum, 687 Gyrosigma spenceri, 677 Habia Habia atrimaxillaris, 392, 715– 16 Habia fuscicauda, 554 Habronematoidea, 276 Haematoloechidae, 275 Haematoloechus meridionalis, 275 Haematoxylum brasiletto, 255, 296 Haemulidae, 546, 547, 548 Halictinae, 271 Halipegus eschi, 275 Halodule wrightii, 602 Halophila Halophila baillonii, 111 Halophila decipiens, 602 Hampea appendiculata, 442 Harpella tica, 634 Harpia harpyia, 394, 716 Hauya elegans, 351, 352 Hebeloma, 257 Hedyosmum, 52 Hedyosmum brenesii, 377 Hedyosmum racemosum, 214 Heisteria longipes, 374, 715 Helianthemum, 508 Helicarionidae, 511 Heliconaceae, 396 Heliconia, 52, 557 Heliconiinae, 383 Heliconius, 379, 384, 384, 715 Heliconius cydno, 383 Heliconius hewitsoni, 383, 386 Heliconius pachinus, 383, 386

Systematic Index of Scientific Names 765 Heliconius sapho, 383 Heliconius sara, 386 Heliocarpus appendiculatus, 442 Heliornis fulica, 630 Heliornithidae, 555 Hemicyclops thalassius, 147 Hemidactylus Hemidactylus frenatus, 552 Hemidactylus garnotti, 552 Hemileucinae, 270 Hemiptera, 231, 269 Hemiuridae, 275 Henriettella fascicularis, 213, 713 Hepaticae, 211, 431 Herbertus, 463 Herichthys, 550 Hernandia didymantha, 697 Heros, 550 Herotilapia multispinosa, 269, 547, 548 Herpetotheres cachinnans, 339 Hesperiidae, 270, 275 Hesperomeles, 514 Hesperomeles heterophylla, 512, 685, 721 Hesperomeles obtusifolia, 514 Heterocarpus vicarius, 149, 153– 54 Heterodermia, 459, 460, 509 Heterokontophyta, 509 Heteromyidae, 79, 80, 467, 719 Heteromys, 467 Heteromys desmarestianus, 466 Heteromys oresterus, 482 Heteropoda, 592 Heteropogon contortus, 256 Heteroscyphus, 463 Heterospingus rubifrons, 553 Hexagonia glaber, 257 Hexaplex radix, 153 Hexarthra intermedia, 675 Hibiscus pernambucensis, 353 Hidrolea elatior, 257 Hieracium, 508, 721 Hieracium irasuense, 514, 686 Hieronyma Hieronyma alchorneoides, 543, 715 Hieronyma oblonga, 348 Hillia, 462 Hillia loranthoides, 377 Hippolyte obliquimanus, 594 Hirundinidae, 556 Hispinae, 559 Historis Historis acheronta, 325 Historis odius, 227– 28, 230 Hoffmannia, 349, 457, 461 Hoffmannia piratarum, 216 Holochroa ochra, 323 Holomitrium, 463 Homalium racemosum, 695 Homoptera, 231, 269, 559 Homo sapiens, 335 Hortensia similis, 511 Huberodendron, 374

Huperzia, 462, 510 Huperzia branchiata, 211, 213 Huperzia pittieri, 213 Hura, 294 Hura crepitans, 348 Hyalella azteca, 666 Hydrangea, 461, 469, 719 Hydrangea peruviana, 432 Hydrilla, 696 Hydrocharitaceae, 668 Hydrocotyle, 476 Hydrocotyle umbellata, 214 Hydrolea spinosa, 256, 689 Hydrozoa, 172 Hygrocybe, 458 Hygropus, 458 Hyla Hyla calypsa, 634 Hyla picadoi, 464 Hyla rosenbergi, 391, 392 Hylesia lineata, 270 Hylidae, 551, 628 Hylocereus costaricensis, 275, 712 Hylocichla mustelina, 394, 561 Hyloctistes subulatus, 393 Hylophilus Hylophilus decurtatus, 554 Hylophilus ochraceiceps, 393 Hylophylax nevioides, 554 Hymenachne, 377 Hymenachne amplexicaulis, 687, 689 Hymenaea, 711 Hymenaea courbaril, 254, 273– 74, 328– 29, 330, 333, 353, 712 Hymenocalis litoralis, 696 Hymenochne amplexicaulis, 623 Hymenolobium mesoamericanum, 540, 715 Hymenophyllum, 52, 462, 718 Hymenoptera, 228, 271, 275, 463, 511, 559 Hyparrhenia rufa, 255, 276, 300, 306, 306, 335, 713 Hyperbaena Hyperbaena eladioana, 350 Hyperbaena tonduzii, 353 Hypericum, 52, 458, 461, 500, 508, 512 Hypericum cardonae, 513 Hypericum costaricense, 512 Hypericum irazuense, 512, 514 Hypericum stenopetalum, 512 Hypericum strictum, 474, 512, 514, 686, 721 Hyphessobrycon Hyphessobrycon savagei, 389 Hyphessobrycon tortuguerae, 547 Hypholoma, 458 Hypnum, 463 Hypochoeris, 512 Hypolytrum amplissimum, 213 Hypopomus occidentalis, 548 Hypotrachyna, 458, 459, 460, 509 Hypsibius Hypsibius convergens, 511 Hypsibius scoticus, 511

Hypsophrys nicaraguense, 548 Hyptis, 461 Icacinaceae, 292 Icteridae, 196, 556 Icterus Icterus mesomelas, 196 Icterus pectoralis, 196, 221, 222, 265 Iguana, 552 Iguana iguana, 268, 339, 558, 712 Iguanidae, 553 Ilex, 52, 81, 471, 719 Ilex lamprophylla, 468, 469 Ilex pallida, 469, 471, 472, 482 Ilex vulcanicola, 482 Iltisia, 509, 720 Imantodes, 552 Impatiens sultana, 438 Indigofera, 300 Inga, 347, 440, 461, 534, 539, 695, 715, 718 Inga bella, 374 Inga edulis, 352 Inga jimenezii, 349 Inga punctata, 351, 352 Inga sheroliensis, 52 Inga vera, 327, 697 Inocybe, 458 Insectivora, 354, 511 Ipomoea, 215, 217, 257, 687, 721 Ipomoea alba, 230 Ipomoea batatas, 86 Ipomoea digitata, 338 Ipomoea indica, 230 Ipomoea pes-caprae, 215, 230 Ipomoea philomega, 230 Iriartea Iriartea deltoidea, 562, 697, 699 Iriartea gigantea, 374, 715 Iryanthera, 374 Ischnochiton dispar, 107 Ischnocodia annulus, 269 Isoetes, 513, 721 Isoetes panamensis, 256 Isoetes storkii, 672, 686, 721 Isopoda, 463 Itaballia demophile, 270 Ixora Ixora finlaysoniana, 697 Ixora nicaraguensis, 695 Jabiru mycteria, 266, 691, 692, 722 Jacana spinosa, 276, 354, 630 Jacanidae, 555 Jacquemontia mexicana, 255 Jacquinia nervosa, 256, 257 Jamesonia, 52 Jatropha costaricensis, 255 Javania cailleti, 179 Jessea, 509, 720 Johngarthia cocoensis, 232 Joturus pichardi, 548, 640, 642 Juglans olanchana, 52 Juncaceae, 482, 686

766 Systematic Index of Scientific Names Junco vulcani, 511 Juncus, 686, 721 Jussiaea, 687 Jussiaea latifolia, 696 Justicia comata, 689 Karatophyllum bromeliodes, 52 Karwinskia calderoni, 255 Keratella, 667 Keratella americana, 675 Killinga nudiceps, 211 Kinorhyncha, 119, 144 Kinosternidae, 553, 630, 722 Kinosternon, 552 Kinosternon leucostomum, 630 Kinosternon scorpioides, 268 Kirchneriella, 672 Kiwa puravida, 118 Kogiidae, 116 Kohleria spicata, 216 Krameria ixine, 255 Kricogonia lyside, 270 Kronitta, 148 Laccaria, 458 Lachemilla, 510, 513 Lachesis, 552 Lachesis melanocephala, 357, 391, 391, 392, 712 Lacistema aggregatum, 260, 261 Lactarius, 458 Ladenbergia Ladenbergia brenesii, 469 Ladenbergia sericophylla, 377 Laelia, 275 Laelia rubescens, 275 Laestadia, 509, 720 Laetiporus, 458 Lagomorpha, 354, 511 Laguncularia racemosa, 109, 143, 353, 377, 599, 710 Lamellibrachia, 117 Lampropeltis, 552 Lampyridae, 269, 313 Lanio leucothorax, 393, 554 Laportea aestuans, 216 Lasciacis, 721 Lasciacis procerruna, 687 Laterallus ambigularis, 222 Laubierus alivini, 118 Lauraceae, 52, 348, 350, 352, 387, 438, 439, 457, 460, 461, 467, 468, 471, 553, 719 Lecane, 675 Lecanorales, 509 Leccinum, 458 Lecythis ampla, 715 Legatus leucophaius, 553 Leguminosae, 273, 274, 473 See also Fabaceae Leiuperidae, 551 Lejeunea, 463 Lejeuneaceae, 211, 463 Lemna, 349

Lennoa madreporoides, 256 Lentibulariaceae, 668 Leopardus, 511 Leopardus pardalis, 262, 467, 511, 557 Leopardus tigrinus, 482 Leopardus wiedii, 262, 467 Lepanthes, 462, 718 Lepidoblepharis, 552 Lepidobotryaceae, 374 Lepidochelys olivacea, 106, 220, 268, 709 Lepidocolaptes affinis, 466 Lepidoptera, 6, 229– 30, 231, 270, 275, 511, 557, 559– 60 Lepidozia, 463 Lepidoziaceae, 463 Lepisosteidae, 547, 692 Leptobasis guanacaste, 633 Leptodactylidae, 551 Leptodeira, 552 Leptodeira rubricata, 392 Leptodesmus folium, 235 Leptodontium, 463, 510 Leptogium, 440, 460, 509 Leptophis, 552 Leptoscyphus, 510 Leptoseris Leptoseris papyracea, 113, 179 Leptoseris scabra, 165, 175, 179 Letis, 325 Leucauge argyra, 232 Leucobryum, 463 Lewisia, 512, 720 Lewisia megarhiza, 510 Liabum, 462 Libellula, 666 Licania Licania arborea, 254, 260, 712 Licania operculipetala, 353 Ligia, 174 Limacodidae, 323 Limnephilus, 666 Limnobium laevigatum, 349, 690 Lingula, 145 Liomys salvini, 262, 274 Lipaugus unirufus, 393 Lithophorella, 52 Lithothamnion, 52 Lithothamnion corallioides, 114 Littorina modesta, 174 Littorinidae, 106 Lobaria, 458, 459 Lobaria pulmonaria, 459 Lobariella pallida, 686 Loganiaceae, 260 Lonchocarpus, 257 Lonchocarpus hughesii, 259 Lonchocarpus minimiflorus, 257, 482 Longidorus, 76 Lontra Lontra longicaudis, 482, 557, 630 Lontra provocax, 277 See also Lutra Lophiodes spilurus, 149

Lophocolea, 463 Lophosoria, 719 Loranthaceae, 461, 462, 469 Loricariidae, 391, 546, 628 Lozania mutisiana, 469 Ludwigia, 377, 696 Ludwigia inclinata, 690 Ludwigia pepliodes, 689, 690 Ludwigia sedioides, 689 Luehea, 254, 712 Luehea candida, 254, 712 Luehea seemannii, 349, 377, 695, 696, 699 Luehea speciosa, 254 Lupinus, 500 Luticola mutica, 669 Lutjanidae, 148, 711 Lutjanus, 154, 389 Lutjanus argentiventris, 389 Lutjanus colorado, 389 Lutjanus novemfasciatus, 389, 390 Lutra, 634 Lutra longicaudis, 277, 722 See also Lontra Luziola subintegra, 689 Lycopodium, 462, 510 Lycopodium brachiatum, 211 Lygaidae, 231 Lygodium venustum, 275 Lyngbya, 624, 634, 720 Lysiloma Lysiloma auritum, 272 Lysiloma discaritu, 351 Lysiloma divaricatum, 257 Lysipomia, 513, 720 Lysipomia acaulis, 510 Lytechinus variegatus, 592 Mabuetia guatemalensis, 696 Machaerium, 461 Machaerium kegelii, 256 Machaerium robiniifolium, 257 Macleania, 461, 469, 719 Macleania rupestris, 462, 685 Macleania talamancensis, 461 Macrobiotus occidentalis, 511 Macrobrachium, 233, 389, 630, 631, 632– 33, 634, 642, 715, 722 Macrobrachium acanthurus, 632 Macrobrachium amazonicum, 632 Macrobrachium americanum, 233– 34, 271, 632, 713 Macrobrachium carcinus, 631, 632 Macrobrachium cocoensis, 234– 35 Macrobrachium digueti, 632 Macrobrachium hancocki, 234, 632 Macrobrachium heterochirus, 632 Macrobrachium occidentale, 632 Macrobrachium olfersii, 632, 633 Macrobrachium panamense, 632 Macrobrachium tenellum, 632 Macrocnemum roseum, 348 Macrolepidoptera, 229– 30 Macromitrium, 463, 510

Systematic Index of Scientific Names 767 Magnolia, 457, 718 Magnolia poasana, 469 Magnolia sororum, 469 Mahonia, 508 Maianthemum, 462, 469 Mallomonas Mallomonas acaroides, 672, 676 Mallomonas crassisquama, 672, 676 Mallomonas cyathellata var. chilensis, 672 Malpighiaceae, 254 Malvaceae, 254, 257, 539 Malvaviscus arborea, 338 Mammuthus columbi, 50, 51– 52 Manacus candei, 561 Manduca Manduca dilucida, 314, 323 Manduca lanuginosa, 314, 323 Manicaria, 696 Manicaria saccifera, 694– 95, 721 Manihot Manihot aesculifolia, 256 Manihot esculenta, 534 Manilkara, 294, 374, 715 Manilkara chicle, 256, 260, 273, 319, 333 Manilkara zapota, 254, 319, 712 Mantodea, 266 Marantaceae, 560 Marasmiellus, 458 Marasmius, 458 Marcgravia Marcgravia brownei, 432 Marcgravia waferi, 211 Margarornis rubiginosus, 466 Marmosa mexicana, 354 Marpesia petreus, 270 Marsilea deflexa, 256 Matayba oppositifolia, 350 Mauria, 473 Mauria heterophylla, 351 Maxillaria, 347, 462, 718 Maxillaria adendrobium, 211 Maxillaria biolleyi, 462 Maxillaria parviflora, 211 Maytenus, 353 Mazama Mazama americana, 354, 467, 482, 559, 686 Mazama temama, 559 Mediomastus californiensis, 110, 144, 145 Megabalanus coccopoma, 173 Megachilinae, 271 Megalops atlanticus, 546, 547, 626, 640 Megalopygidae, 323 Megaptera novaeangliae, 116, 154, 169, 170 Melaneris chagresi, 558 Melanerpes formicivorus, 466 Melanthera nivea, 255 Melastomataceae, 213, 347, 348, 354, 439, 460, 461, 462, 468, 473, 539, 561, 719 Meliaceae, 348, 468 Meliosma, 457, 718 Meliosma glabrata, 469 Meliosma vernicosa, 438 Meliponinae, 271

Mellitella stokesii, 110 Melloa, 257 Melocactus curvispinus, 256 Meloidogyne incognita, 76 Melongena, 153 Memphis, 270 Memphis forreri, 270 Menegazzia neotropica, 686 Mephitis macoura, 262 Merismopedia, 675 Merismopedia cf. chondroidea, 667 Merismopedia tenuissima, 667 Mesaspis monticola, 464, 511, 719 Mesembrinibus cayennensis, 630 Mesocheira, 271, 712 Mesocyclops thermocyclopoides, 660, 721 Mesoplia, 271, 713 Meteoriaceae, 463 Meteoridium, 463 Metzgeria, 510 Miconia, 347, 460, 461, 468, 469, 471, 473, 500, 512, 514, 539, 715, 718, 719 Miconia affinis, 561 Miconia argentea, 353 Miconia centrodesma, 561 Miconia dodecandra, 213, 713 Miconia kappellei, 461 Miconia lauriformis, 469 Miconia nervosa, 561 Miconia pittieri, 469 Miconia tonduzii, 472, 474 Microcerculus Microcerculus marginatus, 552 Microcerculus philometa, 552 Microcyclops Microcyclops ceibaensis, 667 Microcyclops varicans, 675 Microcystis, 672 Microhylidae, 551 Microrhopias quixensis, 393, 554 Microspora, 624 Microtenochira ferranti, 269 Microtia elva, 270 Microtropis, 457 Microtropis occidentalis, 469 Microtylopteryx hebardi, 559 Micrurus clarki, 392 Mikania, 461 Milnesium tardigradum, 511 Mimidae, 556 Mimosa Mimosa aspereta, 257 Mimosa pigra, 257, 691 Mimosa trichephala, 255 Mimosa xanthocentra, 257 Mimosoideae, 274 Minquartia guianensis, 374, 715 Mionectes oleagineus, 393, 561 Mitrospingus cassinii, 554 Mixonera, 52 Mixotoxodon larensis, 51, 52 Modisimus coco, 231 Mollinedia, 468

Mollusca, 119, 144 Momotidae, 555 Monera, 6 Monimiaceae, 468 Monnina, 471, 514 Monnina crepinii, 473 Monnina xalapensis, 472 Monochaetum, 442, 461, 718 Monorhaphidium griffithii, 665, 721 Monstera, 462 Montanoa guatemalensis, 351 Montricardia, 721 Montricardia arborescens, 687, 696, 697 Mora, 696 Mora oleifera, 353, 377, 696 Moraceae, 52, 230, 254, 348, 349, 350, 396, 468 Morphnus guianensis, 355, 394 Mougeotia, 667 Mouriri, 696 Mucuma Mucuma mutisiana, 214 Mucuma sloanei, 214 Muehlenbeckia, 469 Mugilidae, 269, 389, 546, 547, 548 Muhlenbergia, 500 Muhlenbergia flabellata, 512 Muntingia calabura, 339 Muridae, 5, 79– 80, 467, 719 Musa, 335 Musa acuminata, 377 Musa velutina, 541 Musci, 211 Mustela frenata, 467 Mustelidae, 5 Mustelus Mustelus dorsalis, 154, 711 Mustelus lunulatus, 154, 711 Myadestes melanops, 466 Mycena, 458 Mycorrhizae, 75, 87 Mycosphaerella musicola, 564 Mycteria americana, 276, 699, 702 Myiobius Myiobius sulphureipygius, 554 Myiobius torquatus, 466 Myiodynastes maculatus, 553 Myrcia Myrcia oerstediana, 469 Myrcia splendens, 352 Myrcianthes, 718 Myrcianthes fragrans, 352, 353, 712 Myrcianthes rhopaloides, 472 Myrcianthes storkii, 469 Myrica, 52, 440, 471, 514, 718 Myrica phanerodonta, 442 Myrica pubescens, 472 Myrmeciza Myrmeciza exsul, 393 Myrmeciza immaculata, 554 Myrmecophaga, 5 Myrmecophaga tridactyla, 265, 277, 331, 555

768 Systematic Index of Scientific Names Myrmecophila, 275 Myrmelachista, 433, 719 Myrmelachista lauropacifica, 387 Myrmotherula Myrmotherula axillaris, 554 Myrmotherula fulviventris, 393 Myrmotherula quixensis, 393 Myroxylon balsamum, 351, 482 Myrrhidendron, 512 Myrrhidendron chirropoense, 513 Myrsinaceae, 217, 269, 457, 461, 467, 468 Myrsine, 461, 500, 514, 718 Myrsine coriacea, 469, 685, 721 Myrsine pittieri, 469, 501 Myrtaceae, 217, 348 Myscelia pattenia, 325 Mytella guyanensis, 153 Myxomycetes, 208– 9 Najas guadalupensis, 256 Nasua narica, 264, 466, 557 Nasutitermes, 339 Natalus stramineus, 265 Natica, 145 Natica unifasciata, 145 Natsushima sashai, 118 Navanax Navanax aenigmaticus, 103, 594 Navanax gemmatus, 594 Navicula, 677, 721 Navicula cf. laevissima, 676 Navicula cryptocephala, 677 Navicula incarum, 624, 626 Navicula ingapirca, 624, 626 Navicula kohlenbachii, 624, 626 Navicula radiosa, 677 Navicula seminulum, 626 Navicula subminuscula, 626 Neckera, 463 Neckeraceae, 463 Nectandra, 81, 461, 469, 471 Nectandra aerolata, 52 Nectandra cufodontisii, 471, 472, 474 Nectandra membranacea, 260 Nectandra silicifolia, 353 Nectandra woodringi, 52 Neea laetevirens, 539 Neetroplus nematopus, 548, 549 Nematoda, 119, 144, 276 Nemertea, 119 Neoheterandria umbratilis, 547, 548, 558 Neomorphus geoffroyi, 394, 554 Neonicholsonia watsonii, 260 Neotuerta sabulosa, 323 Nephroma helveticum, 686 Nephronias tempisquensis, 693 Neptunia, 721 Neptunia natans, 257, 690 Neptunia plena, 256, 689 Nerita Nerita funiculata, 173 Nerita scabricosta, 173– 74 Neritidae, 106

Neritina latissima, 389, 635 Nesiteria concinna, 350 Nesotriccus ridgwayi, 222 Neuroptera, 231, 463 Neusticurus apodeumus, 392 Newtonia suaveolens, 353 Nitzschia Nitzschia amphibia, 664 Nitzschia cf. vitrea, 676 Nitzschia frustulum, 664 Nitzschia palea, 626 Nitzschia pungens, 146 Noctilio Noctilio albiventris, 630 Noctilio leporinus, 630, 722 Noctilionidae, 630 Noctiluca scintillans, 146 Nodilittorina modesta, 173– 74 Norops, 552 Norops altae, 435 Norops aquaticus, 392 Norops intermedius, 435 Norops oxylophus, 276 Norops pentaprion, 267 Norops polylepis, 392 Norops townsendi, 220, 221 Norops tropidolepis, 435 Notonecta, 666 Numida meleagris, 196 Nyctaginaceae, 539, 559 Nyctibiidae, 555 Nyctomys Nyctomys nyctomys, 339 Nyctomys sumichrasti, 558 Nymphaea, 257, 721 Nymphaea amazonum, 690 Nymphaea ampla, 689 Nymphaea blanda, 687, 689 Nymphaea prolifera, 257 Nymphaea pulchella, 690 Nymphalidae, 270, 386 Nymphoides humboldtianum, 690 Ochetomyrmicini, 561 Ochroma, 381, 382, 715 Ochroma lagopus, 339 Ochroma pyramidale, 214, 261, 349, 353 Ochrophyta, 119, 509 Ocotea, 81, 347, 387, 461, 468, 469, 471, 695, 711, 718, 719 Ocotea austinii, 472 Ocotea cf. viridiflora, 429 Ocotea endresiana, 438, 439 Ocotea insularis, 211, 213, 216, 472, 713 Ocotea pharomachrosorum, 472, 472 Ocotea pittieri, 472, 472 Ocotea praetermissa, 474 Ocotea pseudopalmana, 472 Ocotea veraguensis, 256 Ocypode gaudichaudii, 232 Ocypodidae, 232 Odocoileus virginianus, 196, 224, 265, 559 Odonata, 269, 633

Odontomachus, 561 Odontomachus erythrocephalus, 387 Odontophoridae, 555 Oeceoclades maculata, 335 Oedipina alleni, 391 Oedogonium, 624, 720– 21 Oligochaeta, 463 Olivella semistriata, 145 Olmedia aspera, 349 Ommatolampinae, 559 Oncaea venusta, 147 Oncidium, 275 Oncidium cebolleta, 275 Oncorhynchus, 336 Oncorhynchus mykiss, 463, 719 Onychophora, 78 Onychoprion fuscatus, 222 Oocystis, 667, 672 Oophaga pumilio, 551 Operculina triqueta, 257 Ophisternon aenigmaticum, 692 Ophistonema, 154 Opiliones, 231 Opisthacanthus valerioi, 227, 229, 231 Oporornis Oporornis formosus, 394 Oporornis philadelphia, 394 Opuntia Opuntia cochenillifera, 256 Opuntia elatior, 257 Opuntia guatemalensis, 256 Opuntia lutea, 260 Orchidaceae, 347, 354, 462, 468, 469, 509, 510, 539, 540 Oreobolus, 512 Oreobolus goeppingeri, 513 Oreochromis, 336, 649, 692 Oreochromis aereus, 648 Oreochromis mossambicus, 648 Oreochromis niloticus, 648, 692, 722 Oreomunnea pterocarpa, 377 Oreopanax, 461, 462, 468, 469, 473, 501, 514, 718 Oreopanax capitatus, 473, 474 Oreopanax nubigenus, 429, 432, 442, 473, 474 Oreopanax oerstedianus, 482 Ormilthidium adendrobium, 211 Ormosia macrocalyx, 260 Oropogon, 509 Orthalicidae, 511 Orthogeomys Orthogeomys heterodus, 482 Orthogeomys underwoodii, 354 Orthomorpha coactata, 235 Orthoptera, 231, 463 Orthotrichaceae, 463 Orthrosanthus, 512 Oryctolagus cuniculus, 196 Oryza Oryza latifolia, 623, 687, 689 Oryza sativa, 377 Oryzobus nuttingi, 553

Systematic Index of Scientific Names 769 Oryzomys, 467 Oryzomys albigularis, 440, 466 Osaecilia osa, 391 Osa pulchra, 374, 383 Oscillatoria, 624, 721 Ossaea Ossaea bracteata, 216 Ossaea macrophylla, 216 Osteopilus septentrionalis, 551 Ostracoda, 144, 710 Ostrea iridescens, 151– 52 Otoba novogranatensis, 348, 699 Ottoa oenanthiodes, 513 Ouratea, 699 Ouratea lucens, 256 Oxalis, 458 Oxalis frutescens, 255 Oxybelis, 552 Oxycarium cubense, 689– 90 Oxydia hogei, 231 Oxyethira, 666 Pacarina, 269 Pachira Pachira aquatica, 697, 699 Pachira quinata, 254, 257, 259, 260, 262, 272, 279, 377, 712 See also Bombacopsis; Pochota quinata Pachyarmatherium, 50 Pachycondyla, 561 Pachycondyla bugabensis, 387 Pachycondyla harpax, 387 Pachycondyla theresiae, 387 Pachylia ficus, 230, 325 Paepalanthus, 721 Paepalanthus costaricensis, 514, 686 Paguridae, 232 Pagurus californiensis, 232 Palaemon, 632 Palaemon gracilis, 632 Palaemonidae, 233, 271 Palaeolama mirifica, 51 Palicourea, 457, 461, 468, 469, 471, 719 Palicourea fastigiata, 696 Palicourea guianensis, 262 Palicourea salicifolia, 472 Palmacites berryanum, 52 Palmae, 52 Panicum, 687, 721 Panicum maximum, 377, 623 Panicum parvifolium, 689 Panopsis costaricensis, 350 Panterpe insignis, 469 Panthera onca, 262, 354, 467, 482, 557 Panulirus argus, 594 Panus fulvus, 257 Papilionidae, 270, 386, 539 Paracalanus parvus, 147 Parachromis Parachromis dovii, 269, 390, 547, 548, 550, 640, 648, 667, 675, 722 Parachromis loisellei, 548 Parachromis managuense, 546, 547

Paracyclops chiltonii, 666 Paralichthyidae, 547 Paramachaerium gruberi, 374 Paraphysomonas vestita, 676 Paraponera clavata, 387– 88 Paraponerinae, 388 Paraprionospio pinnata, 110, 144 Parathesis, 461 Paratrechina caeciliae, 387 Parhadjelia cairinae, 276 Parkia, 374 Parkia pendula, 353 Parkinsonia, 701– 2 Parkinsonia aculeata, 257, 258, 690, 691, 692, 701, 702, 721 Parmeliaceae, 459 Parmentiera valerii, 304 Parmotrema 459, 460 Parula gutturalis, 466, 511 Parulidae, 466, 556, 719 Paspalidium germinatum, 687, 690 Paspalum, 257, 347 Paspalum pectinatum, 255 Paspalum repens, 257, 689, 690 Passalidae, 231 Passarina cyanea, 224 Passeridae, 556 Passiflora, 347, 383, 384, 384, 461, 469, 715, 719 Passiflora vitifolia, 383, 383, 715 Pavona Pavona chiriquensis, 179 Pavona clavus, 113, 175, 179, 710 Pavona gigantea, 112–13, 120, 165, 179, 710 Pavona maldivensis, 179 Pavona varians, 175, 179 Pavona xarifae, 179 Pavonia spicata, 696 Pecari tajacu, 263, 264, 354, 395, 467, 558 Pecopteris, 52 Pedilanthus nodiflorus, 256 Pelamis platurus, 221 Pelecanus occidentalis, 223 Pelliciera, 13 Pelliciera rhizophorae, 109, 143, 353, 377 Pellobunus insularis, 231 Peltigera, 509 Peltogyne, 374 Peltogyne purpurea, 349, 374, 715 Penaeus Penaeus brasiliensis, 594 Penaeus brevirostris, 146 Penaeus stylirostris, 146 Penelope purpurascens, 266, 466 Peniocereus hirshtianus, 256 Pennisetum, 687 Pennisetum clandestinum, 86 Pentacalia, 512 Pentacalia andicola, 512 Pentacalia firmipes, 474 Pentaclethra, 532, 533, 677, 699 Pentaclethra macroloba, 400, 540, 543, 695– 98, 715, 722

Pentatomidae, 231 Peperomia, 347, 440, 461, 462, 468– 69, 539, 715, 718 Peperomia costaricensis, 440 Peponecephala electra, 154 Perenniporia, 458 Pereskia lychnidiflora, 256 Peridinium willei, 672 Peripatidae, 78 Peripatus acacioi, 78 Perissodactyla, 354, 511 Perlesta, 633 Pernettya, 458, 512, 721 Pernettya coriacea, 474 Pernettya prostrata, 512, 514, 686, 721 Peromyscus, 472 Peromyscus mexicanus, 466, 467 Persea, 438, 457, 461, 471, 718 Persea americana, 335, 461 Persea caerulea, 350, 351 Persea schiedeana, 461, 482 Persea vesticula, 469 Petrolisthes armatus, 106, 146, 709 Pezopetes capitalis, 466, 511 Phaenostictus mcleannani, 339, 394, 554 Phaeocollybia, 458 Phaeophyta, 147 Phaeothlypis fulvicauda, 222 Phaethornis superciliosus, 393 Phaeton lepturus, 223 Phalacrocoracidae, 555 Phallichthys Phallichthys amates, 547, 548 Phallichthys quadripunctatus, 548 Phallichthys tico, 547, 548 Pharomachrus Pharomachrus mocinno, 553, 719 Pharomachrus mocinno ssp. costaricensis, 466 Phascolosoma perlucens, 146 Phaseolus, 461 Phaseolus vulgaris, 75, 78, 85, 475 Phasmatodea, 266 Pheidole, 561 Pheidole bicornis, 387 Pheidole browni, 387 Pheidole fiorii, 387 Pheidole multispina, 387 Pheidole pugnax, 387 Pheidolini, 561 Phellinus, 458 Phellinus gilvus, 257, 354 Phellinus linteus, 354 Pheucticus tibialis, 466 Philander opossum, 354 Philodendron, 347, 457, 462, 539, 715 Philodendron thalassicum, 432 Phoebe, 471 Phoebis Phoebis argante, 327 Phoebis hersilia, 327 Phoebis philea, 327 Phoebis sennae, 327

770 Systematic Index of Scientific Names Phoradendron, 457 Phoradendron tonduzii, 462 Phormidium, 624, 720 Photinus, 269 Phragmatopoma attentua, 147 Phrygionis steeleorum, 231 Phyllites costaricensis, 52 Phyllogonium viscosum, 469 Phylloporus, 458 Phyllostomus discolor, 265, 272 Phylobates vittatus, 391 Phymatolithon calcareum, 114 Physciaceae, 459 Physeteridae, 116 Physimera, 560 Picidae, 555 Pieridae, 270, 386 Pilea gomeziana, 216 Pilotrichella, 463, 719 Pilotrichella flexilis, 469, 464 Pimelodidae, 268, 389, 547, 548, 692 Pinaroloxias inornata, 222– 23, 226, 230 Pinctada mazatlanica, 151 Pinnipedia, 219 Pinnularia, 624 Pinnularia braunii, 668, 669, 674 Pinus, 478 Piper, 273, 347, 349, 387, 440, 461, 468, 469, 539, 560, 715 Piper amalago, 339 Piper arieianum, 560 Piper flavidum, 256 Piper marginatum, 339 Piper psilorhachis, 339 Piper retalhuleuense, 257 Piper reticulatum, 262 Piper sagittifolium, 461 Piper trigonum, 560 Piperaceae, 52, 347, 349, 440, 457, 462, 539, 560 Piperites Piperites cordatus, 52 Piperites quinquecostatus, 52 Pipra Pipra coronata, 393 Pipra mentalis, 393, 561 Pipridae, 556 Pistia stratiotes, 257, 377, 689, 690, 696, 697, 721 Pitcairnia, 275 Pitcairnia calcicola, 257, 260 Pithecellobium Pithecellobium lanceolatus, 257 Pithecellobium latifolium, 695 Pithecellobium valerioi, 699 Plagiochila, 463, 510, 719 Plagiochilaceae, 463 Plagiorchioidea, 275 Plagiothecium, 463 Plantago, 458, 508, 512 Platyhelminthes, 119, 275, 634 Platymiscium Platymiscium curuense, 260, 262

Platymiscium parviflorum, 259, 276, 353 Platymiscium pinnatum, 374, 482 Platyrinchus Platyrinchus coronatus, 552 Platyrinchus mystaceus, 552 Plecoptera, 633 Pleiostachya pruinosa, 560 Plethodontidae, 551 Pleuranthodendron lindenii, 260– 61 Pleuromanna robusta, 147 Pleuroncodes Pleuroncodes monodon, 118 Pleuroncodes planipes 118 Pleurothallis, 347, 462, 539, 715, 718 Pleurotus, 458 Plicopurpura Plicopurpura patula, 152 Plicopurpura patula pansa, 152 Plina puriscalensis, 352 Pliocardia krylovata, 118 Plocosperma buxifolium, 257, 260 Plumeria rubra, 260, 262, 353, 429 Poa, 720 Poa chirripoensis, 510 Poaceae, 52, 254, 257, 347, 350, 461, 467, 468, 499, 509, 510, 539 Pochota quinata, 272, 377 See Bombacopsis quinata; Pachira quinata Pocillopora, 112, 113 Pocillopora damicornis, 179 Pocillopora elegans, 179 Pocillopora eydouxi, 112, 179, 710 Pocillopora meandrina, 113, 179 Podicipedidae, 555 Podocarpaceae, 461, 469 Podocarpus, 52, 461, 718 Podocarpus macrostachys, 469 Poecilia, 389 Poecilia gillii, 268, 389, 547, 548, 550, 634, 637, 692, 722 Poecilia mexicana, 547, 550 Poecilia sphenops, 268 Poeciliidae, 268, 389, 546, 547, 548, 558, 627, 692, 712, 715, 722 Poeciliopsis, 389 Poeciliopsis gracilis, 269 Poeciliopsis santaelena, 269 Poeciliopsis turrubarensis, 389 Pogonophora, 33 Pogonopus speciosus, 260, 261 Polistes, 321 Polistes instabilis, 327– 28, 328 Polistes variabilis, 271 Polyarthra, 667 Polyarthra vulgaris, 675 Polychaeta, 144 Polychrotidae, 552, 553 Polycyathus hondaensis, 179 Polydesmida, 235 Polygonaceae, 254 Polygonum, 377, 687, 721 Polygonum acuminatum, 689 Polygonum hispidium, 689

Polygonum punctatum, 689 Polygonum segetum, 668, 689 Polymesoda radiata, 151, 153, 700 Polyommatus, 531 Polyplacophora, 153, 594 Polypodium, 347, 462 Polypodium attenuatum, 275, 348 Polypodium wagneri, 275 Polyporus, 458 Polytrichadelphus, 463 Pomacea costaricana, 693 Pomadasys Pomadasys bayanus, 389 Pomadasys croco, 547, 548 Pompholix complanata, 675 Ponerinae, 433 Pontederia rotundifolia, 689, 690 Pontoscolex corethrurus, 78– 79 Porella, 463 Porichthys, 148 Porites, 13 Porites evermanni, 113, 114 Porites lobata, 112, 113, 113– 14, 169, 171, 175, 179, 180, 710 Porites panamensis, 113, 165 Porophyllum punctatum, 256 Porotrichodendron, 463 Porotrichum, 463 Porthidium, 552 Porthidium nasutum, 392 Porthidium porrasi, 392 Posoqueria Posoqueria grandiflora, 696 Posoqueria latifolia, 353, 695 Potamocaranus, 634 Potamogetonaceae, 111 Pothomorphe, 440 Potimirin, 235 Potos flavus, 557 Poulsenia armata, 374, 715 Pouteria Pouteria macrocarpa, 482 Pouteria subrotata, 353 Pouteria zapota, 260 Pradosia atroviolacea, 353 Prestoea, 461, 473, 719 Prestoea acuminata, 429 Prestoea decurrens, 377, 696 Priapichthys annectens, 548 Prionodon, 463 Prioria copaifera, 66, 695, 697– 98, 699 Pristidae, 268, 547 Pristimantis, 531, 551 Pristis pristis, 268, 546, 547 Procnias tricarunculata, 355, 394, 553, 712, 719 Procyon Procyon cancrivorus, 355, 355 Procyon lotor, 264, 355, 466, 557 Procyonidae, 5 Proechimys semispinosus, 51 Prosapia, 437 Prosopis, 294

Systematic Index of Scientific Names 771 Protium, 374, 715 Protium paramense, 260, 348 Protium pittieri, 482, 540, 715 Protographium Protographium epidaus, 323 Protographium philolaus, 323 Protonotoria citrea, 394 Protozoa, 6 Protura, 77 Prumnopitys, 461 Prumnopitys standleyi, 461, 469 Prunus, 718 Prunus annularis, 469, 474 Prunus cornifolia, 81 Prunus subcorymbosa, 377 Psammisia, 461, 469 Psammisia ramiflora, 462 Psammocora Psammocora stellata, 179 Psammocora superficiales, 179 Psathyrella, 458 Pselliphorus tibialis, 466 Pseudobombax septenatum, 262, 353 Pseudocolaptes lawrencii, 466 Pseudodiaptomus, 147 Pseudolmedia oxyphyllaria, 261, 350 Pseudomyrmex, 271, 274, 338, 713, 715 Pseudomyrmex caeciliae, 387 Pseudomyrmex ferruginea, 274 Pseudomyrmex flavicornis, 338, 387 Pseudomyrmex nigrocinctus, 338, 387 Pseudomyrmex particeps, 387 Pseudomyrmex spinicola, 338, 387 Pseudo-nitzschia pungens, 154 Pseudophallus Pseudophallus elcapitanensis, 268 Pseudophallus mindii, 546, 548 Pseudophallus starksi, 389 Pseudorca crassidens, 169, 170 Pseudostaurosira brevistriata, 664 Pseudothelphusidae, 632 Pseustes, 552 Psidium, 461 Psiguria, 384 Psittacidae, 555 Psychotria, 347, 349, 461, 462, 469, 539, 715, 718, 719 Psychotria chagrensis, 696, 699 Psychotria cocoensis, 230 Psychotria gracilenta, 217, 230 Psychotria grandis, 539 Psychotria poeppigiana, 699 Psychotria turrubarensis, 350 Pteris, 458 Pterobyron, 463 Pterocarpus, 696 Pterocarpus officinalis, 377, 598, 599, 695, 696, 697, 699, 710, 722 Pteroglossus Pteroglossus franzii, 356 Pteroglossus torquatus, 562 Pterogramma cardiosomi, 232 Pteronotus, 265

Pteropsida, 52 Pterygoplichthys, 628 Ptillidae, 231 Ptychophallus paraxanthusi, 632 Ptygura, 667 Puma Puma concolor, 262, 263, 467, 557 Puma concolor ssp. costaricensis, 511 Puma yagouaroundi, 262 Puya, 52, 512, 514 Puya dasylirioides, 513, 686, 686, 721 Pycnarthrum pseudoinsularis, 229 Pylopagurus longimanus, 232 Pyramica margaritae, 387 Pyrenulales, 509 Perginae, 275 Pyrrhobryum, 463 Quadrigula, 672 Quadrus cerealis, 560 Qualea paraensis, 374, 377, 715 Quararibea funebris, 260 Quercus, 13, 52, 353, 458, 460, 461, 462, 467, 468, 469, 472, 475, 500, 507, 718 Quercus cf. seemannii, 429 Quercus copeyensis, 81, 463, 469, 470, 473, 475, 478 Quercus corrugata, 52, 349, 429 Quercus costaricensis, 81, 467, 468, 469, 473, 475, 482 Quercus guglielmi-treleasei, 469 Quercus insignis, 377 Quercus oleoides, 254, 254, 255, 257, 272, 293, 314, 325, 712 Quercus oocarpa, 469 Quercus rapurahuensis, 377, 469 Quercus seemannii, 349, 469, 514 Quilopoda, 77 Radula, 463, 510 Radulaceae, 211 Rallidae, 555 Ramalina, 460 Ramphastidae, 555, 561– 62 Ramphastos Ramphastos sulfuratus, 554, 562 Ramphastos swainsonii, 355, 554, 562 Ramphocelus passerinii, 196 Rana, 628 Rana vaillanti, 267, 275 Rana vibicaria, 464 Rana warszewitschii, 628, 722 Ranidae, 551 Ranunculus, 513, 720 Ranunculus crassirostratus, 510 Raphia, 12, 66, 368, 377, 398, 695, 696 Raphia taedigera, 9, 377, 598, 694– 95, 694– 95, 710, 721 Rattus Rattus norvegicus, 219, 224, 236, 335 Rattus rattus, 193– 94, 219, 224, 236 Rauvolfia, 695 Recurvirostridae, 555

Rehdera trinervis, 257, 315 Reithrodontomys, 467 Reithrodontomys creper, 440, 466 Reithrodontomys gracilis, 262 Reithrodontomys mexicanus, 51 Reithrodontomys paradoxus, 262 Relbunium, 462 Renealmia Renealmia alpinia, 561, 562 Renealmia aromatica, 696 Rhamdia Rhamdia guatemalensis, 268, 389, 548 Rhamdia nicaraguensis, 268, 547, 692 Rhamdia rogersi, 548 Rhamnaceae, 513 Rhamnus, 458, 514, 718 Rhamnus oreodendron, 469, 474 Rhamphichthyidae, 548 Rhapalodia gibba, 677 Rhincalanus nasutus, 147 Rhinochenus 273– 74, 329– 30 Rhinoclemmys, 531, 722 Rhinoclemmys annulata, 552, 558, 636 Rhinoclemmys funerea, 552, 558, 636 Rhinophrynidae, 551 Rhipidocladum racemiflorum, 256 Rhissomatus subcostatus, 86 Rhizobium, 75– 76, 87 Rhizobium leguminosarum, 75 Rhizophora, 531 Rhizophora harrisonii, 109, 143 Rhizophora mangle, 9, 108, 108, 109, 143, 353, 377, 599, 600, 696, 710 Rhizophora racemosa, 109 Rhizopsammia verrilli, 179 Rhizosolenia, 146 Rhizosolenia stolterfothii, 146 Rhodobryum grandifolium, 256 Rhodocollybia 458 Rhodophyta, 119, 147, 509, 624 Rhopalodia gibberula var. argentina, 624, 626 Rhus, 473 Rhus striata, 469 Rhynchospora Rhynchospora corymbosa, 689, 690 Rhynchospora polyphylla, 216 Rhynchospora schaffneri, 514, 686 Rigodium, 463 Riodinidae, 270 Rivulidae, 268, 546, 547, 548 Rivulus, 549– 50 Rivulus fascolineatus, 268 Rivulus isthmensis, 547, 548 Rodentia, 273, 511, 555, 558 Roeboides bouchellei, 268, 547 Roldana scandens, 461, 476 Romaleidae, 559 Rondeletia Rondeletia amoena, 469 Rondeletia buddleoides, 469 Rondeletia hameliifolia, 256 Rooseveltia franckianiana, 211

772 Systematic Index of Scientific Names Rosaceae, 458, 461, 468, 499, 510 Rothschildia Rothschildia erycina, 323 Rothschildia lebeau, 323 Rotylenchulus reniformis, 76 Roupala, 473 Roupala montana, 255, 260, 350, 469 Rubiaceae, 216, 217, 230, 254, 259, 347, 348, 349, 354, 374, 439, 460, 461, 462, 468, 539, 719 Rubus, 458, 461, 468, 475, 719 Ruppia maritima, 111, 111 Ruptiliocarpon, 374 Ruptiliocarpon caracolito, 374 Russelia sarmentosa, 255 Russula, 257, 458 Rustia occidentalis, 216, 696 Rutaceae, 349 Rynchops niger, 693 Sacciolepis myuros, 256 Sacoglottis Sacoglottis holdridgei, 194, 213, 214, 215, 216, 713 Sacoglottis thrichogyne, 698 Sagitta, 148 Sagitta enflata, 148 Sagitta friderici, 148 Sagittaria guyanensis, 256, 690 Saimiri oerstedii, 265, 354, 394, 399, 712, 716 Salpidae, 592 Salvia, 458 Salvinia, 377, 721 Salvinia auriculata, 257, 689, 690, 691 Salvinia minima, 349 Salvinia sprucei, 689 Samanea, 294 Samanea saman, 259, 261 Sapindaceae, 254, 257 Sapium, 353, 471 Sapium allenii, 374 Sapium glandulosum, 350, 353 Sapium pachystachys, 471, 472 Sapium rigidifolium, 429 Sapotaceae, 276, 348 Sarchorachis, 440 Sarcoramphus papa, 355 Sargassum liebmanni, 105 Saturniidae, 270, 330 Satyria warszewiczii, 462 Saurauia, 438 Saurauia veraguasensis, 469 Sauria, 267 Sauvagesia pulchella, 255 Scaphiodontophis, 552 Scaphyglottis, 275, 462, 718 Sceloporus malachiticus, 464, 511, 719 Scenedesmus, 675 Scenedesmus ecornis, 667 Schausiella santarosensis, 323, 330 Scheelea, 369 Scheelea rostrata, 315, 696

Schefflera, 461, 468, 473, 514, 718 Schefflera morototoni, 260 Schefflera rodriguesiana, 429, 432, 440, 469, 475, 501 Schizolobium parahyba, 262, 349, 402 Schlegelia, 461 Schlegelia brachyanta, 213 Schoenocaulon officinale, 255 Schwenckia americana, 255 Sciaenidae, 148, 154, 711 Scincidae, 553 Sciuridae, 79, 273 Sciurus Sciurus granatensis, 466, 472 Sciurus variegatoides, 273 Scleractinia, 172 Scleria, 687, 721 Scleria macrophylla, 689 Scleria microcarpa, 696 Scolelepis Scolelepis agilis, 145, 600 Scolelepis squamata, 600 Scolopacidae, 555 Scolytidae, 228– 29, 231 Scorpiones, 231 Scotinomys xerampelinus, 466, 467 Scrophulariaceae, 510 Seiurus noveboracensis, 394 Selaginella Selaginella pallescens, 275, 429 Selaginella sertata, 275 Selasphorus flammula, 511 Selenastrum, 672 Selenicereus Selenicereus testudo, 275 Selenicereus wercklei, 275 Sellaphora pupula, 672 Sematophyllum, 463 Senecio, 458, 461, 462, 500, 512, 718, 719, 720 Senecio andicola, 512 Senecio kuhbieri, 510 Senecio oerstedianus, 512 Senna, 327 Senna atomaria, 327, 338 Senna pallida, 303, 338 Senna reticulata, 696 Serjania, 257 Serpentes, 267 Setaria geniculata, 214 Shinkai Shinkai fontefridae, 118 Shinkai longipedata, 118 Sibon, 552 Sickingia maxonii, 695 Sicydium, 220 Sicydium adelum, 548 Sicydium altum, 548, 642 Sicydium cocoensis, 220 Sicydium salvini, 389 Sida, 257, 303, 338 Sida acuminata, 338 Sida salviifolia, 256

Siderastrea siderea, 595, 605, 607 Sideroxylon, 294 Sideroxylon capiri, 259, 260, 276, 351 Sigmodon hispidus, 51, 300 Simaba cedron, 386 Simarouba Simarouba amara, 348, 559 Simarouba glauca, 256 Simaroubaceae, 559 Simsia santarosensis, 255 Simuliidae, 634 Siphonaria gigas, 107, 120, 153, 173– 74, 175 Siphonopora, 592 Skeletonema costatum, 146– 47 Sloanea, 380 Sloanea picapica, 353, 695 Sloanea terniflora, 254, 260, 712 Smilax, 461, 469 Smilisca Smilisca baudinii, 392 Smilisca phaeota, 392 Smilisca sila, 391– 92 Sobralia, 275 Socratea Socratea durissima, 374, 715 Socratea exorrhiza, 540, 715 Solanaceae, 52, 254, 257, 260, 347, 349, 439, 461, 462, 476, 559, 719 Solanum, 257, 347, 349, 458, 461, 468, 471, 500, 539, 715, 718, 719, 721 Solanum campechiense, 689 Solanum dotanum, 472 Solanum lancefolia, 687 Solanum longiconicum, 461 Solanum storkii, 469 Solenocera agassizii, 153 Solenopsidini, 561 Solenopsis altinodis, 388 Solifugae, 231 Solpugidae, 231 Sorocea cufodontisii, 374, 715 Sotalia guianensis, 595 Spathiphyllum Spathiphyllum friedrichstallii, 687, 696, 721 Spathiphyllum laeve, 216 Sphaeradenia, 462 Sphaeroceridae, 231, 232 Sphaerodactylus pacificus, 220, 222 Sphaeroma peruvianum, 143 Sphagneticola trilobata, 214 Sphiggurus mexicanus, 264, 466 Sphingidae, 229– 30, 314, 326 Sphoeroides annulatus, 389, 635 Sphyrna lewini, 154, 170 Sphyrospermum cordifolium, 462 Spilogale putorius, 467 Spionidae, 110 Spirodela intermedia, 349 Spondias, 397 Spondias mombin, 254, 259, 273, 349, 695, 712 Spondias purpurea, 335, 338

Systematic Index of Scientific Names 773 Spondylus calcifer, 151 Squamidium, 463 Squilla Squilla biformes, 118 Squilla hancocki, 154 Squilla parva, 154 Stator Stator limbatus, 269 Stator pruininus, 269 Staurastrum, 667 Staurastrum paradoxum, 666 Staurodesmus, 667 Stauroneis, 624, 721 Stegastes partitus, 595 Stelis, 462, 718 Stellifer, 148 Stemmadenia donnell-smithii, 697 Stenella Stenella attenuata, 102, 116, 154, 710 Stenella longirostris, 154 Stenocereus aragonii, 256, 259, 260, 262 Stenopterobia pumila, 624, 626 Stephaniella, 513 Sterculia apetala, 262 Sterculiaceae, 254 Stereocaulon, 509 Stereocaulon vesuvianum, 512 Steriphoma paradoxum, 349 Stevia, 720 Stevia westonii, 510 Sticherus remotus, 217 Sticta, 458, 459, 460, 509 Stictocardia tiliifolia, 230 Stipa, 512 Stipa hans-meyeri, 513 Stomatopoda, 118, 146 Strabomantidae, 551 Stratiomyidae, 231 Strigidae, 555 Strombus galetus, 153 Sturnira Sturnira lilium, 265 Sturnira ludovici, 467 Styrax, 457 Styrax argenteus, 81, 469, 474 Styrax glabrescens, 350 Sula Sula dactylatra, 222 Sula leucogaster, 170, 222 Sula sula, 170, 222, 226 Sus scrofa, 194, 224, 227 Swallenochloa, 512 Swartzia panamensis, 353 Swietenia Swietenia humilis, 259, 276 Swietenia macrophylla, 256, 273, 276, 296, 332, 348, 350, 482 Sycidium salvini, 635 Sylviidae, 556 Sylvilagus, 511 Sylvilagus brasiliensis, 559 Sylvilagus dicei, 354, 466, 482 Sylvilagus floridanus, 264

Symphonia, 698 Symphonia globulifera, 9, 374, 377, 399, 696, 697, 697, 698, 699, 715, 716, 722 Symphyla, 77 Symplocos, 457, 471, 718 Symplocos austin-smithii, 469 Symplocos serrulata, 471 Synbranchidae, 546, 547, 548 Synbranchus marmoratus, 268, 547, 548, 693 Syncuaria, 276 Syngnathidae, 268, 389, 546, 548 Syngonium, 462 Synurophyceae, 666, 676 Syringodium filiformis, 602, 603, 710 Syrrhopodon, 463 Tabebuia Tabebuia ochracea, 254, 257, 350, 712 Tabebuia rosea, 349, 350, 351, 353, 696, 711 Tabellaria binalis, 670 Tabernaemontana Tabernaemontana alba, 256, 260 Tabernaemontana chrysocarpa, 696 Tachigali versicolor, 349, 374 Tachyphonus delattrii, 554 Tagelus, 153 Talamancalia, 509, 720 Talipariti, 225 Talipariti tiliaceum var. pernambucense, 214, 215, 217 Tamandua mexicana, 354 Tangara, 394 Tangara gyrola, 393– 94 Tangara inornata, 553, 554 Tangara larvata, 394 Tantilla, 552 Tapirira mexicana, 350 Tapirus, 51 Tapirus bairdii, 262, 263, 277, 318, 319, 354, 397, 467, 473, 482, 511, 559, 686, 715 Tapirus cf. terrestris, 51 Tardigrada, 511 Tassadia ovovata, 230 Tayassu Tayassu pecari, 262, 263, 277, 354, 395, 396, 559, 715 Tayassu tajacu, 467 Tayassuidae, 5, 395 Taygetis kerea, 270 Tecoma stans, 350 Tectona grandis, 73, 279, 377, 402, 543 Teiidae, 553 Telipogon, 462, 509, 718 Terminalia, 377 Terminalia catappa, 214, 273, 402 Terminalia oblonga, 262, 697 Tethocyathus prahli, 179 Tetracera volubilis, 269 Tetraclita Tetraclita rubescens, 146, 709 Tetraclita stalactifera, 106, 146, 173, 709

Tetragastris panamensis, 260 Tetranema floribundum, 350 Tetrathylacium, 388, 388 Tetrathylacium johansenii, 353 Tettigoniidae, 231 Thais brevidentata, 107, 155 Thalassia testudinum, 593, 602, 603, 710 Thalassiosira pseudonana, 667 Thalia, 721 Thalia geniculata, 257, 687, 690, 691, 696 Thalurania colombica, 553 Thamnophilidae, 555 Theaceae, 214 Thelypteris, 52, 347 Thelypteris cocos, 211 Thelypteris gomeziana, ix Thelypteris minor, 275 Theobroma angustifolium, 261 Theraps Theraps maculicauda, 546, 547 Theraps underwoodi, 628, 640, 645 Thermocyclops tunuis, 666 Thioplaca cf. chileae, 117 Thoinia serrata, 255 Thor, 169 Thouinidium decandrum, 254, 260, 353, 712 Thraupidae, 196, 466, 556, 719 Thraupis episcopus, 196 Threskiornithidae, 555 Thryorchilus browni, 511 Thuidium, 463 Ticodendraceae, xix, 718 Ticodendron incognitum, 377, 718 Tigrisoma, 630 Tilapia, 656, 664, 699 Tillandsia, 275, 347, 462, 718 Tillandsia punctulata, 462 Tillandsia schiedeana, 275 Tillandsia streptophylla, 256 Tilopus, 257 Tinamidae, 555 Tinamus major, 466 Tineidae, 231 Tipulidae, 231 Tococa guianensis, 699 Tocoyena pittieri, 482 Tolmomyias Tolmomyias assimilis, 554 Tolmomyias sulphurescens, 275– 76 Tomocichla Tomocichla tuba, 549 Tomocichla underwoodi, 548, 549, 550 Tonina fluviatilis, 689 Topobea, 432, 462 Tortricidae, 231 Toxicodendron striatum, 350, 351 Trachelomonas, 667 Trachelomonas volvocina, 667 Trachelomonas volvocinopsis, 667 Trachemys, 552 Trachypenaeus byrdi, 146

774 Systematic Index of Scientific Names Trachypogon plumosus, 255, 299, 306, 308, 334, 335 Tradescantia petricola, 260 Trametes, 458 Trema micrantha, 339, 352, 353, 712 Triaenodon obesus, 170– 71 Trichechus manatus, 265, 555, 595, 630, 696, 716, 722 Trichilia, 257, 374, 473, 715, 718 Trichilia havanensis, 351, 469 Trichilia pallida, 353 Trichilia pleeana, 260 Trichilia tuberculata, 261, 696 Trichodesmium erythraeum, 154 Trichomanes, 462 Trichomorpha hyla, 235 Trichomycetes, 633– 34 Trichomycteridae, 391 Trichoptera, 633 Trigonalidae, 275 Trigonia rugosa, 272 Trigonidium, 275 Trimalaconothus novus, 666 Trinectes paulistanus, 547 Tripanurgus compresus, 392 Triplaris melaenodendron, 261, 348, 712 Tripneustes ventricosus, 592 Trixis inula, 255 Trochilidae, 230, 466, 555, 719 Troglodytes ochraceus, 466 Troglodytidae, 556 Trogon Trogon collaris, 466 Trogon melanocephalus, 266 Trogonidae, 555 Trophis racemosa, 260 Tropidacris cristata, 433 Tropocyclops Tropocyclops prasinus, 666 Tropocyclops prasinus prasinus, 665, 721 Tubastrea coccinea, 179 Turdidae, 196, 466, 556, 719 Turdus Turdus albicollis, 394 Turdus grayi, 196 Turdus nigrescens, 511, 686, 721 Turdus plebejus, 466 Turnera diffusa, 255 Turpinia, 457, 473 Tursiops truncatus, 116, 154, 169– 70, 595 Tylomys watsoni, 51, 466 Tylopilus, 458 Typha, 249, 659, 661, 663, 691, 701– 2 Typha dominguensis, 257, 280, 690, 691, 701, 721 Tyrannidae, 466, 556, 719 Tyromyces, 458 Tytonidae, 555 Uca, 145 Uca panamensis, 232 Uca zacae, 232

Ugni myricoides, 514 Uleobryum peruvianum, 256 Ulmus mexicana, 349 Uncinia, 720 Uncinia hamata, 462 Uncinia koyamae, 510 Ungaliophidae, 553 Urbanus proteus, 325 Urera caracasana, 696 Uribea, 374 Urocyon cinereoargenteus, 265, 277, 466 Uroderma bilobatum, 557 Urotheca, 552 Urotrygon cimar, 149, 711 Urticaceae, 52, 216, 458, 469 Usnea, 458, 459, 509, 685 Utricularia, 377, 668, 721 Utricularia aff. subulata, 514, 686 Utricularia alpina, 432 Vaccinium, 432, 458, 461, 471, 512, 514, 719 Vaccinium consanguineum, 81, 469, 472, 474, 475, 512, 514, 685 Vaccinium floribundum, 474 Vachellia, 271, 274, 713, 715 Vachellia allenii, 374, 387, 388 Vachellia collinsii, 257, 262, 274, 338 Vachellia cornigera, 274, 338 Vachellia farnesiana, 256, 257, 335, 338 Vachellia villosa, 255 Valeriana, 458 Valeriana sorbifolia, 513 Vampyressa thyone, 557 Vampyrum spectrum, 264 Vanilla, 461 Vanilla planifolia, 275 Vantanea, 374 Vantanea barbourii, 374 Verbenaceae, 254, 315 Vermivora peregrina, 394 Vespidae, 271, 328 Viburnum, 52, 458, 471, 514 Viburnum costaricanum, 350, 469, 471, 472 Viburnum venustum, 429 Viola, 458 Viperidae, 553 Vireo Vireo flavoviridis, 553 Vireo leucophrys, 466 Vireo olivaceus, 394 Vireo philadelphicus, 394 Vireonidae, 556 Virola, 374, 715 Virola koschnyi, 348, 353, 696 Virola multiflora, 696 Virola sebifera, 353 Virola surinamensis, 260 Viscaceae, 462 Vismia, 461 Vismia baccifera, 339

Vitex cooperi, 353, 482 Vittaria, 462 Vittaria graminifolia, 462 Vochysia Vochysia ferruginea, 715 Vochysia guatemalensis, 85, 543 Vochysia hondurensis, 374, 715 Voyria, 699 Vriesea, 462, 718 Vriesea orosiensis, 462 Wallinia chavarriae, 276 Waltheria indica, 255 Warszewiczia coccinea, 540, 715 Wasmannia auropunctata, 228 Websteria confervoides, 256 Weinmannia, 52, 458, 461, 473, 514, 718 Weinmannia pinnata, 81, 432, 469, 474, 475 Weinmannia trianae, 469, 474 Welfia Welfia georgii, 374, 699, 715 Welfia regia, 540, 715 Werauhia, 275 Westoniella, 497, 500, 509, 720 Westoniella chirripoensis, 510 Westoniella eriocephala, 510 Whallwachsia illuminata, 275– 76 Wigandia urens, 261 Williamodendron glaucophyllum, 374 Xanthosoma robustum, 438 Xantusiidae, 553 Xenarthra, 265, 354 Xenops minutus, 554 Xiphorhynchus Xiphorhynchus lachrymosus, 393 Xiphorhynchus susurrans, 394 Xyleborinus Xyleborinus cocoensis, 229 Xyleborinus sparsegranularum, 229 Xyleborus Xyleborus bispinatus, 229 Xyleborus ferruginosus, 229 Xylocopa, 271 Xylophanes Xylophanes anubus, 325 Xylophanes chiron, 325 Xylophanes juanita, 323 Xylophanes libya, 326 Xylophanes porcus, 326 Xylophanes tersa, 230 Xylophanes turbata, 314, 323 Xylophragma seemannianum, 257, 327 Xylopinae, 271 Xylosma intermedia, 469 Xyris, 512, 721 Xyris nigrescens, 514, 686 Xyris subulata, 686 Zalophus Zalophus californianus, 170 Zalophus wollebaeki, 169, 170, 219

Systematic Index of Scientific Names 775 Zanthoxylum, 473, 718 Zanthoxylum caribaeum, 350, 352, 712 Zanthoxylum limoncello, 469 Zanthoxylum melanostictum, 469 Zaretis, 270 Zea mays, 85, 475 Zeledonia coronata, 511

Zingiberales, 560 Zinowiewia Zinowiewia costaricensis, 352 Zinowiewia integerrima, 350 Ziphiidae, 116 Ziphius cavirostris, 169 Zonotrichia capensis, 196, 511

Zooxanthellae, 607 Zoraptera, 231 Zorotypidae, 231 Zygia longifolia, 260, 327 Zygothrica neolinia, 438