The New Neotropical Companion 0691115257, 9780691115252

Table of contents :
Cover
Title
Copyright
Dedication
Contents
Preface
Acknowledgments
How to Use This Book
Chapter 1. Welcome to the Torrid Zone
Chapter 2. Why It Is Hot, Humid, and Rainy in the Tropics
Chapter 3. Rain Forest: The Realm of the Plants
Chapter 4. Finding Animals in Rain Forest
Chapter 5. Sun Plus Rain Equals Rain Forest
Chapter 6. Essential Dirt: Soils and Cycling
Chapter 7. If a Tree Falls ... Rain Forest Disturbance Dynamics
Chapter 8. Evolutionary Cornucopia
Chapter 9. Why Are There So Many Species?
Chapter 10. Tropical Intimacy: Mutualism and Coevolution
Chapter 11. Evolutionary Arms Races: More Coevolution, More Complexity
Chapter 12. Cruising the Rivers to the Sea
Chapter 13. Scaling the Andes
Chapter 14. Don’t Miss the Savannas and Dry Forests
Chapter 15. Neotropical Birds: The Bustling Crowd
Chapter 16. From Monkeys to Tarantulas: Endless Eccentricities
Chapter 17. Human Ecology in the Tropics
Chapter 18. The Future of the Neotropics
Appendix. Words of Caution: Be Sure to Read This
Further Reading
Index

Citation preview

The New Neotropical Companion

The New Neotropical Companion

John Kricher

PRINCETON UNIVERSITY PRESS PRINCETON AND OXFORD

Copyright © 2017 by Princeton University Press Published by Princeton University Press, 41 William Street, Princeton, New Jersey 08540 In the United Kingdom: Princeton University Press, 6 Oxford Street, Woodstock, Oxfordshire OX20 1TR press.princeton.edu All Rights Reserved ISBN (pbk.) 978-0-691-11525-2 Library of Congress Cataloging-in-Publication Data Names: Kricher, John C., author. Title: The new neotropical companion / John Kricher. Other titles: Neotropical companion Description: Princeton : Princeton University Press, 2017. | Revised edition of: A neotropical companion. 2nd ed., rev. and expanded. c1997. | Includes bibliographical references and index. Identifiers: LCCN 2016027794 | ISBN 9780691115252 (pbk.) Subjects: LCSH: Ecology—Latin America. | Natural history—Latin America. | Natural history—Latin America—Pictorial works. Classification: LCC QH106.5 .K75 2017 | DDC 577—dc23 LC record available at https://lccn.loc. gov/2016027794

British Library Cataloging-in-Publication Data is available This book has been composed in Minion Pro and Myriad Pro Printed on acid-free paper. ∞ Printed in China

10 9 8 7 6 5 4 3 2 1

To my parents, who introduced me to the world we live in and to the wonders of life on Earth.

Contents Preface

9

Acknowledgments

11

How to Use This Book

12

Chapter 1.

Welcome to the Torrid Zone

15

Chapter 2.

Why It Is Hot, Humid, and Rainy in the Tropics

29

Chapter 3.

Rain Forest: The Realm of the Plants

39

Chapter 4.

Finding Animals in Rain Forest

58

Chapter 5.

Sun Plus Rain Equals Rain Forest

73

Chapter 6.

Essential Dirt: Soils and Cycling

81

Chapter 7.

If a Tree Falls . . . Rain Forest Disturbance Dynamics

95

Chapter 8.

Evolutionary Cornucopia

113

Chapter 9.

Why Are There So Many Species?

134

Chapter 10. Tropical Intimacy: Mutualism and Coevolution

155

Chapter 11. Evolutionary Arms Races: More Coevolution, More Complexity

181

Chapter 12. Cruising the Rivers to the Sea

205

Chapter 13. Scaling the Andes

235

Chapter 14. Don’t Miss the Savannas and Dry Forests

250

Chapter 15. Neotropical Birds: The Bustling Crowd

262

Chapter 16. From Monkeys to Tarantulas: Endless Eccentricities

319

Chapter 17. Human Ecology in the Tropics

365

Chapter 18. The Future of the Neotropics

377

Appendix.

389

Words of Caution: Be Sure to Read This

Further Reading

392

Index

417

9

Preface Why a New Neotropical Companion? It was first published in 1989 and it soon became known to travelers, both literal and armchair, as “The Little Green Book” (plate A). The “it” was the first edition of a relatively humble book that bore the title A Neotropical Companion. The subtitle was more explanatory: An Introduction to the Animals, Plants, and Ecosystems of the New World Tropics. It was a small book that fit easily into the pocket of a field jacket or a backpack. Illustrations were limited in number, comprising only a few black-and-white line drawings. The text of the book attempted to capture the ecological allure of the tropics, and in particular what ecologists were learning about the complexity and splendor of the uniquely diverse rain forest biome. At that time most of my field

Plate A. The Little Green Book. Photo by John Kricher.

experience was confined to Middle America, Belize in particular, plus Venezuela, Peru, and Ecuador, to which I had taken a few research trips, and thus the book omitted much information about the central Amazon Basin. Nonetheless the book resonated with travelers to the American tropics as well as students taking collegelevel courses in tropical ecology (many of which included some brief field time at a tropical location). I think the real reason the book found success was the remarkable subject matter it discussed. As I wrote the book I was continually amazed that so much hardearned scientific insight (real “boots on the ground” ecology) about the tropics was still essentially confined within scientific circles rather than readily available to interested lay readers and introductory students. I don’t mean how to identify this plant or that bird. I mean how the myriad species of tropical organisms interact to form a complex web of interdependency. I knew about this uniquely complex ecology (I described it as a “Gordian knot”) from firsthand experience as well as from my extensive reading of the scientific literature. How could this stuff be any more interesting? It was so cool! People ought to know about such things. I wrote at a time when field research in tropical ecology had really begun to burgeon. More and more researchers were in the tropics making that region their lifetime focus, and new field stations were appearing throughout the tropics, in particular in the New World, or Neotropics. The research was ongoing, the data were pouring in, and data analyses were revealing all manner of fascinating ecological and evolutionary insights. I just had to tell some of that story, and so I did. In the mid-1990s my editor at Princeton University Press asked me to consider expanding the Little Green Book, adding more breadth and detail. In addition to black-and-white line drawings there would be several groupings of photographs, all reproduced in color. By then I had the benefit of many more trips to the tropics, including several to the Brazilian Amazon. So the Little Green Book morphed into a bigger book, both in dimensions and page count, expanding to 451 pages. It contained far more coverage of the region and lots more basic information and examples. The second edition of A Neotropical Companion was published in 1997 and has remained useful to students, travelers, and general readers.

10

preface

Why a New Edition Now, and Why Call It “New”? In the 1997 edition coverage expanded and, as in the 1989 edition, I really did strive to be a real “companion” to my readers and write in layperson’s terms without becoming overly reliant on scientific jargon. I tried to tell in a basic and uncluttered way just how the ecology of the tropics works and why it is so remarkable. But I also added a considerable amount of academic material, and in accordance with that, citations from the scientific literature, some 800 of them, were interspersed throughout the book. Nonetheless, some academics thought it to be too general. A few professors told me it was just not rigorous enough for use in their courses (forgetting, I suppose, that it was never meant as a textbook). Some academically focused folks also commented that they thought I was too colloquial, inserting myself too often into the book. Other, more general readers had the opposite reaction and thought the writing to be a bit too much like that found in a textbook, at least in a few places, and said it was a bit arcane for a field guide, even regarding a complex subject like tropical ecology. Fortunately, many (hopefully most) readers accepted my attempt to balance academics and basic natural history, and thus the book has enjoyed a strong continued readership to this day. It has been translated into Spanish, through the efforts of the Birders Exchange Program of the American Birding Association; several thousand copies of the Spanish edition have been handed out free of charge to Latin American scientists, conservationists, and students, and it is available as a free download from the ABA website. It pleases me to know the book has been useful to so many. My next project was major in scope: an outgrowth of A Neotropical Companion but far more extensive. Scientific knowledge and new insights about the tropics continued to burgeon and there was a clear need for a rigorous and comprehensive book that

would provide a solid academically based introduction to not only the Neotropics but also the global tropics in general. Thus I elected to write such a book and did so. That effort resulted in Tropical Ecology, a comprehensive upper-level college textbook, published by Princeton University Press in 2011. This was meant, wholeheartedly, to be a rigorous and thorough text. The book seems to have found its intended audience among the offerings of colleges that include Tropical Ecology courses within their curricula. Since the publication of Tropical Ecology I have come full circle, back to wondering what to do about what was once the Little Green Book. The information in A Neotropical Companion needs to be updated. Science is always a work in progress, and that is certainly true of tropical ecology. There remains, in my view, a need for a general book for nonacademically focused readers and travelers that with a broad brush describes New World tropical ecology and that serves to interpret and explain the most biologically diverse terrestrial ecosystems on Earth. And thus it is that I chose to revise A Neotropical Companion and call it The New Neotropical Companion. It is new. It has been written to be much less academic in tone. I have adapted some of the former edition to this new edition and, as well, borrowed liberally from my 2011 text, Tropical Ecology, converting the academic writing to a more user-friendly and generalized treatment. There is an abundance of color illustrations that adds immeasurably to the utility of the book. You not only read about the Neotropics in these pages, you see the Neotropics. The writing is up to date, with full discussions of some of the newest and coolest scientific insights. Some of what was in the previous edition is essentially unchanged, some is somewhat changed, much is very changed. And, of course, there are numerous insights in the NNC not in the previous edition because they were not known then. That is the nature of science. And that is why there is a New Neotropical Companion.

11

Acknowledgments The list grows. In the previous two editions of A Neotropical Companion I have acknowledged many folks who have in various ways contributed to my continuously growing knowledge base about the Neotropics. These are still the folks who in so many ways made this book possible. The list includes former students, many friends with whom I have traveled, and the talented guides from whom I have learned. I have received travel support from Wheaton College (Norton, MA), where I teach, as well as from the American Birding Association, for whom I have led tours and run workshops at various Neotropical venues. I express my gratitude to all of these people for their assistance and companionship over the years. In particular and thinking back to how it all began, I thank, yet again, Fred Dodd of International Zoological Expeditions for introducing me to Belize in 1978 and for providing me with a delightful addiction that is satisfied only by being in the realm of palm trees and toucans. The New Neotropical Companion stands out from its predecessor volumes in one obvious way. The book is stunningly illustrated with some of the finest nature photography there is. I say this unabashedly, because many of the images to which I refer were not taken by me. I approached various friends asking if they would permit me to use their work in my book. No one turned me down. Photos began arriving, lots of them. I only wish I could have included more. It was almost physically painful to leave some of them out. I know you will want to just thumb through the book and revel in the photos—and never mind about the text. But I do hope you get around to reading the book after admiring the multiple images that make it special. If one picture really is worth a thousand words, this volume is indeed a major expansion. It has come of age. Therefore, thank you so much to James Adams, Steve Bird, Beatrix Boscardin, Edison Buenaño, Diana Churchill, David Clapp, Peter Crosson, Fred Dodd, Carl Goodrich, Bruce Hallett, Ed Harper, Jill Lapato, Bruce and Carolyn Miller, Gina Nichol, Nancy Norman, Dennis Paulson, Scott Shumway, Clay Taylor, Andy Whittaker, Alex Wild, Sean Williams, and Kevin Zimmer. Your long lenses and photographic talents have brought the art of tropical nature to these pages. Since the publication of the second edition of A Neotropical Companion, and while collecting information for this volume, I have been fortunate to travel with some exceptional guides including Domiciano Alveo, Carlos Bethancourt, Edison Buenaño, Damien and Camilio Montanez, Olger Licuy, Marcelo Padua, Benjamin Schwartz, and Jose Rafael Soto. My good friend Raul Arias de Para has made my continuing tropical education

a particular joy as I have made multiple and memorable visits to his Canopy Tower, Canopy Lodge, and Canopy Camp. Indeed, in my experience, the entire Canopy Family is “as good as it gets.” Muchas gracias, mis amigos. I thank my friends Tony White and Elwood Bracy for introducing me to the Bahamas and its remarkable habitats and wildlife, and Tony again for arranging a day in the field with Paul Dean, and Woody for showing me Abaco. Dick Payne, Mike Ord, and Terry Moore were terrific traveling companions, inviting my wife Martha and me to join them for what was a wondrous tour of Ecuador organized by Jane Lyons of Mindo Bird Tours (lots of hummingbirds). In appreciation for help with Lepidoptera ID, I thank Marj Rines and Sheri Williamson. Over the years I have received e-mails and letters from individuals who have made suggestions for what might be included in a new edition and who have pointed out various errors or omissions, and even a few grammatical hiccups. I thank each of you who took the time and interest in this book to offer that help to me. Since the publication of the first edition I have enjoyed a highly cordial relationship with Princeton University Press. Again I thank my editor, Robert Kirk, for his continued patience, guidance, and support. I am proud to be a Princeton author. And thanks also to Robert for putting together such a fine team to make this book happen. I am grateful to Karen L. Carter for stewarding the project through the complex conversion of manuscript to book; to Ryan Mulligan for handling the details pertaining to the multiple photographs; and to the ever-so-amazing Amy K. Hughes, whose copyediting efforts and unflagging attention to detail have made this book so much better. Only I know that. You, the reader, are the beneficiary. So, thanks big time, Amy. It was a pleasure. Just a quick acknowledgment to my grandchildren, Liam and Rory O’Toole, for the fun we have together. They are really going to enjoy the pictures in this book. Though Liam is only six years old and Rory only four, both know what a toucan is. My wife, Martha Vaughan, has supported and encouraged me in numerous ways as we journey through life. During the course of various book projects she has been a meticulous copy editor and the best of field companions, and she does remarkably well in patiently putting up with ongoing authorial angst. Ah, but when next she asks me whether I have finally completed “that book,” I will happily answer, “Well, as a matter of fact, yes, I have.” And that will make her happy, and that is what I most like to do.

12

How to Use This Book Readers already familiar with previous editions of A Neotropical Companion will immediately understand the tone and objectives of this book. This edition is not written in an academic style, even more deliberately so than its predecessor. Most important, it is not about how to identify various plants and animals of the tropics. When I visited Antarctica a few years ago I brought with me a book that illustrated literally every species of mammal and bird I was likely to find in Antarctica (mostly, of course, in the waters around the continental landmass). I had but to match the animal with its picture and bingo, a name! I saw most of the species listed. I did not have to worry about reptiles and amphibians, as there are none in Antarctica. The insects are few to none as well. But that is because Antarctica is very cold and windy, a basically inhospitable place to terrestrial life in general. Not so with the tropics. Consider birds, for example, a group with which I have considerable familiarity. On my Antarctica trip I saw almost all of the bird species present, and the list was fewer than 50 species. If I told you there are nearly 350 species to be found in the Neotropics, and you compared that with the number of Antarctic bird species, you would quickly see why it would take a much bigger book to cover just the bird species of the Neotropics, to say nothing of mammals and other animal groups. But in reality, there are nearly 350 species of hummingbirds (family Trochilidae) alone in the Neotropics. Several other bird families (Furnariidae, the ovenbirds and woodcreepers), Tyrannidae (the tyrant flycatchers), and Thraupidae (tanagers and related species) have similarly high species richness. Add to those all the other bird species, and you have about one-third of the world’s approximately 10,000 bird species, present and accounted for in Central and South America, most of them in either the Andes or the Amazon regions. So it becomes immediately obvious that it would take many volumes to catalog each and every bird, mammal, reptile, and amphibian species of the region. Add insects and other invertebrates, whose diversities are in the high thousands (likely well over a million), and it soon becomes hopeless to generate any sort of comprehensive field guide to the identification of Neotropical animals. Just to thoroughly catalog the butterflies of the relatively small country of Costa Rica, for example, requires two thick volumes. The distribution and identification of birds found in Ecuador, another small country, also requires two volumes.

And consider plant species. If you visit the lush cove forests of the central Appalachians, such as those found in Great Smoky Mountains National Park, you can, with skill and patience, find about 25 to 35 tree species in a single tract of 2 hectares, or about 5 acres of forest. (Note: hereafter in this book, we’ll use the abbreviations ha for hectares and ac for acres.) Take that numerical range, multiply it by 10, and you get the picture for parts of Amazonia. That’s right, more than 300 tree species may be present in just 2 ha. And many of them look very similar, requiring expert training in tree identification techniques. It is thus obvious that no book purporting to discuss the general ecology and natural history of the Neotropics could possibly focus on identification of each and every species. The good news is that you do not by any stretch of the imagination have to be competent in identifying all of the trees, birds, or bugs in order to comprehend, appreciate, understand, and enjoy what you are seeing and experiencing as you walk a rain forest trail. Of course some degree of identification knowledge is very useful: Is that a howler monkey or a capuchin? Is that a toucan or a parrot? Is that tree a legume? Is that flower a heliconia? Thus I have selected to illustrate and discuss examples of widespread organisms that tend to be consistently encountered in many places throughout the Neotropics. There are two words to keep in mind as I accompany you through the pages of this book: observation and interpretation. I have learned to see the world through the eyes of an ecologist, to “read” the landscape, to “see and comprehend” interactions among species. Ecologists typically identify patterns in nature that serve as initial jumping-off points that lead to investigative science. One global pattern, for example, is the distribution of species groups, such as trees, mammals, birds, and beetles. By far the majority of species from these various groups are found in equatorial regions, and species numbers (measured in units of area, such as number of breeding species per hectare) decline sharply as you move away from equatorial regions. Polar regions, the most inhospitable of terrestrial environments, have the fewest species (recall the Antarctica example above). This is a broad and consistent pattern, one that interested Charles Darwin (he talks about it in his most famous book, On the Origin of Species). Ecologists try to learn what the factors are that force such patterns, the causal factors.

13

Plate B. This is the Saffron Playboy (Xanthiris flaveolata). At first glance it appears to be a butterfly. But, no, it is a day-flying moth, common to southern Amazonian rain forests. Wow, what coloring! It almost glows. That brightness suggests that the insect is noxious to its potential predators, birds. It is likely exhibiting warning coloration (described in chapter 11). But no one has yet shown it to be unpalatable to birds. The pattern of coloration suggests such a conclusion, based on numerous other examples. It awaits further study. Ecologists identify wide-ranging patterns and, using the methods of science, explain why they might be adaptive to the organisms. Oh, and note the tiny fly on its left wing. Who knows what that’s doing there? Photo by John Kricher.

This example, called a latitudinal diversity gradient, will be discussed in much greater detail later in this book. My goal will be to teach you how to spot patterns, to observe, to see, and to understand a tropical ecosystem as an ecologist does. I will describe in some cases how ecologists have cleverly wrested information from nature that has resulted in much greater understanding of infrastructure of tropical ecosystems. As you move through the chapters you will begin thinking like an ecologist. Your focus will be less on putting a name on a particular organism that you encounter and more on understanding what it might be doing and what it might be interacting with (plate B). The book is written in a reader-friendly, colloquial style that I have attempted to keep relatively free of technical jargon and embedded annotations and citations. A further-reading list is included for each chapter; these are listed before the index. The entries highlighted in boldface are those used directly in the chapter, while the others enhance the lessons of the chapter and take you deeper into the subject matter.

Unlike its two predecessors, the New Neotropical Companion is prolifically illustrated with color photographs throughout. That is huge! Ecology is a visual science. Describing something in words or with a few drawings goes only so far. Seeing it in a color photograph goes so much further. With the kindness of some of the best photographers I know, I have been able to put together a visual tour of the Neotropics to accompany my narrative. The photos tell the story too. Obviously I have not been able to do more than offer a representative sample of what you might see, but it’s a darned good sample. Test it in the field. My textbook, Tropical Ecology (Princeton University Press, 2011), I will tell you unabashedly, may be of interest if you seek a broader, more rigorous, and technical college-level treatment of the subject matter. But if you’re heading off to the New World tropics or just want to sit down and read about this extraordinary region of the world: Welcome to the New Neotropical Companion.

14

Plate 1-1. Sunrise in the Torrid Zone. Photo by John Kricher.

Plate 1-2. The face of a Jaguar (Panthera onca). Photo by John Kricher.

15

Chapter 1 Welcome to the Torrid Zone Into the Torrid Zone The lure of the tropics, the desire to visit a land of relentless heat and humidity, of scorching sun and torrential rain, may at first seem a bit hard to explain (plate 1-1). But it’s not. It can be explained in one image: plate 1-2. Seeing a Jaguar (Panthera onca) for the first time, in its element, its home, its piece of rain forest, is worth any long bumpy and dusty ride, a few annoying mosquitos, muddy boots, an airport delay, or any other minor inconvenience typical of modern travel. Observing a real live Jaguar in the wild provides a remarkable connectivity with Earth’s natural world that is simply unrivaled. You have really seen something special. And there is so much more. The majesty of myriad imposing tall rain forest trees and the chance of encountering some of the multitudes of creatures that dwell within those forests is an experience that is nothing short of precious (plate 1-3). The tropics, a land of heat and humidity historically termed the Torrid Zone, contains most of the world’s species of, well, pretty much everything: plants, birds, mammals, reptiles, insects,

you name it. And that is what this book is about. We are going to visit the Neotropics. Let’s begin with some geographical perspective. Beginning about 248 million years ago, just after the end of the Permian period and the Paleozoic era, the world’s continents began drifting apart, a process that continues today. This separation is the result of a dynamic geological process known as plate tectonics. Continents made primarily of granite ride passively atop large and slowly moving plates of basalt (which compose the earth’s crust) kept in motion by the convective heat of the planet itself. The result, in a nutshell, has been that widely separated continents now contain markedly different groups of organisms. That is because 248 million years allow for a lot of evolutionary change, for new species to diverge and evolve, for whole new groups of organisms to develop. For example, the primates of the New World tropics (the Neotropics), the monkeys, marmosets, and tamarins of Middle and South America, are distinctly different from the Old World monkeys and apes, though they all (along with us), of course, ultimately share common ancestry in the order Primates (plate 1-4).

Plate 1-3. Tropical rain forest is the most structurally complex and biodiverse terrestrial ecosystem in the world. Photo by John Kricher.

16

chapter 1

Plate 1-4. These Humboldt’s White-fronted Capuchins (Cebus albifrons) are representatives of the New World monkeys, distinct from the Old World monkeys. Photo by Andrew Whittaker.

Plate 1-5. This colorful Saffron Toucanet (Pteroglossus bailloni), from southeastern Brazil, is in the family Ramphastidae, a group of birds found only in the Neotropics. Photo by Andrew Whittaker.

Plate 1-6. Tropical forests are generally warm and wet throughout the year, mostly due to the constancy of direct solar radiation. Photo by John Kricher.

Hornbills, large birds with colorful, elongate, bananalike bills, are found only in Africa and Asia. However, an anatomically similar but only distantly related group of birds, the toucans, toucanets, and aracaris (plate 1-5; discussed in chapter 8), is found only in the American tropics. Through these and numerous other examples, biogeographers have identified wellseparated geographic realms comprising largely distinct floras and faunas. North America is in the Nearctic biogeographic realm, which is primarily temperate in climate. Europe and northern Asia are in the Palearctic realm and are

likewise mostly temperate. The African realm and Australasian realms (including islands such as Borneo and New Guinea) are largely tropical in climate, though with large areas of hot desert. The realm known as the Neotropics begins in central Mexico, extends through the Caribbean region, and reaches to the tip of South America. Although temperate at both its northern and southern extremes, the realm of the Neotropics is largely tropical. Here’s why. The bulk of the Neotropic land area lies between the Tropic of Cancer to the north and the Tropic of Capricorn to the south, with the equator in the middle.

welcome to the torrid zone

The names Cancer and Capricorn refer, of course, to constellations of the zodiac through which the sun appears to trace its annual course. Because Earth is tilted on its axis, by 23.44°, it is a seasonal planet, its north side facing the sun part of the year (the northern summer months) and its south side facing the sun part of the year (the northern winter months). Thus on the dates of the summer and winter solstices the sun is either 23°26´22˝ (about 23.44°) north (directly over the Tropic of Cancer) or 23°26´22˝ south (directly over the Tropic of Capricorn). For those of us at northern latitudes, the sun appears low in the sky in winter and high, virtually overhead, in summer. On the dates of the equinoxes heralding the official beginning of spring and, six months later, autumn, the sun sits directly over the equator. It is thus obvious that the part of Earth receiving the most solar radiation (i.e., direct sunlight) within the course of a year is the region lying between the Tropics of Cancer and Capricorn, a 46.88° belt that essentially defines what we call the tropics. The fact that the sun is never more than 23.44° north or south of the equator is the major reason the tropics exist. Earth receives different amounts of solar radiation depending upon latitude. But if you are in the Torrid Zone, no matter where on Earth, you get a lot of direct sunlight throughout the year and thus, unless you are at a high elevation, you experience a lot of heat. It is therefore consistently warm in the lowland tropics (plate 1-6). North of the Tropic of Cancer and south of the Tropic of Capricorn you enter the temperate zone, an area of more extreme annual climate variability. North of the Arctic Circle (66°33´39˝ N) you enter the northern polar zone, historically termed the Frigid Zone, a region of extreme climatic stress that supports an ecosystem called tundra, realm of musk oxen and polar bears. The same, of course, is true climatically when you cross the Antarctic Circle (66°33´39˝ S) and enter the southern polar zone, the land of vast ice and diverse penguins. Immediately beyond the Torrid Zone latitudes you move into the subtropics (plate 1-7). It is not unusual for parts of Florida to experience winter frosts, but nonetheless the southern areas of Florida, including Everglades National Park, are ecologically subtropical. Species of typically tropical plants such as mangroves and the Gumbo Limbo tree (Bursera simaruba) are found here. Many physical characteristics of typical tropical forests (such as the presence of high levels of

17

Plate 1-7. The American Alligator (Alligator mississippiensis), here shown in a tableau along with several Yellow-bellied Slider turtles (Trachemys scripta), is a subtropical reptile that is the northernmost representative of its family. This photo is from coastal Georgia, near Savannah. In the Neotropics, there are species similar to alligators called caimans, along with several crocodile species, one of which, the American Crocodile (Crocodylus acutus), just reaches southern Florida. Photo by John Kricher.

epiphytic plants and buttressed roots) are evident to various degrees in coastal forests as far north as the Georgia–South Carolina border (plates 1-8–9). This is because the warm oceanic currents of the Gulf Stream (discussed below) allow the coastal Southeast to remain relatively balmy throughout the year, extending the subtropics northward (plate 1-10).

But Where, Exactly, Are the Neotropics? Because of the mild climate provided by the warm and complex current known as the Gulf Stream, the Caribbean islands all are part of the Neotropical realm, even though some (such as the Bahamas and Bermuda) are outside of the Torrid Zone. Therefore, the islands of the Bahamas, the Greater and Lesser Antilles, the West Indies, and so forth, are all in the Neotropics. So if you have taken a trip to Abaco, Jamaica, Puerto Rico, Martinique, or Cuba, you have visited a Neotropical place. Much of northern and western Mexico is either subtropical or temperate (because of the influence of

18

chapter 1

Plate 1-8. A tree branch covered by epiphytic plants is typical of tropical forests throughout the world. However, this branch belongs to a Southern Live Oak (Quercus virginiana), found not within the Torrid Zone but near Savannah, Georgia, in the subtropics. Characteristics of tropical forests are evident to varying degrees in subtropical forests. Photo by John Kricher.

Plate 1-9. Root buttresses are characteristic of many tropical trees but are not confined to tropical trees. This strongly buttressed tree is a Bald Cypress (Taxodium distichum), photographed in the temperate subtropics near Savannah, Georgia. Photo by John Kricher.

Plate 1-10. The Zebra Longwing (Heliconius charithonia) is widespread in the Neotropics and subtropics, ranging from Texas and Florida through South America. It is one of the only heliconius butterflies to reach North America. Photo by John Kricher.

mountain ranges) in climate, but the lowland eastern slope of Mexico adjacent to the warm Caribbean Sea (Veracruz, for example) is warm and humid. Indeed, it is in this region that you find the most northerly extension of Neotropical evergreen moist forests. The remainder of Middle America, Belize, Guatemala, Costa Rica, Nicaragua, Honduras, El Salvador, and Panama, is Neotropical, and each of these countries contains typical tropical ecosystems. Finally, and perhaps most obviously, we come to South America. This huge continent contains the largest

tract of remaining tropical rain forest in the world, the immense Amazon Basin. While the country of Brazil holds claim to most of Amazonia, all neighboring countries share part of it. Thus you can visit diverse tropical lowland evergreen forest not only Brazil but also in Bolivia, Peru, Ecuador, Colombia, Venezuela, Guyana, Suriname, French Guiana, Paraguay, and parts of northern Argentina. Note that the southern regions of South America in Chile and Argentina are south of the Torrid Zone and have a temperate, seasonal climate.

welcome to the torrid zone

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It’s Not All “Tropical” Even in the Torrid Zone Imagine that you are exiting your hotel in Guayaquil, Ecuador, a sea-level port city, for a brief ride to the airport. You walk out from the air-conditioned lobby into hot and decidedly humid air. It’s muggy and feels very “tropical.” After a short and scenic flight, your aircraft touches down in Quito, about 267 km (166 mi) away, as the Andean Condor flies. You have left the sultry sea-level climate of Guayaquil for the clear Andean air of Quito, which is located at about 2,800 m (9,200 ft) above sea level. The climate feels decidedly temperate, cooler and drier. That’s because it is. Latitude alone does not determine the tropics. Elevation is also a critical variable. The youthful and dynamic Andes Mountains run the western length of South America, extending from Tierra del Fuego at the southern tip of the continent all the way north and east through Venezuela, ending in the gentle northern and central ranges of the island of Trinidad. The great European explorer Alexander von Humboldt (1769– 1859) was the first to describe in detail how habitats change with elevation (plate 1-11). He is credited with having elucidated the concept that was later formalized and called the ecological life zone (detailed in chapter 2). Humboldt realized that climate characteristics change with elevation and that climate, as you might have surmised by now, is the most important variable in determining what sort of habitat or ecosystem will be present. Humboldt documented how a zone of lowland tropical forest (i.e., rain forest) gradually transitions into cloud forest with increasing elevation and how, above cloud forest, trees become increasingly stunted until a zone is reached called páramo, a cold and windswept ecosystem of tussock grass and dwarfed trees. Snow is common at this elevation. When it comes to ecological

Plate 1-11. Alexander von Humboldt was the first explorer to carefully document how life zones change with elevation and thus elucidate the importance of mountains, such as the Andes, shown here in Ecuador, to the diversity of ecosystems in the tropics. Photo by John Kricher.

Plate 1-12. Snow in the tropics? Tussock grass and low-growing plants poking out from newly fallen snow might suggest an ecosystem such as the moors of England and Scotland. But this is just outside of Quito, Ecuador, at an elevation of about 3,355 m (11,000 ft), in the Andes Mountains. Photo by John Kricher.

Humboldt on the Rain Forest The German-born naturalist and explorer Alexander von Humboldt led an expedition to Central and South America from 1799 to 1804. He wrote of his first impressions of rain forest: An enormous wood spread out at our feet that reached down to the ocean; the tree-tops, hung about with lianas, and crowned with great bushes of flowers, spread out like a great carpet, the dark green of which seemed to gleam in contrast to the light. We were all the more impressed by this sight because it was the first time that we had come across a mass of tropical vegetation. . . . But more beautiful still than all the wonders individually is the impression conveyed by the whole of this vigorous, luxuriant and yet light, cheering and mild nature in its entirety. I can tell that I shall be very happy here and that such impressions will often cheer me in the future. (Quoted in Meyer-Abich 1969.)

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montane (i.e., mountainous) life zones, the latitude may be well within the Torrid Zone, but elevation makes all the difference. Indeed, if you have a strong enough arm you could stand on the equator high in the Andes and toss a snowball east into the hot and steaming jungles of Amazonia far below (plate 1-12).

So What Actually Are the Tropics? The climate of the tropics will form the main topic of the next chapter, but for now, know this: a tropical climate is consistently warm but variably wet. Much of the area within the tropic zone is not rain forest. There are, for example, deserts in the tropics, including the desolate Atacama Desert of coastal Peru and Chile. The African Serengeti, which is a vast savanna of grassland and scattered trees, is famous for the forced annual migrations of herds of large animals such as wildebeest, which must move seasonally to find water. Much of central and southern Brazil is cerrado, an ecosystem

ranging from dry forest to open grassland depending upon seasonal moisture input and occurrence of natural fire (chapter 14). Therefore, a large part of the tropics experiences a seasonal climate in which the seasons vary between rainy and dry rather than hot and cold. Tropical areas have relatively little annual variability in air temperature (and the temperature is generally quite warm), but rainfall amounts may vary dramatically throughout the year, something to bear in mind when you plan a trip. Tropical ecologists speak of wet and dry seasons rather than winter (implying cold) and summer (implying heat). However, in many lowland rain forests rainfall is sufficiently abundant on a daily basis throughout the year that the dry season is scarcely expressed, and thus the forest remains constantly wet and lush year-round. This is true rain forest. Most people who visit the Neotropics tend to seek a rain forest experience and thus should be prepared for heat, humidity, and a bit of rain, sometimes quite a bit of rain, often daily.

Plate 1-13. Dense, complex tropical rain forest is home to more species than any other terrestrial ecosystem on Earth. Photo by Beatrix Boscardin.

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Welcome to the Jungle: A Quick Overview Because of the relatively constant presence of heat, rain, and humidity, much of the Neotropics is biologically lush, profligate with species of plants and animals (plate 1-13). It is this profusion of diverse life that attracts so many ecologists as well as ecotourists to tropical destinations and has long fascinated explorers and naturalists, including Charles Darwin, Alfred Russel Wallace, and Theodore Roosevelt. Lifeforms are not randomly distributed on Earth. Tropical terrestrial ecosystems occupy only about 7% of Earth’s surface but are believed to hold more than 50% of the world’s terrestrial plant and animal species. There is a very basic observation nested in this reality: tropical climate is conducive to supporting diverse life, more so than any other climate to be found on the planet. As climate becomes less warm, less moist, less equable, fewer species are to be found. The term biodiversity, referring generally to the sum total of species present in an area or region, has come into common usage over the past decades. Indeed, one of the principal concerns of ecologists is that the present century will see a severe reduction in global biodiversity, including many species of tropical organisms (chapter 18, and see “Conservation Issues,” below). The profusion of life in the tropics takes physical form in the concept of the rain forest biome once commonly referred to as “jungle.” Tarzan, as most of us know, lived happily in the African jungle, moving easily from one place to another by swinging on vines while hollering loudly. As a child in the early 1950s I used to watch a television show titled Ramar of the Jungle, about a medical doctor facing heroic weekly situations as he plied his way through the jungles of Africa and India. It wasn’t a great show but it did get me interested in the tropics. And one of my first really good introductions to tropical plants and animals was Ivan Sanderson’s classic Book of Great Jungles (1965). So what is a jungle? The term (derived from the Sanskrit word jangala) has always been associated with dense tropical forests and usually invokes visions of plant growth so prolific as to be virtually impenetrable. The mind’s eye sees massive trees draped with thick vines, a mysterious and somewhat foreboding blanket of vegetation hosting a strange cacophony of birds and insects. But that vision is not entirely accurate, and rain forest and jungle do not mean quite the same thing.

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It is true that there are many places in the tropics where the vegetation is so profuse as to require the skilled use of a tool such as a machete to move through it. But these are typically areas of relatively recent disturbance (chapter 7), such as cleared areas that then receive abundant sunlight that promotes rapid and prodigious plant growth. Where there is mature, old-growth rain forest the sense of impenetrability is much reduced. It is actually no more difficult to maneuver through rain forest than through most temperate-zone forest. Large trees are relatively widely spaced, and the lack of light at the ground surface (because of the dense leafy canopy above) prevents much in the way of plant growth that would impede movement along the forest floor. Tropical rain forest is tall, lush, and most of all diverse with species. (It will be described in detail in chapter 3). It is without doubt the ecosystem that most visitors to the Neotropics seek to experience. Fortunately, there are still many places where that is easily possible.

Visiting the Neotropics When A Neotropical Companion was first published (in 1989) there were relatively few well-known and reliable tourist facilities within the Neotropics. The famous Asa Wright Nature Centre on Trinidad was one of them. This one-of-a-kind guesthouse, now much expanded, offers easy access to lush forest abounding in tropical wildlife (about 2,200 plant species, 617 butterfly species, and 400 bird species) and has been visited by thousands of naturalists since the 1950s. It remains today one of the premier destinations in which to experience the Neotropics. Since 1989 Neotropical ecotourism has burgeoned and, unsurprisingly, so has the availability of fine accommodations throughout the region. It is now possible to book a stay at any number of highly comfortable and commodious lodgings (far too many to list in this book) in virtually any Neotropical country, each of which generally offers a tasty (and safe) cuisine, hot showers, clean and comfortable rooms, and, most important, highly competent local guides. One example is the Canopy Tower, located in Soberania National Park, Panama, very near the Panama Canal and just a short drive from Panama City (plate 1-17). This unique facility, located high atop Semaphore Hill Road, is an old radar installation that has been completely renovated, upgraded, and converted to an ecotourism

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The Asa Wright Nature Centre and Simla The Asa Wright Nature Centre bears the name of a courageous and formidable woman, Asa Wright, who, along with her husband Newcombe Wright, developed a lush plantation in the Arima Valley within the northern mountain range in Trinidad, where they grew coffee, cacao, and various citrus species (plate 1-14). Asa and Newcombe Wright hosted many illustrious visitors at their Spring Hill Estate, as the house and property that became the center was then known. Most famous among them was the eminent naturalist, author, and explorer William Beebe (1877–1962). When Beebe was 73 he purchased land in the Arima Valley near the Spring Hill Estate and moved there, starting a field station in 1950, which he named Simla. Beebe welcomed researchers to the tropics and encouraged them to work with live animals, not just collect specimens for museums. Ornithologists such as David and Barbara Snow came frequently and contributed immensely to the understanding of tropical bird ecology and evolution (as will be discussed often in this book).

Large numbers of visitors enjoy the spacious veranda at Spring Hill Estate as well as the many trails that provide access to the Arima Valley and its magnificent forest (plate 1-15). When Newcombe Wright died in 1967 an effort was made to secure the property for education and conservation. With the help of numerous individuals and organizations, including the renowned bird artist Donald Eckelberry and the philanthropist Erma J. Fisk, the Asa Wright Nature Centre was established. Asa Wright remained a resident of the house until her death in 1971 (plate 1-16). Today the property includes in excess of 400 ha (approx. 1,000 ac) of protected land, including the Dunston Cave, perhaps the easiest place in the Neotropics to see the remarkable Oilbird (Steatornis caripensis; chapter 10). The spacious veranda of the original house overlooking the Arima Valley is one of the best places in the tropics to see and enjoy numerous birds and other species. And yes, complimentary rum punch is served every afternoon, in the fine tradition established by Asa Wright.

Plate 1-14. The magnificent Arima Valley, as seen from the veranda of the Asa Wright Nature Centre. Photo by John Kricher.

Plate 1-15. The famous veranda at the Asa Wright Nature Centre. Photo by John Kricher.

Plate 1-16. Asa Wright’s original living room at Spring Hill Estate, now the Asa Wright Nature Centre, has been and continues to be enjoyed by thousands of visitors over the years. Photo by John Kricher.

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facility of the highest quality. It offers an outstanding rain forest experience that includes daily guided tours to such places as the famous Pipeline Road, one of the most important field sites in historic and ongoing studies of Neotropical ecology (and located very near Barro Colorado Island, one of the most important research stations in the Neotropics). As with most other lodges, it is easy to book reservations on the Internet for the Canopy Tower (and its sister facilities, the Canopy Lodge, Canopy Camp, and Canopy B&B, take your choice).

Canopy Walkways and Towers It was long ago realized that many species of tropical animals spend most of their energy foraging in the forest canopy. But that means that everything from colorful butterflies to numerous birds may be 30 m (98 ft) or more away from the ground-based observer. What if you could actually get up into the canopy of a tropical forest, among the foliage, what would you see? The answer is becoming more and more evident, as various research stations and ecotourism lodges erect canopy towers and walkways that allow visitors some limited but significant access to this remarkable zone of life (plates 1-18–19). Carefully engineered and constructed canopy towers and walkways allow you to look directly into fruiting trees and watch monkeys, toucans, parrots, tanagers, and many other species as they forage. There is nothing quite like it. The View from Above As astronaut John Glenn passionately stated while he was rocketing high above Earth at the commencement of his orbital mission in Friendship 7 in 1962, “Oh, the view is tremendous.” That holds true for canopy walkways and towers throughout the tropics. My first visit to a canopy walkway was at the ACEER Foundation, the Amazon Center for Environmental Education and Research (plate 1-20). It is located in one of the most species-rich areas in upper Amazonia, along the Amazon River, about 160 km (100 mi) east of Iquitos, Peru. The site includes a superbly engineered canopy walkway about 0.4 km (0.25 mi) in length, an elaborate arboreal pathway interconnected with 14 emergent trees, permitting one to literally walk through the rain forest canopy. Each of the trees used in the walkway is fitted with strong wooden platforms

Plate 1-17. The wraparound observation deck on the Canopy Tower near the Panama Canal in Panama allows for a full, 360° panorama of the landscape at treetop level. Monkeys, toucans, and other tropical animals are easy to observe. Photo courtesy of Canopy Family.

Plate 1-18. This wooden canopy tower at Sacha Lodge in Ecuador literally circles a huge emergent tree, affording views at various levels as you climb the tower. Photo by John Kricher.

Plate 1-19. The canopy walkway at Sacha Lodge allows one to safely peruse a large swath of tropical forest from treetop level. Photo by John Kricher.

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allowing several people to stand and look out at the canopy. The narrow spans between the tree platforms are built rather like suspension bridges, supported by strong metal cable and mesh-lined at the sides to provide total security and safety. The spans vibrate a bit, especially when more than one person is walking across. One of the spans, when I visited, was nearly the length of a football field, affording a breathtaking, if shaky, look at the rain forest below. The first of the platforms is about 17 m (55 ft) above the forest floor, but the spans eventually take you to a platform that is fully 36 m (118 ft) above the ground. From that privileged position, you gaze upon a panorama of unbroken rain forest for many, many miles. The view is tremendous. From within the canopy you get an immediate, almost overwhelming impression of the richness of the rain forest. Trees are anything but uniform in height— and of so many species that you wonder whether any two along the walkway’s length are the same, or if every tree is different from every other. You notice the many different leaf sizes and shapes and see that some leaves are damaged by leaf-cutter ants, the insects having traveled 30 m (98 ft) up the tree bole to collect food for their subterranean fungus gardens. Now you can really look at the fine details of epiphytic plants such as orchids and bromeliads. You can see down into the cistern-like bromeliads and learn what kinds of tiny animals inhabit these microhabitats high above the forest floor. You note the uneven terrain below and realize that the canopy is by no means continuous but is punctuated by frequent openings of various sizes, called gaps. A male Collared Trogon (Trogon

collaris) is perched 6 m (20 ft) below the walkway. How odd it is to actually look down on such a creature. A male Spangled Cotinga (Cotinga cayana), a stunning turquoise bird whose plumage seems to shimmer with iridescence in the full sunlight, sits in display at eye level (plate 1-21). A tree near one of the platforms is in heavy fruit, hundreds of small orange berrylike fruits peppering the branches. Fruit trees normally attract a crowd, and this one is no exception. Colorful tanagers of six different species fly in to feast on the fruits, at most just 3 m (10 ft) away from us. Equally gaudy aracaris and toucanets join the tanagers. Two sedate, long-haired saki monkeys (Pithecia spp.; plate 1-22), apparently a female and an adolescent, stop at the fruiting tree. The monkeys’ long, bushy tails hang limply below the branch on which they sit, as these simians do not have prehensile tails, as do their forest cohabitants, the howler, spider, and woolly monkeys (see chapter 16 for more on monkeys). The simians soon realize they are not alone. The female sees us and rubs her chin on the branch. She stands fully erect and emits a short, demonstrative hoot to warn us to come no closer. She needn’t worry. We are not about to leave the security of the walkway. We marvel at how monkeys have adapted the requisite skills to move effortlessly through such a tenuous threedimensional world as the rain forest canopy. A frenetic Amazon Dwarf Squirrel (Microsciurus flaviventer), a chipmunk-size evolutionary relative of the northern acorn collectors, scurries with nonchalance on the underside of a branch over 30 m (98 ft) from the ground

Plate 1-20. Early morning in the canopy at the Amazon Center for Environmental Education and Research (ACEER), looking down. Photo by John Kricher.

Plate 1-21. A male Spangled Cotinga at eye level, a view that is impossible unless you have access to the rain forest canopy. Photo by Gina Nichol.

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below. A thought occurs, and recurs many times: from the ground, we’d never know this little animal was up here. The canopy walkway affords a unique and broad window into the life above the forest understory. It is exciting to visit it, to be on it at dawn, when the forest below is still clothed in mist, or to watch the sun set over what seems like an endless vista of rain forest. But it also affords an opportunity for the kind of research that needs to be done to accurately ascertain an understanding of the rhythms of life in this essential habitat.

Ecotours and Lodges The Canopy Tower and its associated sites the Canopy Camp and Canopy Lodge (in Panama), noted above, are all wonderful destinations in the Neotropics. And there are numerous other fine lodges and facilities. A quick but thorough Internet search will turn up many possibilities for places to stay, depending upon which countries you wish to visit and how long you wish to stay. For example, if you want to sail the Amazon River, you can book passage on a comfortable, wellappointed boat and take a river tour from Iquitos, Peru, or Manaus, Brazil. Another approach to visiting the Neotropics, also easily accomplished on the Internet, is to book an ecotour with an established tour company. Many such companies exist, and they offer customized itineraries tailored to show you the most wildlife in the shortest time period, all the while attending to your comfort and safety. Many of these tour companies routinely base their tours at outstanding facilities such as the Asa Wright Nature Centre (Trinidad), the Lodge at Pico Bonito (Honduras), the Canopy facilities (Panama), Monteverde and Selva Verde (Costa Rica), Chan Chich Lodge (Belize), Explorama (Peru), and Sacha Lodge (Ecuador), a list far from exhaustive. Most will categorize their tours as to whether or not they are strenuous, relaxed, and so forth. Many companies specialize in birding tours, but even highly focused birding tours rarely neglect the many other amazing animals as well as plants that are part of the tropical landscape. If you elect to take an ecotour, once you meet your guide everything else is pretty much done for you. You are told when to be at breakfast, how long you will be in the field, what to wear, what to expect, and there is usually a nightly session (either before or after dinner) devoted to summarizing the day’s observations and briefing you

Plate 1-22. Face to face with a saki monkey. Photo by Sean Williams.

about tomorrow’s activities. It is a great way to learn a lot in a short time span. Finally, if sufficiently independent, you might want to go it alone. The Pan American Highway extends through Mexico and Central America, stopping within the Darién in Panama. It picks up again in Colombia and extends south from there through Ecuador, Peru, and Chile. I don’t recommend that you drive the length of the Pan Am Highway unless you are highly adventurous. It is much easier to pick a destination, fly there, and rent a vehicle if you choose to explore on your own. Be aware that if you are on your own you must take care to assure all aspects of your comfort and safety. In most places, knowing a reasonable amount of Spanish is essential (or Portuguese if you are in Brazil).

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What about Bugs, Spiders, and Snakes? It is the question I am asked the most often. “If I go anywhere in the Neotropics, am I going to be consumed by hordes of biting insects (that are sometimes vectors for malaria and other serious maladies), carried off by army ants, or bitten by a venomous spider or snake?” The patterns of arthropod abundance as well as the ecology of army ants will be treated in detail (chapter 10), as will snake distribution and abundance (chapter 16). But for this overview, suffice it to say that indeed, mosquitoes, ticks, and biting flies of various species are present, on occasion in abundance. Mosquitoes tend to be most numerous in rainy season, while forest ticks sometimes abound in dry season. It is wise to bring ample repellent (yes, with Deet, though some less noxious organically based repellents suffice in many situations) and to keep yourself reasonably well covered when you can plainly see that biting insects are present. If you are going into a region where forms of malaria are known to occur, consider consulting your physician about taking a malaria-prevention drug beforehand. Caution also suggests getting inoculated for yellow fever prevention, as that mosquito-vectored virus occurs in many Neotropical areas. Some countries require that you be inoculated against yellow fever before they permit you to enter. See the Appendix for more on this subject. Spiders and scorpions are generally little cause for any alarm, but a few species can inflict sufficient toxin that one needs to observe prudent caution when around them. Most people seem to have a more or less natural aversion to picking up spiders and scorpions— and rest assured, the spiders and scorpions prefer it that way. But also be aware that spiders and their kin are really quite diverse and fascinating and, viewed from a respectful distance, only add to your tropical experience (plate 1-23). As for snakes, they are plentiful, and there are indeed areas throughout the Neotropics where venomous species are among the most commonly encountered serpents (plates 1-24–25). That being said, encountering snakes in general is not very common. Many visitors to the Neotropics return somewhat disappointed that they have not gotten to see a venomous (or even a nonvenomous) snake during their stay. Still, venomous snakes are there and really are relatively numerous, occurring in fields, in forests, and sometimes around

Plate 1-23. Closely observing a colorful Golden Orb (or Banana) Spider (Nephila clavipes) is a cause for wonder and celebration, not fear. Learn to love invertebrates, and you’ll be glad you did. Photo by Dennis Paulson.

Plate 1-24. Snakes are widespread in the tropics. Many, like this cryptically colored Cope’s Parrot Snake (Leptophis depressirostris), are harmless, containing no venom. Photo by Dennis Paulson.

Plate 1-25. Some snakes, like this Fer-de-lance (Bothrops atrox), are highly venomous and must be avoided. Do not disturb. Photo by James Adams.

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habitations. Most are not obvious until you are right upon them (sometimes literally!). So be careful, carry a flashlight when you are out at night, even on clear trails, and do not wander off the trails, for doing so strongly adds to potential risk of a snake encounter.

Conservation Issues: A Roomful of Elephants It is not possible for any well-informed person to be unaware of the numerous conservation issues facing our planet and our species in the present century. I devote the final section of this book (chapter 18) to a summary of conservation issues that apply to the tropics. But at this early juncture, it is important to provide an overview. Much attention has been given to reduction of rain forest and other tropical ecosystems. Without question, ecologists agree that loss of natural habitat—to human colonization, agriculture, plantation development, pasturage, and the increasing construction of hydroelectric dams—ranks at the top of tropical conservation concerns. The so-called human footprint is continually expanding in the tropics as it is elsewhere. Given the tropics’ high incidence of endemic species (one that has a range strictly limited to one given area, presumably where the species originally evolved; see chapter 8), the potential for loss by extinction is increased with habitat reduction. For example, the Golden Lion Tamarin (Leontopithecus rosalia; plate 1-26), a small, colorful monkey, is endemic only to the much-reduced and endangered Atlantic Forest in southeastern Brazil. Its future is uncertain. Human conversion of tropical ecosystems typically results in much (sometimes extreme) simplification of ecosystem structure and consequently the reduction of its overall biodiversity. In southern Brazil as well as parts of Panama, I have seen innumerable acres of planted Asian Teak (Tectona grandis), all in straight rows, reducing local biodiversity. It is interesting to note that no form of human activity results in increasing biodiversity unless it is specifically directed toward that goal. Virtually all manifestations of human development reduce biodiversity by ecosystem simplification. Habitat loss is often accompanied by such effects as fragmentation of forest and other ecosystems into smaller and smaller, more isolated parcels. Further, even what appear to be intact forests

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may be significantly degraded by logging, hunting, and other practices. At the time of this writing there are ongoing projects to construct major hydroelectric dam complexes at various places in Brazil. These immense dams will result in further loss of forest, displacement of possibly thousands of indigenous people, and potential alteration of the Amazonian rainfall pattern, a result that could accelerate drought frequency. There has been much attention given to the rate of deforestation in tropical regions, particularly in Amazonia. Most people assume that deforestation applies only to lowland rain forest, but that isn’t so. Other ecosystems, many with unique biological characteristics, are also subjected to degradation and clearance. An example is the cerrado (chapter 14), a region of grassland and dry forest bordering parts of Amazonia. Much of this region of high endemism, particularly regarding plant species, is now devoted to soybean and teak cultivation. But in general the rate of deforestation has declined in Amazonia, and since 2004 it has fallen below what it was at its peak in the 1980s. Numerous websites from various organizations report different totals, but one widely cited figure is that at least 580,000 km2 (224,000 mi2)—an area about 83% of the size of Texas—have been cleared in Brazil since 1980. A major question on the minds and research agendas of tropical ecologists is whether or not degraded or cleared tropical areas will recover if left to do so. Will areas cleared for agriculture, if abandoned, return to rich forest, and if so, how long will that process take? The question of the resiliency of tropical forests is a current topic of debate.

Plate 1-26. The Golden Lion Tamarin, endemic to forests of southeastern Brazil, is endangered by habitat loss. Photo by Andrew Whittaker.

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Another source of conservation concern is the changes that are occurring in the global cycling of such essential elements as nitrogen and phosphorus, as well as more esoteric chemicals that act as global pollutants. By altering natural biogeochemical cycles (chapter 6) it is possible to alter whole ecosystems, reducing the efficacy of such systems with regard to photosynthesis and carbon sequestration (chapter 5). Throughout much of the world, ecosystems are changing rapidly in large part because of the accidental and sometimes intentional introduction of species that are not native to the region. Some of these alien plants and animals become invasive species and rapidly replace numerous native species, resulting in extreme ecosystem simplification. Ecologists speak of no-analog ecosystems to describe ecosystems now consisting of unique assemblages of species that have no historical precedent. These kinds of ecosystems are becoming common in many areas. Thus far the tropics, and in particular the highly diverse lowland rain forests, seem less affected by this global trend toward unique species mixing. This observation may be premature, but if it is true it might be due to the high diversity of well-adapted native species populating these rich ecosystems. Such a richly diverse

community may be relatively resistant to invasive species. The event of most potential significance throughout the century is global climate change, the really big “elephant in the room.” Climate change is being documented most dramatically in polar regions (such as with the progressive melting of the polar ice cap, melting of permafrost, and the reduction of glaciers), though its effects, both physical and biological, are also being measured in numerous other regions. Tropical climate was once far more extensive on Earth than it is today, and with the overall rising of Earth’s temperature the tropics may again expand. But in the short run, in time units meaningful to humans, the initial result of global warming in the tropics will likely be what ecologists term lowland species attrition. What this means is that if tropical plants and animals typical of lowland rain forest are forced out of their respective tolerance zones for temperature, they may be very limited in their ability to disperse to other more suitable regions or to genetically adapt to the increasing warmth (plate 1-27). No one really knows what the result of global climate change will be in the tropics. There is much about the tropics and their ecology that remains to be discovered as well as understood.

Plate 1-27. The Cone-billed Tanager (Conothraupis mesoleuca) is a critically endangered species that was known only from a specimen collected in 1938. It was recently rediscovered in the southwestern Brazilian Amazon region. Only about 50 individuals are thought to exist, but much remains to be learned about the species and its current distribution. Photo by John Kricher.

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Chapter 2 Why It Is Hot, Humid, and Rainy in the Tropics “Hot, humid, and rainy” is the first observation virtually everyone makes about the tropics, particularly the lowland tropics. The aircraft door swings open, and as you exit there is a rush of hot and humid air in your face. The cool and dry air-conditioned cabin of the aircraft is past tense as you enter a world where the dew point is rarely out of the uncomfortable range and often in the oppressive range. No, it is not just the heat; it’s also the humidity. It takes some getting used to. In this chapter I will explain why the tropical climate is so hot and muggy and why that is really important with regard to ecology, particularly of rain forests.

climate (and only three), to accurately determine just what sort of terrestrial ecosystem would occur in any area on Earth. Those three measurements are (1) mean annual temperature, (2) total annual precipitation, and (3) ratio of potential evapotranspiration (which is a function of both moisture and temperature) to mean annual precipitation. Holdridge published a now famous triangular diagram in which each side of the triangle represented one of the three climate variables he had identified (fig. 2-1). He was able to show that each of the world’s major ecosystem types fell into a climate-determined hexagonal spot on the triangle. Holdridge referred to each of the hexagons as a life zone. Rain forest was at the lower right of the triangle; its climate was described as super humid and uniformly warm, with high annual precipitation. Holdridge noted that his life-zone diagram applied both latitudinally and elevationally. The power of Holdridge’s approach was that he showed unequivocally that climate and climate alone is the principal determinant of the structure of terrestrial ecosystems. All other variables are secondary. Though Holdridge’s triangle diagram is conceptually simple, it may be further simplified by graphing mean

On Biomes and Life Zones: Just Three Numbers

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Figure 2–1. Leslie R. Holdridge’s classic and innovative triangle diagram spoke clearly to the power of climate to determine fundamental characteristics of terrestrial ecosystems. From Holeridge, L. R. 1947. Determination of world plant formations from simple climatic data. Science 105: 357–368. Image adapted from Peter Halasz. Reprinted with permission from AAAS.

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annual temperature against mean annual precipitation (fig. 2-2). Tropical rain forests will fall into the area on the graph where mean annual temperature is 20–30° C (68–86° F) and annual precipitation is 250–450 cm (98–177 in). Tropical seasonal forests (often referred to as tropical moist forests) are in exactly the same range of annual temperature range, but precipitation is lower, between 150 and 250 cm (59–98 in), and often uneven throughout the year, so there are distinct rainy and dry seasons. Note that for most visitors to the tropics, what passes for tropical “rain forest” is actually within the definition of tropical moist forest. Nonetheless, these forests are extremely wet and lush, and they look and “feel” 100% tropical. In areas with even less annual precipitation the tropics support dry deciduous forest or perhaps savanna, primarily a form of grassland, usually with scattered trees of varying density (chapter 14). The power of Holdridge’s analysis is in how it shows the pervasive influence of climate in determining the structure of terrestrial ecosystems. Other variables also come into play but to lesser degrees. Geology as it affects soil characteristics (what ecologists call edaphic factors) is very influential on ecosystem characteristics, as are various biological factors. Nonetheless, rain 15

forests and other ecosystems are products primarily of climate. The meaning of that statement will become increasingly clear as we look at rain forest plant characteristics and plant adaptations (chapter 3).

How’s the Weather Today? The Feel of the Tropics Should you decide to move to Manaus, Brazil, or perhaps to Iquitos, Peru, both well within the Amazon Basin, you should expect at least 130 days of rain per year and in some places up to 250 days with at least some rain. So, bring an umbrella. But wear light clothing because the air temperature will be consistently warm, indeed, often rather hot, with daytime high of about 31° C (88° F) and a nighttime low of about 22° C (72° F). The relative humidity is rarely less than 80%, so the combination of heat and humidity means the “feel” of the weather can be much more stifling than temperature alone would indicate. Though it can rain on any given day, rainfall, in most places, is relatively seasonal (fig. 2-3). In the Amazon Basin, the very heart of the lowland Neotropics, the climate is permanently

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Figure 2–2. By comparing mean annual precipitation and mean annual temperature it is easy to see that the area we call the humid tropics falls into the maximum category for both climatic variables. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

why it is hot, humid, and rainy in the tropics

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Figure 2–3. The two graphs show the sharp contrast between a typical temperate climate, such as is found in Toronto, Canada, and conditions in the Torrid Zone, such as you would find in Belém, Brazil. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

hot and humid, with the temperature averaging somewhat higher during dry season than in rainy season. Realize that in the tropics, daily air temperature fluctuation actually exceeds average annual seasonal fluctuation, and humidity remains high, at about 88% in rainy season and 77% in dry season.

Trade Winds, Doldrums, and the Amazonian Heat Engine As mentioned in chapter 1, the tropics are warm and generally wet because the sun’s radiation falls most directly and most constantly upon the equator, thus disproportionally warming Earth in the tropical zone. At the equator, day length is 12 hours throughout the year. As one travels either north or south from the equator, Earth’s axial tilt results in the sun’s rays falling much more obliquely and for shorter periods of time (both of which make for colder air temperatures) for part of the year (called winter) and in the well-known cycles of day length associated with the changing seasons within temperate and polar regions. Equatorial heat quickly builds up, and the air rises, carrying the warmth. Heat strongly facilitates the evaporation of water, so water vapor rises as well. The warm, moist air is cooled as it rises, some eventually condensing as liquid water, which then falls as precipitation, accounting for the rainy aspect of tropical climates. The normal flow of warm, moisture-laden air is from equatorial to more northerly and southerly

latitudes. Again, as air rises, it cools and becomes increasingly dense. Moisture condenses, falling as rain, creating a backward flow of drier air toward the equator, where the cycle will, of course, be repeated. At the equator are two giant convective air masses, one from the north and one from the south, called Hadley cells. These, along with major ocean currents, form the Intertropical Convergence, or ITC, the major climatic heat engine on the planet. In the Amazon Basin, precipitation ranges between 150 and 300 cm (59–118 in) annually, averaging around 200 cm (approx. 80 in) in central Amazonia. What is most interesting about this pattern is that approximately half of the total precipitation is brought by incoming easterly trade winds off the Atlantic Ocean, while the other half is the result of internal ecological evapotranspiration from the vast forest that covers the basin. (Evapotranspiration is the evaporation of water taken up by tree roots and transferred through the vascular system of trees to leaves, where the water is evaporated into the air as an adaptation that aids in keeping the tree tolerably cool.) Up to 75% of the rain falling within a central Amazonian rain forest may come directly from evapotranspiration. This represents a tight recycling of water and, in essence, shows that Amazonia helps produce its own climate, a rather remarkable reality. This vast precipitation and waterrecycling system is essentially in equilibrium, though increasing large-scale deforestation would significantly disrupt it. Tropical areas generally fall within the belts of the trade winds (so-named because they proved favorable

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for sailing ships carrying goods for trading), except near the equator at the ITC, an area called the doldrums (fig. 2-4). In the doldrums the winds are usually light (often becalming sailing ships during historic times). From the equator to 30° N, the easterly trade winds blow steadily from the northeast, a direction determined by the constant rotation of Earth from west to east. South of the equator to 30° S, the easterly trades blow from the southeast, again due to the rotational motion of the planet. As Earth, tilted at its axis, moves in its orbit around the sun, its direct angle to the sun’s radiation varies with latitude, causing seasonal change. Such change is manifested in the tropics essentially by changing heat patterns of air masses around the ITC, resulting in seasonal variation in rainfall. In the Western Hemisphere, severe wind with accompanying anticyclonic rainstorms, called hurricanes (see “The Impact of Hurricanes,” below), often occurs from July throughout October in parts of the Neotropics. Similar kinds of storms are referred to as monsoons in the Old World tropics.

Length of the growing season is key to understanding how biomes vary. For example, the growing season in Ontario, Canada, which falls in the boreal forest biome, is a mere 140 days per year (obviously during the summer months). In comparison, North Carolina enjoys a growing season of about 200 days per year. This is why as you move south in March from, say, central New England to Georgia, the landscape becomes progressively greener. The growing season is longer in the South. In the tropics the growing season is generally year-round. This fact is extremely important in understanding the nature of ecosystems such as rain forest. The only factor limiting growing season in the lowland tropics is distribution of moisture. In areas of extreme dry season, the growing season is confined mostly to times when rainfall is adequate to support continued plant growth.

Direction of rotation

The Biome Concept Ecologists have long understood that the terrestrial world is organized into belts of major ecosystem types termed biomes. The tropical rain forest biome is equatorial, within the Torrid Zone. At the planet’s northern extreme is the arctic tundra biome, a vast polar region of treeless, windswept plains composed of mosses, lichens, and numerous perennial prostrate plants. South of the tundra is the northern boreal forest biome, often called the “spruce-moose” biome, a dense latitudinal belt extending around the world composed of mostly evergreen needle-leaved trees such as spruces, firs, and various pines. South of the boreal forest is the deciduous forest biome, a forest numerically dominated by broad-leaved tree species such as sycamores, oaks, maples, hickories, and numerous others, all of which drop leaves relatively synchronously in autumn and endure the cold of winter in a leafless state. There are also grassland and desert biomes, where water is variously limited. Most of the Great Plains of North America is natural grassland. The huge Mojave Desert west of the Rocky Mountains is cold desert, with winter snow. The Chihuahuan and Sonoran Deserts of the American Southwest and northern Mexico are considered hot deserts, where snow is rare.

North pole

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Figure 2–4. As planet Earth rotates from west to east it influences the movement of the various heat belts of the planet, creating trade winds north and south of the equator and the doldrums at the equator. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

why it is hot, humid, and rainy in the tropics

The Rain Forest Biome: Is the Climatic Devil in the Details? By now you ought to understand how much annual air temperature and moisture patterns affect, indeed determine, the actual nature of the world’s various biomes. What then is a rain forest? The physical structure of tropical rain forest will be the subject of chapter 3. But let’s define tropical rain forest here. It turns out that there are actually several definitions of rain forest in use by ecologists, and while generally similar, they are not precisely the same. You will have to choose the one you like when you visit there. The definition given by Holdridge in his life-zone model represents extreme rain forest, one that receives very high and continuous input of rainfall. Thus a “real” rain forest, in its purest form, is essentially a nonseasonal forest dominated by broad-leaved evergreen trees, sometimes of great stature, where rainfall is both abundant and relatively constant. Rain forests are the very definition of lushness, with many kinds of vines and epiphytes (air plants) draping the statuesque trees. In general, a rain forest receives at least 200 cm (just under 80 in) of rainfall annually, though it can be much more), with this precipitation spread relatively evenly from month to month. Much of the tropics consists, however, of forests where some seasonal variation in rainfall is both typical and ecologically important. Tropical forest with abundant but seasonal rainfall is often termed a moist forest rather than a rain forest. That being said, a moist forest is scarcely discernible from a rain forest. It is an evergreen or partly evergreen (some trees may be deciduous) forest receiving not less than 10 cm (nearly 4 in) precipitation in any month for two out of three years, frost-free, and with an annual temperature of at least 24° C (about 75° F) or more. Since the term rain forest is in such widespread and common usage, in this book I will continue to refer to lush, moist tropical forests, seasonal or not, as rain forests. I’ve had the pleasure of wandering in many moist forests from Belize to Brazil, and believe me it rains a lot in those moist forests, and gets pretty muddy too. So what it comes down to is seasonality. How extreme is dry season? That is really at the essence of understanding the ecological dynamics of tropical forests.

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The Importance of Seasonality Precipitation, all of which falls as rain in the lowland tropics, sometimes varies considerably from month to month and from one location to another. Overall, precipitation is highest in the central Amazon Basin as well as on eastern Andean slopes and lowlands, and is lower to the north and to the south, varying from about 150 cm (59 in) in the extreme north or south to about 600 cm (236 in) along some eastern Andean slopes. Even within the central Amazon Basin, seasonal rainfall is variable from place to place. For example, Iquitos, Peru, along the Amazon River, receives an average of 262 cm (103 in) of rainfall annually, while Manaus, Brazil, also on the Amazon River, receives an average of 177 cm (70 in) and experiences a distinct dry season. Forest structure varies between Iquitos and Manaus, mostly due to the difference in seasonal rainfall pattern and overall amount. As a more extreme example, Andagoya, in western Colombia, receives 709 cm (279 in) annually. (The highest rainfall on Earth, according to some authorities, occurs in Mawsynram, in Meghalaya, India, which annually receives 1,187 cm/467 in.) Where dry season is pronounced, many trees are deciduous, shedding leaves during dry season, rather as trees in the temperate zone do in the autumn months. Such tropical dry forests are sometimes termed monsoon forests, since they are in leaf only when the monsoon rains are present. Dry season is defined as less than 10 cm (4 in) of rainfall per month, and rainy season features up to 100 cm (39 in) of rainfall per month. A typical lowland tropical forest receives a minimum of between 150 and 200 cm (approx. 60–80 in) of rainfall annually. The rainy season varies in time of onset, duration, and severity from one area to another in the tropics. For example, at Belém, Brazil, virtually on the equator, dry season extends from August through November, and the wettest months are January through April. In Belize City, Belize, at 17° N, the rainy season begins moderately in early June but in earnest in mid-July and lasts through mid-December and sometimes into January. The dry months are normally mid-February through May. In general, when it is rainy season north of the equator, it is dry season to the south. Because the Amazon River flows on both sides of the equator (which side depends on location), parts of the huge river are experiencing wet season while other parts are in dry season.

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Why Be So Concerned about Seasonality? The seasonal shift from rainy to dry seasons has direct effects on plants and animals inhabiting rain forests as well as other tropical ecosystems. One common misconception about the tropics is that seasonality can generally be ignored. Far from true. Images of yearround sunny skies and soft trade winds are the stuff of myths. During the rainy season, skies are typically cloudy for most of the day, and showers, some heavy, are intermittent, often becoming especially torrential during late afternoon and evening. Such cloud cover, blocking sunlight from reaching the forest, can be a limiting factor on total photosynthesis, the overall productivity of the forest (chapter 5). Seasonal shifts are normal and often pronounced, and many ecological patterns, ranging from photosynthesis to flowering, reflect responses to seasonal changes. Some shifts are obvious, but many tend to be subtle; they vary considerably depending on the magnitude of the seasonality. Unlike an oak forest in Ohio in winter and summer, a moist forest in Panama will not look

very different in December compared with July. But there are differences, such as leaf drop by deciduous trees (plate 2-1). Henry Walter Bates, in The Naturalist on the River Amazons (1863), wrote of seasonal patterns as they affect life along the Amazon. At the onset of rainy season, he observed: All of the countless swarms of turtle of various species then leave the main river for the inland pools: sand banks go under water, and the flocks of wading birds then migrate northerly to the upper waters of the tributaries which flow from that direction, or to the Orinoco; which streams during the wet period when the Amazons are enjoying the cloudless skies of their dry season. Many more recent studies have abundantly documented the compelling drama of the changing seasons of the tropical forest. Many species of trees flower more commonly during the dry season, when less frequent and intense showers permit insect pollinators to be active for longer periods,

Plate 2-1. The bare trees in this Panamanian forest are Cuipos (Cavanillesia platanifolia). The Cuipo is deciduous, losing its leaves in dry season, which is when this photo was taken. Photo by John Kricher.

why it is hot, humid, and rainy in the tropics

thus enhancing efficacy of cross-pollination. Some tree species synchronize their flowering after downpours, an adaptation that may increase pollination efficiency by concentrating the number of pollinators. These patterns reflect the reality that most species of tropical trees rely on animals to cross-pollinate them, rather than wind-blown pollen dispersal, which is common in many temperate forest tree species (oaks and pines, for example). Dry season pollination also enables more seedlings to survive, because they sprout at the onset of rainy season, when there is adequate moisture available to ensure their initial growth. Patterns of plant reproduction vary, even within a single area. A study by N. C. Garwood of 185 plant species on Barro Colorado Island in Panama determined that most seedlings emerged within the first two months of the eight-month rainy season. That seems logical, given the plants’ need for water to grow. Forty-two percent of the plant species studied underwent seed dispersal during dry season and germination at the onset of rainy season. Forty percent of the species experienced seed dispersal at the beginning of rainy season, with germination occurring later in rainy season. So although time of seed dispersal varied (likely due to how the seeds were dispersed), germination always occurred at some point in rainy season. Approximately 18% of the species produced seeds that were dispersed during one rainy season, dormant during the next dry season, and germinated at the onset of the second rainy season. The species most sensitive to the onset of rainy season were “pioneer” tree species, lianas, canopy species, and both wind- and animal-dispersed species. Understory and shade-tolerant species were less sensitive.

The Increasing Prevalence of ENSO in the Tropics Beginning in the mid-20th century, short-term but major climatic shifts began happening with increasing frequency in the tropics. The shifts are due to ENSO, El Niño/Southern Oscillation. (Note that the original term for this climatic event was simply El Niño, but with increasing understanding of what is actually happening, the term now in use is ENSO.) ENSO, though becoming more frequent, remains difficult to fully explain with regard to exact cause. El Niño occurs approximately every two to seven years when a high-

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pressure weather system that is normally stable over the eastern Pacific Ocean breaks down, destroying the pattern of the westward-blowing trade winds. The trade winds weaken and sometimes reverse from their normal westward direction. Warm water from the western Pacific flows eastward, causing an influx of abnormally warm water toward the western coast of South America. This water column reaches a depth of up to about 150 m (approx. 500 ft) and, because it is warm and thus less dense, flows over and blocks the colder, more nutrient-rich waters below. This prevents the upwelling of nutrients into the upper water column, where they become available to phytoplankton. The result is that oceanic food chains are severely disrupted. When that happens, warm waters flow along the normally cold South American coast. Weather systems change, resulting in heavy downpours and flooding in some regions and droughts where there should be rainfall, effects which range ecologically from mildly stressful to highly significant. The El Niño of 1982–83 was considered at the time to be the most powerful of the 20th century, and is estimated to have caused $8.65 billion worth of damage worldwide. There have been eight major El Niño events since 1945, including several since 1982, and their frequency seems to be increasing. A severe El Niño occurred in 1986–87, and another occurred in 1994– 95, comparable to the two of the 1980s. Satellite data indicated that the northern Pacific Ocean was nearly 20 cm (8 in) higher than normal, due to the influx of warm surface waters. Yet another El Niño occurred in 1997–98, and its combined global effects are estimated to have resulted in 2,100 human casualties and property damage totaling a staggering $33 billion. In 2009–10 another El Niño altered weather patterns around the world. The winter of 2015–16 was characterized by the most significant ENSO event ever recorded, with massive amounts of rainfall and flooding in the Pacific Northwest and a severe dry season in parts of the tropics such as Panama (plate 2-2). The specific causal factors responsible for the periodicity of El Niños are thus far unknown but it is clear that the Intertropical Convergence zone, a complex system of oceanic and air currents, migrates to a lower latitude, raising sea surface temperatures and destroying the normal upwelling pattern along the western coast of South America. The cessation of an El Niño occurs when the ITC returns northward to its normal position. Though El Niño has global effects,

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tropical ecosystems in particular can be anywhere from moderately to severely affected. El Niños tend to alternate with another climatic phenomenon that produces largely the opposite effects called La Niña. Like El Niño, La Niña systems begin when normal trade winds are altered. In this case however, the westward trade winds gain abnormal strength and move further westward than normal, carrying warm surface water toward Asia. This creates enhanced upwelling of colder, deeper, more nutrient-rich water along the South American coast. Because the colder waters evaporate more slowly, rain is reduced and drought may result. La Niñas have followed El Niños after the 1982–83, 1986– 87, 1994–95, and 1997–98 El Niños. Ecologists realize that ENSO events cause shortterm but nonetheless significant perturbations in ecosystems including the lowland tropics. A major El Niño affected Barro Colorado Island (BCI) in Panama during 1982–83. One of the most dramatic effects of that El Niño was the failure of trees to produce fruit

during the second of two fruiting seasons. The failure of the fruit crop resulted in a cascade of severe impacts on various animals. Researchers on the island noted that normally wary species such as the Collared Peccary, coatis, Baird’s Tapir, and Kinkajou made regular visits to the laboratory area where food had been put out for them. Some of these animals appeared emaciated, obviously under stress from lack of food. Robin Foster, a researcher at BCI, wrote: The spider monkeys, which normally visit the laboratory clearing at least once every day, now launched an all-out assault on food resources inside the buildings, learning for the first time to open doors and make quick forays to the dining room table, where they sought bread and bananas, ignoring the meat, potatoes, and canned fruit cocktail, and brushing aside the startled biologists at their dinner. Dead animals, Foster wrote, were also encountered far more frequently than usual:

Plate 2-2. This photo was taken in January 2016, at extreme low water in a Panamanian river during a drought attributed to the most severe El Niño/Southern Oscillation event on record. Photo by John Kricher.

why it is hot, humid, and rainy in the tropics

The most abundant carcasses were those of coatis, agoutis, peccaries, howler monkeys, opossums, armadillos, and porcupines; there were only occasional dead two-toed sloths, three-toed sloths, white-faced monkeys and pacas. At times it was difficult to avoid the stench: neither the turkey vultures nor the black vultures seemed able to keep up with the abundance of carcasses.

The Impact of Hurricanes A large portion of the Neotropics north of the equator occurs within what is termed the hurricane belt. Storms, sometimes massive, form during the summer months in the Atlantic off the coast of western Africa and typically intensify as they slowly drift westward, toward the Neotropics. Hurricanes are generated by the heat rising from the ocean and thus may (and usually do) intensify as they move over the warm tropical seas. In the Northern Hemisphere these immense systems spin in a counter-clockwise rotation, easily seen in satellite photos. In the Southern Hemisphere they spin in a clockwise direction. Hurricane season begins in June and lasts until mid-November, but most major hurricanes tend to occur from August through October. Beginning as a tropical depression and intensifying to

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a tropical storm and then to a hurricane, these storms exert significant impacts on the ecology of the region. The word hurricane is derived from a Spanish word that is, in itself, taken from a Mayan word. Thus the word references a cyclonic storm in the New World. However, the actual storm is, for all intents and purposes, the same kind of storm that in much of the tropical Pacific region is called a typhoon. Hurricanes are evaluated on the Saffir-Simpson scale, on which they are given a ranking between one and five in order of wind intensity. A category 1 hurricane has winds of between 119 and 153 km/h (74–95 mph), while a category 5 hurricane has wind speeds of 252 km/h (157 mph) and above. Any hurricane, no matter what its category, is likely to damage landscapes. In the Neotropics, hurricanes typically move over the Bahamas and the Greater and Lesser Antilles, and often continue up the eastern coast of North America. But many hurricanes do not follow that course; some enter the Gulf of Mexico, while others continue directly westward across the Caribbean Sea, making landfall in eastern Central America. When this occurs large tracts of tropical forest, especially near coastal areas, are affected. Trees may be leveled over a large area. Thus hurricanes act as major disturbance factors that open large areas of forest to intensive sunlight, changing the characteristics of the ecosystem (chapter 7).

Global Climate Change Discovered on a Tropical Mountaintop The reality of global climate change has been well established, both historically, as it has occurred repeatedly over Earth’s long history, and as it is occurring in the present century. Climatologists study ice cores taken from glaciers to search for chemical and other signals that demonstrate temporal climatic oscillations and variation. Dr. Lonnie Thompson from Ohio State University has collected ice core samples from the Quelccaya ice cap, a glacier in the Andes Mountains of Peru. The ice cap, which sits at an elevation of about 5,486 m (18,000 ft), ranks as the largest area of alpine glacier within the tropics. The ice record from Quelccaya extends back in time for about 1,500 years and demonstrates that climate change in equatorial areas (such as dry periods and wet periods) has been a common occurrence. What is important about the Quelccaya ice cap today is its rate of melting, which has significantly accelerated in the present century. This high rate of glacial retreat is happening not only with Quelccaya but also elsewhere around the world. The work of Dr. Thompson and colleagues on Quelccaya ranks among the first studies to clearly demonstrate that Earth has entered a period of rapid climate change.

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Plate 3-1. The tropical rain forest is tall and structurally complex, challenging the naturalist to make sure to see the forest and the trees. Photo by John Kricher.

Plate 3-2. Imposingly tall and heavily buttressed trees are common to all of the world’s rain forests. Though mature Amazonian rain forests essentially look just like this, this photo was actually taken in Sabah, Malaysia, in northern Borneo. Photo by John Kricher.

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Chapter 3 Rain Forest: The Realm of the Plants First Impressions: Into the Forest Welcome to the green and complex world of the rain forest. As for first impressions, it doesn’t matter whether you’re standing in Peruvian, Brazilian, Ecuadorian, Belizean, Costa Rican, or Venezuelan rain forest—at first glance it all looks pretty much the same (plates 3-1–2). It even sounds, smells, and feels generally the same. All over the equatorial regions of the planet where rain forest occurs, the forest tends to have a similar physical structure and appearance. But this impression is deceptive. On closer inspection, numerous differences become apparent in rain forests both within and among various geographical areas. On a global scale, evolution has produced very different species, indeed different families of plants and animals from one biogeographic region to another. One does not find orangutans or rattan palms in Venezuela or sloths or hummingbirds in Borneo. Leaf-cutter ants, unmistakable and nearly ubiquitous throughout the Neotropics, exist nowhere else. And within the Neotropics, rain forests in Costa Rica are different in many significant ways from their counterparts in Brazil. And in Brazil, Amazonian forests show considerable differences from site to site. Some sites have dense rain forest, some more open forest with an abundance of palms, some open forest without palms, and some open forest with abundant lianas. Rain forests on poor soils differ markedly from those on richer soils, just as rain forests on terra firme (terra firme is a term used for area of forest and savanna that occur off the riverine floodplain) are distinct in some important ways from those on Amazonian floodplains (várzea). Yet the overall similarities, apparent as first impressions, are indeed striking. Charles Darwin (1906) wrote of his initial experience in tropical rain forest: When quietly walking along the shady pathways, and admiring each successive view, I wished to find language to express my ideas. Epithet after epithet was found too weak to convey to those who have not visited the intertropical regions the sensation of delight which the mind experiences. Imagine we are standing at the edge of a Neotropical rain forest. It’s just after dawn; the hot sun has not yet risen high, and the air is sufficiently humid that the dampness makes it seem almost cool. Rain clouds are

already gathering, but it’s not yet raining. There is a well-marked trail leading us into the forest. It rained during the night, and the trail is muddy and slippery. There is much to take in. It seems strangely quiet, though a few bird and insect calls, especially those of cicadas, periodically break the serenity. Eyeglasses fog because the humidity is so high. The sky is pale, not blue, and the brightness makes it difficult to discern color on the large toucan that sits partially exposed on a protruding bare limb high in the forest canopy. Fallen dry leaves rustle, for some sort of animal, perhaps an agouti or a tinamou, is moving through them. But it is the trees, so many trees, to say nothing of the vines and epiphytes, that first grab our attention. How immense the forest seems, and how dark and enclosing. Dense canopy foliage shades the forest interior, especially in the attenuated early-morning light. Even at midday, when the sun is high overhead, only scattered flecks of sunlight dot the interior forest floor. Shade prevents a dense undergrowth from forming, and the forest floor appears fairly open, lacking a thick shrub layer. Plants we’ve seen only as potted houseplants grow here in the wild. There’s a clump of Dieffenbachia directly ahead on the forest floor. Large arum vines, philodendrons such as Monstera, with its huge, sometimes deeply lobed leaves, are climbing up some of the tree trunks. The biggest trees tend to be widely spaced; many have large, flaring buttressed roots, and some have long, extended prop roots. All the trees are broad-leaved. Absent are the needleleaved trees of the temperate zone, the pines, spruces, and hemlocks. Instead, palms abound, especially in the understory, many with whorls of sharp spines around their trunks. Tree boles are impressively straight, rising to considerable height before spreading into crowns, which are hard to clearly discern because so much other vegetation grows among them. Clumps of cacti, occasional orchids, many kinds of ferns, and an abundance of pineapple-like plants called bromeliads adorn the widely spreading branches. It’s frustrating to try to see the delicate flowers of an orchid clump so high above us, but binoculars help. Vines hang seemingly haphazardly, some draping through several nearby trees. Rounded, basketball-size termite nests are easy to spot on the trees, and the dry tunnels made by their colonial inhabitants vaguely suggest brown ski trails running along the tree trunks. On the forest floor we see trails made by the comings and goings of

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troops of leaf-cutter ants, and some individuals are evident, carrying their burdens of clipped leaves to their massive underground colony. North American broad-leaved forests are often layered: there is a nearly uniform canopy, the height to which the tallest trees such as the oaks and maples grow; a subcanopy of understory trees, such as Sassafras and Flowering Dogwood; a shrub layer of viburnums or Mountain Laurel; and a herbaceous layer of ferns and wildflowers. The tropical rain forest, in contrast, is not neatly layered. Trees are far more variable in height, and identifying horizontal strata within the forest is difficult in most cases. Forest structure is complex. Some trees, called emergents, tower above most other trees, making the forest canopy irregular in height. Trees of varying heights, including numerous palms, occur both in the understory and the canopy. Most trees are monotonously green, but a few may be bursting with colorful blossoms, while some may be essentially leafless, revealing the many epiphytes, or air plants, that have attached themselves to their main branches. A thin covering of herbaceous plants shares the heavily shaded forest floor with numerous seedling and sapling trees, ferns, and palms. It is difficult to perceive a simple pattern in the overall structure of a rain forest. Complex indeed.

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Rain Forest Characteristics: A Checklist Now that you have some sense of what to expect as you wander through a tropical rain forest, here is a bullet list of characteristics to note as you make your observations. These will be explained in additional detail below. • Tall trees of many species, some reaching higher than 30 m (98 ft). • Species identification is in many cases quite difficult without expert help because so many trees look generally the same and leaf shape is very similar among many species. • Deep shade with scattered sun flecks at ground level. This is because the tall canopy of leaves is generally quite good at absorbing sunlight. • Scattered emergent (unusually tall) trees reaching well above most of the tree canopy. This characteristic gives the forest an uneven canopy. Though emergent

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trees also may be seen in many temperate forests, they are usually much more apparent in tropical forests. No clearly delineated understory, shrub layer, or herb layer. Many tree species of various sizes typically compose the understory and mid-elevation levels. Palms often dominate in the understory, and palms may reach canopy height and persist for long time periods. Forest gaps, openings due to such events as tree fall, ranging from single tree falls to moderate-size blowdowns, are common. Gaps are flooded with sunlight, and rapidly growing sun-dependent plant species are common; large gaps become junglelike. Gaps add a major component of horizontal patchiness to forests, accounting for the shifting mosaic pattern typical of rain forests. (The term shifting mosaic refers to patches of forest that change with time, the result of accumulated disturbances in various areas of forest.) Many tree species tend to rise nearly to canopy height before widely branching; thus the pattern is often umbrella-like, the branches appearing to radiate as spokes from the trunk. Trees most commonly have animal-pollinated flowers, many of which are colorful, though some tree species are wind-pollinated and have nondescript flowers. Some flowering and fruiting is evident in any month. You should see some trees and shrubs bearing fruit at pretty much any time of year, though patterns of flowering and fruiting are affected by rainfall amount. Leaves tend to be thick and waxy. They are usually oval, with little or no lobing but with pointed drip tips, sharp points at the apex that permit water to drain easily from the leaf. Compound leaves are common in many species, such as those within the legume family (Fabaceae). Large leaves are common. Most trees are broad-leaved evergreens, but some deciduous tree species occur. Within rain forest, deciduous leaf drop (confined to isolated trees of certain species) is often correlated with flowering and fruiting. Bursts of colorful flowers will be evident on bare branches. Within moist forest, where dry season is pronounced, deciduous leaf drop is associated with water stress. Trees often display buttressed roots; some have prop (or stilt) roots, and many exhibit surface roots that radiate across the forest floor. A buttress is a flaring

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of the root from aboveground. Prop roots are root clusters that emerge from the trunk well above ground. Surface roots, as the name implies, wind conspicuously over the surface of the forest floor. Bark is variable among tree species. It may be light or dark, smooth or ridged, depending upon species. There is no generalized pattern for bark color or texture. Many epiphytic plants grow on branches and bark, often densely, including various lichens, orchids, ferns, and others. Other plants, many vine-like, of many kinds (stranglers, lianas) are common and often abundant. The litter layer is often thin, as leaf decomposition rates are high. Soil is usually reddish but may be of some other color and is typically acidic, often high in clay content. There is much variability in soil characteristics. Some tropical soils are sandy, and some are rich in nutrients, but many are thin and poor in nutrient content. In general, floodplain soils are rich in nutrients, and upland soils are nutrient-poor.

Identifying Neotropical Plants (or Not) The plants of the Neotropics are not well catalogued, the way birds, butterflies, and mammals are. Because of the remarkable profusion of Neotropical plants, there are no real species-by-species field guides with which to match up a plant with a species name. The vast majority of students of Neotropical biology will not find it possible to accurately identify most plants they see to the level of species. There are just too many look-alike species, and the ranges of many species are not precisely known. Thus species identification must be left to taxonomic experts. With the help of identification guides it is possible to identify many Neotropical plants to the level of family, and many of those to the level of genus. Using combinations of characteristics such as leaf shape (palmate, pinnate), compound vs. simple leaves, opposite vs. alternate leaves, presence or absence of tendrils, presence or absence of spines, smooth or serrate leaf edges, fruit and/or flower characteristics, and even, in many cases, odor and taste, you can master the flora at least to the level of family. Hopefully, there will be more identification guides published on the plants of various Neotropical regions.

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Typical Tropical Trees Though there are more individual tree species in the tropics than anywhere else (something about which we will have much more to say), many trees are sufficiently similar in appearance that we can meaningfully describe a “typical” tropical tree. The world’s tropical forests have converged in many of the basic structural characteristics. First and foremost, tropical trees are broad-leaved and most remain in leaf throughout the year.

Stature Tropical rain forests are known for having huge trees. Old engravings depict trees of stunning size with up to a dozen people holding hands around the circumference of the trunk. These giants still exist in some uncut forests, but in most places you are apt to visit, the trees, though large and surely impressive, are not as huge because of past disturbances to the forest. Tropical tree branches do not radiate from the trunk until almost canopy level, thus enhancing the appearance of height (plate 3-3). The tallest tropical trees are found in lowland rain forests, and these range from 25 to 45 m (approx. 80–150 ft) in height; the majority are about 25–30 m (80–100 ft) tall. Tropical trees occasionally exceed heights of 45 m (150 ft), and some emergents do top 60 m (200 ft) and may occasionally approach 90 m (300 ft), though such heights are uncommon. Some temperate-zone forests have equally tall or

Plate 3-3. Typical tropical trees are tall and straight, with major branches emerging near canopy level and making the tree shape somewhat like that of an umbrella (which you often need in rain forest). Photo by John Kricher.

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taller trees. In the United States, Sierra Nevada Giant Sequoia groves, coastal California Redwood groves, and Pacific Northwest old-growth forests of Sitka Spruce, Douglas-fir, Western Redcedar, and Western Hemlock all routinely exceed the height of the majority of tropical forest trees. So do the temperate bluegum (Eucalyptus) forests in southeastern Australia. Neither the tallest, the broadest, nor the oldest trees on Earth occur in rain forest: the tallest is a California Redwood, at 115.85 m (380.08 ft); the broadest is a Montezuma Cypress in subtropical Mexico, with a circumference of about 36 m (118 ft); and the oldest is a Great Basin Bristlecone Pine in the White Mountains of eastern California, about 4,600 years old. Tropical trees the world over exhibit a distinctive parasol shape, alluded to earlier, and this distinctive morphology is most clearly evident when you observe emergent trees from open areas, as when you traverse a river (plate 3-4). Take a moment and look up into the canopy, observing the spreading, flattened crown. See how the branches radiate out from one or a few points, resembling the spokes of an umbrella. Each of these main radiating branches contributes to the overall symmetry of the crown, in an architectural pattern called sympodial construction. The effect of crowding by neighboring trees can significantly modify crown shape. Single trees left standing after adjacent trees have been felled often have irregularly shaped crowns, a result of earlier competition for light with neighboring trees. Trees in the understory tend to be lollipop-shaped. Because they have not yet reached the canopy, their crowns are composed of lateral branches emerging from a single main trunk. Lower branches will eventually drop off through self-shading as the tree grows and becomes a sympodial canopy tree. Trees growing in forest gaps, where sunlight is abundant (see “The Understory and Forest Gaps,” below; and chapter 7), are densely multilayered with leaves, an adaptation to intercept abundant sunlight.

Plate 3-4. The spreading sympodial crown of this riverside tree shows the radiating branching pattern and overall parasol shape characteristic of many tropical tree species. Photo by John Kricher.

Plate 3-5. Buttressed roots are common throughout the world’s tropical forests. They occur as growth patterns in numerous tree species. Photo by John Kricher.

Buttresses, Prop Roots, and Surface Roots Many rain forest tree species are buttressed. Indeed, buttresses are iconic features of trees of tropical forests the world over. A buttress is a root flaring out from the trunk aboveground to form a flange-like base (plate 35). Because so many trees have buttressed roots, this characteristic gives a tropical forest a distinctive look in comparison with temperate forests. Buttresses radiate

Plate 3-6. Buttressed and spreading surface roots are evident in many trees that inhabit riverine areas in the tropics. Photo by John Kricher.

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from above the base of a tree, surrounding the bole, sometimes making cozy retreats for snakes and other denizens of the forest. Buttresses can be impressively large, often radiating from the bole 1.8 m (6 ft) or more from the ground. Buttressing is particularly common among trees of streamsides and riverbanks, as well as among trees lacking a deep taproot (plate 3-6). Many plant ecologists believe that buttressing acts principally to support major roots just below and often on the surface of the soil. Roots generally are shallower in tropical forests than they are in temperate forests. Some tropical trees lack buttresses but have stilt or prop roots, which radiate from the tree’s base, remaining aboveground (plate 3-7). Stilt roots are particularly common in areas such as floodplains and mangrove forests that become periodically inundated with water. Other tropical trees, including the huge Brazil Nut (Bertholletia excelsa), lack buttresses or prop roots, and some of these have relatively deep taproots. Finally, you will note that many tropical trees exhibit surface roots (plates 3-8–9). It is rather easy to trip on these roots as they wind across trails. The function of surface roots is related to the rapidity of mineral recycling in the tropics and will be discussed further in chapter 6.

Many Patterns of Bark It was once thought that tropical trees tend to have light-colored bark, but in reality there is no generalized pattern associated with bark of tropical trees. Bark may be smooth or rough and light or dark, ranging from almost white in some cases to almost ebony in

Plate 3-8. Thick surface roots characterize many tropical rain forests. Note the thin litter layer, also a characteristic of tropical forests, where decomposition rates are high. Photo by John Kricher.

Plate 3-7. Stilt or prop roots are common in many tree species along riverine, floodplain, and swampy areas. Photo by John Kricher.

Plate 3-9. Surface roots extend from buttresses across the floor of the forest. Photo by John Kricher.

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others (plates 3-10–15). Bark is often splotchy, with pale and dark patches. And many tropical trees have bark adorned with lichens and various kinds of small plants (called epiphylls, discussed below). Tropical tree bark may be thin and peeling, but on some trees it can be thick and deeply ridged (and the wood inside may be very hard—remember that wood-eating termites abound in the tropics). There is much variability. Bark is therefore not usually a good means of identifying a tree, as many different species may have similar-appearing bark. Some trees, however, such as the Chicle (Manilkara zapota) of Central America, have distinctive bark. Chicle bark is black and vertically ridged into narrow strips, with the inner bark red, and yields white resin (the original source of the latex base from which chewing gum was manufactured).

Cauliflory

Plates 3-10–3-15.These six examples demonstrate the variability in bark characteristics evident in tropical forests. The photos were taken within a stretch of about 50 m (165 ft) along a floodplain forest trail in southern Brazil. Photos by John Kricher.

Plate 3-16. The ripe cauliflorous fruits of the Cacao tree. Photo by Scott Shumway.

Many tropical trees exhibit a characteristic called cauliflory, in which the flowers and subsequent fruits abruptly grow from the trunk, rather than from the canopy branches. Cauliflory generally does not occur outside of the tropics. Cacao (Theobroma cacao; plate 316), from which chocolate is produced, is a cauliflorous understory tree. Some trees may be cauliflorous due to the large size and heaviness of the fruits they produce, the weight of which could not be supported on thin outer branches (though it is equally arguable that the opposite may be the case—the fruits may have grown large and heavy because they grow from the trunk, not the outer branches). The presence of cauliflorous

Plate 3-17. These flower clusters are cauliflorous, growing directly from the branch rather than the branch tip. Photo by John Kricher.

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flowers (plate 3-17) may facilitate pollination by animals such as bats. Equally likely, cauliflorous fruiting may facilitate dispersal of seeds from fruit consumption by large, terrestrial animals that could not reach canopy fruits.

Leaf Characteristics

Plate 3-18. The huge leaves on these plants growing in a sunny gap in Ecuador are sufficiently large that they can be used as umbrellas if it begins to rain. Photo by John Kricher.

Plate 3-19. This selection of leaves from tropical trees illustrates many of the basic leaf characteristics: drip tips, waxy appearance, lack of complex lobing. Two of the six are compound leaves. Photo by John Kricher.

One feature of the Neotropics that you cannot miss is leaves; from large to small, they are everywhere (plate 3-18). Leaves of tropical tree species are surprisingly similar in shape, which makes species identification difficult (plate 3-19). The distinctive lobing patterns of many North American maples and oaks are missing from most tropical trees. Instead, leaves are characteristically oval, unlobed, and often possess sharply pointed ends, called drip tips, that help facilitate rapid runoff of rainwater (plate 3-20). Leaves of most species have smooth rather than toothed margins, though serrate leaves are found in some species. Both lowland and montane tropical forest trees produce thick, leathery, and waxy leaves that can remain on the tree for well over a year. Many tropical species produce palmate compound leaves, in which the leaflets radiate like spokes from a center, forming a shape similar to that of a parasol. Some leaves, particularly those on plants that are found in disturbed areas such as gaps, are conspicuous for their large size, well in excess of the leaves of any temperate-zone species. Though many trees have simple leaves, compound leaves are common, particularly due to the abundance of legumes, a highly species-rich plant family.

Plate 3-20. This understory plant clearly shows drip tips. Note that the leaves hang down, facilitating the flow of water from the plant during heavy rain. Photo by John Kricher.

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Plate 3-21. Plate 3-22. Plates 3-21 and 3-22. Many flowers, such as some species of passionflowers (Passiflora, 3-21) and Pachystachys (3-22), are brilliant red, an adaptation that attracts insects and birds to cross-pollinate the plant. The tubular flowers of Pachystachys plants are ideal for hummingbirds. Photos by John Kricher.

Flowers Many tropical plants have colorful, fragrant blossoms, often large ones. Typical examples of Neotropical flowering plants include coral trees (Erythrina spp.), Pink Poui (Tabebuia pentaphylla), Cannonball Tree (Couroupita guianensis), frangipani (Plumeria spp.), Morning-glory Tree (Ipomoea arborescens), passionflowers (Passiflora spp.), and Pachystachys species (plates 3-21–23). But note that many striking trees that are abundantly represented in the Neotropics are actually imported from other tropical regions. For instance, the gorgeous and widespread Flamboyant Tree (Delonix regia), the national tree of Puerto Rico, is actually native to Madagascar. The Common Bottlebrush (Melaleuca citrina) is from Australia, and the Norfolk Island Pine (Araucaria heterophylla) is from Norfolk Island in the southern Pacific Ocean. Some trees that are widely distributed in the Neotropics, such as the many species of Jacaranda, with their sprays of lavender blossoms, are originally from more restricted locations. Jacaranda mimosifolia comes from northwestern Argentina and is now cultivated throughout the tropical world. The flowers of bird-pollinated plants, such as Heliconia, are very often red, orange, and yellow, while lavender flowers, such as those of Jacaranda mimosifolia, are more commonly insect-pollinated. Some trees, such as Silkcotton or Kapok Tree (Ceiba pentandra), flower mostly at night, producing conspicuous white flowers that, depending on species, attract bats or moths. Fragrant flowers are pollinated mostly by moths, bees, beetles, and other insects. Bat-pollinated flowers smell musty,

Plate 3-23. This is the large and colorful blossom of the Cannonball Tree. It is cauliflorous, growing directly from the tree trunk. Photo by Dennis Paulson.

their odor possibly an attractant to their pollinators. Because of the high incidence of animal pollination, especially by large animals such as birds, bats, and large lepidopterans (members of the butterfly and moth order, Lepidoptera), flowers tend not only to be large but also to be nectar-rich and borne on long stalks or branches away from leaves, or else on the trunk (see “Cauliflory,” above). Many flowers are tubular or brush-like in shape, though some, particularly those pollinated by small insects, are shaped as flattened bowls or plates. The vivid colors and shapes of many flowers reflect the prevalence of animal pollination, an important characteristic of the ecology of all tropical forests (plates 3-24–27). Wind pollination is proportionally more

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Plate 3-24. Some trees, such as the Cochlospermum pictured, lose their leaves before they set flowers, an adaptation that helps advertise the bright yellow blossoms to potential pollinators. Photo by John Kricher.

Plate 3-25. The bright red bracts of the well-known and widely distributed Lobster Claw Heliconia (Heliconia rostrata) enclose the small greenish-yellow flowers within the bracts. Hummingbirds called hermits are attracted to and crosspollinate heliconia plants. Photo by John Kricher.

Plate 3-26. The Pale-bellied Hermit (Phaethornis anthophilus) is attracted to the colorful bracts of various Heliconia species. Photo by John Kricher.

Plate 3-27. A close look at a heliconia shows the nondescript flowers “advertised” by the colorful bracts. Photo by Dennis Paulson.

common in temperate forests, though wind pollination occurs in some species of tropical canopy trees.

of the element selenium, perhaps serving to protect the tree from seed predators (animals that destroy rather than disperse the seed when consuming it). The Milk Tree (Brosimum utile) forms succulent, sweet-tasting edible fruits, each with a single large seed inside. Named for its white sap (which is drinkable), the Milk Tree may have been planted extensively at places like Tikal by Maya of the Classic Period (see chapters 7 and 17). The famous Brazil nut comes from the forest giant Bertholletia excelsa. The nuts are contained in large, woody rounded pods that break open upon dropping to the forest floor. Most tree species in the huge legume family package seeds in long, flattened pods, and the seeds tend to contain toxic amino acids (plate 3-32). Among the

Fruits and Seeds Many tropical trees produce small to medium-size fruits, but some produce large, conspicuous fruits, and the seeds contained within are large as well (plates 328–31). Many palms—the Coconut (Cocos nucifera), for example—produce large, hard fruits in which the seeds are encased. The Monkey Pot Tree (Lecythis ampla) produces thick cannonball-like fruits, 20 cm (8 in) in diameter, each containing up to 50 elongate, 5 cm (2 in) seeds. The seeds are reported to contain toxic quantities

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Plates 3-28 and 3-29. These two photos show examples of fruits that depend on animals to disperse their seeds. The bright colors of the fruits advertise them to potential seed dispersers. Photos by John Kricher.

Plates 3-30 and 3-31. This large, 18 cm (7 in) long seedpod is not from a tree but from a woody vine, or liana, of the Bignoniaceae family. Plate 3-30 shows the closed pod, 3-31 the seeds contained within the pod. Photos by John Kricher.

legumes, the Stinking Toe Tree (Hymenaea courbaril) produces 12.5 cm (5 in) oval pods with five large seeds inside. The pods drop whole to the forest floor and often provide food for agoutis and other forest mammals as well as various weevils. Fruit “advertises” itself to potential seed dispersers. The equitable tropical climate allows for some fruiting to occur every month of the year, at least in moist forests. Much more will be said of the relationships between fruits and their seed dispersers in chapter 10. What follows here is a sampler. The wide variety of fruit types is indicative of extensive consumption by animals and subsequent dispersal of seeds. But fruit consumers do not always disperse seeds and in fact often consume them. Among the mammals, monkeys, bats, various rodents, peccaries, and tapirs are common consumers of fruits and seeds, oftentimes dispersing the seeds, sometimes destroying them.

Agoutis, which are rodents, skillfully use their sharp incisors to gnaw away the tough, protective seed coat on the Brazil nut, thus enabling the animal to eat the seed contained within. Some extinct mammals, such as the giant ground sloths and elephantine gomphotheres, may have been important in dispersing large seeds of various tropical plants. Birds such as tinamous, guans, curassows, doves and pigeons, trogons, toucans, and parrots are also attracted to large fruits and the seeds within them. Along flooded forests, some fish species are important fruit consumers and seed dispersers. Animals consume small fruits and seeds as readily as larger ones. Insects especially are frequent predators of small seeds. Some trees have wind-dispersed seeds, and thus the fruits are usually not consumed by animals. The seeds of Ceiba pentandra are dispersed by parachutelike, silky fibers called kapok, which give the tree both of its common names, Kapok and Silk-cotton Tree.

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Plate 3-32. Swirls of pods have formed on this legume. Photo by John Kricher.

Mahogany trees (Swietenia macrophylla and S. humilis), famous for their superb quality wood, develop 15 cm (6 in) oval, woody fruits, each containing about 40 seeds. The seeds are wind-dispersed and would be vulnerable to predation were it not for the fact that they have an extremely pungent, irritating taste.

Palms Palms occur worldwide and are among the most distinctive of tropical plants, frequenting interior forests, disturbed areas, and grassy savannas. They are particularly abundant as components of swamp and riverine forest. All palms are members of the family Arecaceae, formerly known as Palmae, and all are monocots, sharing characteristics of such plants as grasses, arums, lilies, and orchids. The most obvious monocot feature of palms is the parallel veins evident in the large leaves, which themselves are referred to as fronds (plate 3-33). There are approximately 2,500 palm species in the world and about 550 in the Americas. Alfred Russel Wallace made a detailed study of South American palms and published an important book on the subject. Palms are widely used by indigenous peoples of Amazonia for a diversity of purposes: thatch for houses, wood to support dwellings, various ropes, strings, weavings, hunting bows, fishing line, hooks, utensils, musical instruments, and various kinds of food and drink. Indeed, many palm species have multiple uses and are thus among the most important species for humans. Palms are often abundant in the forest understory and are frequently armed with sharp spines along the

Plate 3-33. Palms abound in tropical forests, especially along rivers but also in the forest interior. Large parrot species such as macaws devour palm fruits. Photo by John Kricher.

Plate 3-34. Beware of inadvertently grabbing onto the trunk of understory palms such as this one. The spines are very sharp. Photo by John Kricher.

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trunks and leaves (plate 3-34). Be especially careful not to grab a palm sapling, as the spines can introduce bacteria as they create a wound.

Vines, Climbers, Stranglers, Epiphytes While trees dominate tropical moist forests, there are numerous other plant growth forms that add a great deal to the biodiversity and structural complexity of the ecosystem. Vines abound in many tropical forests, as do air plants or epiphytes.

Vines and Lianas Vines occur in many plant families and exhibit a variety of growth forms. They are a conspicuous and important

component of most tropical rain forests, though vine density is variable from site to site (plate 3-35). Of course, vines of many species also occur in forests throughout much of the temperate zone, but their more prodigious representation in tropical forests is noteworthy. Because of their abundance, vines form a distinct and important structural feature within tropical rain forests. They exhibit high biomass in some rain forests, and compete with trees for light, water, and nutrients. Many provide essential foods for various animals. Woody vines, called lianas, entwine elaborately as they hang from tree crowns, actually interconnecting trees. Others, the bole climbers, attach tightly to the tree trunk and ascend. Tropical vines occur abundantly in disturbed sunlit areas as well as in forest interiors and occur at varying densities on virtually all soil types. Humans make extensive use of vine plants for foods, medicines, hallucinogens, poisons, and construction materials.

Plate 3-35. Extensive vine growth draping throughout vegetation in an Ecuadorian rain forest. Vines are particularly evident in areas rich in light, such as the large gap shown here. Photo by John Kricher.

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Lianas A liana is a woody vine rooted in the ground that typically gets its start when a forest opening or gap is created, permitting light penetration. Lianas begin as shrubs but eventually become vines, retaining their woody stems. Lianas are not restricted to the tropics. There are many woody vines in the temperate zone, such as the familiar Poison Ivy (Toxicodendron radicans). But lianas are sufficiently abundant throughout many tropical rain forests that they represent a distinct characteristic of these ecosystems. Tendrils from the liana branches entwine neighboring trees as they climb upward, reaching the tree crown as both tree and liana grow. Lianas spread in the crown, and a single liana may eventually loop through several tree crowns. Lianas seem to drape limply, winding through tree crowns or hanging as loose ropes parallel to the main bole. Their stems remain rooted in the ground, often at multiple points, and are oddly shaped, often being flattened, lobed, coiled like a rope, or spiraling in a helix (plates 3-36–38). The thinnest have remarkable springiness and will often support a person’s weight, at least for a short time. Lianas have exceptionally long vessels within their stems, and when a section of a liana is severed water runs out. Liana is a growth form, not a family of plants, and thus lianas are represented among many different plant families (e.g., Fabaceae, Sapindaceae, Cucurbitaceae, Bignoniaceae, Vitaceae, Smilacaceae, and Polygonaceae, to name but a few). Lianas, like tropical trees, can be difficult to identify, but some lianas can be identified to the level of genus by noting the distinctive crosssectional shapes of their stems. In a classic study of liana abundance by Francis Putz in Panama, a single hectare (10,000 m2, or about 2.5 ac) hosted 1,597 climbing lianas, distributed among 43% of the canopy trees. In the understory, 22% of the upright plants were lianas, and lianas were particularly common in forest gaps. A heavy liana burden reduced the survival rate of trees, making them more likely to be toppled by winds. Fallen lianas merely grew back into other trees. When tree falls bring lianas to the ground, the vines may be sufficiently dense so as to reduce the speed with which trees reattain canopy status.

Hemiepiphytes Hemiepiphytes are among the most important and unusual of plant growth forms in the tropics. Primary

Plate 3-36. This helix-shaped liana stem is typical of many types of lianas, woody vines that are abundant in many tropical forests. Photo by Scott Shumway.

Plate 3-37. Lianas weave conspicuously through many tropical forests. Photo by John Kricher.

Plate 3-38. Lianas begin as seeds in the ground and grow toward trees, which they can eventually entwine as they grow upward to canopy level. Photo by John Kricher.

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Plate 3-39. Strangler fig anastomosing, or forming a connected network, as its tendrils and branches surround a tree trunk. Stranglers are hemiepiphytes, and typically grow down a host tree to eventually reach the ground. Photo by John Kricher.

Plate 3-40. Numerous strangler figs have engulfed their host tree, which is all but invisible here. Photo by John Kricher.

hemiepiphytes begin their life cycles as epiphytes but eventually become rooted in the ground. Perhaps the best-known group of primary hemiepiphytes is the stranglers (Ficus spp.), members of the fig family (Moraceae). There are approximately 750 species of Ficus (figs) throughout the global tropics. Stranglers germinate in the tree crown from seeds dropped by a bird or mammal. The seedling’s tendrils grow toward the tree bole and then grow downward around the bole anastomosing, or fusing together like a crude mesh (plate 3-39). The strangler eventually reaches the ground and establishes its own root system (plate 3-40). The host tree often dies and decomposes, leaving the strangler standing alone. The mortality of the host tree results from being girdled by the strangler, which prevents the host’s bole from expanding. Stranglers also may shade the tree on which they grow, reducing its ability to photosynthesize. A mature strangler, its host tree having died and decomposed, is a common sight in tropical forests (plate 3-41). The strangler’s trunk is a dense fusion of what were once separate vines, now making a single, strong woody labyrinth that successfully supports a wide canopy, itself now laden with vines.

Plate 3-41. Strangler figs, such as this Ficus tree from Panama (with the author standing at its base), become towering canopy trees in many tropical lowland forests. Photo by Diana Churchill.

Secondary hemiepiphytes begin as rooted plants and eventually become epiphytic climbers. In humid tropical forests it is common to see boles partially enshrouded by the wide, thick leaves of climbers (plate 3-42). The well-known ornamental arum Monstera deliciosa is a philodendron that begins life on the ground. Seeds germinate and send out a tendril toward shade cast by a nearby tree. The tendril soon grows up the tree trunk, attaching by aerial roots, and the vine thus moves from the forest floor to become anchored on a tree (plate 3-43). As it grows the plant ceases to be rooted in the ground at all, and its entire root system is invested on the tree bark. It continues to grow ever upward on its host tree, often encircling the bole as it proliferates.

Epiphytes Epiphytes are commonly called air plants. As the prefix epi- implies, these plants live on other plants. They are not internally parasitic, but they do claim space on a branch where they set out roots, trap soil and dust particles, and photosynthesize as canopy residents. Rain forests, both in the temperate zone (such as the rain forests of

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Plate 3-44. Epiphytes, or air plants, of various sorts often coat trunks and branches in tropical forests. Photo by Beatrix Boscardin

Plate 3-42. Climbers often adhere tightly to the bark of the host tree, as shown in this photo, taken in Panama. Photo by John Kricher.

Plate 3-43. A large-leaved philodendron (Monstera sp.) grows on the trunk of this tree in Guatemala. Photo by John Kricher.

Washington’s Olympic Peninsula and of coastal Oregon) and throughout the tropics, abound with epiphytes of many different kinds. Cloud forests also host an abundance of air plants. In a lowland tropical rain forest nearly one-quarter of the plant species are likely to be epiphytes, though the representation of epiphytes varies substantially among forests. As forests become drier, epiphytes decline in both abundance and diversity. Many different kinds of plants grow epiphytically. In Central and South America alone there are about 15,500 epiphyte species. Looking at a single tropical tree can reveal an amazing diversity. Lichens, liverworts, and mosses, many of them tiny, grow on trunk and branches and often on leaves (plate 3-44). Cacti, ferns, and colorful orchids line branches. Bromeliads, with distinctive sharply pointed daggerlike leaves, are abundant and conspicuous on both trunk and branch alike. Epiphytes attach firmly to a branch and survive by trapping soil particles blown to the canopy and using the captured soil as a source of nutrients such as phosphorus, calcium, and potassium. As epiphytes develop root systems, they accumulate organic matter, and thus a soil and organic litter base, termed an epiphyte mat, builds

Plate 3-45. This deciduous tree in Belize looks fuzzy due to the dense epiphytic growth covering the major branches. Photo by John Kricher.

up on the tree branch, adding weight (plate 3-45). Just as most terrestrial plants, most epiphytes have root systems containing fungi called mycorrhizae (chapter 6), which greatly aid in the uptake of scarce minerals. (Mycorrhizae are also of major importance to many trees, especially in areas with poor soil.) Epiphytes efficiently take up water and thrive in areas of dense cloud cover and heavy mist. Though epiphytes are not parasitic in the strictest sense, they may indirectly harm their host trees through competition for light, water, and minerals. Epiphytes get “first crack” at the water dripping down through the canopy. However, some temperate and tropical canopy trees develop aerial roots that grow into the soil mat accumulated by the epiphytes, tapping into that source of nutrients and water. In such cases the host tree benefits from the epiphytes’ presence by obtaining nutrients from its own canopy. The accumulating weight of epiphytes, however, may become sufficient to cause limbs to break off, damaging the tree. Bromeliads (family Bromeliaceae) are abundant in many Neotropical forests. The most well known bromeliad is the pineapple. Approximately 3,000 bromeliad species, distributed among 56 genera, are known. Leaves of many

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Plate 3-46. The sharply spiked leaves of bromeliads make the growth form easy to recognize. Photo by John Kricher.

Plate 3-47. Bromeliad flowers grow on a central spike and are usually bright red, attracting many kinds of hummingbirds. Photo by John Kricher.

Plate 3-48. Euphonias, such as this White-vented Euphonia (Euphonia minuta), are frequent nesters in bromeliad clusters. They feed on various berries, particularly mistletoe, which is the only true parasitic epiphyte, growing into the plant upon which it attaches and claiming nutrients from the plant. Euphonias are important seed dispersers for mistletoes. Photo by John Kricher.

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Plate 3-49. Pineapple crop. Photo by John Kricher.

Plate 3-50. Harvested pineapples. Photo by John Kricher.

The Tasty Pineapple Pineapple (Ananas comosus) is a terrestrial bromeliad originally from Brazil and Paraguay. It was widely cultivated by indigenous peoples before Columbus and the Spanish arrived in the New World, and thus it spread north into Central America. After its discovery by Europeans it was soon cultivated in various other parts of the tropical world. The spiky, sharply spined leaves protect the plant, whose single flower cluster grows in the center of the leaf rosette. Wild pineapples have flowers ranging in color from purple to red and are normally pollinated by various hummingbird species. Domestic pineapples must be artificially propagated, though some pollination by insects can occur. Most farming families throughout the tropics have a few pineapples as part of their “dessert” crops. In addition, pineapples are now grown commercially in numerous tropical countries throughout the world and have become one of the region’s leading export crops (plates 3-49–50).

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species are arranged in an overlapping rosette, forming a cistern that holds water and detrital material; the flower grows from the rosette’s center (plates 3-46–47). Some species have a dense covering of hairlike filaments, called trichomes, on the leaves that help rapidly absorb water and minerals. Though most bromeliads are epiphytic, there are many areas where terrestrial bromeliads make up a significant portion of the ground vegetation. Epiphytic bromeliads provide a source of moisture for many canopy dwellers. Tree frogs, mosquitoes, flatworms, snails, salamanders, and even crabs complete their life cycles in the tiny aquatic habitats provided by the cuplike interiors of bromeliads. Some species of small colorful birds called euphonias (Euphonia spp.; plate 3-48) use bromeliads as nest sites. Orchids are a global family (Orchidaceae) abundantly represented among Neotropical epiphytes. There are estimated to be approximately 25,000 to 35,000 orchid species worldwide. In Costa Rica, approximately 88% of the orchid species are epiphytes, while the rest are terrestrial. Many orchids grow as vines, and many have bulbous stems (called pseudobulbs) that store water. Indeed, the name orchid comes from the Greek word meaning “testicle,” a reference to the appearance of the bulbs. Some orchids have succulent leaves filled with spongy tissue and covered by a waxy cuticle to reduce evaporative water loss. Like virtually all other plants, all orchids depend on mycorrhizal fungi during some phase of their life cycles. These fungi grow partly within the orchid root and facilitate uptake of water and minerals. The fungi survive by ingesting some of the sugary products the orchid generates by photosynthesis. Thus, the association between orchid and fungus is mutualistic: both species benefit (chapter 10).

Plate 3-51. Flowering orchids are a highlight of the Neotropical epiphyte community. Photo by Beatrix Boscardin.

Plate 3-52. This beautiful flower is an orchid of the genus Sobralia. In Spanish it is called flor de un día, because the flower lasts for only a single day. Photo by Scott Shumway.

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A close look at some orchids will reveal two types of roots: those growing on the substrate and those that form a “basket,” up and away from the plant. Basket roots aid in trapping leaf litter and other organic material that, when decomposed, can be used as a mineral source by the plant. Orchid flowers are among the most beautiful in the plant world (plates 3-51–52). Some, like the familiar Cattleya, are large, while others are delicate and tiny. Binoculars help the would-be orchid observer in the rain forest. Orchids are cross-pollinated by insects; certain orchids can be pollinated only by specific insects. Bees are primary pollinators of Neotropical orchids. These include long-distance fliers, like the euglossine bees, which cross-pollinate orchids separated by substantial distances. Some orchid blossoms apparently mimic insects, facilitating visitation by insects intending (mistakenly) to copulate with the blossom—something that Charles Darwin discovered. Many orchids have value as ornamentals. Of particular significance to humans is the orchid genus Vanilla, which contains 90 species, two of which are of economic importance, their use dating back to the Aztec.

Plate 3-53. Epiphylls of various kinds adorn this large leaf in the forest understory. Photo by Scott Shumway.

Epiphylls In many tropical moist forests, even leaves have epiphytes. Tropical leaves often are colonized by tiny lichens, mosses, and liverworts, which grow only after the leaf has been colonized by a diverse community of microbes: bacteria, fungi, algae, and various yeasts, as well as microbial animals such as slime molds, amoebas, and ciliates (plate 3-53). This tiny assemblage that lives upon leaves is termed the epiphyll community. Its existence adds yet another dimension to the vast species richness of tropical moist forests.

Plate 3-54. Light areas called sun flecks penetrate the otherwise dark interior of a closed-canopy rain forest. Photo by John Kricher.

The Understory and Forest Gaps Much of the understory of a closed tropical forest is deprived of light (plate 3-54). Low light intensity is a characteristic feature of rain forest interior and is an important potential limiting factor for plant growth. This is the reason it is fairly easy to traverse your way through a closed-canopy rain forest. Many of the seedlings and shoots that surround you are those of trees that may or may not eventually attain full canopy status; a small, unpretentious-looking sapling could be well over 20 years old.

Plate 3-55. Forest gaps allow much light, stimulating rapid growth. Photo by John Kricher.

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Certain families of shrubs frequently dominate rain forest understory. These include members of the families Melastomataceae (e.g., Miconia), Rubiaceae (e.g., Psychotria), and Piperaceae (e.g., Piper). In addition, there are often forest interior heliconias (Heliconiaceae) and terrestrial bromeliads. Many ferns and fern allies, including the ancient genus Selaginella, can carpet the forest herb layer. The forest understory is often far from uniform. The deep shade is interrupted by areas of greater light intensity and denser plant growth. The careful observer inevitably notices the presence of many forest gaps of varying sizes, openings created by fallen trees or parts thereof (plate 3-55). Gaps permit greater amounts of light to reach the forest interior, providing enhanced growing conditions for many species (plate 3-56). Though understory plants and juvenile trees are adapted to grow slowly, many plants are adapted to respond with quickened growth in the presence of a newly created gap. Recent research at La Selva Biological Station in Costa Rica has revealed a surprisingly high disturbance frequency caused by tree falls and branch falls. Estimates are that

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the average square meter (about 11 ft2) of forest floor lies within a gap every 100 years or so. As described by Deborah Clark (1994): The primary forest at La Selva is a scene of constant change. Trees and large branches are falling to the ground, opening up new gaps and smashing smaller plants in the process. Smaller branches, bromeliads, and other epiphytes, 6 m–long palm fronds, smaller leaves, and fruits fall constantly as well. The lifetime risk of suffering physical damage is, therefore, high for plants at La Selva.

Summing Up (for Now) Plant growth, density, and diversity dominate the senses when one is within a tropical rain forest. The structure of these ecosystems, as we have seen, is complex, but it is also changing, to some degree by the day. Tropical rain forests are dynamic, a point that will become much clearer in chapter 7.

Plate 3-56. Dense, tangled plant growth characterizes gap openings. Photo by John Kricher.

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Chapter 4 Finding Animals in Rain Forest The Challenges of Finding Wildlife in Rain Forests A rain forest—unlike, say, the open and sweeping African savanna—typically does not provide easy views of its abundant animal life. The very structural complexity of the ecosystem itself (described in chapter 3), forces the naturalist to work harder to see its animal inhabitants (plate 4-1). Trails are often narrow, and traversing them in a group often means that some members, particularly those in the front of the line, get a quick but satisfactory look at the agouti scampering across the trail, while others miss it entirely. Of course, group participation also has many advantages. There are more eyes looking for animals, and often an expert guide to help find them. But the reality remains that the forest is usually sufficiently dense that getting a clear view of a bird or mammal in a tree is often a challenge, as so many branches are in between you and the animal you seek to observe. Many tour leaders are highly skilled not only at finding wildlife but also at showing it to their group.

Wildlife spotting is a learned skill. While it is very rewarding to be in the company of a competent guide, you will also want to develop your own degree of expertise in seeking and seeing animals in the forest. Being alone or with only one or two others makes it more likely that you will come upon an animal and not immediately frighten it away. Groups typically make quite a bit of noise as they move along a forest trail. In searching for rain forest animals you should try to adhere to the following guidelines: • First, move slowly and move quietly. Keep your body motions minimal. • Take a few steps along a trail and then stop and look around, beginning with the understory and working your eyes up to the canopy. Be patient. • Look for movement and listen for sounds. Leaf movement among the foliage suggests a bird or other animal in motion. Listen for the soft crackle of leaves on the forest floor. Secretive birds such as tinamous and wood-quail as well as mammals such as agoutis and coatis are often best located by the sounds they make as they walk.

Plate 4-1. This Hoffmann’s Two-toed Sloth (Choloepus hoffmanni) is obscured by the very branches and leaves that are its arboreal home, food, and habitat. It is a challenge to get unobstructed views of animals inside a rain forest. Photo by John Kricher.

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• Dress in dark, subdued clothing; you don’t need to wear military-type camouflage, but dark clothing is definitely preferable to light. A bright white T-shirt that says “Save the Rain Forest” in Day-Glo pink letters is fine back at the field station or lodge, but it will give away your presence in the forest. • Remain on the trail. This is important for safety reasons. Regarding this last point, suppose you come upon a really good sighting, perhaps a striking Orangecrowned Oriole (Icterus auricapillus; plate 4-2). The oriole is perched in understory just beside the trial. You raise your binoculars and get a quick but good look at it before it flies a short distance into the forest. Now the temptation arises. Do you go off trail to get another, perhaps better look at the bird or perhaps a great photo of it? Remember, there are snakes and many are inconspicuous. Going off trail in a tropical rain forest carries risks, especially if you are unskilled at seeing snakes before they see you. The risk is low but not zero. If you are not wearing snake chaps or high boots be really careful if you go off trail. Bushwhacking is not recommended. But bear in mind that some professional guides who are skilled at keeping an eye out for serpents will on occasion take their group off-trail to see wildlife. I have never felt unsafe in the company of such guides. And then there are the hard realities of the rain forest itself. Consider how many species remain almost entirely in the canopy, far from where you are standing on the forest floor. How can you see them? It takes work, patience, and skill to see rain forest animals well. Many species are cryptic, a result of evolution in a predator-rich environment (plate 4-3; see discussion in chapter 11). Even gaudily colorful birds, such as various tanagers and cotingas, may appear surprisingly dull in the forest shade. To make matters worse, some tropical birds, such as trogons and motmots, tend to sit still for long periods and can easily be overlooked even when close by (plate 4-4). It requires luck and the ability to develop a search image, or mental image of certain species, to find them on a regular basis. In other words, you must become sufficiently familiar with trogons (for example) that they begin to “pop out” at you as you scan likely perches. You will also be presented with light problems when looking up. Skies in rain forest areas are frequently overcast, and the white sky background makes it more

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Plate 4-2. A clear and unobstructed view of an Orangecrowned Oriole. If it flies into the forest, and you go off the trail to chase it, realize you are taking a risk. Photo by John Kricher.

Plate 4-3. Looking up into a tall tree, you may notice a snag that isn’t a snag but a bird. It’s a Great Potoo (Nyctibius grandis), cryptically colored and perched so as to mimic the bare snag and seemingly become part of it. It takes skill to find such well-camouflaged species. Photo by John Kricher.

Plate 4-4. This female Slaty-tailed Trogon (Trogon massena) is perched quietly on a limb and may remain so, virtually unmoving, for many minutes. Thus it can easily be overlooked in the forest shade. Photo by John Kricher.

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of a challenge to make out the colors of birds and other animals. A bird perched atop a tree silhouetted against a white background is a commonplace sight in the tropics (plate 4-5). Getting unobstructed views of animals is a challenge. And not only do branches and leaves obstruct your view, so do shadows. Get used to that. The animals are there, but finding them is a different matter. Monkeys noisily scamper through the canopy, but tree crowns may be so dense that you can catch only a glimpse. You may pass below an iguana sitting idle in a tree without ever seeing it. Most guides will focus on finding vertebrates, particularly birds, since most bird species are diurnal, and they are often relatively easy to observe, particularly when a mixed-species foraging flock suddenly appears and seems to surround you. Another reason for an avian focus is that many, if not most, visitors to Neotropical rain forest sites are primarily seeking birds to add to their life lists. But mammals, snakes, lizards, and anurans (toads, frogs, and tree frogs) can be found with regularity, as can many fascinating insects and other invertebrates (plates 4-6–7). Sounds reveal some of the forest dwellers: there is often a predawn chorus of howler monkeys, the various troops proclaiming their territorial rights to one another, their tentative low grunts soon becoming loud, protracted roars, their combined voices one of the most exciting, memorable sounds of Neotropical forests. Many bird species are vocal beginning before sunrise, an event ornithologists call the dawn chorus. Parrots, hidden in the thick foliage of a fruiting fig tree, reveal themselves by an occasional harsh squeak. Scarlet Macaws (Ara macao), flying serenely overhead with deep, dignified wing beats, so close to us that they fill the binocular field, suddenly emit a guttural, high-decibel squawk, about as musical as screeching brakes. Macaws are a feast for the eyes, but they can be an assault on the ears. Peccaries, the Neotropical equivalent of wild pigs, grunt back and forth to one another in low tones as they root for breakfast. A Whooping Motmot (Momotus subrufescens; plate 4-8) reveals itself as it calls softly, Hoop, hoop. Cicadas provide a constant background din, their loud, monotonous sound continuing throughout much of the day (plate 4-9). A reality of tropical rain forest wildlife observation is that on any given outing, the experience can seem underwhelming. It is not unusual to take a morning walk and see little in the way of birds

Plate 4-5. This Blue-headed Parrot (Pionus menstruus) is perched high atop a tree against an utterly white background, so typical of tropical daytime skies. Good binoculars or a good spotting scope will bring out its colors. Photo by John Kricher.

Plate 4-6. It is useful to look at the ground as you walk a forest trail. Sure, you might see a venomous snake— and thus avoid stepping on it—but more likely you will encounter an interesting insect, spider, or, as in this case, the cryptically colored and well named Leaf Litter Toad (Rhaebo haematiticus). Photo by John Kricher.

Plate 4-7. Learning to look carefully has its rewards. This slender serpent, called the Blunthead Tree Snake (Imantodes cenchoa), could be easily missed unless you look sharply. It ranges throughout the Neotropics, from Mexico through Amazonia. Photo by Dennis Paulson.

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Plate 4-8. The Whooping Motmot, like most motmots, is often hard to spot in the shaded understory. But its distinctive voice will reveal its presence. Photo by John Kricher.

Plate 4-9. Cicadas, members of the insect order Hemiptera, are a diverse group seen and heard (loudly) in pretty much any tropical rain forest. Photo by Dennis Paulson.

and mammals. And, of course, just the opposite might happen. You might come upon a fruiting tree that has attracted multiple species of birds and mammals. You might encounter a big mixed-species foraging flock of birds (either in the canopy or understory). Maybe you will have a lucky sighting of a group of peccaries or perhaps even a cat, such as an Ocelot (Leopardus pardalis). You might be surprised at how sparse your list of sightings is after an hour or two in the forest. This is normal. It takes lots of field hours to build up a long list of sightings. Experienced naturalists learn to

Plate 4-10. This Brazilian Tapir (Tapirus terrestris) is attracted to a mass of fallen fruits, and its feeding time makes for a good photo op. Tapirs are most active at night. Photo by Andrew Whittaker.

revel in what they find. They focus on the quality of the observation, not the quantity of species tallied. The rain forest is active after dark. Night is a good time to look for animals such as the Kinkajou (Potos flavus) and, of course, the numerous bat species that are foraging. Many lodges feature night walks through the forest or night drives along isolated roads that species such as tapirs, pacas, or even cats frequent (plate 4-10; see chapter 16). With good lights and some luck a night walk may even turn up a prowling Jaguar (but don’t count on it).

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Plate 4-11. Let’s head into the forest and see what’s in it. Photo by Bruce Hallett.

A Sample Walk in a Panamanian Rain Forest To help you get a feel for how a rain forest walk might unfold, I have chosen to take you to southern Panama. We begin our walk along the muddy forest trail, being careful to listen and look (plate 4-11). At several places we can’t help but notice lines of leaf-cutter ants (genus Atta), their well-worn trails crossing ours (plate 4-12). Leaf-cutters are abundant throughout the Neotropics and occur nowhere else on Earth. We notice that the ants come in various sizes, and some have impressively large mandibles. Most of the ants are bearing leaf fragments, neatly clipped in a circular pattern. The leaves won’t be eaten by the ants but will, instead, be taken to a vast underground colony, where they will be used to cultivate a fungus species that the ants farm. It is the fungus that is the real food of the ants, and so their alternative common name is fungus garden ants (chapter 10). Rain begins, soft at first, soon more intense. We are surprised at how little of it seems to wet us. The dense, leafy rain forest canopy intercepts most of the rain. Soon the shower ceases, though for a while the steady dripping from the canopy makes it seem as if it is still raining. A loud sound, not too distant, indicates that a big branch, or perhaps a full-size tree, has fallen. Tree falls during storms are not only common in tropical moist forests but essential to the overall ecological functioning of the forest (plate 4-13). Light gaps created by falling trees and branches will be discussed in detail in chapter 7. A small, richly brown animal resembling a tiny deer crossed with an oversize, tailless mouse tentatively

Plate 4-12. Usually the first sign of leaf-cutter or fungus garden ants that a visitor sees is a line of leaf fragments moving across a forest floor or, in this case, a log. A closer look will reveal the ants that are carrying them after they are clipped from the trees. Photo by John Kricher.

prances across the trail, pausing in a light gap just long enough for us to get a binocular view of it. It’s an agouti, in this case a Central American Agouti (Dasyprocta punctata; plate 4-14), a common fruit-eating rodent unknown outside of the Neotropics. We continue slowly along the forest trail, stopping frequently to look and listen. Looking up we notice a large bird moving through the canopy. It lands, and we get a good look at one of the gaudiest and most distinctive of the hundreds of Neotropical bird species. It’s a Yellow-throated (also called Black-mandibled) Toucan (Ramphastos ambiguus; plate 4-15). Toucans and their close relatives toucanets and aracaris are among the numerous birds unique to the New World tropics. They feed on many items, ranging from eggs and baby birds to their more common diet of various fruits. Continuing along, we hear an odd but distinctive snapping sound in the dense understory beside the trail. A small bird appears, its wings whirring as it lands on an understory branch. Patience affords an eventual good look. There are several of these birds, and they periodically begin snapping and whirring, their throat feathers puffed out. The birds are male Golden-collared Manakins (Manacus vitellinus; plate 4-16). Manakins gather together in forest areas called leks, areas of courtship behavior. The objective of the birds’ collective behaviors is to attract a female to mate with one of them. Lekking behavior is common among manakins and cotingas and will be discussed much more in chapters 10 and 15.

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Plate 4-13. Tree falls, surprisingly common in lowland humid forests, create openings called gaps that add to the complexity of forest ecology, as light floods into the gap and stimulates the growth of plants. Photo by John Kricher.

Plate 4-14. Agoutis are rodents, common in many lowland forests and often seen crossing trails. This species is the Central American Agouti. Photo by James Adams.

Plate 4-15. The large bill of the Yellow-throated (or Blackmandibled) Toucan is adaptive in reaching out to branch tips to bite off fruits. Photo by John Kricher.

Plate 4-16. A male Golden-collared Manakin with throat puffed out delivering its simple but hopefully effective twonote mating call. Photo by John Kricher.

Plate 4-17. The Green Iguana often basks over ponds, streams, and rivers. Not only does it get rich sunlight, but if threatened by a predator it can drop into the water below and skillfully swim away. Photo by John Kricher.

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Plate 4-18. At 13 cm (5 in) long, the diminutive American Pygmy Kingfisher is the smallest of the New World kingfishers. This bird is a female. Photo by John Kricher.

Plate 4-19. The large Blue Morpho butterfly, which rarely sits for its portrait, is most often seen flying with purpose along forest trails, openings, and along streams, all the while flashing its electric-blue upper-wing coloring. Photo by James Adams.

Plate 4-20. One of many Heliconius butterfly species inhabiting the Neotropics. The group, composed of many look-alike species, presents a remarkable example of coevolution and mimicry (chapter 11). Photo by John Kricher.

Plate 4-21. A cracker butterfly in a typical head-down position on tree bark. The name cracker is given to these butterflies because they make an audible sound when in flight that has been described as a “cracking.” Photo by John Kricher.

We come to an opening, a pond beside the trail. Overhead, where the leaves are in full sunlight, we spot a sizeable Green Iguana (Iguana iguana; plate 4-17). The iguana is basking, likely having eaten its fill of leaves earlier. Iguanas are carnivores, like virtually all other lizards, but only when they are small. As they mature into adults, they switch to a mostly vegetarian diet and remain arboreal, like reptilian sloths. Before we have finished looking at the arboreal lizard, a tiny, brightly colored, green and rufous bird pauses on a branch before us over the pool of water. It is an American Pygmy Kingfisher (Chloroceryle aenea; plate 4-18). At 13 cm (5 in) long, it is the smallest of

the six kingfisher species that inhabit the Neotropics. Kingfishers will be discussed more in chapter 9. Suddenly our eyes are drawn to the rapid, bouncing flight of a large, brilliantly colored Blue Morpho butterfly (Morpho didius; plate 4-19). This impressive lepidopteran appears dazzling electric blue in flight, as its shimmering upper-wing surfaces are illuminated by the sun flecks. Butterflies and moths are lepidopterans, a group very well represented by numerous tropical species. Some are brightly colored, others are cryptic; they are discussed in much more depth in chapter 11. Another butterfly, boldly perched on a flower as it feeds, draws our attention. It is a heliconius butterfly

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(Heliconius sp.; plate 4-20). There is much to be learned about this diverse group of lepidopterans, known sometimes as longwing butterflies, and we will say much more about them in chapter 11. We notice something on the bark of a nearby tree. Is it merely a feature of the bark? No, it’s yet another butterfly, perched head down on the tree trunk. It is one of the cracker species (Hamadryas spp.; plate 421), of which there are several that are highly similar in appearance). Also called calico butterflies, they range widely from the southern United States through Amazonia. Not all are cryptically colored. We begin to notice the quiet. Rain forests often seem serene, especially toward midday and into the afternoon hours. Birdsong has seemingly ceased entirely. Insect stridulations continue, and about the only other sound to be heard is of leaves rustling in the light wind at canopy level. But there are still things to be discovered. A loud, sharp rapping alerts us to the activity of a woodpecker. We see it, getting a good look at a female Lineated Woodpecker (Dryocopus lineatus; plate 4-22), one of the most widely distributed of the Neotropical woodpeckers. Looking into the understory, we spot something. It’s a small animal, and it is looking back at us, its long tail hanging limply below it. Is it some form of squirrel? A binocular view reveals that it is a monkey, a Geoffroy’s Tamarin (Saguinus geoffroyi; plate 4-23), a small monkey species common to Panama and Colombia. Unlike the larger capuchins, spider monkeys, woolly monkeys, and howler monkeys, tamarins (along with marmosets and saki monkeys) lack a prehensile tail, so they do not wrap their tails around tree limbs, using them as a fifth appendage. Monkeys are a major subject of chapter 16 and are also discussed elsewhere in the book. There are sounds, bird sounds. We have encountered an understory flock of various species traveling through the forest together as they collectively search for prey. For a few minutes they seem to surround us, and before they move on through the understory, we see a few pretty well. In the silence that follows, we pause for a few minutes and scan the forest around us, from low to high, looking for more birds (plates 4-24–27). The trail has brought us out to an open area, a large forest gap (chapter 7), where it seems suddenly much hotter, especially with the accompanying high humidity. Some bright flowers are evident at the edge of the gap, a cluster of heliconias (plate 4-28). Sitting on a small

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Plate 4-22. This female Lineated Woodpecker pauses to stretch her right wing while hitching up a tree in search of insect grubs or ants. Photo by John Kricher.

Plate 4-23. A Geoffroy’s Tamarin studies us as we study it. Photo by John Kricher.

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Plate 4-24. A Streaked Flycatcher (Myiodynastes maculatus) perched in the shady understory. Like most flycatchers it is a sit-and-wait predator, perching quietly until it sights a potential prey item and then flying out to snatch it. Photo by John Kricher.

Plate 4-25. Scanning the branches in the understory rewards us with a White-whiskered Puffbird (Malacoptila panamensis), perched motionlessly as it waits for a potential prey item to fly within reach. It is, like the Streaked Flycatcher, another sit-and-wait predator. This is a “typical” binocular view of an understory species. Many such species are easy to overlook. Photo by John Kricher.

Plate 4-26. A woodpecker? No, it’s a woodcreeper, a member of the large Furnariidae family, the ovenbirds and woodcreepers. This Northern Barred Woodcreeper (Dendrocolaptes sanctithomae) is one of the larger species. Woodcreepers do not hammer on wood as woodpeckers do; they use their beaks to probe for animal food among the bark and epiphytes. Photo by John Kricher.

Plate 4-27. The Chestnut-backed Antbird (Poliocrania [Myrmeciza] exsul) is an understory species that is often vocal but hard to see clearly. This view, a small visual hole between many branches and leaves, reveals the bird clearly. Antbirds do not eat ants, and many of them do not follow ant swarms; those that do eat arthropods flushed by the marauding ants. Photo by John Kricher.

branch near the heliconia cluster is a hummingbird with a long, down-turned bill, a Long-billed Hermit (Phaethornis longirostris; plate 4-29). There are several hermit species throughout the Neotropics, and they are typically birds of the forest understory and gaps. This group of hummingbirds typically moves from flower clump to flower clump along an established route, a foraging behavior called traplining.

We notice dense clumps of thin, spindly trees with huge, umbrella-like lobed leaves. These distinctive trees, whose slender trunks are reminiscent of bamboo, seem to occur wherever an opening exists, and they are particularly common along roadsides. They are cecropias (Cecropia spp.; plate 4-30), among the most abundant tree species on disturbed sites. We will look at these in more detail later (chapter 7), but

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Plate 4-28. Heliconias, with large and colorful bracts surrounding their small flowers, are easy for hummingbirds to find at forest edges and gaps. Photo by John Kricher.

Plate 4-29. A Long-billed Hermit taking time to rest from having made multiple visits to heliconia clumps. Photo by James Adams.

Plate 4-30. Cecropia trees, characteristic of forest edges and gaps, are very easy to identify (at least to genus level), with their distinctive spreading shape and large palmate leaves. Photo by John Kricher.

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for now we pay little attention since, sitting idly in the middle of a large cecropia, is a serene-looking Brownthroated Three-toed Sloth (Bradypus variegatus; plate 4-31). Sloths have such a slow metabolism that they barely move, and this one proves no exception to that rule. Slowly its left forearm is raised, a parody of slowmotion photography. Like the Tin Man’s joints in the Wizard of Oz before they were oiled, the sloth’s muscles seem to begrudge it the ability to move. The sloth’s cecropia is flowering, the slender, pendulous blossoms hanging down under the huge leaves. Soon a mixed-species flock of tanagers, honeycreepers, and euphonias fills its branches, gleaning both insects and nectar from the tree. Unlike the earlier flock, this group is brilliantly colored, displaying metallic violets, greens, and reds. The sky begins to cloud up again; the high humidity has taken its toll. We are feeling a bit tired, but we come upon one more small trail leading back into the forest. Should we do just a little bit more exploring? It’s going to rain again soon, that’s obvious, but still we take the trail. We see an odd-looking liana twisting from some trees and note that, on second glance, there is something peculiar about this particular liana. Is it a liana? Look again: it’s a snake, curled on a branch. We have found a small Boa Constrictor (Boa constrictor). And it has apparently attracted a hummingbird! A brightly colored male Violet Sabrewing (Campylopterus hemileucurus) hovers in the vicinity of the serpent (plate 4-32). The rain begins again in earnest; it feels cool, helping offset the effects of high humidity (plate 4-33). We put our binoculars and camera equipment in tightly sealed waterproof bags and begin walking back to the field station. After a refreshing beer or soda and some dinner, it will be time to think about doing a night walk (plate 4-34). As dusk falls we notice that the bats are appearing. The plaintive call of a Great Tinamou (Tinamus major) is heard. We are in the American tropics and feeling very good about being here.

Trail Etiquette: Top 10 Tips Most visitors to the Neotropics go as part of a tour, or they visit various lodges where local and highly competent guides will organize walks of up to 10 or sometimes more participants. It is important to observe good trail etiquette on the occasions when you are part of a group. Here’s how:

Plate 4-31. A Brown-throated Three-toed Sloth slowly ascending in a cecropia tree. Photo by Dennis Paulson.

1.

Keep talking to a minimum. Loud voices are one of the easiest ways to frighten wildlife. Unfortunately, some folks cannot seem to resist using a walk as a source of good conversation. That is not what it is intended to be. Resist the temptation to babble on about your recent Brazil trip when you are walking the trail with a group trying to see wildlife in Panama.

2.

Move around in the line. If you are on a relatively narrow trail, don’t always try to be in the front of the line next to the guide. It is a simple reality that those in the front of the line tend to see the most animals. Etiquette demands some measure of sharing. Shifting positions in line makes opportunities for good sightings more probable for all involved.

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Plate 4-32. Expect the unexpected in the tropics. Being out and on the trail always seems to have its rewards. Here is a Violet Sabrewing apparently curious about a small Boa Constrictor on the branch in front of it. The hummingbird would be wise to use extreme caution. Photo by James Adams.

Plate 4-33. Rain helps fill this small rain forest pool, but rain clouds cause a reduction in light, making observations more challenging. As the day wanes, it is time to head back to the field station or lodge. Photo by John Kricher.

Plate 4-34. Night walks are often good for finding active nocturnal foragers, such as this Lowland Paca (Cuniculus paca), caught with a fruit in its mouth. Photo by Sean Williams.

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Listen to your guide when he or she is giving directions to where something is. It is not always easy to describe where a small bird or monkey is in the complex foliage of a rain forest. Guides are amazingly good at doing this, and you must listen and follow their directions. Guides will usually have a green laser pointer to shine in the vicinity of (but never on) the animal they are attempting to show you. Above all resist the impulse to raise your voice in frustration at not yet having located the animal in question. Be cool. You’ll see it. And remember to let the guide do the talking. Even if you are looking at the animal, do not blurt out your version of directions, because all things considered, it is likely that the guide will be more concise, clear, and accurate, thus helping more folks zero in on it. And finally, do not point. If a bird or other animal is close, and you abruptly point at it, the sudden movement of your arm is often enough to alert the animal—and off it goes. If you have questions, try to save them for when the walk is concluded or when the guide asks if anyone has questions. Guides are trying to find wildlife for you to see, and peppering them with questions while walking causes unnecessary talking and can be distracting to the guide. Do not, for example, ask for a detailed explanation of the ecology of leaf-cutter ants while the guide is attempting to find wildlife for all to see. Experienced guides will typically stop the group at various convenient spots and entertain questions and provide information to the group. Remember that guides appreciate having things pointed out to them. The value of group travel is that many eyes are searching in many directions. If you see something, do not be reluctant to call attention to it. And don’t be embarrassed if it turns out to be something common. What may be common to some is not common to others. And besides, common stuff is still well worth a second, third, or hundredth look.

6.

Do not be upset if you call out a sighting and you turn out to be wrong. “There’s a spider monkey in that big green tree with the vines!” Your guide patiently figures out which “big green tree” you mean, and then gently tells the group that it’s a great sighting but actually is a young howler monkey, which can sometimes be mistaken for a spider monkey. It’s still a fine sighting.

7.

Be aware that you may not be the only one in the group with a camera. Digital photography has provided unrivaled opportunities to document wildlife. The illustrations that grace this book are testament to that reality. Even small pointand-shoot digital cameras are now available with extremely good telephoto capacity. But alas, I have seen some overzealous photographers actually push folks out of the way to get positioned for a clear shot. So please don’t thrust your 500mm lens in front of someone’s field of vision so you can get that “perfect shot” of the Swallow Tanager (Tersina viridis; plate 4-35) perched in the open. Of course, if you are alone, shoot away.

8.

Try to resist one-upmanship. Suppose the group notices a flock of Turkey and Black Vultures circling the forest over the canopy. Among them is one adult King Vulture (Sarcoramphus papa; plate 4-36), a wonderful sighting. Everybody gets a good binocular look and is pleased—smiles all around. Then someone cannot resist saying that he saw a King Vulture much closer when he was at such and such place. This is not OK.

9.

If you happen to miss something noteworthy, suck it up. It happens. Brooding and complaining about a missed sighting makes others around you uncomfortable and does you no good anyway. Remember, lodges typically have well-stocked bars. Consider that you likely experienced a great many more really cool sightings than you missed (plate 4-37). Celebrate them at happy hour, and be happy.

10. Last, and most important, enjoy what you see and learn from it. That is why you made the trip.

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Plate 4-35. The Swallow Tanager ranges widely throughout Amazonia, and is often seen perched in the open along forest edges. No need to crowd one another to get a fine photo of it. Photo by John Kricher.

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Plate 4-36. A soaring King Vulture. Seeing this magnificent species this well should be cause for celebration. Photo by John Kricher.

Plate 4-37. This female Lineated Woodpecker (Dryocopus lineatus) is perched aside a bromeliad on an exposed tree, making for a memorable view indeed. Photo by John Kricher.

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Plate 5-1. This forest in the Arima Valley in Trinidad is full of chlorophyll. Photo by John Kricher.

Plate 5-2. Tropical forests have the highest annual net primary productivity (NPP) of any terrestrial ecosystem. Photo by John Kricher.

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Chapter 5 Sun Plus Rain Equals Rain Forest A Quick Primer on How Nature Really Works Everything alive needs food. Everything alive is potential food. Food consists of chemicals, molecules structured so as to contain potential energy, or what is called “calorie content” on packaged foods. We eat food and thus we gain some of what’s in it, proteins, carbohydrates, fats, and minerals such as potassium, phosphorus, and calcium. And we also gain calories, some of the potential energy contained in the food. Pretty simple, right? Well, not so much. Aside from the mighty complex biochemistry and physiology we have merely alluded to, where does the food come from? In all but a few cases (mostly in the deep oceans), ultimately it is green plants, those with the unique pigment chlorophyll, abundant in terrestrial as well as in various aquatic species. Plants incorporate a tiny amount of solar radiation (sunlight) into low-energy molecules, thus converting them to high-energy molecules. To do this plants need three raw materials: sunlight, water, and various atoms. This biochemical process, which is the key to life on Earth, is called photosynthesis. Without it, life as we know it would not be possible. Earth’s biodiversity would not exist. By now you know that there is an abundance of light, water, and various atoms in the tropics. So the tropics are areas with high rates of photosynthesis, or what ecologists call primary productivity.

Primary Productivity: An Introduction Notice how green the rain forest shown in plate 5-1 is? That is because of a pigment molecule called chlorophyll. Here’s how it works. Primary productivity is the total amount of solar radiation (sunlight) converted by plants into high-energy molecules such as carbohydrates. Photosynthesis is the complex biochemical process by which this energy transformation is accomplished. Plants capture red and blue wavelengths of sunlight, what is called the photosynthetically active radiation. Plants use some of the energy from sunlight to split water molecules into their component atoms, hydrogen and oxygen. To accomplish this, plants utilize the green pigment chlorophyll. The reason a tropical forest

(or any forest, lawn, or grassland) is green is because chlorophyll reflects light at green wavelengths, while absorbing light in the blue and red portions of the spectrum. The essence of photosynthesis is that energyenriched hydrogen taken from water is combined with the simple, low-energy compound carbon dioxide (an atmospheric gas) to form high-energy carbohydrates (such as glucose) and related compounds. This is an evolutionarily ancient and fundamental process rooted in deep time. Oxygen from water is released as a byproduct. Photosynthesis, occurring over the past 3 billion years, has been responsible for changing Earth’s atmosphere from one of virtually no free oxygen to its present 21% oxygen. Take a deep breath and recall an old bumper sticker message: “Have you thanked a green plant today?” Of all natural terrestrial ecosystems on Earth, none accomplishes more photosynthesis than tropical rain forest. On an annual basis, a hectare (10,000 m2, or about 2.5 acres) of rain forest is more than twice as productive as a hectare of northern coniferous forest, half again as productive as a temperate forest, and between three and five times as productive as savanna and grassland (plate 5-2). Ecologists distinguish between gross primary productivity (GPP) and net primary productivity (NPP). The former refers to the total amount of photosynthesis accomplished, while the latter refers to the amount of carbon fixed (which means captured in compounds used in growth) in excess of the respiratory (metabolic) needs of the plant. In other words, NPP is the amount of carbon (as plant tissue) added to the plant for growth and reproduction. The simple equation GPP = NPP + R describes the relationship (R stands for respiration). Most published data on productivity is expressed as NPP. By way of example, if you measure the growth in biomass of a field of corn from seed to harvest, you are computing net primary productivity. You do not know how much energy the corn has used to maintain itself during its growing season. Such respiratory energy, essential to the metabolism of the plants, has been radiated back to the atmosphere as heat energy (along with a certain amount of carbon dioxide, oxygen, and water vapor from transpiration). A growing cornfield photographed from above with an infrared camera would reveal a deep red image, indicating the heat that is continually emitted from the corn. This is the energy of

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respiration, and it is common to all ecosystems, including tropical forests. Net primary productivity is easier to calculate than gross primary productivity, because NPP can be measured by weighing biomass change over a period of time (keeping in mind that some biomass will likely be consumed by herbivores). To calculate GPP we would need to assess respiration, which would require detailed physiological measurements of carbon dioxide output, making it considerably harder to determine. Tropical forests currently cover about 7–10% of the global land area (this amount was considerably greater before human deforestation), and because tropical moist forests exhibit high net productivities, they store about 40–50% of carbon present within terrestrial ecosystems. That is essentially what you are looking at when you behold the massive trees and dense green of a rain forest: carbon stored in the form of leaves, branches, bark, roots, wood. As noted above, tropical humid forests, particularly rain forests, are the most productive of Earth’s natural terrestrial ecosystems. And keep in mind that tropical humid forests store that carbon (in the form of wood) for long time periods. This is why tropical rain forests are sometimes referred to as carbon sinks. They make wood and keep it, and what is wood but large carbon-based compounds. But it is also true that rain forests have high rates of respiration, so they have the capacity to emit much carbon dioxide. Rain forests expend as much as 50–60% of gross primary productivity in respiratory metabolic needs. What this means, of course, is that gross primary productivity, the total rate of photosynthesis (net productivity plus energy used for respiration), is very high in rain forests, but the cost of photosynthesis, as measured in respiration rates, is also high (plate 5-3). Many physical factors, such as water availability, light intensity, and distribution of mineral nutrients, affect the outcome of GPP, which is why productivity varies significantly among global ecosystems. In the tropics, solar radiation, the most fundamental ingredient, varies mostly because of seasonal variation in cloud cover. The component molecules necessary for photosynthesis, carbon dioxide and water, are essential to support primary productivity. Water is limited in many ecosystems, including some tropical forests during dry season, thus water availability has a significant influence on global patterns of productivity. In addition, GPP is dependent on atoms such as nitrogen, phosphorus, calcium, and potassium (an incomplete list). In tropical forest ecosystems, as you will learn in

Plate 5-3. Tropical rain forests have high rates of NPP but also high rates of respiration. The forest breathes. Photo by John Kricher.

chapter 6, phosphorus tends to be a common limiting factor of NPP. Atmospheric carbon dioxide has been increasing since the onset of the Industrial Revolution and continues to rise, potentially contributing to global GPP as well as to current climate change. If water or other factors are not limiting, the addition of carbon availability in the atmosphere, as is now occurring, could act to stimulate additional primary productivity, one of the reasons for the focus of research on tropical forests as potential carbon sinks.

Rain Forest Net Productivity in Global Context In the course of one year, a square meter (10.75 ft2) of rain forest captures nearly 30,000 kilocalories of sunlight (GPP). Of this total, the plants devote about 35% to new growth and reproduction (NPP), using the remaining 65% for metabolic energy. These percentages are crude, and forests vary with regard to NPP in relation to GPP. Tropical forest is estimated to account for one-third of global potential terrestrial net primary productivity (fig. 5-1). The high productivity typical of tropical rain forests is facilitated by a growing season considerably longer than any in the temperate zone. At the height of the summer growing season, the daily NPP per hectare of temperate forest, such as is found in the Great Smoky Mountains, will be similar to that of a tropical humid forest. However, growth in a tropical humid forest is essentially continuous throughout the year, never

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interrupted by a cold winter when plants become essentially dormant. Temperature hardly varies, and because the tropical year is frost-free, there is no time at which all plants become dormant, as they are forced to do in winter throughout much of the temperate zone. Thus, more NPP occurs in the course of a year in the tropics than in other regions. Water availability is an important variable in tropical primary productivity. A strong dry season in the tropics may mean slower growth. In areas where dry season is acute, many trees are deciduous, dropping leaves at the onset of dry season and growing new leaves with the onset of rainy season. Droughts may exert severe effects on forest productivity (see “Drought Sensitivity of Tropical Forests,” below), often killing large numbers of trees. As rain forests are cut and replaced by anthropogenic (human created and controlled) ecosystems, much more NPP is directed specifically toward humans (in the form of agriculture or pasturage) and some is lost altogether (fields and pastures are less productive than forests), making less energy available for supporting biodiversity and reducing the potential efficacy of tropical forests as carbon sinks. For example, when a forest is cleared, the slash burned, and the site converted to agriculture or pasture, there is far less biomass available for carbon absorption (plate 5-4). Agricultural ecosystems (including pastures) do not store nearly as much carbon as forests. It is estimated that almost 40% of the world’s terrestrial NPP has either been directed to humans or lost due to humandirected habitat conversion. About three decades ago tropical forests were estimated to store about 46% of the world’s living terrestrial carbon and 11% of the world’s soil carbon. That figure is likely less now due to forest clearance.

Net Ecosystem Productivity Though tropical humid forests throughout Earth have the highest net primary productivities per hectare of any terrestrial ecosystem, one must realize that these forests are more than just trees. Ecologists understand that net primary productivity and respiration of the tree community does not, in itself, explain carbon flux (the rate in which carbon enters and leaves an ecosystem) at the ecosystem level. Why? Well, animals and fungi and bacteria are why. They live there too, and they all expire carbon dioxide. What this means is that carbon

Type of ecosystem Open ocean

Tropical rain forest Temperate forest

Savanna

Northern coniferous forest (taiga)

Continental shelf

Agricultural land

Temperate grassland

Woodland and shrubland

Estuaries

Swamps and marshes

Desert scrub

Lakes and streams

Tundra (arctic and alpine)

Extreme desert 20

40

60

80

100

120

140

160

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Average world net productivity (billion kcal/yr)

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Figure 5–1. This figure plots the net primary productivity (NPP) of major ecosystem types. The open ocean and tropical rain forest are close to equal, but their NPP rates are high for very different reasons. The oceans are vast in area but low in per unit area NPP. The rain forests are much more limited in area but high in per unit area NPP. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

Plate 5-4. This old pasture contains far less biomass and thus stores far less carbon than the tropical forest it replaced. Photo by John Kricher.

flux in the ecosystem is dependent on the net primary productivity of all plants minus the total respiration of all plants, animal consumers, and decomposers. Ecologists call this net ecosystem productivity (NEP). This simple equation describes this process: NEP = NPP – R (plants) – R (consumers) – R (decomposers)

The overall metabolism of a tropical forest, especially considering its complex decomposer food web, makes it possible for tropical forests to release more carbon (in

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some areas) than they capture, making them potential carbon sources rather than carbon sinks.

Tropical Forests: Potential Carbon Sinks? Because of atmospheric rise in carbon dioxide that correlates with industrialization and fossil fuel usage, it has been proposed that lowland tropical rain forest may act as a carbon sink, taking up and storing “excess” carbon dioxide added to the atmosphere through human activities (and thus reducing the atmospheric accumulation of this important greenhouse gas). But the question is, how much of this additional carbon actually becomes sequestered in rain forests? That is not an easy question to answer. One reason for the potential of tropical forest to store carbon is the sizes of the trees (plate 5-5). They are big, and there are lots of them. Ecological mathematical models (applied to Amazon forests) that incorporate such variables as maximum tree size, wood density, wood decomposition, recruitment (the growth of new trees from seeds), growth, and mortality of trees have indicated that if net primary production increased due to added atmospheric carbon dioxide, the production of wood would continue, and that Amazonian forests could potentially act as an important carbon sink. It sounds logical: big trees, long growing season, and high gross productivity combine to make a perfect machine to act as a carbon sink. But not so fast. The devil is in the details, and the details are not very clear. There are numerous sources of potential carbon loss in rain forest metabolism. Here’s what some of them are.

Plate 5-5. The immense amount of wood in tropical forests is why they seem to be ideal potential carbon sinks. Photo by John Kricher.

Seasonal Flux and Carbon Loss Tropical rain forests are not always gaining carbon. A study conducted by Scott Saleska and colleagues in two old-growth forest sites in Tapajós National Forest near Santarém, Brazil, showed a seasonal pattern of carbon gain and loss. The annual rainfall is 192 cm (76 in), and the wet season (>10 cm/4 in rainfall per month) lasts for seven months. Researchers examined changes in forest structure and monitored carbon stored in live wood and dead wood. The results were surprising. Net carbon gains occurred during the dry season, but carbon loss happened in wet season. Gross primary production was about the same in wet and

Plate 5-6. Is this tropical forest gaining or losing carbon? Look carefully and notice that it is a young forest with many small trees. As such it is growing rapidly and gaining carbon in the form of incremental biomass. Photo by John Kricher.

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dry season, but respiration was 40% higher at the peak of wet season (March) than it was at the peak of dry season (November). Of most importance, release of carbon dioxide from dead wood (through decomposer activities) exceeded the uptake of carbon by live biomass. Carbon was captured mostly by growth of small trees in forest gaps (plate 5-6). When dead trees dropped and decomposed, carbon was released from them, their loss opened gaps, and that stimulated growth of young trees.

Carbon Loss from Deforestation and Fire If tropical forests are cut and burned, an immense amount of carbon is quickly released back into the atmosphere (plate 5-7). One study by Emilio Moran and colleagues concluded that 336 million tons of carbon emissions enter the atmosphere each year from deforestation in Brazil alone. Another study, by M. Holloway, concluded that about 220 tons of carbon is released from soil and woody biomass to the atmosphere for every hectare of tropical forest that is cleared and burned. The loss of carbon to the atmosphere is an unavoidable outcome when tropical forests are cut and converted to ecosystems with less biomass and lower overall primary productivity. Largescale deforestation obviously increases the potential for a huge loss of carbon from tropical ecosystems, reducing their collective efficacy as carbon sinks.

Carbon Loss from River Outgassing We must consider the metabolism of riverine ecosystems in order to attain a full understanding of carbon flux in forests. Rivers and marshes are ubiquitous throughout the tropics, particularly in Amazonia. The metabolism of these systems is closely associated with inputs of organic and other matter from bordering terrestrial ecosystems. This is because organic matter from forests is transported by flood and normal precipitation (as well as natural leaf and branch fall) from terrestrial to riverine ecosystems. This allochthonous (externally produced) organic matter forms an energy base for river-dwelling decomposers ranging from fish to bacteria, the result of which is the eventual release of carbon back into the atmosphere. It is true that rivers contain a diversity of primary producers that fix carbon (providing autochthonous input). But does their combined activity capture more carbon than is released?

Plate 5-7. Fires severely reduce the potential for forests to act as carbon sinks, instead returning carbon dioxide to the atmosphere. Photo by John Kricher.

Plate 5-8. Outgassing by some tropical rivers reduces the efficacy of forests as carbon sinks. Photo by John Kricher.

Studies that measure the amount of carbon dioxide emitted from Amazonian rivers and wetlands suggest that outgassing (also known as degassing or evasion) may be important in returning carbon to the atmosphere (plate 5-8). Outgassing, which involves release of carbon dioxide and methane in gaseous form, represents a net loss of carbon via riverine metabolism. Data show that carbon loss by outgassing is far in excess of what could have been synthesized within the rivers and wetlands themselves. This means that allochthonous material from surrounding forest that washes into and accumulates in the riverine ecosystems forms the basis of metabolic activities of decomposers within the rivers and wetlands. Much of that carbon is ultimately released to the atmosphere both as carbon dioxide and as methane (plate 5-9). A study by Jeffrey Richey and colleagues that focused on carbon flux in rivers in central Amazonia

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throughout the year provides us with an example of this process. The research showed that rivers are not in carbon equilibrium, because they typically release more carbon than they acquire. Carbon loss is seasonal and varies among mainstream floodplain, mainstream channel, tributaries over 100 m (328 ft) wide, and streams less than 100 m wide. The high level of river outgassing observed in this study shows that outgassing obviously tempers the efficacy of tropical forests as carbon sinks, moving them closer to being, at best, in carbon equilibrium.

Drought Sensitivity of Tropical Forests It may seem surprising to invoke drought as an important variable in ecosystem function in tropical lowland humid forests. After all, don’t we call them rain forests? But tropical moist forests are seasonal, experiencing dry seasons of varying intensity. El Niño/Southern Oscillation (ENSO) events, which produce droughts, substantially add to that variability (chapter 2). The 2015–16 ENSO event produced a protracted dry season in Panama and other parts of the tropics, resulting in a vastly reduced rainy season. Historical long-term droughts are known throughout tropical regions. Given that tropical lowland forest plant species are adapted for high moisture levels, it should be expected that drought would exert a strong effect on these ecosystems. To what degree do tropical plant species vary in drought sensitivity? If climate change and increasingly frequent ENSO events result in more frequent and severe droughts, what sorts of changes in community composition might result? Ecologists have learned that there is strong variation in drought sensitivity among plant species, such that a prolonged drought could change the species composition of a forest as well as alter its net primary productivity. In times of drought NPP is reduced, and that is yet another factor in tempering the concept of rain forest as a carbon sink.

The Amazonian Drought of 2005: Some Surprises A severe and widespread drought occurred over Amazonia in 2005. The worst of the drought occurred in dry season, July through September, and was focused in southwestern and central Amazonia. The

Plate 5-9. Methane bubbles the water as it outgasses from a river in Brazil. The river sediment was stirred up with a canoe paddle, and the resultant release of methane momentarily supported a flame. Methane represents a significant amount of carbon released by rivers. Photo by John Kricher.

expectation would be that such an event would alter the pattern of carbon flux and primary productivity throughout the region. This happened, but not as predicted. A study led by Scott Saleska using data from the Moderate Resolution Imaging Spectroradiometer (MODIS) carried on NASA’s Terra satellite produced surprising results. The MODIS program enabled measurement of leaf area and chlorophyll content, which allowed the researchers to track the patterns of net primary productivity. The satellite data showed an increasing greening of the region during the drought. What? The expectation was clearly that drought would limit water availability and therefore reduce photosynthesis. But that did not happen, and increased greening was, to put it mildly, a surprise. But maybe it should not have been. One factor to be considered is that tropical trees have extensive, efficient root systems that capture groundwater, so perhaps they were less water-stressed than expected. Of even more importance, drought reduced rainfall, which, in turn, reduced cloud cover. More light, more NPP. Increased irradiance may have been the principal cause of the enhanced greening, and thus rain forest function may be relatively resilient to short-term droughts, severe though they may be. What of carbon flux? Satellite data showed only some of what was happening during the drought. The forest may have been greener, but it actually lost carbon. A team of 67 researchers led by Oliver Phillips made it their goal to document the effect of the drought on carbon flux. The study was conducted on permanent

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plots established as part of a long-term monitoring network known as RAINFOR, which consists of 136 permanent plots located in old-growth forest across 44 landscape types. These plots have been monitored for 25 years. Data are periodically collected on tree diameter and wood density. Mathematical models are used to calculate biomass and rate of change in biomass. For the 2005 drought, researchers focused on 55 plots; they measured net biomass change, growth, and mortality, and compared these data with those of earlier years. Prior to the 2005 drought, the 55 plots considered together showed a net increase in aboveground (dryweight) biomass, indicative of the forest acting as a carbon sink. During the drought year there was no net gain in biomass, but rather an overall loss. Analysis indicated that the biomass loss coincided closely with drought conditions and represented the first time since the plots were monitored that there was a net biomass decline. Tree mortality rates were also elevated in forests that experienced the most severe drought conditions. The large sample size of the study confirmed that the biomass loss and mortality increase were widespread, not confined to just a few areas. Should droughts such as that of 2005 become more frequent or more severe (as climate change models predict), we can expect to see more of these changes in forest composition and net primary productivity throughout Amazonia and, presumably, the rest of the tropical world. And the efficacy of lowland humid forests as carbon sinks would be very much reduced.

Will Too Much Rain Reduce NPP? Drought is at one end of a spectrum of factors affecting levels of NPP in tropical forests. At the other end is precipitation (plate 5-10). Models of climate change suggest increases in mean annual temperature (MAT) and mean annual precipitation (MAP) in the coming decades. The response of tropical forests to drought or added rainfall will determine whether these forests act as carbon sinks or carbon sources. It is clear that tropical forests are sensitive to drought. How sensitive are they to increased precipitation? To answer the question, E. A. Schuur performed a study using data from a source called the International Biological Program (IBP) combined with that from a recent survey of tropical forest NPP. The results showed

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Plate 5-10. In some tropical forests, precipitation may be sufficiently frequent to limit net primary productivity. Photo by John Kricher.

that as mean annual temperature increased, so did net productivity—initially not surprising. But more important, as mean annual precipitation continued to increase, productivity peaked and then declined fairly steeply. The maximum NPP was attained at a MAP level of 244.5 cm (96.25 in). Above that, NPP declined. In other words, above a threshold, rain reduced primary productivity. This result was initially a bit of a surprise. Why should increased precipitation result in declining NPP? One reason might be that reduction in total amount of solar radiation caused by persistent thick clouds lowers productivity. Another effect of added moisture might be to decrease the efficacy of nutrient cycling by leaching nutrients out of the soil and by decreasing decomposition rates. This could result from rainfall saturating soil, interfering with the aerobic demands of root systems and microbial organisms such as fungi and bacteria, the principal decomposers. There are thus two possible avenues, reduced sunlight and interrupted biogeochemical cycling (chapter 6), by which NPP rates may be driven lower with increased precipitation. Such an occurrence, as with severe drought, would temper the function of tropical forests as carbon sinks.

***

It is unclear whether global tropical forests will ultimately prove to be carbon sinks or carbon sources. The studies described above show that tropical forests have the potential to act as carbon sinks but rising global temperature and more severe and frequent droughts, to say nothing of increasing anthropogenic impacts, may collectively outweigh enhanced NPP, making tropical forests carbon sources, not sinks.

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Plate 6-1. Leaves showing damage from insect herbivory. Still, the scene is pretty green with plant biomass. Photo by John Kricher.

Plate 6-2. Caterpillars are collectively major herbivores in tropical forests, but they actually consume but a tiny percentage of the leaf biomass, most of which finds its way to the decomposer food web. Photo by Dennis Paulson.

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Chapter 6 Essential Dirt: Soils and Cycling Primary productivity brings solar energy into ecosystems, some of which is converted to potential energy incorporated into organic compounds. As energy passes through food webs, it does so in material form as high-energy, structurally complex compounds that make up organisms, organic waste, and eventually detritus. Thus energy and chemical elements are tightly coupled as they move through food webs. Energy is ultimately lost as heat, never recycled. In stark contrast, elements, the atoms and molecules of life, are recycled. The material basis for nature is the usage of key elements (in various proportions), each essential to life’s biochemistry; those elements are “shared” by life-forms in the process of biogeochemical cycling. Because Earth has no significant input of matter from space (a year’s worth of meteorites adds up to very little), atoms present in waste products and dead tissue must be reacquired, recycled back to living tissue. Decomposition and subsequent recycling is the process by which life’s chemicals move between the living and nonliving components of an ecosystem. Recycling is a by-product of decomposition, and decomposition is the means by which decomposer organisms acquire energy and nutrients. In a rain forest, energy in the form of biomass (from net primary productivity—think of a leaf, for example) will ultimately move in one of two paths. It may be consumed as part of living tissue, as when a caterpillar chews a leaf, in which case it will begin moving through the food web, possibly to pass through several animals. The path is called the grazing food chain (plant captures sun’s energy, caterpillar eats part of plant, antbird consumes caterpillar, forest-falcon eats antbird). Or it may remain within the leaf structure until the leaf eventually drops from the tree, at which time the energy becomes available to the multiple organisms composing the soil community. This latter direction moves energy directly into what is termed the decomposer food web. The decomposer food web is a rich and diverse array of organisms that are heterotrophic (meaning that they require organic carbon sources), ranging from vultures to bacteria and fungi that rely on dead material and waste products as their energy source. A glance at a lush, green rain forest, plus a dash of pure logic, is enough to show that the vast majority of the energy captured during photosynthesis is destined to directly enter the decomposer food web. If it were otherwise, trees, shrubs, and other green plants would show

far more leaf damage than they typically do (plates 6-1–2). Most net primary productivity remains as potential energy in the structural tissue of leaf, bark, stem, and root. This potential energy will eventually be released by a host of soil community organisms as they unpretentiously make their livings below your muddy boots among the forest litter and soil. Numerous species of microbes, in particular fungi and bacteria, are the principal organisms in this ongoing and essential process of decomposition, one of nature’s most fundamental processes. Using a series of reduction-oxidation reactions, microbes ultimately convert complex high-energy organic tissue back into simple low-energy inorganic compounds, making them available for uptake by the root systems of plants. Many other organisms also significantly contribute to decomposition: slime molds, actinomycetes, protozoans, and hordes of animals ranging from vultures to arthropods, earthworms, and other invertebrates. Termites (discussed later in this chapter), are uniquely important decomposers in tropical ecosystems. This host of life-forms collectively influences the complex process of converting a senesced fig leaf, a dead sloth, or a tapir’s feces back into basic chemical elements (plate 6-3). The soil community forms such a diverse, complex food web that it may rival the biodiversity found in the leafy canopy. Few studies have made detailed estimates of such parameters as fungal biomass or pathways of energy movement among the constituent flora and

Plate 6-3. A fallen leaf in a tropical humid forest undergoes a complex process of decomposition involving multiple organisms, as the minerals contained in the leaf are eventually released back into the abiotic element pool, and again available to plants. Photo by John Kricher.

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fauna of the decomposer community. Those that exist demonstrate the high complexity of the microbial components of the decomposer community. Fungi are abundant in the tropics, as well as elsewhere on Earth. An individual fungal strand is called a hypha, and a network of hyphae is called a mycelium. In some tropical forests the mycelium, a mesh-like interconnected array of fungal strands, is sufficiently dense as to be visible on the forest floor. Fungi, like bacteria, are essential decomposers. They ultimately liberate atoms back to the soil. In addition, many fungal species, collectively termed mycorrhizae (discussed below) are essential to trees and other plants in aiding the uptake of atoms from the soil. Microbial organisms facilitate a process called humification, in which complex soil organic matter (humus) is maintained at the interface between the tree roots and soil. Humus helps aerate the soil. Humus particles are negatively charged and by electrostatic attraction act to help retain mineral nutrients in the soil, such as potassium, magnesium, and calcium, that carry positive charges. Without such electrostatic attraction rain could leach these essential minerals from the soil. Soil represents a temporary repository for mineral nutrients such as phosphorus, nitrogen, calcium, sodium, magnesium, and potassium. Each of these minerals, as well as others, is necessary for biochemical reactions in organisms (fig. 6-1). A shortage of any one of them can significantly limit productivity. For example, phosphorus and nitrogen are important in the structure of nucleic acids (DNA and RNA) as well as proteins and other necessary molecules. Magnesium is an essential part of the chlorophyll molecule, without which photosynthesis could not occur. Sodium is essential for the functioning of nervous and muscular systems in animals. Consider how an atom is cycled. A leaf drops to the ground. Inside the leaf are billions of atoms, but let’s select a single atom of phosphorus (a propitious choice, as you will see later). This phosphorus atom may initially pass through a termite or other invertebrate that consumes the dead leaf tissue, only to be returned to the litter through elimination of waste or the death and subsequent decomposition of the creature itself. Indeed, the atom may move through numerous organisms before becoming part of the humus. Or the atom may be directly taken up by a fungus. This same atom eventually may pass through several dozen fungal and bacterial species,

Figure 6–1. Simplified compartment model showing the recycling system of an ecosystem such as a tropical forest. Compartments are not to scale. Note that decomposers ultimately make mineral nutrients such as phosphorus available again to primary producers, which take them up during the process of photosynthesis. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

each of which gains a modicum of energy by ingesting, digesting, and thus decomposing the deceased leaf (or termite). Within days the phosphorus atom, likely bound through chemistry to other atoms, becomes part of the inorganic components of the soil. At that point a tree root grabs the phosphorus, aided in doing so by the mutualistic fungi called mycorrhizae (discussed below), which penetrate or grow atop tree roots and take up the element and pass it along to the tree. The phosphorus atom will henceforth serve the biochemistry of the tree. The cycle is now complete. This nutrient cycling is also called biogeochemical cycling, a term that describes the fundamental process of chemicals moving continuously between the bios (living) and the geos (nonliving) parts of an ecosystem. The movement of minerals in an ecosystem is strongly influenced by both temperature and rainfall; thus, abetted by high temperatures and ample rainfall, biogeochemical cycling is efficient in the tropics. Heat stimulates evaporation. As plants warm they evaporate water; this heat-driven pumping process, called transpiration, cools the plants and returns water to the atmosphere. Transpiration is an essential process in plant physiology. It brings water and minerals up from the soil, helps cool the plant, and supplies essential water needed for metabolism. Water from rainfall is taken up by plants and transpired, returning to the atmosphere, under the stress of tropical heat. Nowhere is this continuous process of transpiration

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more obvious than along the wider stretches of the Amazon River. At midday, skies immediately above the great river tend to be clear and blue, but should you look over the distant forest on either of the riverbanks you will likely see big, puffy white clouds, formed by the condensing moisture transpired by the forest; you are literally watching the forest breathe (plate 6-4). Indeed, studies show that approximately 50% of the precipitation falling on the Amazon Basin is directly recycled via transpiration from the vegetation. Roots acquire essential minerals by transpirational uptake of water from soil. But transpiration can be a mixed blessing. Plants may lose too much water when subjected to constant high temperature, which causes desiccation. Many tropical plants retard evaporative water loss both by closing their stomata (openings on the leaves for gas exchange) and by producing waxy leaves that inhibit excessive evaporation of water.

Leaching High rainfall typical of the tropics in rainy season washes essential minerals and other chemicals from leaves, a process called leaching. Leaching is especially severe in areas subject to frequent heavy downpours. The protective waxy coating typical of tropical leaves contains lipid-soluble (but water-insoluble) secondary compounds, such as terpenoids, that act to retard water loss and discourage both herbivores and fungi. Drip tips (the sharply pointed tips of many tropical leaves) likely reduce leaching by speeding water runoff. Such adaptations enable a typical tropical leaf to retain both its essential nutrients and adequate moisture. Rainfall leaches minerals from soil, washing them downward into the deeper soil layers. The degree of leaching in any area is in part related to soil particle size. The largest soil particle size is rocky gravel, but gravel is not a prominent part of tropical soils except in regions with recently formed volcanic soils. More typically, soil is a mixture of sand, silt, and clay. Sand particle size ranges from 2.0 (0.07 in) to 0.5 mm. Silt particles are dust-like, ranging from 0.5 to 0.002 mm. Clay particles are microscopically small: coarse clay ranges from 0.002 to 0.2 µm (micrometer) and fine clay is less than 0.2 µm. Tropical soils are typically rich in clay, the structure of which strongly affects leaching as well as other characteristics, such as making tropical soils slippery when wet.

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Plate 6-4. A wide point in the Amazon River at midday. Notice that clouds have formed over the forest but not over the river. The clouds reflect the transpiration process vital to the physiology of the forest trees. Photo by John Kricher.

Clay particles, like humus, have negative electrostatic charges that attract minerals with positively charged ions, or cations, such as sodium, magnesium, calcium, and potassium. Clay also attracts alkaloid compounds, such as those produced in most tropical leaves, because these compounds also carry positive charges. Because rainfall adds positively charged hydrogen atoms to the soil, these abundant H+ ions exchange with those of elements such as calcium or potassium, which, when free, then leach to a deeper part of the soil or may leach out of the soil entirely by washing into streams and rivers. This process has the potential to reduce soil fertility. Rainfall also influences soil acidity, because the accumulation of hydrogen ions, either on humus or clay, lowers the pH (the definition of pH is hydrogen ion concentration), thus increasing the acidity of the soil. In the tropics, the combination of high temperatures and heavy rainfall may cause much leaching and result in strongly acidic soils. The pH of tropical soils is usually but not always acidic, typically ranging between 4.0 and 6.0 (but it can be less than 4.0 or as high as 6.7). Amazon soils are typically mineral-poor, high in clay, acidic, and low in available phosphorus, and the nutrient-poor nature of the soil is a limiting factor to plant productivity. A study by a team of researchers headed by J. J. Nicholaides concluded that nearly 75% of the soils in the Amazon Basin are acidic and generally infertile. Age also affects soil mineral content. Older soils are more leached of minerals than younger soils. This reality is all the more interesting because although much of the soil is considered nutrient poor and acidic, forest plants have nonetheless adapted to thrive on most of these soils. How do they manage that?

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One major difference between tropical and temperate forests is that in tropical forests the vast bulk of the rapidly cycling minerals is contained in the living plants, the biomass. Many researchers have shown that most of the calcium, magnesium, and potassium in a rain forest is located not in the soil but in the living plant tissue. For example, in a study Rafael Herrera performed near San Carlos de Río Negro in Venezuela, the distribution of calcium was as follows: 3.3% in leaves, 62.2% in wood, 14.0% in roots, 3.1% in litter and humus, and only 17.4% in soil.

Mycorrhizae Throughout the tropics as well as most of the temperate zone, there is an intimate mutualistic (mutually beneficial) association between tree roots and a diverse group of fungi collectively termed mycorrhizae. Up to 80% of all land plants contain mycorrhizae either on or inside their roots; a single gram (0.035 oz) of soil may contain 100 m (328 ft) of mycorrhizal filaments. Mycorrhizae are ubiquitous components of soils throughout most terrestrial ecosystems. Part of the mycorrhizal mycelium is inside a plant root, and part extends out into the soil. The fungus uses some of the plant’s photosynthate as food. In this regard, the fungus would appear parasitic. But though mycorrhizae take food from the plant, they are essential to the plant’s welfare, as they greatly facilitate the uptake of minerals from the forest litter. When the soil is nutrient poor, the benefit to the plant outweighs the energy cost it pays to the fungus. The mutualistic plant-fungus relationship is win-win. Many trees dependent on mycorrhizae have poorly developed root hairs; the fungal strands substitute for the missing root hairs. Mycorrhizae are essential in uptake of phosphorus, a nutrient that tends to be of limited availability in rain forest soils (it is discussed more below). Mycorrhizae may also have a role in direct decomposition and cycling, moving minerals from dead leaves into living trees without first releasing them to the soil, in essence taking a shortcut through the usual pathway of recycling. Mycorrhizae may also affect competitive interactions among plants, thus influencing the biodiversity of a given forest. Though mycorrhizae abound in the tropics, it should not be forgotten that not all fungi are mutualistic

Plates 6-5 and 6-6. Two examples of the fruiting (sporeproducing) bodies of the many kinds of fungi found in Neotropical forests. Photos by John Kricher.

with vascular plants. Various studies have shown that many fungi are important destroyers of seeds, having a greater negative effect than insects and rodents. Fungi are of vast importance in the functioning of a tropical forest, but most of their work goes unseen. Visitors who wander the trails usually see only the reproductive bodies, such as the many forms of mushrooms, which are often of remarkable beauty (plates 6-5–6). These mushrooms produce the nearly microscopic spores that, of course, are the essential components of fungal reproduction.

Where Do the Dead Leaves Go? Stop along the trail and look at the leaves. No, not the ones on the trees; look at the ones on the ground. There is surprisingly little accumulation of dead leaves and wood on rain forest floor, making for a generally thin

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Plate 6-7. Leaf litter is abundant in tropical moist forests, but decomposition is sufficiently rapid that in many areas the litter layer is relatively thin. Photo by John Kricher.

Plate 6-8. The species of leaf and the overall quality of the leaf litter, including the quantity of such components as available phosphorus, are important in determining how rapidly it will be decomposed. Photo by John Kricher.

litter layer (plate 6-7). Unlike the northern coniferous forests, for example, which typically have a thick spongy carpet of soft fallen needles, or the broadleaved temperate forests, where layer after layer of fallen oak, hickory, and maple leaves accumulate, a rain forest floor is often sparsely covered by fallen leaves. This is even more noteworthy when you keep in mind that more and heavier leaves occur in rain forest. The explanation for this seeming paradox is that the rates of decomposition and recycling occur with much greater speed in rain forests than in temperate forests. Just as productivity is continuous, uninterrupted by the frozen soils of a northern winter, biogeochemical cycling continues unabated throughout the year. In tropical wet forests, litter may be totally decomposed in less than one year, and minerals efficiently conserved. There is, of course, variability, and leaf decomposition rates are higher on richer compared with poorer soils. The most important variable in the rate of litter decomposition is climate; a warm and very wet climate hastens the decomposition rate. But beyond climate, the quality of the litter strongly affects the decomposition rate. Litter rich in phosphorus decomposes more rapidly than litter with less phosphorus (plate 6-8). Tropical moist forests typically cycle minerals “tightly.” The resident time of an atom in the nonliving component of the ecosystem is usually brief. This means that litter does not tend to accumulate. Estimates are that perhaps up to 80% of fallen leaf biomass is decomposed and recycled per year.

Rain Forest Soil Types and Nutrient Cycling In some regions, such as the eastern and central Amazon Basin, soils are old and mineral poor (oligotrophic), while in other regions, such as volcanic areas of Costa Rica or much of the Andes, soils are young and mineral rich (eutrophic). Soil characteristics, referred to as edaphic characters, vary regionally in the Neotropics because soil is the product of several variables: climate, vegetation, topographic position, parent material, and soil age. Even within a relatively limited region there may be variability among soil types. For instance, a single day’s ride in southern Belize will take you from orange-red iron-rich soil to clayey gray-brown soil. The gray-brown soil is calcium-rich, having weathered from limestone, and common throughout much of Belize. Most of the soils throughout the humid tropics fall into one of three classifications: ultisol, oxisol, or alfisol. Ultisols are generally well-weathered, meaning that minerals have been washed (leached) from the upper parts of the soils. Oxisols, also called ferralsols or latosols, are deeply weathered, old, acidic, and found on well-drained soils of humid regions; typically, these soils occur on old geologic formations, such as the ancient Guiana Shield in northeastern South America. These soils have high iron content and are reddish (plate 69). Common throughout the global tropics, oxisols are heavily leached of minerals and are strongly acidic. Alfisols are common in the subhumid and semiarid

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tropics and are closer to a neutral pH (though still acidic), with less overall leaching than typical oxisols. It is estimated that ultisols, oxisols, and alfisols, taken together, make up about 71% of the land surface in the humid tropics worldwide. Semiarid and arid regions in the tropics, because of climatic differences, have different soil types from those of humid and semi-humid regions. Some of these soils are dark, heavily textured, and calcareous, and some are subject to salt accumulation. Because of frequent occurrences of burning, and sometimes animal grazing, litter is thin and poorly developed on savanna soils, and the decomposer ecosystem is more limited. Termites, however, can be particularly abundant in arid, grassy areas (termites are discussed below). To summarize, the general pattern throughout much of the humid tropics is that heat and heavy moisture input result in formation of oxides of iron and aluminum (which are not taken up by plants), giving the soil its characteristic reddish color. Clay content is normally high, evident as you slip and slide your way over a wet trail. Mountain roads become more dangerous and often impassable during rainy season, because wet clay makes the roads slippery. Clay also has reduced porosity, impeding penetration by water. Thus clay soil enhances flooding potential. In the Amazon Basin, sediments eroded from highland areas during the Late Tertiary period were deposited in the western end of the basin, forming a flat surface about 250 m (820 ft) above sea level. Much of this surface, called the Amazon Planalto, is made up of kaolinitic clay, a substance devoid of most essential minerals but rich in silicon, aluminum, hydrogen, and oxygen. In the eastern part of Amazonia, soils are sandy, though remaining acidic and nutrient poor.

Laterization A process called laterization, which results from the combined effects of intensive erosion and heat acting on soil, is associated with some tropical soils. If vegetation cover is removed and bare soil is exposed to heavy downpours and heat, soil may be converted into a brick-like substance, preventing future plant growth. Laterization has long been utilized by tropical peoples around the world for making bricks used in buildings as impressive and venerable as some of the ancient temples in Cambodia. Though laterization has been

Plate 6-9. Soils known as red oxisols are common throughout much of the tropics. Photo by John Kricher.

Plate 6-10. This small subsistence farm along the Amazon River is sustained by the rich várzea soil (ultimately from the Andes Mountains) that is annually renewed in the flooding cycle. Note the grove of bananas. Photo by John Kricher.

widely reported as demonstrating the extreme delicacy of tropical soils and thus the futility of farming such soils, such a generalization is unfounded. Laterization occurs only with repeated wetting and drying of the soil in the absence of any vegetative cover. The loss of roots (which utilize and indeed produce aeration channels in the soil) and the repeated wetting and drying act to break up soil aggregates of bound clay particles. Only when these aggregates are broken up and eliminated, and the soil is thus subject to extreme compaction, does laterization ensue. In Amazonia, only about 4% of the soils are at actual risk of laterization.

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Tropical Soils and Agriculture Laterization is an extreme, but even attempts to farm the tropics by applying intensive agriculture often cause rapid loss of soil fertility. This need not be the case. Studies led by J. J. Nicholaides, Chris Uhl, Georg Irion, and others have shown that agriculture does succeed on poor tropical soils. For example, much of the soil composition in Amazonia is surprisingly similar to that found in the southeastern United States, where successful agriculture is routinely practiced. Soil infertility, though generally common throughout the Amazon Basin, does not preclude sustained agriculture. Where Amazonian soils are most fertile, as along floodplains, they will support continuous cultivation by small-scale family units (subsistence agriculture), with crops such as maize, bananas, and sweet potatoes, as well as small herds of cattle (plate 610). Tropical agricultural practices are discussed more in chapter 17.

Mineral Cycling on Oligotrophic Soil In parts of the Amazon Basin, white and sandy soils predominate, most of which are derived from the Brazilian and Guiana Shields, both ancient, eroded mountain ranges. Because these soils have eroded for hundreds of millions of years; they have lost their fertility and are thus poor in mineral content. The paradox is that lush broad-leaved rain forests grow on these essentially infertile soils. I stress on and not in the soil because most recycling occurs very near or actually on the soil surface. The word oligotrophic means “nutrient-deprived.” Oligotrophic-soil forests are found on both terra firme and on igapo floodplain (see “Blackwaters and Whitewaters,” below). Note that terra firme soils occur off floodplains, while igapo soils are part of floodplains, so the flood cycle has little to do with soil fertility. Soil fertility depends mostly on soil history. Forests on oligotrophic soils are less lush and of smaller stature than forests on rich soils. Henry Walter Bates (1862) commented on forest on poor-soil igapo (which he spelled Ygapo) floodplain, comparing it with the forest on the rich-soil delta: “The low-lying areas of forest or Ygapos, which alternate everywhere with the more elevated districts, did not furnish the same luxuriant vegetation as they do in the Delta region of the Amazons.”

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In forests with oligotrophic soil, up to 26% of the plants’ roots can be on the surface rather than buried within the soil, and root mats as thick as several centimeters sometimes develop. This obvious mat of surface roots (you can actually trip over it), which is intimately associated with the litter ecosystem, is much reduced or entirely absent from forests on eutrophic, or nutrient-rich, soil, where subsurface root mats occur. Surface roots are obvious as they radiate from the many boles across forest floor. A thin humus layer of decomposing material also covers the forest floor, and thus the root mat of surface roots, aided by mycorrhizal fungi, directly adsorbs available minerals.

Rapid Recycling Carl F. Jordan and colleagues have made numerous and extensive studies of nutrient conservation in Amazon forests. Using radioactive calcium and phosphorus to trace mineral uptake by vegetation, they found that 99.9% of all calcium and phosphorus was adsorbed (attached) to the root mat by mycorrhizal fungi plus root tissue. The root mat, which grows quickly, literally grabs and holds the minerals. In one study, in Venezuela, the decomposition of fallen trees did not result in any substantial increase in nutrient concentration of leachate water, suggesting strongly that nutrients leached from fallen vegetation moved immediately back into living vegetation. Phosphorus is usually limited in tropical soils because it complexes tightly with iron and aluminum, and, due to high acidity, is held in stable compounds that make it unavailable for uptake by plants. It is thus the key nutrient most difficult for plants to procure. Fortunately for plants, some mycorrhizae enhance uptake of phosphorus, a critical function in maintaining the productivity of the ecosystem. Buttressing of roots may aid in rapid recycling of minerals. The buttresses allow the root to spread widely at the surface, where it can reclaim minerals, without significantly reducing the anchorage of the tree. Tropical rain forests appear to represent the tightest recycling system in nature. If the thin layer of forest humus with its mycorrhizal fungi is destroyed, this recycling system is stopped, and the fertility is lost. Removal of forest from white sandy soils may result in the regrowth of savanna rather than rain forest because of the destruction of the tight nutrient cycling system.

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Other Nutrient-Retention Adaptations Some tropical plants have root systems that grow vertically upward, from the soil onto the stems of neighboring trees. These apogeotropic roots can grow as fast as 5.6 cm (2.2 in) in 72 hours. The advantage of growing on the stems of other trees may be that the roots can quickly and directly absorb nutrients leached from the trees as precipitation flows down the stem. This unique system, thus far described only for some plants growing on poor-quality Amazon soils, results in recycling without the minerals ever entering the soil! Both epiphytes and understory plants, especially the wide crowns of certain palms (nicknamed “wastebasket plants”), catch litter as it falls from the canopy. This arrested litter subsequently decomposes aboveground, enriching the mineral content of stem flow and thus having the effect of fertilizing the soil in the immediate vicinity of the wastebasket plant. Canopy leaves play a direct role in taking up nutrients. Algae and lichens on the surface of leaves are nutrient scavengers, adsorbing nutrients from rainfall and trapping nutrients on the leaf surface. When the leaf dies and decomposes, these nutrients are taken up by the root mat and returned to the canopy trees. Some trees both in temperate and tropical regions have what are termed canopy roots. These adventitious roots, similar in structure to subterranean roots, grow into the thick litter and epiphyte layer that accumulates on the surface of thick branches far from the forest floor. This adaptation enables trees to tap into nutrients far above the forest floor and is confined to forests where epiphyte density is high.

Nitrogen Fixation in the Tropics Approximately 79% of Earth’s atmosphere is gaseous nitrogen, a form of nitrogen not used in routine metabolism. But some organisms convert gaseous nitrogen into ammonia and nitrate, readily useable not only by themselves but also by other organisms, a process termed biological nitrogen fixation. This process is familiar in the temperate zone and is prominent throughout the tropics. It is the likely reason nitrogen is generally not a limiting nutrient in tropical soils. In some parts of the tropics the availability of nitrogen may exceed the demand for it, thanks to the prevalence of nitrogen fixation.

Plate 6-11. In Amazonian areas where soils are old and depleted of minerals, the soils are characteristically white and sandy. These areas drain into blackwater rivers, clear waters darkly colored by only the tannins and phenols from plant decomposition. Photo by John Kricher.

Two kinds of biological nitrogen fixation are recognized, symbiotic and free-living. Symbiotic nitrogen fixation is most closely associated with plants of the legume family (Fabaceae). Free-living nitrogen fixation occurs in soil with nitrogen-fixing genera such as Azotobacter and is also associated with epiphyllous microbes and lichens. Because of the distributions of legumes and free-living microbial nitrogen fixers, nitrogen fixation in the tropics extends vertically from canopy to soil. Plants of the huge and diverse legume family, abundantly represented in biomass and biodiversity throughout the global tropics, typically engage in symbiotic nitrogen fixation. Nitrogen is acquired through nodules in legume root systems. The nodules contain bacteria formerly called Rhizobium but now recognized to belong to four main genera and about nine others. Both the plant and the bacteria benefit from their interaction, as the bacteria convert free nitrogen into ammonium and in turn are supplied with potential energy from the plant, an obligate mutualistic association. Free-living nitrogen fixation also occurs abundantly in tropical forests. Certain epiphyllous lichens convert gaseous nitrogen into useable form for plants in a manner similar to that of leguminous plants. Studies have shown that leaf-surface microbes (microbial film) and liverworts facilitate uptake of gaseous nitrogen. Nitrogen fixation also occurs in termites, brought about by the metabolic activities of microbes in termite guts. Because of the abundance of termites throughout the tropics, these insects may contribute a substantial amount of nitrogen to the soil. Rates of nitrogen fixation both in soil and canopy vary widely. Though nitrogen is usually not considered

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Plate 6-12. Thick deposits of Andean sediment, which is rich in nutrients, characterize this section of the Río Napo in Ecuador. Colored by the sediment load it carries, it is known as a whitewater river. Photo by John Kricher.

Plate 6-13. This photo shows sediment deposit on an island along the Amazon River approaching Manaus, Brazil. The river deposits sediment but also sweeps it away, depending on the stage of the flood cycle. This creates dynamic islands within the river. Photo by John Kricher.

to be a primary limiting factor in forest net primary productivity, wet forests that experience high rates of leaching could conceivably experience high nitrogen loss from leaching and denitrification (a chemical reduction process by which certain bacteria liberate gaseous nitrogen into the atmosphere). The complexity of nitrogen flux and the patterns by which basic elements are differently concentrated in tropical soil and vegetation is essential to an understanding of Neotropical ecology. Generalities may be of limited value. Variability is apparent throughout the tropics.

Blackwaters and Whitewaters: The Poor and the Rich

Is It All about Phosphorus? In answer to the question posed in this heading: well, yes, it is. As stated above (see “Rapid Recycling”), phosphorous is a key nutrient for plants and the most difficult to procure. There is widespread agreement that phosphorus (P) limits primary productivity on many sites throughout the global tropics, particularly on soils of poor quality. Researchers have identified different “strategies” associated with plants on P-rich soils compared with those on P-poor soils. On rich soils with little P limitation, trees grow rapidly and retain P for short periods. But on P-poor soils, growth is slower and plants retain P for longer periods. In both cases, the forests appear to thrive. It is not possible just from observation to readily see the difference between the extremes (rich and poor) in the structure of forests even though the efficiencies of nutrient cycling of phosphorus vary dramatically between them.

White, sandy soils are usually drained by rivers called blackwaters, best seen at areas such as the Río Negro near Manaus, Brazil, or Canaima Falls in southeastern Venezuela. Water appears tea-like, dark and clear, colored by tannins, other phenols, and related compounds and by the humic matter. Blackwaters occur throughout the tropics and the temperate zone, including North America, especially such habitats as boreal peatlands and coniferous forests with mineral-poor, sandy soils. Part of the humic matter in blackwaters consists of defense compounds (chapter 11) leached from fallen leaves. It has been hypothesized that leaves are costly to grow on poor soils because raw materials to replace a fallen or injured leaf are in limited supply. Therefore, leaves on plants growing on white, sandy soils tend to concentrate defense compounds that help discourage herbivory. Carl Jordan has shown that leaf production in these conditions may be less than half that in forests on richer soils, and leaf decomposition time can be in excess of two years. When the old leaf finally does drop, rainfall and microbial activity eventually leach it of tannins and phenols, making the water dark, a kind of tropical tannin-rich “tea,” called blackwater (plate 6-11). In South America, blackwater tributaries drain into the Río Negro (Black River). This dark water is clear because there is little unbound sediment to drain into streams and rivers. Gallery forests bordering blackwater rivers (called igapo forests), are subject to seasonal flooding, and their ecology is intimately tied to the flooding cycle (chapter 12).

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In contrast, soils in various places—Puerto Rico, many parts of Central America, including much of Costa Rica, and throughout much of the Andes Mountains—are not mineral poor but mineral rich. Mostly volcanic in origin, these eutrophic soils are younger, some up to 60 million years old, some much more recent. Though exposed to high rainfall and temperature, they can be farmed efficiently and will maintain their fertility if basic soilconservation practices are applied. Because so much sediment leaches by runoff from the land into the river, waters that drain rich soils are typically cloudy, and are called whitewaters. This terminology can be confusing: whitewater rivers do not drain white, sandy soils; blackwater rivers do. Whitewaters drain nutrient- and sediment-rich Andean soils, and the term white refers to the cloudy appearance of the water, loaded as it is with sediment (plates 6-12–13). Mocha would perhaps be a better term to describe the water color.

Plate 6-14. The “wedding of the waters,” where the cloudy mocha-like sediment-rich Amazon intersects with the clear, dark, sediment-poor Río Negro. The confluence occurs near Manaus, Brazil. Photo by John Kricher.

The Wedding of the Amazonian Waters A dramatic example of the difference between blackwater and whitewater rivers occurs at the confluence of the Amazon River and the Río Negro near Manaus, Brazil. The clear, dark Río Negro, a major tributary draining some of the white, sandy soils of the ancient Guiana Shield, meets the muddy, whitewater Amazon, rich in nutrient load, draining mostly from the youthful though distant Andes. The result, locally called the “wedding of the waters,” is a swirling maelstrom of soupy mochacolored Amazonian water irregularly mixing with clear blackwater from the Negro, a process that continues downriver for anywhere from 15 to 25 km (9–16 mi), until the mixing is complete (plate 6-14). The most remarkable feature is that both soil types support impressive rain forest, igapo in the blackwater areas, várzea in the whitewater areas.

Why Parrots Eat Dirt Many species of animals throughout the world have been observed to intentionally ingest soil, a behavior known as geophagy. Geophagy is common among many bird, mammal, and insect species throughout the tropics. It is also widely practiced by humans in many tropical areas. Several reasons for geophagy have been suggested, and they are not mutually exclusive. Geophagy typically involves ingestion of soils high

Plate 6-15. Parrots of several species at a collpa (clay lick) along the Río Napo in Ecuador. Photo by John Kricher.

in clay content. Clay, because of its negative charge, binds potential toxins such as alkaloids and phenols. Ingested, it may aid in preventing diarrhea, help treat intestinal parasites, and supply vital minerals. In humans, geophagy is associated with pregnancy and may be an adaptation to eliminate plant toxins that could cause morning sickness. Parrots throughout the tropical world are known to ingest clay. In western Amazonia many parrot species (family Psittacidae) gather along certain outcroppings of soil, usually along riverbanks, called collpas, or clay licks (plate 6-15). The birds, which may number

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well over 100 at any given time in some places, are exposed to predation as they cling to an embankment, but their repeated presence suggests that they are somehow enhancing their fitness by acquiring a necessary chemical from ingesting the soil. A total of 28 bird species were observed, all ingesting soil, at one clay lick—a dirt cliff 500 m (1,640 ft) long and 25–30 m (80–98 ft) high—studied by Donald Brightsmith and his colleagues in southeastern Peru. Up to 1,700 parrots of 17 species visited daily. Research has shown that, in comparison with soils from other areas, the soil of clay licks: • has a greater percentage of clay, • a higher cation exchange capacity (CEC), • greater quinine binding (quinine is an alkaloid used to test for absorption of toxins), • greater sodium content, • lower sand percentage. Use of collpas correlated closely with the soil’s clay percentage, CEC, sodium, and quinine binding. The study showed that sodium was nearly 40 times more concentrated in the collpa soil, compared with surrounding soils. Parrots feed on plant material, particularly seeds and fruits, vegetation that is poor in sodium content. Clay lick soil had sodium concentrations of greater than 245 parts per million, about six times the sodium available in the parrots’ natural foods. That fact alone may go a long way in explaining why parrots, and perhaps other species, utilize collpas.

The Ecological Importance of Termites Termites are pantropical social insects occurring in great abundance. Termites are essential to biogeochemical cycling in the tropics. Like ants and certain bees, termites are complex social insects that have distinct castes (workers, soldiers, king, queen). They resemble ants but are easily differentiated by the termites’ lack of a sharp constriction between the thorax and the abdomen. Another important difference is that termites do not undergo a complete metamorphosis—larvae, pupae, adult—as hymenopterans (bees, ants, wasps), as well as many other insect groups, do (fig. 6-2). There are about 2,650 species of termites, and the majority of them occur within tropical and subtropical latitudes. Termites represent the ancient insect order

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Figure 6–2. The basic life cycle of termites. If you look carefully at termites around a nest, you will easily see workers and soldiers and, at various times, winged termites. Termites have a complex life cycle in which all reproduction is accomplished by a queen. The queen is always well hidden within the nest. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

Isoptera; their closest relatives are cockroaches and mantises (also abundant in the tropics). Unlike other social insects, such as bees and ants, termites are not haplodiploid (females diploid, males haploid). All termite individuals, like most other animals, are diploid. This tells us that termites evolved their complex societal structure independently of other social insect groups. Termites occur in all habitats, from rain forest to grassland, savanna, and mangrove forest. No one can visit the Neotropics without seeing termite nests and/or mounds. Basketball-size termite nests are typically attached to tree trunks and branches (plates 6-16–17). From the rounded, blackish-brown nests radiate termite-constructed tunnels in which the workers pass to and from the colony. In addition, especially in grassland, dry forest, and savannas, coneshaped termite mounds, some rising to heights of 2 m (6.5 ft) or more, erupt directly from the ground (plate 6-18). Many termite species also nest underground

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in vast subterranean colonies that are not in any way obvious from aboveground. Termites are generally well protected within their colonies but are preyed upon by anteaters. Emerging termites (which are flying to initiate new colonies) are fed upon by numerous bird species. Among the most abundant of the termites are the many species of Nasutitermes (family Termitidae, subfamily Nasutitermitinae), which range throughout the tropical world and are particularly diverse and abundant in the Neotropics. The life history of Nasutitermes is typical of many termite species. There are four castes: worker, soldier, king, and queen. If you wish to see workers and soldiers, locate a nest

(usually on a tree) and make a small cut into it. Nests are a paperlike material, carton, made from a gluelike combination of digested wood and termite fecal matter. When a nest is breached, scores of workers and soldiers swarm out in reaction to the disturbance. Workers are pale whitish with dark mahoganycolored heads. Soldiers are similarly colored but are larger than workers and have prominent heads and long snouts. Soldiers eject a sticky substance with the odor of turpentine that apparently irritates would-be predators, including anteaters of the genus Tamandua (chapter 16). Termites quickly repair an injured nest. They swarm about the surface, laying down new material to repair the damaged area.

Plate 6-16. Basketball-size termite mounds such as this are a common sight throughout much of the Neotropics. Photo by John Kricher.

Plate 6-17. This termite nest has been cut open and is swarming with worker termites repairing the damaged nest. Photo by John Kricher.

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Another way to see termites is to break open their tunnels. Workers are blind and follow chemical trails laid down by other workers. They will continue to pass en masse along an opened tunnel, though some will eventually repair it. The termite queen (or queens— some species have multiple queens) is located deep within the nest and cannot be seen unless the entire nest is dissected. Queens are immense compared with workers and soldiers. Virtually immobile, weighed down by an enlarged, gourd-like abdomen, the queens pass their lives producing the colony’s eggs, while workers attend to their needs. Termite species typically digest the cellulose in wood with the aid of the collective metabolism of mutualistic flagellate protozoans and bacteria inhabiting their hindguts. Once cellulose is reduced to simple sugar molecules, termites gain nutrition from the process of gut faunal and floral metabolism (much as ruminant mammals do). Removal of the protozoans will prevent a termite from digesting cellulose and other large molecules of wood. The termite, the bacteria, and the protozoans are obligate symbionts, an example of a complex coevolutionary mutualism (chapter 10). The flagellate protozoans gain fitness by inhabiting the termite, which provides continuous food, shelter, and a means of dispersal. The very hard wood we find in many tropical trees is perhaps an evolutionary response to selection pressures posed by continuous termite herbivory. Termites do not feed just on wood. Many species are essential decomposers of forest-floor litter. A study in Amazonia by Christopher Martius showed that termites, which collectively attain a biomass of 2,000 kg per hectare (1,800 lb/ac) and number in excess of 1,000 individuals per square meter (10.75 ft2) of forest floor, feed on somewhere between 20 and 50% of the forest’s fallen leaves. Termites chew up leaves as they pass them through their digestive systems. This action increases leaf surface area and enhances the microbial film, facilitating continued decomposition. Termitaria, the termite nests, form patches of high nutrient concentrations in otherwise nutrientpoor tropical soils. A study conducted along the Río Negro in Venezuela by J. Salick and colleagues showed that termites consumed between 3 and 5% of the annual litter production, transporting it to their termitaria. Termitaria contained more nutrients than litter, and litter was more nutrient-rich than the soil. When termites abandon termitaria, which they do

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Plate 6-18. A Rufescent Tiger-Heron (Tigrisoma lineatum) perched atop a termite mound in southern Brazil. Photo by John Kricher.

regularly—nest rate abandonment averaged 165 nests per hectare (65/ac) per year—these sites form patches of high nutrient level ideal for many tree species. Termite activity has a potentially important influence on nutrient cycling and tree establishment in this area of nutrient-deficient soils. Many termites feed on soil, including in their intake various soil-inhabiting fungi. The actions of soilfeeding termites are believed to help release nitrogen and phosphorus, contribute to humification, improve soil drainage, and help aerate soil, as well as increase exchangeable cations such as calcium and potassium. Termites are so abundant in the world’s tropical areas that they may contribute to global climate warming by enhancing the greenhouse effect. Their collective digestive abilities produce significant quantities of atmospheric methane, carbon dioxide, and molecular hydrogen. Forest clearance and the conversion of forests to agricultural ecosystems often result in increased termite abundance, thus accelerating the production of these atmospheric gases. On the other hand, some areas that have experienced forest clearance or have been converted to uses such as banana plantations appear to have lost termite diversity and biomass. In any case, when you happen upon a termite nest or mound, pause, look at it, and consider what a remarkable and venerable group of insects termites happen to be.

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Plate 7-1. Cleared forest represents a major disturbance patch. The photo shows a pasture at a forest edge. If left alone, forest will not become pasture, but pasture will return to its former state, forest. Photo by John Kricher.

Plate 7-2. Landslides, such as this one along a forested area on an Ecuadorian mountainside, create a large gap, initiating ecological succession. Photo by John Kricher.

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Chapter 7 If a Tree Falls . . . Rain Forest Disturbance Dynamics How (and Why) to Notice Disturbance When you first experience being in rain forest you are sure to be impressed by the density of the plant growth. Everything appears so lush, so dense, so green. But perambulate slowly through the forest, and look around carefully. Take in the full picture, from ground level to canopy. As you move from one place to another, you will see that the forest is not uniform in structure. There are scattered fallen branches and toppled trees that have opened the canopy, allowing sunlight to illuminate part of the forest floor. Youthful, riotous plant growth typifies such openings. Whole sections of forest may be composed of denser and smaller trees. Tropical forests are patchy, not uniform. And consider too the vegetation you see as you drive the roads. The trees and shrubs along roadsides and fields are largely different from those inside the forest. Yet even some of these species may be present inside forest, but only if there is an opening where light is abundant. Tropical humid forests are composed of vegetation patches of varying ages that result from the local disturbance history of the site. You can see this once you start to notice such things as differences in the density of trees in various forest areas, in the thicknesses of tree boles, and in the amount of light reaching the ground. Changes in species assemblages occur at various scales of space and time because of periodic and generally unpredictable natural or human-caused disturbance. Disturbances are relatively frequent in tropical forests, more the rule than the exception. Indeed, a common sound within rain forest is that of a big tree branch crashing to the ground. The magnitude of disturbance is variable. A disturbance may range from a single branch that falls from the canopy to the forest floor to a major hurricane that flattens hundreds of hectares (1 ha = 2.47 ac) of forest. Small disturbances, such as tree falls, are far more frequent than large-scale devastation. In fact, they are normal. Local disturbance history results in a dynamic mosaic of small and large vegetation patches. These patches may not loom large to the human visitor but they do to the plants and associated animals. Like the varioussize craters evident on the moon, disturbance patches sometimes overlap, adding to the spatial heterogeneity of the site.

Disturbance frequency is variable and strongly stochastic. This results in what ecologists like to term a shifting mosaic of local patch histories throughout a forest. The forest is a living, changing patchwork quilt of greenery, where each patch is somewhat different in size and age. This is what disturbance does to a lowland humid forest. Forest clearance for logging (either selective or clearcutting), agriculture, and pasturage represent humaninduced disturbances that vary from tiny clearings to hundreds of cleared hectares (plate 7-1). Anthropogenic disturbance is different from natural disturbance, though both may initiate an important ecological process called ecological succession (discussed below). Local areas of natural disturbance are called gaps, and the pattern of plant growth that follows the creation of a gap is called gap dynamics. Gap dynamics unfold in temperate as well as tropical forests. Once you develop an eye for spotting gaps, you’ll notice that they are common features of tropical forests. What happens when a gap is created? That’s pretty much what this chapter is about, but in a nutshell, gaps support an array of light-tolerant and light-demanding plant species that typically exhibit rapid growth thanks to the abundance of sunlight. Soon a jungle of trees, shrubs, and vines covers the gap, as plants compete for access to light. The vegetation development following a disturbance event is termed ecological succession. The word succession implies an orderly process, and as you will see, that is somewhat accurate. It is possible to predict which groups of species will first appear in gaps where sunlight abounds. But there is much variation from site to site. Heavy rains in tropical lowland forests are often accompanied by strong winds that bring down large branches and entire trees, creating gaps. Natural fire and landslides are other agents of disturbance (plate 72). Human-caused disturbance is different in that land is normally cleared of forest, the slash typically burned on site, and the vegetation replaced by agriculture or pasture. In the case of logging, forests are penetrated by logging roads and trails, and collateral damage to the forest ensues as select trees are removed (chapter 18). A diverse community of rapid-growing, shadeintolerant, sun-loving plant species quickly becomes evident in a disturbed area. Over time these species are,

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for the most part, gradually replaced by slower-growing more shade-tolerant species as the once open gap regains a closed canopy and shade predominates at ground level. This successional process is characteristically viewed as one of interspecific competition among plants for light and soil resources. Ecologists sometimes use the term recovery when describing the pattern of how ecosystems respond to natural disturbances. This term is inappropriate, as it suggests that the ecosystem was somehow wounded and that time heals the wound. It is important to realize that the species colonizing and thriving after the disturbance are specifically adapted to just such conditions, and so they represent part of the continuum of evolved species adaptations characteristic of that ecosystem. Their very existence as species clearly adapted to disturbance sites speaks to the routine nature of periodic natural disturbance events.

Plate 7-3. Early succession in the tropics is characterized by dense growth of sun-demanding plant species. Photo by John Kricher.

Succession in the Neotropics: A Closer Look Astute naturalists should enjoy perusing gaps and successional areas. These sunlit habitats, which may include large roadside fields, are ideal for encountering species of plants and animals that are not seen nearly as frequently in closed forests. Tropical succession typically begins with the appearance of rapidly growing sun-demanding plant species, some of which germinated from the soil seed bank, others of which arrived by natural seed dispersal, and still others that were present as seedlings (plate 7-3). Many are herbaceous and many are vines, both woody and nonwoody. Some shrubs and small trees are readily evident too. Seedlings of trees, some typical of closed forest, begin to grow into saplings. Growth rates are fast because light is abundant. Biomass increases. Sometimes vine growth is sufficiently dense as to envelop the brushy growth of other species, and a blanket of vines may cover the trees. Spindly trees and feathery palms push aggressively upward above the tangled mass. Biomass and the richness of plant and animal species continue to increase over time. Clumps of huge-leaved plants, typical sun-demanding species, are sometimes evident. One such group is Heliconia, its name derived from the Greek word helikonios (plate 7-4). The canopy is a dense, low, irregular, tangled assemblage of competing plants. Eventually more shade-tolerant tree species appear. Many of these may have been present from the

Plate 7-4. This disturbed gap in Ecuador experiences an abundance of sunlight (note the shiny leaves), ideal for species such as this flowering heliconia. Photo by John Kricher.

Plate 7-5. This field adjacent to a rural village in Belize, now abandoned, is undergoing early succession. The large-leaved plants are bananas grown by the former inhabitants. Photo by John Kricher.

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outset as seedlings or saplings, but their growth did not accelerate until the gap formed and light was available. Within a century, often sooner, a closed forest has filled the original opening. It is now second-growth forest, and its tree species composition may be somewhat different from the forest that was present before the initial disturbance event. The relative abundances and size-class distributions of tree species are different from those before the disturbance as well. Ecological succession, whether studied in the temperate latitudes or in the tropics, is affected by many factors, including chance dispersal and local soil conditions. Succession in the tropics differs from that at higher latitudes because there is a greater pool of plant species, and thus the outcome of succession in the tropics is more variable than in temperate latitudes. Plant species exhibit varying degrees of overlap in tolerance to light, temperature fluctuation, and soil characteristics; species with effective means of dispersal or with seeds that persist in soil banks invade first, followed by slowergrowing species that are typically more shade tolerant. Some species of plants have difficulty colonizing large gaps because they rely on animals as seed dispersers, and some of these do not typically enter large open areas. Succession is often initiated by human activity, frequently the appropriation of land for agriculture, eventually followed by abandonment (plates 7-5–6). But succession in the tropics is normal in the absence of human activity, as ecosystems periodically experience disturbance events. As you will learn, the moderate

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Plate 7-6. This abandoned house in Belize is literally vinecovered, as succession gradually reclaims the abandoned site. Photo by John Kricher.

The Word Jungle, Revisited One dictionary definition of jungle is “land overgrown with tangled vegetation, especially in the tropics” (Oxford American Dictionary, 1980). But as briefly mentioned in chapter 1, jungles are areas of active ecological succession where vegetation is dense and, yes, often impenetrable (plate 7-7). Of course that differs from the historic concept of jungle, which goes further, the connotation being a kind of forest primeval, dark and mysterious, with trees draped in vines and all sorts of exotic sounds. But the word jungle is rarely used in ecology today, because areas either of closed forest or open gaps are not really “overgrown” as the above dictionary definition suggests. They are normal results of plant dynamics in the tropics. But if you wish, feel entirely free to call it the jungle. It’s still a nice term with a certain romance associated with it, and it’s fun to tell your friends that you have just returned from a wonderful trip Plate 7-7. It’s a jungle out there. Note how dense the to “the jungle.” vegetation is. Photo by Beatrix Boscardin.

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frequency of disturbance may be at least partly responsible for why there are so many coexisting species of trees in tropical forests. Heavy rainfalls, landslides, hurricanes, fires, occasional lightning strikes, and high winds typical of rainstorms destroy individual or groups of canopy trees, create forest gaps, and sometimes level whole forest tracts. Isolated branches, often densely laden with epiphytes, break off and crash down through the canopy. This is normal in tropical forests.

How Does Succession Work? Studies conducted by Chris Uhl and others and by James Dalling and colleagues have shown that within Amazonia, a typical square meter (10.75 ft2) of soil is estimated to contain between 500 and 1,000 seeds, the seed bank. Think about that: when you are anywhere in the forest you are standing on future generations

of trees and other plants. All that is needed is some light for germination. Seeds of some species of pioneer plants, which are plant species that are first to occupy disturbed sites, may remain dormant in soil for nearly 40 years and still germinate after a disturbance occurs. Other seeds have far shorter residence time in the seed bank. But it is not just the seed bank that is important for regeneration after disturbance. Seeds transported either by wind or animals also reach disturbed areas and germinate. Now look closely at the shaded floor of a closed moist forest. Notice the shoots of trees? Observe the seedlings and saplings (plate 7-8). Once you start to really look, you are likely to see many small tree stems per square meter. Their growth is typically suppressed in the dense forest shade. Many of these will not grow further until a gap forms, providing sunlight. In Amazonia, between 10 and 20 seedlings and small saplings (10 cm/4 in) was 1.58% per year, implying an average life span of 63.3 years. At San Carlos de Río Negro in Amazonian Venezuela, mean annual mortality rates for trees of >10 cm dbh was 1.2%. Most tree deaths resulted in small gaps (large gaps were much rarer), and approximately 4–6% of the forest area was in gap phase at any given time. At Manaus, Brazil, mortality was 1.13% for adult trees, indicating a turnover time of 82 to 89 years for adult trees with a minimum size of >10 cm dbh. A tree often lives many years before attaining such a diameter, so the total age, from seedling to death, would be considerably longer. In the Manaus study it was learned that the larger a tree grew to be in diameter, the longer its probable life span (plate 7-15). For trees greater than 55 cm (21.5 in) dbh, the turnover time increases to 204 years. Mortality rates of seedlings and sapling trees exceed those of adults. Any recently germinated seedling stands a fairly high chance of being smashed by a

Plate 7-15. Trees of various ages growing together in an Amazonian floodplain forest. As they age, their survivorship potential changes. Photo by John Kricher.

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falling branch, or a single fruit, or whole tree, or perhaps buried beneath a fallen palm frond or some other large leaf. Herbivores also occasionally consume seedling and sapling leaves to the point of killing the tree. For Dipteryx panamensis, a common canopy species, seedlings ranging in age from seven to 59 months experienced a 16% mortality rate from litter fall alone. Mortality rates are consistently highest in juvenile plants, declining steadily as the plants age. Furthermore, many seeds never germinate because they are destroyed by a diversity of seed predators as well as fungal pathogens. For most of a tree’s life cycle, light acts as a significant limiting factor. Growth rates of trees in shaded interior forest are much lower than rates of those in more lighted, open areas. Dipteryx panamensis, like many tree species, shows extremely slow growth in low light conditions but grows quickly taller and wider in a gap. For this reason, growth rates tend to fluctuate during the typical life cycle of a tree. Gaps open, close, and can reopen, so that any given tree might experience several periods of rapid growth (when in gaps), alternating with periods of extreme slow growth (under a fully closed canopy). As described earlier, a substantial majority of tropical forest tree and shrub species show high levels of shade tolerance, with an accompanying high degree of growth plasticity—that is, the ability to survive in very low light levels of the forest understory and grow rapidly in gaps. The existence of emergent trees has long been recognized as a characteristic of rain forests. Of what possible benefit is it to a tree to invest additional energy to grow above the majority of other trees in the canopy? Added light availability is certainly one possibility. But in a study of five emergent tree species at La Selva, these trees showed significantly lower adult mortality rates than non-emergent trees. Perhaps emergents are more protected from being damaged by other falling trees, given that their crowns rise above the rest.

The Dynamics of Drought Drought was discussed in chapter 5. Drought often results from El Niño/Southern Oscillation (ENSO) effects. Beginning in 1980, a 50 ha (125 ac) permanent plot was established at Barro Colorado Island in Panama. Under the direction of Richard Condit, all woody plants at least 1 cm dbh were identified to species, measured,

and mapped, which is a lot of work. Censuses were done in 1982, 1985, and 1990. Over the three censuses, 310 species were recorded in the plot, and data were taken on 306,620 individual stems. In the brief time frame of this study, weather was an unexpectedly strong factor. An unusually protracted dry season coincident with a strong El Niño brought a severe drought to BCI in 1983. It has been well established that an ENSO, particularly a strong one, will have significant effects on patterns of secondary succession. Tree mortality rates were strongly elevated in the years immediately following the drought. For trees with >16 cm (6.3 in) dbh, mortality was elevated fully 50%. The increased death rate among shrubs and trees was attributed entirely to the drought. Approximately two-thirds of the species in the plot experienced elevated mortality from 1982 to 1985. Those plants surviving the drought showed elevated growth rates. For example, growth of trees with 16– 32 cm (6.3–12.6 in) dbh was more than 60% faster in 1982–85 than from 1985 to 1990. While this result may seem surprising at first, it is really to be expected. The death of so many trees permitted much more light into the forest (the gap effect) and reduced root competition for water and nutrients among plants. Total gap area on the plot increased after the drought but returned to its pre-drought level by 1991, an indication of how rapidly surviving plants responded to the added influx of light. Many species’ populations experienced changes in abundance during the period of the study, 40% of them changing by more than 10% in the first three years of the census (Hubbell and Foster 1992). Ten species were lost from the plot and nine species migrated into the plot from 1982 to 1990. Nonetheless, there was remarkable constancy in the number of species and number of individuals within the plot at any given time: • 1982: 301 spp., 4,032 individuals • 1985: 303 spp., 4,021 individuals • 1990: 300 sp., 4,107 individuals The drought killed many trees but created opportunities for additional growth, with the result that the deceased plants were quickly replaced. The speed of the replacement process was a surprise to the researchers. The analysis of the BCI data suggests some important conclusions: • The forest reacts to short-term fluctuations caused by climate. • The forest as a whole remains intact, though many species undergo population changes.

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• The forest may be undergoing a long-term change in species composition. This, of course, will be increasingly evident with climate change.

Life Histories of Some Representative Successional Plants Heliconia Heliconias (Heliconia spp., family Heliconiaceae) are recognized by their huge, elongate paddle-shaped leaves (similar to banana leaves) and their distinctive, colorful red, orange, or yellow bracts surrounding the inconspicuous flowers (plate 7-16). In some species, the bracts are reminiscent of lobster claws, hence the genus common name lobster-claw. Most heliconias grow best where light is abundant, in early successional patches and forest gaps, and along roadsides, forest edges, and stream banks. They grow quickly, clumps spreading by underground rhizomes. Though named for Mt. Helicon of ancient Greek mythology (the home of the muses), these plants are all Neotropical in origin; approximately 150 species are distributed throughout Central and South America. Colorful, conspicuous bracts surrounding the smaller flowers attract hummingbird pollinators, especially a group called the hermits (see plates 4-29 and 15-40; discussed in chapter 15), most of which have long, down-curving bills that permit them to dip deeply into the 20 yellow-greenish flowers within each of the bracts. Heliconias produce green fruits that ripen and become blue-black in approximately three months. Each fruit contains three large, hard seeds. Birds attracted to heliconia fruits are important in the plant’s seed dispersal. Heliconia seeds have a six- to seven-month dormancy period prior to germination, which assures that the seeds will germinate at the onset of rainy season.

Plate 7-16. Flowering heliconia in the understory of an Ecuadorian rain forest. Note the colorful bracts. The flower is barely visible within the second bract from the bottom. Photo by John Kricher.

Piper Piper (family Piperaceae) is a diverse, pantropical genus of plants with well over 1,000 and possibly as many as 2,000 species. The name Piper and the common name pepper are from the same root wood, and black pepper (from the South Asian species Piper nigrum) is just one of the spices derived from the cultivation of various Piper species. Piper is common in successional areas, though most Piper species are shade tolerant and are found in the

Plate 7-17. This cluster of Piper in Belize is ready for a nocturnal visit by piperphile bats. Photo by John Kricher.

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forest understory. It is estimated that about 700 species occur in the American tropics. (Another 300 species are found in the Asian tropics, 15 species occur in Africa, and up to 40 species are distributed on various islands in the tropical Pacific.) Most Piper species grow as shrubs, but some grow as herbs, some as vines, and some as small trees. The Piper plant’s distinctive small flowers are densely packed on a stalk, which in the Neotropics is called the candela or candellillo, Spanish for “candle.” When immature, the flower stalk droops, but it becomes stiffened and stands fully upright when the flowers are ripe for pollination (plate 7-17). Piper flowers are pollinated by many species of bees, beetles, and fruit flies. Seed dispersal, however, is dependent on bats. Small fruits form on the spike, and are eaten, and the seeds subsequently dispersed, by bats of the genus Carollia, which are called piperphiles. Several species of Piper may occur on a given site, but they do not all flower at the same time, reducing competition for seed dispersers as well as lowering the likelihood of hybridization. Some Piper species are well defended by aggressive ants, and others have their leaves laced with toxic chemicals, in particular various amides.

Plate 7-18. This Miconia shows the characteristically veined leaf pattern that distinguishes the genus. The stalk above the leaf contains the fruits that attract numerous bird species. Photo by John Kricher.

Miconia Miconia is a diverse genus of shrubs and small trees that are found within forests but also abundantly in successional areas. They are members of the family Melastomataceae (popularly called the melastomes), and as a group they are important to various birds and other animals for the abundant, small, nutrient-rich fruits they produce. Miconias have distinctively veined leaves and are thus easy to recognize (plate 7-18). More will be said of them and their relationships with birds in chapter 9.

Plate 7-19. Cecropias, growing in clumps along roadsides and in successional areas, are among the most conspicuous of Neotropical trees. Photo by John Kricher.

Cecropia You cannot miss the cecropias, abundant roadside trees of the Neotropics. Cecropia (family Urticaceae, formerly family Moraceae), comprising 61 species, is one of the most conspicuous and easily identified tree genera of the region. Easy to find, great-looking trees, cecropias, like the miconias, attract many species of birds. Cecropias are easy to recognize. They are thinboled, somewhat spindly trees with bamboo-like rings surrounding a gray trunk (plate 7-19). Their leaves are large, deeply lobed, and palmate, somewhat

Plate 7-20. Cecropias have large palmate leaves, beneath which the flowers and fruits dangle like fingers, attracting numerous bird species. Photo by John Kricher.

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resembling a parasol (plate 7-20). Leaves are whitish underneath and frequently insect-damaged. Dried, shriveled cecropia leaves that have dropped from the trees are a common roadside feature in the tropics. Some cecropias have stilt roots, but the trees do not form buttresses. Cecropias typically occur in areas of large light gaps or secondary growth, though some persist in secondgrowth forests. Pioneer colonizing species, cecropias are well adapted to grow quickly when light becomes abundant. Seeds remain viable in the soil for about a year and germinate when a gap is created. Cecropia seeds are sometimes abundant in the seed bank. An average of 73 seeds per 1 m2 (10.75 ft2) were present on one study site in Suriname. Because there are so many viable seeds present, cecropias sometimes completely cover a newly abandoned field or open area. They line roadsides and are abundant along forest edges and stream banks. Cecropias are effective colonizers because their seeds have a long residence time in the soil and accumulate there over time. Once germinated cecropias grow quickly, up to 2.5 m (8.2 ft) or more in a year. They are, however, generally short-lived, surviving to about 30 years, though some persist longer if established in the canopy. One limit to colonization by cecropia is recruitment from distant seed sources, such as could occur when there has been much forest fragmentation (chapter 16). Without nearby adult trees, seed dispersal is limited. Cecropias are moderate in size, rarely exceeding 25 m (80 ft) in height, though some emergent cecropias reach 40 m (130 ft). They are intolerant of shade, their success hinging on their ability to quickly grow above the myriad vines and herbs competing with them for space. To this end, cecropias, like many pioneer tree species, have a very simple branching pattern and leaves that hang loosely downward. Vines attempting to grow over a developing cecropia can easily be blown off by wind and possibly deterred by Azteca ants (more on these below), though I have seen many small cecropias that were vine-covered. Cecropias have hollow stems, a possible adaptation for rapid growth in response to competition for light, as this structure permits the tree to devote energy to growing tall rather than to the production of wood. Cecropias have separate male and female trees and are well adapted for mass reproductive efforts. A single female tree can produce more than 900,000 seeds every time it fruits, and it can fruit often. The base of each

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Plate 7-21. Large birds such as aracaris (a form of toucan) are among the many that feed on cecropia fruits. Photo by John Kricher.

Plate 7-22. This dried cecropia leaf forms habitat for spiders and insects, which tuck into its curled edges. Photo by John Kricher.

Plate 7-23. The Worm-eating Warbler, a North American migrant, specializes in probing dried, fallen cecropia leaves (as well as large leaves from other species) while on its Neotropical wintering grounds. Photo by John Kricher.

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flower holds four long, whitish catkins, hanging in fingerlike clusters. Research in Mexico showed that 48 animal species, including leaf-cutter ants, iguanas, birds, and mammals, made direct use of Cecropia obtusifolia. More than 30 bird species from 10 families, including some North American migrants, have been documented feeding on cecropia flowers or fruit (plate 7-21). Mammals from bats to monkeys eat the fruit, and sloths gorge (in slow motion) on the leaves. One North American migrant bird, the Worm-eating Warbler (Helmitheros vermivorum), specializes in searching for arthropod prey in dried leaf clusters, often those of cecropias, which abound in Neotropical forest and forest edge. Cecropia leaves are huge, and curl when they drop, forming ideal habitat for arthropods. This wood warbler is specialized to reach deeply into the cave-like curled leaves (plates 7-22– 23). On its breeding grounds it spends about 75% of its time gleaning insects from live leaves. The natural history of cecropia, as with all species, is a series of evolutionary life history trade-offs. Cecropias make a heavy investment in seeds—exhibiting high fecundity—that are generally well dispersed. But the seeds do not persist long in the soil and germinate only in a gap with abundant sunlight. Should a gap occur, the seeds germinate and the tree grows at a rapid rate. It may attain canopy stature, though its persistence in the canopy is usually of shorter duration than that of many other species. Cecropias have obviously profited from human activities, as cutting the forest provides exactly the conditions it requires. Ants (Azteca spp.) reside inside stems of some cecropias. These ants feed on glycogen-rich structures called Müllerian bodies (a form of extrafloral nectary) produced at the leaf axils. More will be said of these resident ants in chapter 11.

Kapok, Ceiba, or Silk-cotton Tree One of the commonest, most widespread, and most impressive Neotropical trees is the Kapok, Ceiba, or Silk-cotton Tree (Ceiba pentandra, family Malvaceae, formerly in Bombacaceae). Kapoks are sometimes left standing when surrounding forest is felled (plate 7-24). The look of today’s tropics throughout much of Central America is a cattle pasture watched over by a lone Kapok. The Kapok is striking in appearance. From its buttressed roots rises a smooth gray trunk often ascending 50 m (165 ft) before spreading into a wide

Plate 7-24. A single distant Kapok Tree is all that remains of a once-forested landscape in Belize. Photo by John Kricher.

flattened crown. Trees may surpass 60 m (about 200 ft) though such giants are rare. Leaves are compound, with five to eight leaflets dangling like fingers from a long stalk. The major branches radiate horizontally from the trunk and are usually covered with epiphytes. Many lianas typically adorn the tree. Kapoks originated in the American tropics but dispersed naturally to West Africa. They are grown commercially (for the fiber accompanying the seeds) in Southeast Asia as well, so today they are distributed throughout the world’s tropics. Ceibas require high light intensity to grow and are most common along forest edges, riverbanks, and disturbed areas. Like most successional trees, they exhibit rapid growth, up to 3 m (nearly 10 ft) annually. They are deciduous, dropping their leaves during the dry season. When the trees are leafless, masses of epiphytes and vines stand out dramatically, silhouetted against the sky. Leaf drop precedes flowering, and thus the flowers are well exposed to bats, their major pollinators. The fivepetaled flowers are white or pink, opening during early evening. Their high visibility and sour odor probably help attract the flying mammals. Cross-pollination is facilitated by the opening of only a few flowers each night, which means it takes two to three weeks for the entire tree to complete its flowering. Flowers close in the morning, but many insects, hummingbirds, and mammals seeking nectar visit the remnant flowers. A single Kapok may flower only every five to ten years, but each tree is capable of producing 500 to 4,000 fruits, each with approximately 200 or more seeds. A single tree can therefore produce up to 800,000 seeds during one year of flowering. Seeds are contained in oval fruits,

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Central American Successional Crop System Slash-and-burn (a.k.a. swidden) agriculture (chapter 17) has much in common with ecological succession in that it mimics the successional process in restoring soil after use for farming. Polycultures (plantings of numerous species in the same plot) can effectively maximize productivity of a given plot. Instead of only one crop, several surface crops, such as corn and beans, share the same plot with root crops (such as manioc or sweet potatoes) while the border of the plot may be planted in peppers and tomatoes. Polycultures are more resistant to insect attack, because crop biodiversity provides habitat for herbivore predators and reduces the competitive effects of competing forbs (weeds). John Ewel and colleagues have done comparisons of various monoculture crops with mixed-species plots, which have shown that the more diverse plots had significantly more root surface area, enhancing the plants’ ability to capture nutrients. They concluded that nutrient uptake and storage of minerals was critical to maintaining productivity in the plot. Robert Hart, working in Costa Rica, has suggested that farming can be directly analogous to succession. He presented a scheme whereby crops are rotated into and out of plots on the basis of their successional characteristics. Using such a system, Hart claims, it would be possible to utilize a plot of land continuously and productively for at least 50 years or more (plates 7-25–26; fig. 7-1). To quote Hart: Early successional dominance of grasses and legumes can be assumed to be analogous to maize (Zea mays) and common bean (Phaseolus vulgaris) mixtures. Euphorbiaceae, an important family in pioneer stages of early succession, can be represented by cassava (Manihot esculenta), a root crop in the same family. In a similar replacement, banana (Musa sapientum) can be substituted for Heliconia spp. The Palmae family can be represented by coconut (Cocos nucifera). Cacao (Theobroma cacao) is a shade-demanding crop that can be combined with rubber (Hevea brasiliensis) and valuable lumber crops such as Cordia spp., Swietenia spp., or other economically valuable members of the Meliaceae family to form a mixed perennial climax. (Hart 1980, p. 77.)

Plate 7-25.

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Subsistence farming is discussed further in chapter 17.

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Figure 7–1. This diagram, from Robert Hart’s study of farming practices, illustrates how a sequence of crops would essentially mimic the overall pattern of succession. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

Plate 7-26. Plates 7-25 and 7-26. Manioc (7-25), which yields the root crop cassava, and bananas (7-26) are common components of the types of plots described by Robert Hart. Photos by John Kricher.

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which open on the tree. Each seed is surrounded by silky, cottony fibers called kapok (hence the names Kapok and Silk-cotton Tree). These fibers aid in wind-dispersing the seeds. Kapok fibers are commercially valuable as stuffing for mattresses, upholstery, and life preservers. Since the tree lacks leaves when it flowers, wind can more efficiently blow the seeds away from the parent. Seeds can remain dormant for a substantial period, germinating when exposed to high light. Large gaps are ideal for Kapok, and the tree is considered successional, though it may persist for many years once established in the canopy. Kapok leaves are extensively parasitized and grazed by insects. Leaf drop may serve not only to advertise the flowers and aid in wind-dispersing the seeds but may also help periodically rid the tree of its insect burden.

Conclusion The daily lives of plants, ranging from newly sprouted seedlings to mature trees, are subject to many vagaries, all of which combine to make tropical forests the complex, indeed dynamic mosaics that they are. Stochastic factors strongly influence whether or not a seedling will ever reach adulthood. The luck of the draw is nature’s way. Both biotic and abiotic hazards influence the likely success or failure of a seedling to endure in a site and to attain adulthood. A newly sprouted seed faces many obstacles before reaching full maturity as a canopy resident—but some make it. From small gaps to large forest disturbances, the dynamics of tropical forests continually raise new questions and new challenges for the tropical ecologist (plate 7-27).

Plate 7-27. Succession put to use. Look carefully, as this is actually a “living fence.” Cuttings of rapidly growing, sun-demanding trees of various species are planted in rows, and the trees grow into pasture fences. This practice is common in many parts of the Neotropics. Photo by John Kricher.

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Chapter 8 Evolutionary Cornucopia Evolution and Biogeography If you visit a tropical moist forest in Brazil and then visit one in Sabah, Malaysia, in northern Borneo, at first glance you might think you are visiting the same place. Both appear structurally similar. The weather is hot and humid. There are many impressively tall trees, buttressed roots, abundant vines and epiphytes attached to the trees. There are palms and strangler figs. Monkeys are common. Colorful and not so colorful birds are skulking in the trees and undergrowth. Gorgeous butterflies are evident. There are a few snakes. Ants are abundant. But a comprehensive species list from these two widely separated forests will contain virtually no species in common. Instead, not only will species differ, but whole families of plants, birds, mammals, insects, and other groups will be distinct between Brazilian rain forest and Bornean rain forest. The forests are structurally similar because natural selection, the process that leads to adaptation, favors certain characteristics in regions of high temperature, high humidity, and abundant rainfall. Broad-leaved evergreen trees, in whichever tropical realm they occur, share various characteristics that confer high fitness (the ability to successfully reproduce) in such areas, just as various forms of colorful butterflies have high fitness within broad-leaved forests. Some of the animals have also converged to be both morphologically and ecologically similar. For example, Neotropical toucans bear an anatomical and ecological similarity to Old World hornbills (family Bucerotidae). Both families are composed of large birds with huge, down-curved, colorful bills and robust bodies. Both nest in tree cavities, and both include fruit as a major part of an otherwise broad diet. Hornbills and toucans are not evolutionarily closely related and as a pair represent an example (one of many) of convergent evolution (plates 8-1–3). Why did tropical forests in Borneo and Brazil evolve such different species? Borneo and Brazil have been isolated from each another for many millions of years, more than enough time for much evolution to occur. And geographical separation, which evolutionary biologists call vicariance, allows populations that are physically separated—or allopatric—and thus unable to interbreed to ultimately diverge evolutionarily, eventually forming new species. This outcome forms the cornerstone of the Biological Species Concept (described below). Separation of continents results

Plate 8-1. No, this is not a toucan. It is a Rhinoceros Hornbill (Buceros rhinoceros), from Borneo. It has evolved to be morphologically and ecologically similar to Neotropical toucans, but is only distantly related to them. Photo by John Kricher.

Plate 8-2. Don’t look for the Whiskered Treeswift (Hemiprocne comata) anywhere in the Neotropics. It is in the family Hemiprocnidae, all members of which are confined to tropical Asia. This species, photographed in Borneo, is common along rain forest edges. Photo by John Kricher.

Plate 8-3. But do look for the Paradise Tanager (Tangara chilensis), a member of the large tanager family (Thraupidae), endemic to the Neotropics. Flocks of Paradise Tanagers, sometimes joined by other tanager species, are found through much of Amazonia. Photo by Andrew Whittaker.

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Plate 8-4. The complex topography of the Andes Mountains, a long chain with numerous ridges, valleys, and elevation gradients, contributes to the high incidence of vicariant populations and thus stimulates speciation. Photographed from Ecuador. Photo by John Kricher.

Plate 8-5. The Bahama Yellowthroat (Geothlypis rostrata) is one of three endemic bird species of the Bahamas. Photo by John Kricher.

Plate 8-6. The Cuban Tody (Todus multicolor) is one of 23 species of birds endemic to the island of Cuba. Photo by Carl Goodrich.

Plate 8-7. No, it’s not the Cuban Tody again. This is a different species, the Puerto Rican Tody (Todus mexicanus). It is one of Puerto Rico’s 18 endemic bird species. Photo by Peter Crosson.

Plate 8-8. The Galápagos Marine Iguana (Amblyrhynchus cristatus) is one of many endemic species of plants and animals of the Galápagos archipelago. Marine iguanas show distinct genetic differences from island to island throughout the Galápagos. Photo by John Kricher.

Plate 8-9. The Rufous Hornero (Furnarius rufus) is one of many species in the Neotropical endemic family Furnariidae. The family takes its common name, the ovenbirds, from the nestbuilding habits of a few of its species, such as the hornero, which builds a mud nest (upon which this bird is standing) that resembles an old-fashioned oven. Photo by John Kricher.

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from ongoing plate tectonics, which is the geological process in which Earth’s large basaltic plates, some bearing continents and islands, move in relation to one another because of heat generated from inside the planet itself. Plate tectonics creates vicariance on a global scale. Similarly, island floras and faunas are unique because following random colonization (from a mainland source) by various organisms, evolution occurred in isolation from mainland influences. The unique floras and faunas of the Hawaiian and Galápagos Islands illustrate this point. On a continent, a physical barrier separating species could be a mountain range, such as the vast Andes chain in South America; a broad river, like the Amazon; or perhaps a desert, such as the Atacama of western Peru and Chile. On a broader scale, oceans form barriers between the continents and around islands. Allopatry imposed by vicariance creates a physical barrier to gene exchange, and that triggers speciation (plate 8-4). When a species’ evolutionary history, its very genealogy, is unique to a given region, and the species is found only in that region, it is termed endemic. Endemism is typically common among island species because of the relative isolation of islands (plates 8-5– 7). For example, of the approximately 100 resident bird species in the Bahama Islands, three are endemic. The island of Cuba contains 23 species of endemic birds. The Galápagos archipelago, isolated from Ecuador by about 1,000 km (620 mi) of ocean, is legendary for its unique assemblage of endemic plants, birds, and reptiles, which inspired Charles Darwin to begin thinking about the possible evolutionary implications of endemism after he visited the islands in 1835 (plate 8-8). Endemism is also a common component of continental areas, where it may take two forms. One of these is taxonomic endemism. The woodcreepers and ovenbirds of the family Furnariidae represent an endemic family, found only in the Neotropics (plate 89). Of course, this type of endemism applies at various taxonomic levels: there are endemic families, endemic genera, and endemic species. Another form of endemism is regional endemism, which occurs when a specific area within a region contains a variety of endemic species, many not closely related. For example, nine distinct areas of avian regional endemism are recognized in Ecuador (plate 8-10). Such centers of regional endemism are of particular conservation concern, since they contain unique arrays of species.

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Plate 8-10. The 20 cm (8 in) long Toucan-Barbet (Semnornis ramphastinus) is one of 44 bird species endemic to the western slope of the Andes in Ecuador. A country with a total area about equal to that of the state of Nevada, Ecuador has nine unique areas of avian endemism that account for 243 species in total. Photo by Steve Bird.

Figure 8–1. Areas of postulated endemism in northern South America. From Cracraft 1985. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

Figure 8–2. Areas of postulated endemism for Amazonia and the Andes Mountains. From Cracraft 1985. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

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Analyses of bird distribution patterns throughout South America by Joel Cracraft, Jürgen Haffer, and others have demonstrated numerous areas of probable endemism throughout the continent (figs. 8-1–2). Each of the postulated areas of endemism contains unique assemblages of species not found in other areas. This helps account for the unusually high diversity of birds throughout the continent, and it suggests that evolutionary patterns have been complex.

Natural Selection Natural selection is defined as differential reproduction among genotypes within a population. That means that not all members of any population survive to the same age or produce the same number of offspring. This is mostly because not every member of the population carries the exact same combination of genes (plate 811). Some combinations of genes are more superior in certain environments than others. There are, so to speak, genetic winners and losers in every population at every generation—kind of the luck of the draw. Genes, the long, coiled molecules of DNA that contain hereditary information, were unknown to Charles Darwin, although he fully understood that many traits evident in

Plate 8-11. These butterflies clustering in Brazil (members of the family Pieridae) are not genetically identical, though they all look alike. The genetic differences among them account for why natural selection acts on them as individuals and ultimately for why this species has evolved as it has. Photo by John Kricher.

the phenotypes of every individual are inherited. It’s no secret that siblings tend to look alike as well as resemble their parents and grandparents. But what Darwin and the independent co-discoverer of natural selection Alfred Russel Wallace both realized was that for all the similarity there is among members of a population, it is the genetic differences among members of populations that make up the currency of evolutionary change and natural selection. When Darwin published his most famous work, On the Origin of Species, in 1859, he challenged the reader to grasp this essential point (many, to this day, do not). As Darwin might be apt to say if he were leading a field trip in Amazonia: realize that all squirrel monkeys within a given population are not alike. Some will be genetically inclined to be heavier, some more lithe; some will be more resistant to certain pathogens and parasites; some will be able to better detect potential predators such as Harpy Eagles. These qualities will determine which are the animals most likely to survive and reproduce and thus send their genes into the next squirrel monkey generation. This is natural selection. As long as a population contains genetic variability among its members, natural selection will potentially act (plate 8-12). Individuals, because they do not share exactly the same genes, will respond somewhat differently to abiotic (such as temperature, water availability, etc.) and biotic (such as threat of predation, competition, parasitism) selection pressures imposed by their environment. This variation inevitably leads to what Darwin called the “struggle for existence.” Natural selection acts only on the present, never “planning” for the future. The survival of the fittest, a term used to describe natural selection (but coined by Herbert Spencer, not Darwin), sums up the generation-bygeneration sorting done by natural selection on any population. Individuals that survive and reproduce more successfully than others in any particular generation—in other words those that are fit—do so because conditions, whatever they may be, suit them somewhat better than others in the population. They are, for the moment, evolution’s winners, at least of that round. Natural selection is a statistical truth. Individuals with genes that confer reproductive advantage will tend to leave the most progeny, thus those genes will proportionally increase generation after generation relative to others in the population’s gene pool. And as gene frequencies change, the appearance, the physiology, and (if an animal) the behavior of the species will change too. The species will evolve.

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Genetic variability originates through the random process of mutation, a sudden and unpredictable change in a gene. Mutation is nondirectional: environments do not cause or produce useful mutants in response to need. The variability resulting from mutation is enhanced by recombination of genes (more accurately called alleles) in sexually reproducing species. Selection can act only on whatever genetic variants are present. Selection, unlike mutation, is not a random process, because only certain members of a population are best suited for a given environment, and thus these individuals have a nonrandom chance of survivorship and reproduction. In recent years both geneticists and molecular biologists have established beyond doubt that large amounts of genetic variability exist in most populations. Thus, in most cases, there is ample raw material for natural selection to act upon. Evolution continues. Natural selection does not guarantee survival. Most species that have ever inhabited Earth are now extinct, and because of all the various human influences on Earth at the current time, more species are moving toward what may become the sixth major extinction event in the history of our planet. But that said, the amazing biodiversity of Earth so evident in tropical latitudes remains the remarkable result of natural selection.

Adaptations An adaptation is any anatomical, physiological, or behavioral characteristic shown to enhance either the survival or the reproductive ability of an organism. Such traits, as they translate into successful reproduction, make up what is called evolutionary fitness. Fitness is reflected in suites of adaptations, all of which result from the action of natural selection. For instance, various opossums, Neotropical porcupines, and the Kinkajou (Potos flavus), as well as many monkeys of the American tropics, possess a prehensile tail (plate 8-13). (And some snakes do too.) Such a structure functions effectively as a fifth limb, lending security and mobility to the animal as it moves through the canopy. It is easy to see intuitively that the prehensile tail is an adaptive structure. Tailless monkeys or opossums would face a smaller lifetime reproductive success because of the added risk of falling. But note that many Neotropical monkeys (sakis, for example) do not possess prehensile tails and yet are fit within their arboreal environments.

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Plate 8-12. This photo shows a flock of Scarlet Ibises (Eudocimus ruber) feeding before roosting at Caroni Swamp in Trinidad. The mangroves in which they roost and the birds themselves are each members of populations experiencing natural selection, along with everything else alive in the mangrove forest. Charles Darwin and Alfred Russel Wallace recognized, in this profound reality of nature, how nature really works. Photo by John Kricher.

Plate 8-13. This Yellow-tailed Woolly Monkey (Oreonax [Lagothrix] flavicauda), found in South America, has a prehensile tail and is demonstrating how to use it. Photo by John Kricher.

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No Old World monkeys have prehensile tails, and they seem to do fine. Thus a prehensile tail, while adaptive to those that have evolved it, is not absolutely required to survive a life in the treetops.

Testing Adaptations Because they seem so obvious, adaptations are often inferred, and such inference may be true, but rigorous testing is the only way in which adaptation can actually be demonstrated. For example, orb-weaver spiders (family Araneidae) throughout the Neotropics and the temperate zone make large webs in which there are some areas of obvious, thickened, zigzag strands called stabilimenta (plate 8-14). Spiders use considerable energy to synthesize the silk for the web, especially the dense stabilimenta. Why should spiders invest in making stabilimenta? Are these conspicuous zigzag strands adaptive? The spiders that make stabilimenta are those whose webs remain intact throughout the daylight hours (many spiders make new webs each evening and take them down at dawn). Stabilimenta make the webs easily visible to humans, and biologists have hypothesized that they have the same effect on birds (which are also visually oriented). A flying bird will thus avoid an orbweaver spider’s web, saving the spider from having to remake a web damaged by a flying bird strike (which would yield no food for the spider, as birds are too big to capture and eat). Spiders that invest energy in making stabilimenta rather than risk having to start from scratch and make a whole new web would be less prone to bird accidents and damage from other animals. Therefore, stabilimenta could represent an adaptation for energy saving in an environment where birds pose a risk to the security of the web. As such, the hypothesis sounds plausible, but, without testing, it is just a story, an educated guess. How could it be tested? First, an observer could simply watch spider webs and note bird behavior. This was done, both in Panama and in Florida, and birds were observed to take shortrange evasive action when approaching webs with stabilimenta. Secondly, using webs that do not have stabilimenta, researchers altered some webs, adding artificial stabilimenta, and kept other webs without stabilimenta as controls. The webs without stabilimenta did not remain intact during the day, while those with stabilimenta generally did. Further direct observations

Plate 8-14. The web of this orb-weaver spider from Honduras displays prominent zigzag structures known as stabilimenta. Photo by James Adams.

implicated birds as the major threat to webs, though other large animals ranging from butterflies to deer could also be forewarned by the presence of stabilimenta. This work demonstrated the adaptiveness of stabilimenta. Not all traits need be adaptive. Organisms represent the combined effects of thousands of genes working in concert. The anatomy, physiology, and behavior of an organism represent various compromises imposed by the interactive effects of the genes that formed it. Thus, when looking at a trait, either anatomical or behavioral, it is essential to ask how the trait is likely to act to enhance fitness of the organism. At that point you might want to perform what Albert Einstein called a “gedanken experiment,” which means a thought experiment. Ask how you might test the hypothesis that you are observing an actual adaptation. Sometimes there is little choice but to do a thought experiment. Here’s an example. There are about 30 species of trees and vines in Costa Rica that produce large and fleshy fruits. These fruits drop from the tree, and most essentially just rot. That is puzzling, considering that fruits function to attract seed dispersers (chapter 10). So why are these fruits not consumed, their seeds dispersed? Some years ago Daniel Janzen and Paul Martin hypothesized that the large fruits represent what they called “ecological anachronisms,” fruits adapted to be dispersed by animals that are now extinct. During the Pleistocene, some 10,000 years ago, about 15 species of large (megafaunal) mammals

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(including horses and ground sloths) became extinct in what is now Costa Rica. These included an elephant-like group called the gomphotheres. Gomphotheres were in all probability essential dispersers of seeds from largefruited plants. As a result of gomphothere extinction, plants such as Guanacaste (Enterolobium cyclocarpum) were left without any agent of dispersal. Their fruits, once well adapted, are no longer as well adapted.

Adaptations in Environmental Context An adaptation must be viewed in the context of the environment. Consider the Brown-throated Threetoed Sloth (Bradypus variegatus; plate 8-15), a common species in much of the Neotropics. Charles Waterton, an eccentric British explorer who traversed the Amazon during the early 19th century, noted that the three-toed sloth appears poorly suited to survive when it is seen struggling over the ground. Tree sloths, however, do not normally perambulate on the ground, at least not today (large ground sloths once did, but they were well adapted by size and strength to function terrestrially). Today’s tree sloths are arboreal, skillfully and slowly moving upside down from branch to branch. In his well-known account Wanderings in South America (1825), Waterton wrote of the sloth, “This singular animal is destined by nature to be produced, to live and to die in the trees; and to do justice to him, naturalists must examine him in this his upper element.” Waterton then went on to describe in detail how well adapted the sloth is for its arboreal life. He put adaptation in context. For more on the wonderful world of sloths, see chapter 16.

Species The species is the basic unit of biology. When we survey an ecosystem, we typically measure the species richness (number of species) of trees, bromeliads, birds, moths, ants, tree frogs, or whatever groups we find to be of most interest. Thus it is important for ecologists to understand what, exactly, a species happens to be. So, what is a species? The question is complex, because it is often difficult to know whether organisms are members of the same species or are of different species. For sexually reproducing species, which is pretty much most of what you will see on a visit to the Neotropics,

Plate 8-15. The Brown-throated Three-toed Sloth is always slow moving but also always highly adept at navigating the tree canopy. It looks awkward when on the ground, but it is not adapted to be on the ground. Photo by Gina Nichol.

the question is answered by observing who breeds with whom. Male howler monkeys do not attempt to mate with female woolly monkeys. But they know another howler when it is time to form a pair bond and breed. The same is true of the colorful heliconius butterflies (chapter 11). A Heliconius erato will not mate with a Heliconius melpomene, even though the two species look remarkably similar. Organisms, including plants, are genetically adapted to accurately recognize others within their species. This profound reality forms the basis of the most widely used definition of a species: populations of actually or potentially interbreeding organisms. In this definition, called the Biological Species Concept (BSC), species designation is based on the notion that the organisms themselves will reveal to which species they belong through their reproductive habits. Under the BSC, the species category becomes a natural unit because the organisms to which it pertains actually recognize it themselves, at least in a manner of speaking. It is doubtful that a howler monkey knows it is a monkey, compared with, say, a Kinkajou or opossum, or if it appreciates that it is a mammal and not a bird. But its genetics make it competent to recognize and interact meaningfully with another howler monkey. The BSC is a theoretically strong definition, heuristically satisfying, but often difficult to apply in

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the field, especially in areas where populations are separated by allopatry. If two populations look alike and seem likely to be part of one species, but if these populations are separated geographically, how do we know if they could mate and produce fertile offspring? The answer ends up being a judgment call on the part of the “experts.” In spite of these obvious difficulties, the BSC has endured as the most widely applied definition of a species. Frequently, characteristics other than reproductive isolation, such as differences in anatomy, voice, and behavior, must be employed to assess whether or not two populations are one or two species. Today it is common for nucleic-acid sequencing, both with mitochondrial and with nuclear DNA, to be utilized to designate species, a clear modification of the BSC. Because of the precision available with molecular analysis of DNA (it is rather like reading a bar code), more and more populations that essentially look much alike and which were considered to be single species are now being split into multiple species. This has happened repeatedly with Neotropical species in recent years and remains an ongoing issue with many species’ populations. For one example, the Emerald Toucanet (Aulacorhynchus prasinus; plate 8-16), is a colorful and common bird in much of Central and South America. Based on differences in plumage, voice, and genetics among geographically separated populations, some ornithologists urge that this species be split, divided into as many as six separate species. The question of how many species of emerald toucanets there are remains, for the moment, unresolved.

Speciation as a Process The model for speciation involves several steps. First, because of a vicariance event, populations become geographically isolated. Second, geographic isolation prevents gene flow, allowing genetic differences between the isolates to accumulate with time. Natural selection acts to promote such genetic divergence. Finally, genetic differences between an isolate population and its parental population reaches a point where even if they should establish secondary contact, natural selection favors reproductive isolation between them, thus establishing them as separate species. It should be emphasized that this process does not require a great

Plate 8-16. The “blue-throated” subspecies of the Emerald Toucanet (Aulacorhynchus prasinus caeruleogularis) has been proposed as a separate species, to be split from the Emerald Toucanet. Photo by Gina Nichol.

deal of genetic difference to occur between the isolated populations, only enough to establish reproductive isolation. Speciation can be surprisingly quick.

Adaptive Radiation Patterns Adaptive radiation is common throughout nature and occurs when one type of organism evolves in such a way that it gives rise to many different species, each adapted to exploit a somewhat different set of environmental resources. Darwin discussed what came to be called adaptive radiation when he observed a group of small finches on the Galápagos Islands, a group that eventually bore his name, Darwin’s finches (Geospiza and other genera; plate 8-17). These small chunky black and brown birds appear similar but vary somewhat in body size and considerably with regard to bill size and shape. They share many traits in common, including how they construct their nests, and they are closely similar genetically, indicating that each species is derived from a common ancestor, which makes them what evolutionary biologists term a monophyletic group. In his account of the voyage of the Beagle, Darwin wrote of these birds, “Seeing this gradation and diversity of structure in one small, intimately related group of birds, one might really fancy that from an original paucity of birds in this archipelago, one species had been taken and modified for different ends.” Adaptive radiation abounds in the Neotropics. Two excellent examples can be found in Neotropical bats and tyrant flycatchers.

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Adaptive Radiation in Bats The basic bat is a marvel of adaptation. Bats are the only mammals capable of powered flight (excluding the unique species that invented airplanes and space shuttles). Bats appear in the fossil record as far back as the Eocene, arising approximately 60 million years ago. Their closest evolutionary relatives are insectivores, the moles and shrews. The most distinctive adaptation of bats is the modification of the forelimb (arm) as a wing, accomplished through elongation and enclosure of the arm and finger bones within a membrane of skin (plate 8-18). Like birds, bats have large hearts, light body weight, and high metabolism. While most birds are diurnal, all bats are nocturnal. In terms of species diversity, birds are much more species rich than bats; there are approximately 10,000 bird species in the world, compared with 1,240 bat species. Nonetheless, bats make up the second-largest order (Chiroptera) of mammals, surpassed only by the rodents. Bats in the American tropics are all members of the suborder Microchiroptera. Most visitors to the tropics have little idea of the true abundance and diversity of bats in the forests and surrounding habitats. Microchiropterans traditionally capture insect prey on the wing and avoid obstacles by using echolocation. They emit loud, high-pitched vocalizations (mostly inaudible to humans) that bounce off objects of approximately the same size as the wavelength of the emitted sound, thus providing the bat with an effective system of sonic radar for locating small nearby objects, such as flying insects. Most microchiropterans display very prominent pinnae, or external ears, that aid in receiving the echolocation signals, including those from inanimate objects such as tree branches. Microchiropteran bats usually have small eyes and presumably poor eyesight, relying instead on their incredible echolocation skills (plate 8-19). The nocturnal nature of bats makes them a challenge to study. Louise Emmons, in her book Neotropical Rainforest Mammals: A Field Guide (2nd ed., 1997) states that there are generally more species of bats in a Neotropical rain forest than all other mammals combined, and that bats make up 39% of all mammal species in the Neotropics. Researcher Bruce Miller has done years of work on the bat community in Belize using a computerized sounddetection system to detect vocalizations of free-flying bats, as well as direct capture of bats to document species present. Miller has been able to census bat diversity by recording the animals’ vocalizations on sonograms and has documented 84 bat species in Belize, a country about

Plate 8-17. The Large Ground Finch (Geospiza magnirostris) has a massive seed-crushing bill. It is one of the 14 Darwin’s finches, which have substantially diverged in bill characteristics. Photo by John Kricher.

Plate 8-18. The Neotropical Pygmy Fruit-eating Bat (Dermanura phaeotis) provides an example of bat external anatomy. Note the large ears and leaf-like nose, adaptations for the bat’s sonar system. The membranous wings are supported by the forearm (prominently visible) and the finger bones. A mammal, the bat is otherwise covered with hair. Photo by Bruce and Carolyn Miller.

Plate 8-19. The well-named Wrinkle-faced Bat (Centurio senex) displays large pinnae (external ears) and wrinkled facial skin, adaptations to enhance high-frequency sound detection. Note the small eyes. Photo by Bruce and Carolyn Miller.

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Plate 8-20. The Greater White-lined Bat (Saccopteryx bilineata) is typical of insect-foraging bats. It is commonly seen around dwellings and forms large colonies. Males court females in part by emitting a “song” audible to humans. Photo by Dennis Paulson.

Plate 8-21. The small fruit-eating Chestnut Short-tailed Bat (Carollia castanea) displays a leaf-shaped nose. The eyes of this species are relatively large, and thus it likely has good vision, helpful in locating fruit on a tree. Photo by John Kricher.

the area of Connecticut. Only 45 bat species regularly occur in the entire continental United States. The adaptive radiation of microchiropteran bats in the American tropics is nothing short of amazing. These animals evolved to feed on insects captured in the air using echolocation. Indeed, many species still feed in this “traditional” way (plate 8-20). However, there are also fruit-eating, nectar-eating, pollen-eating, fisheating, frog-eating, bird-eating, lizard-eating, mouseeating, bat-eating, and even blood-eating bats, and examples of all of these may be found in Neotropical forests. From an insectivorous ancestor (or ancestors) tropical bats have radiated into dramatically different feeding niches, taking advantage of the tremendous diversity of rain forest resources. Daniel Janzen and D. E. Wilson made a classic study of the pattern of bat diversity in Costa Rica and tallied a total of 103 species. Of these, 43 are insectivorous; 25 frugivorous; 11 nectarivorous; two carnivorous; one piscivorous (fish eating); three sanguivorous (blood feeders); and 18 feed on some combination from the above list. Among the insectivorous bats, some capture prey by aerial foraging and some by foliage gleaning.

Plate 8-22. The fishing Bulldog Bat in typical roosting posture (but on the gloved finger of a bat handler). Photo by Bruce and Carolyn Miller.

Aerial foragers catch insects on the wing, while foliage gleaners pick their prey from leaves, branches, and even the ground. The False Vampire Bat (Vampyrum spectrum) is a generalized carnivore. It captures sleeping birds as well as rodents and other bats, and is suspected of locating some of its prey by olfaction. Many bats have a keenly developed sense of smell. The False Vampire is one of the largest of the Neotropical bats, with a wingspread of approximately 75 cm (30 in). It has prominent ears, a long snout, a large “leaf ” nose, and long, sharp canine teeth. Its generally ferocious appearance misled people into believing it to be a vampire, which it is not. Flattened leaf-like noses are common among fruiteating bats as well as carnivores (plate 8-21). The flattened nose may be an adaptation aiding the bat with echolocation. These bats typically carry large food items and must therefore emit their sonar vocalizations through their noses rather than mouths. The leaf nose is thought to aid in focusing the signal. The widespread fishing Bulldog Bat (Noctilio leporinus; plate 8-22), is another excellent example of adaptive radiation. This species uses its sonar not to

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locate insects in the air but instead to locate fish just beneath the water’s surface. It gets the name Bulldog Bat from its flattened puffy face, with small eyes, short pointed ears, and prominent cheek pouches. It is a large bat, with a wingspread of 61 cm (24 in). It has long toes, with prominent, sharp claws. Using its sonar, the bat detects small fish and crustaceans breaking the surface of calm rivers and pools. It swoops down, gaffing the fish with its large well-clawed feet. It then transfers the prey to its mouth, where it stuffs it in its large cheek pouches and then grinds it up, bones and all. It is thrilling to watch Bulldog Bats feed, as they seem to scoop up prey unerringly, but you must hit the right conditions of a moonlit night, a quiet lake or pool, and, of course, the bats. Undoubtedly, the most notorious Neotropical bat species is the Vampire Bat (Desmodus rotundus; plate 8-23). This extraordinary animal feeds entirely on the blood of mammals such as tapirs and peccaries. In many areas Vampire Bats have prospered because of the presence of cattle and swine, both of which afford an easily accessible source of blood. Vampires fly from their roosting caves at night to locate prey. The bat finds its victim both by olfaction and vision. Remarkably agile (for a bat), the Vampire scurries over the ground on its hind legs and thumbs, and then climbs onto the sleeping animal. Using specialized incisors, the bat slices into the superficial skin layers and initiates bleeding. The cut is so sharp that the prey animal rarely awakens. The bat’s saliva contains an anticoagulant, so the blood flows freely while the bat feeds. The bat’s digestive tract is modified to deal with blood, which is extraordinarily high in protein. Vampires occasionally attack humans. I have seen Mayan people in Belize who have been bitten about the face and fingers by vampires. Fortunately for these people, none of the bats was a carrier of rabies, though in some places Vampire Bats are vectors for this serious viral disease. Vampires carrying rabies may show no symptoms themselves, and that indicates a long evolutionary relationship between the Vampire Bat and the rabies virus. Bats exhibit adaptive radiation not only in their diverse feeding behaviors but also in their choice of roosting sites. Bats normally roost upside down, using sharp claws on their feet to attach (plates 8-24–25). A bat spends approximately half of its life at the roost site, which is where most social interactions such as mating, rearing young, and food digestion occur. Bats may

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Plate 8-23. Vampire Bat, in the gloved hand of a skilled bat handler, showing its upper incisors, used to cut into skin and allow the animal to lap flowing blood. Photo by Bruce and Carolyn Miller.

Plate 8-24. These small leaf-nosed bats (family Phyllostomidae) are roosting beneath a big palm leaf. Photo by Sean Williams.

Plate 8-25. The ghost bats (Diclidurus spp.) are small white bats of South America whose ecology is poorly known. They are thought to feed mostly in the rain forest canopy. Photo by Kevin Zimmer.

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Plate 8-27. The Tropical Kingbird ranges from southern Texas south to central Argentina. It is displaying the typical posture of a foraging tyrant flycatcher, sitting in the open as it awaits an opportunity to snatch prey from the air. Photo by Bruce Hallett.

Plate 8-26. This group of Long-nosed (also called Proboscis) Bats (Rhynchonycteris naso) is roosting, as the species habitually does, in the open on a tree trunk along a stream. These bats, which are common and widespread throughout Amazonia, are often seen on river trips. They are known to rock back and forth like leaves hanging in the wind. If approached too closely they will fly off, resembling moths in flight. Photo by Kevin Zimmer.

be colonial or solitary roosters. Roost sites include caves, crevices, hollow trees, and even tree trunks (plate 8-26). Some bats roost in foliage, often modifying it to suit their needs. The small Sucker-footed Bat (Thyroptera tricolor) roosts in furled heliconia and banana leaves, attaching to the slick leaf with adhesive disks on the legs and wrist joints of the wings. The Honduran White Bat (Ectophylla alba), a small, all-white bat, goes one step further. It is one of several species to actually construct a tent, in this case out of a heliconia leaf. The white bat forces the huge leaf to droop by carefully chewing veins that are perpendicular to the midrib. The leaf is only partially chewed, and the result is a protective, thick tent in which a half dozen or so of these diminutive bats can cuddle in safety.

Plate 8-28. This Short-crested Flycatcher (Myiarchus ferox), seen from below, shows the light-colored lower mandible of the wide beak. The rictal bristles are obvious, protruding from the area where the beak meets the mouth. Photo by John Kricher.

Adaptive Radiation in Tyrant Flycatchers One of the most diverse families of birds in the world, Tyrannidae provides another example of the evolutionary process of adaptive radiation. There are 410 species of tyrannids, or tyrant flycatchers, all of which are confined to the New World. The vast majority of species occupy Central and South America, though some migrate to North America to breed. Tyrant flycatchers occupy all terrestrial habitats: towns, villages, rain forests, cloud forests, fields, scrub, savannas, marshes, and the South American puna, páramo, and pampa ecosystems (chapters 13 and 14). Though the name flycatcher is meaningful in most cases, the methods of capture and the types of insects and other arthropods taken vary

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tremendously among species. Many species feed on fruit as well as insects, and a few have diverged entirely from capturing insects and become primarily fruit eaters. As the name suggests, tyrant flycatchers catch flies. Their basic behavior is to sit still on a perch and sally forth in pursuit when a potential prey insect flies sufficiently close to capture. The flycatcher snaps up the prey in its beak and returns to the perch to consume it. The widespread and easily observed Tropical Kingbird (Tyrannus melancholicus; plate 8-27) provides an example of this classic flycatcher behavior, which is termed sally gleaning. Many flycatcher species are typical sally gleaners, flying from a perch to capture an insect, either in the air, on the ground, or on a leaf surface. Because flycatchers often sit on exposed perches, they are well suited to invade open habitats such as forest edges, riverbanks, and savannas. From the fundamental sally-gleaning technique, tyrannids have evolved many specializations. There are hawkers, ground feeders, runners, hoverers, water’s-edge specialists, perch gleaners, and fruit eaters. The ecological diversification among the hundreds of tyrannid species is really quite amazing. Body size and bill characteristics vary considerably among the tyrannid species, representing anatomical forms of specialization within the group. Generally speaking, tyrannid bills are dark above and may be lighter on the lower mandible, an adaptation to foraging in areas of high light intensity, where a dark upper mandible serves well to lessen glare. Bills are usually wide and somewhat flattened. Some flycatchers make an audible bill snap when they capture prey. Bills are usually bordered by hairlike feathers called rictal bristles (plate 8-28). These feathers, which are found on many bird species that capture insects on the wing, help the bird home in on its flying prey. Other birds that specialize in sallying for prey also have prominent rictal bristles, including the large nocturnal nightjars. Large-billed tyrannid species are common in the Neotropics, the bill size likely an evolutionary result of the greater availability of large arthropod prey. Interspecific competition within the group may also have provided selection pressures resulting in divergence of body size, bill, and feeding characteristics. A number of Neotropical flycatcher species that have yellow bellies and striped heads may present identification problems for birders, but body size and bill variation is strikingly evident among them. These differences in body size and bill shape not only help with species identification, they illustrate clearly what adaptive radiation really is. In

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Plate 8-29. The Great Kiskadee is a widespread species that is found from southern Texas to southern Amazonia. It is one of the largest of the tyrant flycatchers. Note the formidable bill, with a hook at the tip of the upper mandible. Kiskadees frequent many habitats and are known to eat diverse kinds of insects, as well as small vertebrates such as lizards and frogs. Photo by John Kricher.

Plate 8-30. The Lesser Kiskadee occupies much of the same range as the Great Kiskadee but is smaller and more slender and has a thinner bill. Photo by John Kricher.

Plate 8-31. No, not a Great Kiskadee. This is a Boat-billed Flycatcher. It is the size of a Great Kiskadee but has a much wider, thicker bill. Photo by John Kricher.

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Plate 8-32. The small (10 cm/4 in) Southern Bentbill (Oncostoma olivaceum) has a distinctly down-curved bill. It is a bird of the shaded forest understory. Photo by John Kricher.

Plate 8-33. The tiny Black-capped Pygmy-Tyrant, here holding nesting material, is found along humid forest borders in foothills and lowlands of western Colombia and northwestern Ecuador. Photo by Edison Buenaño.

Plate 8-34. The small (10 cm/4 in) Common Tody-flycatcher is found throughout much of the Neotropics and is commonly encountered in brushy areas and forest edges. Photo by John Kricher.

Plate 8-35. The Eastern Kingbird is a fiercely territorial migratory species nesting in eastern and central North America. It feeds on arthropods during its breeding season but switches primarily to fruit when wintering in parts of Amazonia. It loses its aggression toward conspecifics during migration and forms large flocks that migrate together. Photo by John Kricher.

Panama alone, seven of these similar species occur. The Great Kiskadee (Pitangus sulphuratus; plate 8-29) and the Boat-billed Flycatcher (Megarynchus pitangua; plate 8-31) are both large and similar in body size (23 cm/9 in), but the latter has a wider, more flattened bill. The Lesser Kiskadee (Pitangus lictor; plate 8-30) looks like a small version of the Great Kiskadee and differs from the very similarly sized Rusty-margined Flycatcher (Myiozetetes cayanensis) in having a somewhat longer bill. The other three species are similar: the Yellow-throated Flycatcher (Conopias parvus) and the Social Flycatcher (Myiozetetes similis), which differ only in minor facial characteristics, and the Gray-capped Flycatcher (Myiozetetes granadensis), whose gray cap helps distinguish it from the others. Other tyrant flycatchers also have distinctively shaped bills, and some of these species are very small in body size.

The Northern and Southern Bentbills (Oncostoma spp.; plate 8-32), both only 9 cm (3.5 in) long, have short but distinctly down-curved bills. The tiny spadebills (genus Platyrinchus), also only 9 cm long, have extremely wide, flattened bills. The Black-capped Pygmy-Tyrant (Myiornis atricapillus; plate 8-33), an inhabitant of lowland and foothill humid forests in Ecuador and Colombia, measures a mere 6.5 cm (2.5 in) in length. It has a small, straight bill adapted for taking tiny arthropod prey. The widespread Common Tody-flycatcher (Todirostrum cinereum; plate 8-34), which occurs in forest edges and disturbed areas, has a long, flattened bill. These present but a small sampling of the range of beak diversity evident in the tyrant flycatchers. Some flycatchers switch their diets regularly, and others are basically opportunistic, switching according to the

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Plate 8-36. The Cattle Tyrant is primarily a ground-dwelling tyrannid flycatcher that inhabits open grassy areas such as cattle pastures. Photo by John Kricher.

Plate 8-37. The White-headed Marsh-Tyrant is a common inhabitant of marshes throughout much of the Neotropics. Photo by John Kricher.

Plate 8-38. The Pied Water-Tyrant, like the White-headed Marsh-Tyrant (plate 8-37), specializes in foraging along the edges of freshwater marshes. Photo by John Kricher.

Plate 8-39. The spectacular Fork-tailed Flycatcher migrates in sometimes immense flocks. It is fairly common in open areas throughout Central and South America. Photo by John Kricher.

relative abundances of various insect prey. One seasonal and dramatic switch is seen with the Eastern Kingbird (Tyrannus tyrannus; plate 8-35). One of 32 tyrannid species that migrate to breed in North America (returning to winter in the Neotropics), the Eastern Kingbird feeds on insects on its summer breeding grounds. However, when on its wintering grounds in southwestern Amazonia it feeds mostly on fruit, forming large flocks that wander nomadically in search of fruiting trees. Another flycatcher, one that resides year-round in the Neotropics, has evolved a fully fruit-based diet. The nondescript Ochre-bellied Flycatcher (Mionectes oleagineus) is an abundant forest flycatcher, widespread in the region. Its inordinate numerical abundance compared with other tyrannids may be due to its diet shift from arthropods to fruit, which is an abundant

and easily “captured” resource. This bird is described in more detail in chapter 10. Overall, the ability of varied tyrannids to find food in virtually all habitats has likely been a major factor promoting speciation within the group. Species have specialized on certain types of arthropods and other food, captured in distinct ways. This tour of flycatcher diversity has only scratched the surface. In plumage and habitat as well, some of these birds show remarkable diversity. The widespread Cattle Tyrant (Machetornis rixosa; plate 8-36) inhabits open fields and grassy areas as well as disturbed areas and pastures (hence the common name). It typically forages on the ground. The White-headed Marsh-Tyrant (Arundinicola leucocephala; plate 8-37) and the Pied Water-Tyrant (Fluvicola pica; plate 8-38) are two tyrannids that are common in marshes.

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The spectacular Fork-tailed Flycatcher (Tyrannus savana; plate 8-39), which is an austral migrant (meaning that it migrates north from its breeding grounds in southern South America), forages in open areas and is a skilled aerialist as it pursues flying insects. One of the most remarkable of the group is the well-named Amazonian Royal Flycatcher (Onychorhynchus coronatus; plate 8-40), which can raise an array of feathers on its head to form an impressive crest.

Speciation in the Neotropics The usual precursor to speciation is vicariance, the occurrence of physical barriers that fragment populations and prevent gene flow. Mountains, rivers, deserts, savannas, all represent possible barriers between rain forest sites. Other factors, most notably climate changes, can fragment species’ ranges and create vicariance (see the refugia discussion in “Time, Endemism, and Refugia,” below). Should a mountain be formed by uplifting of earth’s crust, as has happened extensively in the Andes Mountains, which extend all the way from Trinidad and Venezuela to Tierra del Fuego in South America, what was once a contiguous area of forest will be fragmented by the mountain range, with all its concomitant physical complexity such as separated valleys and climatic differences. Individuals on one side of a mountain, or in an isolated valley, or even at various elevations on the mountainside are prevented from mating with other populations because they cannot easily reach them. Once populations are separated by geographic factors, there is the strong possibility of genetic divergence between the fragmented populations over time. For instance, a population on the western side of a mountain range may be subjected to different selection pressures than a population on the eastern side of the range. Each population will be selected for somewhat different characteristics, and thus for different genes, and genetic differences will result from one population to another. Since vicariance prevents exchanging of genes, fragmented populations diverge. Because of the Andes, much of South America remains geologically active. This mountain chain, which has been uplifting since at least the Mesozoic era and became particularly active during the Cenozoic era (approximately 65 million years), is responsible for the initial creation of diversified habitats as well as for providing numerous

Plate 8-40. One of the most amazing of the tyrant flycatchers, the forest-dwelling Amazonian Royal Flycatcher, rarely displays its extraordinary head feathering when viewed in the field. It likely is used only in displays to other birds. Note the widely flattened bill, prominent rictal bristles, and the large eyes. Photo by Andrew Whittaker.

Plate 8-41. A Brazilian Tapir peering out from its typically dense understory habitat. Photo by Sean Williams.

Plate 8-42. The Brown-backed Chat-Tyrant (Ochthoeca fumicolor) is a member of the chat-tyrant species complex of the Andes and of the family Tyrannidae. It occurs near and above tree line and is one of the most widely distributed of the chat-tyrant species along the Andes. Photo by Edison Buenaño.

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climatic and physical barriers that greatly enhance geographic isolation among populations. More recently, approximately 20 million years ago, additional uplift events affected dispersal patterns, isolating ecological communities and stimulating evolution. Geologists have determined that elevation changes throughout the history of the Andes have occurred in short time spans, from 1 to 4 million years long, and that the mountain chain remained stable for long intervals in between such times of rapid change. The topography of the central Andes is complex, consisting of the Eastern and Western Cordilleras separated by an expansive altiplano (high plain). This complexity makes the Andes chain a veritable engine driving speciation. For example, Baird’s Tapir (Tapirus bairdii) is found in lowland forest only on the western side of the Andes, extending into Central America as far north as tropical Mexico. The similar Brazilian Tapir (T. terrestris; plate 8-41) occurs only on the eastern side of the Andes, occupying the entire Amazon Basin. The mountains geographically isolate these two species and likely provided the main factor in the initial split of the ancestral species into isolated populations. Finally, there is a third Neotropical species, the Mountain Tapir (T. pinchaque),

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which, as the common name suggests, inhabits montane (or mountainous) forests at mid to high elevations of the Central and Eastern Cordilleras of the Andes, in Colombia and Ecuador. The Mountain Tapir is isolated both by range and elevation from the other two species. Chat-tyrants (genus Ochthoeca) are common insectivorous birds in the huge tyrant flycatcher family (Tyrannidae; discussed above). Currently eight species are recognized within the genus. Chat-tyrants have a vicariant distribution along the Andes from Colombia to Bolivia: one group of species occurs on the western side of the Andes, and the other is found on the eastern side. All the birds of this species complex are closely related and phenotypically similar (plate 8-42). Such a pattern has arisen from isolation and subsequent genetic divergence of local populations at various ranges and elevations within the Andes complex. With the rise of the Andes Mountains, the Amazon River began its flow from west to east. The massive Amazon and its numerous wide tributaries have served to isolate tracts of forest and savanna; given the sedentary nature of many animal populations in Amazonia, the rivers have probably served as important forces of geographic isolation. The width of the Amazon

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Figure 8–3. The Amazon River is a barrier that isolates two species of highly similar antbirds, the Dusky Antbird, which occurs on the north side of the river, and the Blackish Antbird, on the south side. Redrawn from Haffer 1985. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

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and its tributaries is sufficient to isolate populations of birds whose individual members are reluctant to cross such a wide expanse of water. Jürgen Haffer (1985) documented that the Amazon River effectively isolates two similar species of antbirds (fig. 8-3). The Dusky Antbird (Cercomacra tyrannina) occurs north of the Amazon, while the similar Blackish Antbird (C. nigrescens) occurs south of the river. Both species occur together only along a section of the northern bank of the river, but here the Blackish inhabits wet várzea forests, and the Dusky favors second-growth vegetation of the terra firme forest. A similar pattern is evident in the distribution of some curassow species (family Cracidae).

Time, Endemism, and Refugia How does the high diversity within tropical regions relate to geologic time—to long periods when speciation might exceed extinction? When South America is compared with other major tropical regions, we find that bird species richness and plant species richness are unequivocally highest in South America. But how did that happen? What factors are responsible? South American species richness, because of how extreme it is, poses vexing questions for evolutionary biologists and biogeographers. Since the 1970s, a debate has been ongoing between those who believe most speciation in South America is recent, dating primarily to events in the Pleistocene (1.64 million to 10,000 years ago) and immediately before, and those who argue that the data do not support such assertions and that much of the speciation occurred millions of years before the Pleistocene. It is unlikely that the equatorial tropics were climatically stable and constant throughout the Pleistocene, undisturbed by the giant glaciers bearing down upon northern temperate areas. Thomas Belt, in 1874, discussed possible effects of northern glaciation on the tropics. More recently, studies by Jürgen Haffer, Ghillean Prance, and Paul Colinvaux have, in various ways, examined geomorphology (the historical development of present landforms), paleobotany (the study of past patterns of plant distribution), and biogeography, and collectively suggest that dramatic changes occurred in Amazonia during the Pleistocene. One hypothesis to account for vicariant events leading to widespread speciation states that during Pleistocene glacial advances in northern latitudes, the tropics became cooler and drier. During part of the

Pleistocene, temperature in the Ecuadoran foothills, east of the Andes, was 4–6° C (7–11° F) cooler than at present. The cooling altered and shifted the distribution of ecosystems (warming is doing the same thing today). Ecosystems such as dry forests and open savannas enlarged, and moist forests contracted. Large continuous tracts of lowland rain forest were fragmented into forest “islands” of varying sizes surrounded by “seas” of savanna or dry woodland. This scenario, in which savanna expansion created vicariance among forest tracts, is called the refugia (or refuge) model. Because of the repeated shrinking and fragmenting of forests, forest organisms became repeatedly geographically isolated from populations in other forest areas. The Amazon Basin became a climatically dynamic “archipelago” of variably sized rain forest islands (refuges, or refugia) that promoted speciation among plants and animals. A classic study by Jürgen Haffer (1974) based on the current distribution of certain kinds of birds postulate that at least nine major and numerous smaller forest island refugia were present in Amazonia during the Pleistocene. The implication is that many taxonomic groups went through periods of rapid speciation because there were repeated episodes of rain forest shrinkage and expansion. During interglacial periods forests expanded and secondary contact was established between newly speciated populations, explaining why so many extremely similar species can be found today in Amazonia. The refugia model has been the subject of considerable debate. Evidence supporting it is based mostly on present distribution and diversity patterns. Ghillean Prance has examined woody plant diversity, for example, and concluded that 26 probable forest refugia existed for these plants. Other studies have supported the refugia concept for groups such as primates, birds, and heliconid butterflies. But it is important to note that centers of endemism, the presumed Pleistocene refuges, do not convincingly overlap among taxa, a reality that lessens support for the refugia model. Supporters of the refugia model respond that different taxa have different dispersal powers and different generation times and thus would be expected to differ somewhat with regard to the degree of regional endemism. Paul Colinvaux pointed out that at least one study showed that refugium locations for plants coincide with areas in which sampling of plants for herbarium specimens has been historically most intense. This, of course, would suggest that the refugia, at least some of them, are artifacts of uneven sampling effort.

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Analysis of pollen taken from sediments of Amazon lakes in Ecuador and Brazil does not support the refugia model. Pollen is resistant to decomposition, particularly in anaerobic sediments of lake basins. As pollen accumulates year after year it forms a vertical pollen profile, a historical indicator of which plant species were present in a region. In studies, lake sediments are cored, and pollen at the bottom of the core is oldest, pollen at the top youngest. Pollen profiles from various Amazonian lakes showed that although the region likely cooled by about 5° C (9° F), it remained fully forested, not broken up by savanna. An analysis of Amazonian sedimentary patterns conducted by Georg Irion suggests that there was no substantive climatic change or reduction in forest cover in Amazonia during the Pleistocene. But the data indicated that sediment patterns were not stable throughout Amazonia, and that strong oscillations occurred throughout the Pleistocene in the distribution of land, water, floodplain forests, and terra firme (areas of forest and savanna that occur off the riverine floodplain). Sea level changes are thought to have led to the alternation of huge Amazonian lakes with strong valley cutting, geological events that would presumably have a strong impact on flora and fauna. This view sees the Amazonian rain forest as subject to vicariance, though not necessarily reduced to scattered refugia. Another objection to the refugia model focuses on the ages of species. The refugia model argues that speciation has been recent, from about 6 million years ago. Molecular analysis (unavailable when the refugia model was proposed) indicates that many bird species in Amazonia originated well before the Pleistocene. A complex of frog species of the genus Leptodactylus exhibits high species richness dating to before the Pleistocene. Much speciation appears to have occurred in the mid-Tertiary period, long before the Pleistocene. Studies of plant fossils and subsequent analyses indicate that the high plant species richness traces back to 52 million years ago, in the Eocene epoch of the Tertiary period. That’s a long time ago. At present the evidence does not strongly support the original refugia model as the “species pump” in tropical regions. But what has been learned indicates that the Neotropics have certainly changed over geologic time, changes that range from dramatic mountain uplifts to shifting patterns of the Amazon and its massive tributaries. These events could very well have promoted speciation in many groups. And it certainly looks as if they did.

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The Great American Faunal Interchange The Panamanian land bridge, now called the Isthmus of Panama, formed approximately 3 million years ago because of a combination of uplift of the northern Andes and a global drop in sea level, of perhaps as much as 50 m (165 ft), a result of the increasing size of the polar ice caps. Thus it was just prior to the onset of the so-called ice age that the continents of North and South America were no longer isolated by water. The Panamanian land bridge profoundly altered the ecology of South America, much more so than it did that of North America. Consider that the faunas of North and South America had evolved independently of each other for at least 40 million years, but their mingling, once the land connection was made, was completed within a mere 2 million years. Once the land bridge formed, various species of South American animals moved northward, beginning as early as 2.5 million years ago, literally walking, generation by generation, to North America. These included two armadillo species (plate 8-43), a glyptodont (a kind of giant version of an armadillo almost the size of a very compact car), two species of large ground sloths, a porcupine, a large capybara, and one phorusrhacoid bird (a large flightless bird with an immense predatory beak that overall resembled an ostrich from hell). Glyptodonts looked like gigantic armadillos, covered with bony armor, but their tail (depending on the species) sometimes terminated in a mace-like club (plate 8-

Plate 8-43. Ancestors of the Nine-banded Armadillo (Dasypus novemcinctus) emigrated from the Neotropics across the Isthmus of Panama land bridge and continue to expand northward in North America both in the Southeast and the Midwest. The species remains common and widespread today throughout the Neotropics. You can easily count the nine bands in this photo. Photo by John Kricher.

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Plate 8-44. Plate 8-45. Plates 8-44 and 8-45. Skeletons of a glyptodont (8-44) and a giant ground sloth (8-45), both part of a display at the Harvard Museum of Comparative Zoology, Cambridge, MA. These bulky creatures managed to invade North America during the great faunal interchange. Photos by John Kricher.

44). Ground sloths, now all extinct, were robust, large terrestrial sloths with long claws (plate 8-45). They were probably largely herbivores, feeding on foliage, though some have suggested they may have been partially meat consumers. As you might guess, ground sloths were closely related to the much smaller tree sloths of the Neotropics, a point not lost on Charles Darwin when he first examined fossil ground sloth bones during the voyage of the Beagle. Capybaras belong to the same rodent subgroup (Caviomorpha) as chinchillas and guinea pigs. One of the two extant capybaras, Hydrochoeris hydrochaeris, abundant in parts of South America, is the world’s largest rodent (chapter 12). Phorusrhacoid birds, now all extinct, have earned the nickname “terror birds.” Some stood almost as tall as a human being. They were flightless but could move quickly, running on long legs. Their huge raptor-like beaks were easily capable of killing small to moderate-size mammals. At the time they lived, they were among the top carnivores of South America. Other northward invaders included Didelphis virginiana, the familiar Virginia Opossum (plate 8-46), North America’s only marsupial mammal. Opossums invaded approximately 1.9 million years ago and continue to expand their range northward today. Finally, at least one species of toxodon, an odd, husky mammal that belonged to a group known as the notoungulates, came north from South America. Toxodons were bulky mammals whose appearance suggests a cross between a cow and a hippopotamus (plate 8-47). The collective impact of the South American invaders was modest at

best. Only armadillos and opossums remain, both of which are thriving. The ground sloths were probably killed by humans as the human population spread southward from Siberian Beringia. The other groups just drop out of the fossil record. Many North American animals made the reverse trek, walking across the land bridge to South America. Their impact on the native fauna appears to have been substantial. The list of invaders includes skunks, peccaries, horses, dogs, saber-toothed and other cats, tapirs, camels, deer, rabbits, tree squirrels, bears, and an odd group of elephant-like mammals, the gomphotheres. Add to this list the field mice, or cricetid rodents— whose travel route to South America is still debated, but

Plate 8-46. The familiar and highly adaptable Virginia Opossum, here enjoying the remains of some cat food on the author’s deck in Massachusetts, first immigrated to North America about 1.9 million years ago and has been spreading northeastward ever since. Photo by John Kricher.

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Plate 8-47. The skull of a toxodon, on display at the Harvard Museum of Comparative Zoology, Cambridge, MA. Photo by John Kricher.

Plate 8-48. Smilodon, the saber-toothed cat, was a species that invaded South America during the faunal interchange, perhaps contributing to the extinction of Thylacosmilus, the catlike sabertoothed marsupial. This skeleton is from the Carnegie Museum of Natural History, Pittsburgh, PA. Photo by John Kricher.

who have since radiated into 54 living genera—and you begin to see why the effect of North American mammals on South American ecosystems was so great. Various amphibians, reptiles, and bird groups also migrated in either direction, some to the north, some to the south. The faunal interchange altered ecological communities on both continents, producing combinations of species that had never before been together. The effect of the North American influx on the South American mammal fauna was so significant that almost half of the current mammalian families and genera of the Neotropics originated in North America. Thus within a period of 3 million years, the Neotropical mammalian communities were significantly restructured. It is unclear how the influx of North American mammals, as diverse as it was, affected abundances of South American mammal species. For example, many hoofed mammals invaded from North America. However, their ecological counterparts in South America, the litopterns (a group that included the Macrauchenia, an animal that looked like a camel with an elephant-like proboscis) and notoungulates, were declining in numbers and diversity before the northern camels and horses arrived. Perhaps the North American ungulates were the primary cause of the extinction of the various South American groups. Among predatory mammals, the large, wolverine-like South American borhyaenoids were essentially outcompeted by the

terror birds, not by mammalian invaders from the north. However, the phorusrhacoid terror birds may have eventually lost out to invading mammals. There is really only one relatively clear-cut example of what appears to have been direct competition between a North American species and a South American species. This is the case of the South American saber-toothed catlike animal Thylacosmilus and the North American saber-toothed cat Smilodon (plate 8-48). The animals bore a striking anatomical similarity but were unrelated, representing an example of convergent evolution. The extinction of Thylacosmilus coincides closely with the arrival of Smilodon, which crossed the land bridge into South America from the north. Many of the extinctions of large mammals on both continents are probably explainable by the proliferation of humans during the Pleistocene and not attributable to competition among the animal groups themselves. The Great American Faunal Interchange demonstrates that ecological communities are subject to major changes over time. The mixing of the two faunas created new communities. One of the most challenging pursuits in ecology, one related both to long-term biogeographic history and to present ecological interactions, is our quest to understand how various factors, including interspecific interactions, structure communities. And yet another major puzzle has to do with biodiversity. Why are there so many species in the tropics? But that’s a question for chapter 9.

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Chapter 9 Why Are There So Many Species? Plants: Uniquely High Species Richness While looking around inside a Neotropical rain forest one cannot help but wonder just how many species of plants and animals inhabit that complex ecosystem (plate 91). Life is obviously abundant and diverse, but so many animal species are secretive and cryptic, and many of the plants look pretty much alike. The term species richness, or biodiversity, refers to the number of different species of any given taxon inhabiting a specified area. Thus we speak of the species richness of flowering plants in Amazonia, or ferns in Costa Rican montane forests, or birds in Belize, or mammals in Río Negro igapo forest, or beetles in the canopy of a single Kapok Tree, or whatever. High species richness among many different taxa is one of the most distinctive features of tropical forests worldwide and Neotropical lowland forests in particular. In a temperate forest it is often possible to count the number of tree species on the fingers of both hands (though a toe or two may be needed). Even in the most diverse North American forests, the lush southeastern Appalachian cove forests, only about 30 species of trees occur in a hectare (10,000 m2, or about 2.5 ac). In the tropics, however, anywhere from 40 to 100 or more species of trees are typically found per hectare. Indeed, one site in the Peruvian Amazon surveyed by the late and legendary botanist Alwyn Gentry (1988) was found to contain approximately 300 tree species per hectare. That’s a lot. Brazil has been estimated to have somewhere around 55,000 flowering plant species. A recent survey estimates that there are 352,000 flowering plant species in the world. Therefore Brazil contains about 16% of the world’s flowering plants. Gentry (1982) estimated that approximately 85,000 species of flowering plants occur in the Neotropics, very nearly 25% of the world’s total. That estimate was made in 1982 and is likely higher now, as more species are being discovered and described. In any case, this is roughly double the richness of tropical and subtropical Africa, about 1.7 times that of tropical and subtropical Asia, and five times that of North America. British naturalist Alfred Russel Wallace, codiscoverer with Charles Darwin of the theory of natural selection (chapter 8), commented upon the difficulty of finding two of the same species of tree near each other in the tropics. Wallace (1895) stated:

If the traveller notices a particular species and wishes to find more like it, he may often turn his eyes in vain in every direction. Trees of varied forms, dimensions and colour are around him, but he rarely sees any one of them repeated. Time after time he goes towards a tree which looks like the one he seeks, but a closer examination proves it to be distinct. As Wallace observed, though richness is high, the number of individuals within a single species often tends to be low, which is another way of saying that rarity is usual among many species in the lowland tropics. Though some plant species are abundant and widespread (for example, Kapok Tree), many are not, existing in small numbers over extensive areas. The concept of identifying a forest type by its dominant species, which works well in the temperate zone (e.g., eastern white pine forest, beech-maple forest, redwood forest), is much less useful in the tropics. Exceptions do occur. On the island of Trinidad one can visit a Mora forest, where the canopy consists almost exclusively of a single species, Mora excelsa, a tree that can reach heights of 50 m (165 ft). The understory is also dominated by Mora saplings. However, examples of such low-diversity forests are extremely rare in the Neotropics.

Patterns of Plant Species Richness Within the Neotropics, plant species richness, though high, is variable. In a classic 1975 study Dennis Knight, working on Barro Colorado Island in Panama, found an average of 57 tree species per 1,000 m2 (0.25 ac) in mature forest and 58 species in young forest. Knight found that in the older forest, when he counted 500 trees randomly, he encountered an average of 151 species. This species richness is far higher than it would be at higher latitudes. In the younger forest, he encountered an average of 115 species in a survey of 500 trees. Barro Colorado Island field station has long been a bastion of plant demographic studies. Back in the early 1980s Stephen Hubbell and Robin Foster established a 50 ha (about 125 ac) permanent study plot in oldgrowth forest at BCI. They surveyed approximately 238,000 woody plants with a stem diameter at breast height (dbh) of 1 cm (0.39 in) or greater and found 303 species: 58 shrub species, 60 understory tree species, 71 mid-story tree species, and 114 canopy and emergent tree species.

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Plant species richness peaks in Amazonia. Alwyn Gentry, working in upper Amazonia and Chocó (Colombia), found between 155 and 283 species of trees of greater than 10 cm (4 in) dbh in a single hectare (a mere 2.47 acres). When he included lianas of greater than 10 cm dbh, he found that the total increased to between 165 and 300 species. In contrast, a research group under the leadership of Ghillean Prance found 179 species of greater than 15 cm (6 in) dbh in a 1 ha plot near Manaus, on a terra firme forest characterized by poor soil and a very strong dry season. The lower species richness was likely a result of the seasonality and the soil quality. An inventory compiled in 1990 by Foster and Hubbell for BCI surveyed all vascular flora (trees, shrubs, herbs, epiphytes, lianas, but excluding introduced weedy species) and found 1,320 species from 118 families. By comparison, the total number of vascular plant species documented by Barry Hammel to occur at La Selva Biological Station in nearby Costa Rica totaled 1,668 species from 121 families. Let’s compare these totals, both from Central America, with those from Amazonian rain forests.

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A floodplain forest on rich soils at Cocha Cashu Biological Station along the Río Manú, a whitewater tributary of the vast Rio Madeira in southeastern Peru, was found by Robin Foster to contain 1,856 species (in 751 genera and 130 families) of vascular plants. At Reserva Ducke, a forest reserve on poor soil near Manaus, Brazil, in central Amazonia, Ghillean Prance found a total of 825 species of vascular plants from 88 families. This lower diversity, as above, speaks to the poor soils. The two contrasting Amazonian sites show a correlation of diversity and soil quality. Comparing Central American sites with Amazonian sites reveals other important differences. Tree species richness is greater in Amazonia but the richness of epiphytes, herbs, and shrubs is greater in Central America. Gary Hartshorn and Barry Hammel found 23% of all vascular plant species at La Selva to be epiphytes, the highest percentage recorded among the closely studied sites. The most species rich of the four sites was Cocha Cashu, located on fertile várzea soils in western Amazonia. A total of 29 plant families that were present at BCI, La Selva, and Cocha Cashu were

Plate 9-1. How many plant species, to say nothing of how many unseen animal species, are part of this panoramic view of an Ecuadorian rain forest? Photo by John Kricher.

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absent from Reserva Ducke, presumably because of the poor soil conditions at that particular site. The similarities among these four geographically separated forest sites are as compelling as the differences. The dozen most well represented plant families were essentially the same in each of the sites. The legume family (Fabaceae), for instance, had the most species richness of any family at BCI, Cocha Cashu, and Ducke, and was the fifth most species-rich family at La Selva. Of the total of 153 vascular plant families represented in at least one of the four sites, 66 (43%) were represented at all four sites, a high overlap. What this suggests is that essentially the same array of plant families has speciated throughout the vast area of the Neotropics.

Animals Also Exhibit High Species Richness The prodigious number of plant species is rivaled by the amazing species richness of many animal groups. Insects, spiders, birds, toads, frogs, tree frogs, and mammals exhibit amazingly high species richness in the Neotropics. Colombia is estimated to contain nearly 1,900 bird species, while Ecuador has approximately 1,600, and Peru has 1,800. In comparison, there are approximately 800 bird species found in all of North America north of Mexico. At Cocha Cashu Biological Station in Amazonian Peru, an area of approximately 5,000 ha (12,355 ac), the total bird species list tops 550. At La Selva Biological Station in Costa Rica, an area of approximately 1,500 ha (3,700 ac), 410 species of birds have been found. Yes, you read that correctly. At La Selva the total bird list equals about half the number of species found in all of North America. Observers at Explorer’s Inn Reserve in southern Peru have seen about 575 bird species within an area of approximately 5,500 ha (13,590 ac). This area may contain more species of birds per hectare than any other in the world. Why do more bird species occupy the Neotropics than the temperate zone? The general answer is rain forest. In a study done by Eliot Tramer in 1974 that looked at bird species richness within grids of equal sizes that covered North America, Central America, and northern South America, it was obvious that bird species richness took a major jump when the grid contained rain forest. Simple as that. Want birds? Visit rain forest (plate 9-2).

Plate 9-2 The Jocotoco Antpitta (Grallaria ridgelyi) was discovered only in 1997. Its range is restricted to a few areas in southeastern Ecuador and Peru. A fairly specialized species, it inhabits wet forests at elevations between 2,250 and 2,700 m (7,380–8,860 ft). At some of these places naturalist-guides have acclimated these birds to come for earthworms, so ecotourists and birders can glimpse this unique species. Look carefully at the photo and notice the earthworms used to coax the normally secretive bird into the open. Photo by Edison Buenaño.

Amphibians are represented in the Neotropics mostly by anurans, the toads, frogs, and tree frogs, and there are lots of species (plate 9-3). At one site in the Ecuadorian Amazon, William Duellman found 81 species of frogs. That is exactly how many species occur in all of the United States. Indeed, Duellman collected 56 different species on a single night of sampling and reported that it is routine to find 40 or more species in areas of rain forest as small as 2 km2 (0.75 mi2). Insect species richness in the Neotropics is staggering (plates 9-4–5). For Costa Rica, not a large country, Philip DeVries describes nearly 550 butterfly species. At La Selva alone, 204 butterfly species have been identified. At BCI in Panama 136 species have been documented. At Explorer’s Inn Reserve in southern Peru, a staggering 1,234 butterfly species have been identified from an area about 2 km2 (0.75 mi2) within the reserve. In an oft-cited study from 1987, Edward O. Wilson reported collecting 40 genera and 135 species of ants from four forest types at Tambopata Reserve in the Peruvian Amazon. Wilson noted that 43 species of ants were found in one tree, a total approximately equal to all ant species occurring in the British Isles. In Panama in the early 1980s, Terry Erwin famously used a fogging technique to extract insects from the forest

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Plate 9-3. The Canal Zone Tree Frog (Hypsiboas rufitelus) is one of many species of tree frogs that occur in the Neotropics. Note the enlarged toe tips, adapted to attaching to vertical surfaces. Photo by Dennis Paulson.

Plate 9-4. This butterfly, Creonpyge creon, belongs to a group called the firetips. Photo by Dennis Paulson.

Plate 9-5. Membracis bucktoni is a unique treehopper from Amazonia. Insect diversity is amazing, as you will see when you start to look carefully in a rain forest. Photo by Dennis Paulson.

Plate 9-6. This colorful insect is a leaf beetle in the family Chrysomelidae. Just this one family in the beetles order, Coleoptera, is thought to contain between 37,000 and 50,000 species. Add to that all the other coleopterans, and add to that all the other insect orders, and—wow! Photo by Dennis Paulson.

canopy. Fogging involves the spraying of insecticide into the canopy of the tree and subsequently collecting (on cloths spread on the ground) the insects and other arthropods that drop from the tree. (Fogging was part of the plot of a 1990 film titled Arachnophobia. Don’t see it if you are easily frightened by spiders.) Erwin, sampling 19 trees, all of the species Luchea seemannii, identified approximately 1,200 species of beetles (including weevils) in his samples. Erwin noted that

there were about 70 tree species per hectare (2.47 ac), and using that estimate, judged that about 13.5% (163) of the beetles were host-specific, occurring only in Luchea. He then calculated that perhaps as many as 11,410 hostspecific beetles could be found within a hectare (70 × 163). He then multiplied this figure by the number of different tree species present in the global tropics and concluded that the potential world species richness of beetles alone was over 8 million! Since beetles are estimated to represent

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approximately 40% of all tropical terrestrial arthropod species (including spiders, crustaceans, centipedes, and millipedes, as well as insects), Erwin suggested that the total arthropod species richness of the tropical canopy might be as high as 20 million, and the figure climbs to 30 million when the ground and understory arthropods are added. Note that Erwin’s estimates are indeed that, based on assumptions about host specificity, a characteristic that may vary considerably among species of trees and other plants. Many tropical entomologists take a much more conservative view of insect species richness and have been critical of Erwin’s estimates. Insects, as a group, remain rather poorly documented as to their actual species richness, and future research is needed. Without question, numerous species await discovery. But one thing is certain whether one chooses to challenge Erwin or not: there are multitudes of arthropod species throughout the world’s tropics (plate 9-6).

Species Richness and Diversity Gradients Most major taxa, including flowering plants, ferns, mammals, birds, reptiles, amphibians, fish, insects, spiders, millipedes, snails, and bivalve mollusks (such as clams and mussels), all have their greatest number of species in the tropics. Some tropical rain forests contain so many species that they exhibit what ecologists have termed hyperdiversity. Why are tropical ecosystems, and rain forests in particular, home to so many species? Charles Darwin realized that species numbers per unit area tend to decline strongly with latitude as one travels away from the equator, a point he noted in chapter 3 of On the Origin of Species. Alexander von Humboldt also observed this trend for plants and believed it to be related to reduced tolerance for cold in higher latitudes. The reduction in diversity with increasing latitude is termed a latitudinal diversity gradient or LDG. The evolutionary biologist Theodosius Dobzhansky, in a seminal paper titled “Evolution in the Tropics” (1950), noted that only 56 species of breeding birds occurred in Greenland, while New York had 195 breeding species (Dobzhansky’s figures would need updating today but are still very much in the ballpark.) Dobzhansky noted that Guatemala had 469, Panama 1,100, and Colombia 1,395 breeding bird species. Breeding bird diversity increased by almost 25 times from Greenland in the Arctic to Colombia on

the equator. Regarding snakes, Dobzhansky noted that 22 species occurred in all of Canada, whereas 210 were found in Brazilian forests and savannas. Dobzhansky suggested that since plants and animals are all products of evolution, any differences between tropical and temperate species result from differences in evolutionary patterns. Selection pressures vary with latitude and, for some reason, result in more species being in the tropics. But, as is often the case in ecology, the devil is in the details. Just what evolutionary selection pressures and other forces might account for the greater richness and variety of the tropical fauna and flora, compared with those of temperate and polar lands? How does life in tropical environments influence evolutionary potentialities? One possibility is that speciation rates exceed extinction rates in tropical regions, thus allowing an incremental buildup of species richness with time. There are other possibilities as well. For example, tropical rain forests, because they remain warm and wet throughout the year, fix more photosynthetic energy per unit area than other ecosystems. Does more energy somehow translate to greater species richness? If so, how? Is high plant productivity essential to species richness? There is high structural complexity in rain forests. Might this greater three-dimensional space not account for greater species richness in groups such as birds, mammals, and arthropods? Dobzhansky suggested that part of the answer to high tropical species richness rested with the equable nature of the tropical climate. Echoing Humboldt, he argued that polar and temperate climates impose significant physical selection pressures such that fewer organisms have been able to adapt over evolutionary time. Speciation is therefore less frequent in the higher latitudes. The tropics, in contrast, offer a climate of abundant rainfall for most if not all of the year, no season of frost or cessation of plant growth, warm and relatively invariable temperature, and less overall severe meteorological fluctuation, all of which may promote speciation to retard extinction to a degree greater than is the case in the higher latitudes. As species are added, many specialize to utilize unique resources. More and more species are packed into the rain forest ecosystem. The high level of plant productivity in the tropics serves as a large and steady food base. Dobzhansky’s hypothesis was obviously speculative and very challenging to test, but it stimulated much thinking about latitudinal diversity gradients.

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The Tropics: Cradle or Museum? Ecologists have offered two metaphoric views of the tropics to account for their high species richness. One, called the cradle, with a nod to Dobzhansky, views the tropics as uniquely suited to high rates of speciation and thus species accumulate in tropical ecosystems, far more than outside of the tropics. The other view, called the museum, presumes that speciation rates are not higher in the tropics but extinction rates are low, so the tropics, like a good museum, “keep” their more ancient species along with whatever new ones evolve, thus maintaining a high species richness. In the museum view, extinction rates outside of the tropics are presumed higher. Dobzhansky’s reasoning also alluded to this view but less directly. Perhaps the tropics can act as both cradle and museum. Most folks do not visit the tropics to see bivalve mollusks such as clams and mussels, but these creatures fossilize well, and so a look at the fossil record of bivalves can offer insights into past patterns of speciation. A study by David Jablonski and colleagues suggests this possibility. The researchers examined the fossil record of 163 genera and subgenera beginning 11 million years ago, in the Miocene epoch. What they learned was that most bivalve families, including those at high temperate latitudes, originated in the tropics, a finding that supports the cradle view of the tropics. Their data showed that first occurrences of bivalve mollusk genera were greatest in the tropics and that many genera subsequently radiated to temperate latitudes. The data further showed that substantially higher extinction rates occurred at higher latitudes over the 11-million-year period covered by the study, supporting the museum view of the tropics (i.e., lower extinction rates at lower latitudes). They concluded that genera originating in tropical areas extended their ranges with time while still occupying the tropics. The study suggests that endemism (the restriction of a species to a specific narrow geographic range) should be proportionally more common in the tropics and decrease with increasing latitude. As we discussed in chapter 8, there are numerous areas of endemism throughout the Neotropics. Conservation priorities (chapter 18) should consider both high species richness and levels of endemism, both of which characterize the tropics and explain why the tropical regions of the world have gained such a focus in conservation biology.

Plate 9-7. The elongated pods of Inga, a member of the large legume family, Fabaceae, are easy to recognize. There are many Inga species throughout the Neotropics; they are evolutionarily young. Photo by John Kricher.

Does speciation occur more rapidly in the tropics, thus packing the ecosystems with species? There are relatively few studies that examine this question, but some studies have utilized molecular techniques to compare similarities in DNA among species. The results of these studies have thus far generated contrasting conclusions. Some suggest that speciation is actually more rapid (for some groups) in the temperate zone. Some temperate species of birds and mammals are more recently evolved than most equivalent tropical species. This is really not surprising. Higher latitudes have been strongly affected by Pliocene and Pleistocene climatic changes, particularly glaciation, with its multiple effects on ecosystems. Such climatic shifts would act to promote speciation in isolated populations (chapter 8). Nonetheless, some speciation patterns have been high throughout the tropics. Consider the Inga, a common tree in shade coffee plantations (plate 9-7). Inga is a widespread Neotropical genus, with some 300 species ranging from Mexico into Argentina. Did these 300 species accumulate over many millions of years or are they more recent in origin? Using molecular techniques that allow comparison of DNA segments, a research team led by J. E. Richardson

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ascertained that the diversification of the genus Inga is no older than 6 million years and may be as young as 3 million years. The authors suggest that Inga divergence was likely caused by the recent Andean mountainbuilding episodes. Pleistocene climate changes and the bridging of the Isthmus of Panama (chapter 8) also likely stimulated speciation in Inga. Though speciation in Inga has been remarkably rapid, it may not represent a typical case among tropical tree genera. Eldredge Bermingham and Christopher Dick conducted a census of 25 ha (62 ac) of rain forest at a site in Ecuador and 25 ha in Panama, resulting in the following tally: • Ecuador: 1,104 woody plant species, 333 genera, 81 families, 43 Inga species. • Panama: 277 woody plant species, 174 genera, 56 families, 14 Inga species. What is noteworthy about those numbers is that in Ecuador, 161 of the 333 genera are represented by but a single species. In Panama, 121 genera have but a single species. Therefore Inga is unusual in exhibiting a pattern of multiple closely related species throughout its range. But it is not unique. Other plant genera such as Psychotria, Piper, and Ficus, all widespread in the Neotropics, show a similar pattern, exhibiting high species richness in relation to other genera. Tropical regions are clearly rich not only in species but in genera and families, and those take longer to evolve, showing that while Inga is clearly a “cradle” species cluster, many families of tropical plants (and by implication, birds, mammals, and other groups as well) may be part of a very old “museum.”

Climate, Energy Availability, and Species Richness The latitudinal belt from the Tropic of Cancer to the Tropic of Capricorn, spanning approximately 47° of latitude, is by and large warm and wet. Winters are far less severe than in temperate and polar regions. Light flows more evenly and constantly, as there is less (and on the equator no) variation in day length. Ecologists have long believed that equitable climate and an abundance of photosynthetic energy, termed net primary productivity (chapter 5), ultimately support greater species richness, helping account for the latitudinal diversity gradient (LDG). Let’s look at climate as it pertains to the LDG of one well-known group, birds.

Ever since Dobzhansky’s 1950 paper, avian species richness has occupied the attention of researchers seeking to explain the LDG. Bradford Hawkins and colleagues correlated seven climatic variables with broad global patterns of bird species richness. The resulting analysis indicated that “actual evapotranspiration” was the variable that explained 72.4% of the variance in global bird species richness. Why is this of interest? Because evapotranspiration is an indirect measure of forest photosynthetic productivity, since it is related to the metabolism of the trees. The conclusion was that productivity, as reflected in actual evapotranspiration, was the best hypothesis to account for the LDG in birds. Why? Productive forests have lots of food and space and thus accommodate numerous bird species. It’s that simple. Hawkins and his colleagues also looked at patterns of plant diversity. For plants, water availability, as it varies from region to region, was the key constraint limiting species richness. This effect was most pronounced in areas of warm temperature where adequate solar energy would otherwise be readily available. It is well known that dry seasons have pronounced effects on ecosystems, so this result should not be surprising. The studies by Hawkins and colleagues showed an apparent shift with latitude in the influence exerted by climatic variables on species richness. In the far north (and by implication in the far south), solar energy was the variable that placed the strongest constraints on richness. In these regions sunlight varies dramatically during the course of the year. But in areas of high solar energy input, as typify the tropics, water was the variable most responsible for constraining species richness. With regard to animal species richness, it should be noted that it was not clear whether solar energy and water availability act to limit species richness or whether richness is limited primarily through plant productivity, which, itself, is limited by solar energy and water availability. But the study does show that climatic variables correlate broadly with species richness patterns across latitudes. Climate appears to rule. Questions remain, however. Hawkins et al. noted that while climate variables may explain up to 90% of the variance in latitudinal species richness in some cases, in other cases it explains less than 50%. Such factors as evolutionary history and ongoing biotic interactions (discussed below) also exert strong influences.

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Diversity in the Tropics: Is It a “Perfect Storm”? Scores of researchers have attempted to summarize the various possibilities for why tropical ecosystems are so rich with species. A thought-provoking 1966 paper by Eric Pianka, now a classic, attempted to summarize the forces that might account for hyperdiversity in the tropics and in lowland rain forests in particular. We have already addressed some possibilities in the form of broad patterns of climate and evolutionary history. But what about the effects of day to day ecological forces within tropical ecosystems as such? What additional forces might act to increase species numbers and to maintain diversity? To borrow a well-known phrase from the writer Sebastian Junger, the tropics may represent a “perfect storm,” with ecological and biogeographic conditions combining in an ideal manner for bringing about speciation and diversity maintenance, just as atmospheric variables on occasion combine to create monumental storms. The result of the tropics’ perfect storm has been to produce prodigious numbers of species and then to keep them. Below I discuss four hypotheses (stability-time, productivity-resources, interspecific competition, and predation intensity) that have been offered to account for why the tropics are so diverse.

The Stability-Time Hypothesis The stability-time hypothesis suggests that the tropics are ancient and that such antiquity coupled with the relatively stable and equitable climate has resulted in the generation and persistence of high species richness. The idea is closely akin to what Dobzhansky believed to be the case (and yes, it is the museum metaphor again). How do we look back into time? How can we ascertain whether climate has been stable in the tropics? Carlos Jaramillo and colleagues conducted a study of the fossil record of plant pollen deposited in lakes from sites in central Colombia and western Venezuela, spanning a time sequence from the Paleocene to the early Miocene (65–20 million years ago). Pollen and spores from plants are resistant to decay, especially in anoxic deep lake and bog sediments, and thus they can be analyzed in what is termed a pollen profile of lake sediment. The deeper sediment contains the oldest pollen. The data analysis showed low plant diversity during the early Paleocene. This was the time just after the end of the Cretaceous

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period, which ended with one of the five mass extinction events in Earth’s history. Thus a low diversity of plants at that time is to be expected. During the early Eocene there was a rapid increase in plant diversity. However, diversity declined beginning in the late middle Eocene and continued to drop until the early Oligocene (34 million years ago). The extinction rate was elevated during the transition from the Eocene to the Oligocene, and the speciation rate increased during the early Eocene. Otherwise, both extinction and speciation rates were steady. Species richness correlated with changes in global temperature. Global warming during the early and middle Eocene permitted the spread of tropical plant species into higher and lower latitudes. Jaramillo also noted that tectonic activity in the Andes Mountains (the Andean uplift) acted as a major stimulus to plant speciation. Most of that mountain building has been recent (within the past 5 million years), so the clear implication is that most speciation has been recent. The study shows that the tropics have never been really “stable” but instead subject to some degree of climatic fluctuation. Speciation is not dependent on vast time periods. Six species of kingfishers (family Alcedinidae), birds that dive headfirst into water and capture fish with their long beaks, inhabit Neotropical rivers and streams. This assemblage represents the total species richness of kingfishers in the Neotropics. Five are permanent resident species, which differ fundamentally in body and bill size (plates 9-8–12); the sixth is the Belted Kingfisher (Megaceryle alcyon), a North American migrant that winters in parts of the Neotropics. The fossil record, as well as biogeographic studies, shows that kingfishers evolved in the Old World, and some eventually colonized the Neotropics, probably during the Pleistocene. What is interesting is that of the 120 kingfisher species in the world, only six occur in the Americas. Four of the six, the “green-backed” kingfishers (genus Chloroceryle; plates 9-8–11) are one another’s closest relatives and evolved in the Neotropics from a recent common ancestor. Interestingly, wherever in the world kingfishers occur there are never more than five species together, coexisting in the same habitat (this raises a question worth pondering about how resources affect species richness and coexistence). The five resident Neotropical kingfishers differ in body size, so they must obviously feed on different-size prey, though there is some overlap. In a monograph on the Neotropical kingfishers, Van Remsen pointed out that the five species of Amazonian kingfishers span the same size range and within-habitat species richness as the kingfishers found

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Plate 9-8. The diminutive American Pygmy Kingfisher (Chloroceryle aenea) is the smallest (13 cm/5 in) of the greenbacked kingfishers. It forages on small prey in streams and pools. This bird is female. Photo by John Kricher.

Plate 9-9. The Green Kingfisher (Chloroceryle americana) is the next largest (18 cm/7 in). This bird is female. Photo by John Kricher.

Plate 9-10. The Green-and-rufous Kingfisher (Chloroceryle inda) is more secretive than the other green-backed kingfishers, inhabiting quiet and shaded streams. It is 23 cm (9 in) long. This bird is a male. Photo by John Kricher.

Plate 9-11. The Amazon Kingfisher (Chloroceryle amazona) measures 28 cm (11 in) and is the largest of the four greenbacked kingfisher species. This one is a male. The species is common and widespread along rivers and streams. Photo by John Kricher.

in the Old World. This means that in the 2 million or so years since kingfishers colonized the New World tropics, they have evolved a local diversity equal to that found in any other global habitat where kingfishers occur. This pattern, like that of Inga (described earlier), suggests that speciation events may occur in geologically short time periods and that species richness is not directly dependent on long time periods. The major premise of the stability-time hypothesis, taken alone, is insufficient to explain high diversity, though the fact remains that the tropics have never been climatically severe. That said, there is almost universal agreement among climatologists, geologists, and

biogeographers that tropical regions have not, in fact, been climatically stable, though they have remained warm and relatively equable. Recall the refugia model discussed in chapter 8.

The Productivity-Resources Hypothesis One frequent suggestion to explain high diversity in the tropics is that high plant productivity allows for more species; the more plant biomass, the more energy, the more of everything. As discussed above, this may be the case in the Neotropics. Variables of climate clearly affect plant productivity and correlate with latitudinal

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Plate 9-12. The Ringed Kingfisher (Megaceryle torquata) is common along major rivers but also can be found in streams. It is the largest of the New World kingfishers (41 cm/16 in). This bird is female. Photo by John Kricher.

species richness. Many questions remain, however. One is the question of how an abundance of plant productivity translates into supporting high species richness of animals. A simple measure of biomass may be insufficient to explain some patterns. Look around in a rain forest. How would you try to ascertain just how many other taxa such as insects, lizards, or birds are there because of the green around you? Perhaps high tropical plant productivity and an abundance of plant biomass translate directly into more space for more species. Daniel Janzen, in a provocative 1976 paper titled “Why Are There So Many Species of Insects?” concluded by saying, “I think that there are so many species of insects because the world contains a very large amount of harvestable productivity that is arranged in a sufficiently heterogeneous manner that it can be partitioned among a large number of populations of small organisms.” Janzen, a legendary tropical ecologist and conservationist, was not restricting his speculation to the tropics, but his remark fits the tropics particularly well. There is indeed a tremendous potential harvestable productivity, and there are lots of spaces for small animals in the three-dimensionally complex rain and cloud forests. Bird species diversity often correlates with a measure termed foliage height complexity in mid to high latitudes. The more layers of foliage there are, the more bird species. But in 1974 Thomas Lovejoy showed that in the tropics, bird species diversity does not correlate closely

with foliage height diversity. This is because tropical rain forests are more spatially complex than temperate forests, offering resources not detected or measured by simple structural analysis (which was based on measuring horizontal strata from ground to canopy). As James Karr first pointed out in 1975, tropical forests offer unique resources for birds and, by implication, for other kinds of animals. Let’s take a look at these offerings: • Among tropical forests’ additional resources are large numbers of vines, high epiphyte density, and large dried leaves (which harbor many kinds of arthropods that are food for birds; plate 9-13), all of which add space, complexity, and potential food resources.

Plate 9-13. Spiders and other arthropods may utilize the cover provided by large dried leaves and epiphyte growth and form a unique food base for other animals. Photo by John Kricher.

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Plate 9-15. This Lovely Cotinga (Cotinga amabilis) approaches a fruiting tree. A species such as this, with its dependency on fruit, could not exist in the temperate zone. Photo by James Adams.

Plate 9-14. The unique and well-named Long-billed Woodcreeper (Nasica longirostris) is one of the largest of the woodcreepers (36 cm/14 in). Its long bill probes for large arthropods. There is no equivalent species outside of the tropics. Photo by Andrew Whittaker.

Plate 9-16. The Spotted Antbird (Hylophylax naevioides) is usually found in the company of army ant swarms. This bird is a male. Photo by Kevin Zimmer.

• There are numerous potential prey items in addition to small prey. In a now classic 1971 study Thomas Schoener showed that insectivorous birds in the tropics have a much wider range of bill length (among all species) than those of the temperate zone. He attributed this variety to the wider resource base available in the tropics, especially of large insect prey items. Peruse any field guide to Neotropical birds and you will marvel at the range of bill sizes and body sizes among families of birds such as tyrant flycatchers, ovenbirds and woodcreepers (plate 9-14), and many others. These

anatomical distinctions are evolutionary results, at least in part, of each species being adapted to focus its energy on capturing prey within a certain size range. • There is also year-round availability of nectar and fruit. Nectar specialists include all the multiple hummingbird species (see chapters 10 and 15) as well as various flowerpiercers and some others (chapter 10). Fruit-eating specialists include cotingas (plate 9-15), many tanagers, guans, curassows, and parrots. Add to those iguanas and other reptiles, scores of monkeys, and rodents such as agoutis and pacas, and you have

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a lot of fruit consumers. None of these groups can exist successfully outside of the tropics, since they are so dependent on constant availability of nectar and/or fruit. • Army ants are a unique resource in the Neotropics in that their activity provides the food base for a complex group sometimes called “professional antbirds,” species that follow army ant swarms to feed on the arthropods driven out by the ants (plate 9-16). Many other bird species, though not as specialized, nonetheless also become active feeders on the arthropods at ant swarms. • Forest gaps also represent a resource. Gaps are a characteristic of all forests, but tropical forest gaps may present more opportunities to specialist species than those outside of the tropics. Gaps occur frequently in tropical lowland forests and their frequency alone would serve to allow many species to become gap specialists. Gap dynamics is discussed in greater detail in chapter 7. Do additional resources translate into ecological specialization? Specialization occurs when a species becomes uniquely adapted to a narrow resource base. Ecologists say that specialist species have narrow ecological foraging niches. (The word niche in the parlance of ecology means in essence how a species makes its living.) For example, the evolution of specialization in the diet of the Black-and-white Owl (Ciccaba nigrolineata; plate 9-17) is rooted in the abundance of Neotropical bats inhabiting rain forest. This owl species, which ranges from southern Mexico to northwestern Peru, is a bat specialist, feeding almost entirely on the furry flying mammals. Another species, the crepuscular Bat Falcon (Falco rufigularis; plate 918), also specializes to a degree in bat capture, feeding on the flying mammals at dawn and dusk. There are now equivalents to these species outside of the tropics. Bamboo stands, which are patchy resources irregularly distributed throughout the Neotropics, allow for specialization (plate 9-19). Van Remsen and the late Ted Parker surveyed Amazonian bamboo stands, in which plants reach heights of up to 15 m (50 ft). These stands supported as many as 21 bird species specialized in some way to feed exclusively within bamboo stands. Nine species specialized on eating bamboo seeds, and 12 were insect foragers. An additional 16 species of insect-foraging birds were found mostly in bamboo but also in other habitats. Ephemeral Amazonian river islands of sandbar scrub and young successional forests (chapter 12) provide

Plate 9-17. The Black-andwhite Owl forages heavily on bats. Photo by Kevin Zimmer.

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Plate 9-18. The well-named Bat Falcon, one of the smallest of the world’s falcons, also focuses its diet largely on bats. Photo by James Adams.

Plate 9-19. Amazonian bamboo stands such as this are habitat for several bird species that occur nowhere else. Photo by John Kricher.

Plate 9-20. This is a Ladder-tailed Nightjar (Hydropsalis climacocerca) on its nest on a riverine sandbar in Ecuador. This nocturnal species is not a “sandbar specialist,” but nonetheless it uses sandbars for breeding real estate. Photo by John Kricher.

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yet another important resource on which some bird species have specialized (plate 9-20). For example, a visit to a sandbar island along the Napo River in Ecuador might, if you look carefully, turn up White-bellied Spinetail (Synallaxis propinqua), Castelnau’s Antshrike (Thamnophilus cryptoleucus), and Parker’s Spinetail (Cranioleuca vulpecula). These three furtive and littleknown species are characterized as sandbar specialists, nesting only among the dense vegetation that colonizes riverine sandbars. It has long been assumed that specialization is widespread in tropical ecosystems, though that should not be taken to mean that all species have narrow foraging niches (see discussion below). Specialization need not be the case for many if not most species if numerous varied resources are available in tropical lowland forests. In a study comparing the woodpecker communities of Maryland, Minnesota, and Guatemala, Robert Askins studied seven woodpecker species in Guatemala, compared with only four in each of the temperate study areas. Although there was almost double the number of woodpecker species in the tropical field site, these species were no more specialized in their foraging behavior than their temperate relatives. Instead, they utilized a wider range of resources. Some of the tropical species fed on termites and ants, probing into the excavations made by these insects, and the tropical species fed more heavily on fruit than the temperate woodpeckers. Two tropical woodpeckers in particular, the Black-cheeked (Melanerpes pucherani; plate 9-21) and the Golden-olive (Colaptes rubiginosus), utilized resources not available to temperate species. The Black-cheeked frequently fed on fruit, and the Goldenolive probed moss and bromeliads. In contrast to woodpeckers, bats (order Chiroptera) do represent a group that has specialized to various degrees in tropical ecosystems. Recall the description of the amazing adaptive radiation of Neotropical bats in chapter 8.

The Interspecific Competition Hypothesis Suppose you are a budding tropical ecologist eager to earn a PhD. You establish a tropical field site in western Amazonia. You are determined to find out what factors account for the high diversity of tree frogs. You consider the possibility that their abundance and distribution is caused by competition among the various species driving them to specialize to exploit different ecological niches. Now, how would you test

Plate 9-21. The Black-cheeked Woodpecker feeds heavily on fruit, a resource not as constantly available to woodpeckers in the temperate zone. Photo by John Kricher.

this idea? (Hint: it will not be easy.) One of the most difficult measures to make in ecological research is the degree to which competition occurs between two or more species. One must be able to demonstrate that two (or more) species are seeking the same limited resource, and then measure the degree to which each species negatively affects the other(s) in contesting for the resource. It is essential to identify the resource being contested and demonstrate that it is, indeed, a limited resource. If it is not limited, there will presumably be enough for both species, and no competition would occur. This of course means that if you observe two different species each using the resource you cannot automatically conclude that they are in competition, anymore than two people ordering steaks at a restaurant are in competition. It is also essential to show how the competition affects each species. Another key component to interspecific competition is that it has a higher cost to each species than intraspecific competition. In other words, each species has to—to some degree—negatively affect the other. The degree to which they negatively affect one another need not be equal. When species compete, there are the following possible outcomes: • One species outcompetes the other, and the loser goes extinct, a process termed competitive exclusion. But this does not seem to be happening in tropical rain forests, which are rich with species of numerous taxa. • The two species somehow subdivide the resource, each specializing on a part of the resource spectrum. This is called niche partitioning. When this happens each species is said to have specialized. There are

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two ways for this to happen. One is that a species’ realized niche (the actual resources it uses) is forced by competition to become narrower than its fundamental niche (the niche space it would occupy in the absence of competing species). The second way is that the actual fundamental niches may evolve to be narrower. • Intraspecific competition might drive each species to gradually expand its original foraging niche and utilize new resources, thus reducing the competition. This could be an ongoing evolutionary process and help explain why specialization is not necessarily more common in the tropics than elsewhere. It has long been argued that high species diversity in the tropics is related to levels of competition among species. Over time, interspecific competition has resulted in greater niche partitioning (a form of increased specialization). Each species evolves into somewhat of a specialist, focusing on a specific resource that it and it alone is best at procuring. This trend toward specialization due to interspecific competition leads to the packing of greater and greater numbers of species into tropical ecosystems while at the same time reducing the intensity of competition among species,

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as each specializes to its exclusive pool of resources. The interspecific competition hypothesis argues that many if not most niches are narrower in the tropics than in the temperate zone because competition inevitably will compress them. The hypothesis is dependent on the reality that greater specialization is possible in the tropics because particular types of resources (such as large lizards or long tubular flowers) are consistently available throughout the year, showing seasonal stability. In the temperate zone many specific types of resources are available only during a brief season each year, so species are forced to be generalists, particularly if they do not migrate. There are problems with this hypothesis. We have already seen from the Askins study that woodpeckers do not exhibit narrower niches in the tropics but rather use a greater range of potential resources. Though competition may have exerted a major influence in the past, now that specialization and niche compression have occurred, competition may be quite minimal or even nonexistent. It should be obvious that this is a very difficult hypothesis to test. For example, both the Ocelot (Leopardus pardalis) and the Margay (L. wiedii; plate 9-22) occur throughout

Plate 9-22. Margays routinely climb trees. See chapter 16 for more on Neotropical felines. Photo by James Adams.

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Plate 9-23. Miconia plants produce fruits used by numerous bird species, many of which, such as manakins, spread seeds. Miconia is in the Melastomataceae family. Photo by Scott Shumway.

Plate 9-24. The Red-capped Manakin (Ceratopipra mentalis) is a common disperser of Miconia seeds. Photo by James Adams.

most Neotropical lowland forests. These two small cats are similar in body size, though the Ocelot is a bit larger. Both are essentially nocturnal, and it is not unreasonable to assume that they feed on many of the same prey items: rodents and other small mammals, birds, snakes, lizards. The two differ somewhat in their foraging behaviors, as the Ocelot is almost entirely terrestrial while the Margay routinely climbs trees in the course of its hunting behavior. Thus the Ocelot and Margay have foraging niches that do not precisely overlap. Did competition between these two small felines cause the divergence of foraging niche, selecting for the smaller cat to become more arboreal? There is no way to know. It cannot be known whether resources were limited, and even if they were, it cannot be known whether that limitation was, indeed, an active selection pressure. In other words, it cannot be known whether Margays that climbed reproduced better than those that did not because they climbed. Even if they did, such behavior may have resulted from the availability of arboreal resources presenting an opportunity for procuring more calories and protein, not because Ocelots were also foraging on the forest floor. As the above example is meant to illustrate, evidence for the interspecific competition hypothesis is mostly circumstantial. Direct demonstrations of interspecific competition are generally lacking in the tropics. Certain patterns suggest, however, that competition among species may be a component of tropical evolution and diversification. Varying bill shapes and gradations in body sizes within many bird groups suggest that competition may have influenced the evolutionary history of these

groups. Recall the six kingfisher species that cohabit Neotropical rivers and backwaters, pictured earlier in this chapter. The size range within the kingfisher complex does suggest an evolutionary resource partitioning, as each species has adapted to feeding on an optimal size range of fish. That could be a result of competition among the evolving populations, but it could just as easily result from the range of prey species available. Ringed and Amazon Kingfishers routinely capture and devour prey that is larger than an American Pygmy Kingfisher. As this example suggests, different body sizes and bill characteristics reflect specialization for capturing differing food items. The very act of food capture per se could and probably does select for such specializations, though it is quite likely that the presence of similar species with similar ecological needs could act as an additional strong selection pressure in producing divergence among species. Insectivorous bats, for example, feed on different-size prey items and also forage at different heights in the rain forest, a pattern possibly reflective of avoidance competition among the bat species. One way to support the possibility of interspecific competition is to demonstrate that a species exhibits a limited foraging niche, presumably because of the presence of other competing species. Thomas Sherry found that each of three flatbill flycatcher species found in Costa Rica forages at a different height in the forest, and certain flatbill species replace others in specific habitats— for example, one species occurs in forest, while another very similar species is only in disturbed brushy areas. This pattern is suggestive of competitive relationships having influenced the birds’ foraging choices.

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Andean bird communities also show indirect evidence for interspecific competition. John Terborgh and John Weske studied two Andean mountain peaks in Peru, one of which was isolated, one of which was not. Colonization by birds was less frequent on the isolated peak, and thus this peak had reduced bird species richness, missing an estimated 80–82% of the bird species that presumably would have occupied the isolated peak had it been part of the main range of the Andes. However, of the species that did occur, 71% had expanded their elevational range (compared with populations on the other, more diverse mountain peak) presumably because of the absence of similar species that would have been competitors. Interspecific competition for pollinators and seed dispersers may have provided a selection pressure resulting in staggered flowering patterns among some plants. In Trinidad’s Arima Valley, 18 species of the shrub genus Miconia (plate 9-23) have flowering times staggered in such a way that only a few species are flowering in any given month. Is this, as suggested by ornithologist David Snow, a possible evolutionary result of competition among Miconia species for access to birds that eat the fruit (plate 9-24) and thus disperse the seeds? Any Miconia species that flowered when most others did not would be able to attract more birds to disperse its seeds, thus it would have a selective advantage compared with others of its own as well as other species. Over time, the staggered flowering pattern emerged. A similar pattern among plants that are bat pollinated has been observed E. Raymond Heithaus in Costa Rica. Of 25 commonly visited plant species, an average of only 35.3% flowered in any given month. The patterns described here for inferred interspecific competition do not, in and of themselves, demonstrate that niches are narrower in the tropics, and none really demonstrate competition in a rigorous manner. This is an ongoing weakness in attributing greater species richness in the tropics to greater interspecific competition. Nonetheless, patterns are compelling. High species richness of rain forests may be partly explained by competition among species, at least for some species groups. It would be very helpful if robust data replaced suggestive patterns.

The Predation Hypothesis Predators abound in the Neotropics. They represent what ecologists term top-down ecological forces,

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Plate 9-25. Predators such as this basilisk lizard abound in the tropics and may collectively exert significant ecological effects in structuring tropical ecosystems. Photo by James Adams.

meaning that in the food chain from sun to plant to herbivore to various predators, predator influence may be strong in potentially affecting species populations lower on the food chain. Suppose the caterpillars of four different species are competing for the same plant. One species is increasing at a much higher rate, causing the others to be driven toward local extinction. What was a four-species system seems destined to become a one-species system. But suppose birds and lizards prey on the caterpillars (they do!). Which of the four are the predators likely to take? The most obvious and abundant species would seem the likely choice. The result of continuous predation would be to reduce the most rapidly growing population, the presumptive “winning” species, allowing the various other “losing” species to regain some control of the resources and increase in population. This scenario shows how predators may maintain species richness by switching among prey based solely on prey abundances. The game of competition is thus never permitted to play out. The predation hypothesis posits that predators prevent prey species from competing within their ranks to the point of extinction. Predators are thought to switch their attention to the most abundant prey, thus the rarer the species, the safer it is from predators. This idea is a form

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of frequency-dependent selection, in which the intensity of selection (in the form of predation) depends directly on the abundance of the prey (such that rare species have a selective advantage). The result of predator pressure is to preserve diversity by preventing extinction by competition (plate 9-25). Note that the predation hypothesis is basically opposite to the interspecific competition hypothesis. The competition hypothesis suggests that competition among species promotes diversity by leading to specialization, narrower niches, and tighter species packing. The predation hypothesis suggests that predators actually reduce interspecific competition, thus permitting coexistence among competing species. The predation hypothesis does not predict specialization. Indeed, specialization would seem less likely to occur because predators keep competition levels low. Likewise, the predator hypothesis allows for wide niche overlap among similar species. Tropical forests contain impressive predator richness, circumstantial evidence for the possible importance of predator effects. In a study conducted by Roman Dial and Joan Roughgarden in a tropical moist forest in Puerto Rico, lizards in the genus Anolis were shown to have strong effects on the arthropod community of the rain forest canopy (plate 9-26). When lizards were experimentally excluded, large arthropods such as orbweaver spiders, cockroaches, beetles, and katydids all significantly increased. What if predators are nonselective, even when prey densities vary? John Terborgh suggested an intriguing model of how predators, specifically cats, might be inadvertently structuring rain forest communities. Citing Louise Emmons’s work, Terborgh began by stating that the Jaguar, Puma, and Ocelot all forage nonselectively, taking whatever they encounter and can catch. The populations of prey species correlate directly with the frequency upon which each prey species is taken by a cat. If agoutis represent 40% of prey species, agouti remains show up in cat scat 40% of the time. Predators are taking what they find as they find it. Terborgh goes on to argue that since prey species differ in their fecundities (rates of reproduction), predation by nonselective cats could significantly reduce certain lowfecundity prey populations. In other words, peccaries can produce more offspring annually than pacas, so if cats do not ever discriminate between peccaries and pacas, pacas must decline more than peccaries, since they cannot replenish their losses as quickly. Because

pacas and peccaries both eat many of the same things, an ecologist might be tempted to conclude that paca reduction was due to its losing the competition for food with peccaries, never guessing that cat predation was the real reason. Terborgh’s argument demonstrates that predation can result in a loss of diversity, as well as act to maintain it, if predation is, in fact, nonselective rather than frequency dependent (plates 9-27–28).

Some Broad Patterns of Tropical Species Richness It should come as no surprise that animal groups such as amphibians and reptiles, unable to physiologically regulate body temperature, decline in diversity and abundance with latitude. The Arctic and Antarctic are inhospitable to crocodiles, lizards, snakes, and turtles. These animals are ectothermic and thus unable to obtain sufficient body heat during times of extreme cold. Such harsh conditions do not occur in subtropical or tropical latitudes, and thus reptiles thrive in such regions. Amphibians are similar in that they too are ectothermic, but they differ from reptiles in being dependent on an aquatic or semiaquatic environment, especially for reproduction, so they are even more limited by harsh climate, and their species richness pattern is closely correlated with water availability as well as warm temperature. Thus, like reptiles, amphibians exhibit highest species richness in low latitudes. Physiological constraint undoubtedly is a major factor in the latitudinal diversity gradient (LDG) for reptiles and amphibians. Insects and other arthropods are also ectothermic, but they are small and often able to overwinter as eggs or pupae. Insect numbers may be impressive during the short Arctic growing season, but arthropod species richness is nonetheless far greater at lower latitudes. Like various vertebrate groups, insects (among arthropods) exhibit their highest species richness within rain forests. LDGs show complex and nonrandom patterns. For example, most of the increase in mammalian diversity in the tropics is due largely to bats (Chiroptera) and rodents (Rodentia). But monkeys, sloths, anteaters, and various marsupials all contribute to enhanced diversity. Mammalian diversity in Neotropical lowland rain forests correlates with both productivity and habitat characteristics. Louise Emmons showed that the density and number of species of Amazonian mammals (excluding bats) correlate positively with

why are there so many species?

Plate 9-26. Anolis lizards in Puerto Rico appear to exert significant effects on various canopy arthropod populations. This male Green Anole (A. carolinensis), which occurs in the southeastern United States, is displaying his red dewlap. Photo by John Kricher.

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Plate 9-27. Collared Peccary (Pecari tajacu) populations may be influenced by predation more than by competition. Photo by John Kricher.

Plate 9-28. These two capuchin monkeys are feeding on a Chestnut-mandibled Toucan (Ramphastos swainsonii) that they apparently killed. Monkeys feed heavily on fruit, but these have apparently augmented their diets to include meat. Predation takes myriad forms in the Neotropics and must be a strong ecological force. Photo by James Adams.

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Is Predation Responsible for Small Clutch Sizes of Neotropical Birds? It is a straightforward fact that forest species of Neotropical birds lay fewer eggs in their nests than do their counterparts in the temperate zone. A clutch size for an American Robin (Turdus migratorius) is typically four eggs and often five. Its Neotropical equivalent, the Clay-colored Thrush (T. grayi; plate 9-29)—which is the national bird of Costa Rica—has a typical clutch size of two or three eggs, though it occasionally will lay four eggs. A study by Alexander Skutch of 115 nests showed an average clutch size of 2.68 eggs. One reason tropical birds may have lower clutch sizes could be food-related. Tropical bird species nest throughout the year, though various species have various peak times. In contrast to the tropics, in the temperate zone there is a major insect flush in the spring as leaves open, which makes protein-rich food abundantly available to nesting birds. Not only that, days are longer, allowing more time for parents to provision food for their growing nestlings. Perhaps this scenario alone allows temperate-zone birds to increase clutch size compared with tropical species. But it is likely not the most compelling factor. Nest predation and thus nest failure are very high in the tropics. Birds that make open-cup nests are vulnerable to predators ranging from monkeys to ants (plate 9-30).

Plate 9-29. The Clay-colored Thrush suffers very high rates of nest failure due to various forms of predation. Photo by John Kricher.

Bridget Stutchbury and Eugene Morton cite that nest failure is in the general range of 80–90%. That’s right— something like eight to nine out of 10 nesting attempts are destined to fail. (The failure rate is significantly lower in the temperate zone.) A study in Panama cited by Stutchbury and Morton that had been performed by Morton found that 58% of Clay-colored Thrush nests were destroyed in dry season, compared with 85% in rainy season. Food is more abundant in rainy season but so is predation risk. Morton also found that thrushes fledge (leave the nest) earlier and when they are smaller in body mass than their temperate equivalents. It appears there is strong selection pressure for the birds to get out of the nest. Given the high rate of nest failure in tropical forest, why aren’t the birds extinct? The answer may be in the adage “if at first you don’t succeed, try, try again.” Really. Temperate passerines have, on average, much reduced life spans compared with tropical species. A small tropical bird like a manakin may live for 15 or more years. Such a life span is unheard of with a temperate species like a chickadee. The lifetime reproductive success of a manakin, with its small annual clutches and its high rate of nest failure, may nonetheless equal or even exceed that of a shorter-lived chickadee. The breeding biology of Neotropical forest birds does indeed suggest that predation acts very strongly as a selection pressure and that it may contribute to influencing diversity patterns.

Plate 9-30. This open-cup nest of a Palm Tanager (Thraupis palmarum) contains two nestlings, a typical clutch size for tropical forest passerine birds. The rate of nest failure from predation is very high. Photo by John Kricher.

why are there so many species?

Does Disturbance Help Explain Why There Is Such High Overall Diversity? As I discussed in chapter 7, disturbances are common in the tropics. Climate and weather disturbances, in a manner roughly analogous to predators, may act to reduce the competitive edge of any one species against another (plate 9-31). The game of competition is in essence restarted after the disturbance. Disturbance intensity and frequency are critical variables in considering disturbance per se as a force for maintaining high species richness (fig. 9-1). Consider what would happen if an area were harshly and frequently disturbed. The severe physical conditions would act to preclude high species richness. Not many species could adapt. This may be, in part, why there are so few species in the high latitudes relative to the tropics. But consider also what would happen if an area never experienced disturbance. Species richness will theoretically decline due to inevitable interspecific competition among species. As with Goldilocks’s porridge, which had to be “just right,” disturbance frequency and intensity must be neither too severe nor too limited. In theory, moderate, intermediate disturbance should result in maximal species richness. This model, termed the intermediate disturbance hypothesis (IDH), was first argued by Joseph Connell to account for high species richness in both rain forests and coral reefs. It postulates that intermediatelevel disturbance is locally patchy but regionally continuous, and that the overall disturbance regime is sufficiently gentle as to maintain high species richness but sufficiently frequent to prevent extinction through interspecific competition. The model envisions the tropics as a mosaic of different-aged disturbance patches (recall the discussion in chapter 7). Bottom line: essentially every place is in some state of recovery from disturbance—there is no real equilibrium in tropical forests. This means that there is no definitive assemblage of species that will form the “end point” of development in any forest community. Instead, species assemblages will change as affected by disturbance events. There

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soil fertility and undergrowth density, both a measure of plant productivity. Large mammalian species tend to range widely and maintain relatively constant densities over large areas, but small species vary dramatically in numbers and diversity from one study site to another.

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Low Disturbances frequent Soon after a disturbance Disturbance large B

A b

Infrequent Long after Small

C b

A. Colonizing

c

c

B. Mixed

c

Canopy c

Understory

C. Climax

Figure 9–1. This figure depicts the possible effect of disturbances ranging from frequent (left) to infrequent (right) on the diversity of tropical ecosystems. Adapted from Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 1999: 1302–1310. Reprinted with permission from AAAS.

Plate 9-31. A severe hurricane cleared much of this mangrove forest on an offshore cay in Belize. Disturbance, of various degrees of magnitude, occurs in all forests and may be a major factor affecting interspecific competition and keeping forests in states of high-diversity nonequilibrium. Photo by John Kricher.

have been studies that test the intermediate disturbance model and most add support to it. There is no shortage of possible topics to study if you are game for looking more deeply into the factors responsible for the generation and maintenance of high species richness and biodiversity in the tropics.

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Plate 10-1. The Keel-billed Toucan (Ramphastos sulfuratus) is a generalist feeder but consumes many fruits. It flies long distances between trees and thus acts to disperse seeds. The plants depend on that. Photo by Nancy Norman.

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Tropical Intimacy: Mutualism and Coevolution

A Tropical World of Interactions With the profligate plant, animal, and microbial life typical of rain forests, it should come as little surprise to learn that the major resources of a tropical forest are the organisms themselves. Species interact on a daily basis in ecological time that, with generations, becomes evolutionary time. The interdependencies that result are often complex, to say nothing of fascinating. Some species become increasingly interlinked as predator and prey. Others are locked into interdependent mutualistic associations through a process that ecologists call coevolution. This is the real fun of visiting the tropics, to witness firsthand some of these amazingly elegant examples of interaction and coevolution (plate 10-1). This and the next chapter will take you into that world.

Kinds of Interactions An interaction between any two species may be positive, negative, or neutral for either party. Both may benefit from the interaction (+/+), one may benefit while the other loses (+/−), both may lose (−/−), though to varying degrees, or one may benefit while the other experiences neither gain nor loss (+/0). Commensalism (+/0) occurs when one species benefits from the interaction and the other is not harmed or significantly compromised. Epiphytic plant species are generally commensal with their host plants (plate 10-2). Normally epiphytes do not seriously reduce the fitness of host plants, and epiphytes obviously benefit from attachment on the host. It is true, however, that epiphytes may, on occasion, weaken a branch by their sheer combined weight, making it more susceptible to breakage, or they may be sufficiently dense to interfere with photosynthesis of the host tree. The relationship in this case is more parasitic than commensal. There are two manifestations of interactions in which one species gains and one loses (+/−), predation and parasitism. Predators and parasites gain while their prey or host species obviously lose. Competition occurs when two individuals both require the same resource, and that resource happens to be in limited supply. In competition among species (discussed in chapter 9), one competitor obtains more of the resource and benefits while the other suffers

some measure of loss. Competition may be viewed as a lose-lose (−/−) type of interaction, but the minuses are not necessarily of equal magnitude, and so the cost is not the same to each competitor. This sort of competition is likely common among species and were it to continue indefinitely, one of the competitors would eventually replace the other. Perhaps the most fascinating of relationships is mutualism (+/+), which occurs when two or more species engage in an interaction from which both species benefit. In evolutionary terms, the fitness of each species is enhanced by the interaction. Animalmediated pollination of plants is an outstanding example of a widespread form of mutualism. Mutualistic relationships are common in tropical rain forests and will form a focus of this chapter. Some are relatively casual and some are entirely obligate.

Seed Dispersal: The Unique Importance of Fruits in the Tropics Fruit is abundant and (relatively) constantly available throughout the year in moist tropical forests and thus an important resource. Fruiting trees attract numerous animal species. Think of fruiting trees as the fast-food restaurants of the tropical forest. Some animals feed on fruit when it is abundant but not as a primary resource.

Plate 10-2. Epiphytes on branch. Epiphytes are normally commensal with their host plant, but sometimes epiphyte load weakens the branch. Photo by Beatrix Boscardin.

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Plate 10-3. This Chestnut-bellied Guan (Penelope ochrogaster) feeds extensively on fruits picked up on the forest floor and from tree branches. Birds such as guans and curassows are important seed dispersers. Photo by Andrew Whittaker.

Plate 10-4. Agoutis are among the most devoted fruit consumers in the mammalian tropical community. Photo by James Adams.

Plate 10-5. This leaf-nosed bat (family Phyllostomidae) is enjoying its fruit. After it flies away, it may disperse the seeds. Photo by Sean Williams.

Plate 10-6. Hyacinth Macaws (Anodorhynchus hyacinthinus) crush and eat palm nuts and, like many parrots, are usually seed predators, destroying rather than dispersing the seeds. Photo by Nancy Norman.

Others feed heavily on fruit at all times. Some bird species feed on almost nothing but fruit (plate 10-3). In the temperate zone, fruit is a seasonal resource, occurring from midsummer through autumn, with some fruits lingering through winter. Many birds migrating to wintering grounds in the tropics feed intensively on fruit during fall migration, but because fruit is ephemeral in the temperate zone, no bird families have specialized to feed entirely on fruit.

Waxwings (Bombycillidae) come fairly close, but they also feed on some animal material. In the Neotropics the most dedicated avian fruit consumers are the cotingas, manakins, parrots, doves and pigeons, toucans, and tanagers. Ground-dwelling birds such as tinamous, wood-quail, and the Ocellated Turkey (Meleagris ocellata) are also fruit consumers. In addition, fruit is a major component of the diets of numerous mammal species, including many bats, rodents, peccaries,

tropical intimacy: mutualism and coevolution

tapirs, deer, and primates (plate 10-4). Fruits provide a calorie-rich, nontoxic, and relatively easily acquired resource (it certainly does not run away). There are downsides to a diet of fruit. Protein is often in low quantity, thus an all-fruit diet, while rich in calories, may be nutritionally deficient and need to be augmented in some way with animal food having more concentrated protein. Fruiting patterns vary, often significantly, both in time and space. Recall that tree species may be widely separated in tropical forests. This means that frugivorous animal species routinely must travel widely to find a suitable fruiting tree. A fruiting fig tree presents a bonanza, but fruiting figs may be few and far between. This is one reason a tree burgeoning with fruit can be a bonanza for the naturalist. Just stand there and enjoy the continuous visitations, as birds and mammals come to feed at the tree. Seasonal changes in fruit abundance occur throughout the tropics, and some montane frugivores such as the Resplendent Quetzal (Pharomachrus mocinno; chapter 15) undergo regular seasonal migration to lower elevations in search of favored fruits.

Fruit as an Adaptation The evolutionary function of fruit is to advertise itself to animals so that it will be consumed. In the evolutionary sense, fruits “want” to be eaten. The nutritious pulp of the fruit is a bribe to an animal. The seeds contained within the fruit pass through the alimentary system of the animal (or are regurgitated) and, because the animal is mobile, are deposited away from the parent plant. And that turns out to be very good for the plant (plate 10-5). Seed dispersal is an essential adaptation. The worst place a seed can fall is in the shadow of its parent tree. Doing so sets up a severe competition for light, water, and soil nutrients with an already established conspecific, the “mother” tree. Ecologists recognize what is called a seed shadow effect, in which the optimal distance for a seed to be is well away from the parent tree but not so distant as to find itself in an unsuitable habitat or where cross-pollination becomes unlikely. Seeds that are distant, like seeds that are close, have reduced likelihood of success. Therefore the real function of a fruit consumer from the evolutionary standpoint of the plant is to take the precious seeds some distance away and drop them where they have a good opportunity to germinate.

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Fruits therefore are anatomical adaptations for seed dispersal. Ideally the animal derives nutrition from the fruit but also disperses seeds; thus, the relationship between animal and plant is fundamentally mutualistic—both parties win. The animal provides mobility, a contribution not unlike that in animalvectored pollination (discussed below). Thus it is to the plant’s ultimate advantage to invest energy to make fruit, and it is to the animal’s immediate advantage to eat the fruit. But it does not always work out that way. Some species digest the seed as well as the pulp of the fruit or else injure the seed, and it does not germinate. Animals that destroy or fail to disperse seeds are not useful to the plant and represent an evolutionary cost to the fruiting plant (plate 10-6). Fruit comes at a cost to the plant. Lots of carbohydrate and fat typically is incorporated in fruit. The plant has to pay the animals to disperse the seeds, so to speak. But not all tropical plants produce expensive animaldispersed fruit. Some rain forest canopy trees, vines, and epiphytes utilize wind or water for dispersal of seeds. Wind dispersal is most common at the canopy level or in open tropical deciduous forests, where leaf drop can help facilitate wind movement of seeds. However, in dense interior rain forests where wind is attenuated, animals are essential for seed dispersal. Plants have little evolutionary choice but to bribe them accordingly.

How Fruit Drives Evolutionary Patterns in Birds Ornithologists David Snow and Eugene Morton have independently committed many years of fieldwork that revealed how a diet heavy in fruit results in evolutionary consequences to some groups of birds. Fruit is temporally and spatially a patchy resource, meaning that it may be abundant on a given tree but, as mentioned above, trees laden with mature edible fruits may be widely spaced in the forest. For much of the year, a fruiting tree may be barren of fruit. Such a resource distribution selects for social behavior rather than individual territoriality. Flocks of avian frugivores can locate fruiting trees more efficiently than solitary birds, and there is little disadvantage to being part of a flock once the fruit is located, since there is usually more than enough fruit for each individual. Even if not, it is extremely difficult

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The Cost of Fig Dispersal It takes lots of patient and persistent fieldwork to unravel how nature works. Pedro Jordano measured fruit volume and seed dispersal from a single fig tree in a lowland deciduous forest in Costa Rica. The estimated total crop was approximately 100,000 figs, all of which, because they were produced synchronously, were taken within five days either directly from the plant or after they had fallen to the ground. During the first three days alone, 95,000 were consumed. Birds were the principal feeders, eating 20,828 figs each day, about 65% of the daily loss. Mammals, most of which ate fruits that had fallen to the ground, were the other source of loss. Parrots, which are fundamentally seed predators, accounted for just over 50% of the daily total of figs. The most efficient seed dispersers (those that flew away from the tree and therefore dropped seeds outside of the seed shadow) were orioles, tanagers, trogons (plate 10-7), and certain flycatchers. However, these birds took only about 4,600 figs per day. Approximately 4,420,000 seeds were destroyed each day, mostly from predation by wasps and other invertebrates. Parrots were estimated to account for 36% of the seed loss. Only 6.3% of the seeds taken from the tree each day were actually dispersed and undamaged—a good indication of the high cost of seed dispersal.

Plate 10-7. The Blue-crowned Trogon (Trogon curucui) is considered a good seed disperser. Photo by Sean Williams.

Fruit Consumption Promotes Sociality in Purple-throated Fruitcrows The Purple-throated Fruitcrow (Querula purpurata; plate 10-8) feeds on both insects and fruits, but David Snow showed that its frugivorous habits may have been instrumental in the evolution of its intricate social behavior. Not a true crow, this species is a member of the highly frugivorous cotinga family (chapter 15). Purplethroated Fruitcrows live in small, closely related communal groups of three or four individuals that roam the forest together in search of preferred species of fruiting trees. Within the social group there is virtually no aggression, and all members of the group appear to cooperate in feeding the nestling bird (they have clutches of only one). Given the degree of relationship among the group, this form of cooperative nesting behavior has the potential to benefit even those individuals that are not parents of the nestling bird. The nest is in the open and is vigorously defended by the entire group.

Plate 10-8. This male Purple-throated Fruitcrow is displaying to another member of his group. Photo by Sean Williams.

The group organization of Purple-throated Fruitcrows likely assists them in both locating and defending trees laden with fruit. Because the fruit that the birds locate is normally sufficient for all of them, there is little or no competition among the birds, a factor likely important in the initial evolution of their social organization.

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for one individual to defend the resource, excluding all others. Therefore it is not surprising to encounter flocks of tanagers, parrots, or toucans. Fruit-eating mammals also tend toward sociality. Pacas, coatis, and peccaries are organized in bands and herds. Because fruits are generally easy to locate and require virtually no “capturing” time and effort, frugivorous birds tend to have much free time. The male Bearded Bellbird (Procnias averano), a South American species that is entirely frugivorous, spends an average of 87% of its time on a perch in the forest subcanopy or canopy calling females to mate (see “Fruits: The Evolutionary Stimulus for Sexual Selection,” below). Another South American frugivorous bird, the male White-bearded Manakin (Manacus manacus; plate 10-9), spends 90% of its day courting females!

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Plate 10-9. The White-bearded Manakin spends the majority of its time courting females. This one appears to be awaiting a female to court. Photo by John Kricher.

The Abundance of Frugivores Frugivorous birds are more abundant per species compared with insectivorous species because fruit biomass is typically high and therefore supports high populations of fruit-consuming species. Insects, on the other hand, are widely dispersed, often difficult to find and capture, and represent far less overall biomass, so insectivorous populations are smaller. In one area of rain forest in Trinidad, David Snow netted 471 Goldenheaded Manakins (Ceratopipra erythrocephala) and 246 White-bearded Manakins, a total of 717 birds. In this same area he caught 11 species of tyrant flycatchers (most of which are strongly if not entirely insectivorous), but their combined abundance did not equal that of the two frugivorous manakins. Flycatchers must focus on a more narrow resource spectrum that requires them to search, locate, and capture their prey. But not all flycatchers catch flies. A study by Barbara Snow and David Snow of the Ochre-bellied Flycatcher (Mionectes oleagineus; plate 10-10) on Trinidad showed that the species is undergoing a major evolutionary diet shift. Though it is a tyrant flycatcher, it now feeds almost exclusively on fruit. The Ochre-bellied is the most abundant forest flycatcher in Trinidad, and its numerical success is attributed to its diet of fruit. The Snows hypothesized that as the resource base for the Ochre-bellied Flycatcher expanded, its population increased. Studies throughout the tropics confirm the high biomass of frugivorous bird and mammal species in

Plate 10-10. The Ochre-bellied Flycatcher, here part of a bird banding study in Belize, is unusually abundant, presumably because it has shifted to a diet primarily of fruit. Photo by John Kricher.

lowland humid forest. This is not surprising. Theodore H. Fleming and colleagues determined that between 50 and 90% of tropical trees and shrubs (depending on the site) have seeds primarily dispersed by frugivorous vertebrates. True, there are fewer frugivorous species overall than insectivorous species, but nonetheless somewhere between 80 and 100 species of primarily frugivorous primates, bats, and birds typically occur in forest sites ranging from Central America to Amazonia.

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Peccaries and Palm Seeds Miles Silman and colleagues, in a study at Cocha Cashu Biological Station in Amazonian Peru, demonstrated how a single species of seed predator affects the abundance and distribution of a tree species. White-lipped Peccaries (Tayassu pecari; plate 10-11) disappeared from the region in 1978 and reappeared in 1990. Peccaries feed heavily on large fruits, including those of palms, in which case they act as seed predators, destroying the seed. Starting in 1978, researchers did transect counts of the number and spatial distribution of seedlings from the palm Astrocaryum murumura, a dominant tree species in the region. The counts were repeated in 1990, when peccaries had been absent for 12 years, and in 1999, after peccaries had reoccupied the region for 10 years. In the years of peccary absence, seedling density of Astrocaryum murumura increased 1.7-fold. Once peccaries returned, seedling density declined to what it had been when peccaries had been present Plate 10-11. White-lipped Peccary. Photo by before. The researchers realized that a single species of seed predator, John Kricher. in this case White-lipped Peccary, exerted a significant influence on the demography of Astrocaryum murumura. These results emphasize how species interactions may have major effects on forest species composition. Peccaries are discussed more in chapter 16.

A diet of fruit is not without potential problems. Interspecific competition is common, because fruit is clustered on one or a few trees, which attract crowds of frugivores. Nutritional balance may be lacking (see “The Oilbird,” below). Seeds, not surprisingly, tend to be indigestible, and many fruits tend to be watery, containing little protein relative to carbohydrate. Small birds eat small, carbohydrate-rich fruit, and many must diversify their diets to include proteinrich animal food. Large frugivores such as toucans eat many different-size fruits, including those rich in oil and fat, but they also eat many forms of protein-rich animal food.

The Oilbird: A Unique Frugivore The Oilbird (Steatornis caripensis), often called Guácharo in its native range, from Trinidad and northern South America to Bolivia, is the only species in the family Steatornithidae. Its unique evolution was revealed in a classic two-part study by David Snow. It is a large nocturnal bird, its body measuring 46 cm (18 in) in length, its wingspread nearly 1 m (39 in). The owl-like plumage is soft brown with black barring and scattered white spots (plate 10-12). Its broad head features a large hooked bill and bulging, wide eyes. Oilbirds are fascinating enough as individuals, but they come in groups. Colonies are widely scattered

throughout the species’ range, as the birds live in caves, venturing out only at night to feed on the fat-rich fruits of palms as well as the fruits of plants belonging to the laurel family (Lauraceae), often obtained only after flying long distances from the cave. Fruits are plucked on the wing: the birds hover at trees, picking off fruits with their sharply hooked beaks. Oilbirds probably locate palms by their distinctive silhouettes and are thought to find aromatic Lauraceae fruits through olfaction. Enter an Oilbird cave and be greeted by a cacophony of sound, a chaotic chorus of growls and screams emitted by the restless birds (plate 10-13). In the dark, dank cave the flapping wings of the disturbed, protesting hosts conjures up thoughts of tropical demons awakened. Soon, however, the birds calm and flutter back to their nesting ledges, snarling as they resettle. You hear some odd clicking noises punctuating the din. These vocalizations are one of the features that make Oilbirds unique. They are among the very few birds capable of echolocation, the same technique by which most bats find their way in the dark. Only a few species of Asian swiftlets, unrelated to Oilbirds, also echolocate. The clicks are sonar signals, sent out to bounce off the dark cave walls and direct the birds’ flight. Oilbird echolocation lacks the sophistication found in that of bats, but it is adequate to keep the birds from crashing against the cave walls as they fly about in total darkness.

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Plate 10-12. Oilbird on its nest. Photo by Edison Buenaño.

Oilbirds are closely related to the diverse family of nightjars (Caprimulgidae; chapter 15), of which the Eastern Whip-poor-will (Caprimulgus vociferus) is a common example. However, nightjars, unlike the Oilbird, are all insectivorous, are not colonial, and do not live in caves. How did the Oilbird evolve frugivory, sociality, and its cave-dwelling habit? David Snow offered an evolutionary scenario for Oilbird evolution that begins with a critical diet shift from insects to fruit. Snow hypothesizes that Oilbirds were originally “normal” nightjars feeding on insects. However, large fruits offer a potentially exploitable high-calorie resource, especially to a nocturnal bird. Furthermore, there are few large bats in the Neotropics. That is not the case in the Paleotropics, where many species of megachiropteran bats (flying foxes) feed on large fruits. In the Neotropics, many microchiropteran bats are frugivores, but none are comparable in size to an Oilbird, so they cannot eat the fruits that Oilbirds devour. Oilbirds thus became Oilbirds when their ancestors shifted to a diet of fruit (fig. 10-1). Frugivory initiated a cascade of adaptations that profoundly affected the evolution of the Oilbird (plate 10-14). The birds’ olfactory sense became enhanced as it provided an advantage in locating aromatic fruits. Social behavior began to evolve because fruits are a patchy resource and birds would tend to come

Plate 10-14. Oilbirds have hooked beaks, which they use to pluck fruits as they hover. Photo by John Kricher. Oilbird Evolution According to (mostly) David Snow Insect diet

Selects against territoriality

Fruit diet

Vision - palms Olfaction - laurels Longer development period before fledging Sociality

More highly conspicuous ground nests due to seed defecation

Nest colonially in caves Time?

Plate 10-13. Dunston Cave in Trinidad, where Oilbirds are easily seen. Note the spindly plants that have germinated at the lower left. They sprouted from seeds dropped by the birds. Photo by John Kricher.

Predator free Echolocation Larger clutch sizes

100 days from egg

Fledging

Occupy cave and same nest all year (mating occurs for life?)

Figure 10–1. This diagram shows the hypothesized evolution of Oilbirds. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

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together at fruiting trees. More important, however, is the fact that a diet of palm and laurel fruit, though rich in calories, is nutritionally unbalanced. Consequently, nesting time is prolonged, and incubation of each egg lasts just over one month. Once Oilbirds hatch, they fatten up immensely in the nest due to a buildup of fat from the oily fruits. But they take a long time to acquire sufficient and proper protein to grow bones, nerve, and muscle. Two months after hatching, a juvenile may weigh 1.5 times either parent’s weight, but it still has not left the nest. The name Oilbird refers to the fact that juveniles put on so much fat that they can be boiled down to render the oil. Indigenous people occasionally used them for torches since they burn so well! The total time it takes an Oilbird to go from newly hatched egg to fledging and independence is nearly 100 days, compared with about 30 days for insectivorous nightjars. It takes six months for a clutch of four Oilbird eggs to develop from embryo to flight. Such an extended development time makes it risky (even absurd) to nest on the forest floor, the traditional nightjar nesting site. Snow notes that the defecated seeds that would surround a ground nest would serve to bring attention to nesting birds. Cave dwelling offers more protection for the nest, but caves are also very patchily distributed resources. Once Oilbirds took up cave dwelling, they became colonial, social species. Cave dwelling selected for the development of echolocation and also for a larger clutch size, one more typical of birds in the temperate zone. Most tropical birds lay only one or two eggs in a given nest, but birds in the temperate zone have clutches often of four or five eggs or more. Predator pressure is likely to be a major reason for the small clutch sizes in the tropics, since nests can be more secretive if there are fewer mouths to feed. Given the safety of caves, Oilbird nests are not under severe predator risk, and clutch size is normally four eggs. The nest is built up with droppings from the birds and located on a cave ledge. Thin, yellowish, light-starved seedlings sprout from defecated seeds around the nest. Oilbirds are thought to pair for life. The Oilbird is an important seed-dispersing species. In an exhaustive study centered in Cueva del Guácharo (Guácharo Cave) near the town of Caripe, in Monagas, a mountainous, heavily forested region in northeastern Venezuela, Ricardo Roca, using radio-tagged Oilbirds, demonstrated that the birds have home ranges that encompass up to 96.3 km2 (37.2 mi2) and may have to fly up to 150 km (nearly 95 mi) between feeding

Plate 10-15. Masked Tityra male at its nest cavity. This species has been shown to be an efficient seed disperser. Photo by James Adams.

sites. Indeed, dispersing individuals fly even farther in search of food, up to 240 km (150 mi) in a single night. Given that an adult Oilbird requires approximately 50 fruits daily, Roca calculated that the entire colony he studied collectively regurgitated approximately 15 million seeds each month, a biomass of about 21 tons of seeds. Roca estimated that about 60% of the seeds were dispersed in forest. Oilbirds are important species in maintaining the plant biodiversity of the forests in which they forage, and as such, merit strict conservation measures, especially around their caves.

Animal Diversity at Fruiting Trees Fruit is an important resource in both mountain and lowland forests. Nathaniel Wheelwright and his colleagues did a comprehensive survey of fruiting trees and fruit-eating birds at Monteverde Cloud Forest in Costa Rica and learned that 171 plant species bore fruit that was fed upon by 70 bird species. Some birds depended heavily on fruit, others consumed it more casually. Among the birds were three woodpecker species, nine tyrant flycatchers, eight thrushes, eight tanagers, and nine finches, as well as toucans, pigeons, cotingas, and manakins. Though some birds were observed to feed on fruit only rarely, it was clear that fruit represents an important resource for a large component of the avian community. In comparison,

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Gulpers and Mashers Birds are selective about the size of the fruits they eat and how they consume them. Species such as toucans, aracaris, and toucanets pluck fruit, juggle it in the bill, and then often reject it by dropping it. Large fruits are particularly at risk of rejection and may be found scarred by bill marks. Nathaniel Wheelwright hypothesized that plants are under strong selection pressure to produce small to medium-size fruits, as larger ones are rejected by most bird species except those with the widest gapes. Thus large fruits will tend to be selected by large birds such as curassows and guans. Large fruits permit more energy to be stored in the seeds, an advantage once dispersal and germination have occurred. Studies by various researchers in Costa Rica indicated two basic methods by which birds devour fruit. Anyone can observe these methods in the field. Some birds (mashers) mash up the fruit, dropping the seeds as they do, while others (gulpers) gulp the fruit whole, subsequently either regurgitating or defecating seeds (plates 10-16–17). Mashers are mostly finches and tanagers, and gulpers are toucans, trogons, and manakins. Mashers appear more sensitive to taste than gulpers, showing a distinct preference for fruits rich in sugars. Gulpers swallow fruit whole and appear taste insensitive.

at the lowland forest at La Selva Biological Station, of 185 tree species studied, 90% produce fleshy fruits; of those, approximately 50% are primarily bird dispersed, 13% bat dispersed, and the remainder dispersed by other mammals, such as monkeys and agoutis. A study of fruit dispersal of Casearia corymbosa (a species of the willow family, Salicaceae) in Costa Rica conducted by Henry Howe in 1977 recorded 21 species feeding on the tree’s fruits, none of which really contributed to seed dispersal. These species consumed the fruit at the tree and so were essentially useless as seed dispersers. But one bird species, the Masked Tityra (Tityra semifasciata; plate 10-15), was considered an efficient seed disperser. This thrush-size black-and-white bird fed heavily on Casearia fruits and regurgitated viable seeds at considerable distance, well outside the seed shadow of the parent tree. Howe’s work is one of many studies to demonstrate that fruiting trees attract a diverse array of birds, mammals, and reptiles (e.g., iguanas) but that not all of these species, or even most of them, are suitable for efficient dispersal of seeds.

Plate 10-16. This Grayish Saltator (Saltator coerulescens) is an obvious example of a masher. Photo by John Kricher.

Plate 10-17. This Toco Toucan (Ramphastos toco) is plucking a fruit that it will then gulp down whole. Photo by John Kricher.

Fruits: The Evolutionary Stimulus for Sexual Selection in Tropical Birds Charles Darwin developed his theory of sexual selection to account for why certain animal species, ranging from beetles to birds and mammals (including humans), show strong morphological differences between the sexes. Why would selection act differently between males and females? Among numerous bird species, males are typically brighter in plumage (a pattern termed sexual dichromatism) and often larger than females. Why females have cryptic plumage seemed an easy question to Darwin. The cryptic female plumage aids in reducing the risk of discovery by predators. But why are males so colorful? Adding to this mystery was the fact that elaborately colored males often augment their already gaudy selves by engaging in bizarre and attention-getting courtship displays. Sexual selection evolves through two pathways operating separately or simultaneously. One is male– male competition for access to females. This helps account for why males tend toward larger body size than

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females. The other is female choice of males that exhibit characteristics signaling high fitness. Characteristics of bright plumage in birds may represent generations of female choice. In the tropics sexual selection in birds is evident in numerous bird families but perhaps the most dramatic examples are among the cotingas (Cotingidae) and manakins (Pipridae), both of which depend heavily on diets of fruit.

An Example: The Guianan Cock-of-the-rock The Neotropical Guianan Cock-of-the-rock (Rupicola rupicola) is one of many marvels that draw people, in particular those with a fondness for birds, to the Neotropics. This large, nearly chicken-size cotinga provides an outstanding example of sexual selection. As the name suggests, the Guianan Cock-of-the-rock is found in northeastern South America (Venezuela, Guyana, Suriname), extending well into the Brazilian rain forest. Pepper Trail, following a well-known series of studies on cotingas by David Snow, documented the elaborate courtship of this species in a classic series of studies. Males are chunky and have brilliant golden-orange plumage, with black on the wings and the short tail (plate 10-18). In flight they resemble winged, Day-Glo orange footballs. Beaks, legs, eyes, and even the very skin is bright, vivid orange. The male’s already striking plumage is further enhanced by delicate, elongate orange wing plumes and a thick, crescent-like fan of feathers extending from the base of the bill to the back of the neck. Females are dull brown, with neither the wing plumes nor the head fan. Males gather in the rain forest understory in confined courtship areas called concentrated leks. Each male clears an area of ground in which to display and defends perches in the vicinity of its display site. The lek becomes crowded, occupied by several dozen males, spaced as closely as 1.5 m (5 ft) apart. When a female approaches a lek, each male displays, first by landing on the ground and posturing to her. Each displaying cock strokes its wing plumes and turns its head fan sideways, presenting its profile to the female while staring at her with its intense orange eyes. The object of each cock’s display is obviously to mate, presumably by suitably impressing the female. Females do not appear to be easily impressed. A hen will typically visit a lek several times before engaging in copulation. These visits,

Plate 10-18. Male Guianan Cock-of-the-rock. Photo by Andrew Whittaker.

called mating bouts, always excite the males to display. Ultimately only one male on a lek will get to mate with a visiting female, who may return to mate with him a second time before laying eggs. No extended pair-bond is formed, only a brief coupling. The cock returns to the lek, continuing to court passing hens, while the newly fertilized hen attends to nest building, egg laying, incubation, and raising the young. Darwin reasoned that in some species female choice was the dominant factor in selecting male appearances. Put very simply, males are colorful (or musical or noisy or perform complex dances) because females have tended through generations to mate mainly with males having these features. Since plumage color is heritable (as are behavioral rituals), gaudy coloration was selected for and continually enhanced. Recent work in sexual selection suggests that females learn much about the evolutionary fitness of males by signals communicated both by plumage condition and male courtship behavior. The appearance and behavior of males has been shown to be an honest signal of good health, correlating with lack of parasites, strong immune system, agility, and coordination. In other words, females are not being frivolous in driving male evolution toward more elaborate, gaudy plumage and exotic behavior but are looking intently for reliable signals, expressed in plumage and behavior, of male fitness. The other facet of sexual selection recognized by Darwin is that males must compete among themselves for access to females. Male–male competition takes

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numerous forms from one species to another: dominance behavior, guarding females, active interference with other males’ attempts to mate, injury to other males, or merely being “sneaky” and mating before other males can react. Bright, conspicuous plumage may contribute to a male’s success by intimidating other males and thus making it easier to gain the attentions of a female. Sexual selection has costs for both males and females. In the case of the Guianan Cock-of-the-rock, although the hen exercises choice in the mating process, she is left solely responsible for the chores of nest building, incubation, and caring for the young. These are risky, energy-consuming tasks. Males may at first glance seem luckier, rewarded by a life of lust in nature’s tropical singles bar, the lek. The combination of male–male competition plus dependency on female choice makes life surprisingly difficult for most males, however. Though some cocks are quite successful, mating frequently, others spend their entire lives displaying to no avail. They eventually may die genetic “losers,” never selected even once by a hen. In Suriname, Pepper Trail found that 67% of territorial males failed to mate at all during an entire year. In a lek that contained 55 cock birds, the most successful male performed an average of 30% of the total number of annual matings, and many of the cocks never mated. Such is the cost of sexual selection for males. In reproductive terms, most females do mate, though success in fledging young may certainly vary considerably among females. Some males habitually disrupt the mating of others. Trail found that aggressive males that disrupted copulations by other males fared better in subsequent mating attempts. He learned that males that were confrontational “were significantly more likely to mate with females that they disrupted than were nonconfrontational males.” He hypothesized that the cost of confrontation in terms of energy expenditure, loss of time from the aggressive bird’s own lek territory, plus risk of actual retaliation kept direct confrontational behavior from becoming even more manifest among the birds. On the other hand, Trail found adult fully plumaged males remarkably tolerant of juvenile males that were still plumaged in drab colors, resembling females. Yearling males would actually attempt to mount adult males as well as females in a crude attempt at mating. Adult males did not respond aggressively to these misguided efforts, possibly because yearling plumage, being drab, does not stimulate an aggressive response.

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The elaborate plumage and courtship behavior of the Guianan Cock-of-the rock is not unique. Most members of the Neotropical Cotingidae (65 species) and Pipridae (51 species) families have colorful, often gaudy males and perform elaborate courtship behaviors. All of these species rely heavily on a diet of fruit. Some hummingbird species such as the hermits also form courtship leks. David Snow and Alan Lill have each independently suggested possible scenarios for the “release” of males from nesting chores (such as feeding young or assisting in nest building), thus initiating the male– male competition and pattern of female choice that resulted both in the gaudy plumages and the elaborate courtship behaviors. Snow points out that cotingas and manakins feed so heavily on fruit that they are easily able to secure adequate daily calories and need devote only a small percentage of their time to feeding. Fruit is abundant and easily collected; it does not have to be stalked or captured and subdued. This makes access to females the limiting resource, initiating an evolutionary trajectory of sexual selection. In addition, a diet of fruit aids in permitting the birds to metabolically synthesize the colorful pigment that characterizes male plumage. A fruit diet may be the primary driver of evolution of sexual selection in some groups of tropical birds. But nest predation is also a factor. A largely frugivorous diet has metabolic costs as well as benefits. Incubation time is relatively long and nestling growth rates slow in frugivorous birds, because fruit is not well balanced nutritionally for a baby bird (low in protein but high in fat and carbohydrate). Alan Lill suggests that because of the slow development time brought about by a diet of fruit (recall the Oilbird discussion), nest secrecy is of paramount importance. Heavy egg and nestling predation are best minimized by having only one bird, the cryptically colored female, attend the nest. A male’s presence at the nest could potentially be detrimental to raising young, since one bird can easily find sufficient food for the small brood (at most two nestlings), and a second bird might inadvertently reveal the presence of the nest to potential predators. Relative to insectivorous bird species that also have small clutch sizes in the tropics, frugivores require more time to fledge young, because the diet is unbalanced for nestling growth. Male absence actually increases the probability of egg and nestling survival. At the nest, males are dispensable, not needed for raising young.

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The Amazing Dancing Manakins: Don’t Miss Them Male manakins are glossy black with bright yellow, orange-red, scarlet, or golden heads and/or throats; some also have bright yellow or scarlet thigh feathers, and others have deep blue on their breasts and/or backs and long streamer-like tails. A few species are sharply patterned in black and white. But fancy feathering notwithstanding, it is dancing at which these birds excel. The White-bearded Manakin (Manacus manacus) has been well studied and provides a fine example of how manakins go about their amazing courtship efforts. The male has a black head, back, tail, and wings but is white on the throat, neck, and breast (plate 1019). Its name comes from its throat feathers, which are puffed outward during courtship, forming a kind of beard. Females are greenish yellow. Thirty or more males may occupy a lek, a single small area in the forest understory. Each male makes his own “court” by clearing an oval-shaped area of forest floor about 1 m (39 in) across. Each court must contain two or more thin vertical saplings, as these are crucial in the manakin’s courtship dance. The male begins courtship by repeatedly jumping back and forth between the two saplings, making a loud snap with each jump. The sound comes from modified wing feathers that are snapped together when the wings are raised. The snapping of many males is audible for quite a distance, drawing females to the lek. In addition to the snap, the male’s short wing feathers make an insect-like buzzing when he flies, and thus active manakin leks can become a buzzing, snapping frenzy when a female visits. The intensity of the male’s jumping between saplings increases until he suddenly jumps from sapling to ground, and then appears to ricochet back to another sapling, from which he slides vertically downward, like a fireman on a pole. David Snow’s film footage of the slide revealed that successful males slide right down to a female perched at the base of the sapling pole. Copulation is so quick that Snow only discovered the presence of the female in the film. He never saw her while he was witnessing the event! Following copulation, the female leaves the lek and attends to nesting. The male starts to dance again. Male manakins spend most of their adult lives at the lek. Some, as in the case of the cock-of-the-rock, are probably consistently successful and mate often. Others may never mate. Observations of banded male White-

Plate 10-19. A male White-bearded Manakin on one of its display saplings, its full “beard” showing. Photo by Jill Lapato.

Plate 10-20. The Swallow-tailed Manakin (Chiroxiphia caudata) of southeastern South America is one of five species of its genus. Males of these manakins coordinate their mating dance in pairs (and sometimes larger numbers) while courting a female. Photo by Andrew Whittaker.

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bearded Manakins in Trinidad have revealed that life on a lek is usually fairly long for individual birds. Some live for a dozen years or more, a very long life span for such a small bird. Males generally leave the lek only to feed on ripe fruits. Another Trinidad species, the Golden-headed Manakin (Ceratopipra erythrocephala), is not a lek dancer; instead, each male displays in his own territory. As with the White-bearded, the male Golden-headed begins its dance darting back and forth on selected twigs, calling zlit as he does so. Unlike the Whitebearded, which dances close to the ground, the Golden-headed usually displays in an understory tree. The cock becomes increasingly vigorous in his dancing, crouching, his body at a 45° angle as he slides along a horizontal twig. His glowing orangy head and sleek black plumage are displayed very conspicuously, but more is yet to come. When a female arrives, the male skitters along the branch toward her, but tail first! As he advances, he bows, spreads his wings, and exposes bright yellow thigh feathers, all the while pivoting his body back and forth. The climax of the dance comes when the male suddenly flies from the dance branch and quickly returns, inscribing an S-shaped curve as he lands, with wings upraised, before the female. Various vocalizations accompany the performance. The blue manakins (genus Chiroxiphia; plate 10-20) carry courtship dancing to the extreme. These manakins dance as a team. Two males engage in a coordinated jumping dance in which both birds occupy a thin horizontal branch, one jumping and hovering while the other crouches on the branch, the other jumping and hovering when the first lands. As they dance, they vocalize. The dance may occur in the presence or in the absence of a female, the males seeming to practice when a female is not present. The dance ends when one of the males bows before the hen, head turned exposing the bright red brow, the blue back upraised. In two species, up to three males coordinate a complex dance before a single female. The three dancers align themselves horizontally on a thin branch, shoulder to shoulder before the female, each male facing in the same direction. The male farthest from the female jumps up, inscribes a 180° angle and lands nearest the female, next to the other males. He immediately turns around, so once again all three dancers face the same direction. A second dancer, again the farthest from the female, repeats the first dancer’s performance, and so on. The dance happens rapidly, a spinning “wheel” of

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Plate 10-21. Wire-tailed Manakin male. Photo by Andrew Whittaker.

Plate 10-22. Wire-tailed Manakin males in display. Photo by Andrew Whittaker.

dancing males, jumping, displaying, and vocalizing in total coordination. No other case of such elaborate team dancing is known in birds. The termination of the performance occurs when one of the males vocalizes sharply, the effect of which is to “turn off ” the other two males. The dominant male then erects his red head feathers as he perches before the female. She and he fly off into the underbrush. One species, the Wire-tailed Manakin (Pipra filicauda), adds a different element to the roster of manakin courtship techniques. Males have stiff tail feathers that terminate in long, delicate filaments (plate 10-21). Wire-tailed males dance in teams of two, rather like the blue-backed species (plate 1022). However, when the dominant male approaches a female, he performs a twisting display in which he

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rotates his posterior side to side, gently touching the female on her chin with his tail filaments. Females apparently respond well to this maneuver, for a female will typically slide toward a male to receive the tail brushing. This is the only known example of tactile stimulation among manakins, and the unique tail is a product of sexual selection. And finally, there is the Club-winged Manakin (Machaeropterus deliciosus; plate 10-23). Like the White-bearded Manakin (described earlier), it has uniquely adapted wing feathers, in this case the secondary feathers of the inner wing, that make a remarkable sound during the courtship display. These feathers are vibrated at about 100 times per second (twice the speed of hummingbird wings), allowing the displaying male to make a highly complex, violin-like sound, an amazing sonorous display. Should you be curious, there are numerous videos on YouTube that show various manakin species, including those described in these accounts, performing their various courtship behaviors. Why do several male manakins cooperate in courting a single female when as a rule only one will get to mate with her? Females are likely the limiting resource for males, living as they do with a relative abundance of food. In competition for females, one male will emerge to be consistently dominant over the others. A subordinate male is best served by biding his time until he manages to replace the dominant male. A successful dominant male will continue to attract females to the display area, and thus subordinate males will have access to females should something happen to the dominant male, or if they are lucky, they may be able to mate on occasion when the dominant male is otherwise occupied.

Why Leks? Given that a combination of factors has released males from attending nests, why have some species organized their courtship bouts in leks, especially the tightly clumped leks that are typical of manakins and cockof-the-rocks? Several hypotheses have been suggested. One, called the female preference model, argues that females “prefer” groups of males when making their selections of with whom to mate. A male that stayed away from the lek would not attract any female, thus males have no choice but to join a lek. Another

Plate 10-23. The Club-winged Manakin making its violin-like courtship sound with it uniquely adapted wing feathers. Photo by Edison Buenaño.

suggestion is that males might associate in leks because the lek area happens to be a place where females, for whatever reason, frequently occur. This idea, termed the hotspot model, presumes that leks form rather accidently, as males gather where they are most likely to encounter females. Both hypotheses place strong emphasis on female choice as causal to lek formation. Yet another, dubbed the hotshot model, emphasizes the role of male–male dominance and interactions between dominant and subordinate males on a lek. “Hotshots” are individuals that control leks. Subordinates occasionally benefit from disrupting leks, but mostly they bide their time while slowly advancing toward dominance. Thus novice males have little choice but to begin as subordinates, working their way up through the ranks to attain dominance status before they can reproduce. Subordinate birds congregate around the dominant males, since they have no hope for mating otherwise. Dominance among males can be subtle, but it is real, and females will almost always select a dominant male with whom to mate. No model for lek evolution has as yet been shown to be conclusive. Indeed, evolutionary biologists refer to the paradox of the lek, an admission that leks are not easy to explain. The lek is by no means exclusively a tropical phenomenon. Leks occur among some shorebirds that nest in the Arctic, among grouse, and among various other birds as well as some mammals. In a provocative paper, Richard Prum argued that evolutionary events dating back perhaps 14–35 million years ago, when frugivory may have permanently released males from parenting duties, may have set in

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motion an evolution of lek behavior such that lekking is now more readily explained by phylogenetic history than by any immediate selection pressures. Prum, perhaps a bit tongue in cheek, writes, “For manakins and a large majority of the lekking birds, the proximate answer to the ‘paradox’ of why they breed in leks is because their parents did; the ultimate answer lies in the ancient past when these behaviors initially evolved.” There are many areas in the Neotropics where you can directly observe various manakin and cotinga species at their leks, engaging in their sexual-selectiondriven behavior. Bearing witness to courting manakins, bellbirds (chapter 15), and cock-of-the-rocks is one of the outstanding opportunities awaiting the Neotropical naturalist (plate 10-24).

Fish as Amazonian Seed Dispersers Fish disperse seeds? That might seem impossible but is far from it. It all has to do with the flood cycle, an annual event throughout Amazonia. Floodplain forests within the Amazon Basin cover an area of approximately 150,000 km2 (58,000 mi2), which is roughly equivalent to the size of the state of Florida. Called várzea in Amazonia (chapter 12), floodplain forests are inundated by the annual flood cycle. Depending upon location, floodplain forests may be submerged anywhere from two to 10 months of the year. The Amazon forest itself (from Manaus eastward), for example, is flooded for about six months, whereas the upper Rio Madeira is in flood for only two to five months annually. Michael Goulding, a reigning expert on Neotropical fish, estimated in the 1980s that there are more than 2,400 fish species inhabiting the waters of the Amazon and its tributaries, and up to 800 additional species may remain yet to be formally described. Approximately 40% of the species thus far described are members of two groups, characins (family Characidae) and catfish (order Siluriformes, numerous families), and many among these multitudes include favorites of the aquarist. During the flood cycle, fish have direct access to forest. Many become fruit and seed consumers and some act as important seed dispersers. Goulding estimates that approximately 200 species of fish consume fruits and seeds in Amazonian waters, far more species than do so in tropical Africa or Asia. A

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Plate 10-24. Wire-tailed Manakin male celebrating the family tradition of display. Photo by Andrew Whittaker.

frugivorous diet is facilitated by the flood cycle, which enables fish to swim well within the gallery forest and forage for dropped fruits, many of which float at the surface, making them easy to find and consume. There is a seasonal shift in diet among characin species in which they move from an omnivorous diet that includes zooplankton and various plants and algae to essentially a diet of fruit when the forest is flooded.

The Tambaqui The Tambaqui (Colossoma macropomum) is an inhabitant of blackwater rivers and igapo forests (flooded forests on poor soil). This bass-like fish is an important seed disperser, particularly for Hevea spruceana, a rubber tree, and Astrocaryum jauari, a palm species. Both of these tree species are widely distributed, are relatively abundant, produce large seed crops, and have fruits that are laden with fat and protein but that are encased within hard nuts that many animals are unable to break. The seeds of the rubber tree are contained in large capsules that eventually pop open and effectively toss their seeds as far as 20 m (66 ft). The seeds float, and Tambaquis gather around rubber trees where seeds are being released. The Tambaqui is an oval-shaped characin, weighing as much as 30 kg (66 lb), and has specialized, rounded, molar-like teeth capable of crushing and grinding very hard fruits. Tambaquis feed almost exclusively on fruits for the first five months of the flooding season. The fruits contain sufficient protein and fat that the fish is able to survive during periods of low water from fat stored during its flood cycle fruit consumption.

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Other Fruit-consuming Fish Even the notorious (and carnivorous) piranhas are known to consume seeds, removing the husk and masticating the soft seeds within. Piranhas (plate 1025) belong to the characin family (Characidae), and many characins are seed predators, possibly the most important seed predators in the flooded forests. Catfish (plate 10-26) are not as destructive to seeds as characin species because they gulp the fruit whole rather than macerate it. In this sense catfish are the piscine equivalent of birds such as toucans, digesting the fruit pulp while the seed passes out of the alimentary canal unharmed. Plate 10-25. Piranhas are among the many kinds of Neotropical fish that on occasion act as seed dispersers. Red Piranhas (Pygocentrus nattereri) are shown. Photo by John Kricher.

Seeds often contain toxins, and thus, though fruit pulp is digested, seeds are not. Seed toxicity enhances the probability of dispersal, as the seeds pass through the digestive system of the fish. At the close of the flood cycle, when the waters drop, adult Tambaquis migrate from nutrient-poor blackwaters to nutrient-rich whitewaters to spawn. Juvenile Tambaquis feed on zooplankton, not fruit, in the whitewaters along várzea floodplains and lakes, where the rich soil provides the water with an abundance of sediment (chapter 6).

Pollination: Animals as Surrogate Sex Organs Brightly colored flowers are ubiquitous throughout most terrestrial ecosystems on Earth, and are certainly well represented in the Neotropics. Flowers invite pollinators as surely as the Golden Arches invite hamburger seekers. Pollination of plants by various animals, a clear example of coevolution, is widespread. Many flowering plants, particularly in the tropics, are dependent upon insects, birds, or bats to facilitate fertilization. Animals use flowers as a food source, ingesting nectar and, in some cases, pollen. As they move

Plate 10-26. Species such as these Amazonian catfish are often important seed dispersers. Photo by John Kricher.

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Plate 10-27. Bees are attracted to the flowers opening on this Kapok Tree (Ceiba pentandra; chapter 7). Many species from bees to bats aid in cross-pollination of Kapoks. Photo by Dennis Paulson.

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Plate 10-28. This Eulaema polychroma is a “long-distance” euglossine bee, shown here stocking up on pollen (note the pollen bulge beneath the abdomen). Photo by Dennis Paulson.

Darwin, Pollination, and Coevolution Charles Darwin, in On the Origin of Species, wrote about the coevolved relationship between bees and the clover they pollinate: “The tubes of the corollas of the common red and incarnate clovers (Trifolium pratense and incarnatum) do not on a hasty glance appear to differ in length; yet the hive-bee can easily suck the nectar out of the incarnate clover, but not out of the common red clover, which is visited by humble-bees alone.” Darwin discussed pollination and coevolution further in a monograph, On the various contrivances by which British and foreign orchids are fertilized by insects, and on the good effects of intercrossing, published in 1862. Darwin’s clear understanding of the interdependency between various plants and their specific pollinators and of how the behaviors of the insects, as well as the morphologies of both insects and plants, have evolved from the exertion of mutual selection pressures makes him the person who discovered coevolution.

from plant to plant, animals disperse pollen, making cross-pollination efficient and ensuring reproduction of the plants. This relationship is mutualistic—both plant and pollinating animal benefit. Animal pollination is widespread throughout tropical ecosystems, particularly forests. As mentioned earlier, in contrast to temperate forests, where wind pollination is common, rain forests are sufficiently dense that wind pollination would tend to be ineffective, except perhaps among emergent trees. It is not surprising that grasses, sedges, pines, and other species of open areas such as savannas are the only tropical plant groups characterized by wind pollination. Insects and vertebrates are major pollinators throughout the tropics. Among insects, pollination is accomplished by numerous species of bees, flies, beetles, butterflies, and moths (plate 10-27). Among vertebrates in the Neotropics, hummingbirds (Trochilidae, about 350 species) feed most heavily on nectar, but other

species including tanagers and orioles also utilize nectar and may act as cross-pollinators. Hummingbird-pollinated flowers take many shapes, but some have long tubes and are red, orange, purple, or yellow. In contrast, bat-pollinated flowers are often white (easy to locate in the dark) and may have a musky odor, an attractant to the bats. Many flowers are visited by a variety of vertebrates and insects that are all potential pollinators. Pollinators that fly long distances are most advantageous to plants, as such behavior helps ensure effective cross-pollination between widely separated plants. Euglossine bees (plate 10-28) are long-distance fliers, and the males pollinate certain widely separated orchids. Compounds in the orchid flower that are absorbed by the male bees contribute to the longevity of the insects. Daniel Janzen documented that male euglossine bees live up to six months, a long life for a bee, adding to the likelihood of numerous long flights that result in successful pollination.

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Plants and Hummingbirds: A Coevolution Hummingbirds have evolved mutualistic relationships with plants, feeding on nectar but facilitating crosspollination. The impressive diversity of sizes and bill shapes exhibited by hummingbirds (plates 10-29–30) is directly attributed to the diversity of flower shapes and patterns that offer nectar, a clear example of adaptive radiation (chapter 8). Hermits feed heavily on the nectar of heliconia flowers. Many heliconias produce relatively constant amounts of nectar per flower but one heliconia studied by Peter Feinsinger in Costa Rica, Heliconia psittacorum, exhibits a bonanzablank pattern of nectar production. Some of its flowers contain abundant nectar (bonanzas), some essentially none (blanks). Many other tropical plants, especially those in open successional areas, also are bonanzablank flowerers. Hermits must visit many flowers in order to encounter one with high nectar content, thus the bonanza-blank pattern presumably aids Heliconia psittacorum in accomplishing cross-pollination. In a study of 10 successional plant species and 14 hummingbird species at Monteverde Cloud Forest in Costa Rica, Feinsinger documented that flowering was staggered among plant species, resulting in a constant nectar supply to hummingbirds. In five plant species that were closely measured for nectar volume, the bonanza pattern was evident. Feinsinger speculated that plants may conserve energy by producing large numbers of “cheap” nectarless flowers and merely a few “expensive” bonanza flowers, forcing hummingbirds to visit many flowers to find satiation. With the birds visiting many flowers, cross-pollination is promoted. Hummingbird species display a range of foraging patterns. Trapliners go from flower to flower, in a sequence, the way a hunter might visit a series of traps (plate 10-31). Some species are high-reward trapliners, which visit but do not defend nectar-rich flowers. The territorialists defend dense clumps of small flowers. Hummingbirds known as low-reward trapliners forage among a variety of dispersed or nectar-poor flowers. Other species are territory parasites; they come in two types, large marauders and small filchers. The large marauders force other hummingbirds to give ground and thus many of these are of large size (for hummingbirds). The small filchers zip in and out, grab a quick sip or two of nectar, and swiftly move on, avoiding agonistic interactions with larger species.

Plate 10-29. Hummingbirds such as this male Black-throated Mango (Anthracothorax nigricollis) have evolved a unique anatomy permitting them to extract nectar while hovering. Note the tongue partially protruding from the bird’s beak. Photo by John Kricher.

Plate 10-30. The Rufous-tailed Hummingbird (Amazilia tzacatl) occurs in forest openings, fields, and gardens from Mexico to southern Ecuador. Here it exhibits typical hummingbird feeding behavior. Photo by Nancy Norman.

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Finally there are generalists, which follow shifting foraging patterns among various resources.

Evolutionary “Cheaters”: The Flowerpiercers Flowerpiercers (a group of 16 bird species related to tanagers), like hummingbirds, consume nectar from flowers (plate 10-32). But they “cheat.” Rather than forage within the flower, where they might encounter pollen and thus aid in cross-pollination, they use their delicately upturned and hooked bills to piece the flower at its base and access the nectar without ever encountering the pollen. Flower traits have been shown to evolve not only to attract certain pollinating species but also to discourage species that are ineffective pollinators or pollen robbers. Adaptations to reduce nectar robbery include adding toxins to the nectar that discourage robbers but not pollinators, flowering at times when nectar robbers are inactive, growing near plants that offer better food sources for nectar robbers, or evolving flowers that are physically difficult for robbers to access. Some plants have evolved extrafloral nectaries that attract insects such as ants, which defend the plant from nectar robbers (chapter 11). It is important to understand that evolutionary patterns have resulting in two kinds of selection pressures on plants that utilize animals as pollen vectors. One is to evolve characteristics that attract and facilitate access by the pollinators, and the other is to evolve characteristics that defend against robbers.

Plate 10-31. Hermits, such as this Saw-billed Hermit (Ramphodon naevius) of southeastern South America, are commonly trapliners, visiting a series of flowers for nectar. Photo by Andrew Whittaker.

Chiropterophily: Using Bats as Pollinators Given the high diversity and abundance of bats throughout the tropics and subtropics, it is unsurprising that pollination of flowers by bats is common; more than 500 plant species are wholly or partly dependent on bats as pollinators. Plants adapted to host bats are termed chiropterophilous, meaning “bat-loving” (bats are in the mammalian order Chiroptera). Coevolution has occurred at behavioral, physiological, and anatomical levels in both bats and plants. Plants adapted to have bats as their primary pollinators typically have large white flowers that

Plate 10-32. The Indigo Flowerpiercer (Diglossa indigotica) occurs in cloud forest in western Colombia and northwestern Ecuador. There are 16 flowerpiercer species in South America. Photo by Andrew Whittaker.

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Pollination of the Victoria Water-lily The huge Victoria (or Royal) Water-lily (Victoria amazonica; plate 10-33) is found in quiet backwaters of Amazonian tributaries. Ghillean Prance has documented the amazing pollination, by beetles, of this striking plant species. Opening in synchrony, the large, conspicuous white flowers emit a strong odor, and are warm, up to 11° C (20° F) warmer than ambient temperature. These characteristics combine to attract beetles (Cyclocephala spp.), which enter the flower, only to become trapped inside at night, when the large petals tightly close. The imprisoned beetles feed on nectar-rich structures throughout the night, getting thoroughly sticky as they become covered with pollen. The next day the flowers open, having changed petal color from white to red, as well as lost their scent and cooled in temperature, all of which means they are no longer an attractant to beetles. The formerly incarcerated pollen-bearing beetles leave the flower and fly off to seek out another white flower from another Victoria Water-lily, where they will inadvertently deposit pollen as they feed.

reportedly emit a musky “bat-like” odor. These flowers open at night, when bats are active. Flowers may be shaped like a deep vase or may be flat and brushy, so as to load the bat’s face with pollen as it laps up nectar. Many bat flowers are cauliflorous, growing directly from tree trunks and branches. Some flowers are flagelliflorous, hanging from long, whip-like branches, while others are penduliflorous, hanging downward as streamers, a condition common in many vines. Cauliflory, flagelliflory, and penduliflory all have in common the fact that the flowers are positioned in such a manner that they are easily accessible to hovering bats. Nectar-feeding bats typically have large eyes and relatively strong vision, in contrast with insectivorous bats. The sonar sense upon which insectivorous bats depend is often reduced in nectarivorous bats, but the olfactory sense is well developed. Nectarivorous bats have long muzzles and weak teeth, both advantageous in probing deeply into flowers. Finally, they have long tongues covered with fleshy bristles that can extend well into the flower, and in some cases their neck hairs project forward, acting as a pollen scoop. The pollen from bat-pollinated plants is significantly higher in protein than that in non-bat-pollinated plants, and bats ingest pollen as well as sugary nectar. Pollen contains the amino acids proline and tyrosine, useless to the plant but important to the bats. Proline

Plate 10-33. Victoria Water-lily with flower, awaiting a beetle to pollinate it. Photo by John Kricher.

is used in making connective tissue, such as is used in wing and tail membranes, and tyrosine is essential for milk production. Once ingested, nectar helps dissolve the tough pollen coat, but bats aid this process, as their stomachs secrete extraordinarily large amounts of hydrochloric acid. Pollinating bats also sometimes drink their own urine, which helps dissolve the pollen, liberating essential proteins. The example of chiropterophily shows that coevolution may involve whole complexes of species, not merely two species evolving together, and that anatomical characteristics may be obvious, but behavioral and physiological characteristics are also part of the coevolutionary process.

Ant Farmers: The Leaf-cutter Ants (Also Known as the Fungus Garden Ants—and for Good Mutualistic Reasons) Ants are abundant and ubiquitous inhabitants of the global tropics, and many ant species have evolved coevolutionary relationships with plants. One group, the attine ants (tribe Attini), has done so with fungus,

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Plate 10-34. Leaf-cutters, or fungus garden ants, marching with their burdens of leaves are a common sight in the Neotropics. Photo by Dennis Paulson.

Plate 10-35. This photo of leaf-cutter ants shows size distinctions among individuals. Photo by John Kricher.

Plate 10-36. A prominent “highway” made by leaf-cutter ants as they cross a field. Look carefully and note the small fragments of leaves the ants are carrying. Photo by John Kricher.

Plate 10-37. The aboveground part of an Atta ant colony. It extends far below the surface. Notice a main trail on the right side of the soil mound and the scraps of leaves on the mound, and notice also that sapling trees are growing from the colony mound. The ants make the soil uniquely fertile. Photo by John Kricher.

a relationship that apparently dates to about 50 million years ago. Attine ants are largely restricted to the Neotropics, where they are obvious to even the most casual observer. Throughout rain forests, successional fields, and savannas, well-worn narrow trails are traversed by legions of ants of the genera Acromyrmex and Atta as they travel (both diurnally and nocturnally) to and from their underground colonies, bearing freshly clipped leaves, and sometimes buds and flowers (plates 10-34– 37). Their trails take them up into trees, shrubs, and vines, where they neatly clip off rounded pieces of leaves to be transported back to their underground colony. The ants live in colonies of up to 8 million individuals, consisting of a single large queen and myriad worker ants, most of which remain subterranean. Workers are of several size

classes: very small (minima), medium-size (media), and large (maxima). Soldiers, the principal defense class, are large and well armed with formidable pincer jaws. Attine colonies are underground, but mounds of displaced soil and discarded leaves mark their multiple entrances on the ground surface. Leaf-cutters are somewhat selective as to which species they clip. In Guanacaste, Costa Rica, one Atta species clipped mature leaves from only 31.4% of the plant species available. Another species used leaves from only 22% of the available plant species. The commonness or rareness of a plant species has no correlation with Atta preference. The ants may travel relatively far from their colony to seek out a certain plant species. Internal plant chemistry appears to influence Atta diet.

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Leaf-cutter ants are part of a larger ant group called the fungus garden ants (Myrmicinae), each species of which, remarkably, cultivates a particular species of symbiotic fungus, which makes up its principal food source (discussed below). There are approximately 200 fungus garden species, of which 37 are leaf-cutters (Attini). The remaining species, most of which are inconspicuous, cultivate their fungus on some combination of decaying plant or animal organic matter. Though most abundant in the tropics, fungus garden ants also occur in warm temperate and subtropical grasslands. One species even occurs as far north as the New Jersey pinewoods. Leaf-cutter ants do not consume leaves but rather clip and carry leaf fragments back to their colonies. There they convert the leaves to media that serve to culture a specific fungus. This fungus is the ants’ food, though they also taste and ingest the sap of the leaves they cut, sometimes using it as an additional food source. Leaves brought to the colony are clipped into small pieces and chewed into a soft pulp. Before placing the pulpy mass on one of many fungus beds within the colony, a worker ant holds it to its abdomen and defecates a droplet of enzyme- and protein-rich fecal liquid on it. The chewed leaf is then added to the fungus-growing bed, and small fungal tufts are placed atop it. Other ants sometimes add their fecal droplets to the newly established culture. The fungus bed is termed a cultivar. Worker ants collecting leaves avoid those that contain chemicals potentially toxic to the fungus. For example, the tree Hymenaea courbaril, a legume, has been shown to contain an antifungal terpenoid, and Atta ants, not surprisingly, avoid clipping its leaves. The tree has evolved a protection from Atta not by defending against the ant but by defending against its fungus. The ants culture only a few fungal species, all of which are members of the family Lepiotaceae, in the class Basidiomycetes, a group whose free-living members include the familiar mushrooms. The fungi are never found free-living outside of ant colonies. The fungus garden is protected from contamination from other fungal species by constant “weeding” by ants (but see more on these fungi below). Without the attention of the ants, the fungus will be overtaken by other fungal species. Both ants and fungi are totally interdependent, an example of an obligate mutualism. Ant and fungus are coevolved, like the fig wasps and fig plants, to produce essentially two united genomes. Fungus and ants disperse together: only the queen reproduces, and

when a queen ant founds a new colony she takes some of the precious fungus with her inside her mouth. Studies of the fungus-ant relationship at the biochemical level have revealed that ants play multiple roles in culturing the fungus. The ants clean the leaves as they chew them to make the culture bed pure. Ant fecal fluid contains ammonia, allantoic acid, the enzyme allantoin, and all 21 common amino acids. These compounds are all low-molecular-weight nitrogen sources, and they are the key ingredients in making the culture optimal for the fungus. The fungus lacks certain enzymes that break down large proteins (all of which are made up of chains of amino acids). Thus it depends totally on the ant fecal fluid to supply its amino acids. Experiments attempting to grow the fungus in a rich protein medium have failed. It can grow only in a medium of small polypeptides and amino acids. Ants also supply enzymes necessary to aid in breaking down protein chains. Michael Martin summarized the functions of the ants: • fungal dispersal • planting of the fungus • tending the fungus to protect it from competing species, • supplying nitrogen in the form of amino acids • supplying enzymes to help generate additional nitrogen from the plant medium. While this may seem complex, it actually gets even more complex, because the system is not confined to just ants and fungus. There is a second fungus, Escovopsis, which is antagonistic, invading and consuming the ants’ cultivar. But ants are able to hold this fungus in check because actinomycete bacteria (order Actinomycetales) that live on the ants manufacture antifungal chemicals that inhibit the Escovopsis. However, yet another organism, a black yeast, feeds on the actinomycete bacteria, making it more difficult for the ants to protect their cultivars. Thus what appears to be a tightly linked two-species system (a very traditional way in which to view a mutualistic relationship) is, in fact, a far more complex five-species interaction of antagonistic and mutualistic interactions that one researcher has called a “balancing act.” Each fungus garden is unique. The cultivar in any given colony is isolated from cultivars in other attine gardens because queens that found new colonies transport only the fungi from their initial colony. The genetic composition of the fungus from each of the colonies is distinct, and there appears to be no

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opportunity for cross-fertilization among colonies. Because of normal evolution, the fungi cultivars diverge genetically. Studies have shown that fungal filaments (mycelia) from neighboring cultivars are rejected by the fungi in any given colony, and the rejection intensity is proportional to the genetic difference between the fungi from the two colonies. The fungus garden ants are the expert agriculturalists of the insect world, and their labors pay off in evolutionary fitness. The fungus symbiont digests cellulose, an energy-rich compound that ants cannot digest. Not only that, but the fungus is unaffected by many, if not most, of the defense compounds contained within leaves of many plant species. By eating the nutritionally rich cultivated fungi, ants circumvent many of the diverse defense compounds typical of Neotropical plants while at the same time tapping into the immense abundance of energy in rain forest leaves.

Are Leaf-cutter Ants the Dominant Herbivores of Neotropical Rain Forest? Leaf-cutter ants have often been assumed to be the major herbivores of Neotropical rain forest trees. Is this true? Hubert Herz and colleagues on Barro Colorado Island (BCI) quantified the impact of leaf-cutters (species Atta colombica) in old secondary forest in a study of 49 leafcutter colonies over a 15-month period. The researchers calculated the refuse deposition rate by measuring the refuse leaf fragments deposited monthly at the ant colonies compared with the harvesting rate. The results showed that leaf-cutter ants were important herbivores. The study revealed that Atta colombica harvested 13.2 tons of biomass and 13.1 ha (32.4 ac) of leaf area, and deposited 9.4 tons of refuse material per year. At the ecosystem level, the ants’ herbivory rates were 132 kg (291 lb) of biomass/ha/yr and 1,310 m2 (14,100 ft2) of foliage/ ha/yr. These figures represent 2.1% of the foliage area in the forest, or 1.7% of the annual leaf-area production. These figures, as impressive as they may seem, are considerably lower than those generated in previous published studies, which estimated that leaf-cutter ants consumed as much as 12% of annual leaf area and 17% of annual biomass. The impact of attines may vary considerably from site to site. Consumption rates among colonies varied six-fold, and thus these ants may have different impacts in different forests, making tropic dynamics ever more complex and generalization that much more problematic.

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The study concluded that on BCI animals such as sloths, deer, and howler monkeys have more impact on leaf herbivory than leaf-cutter ants. Leaf-cutters appear not to be the dominant herbivores, at least at BCI.

It’s Not Always Coevolution: Army Ants and Their (Mutualistic?) Antbirds Leaf-cutter ants, because they are so conspicuous, are often confused with army ants, but the two are very different kinds of ants. Army ants are carnivores and represent a notable predatory force on small animals inhabiting rain forest floor. These remarkable insects may represent the most significant predator in some rain forests, consuming more animal matter even than cats or various snakes. We can trace the history of army ants back to the supercontinent Gondwana, approximately to 105 million years ago in the Cretaceous. Dinosaurs presumably stepped upon army ants. It was once believed that Neotropical army ants (subfamily Ecitoninae) represent a case of convergent evolution with Paleotropical driver ants (subfamily Dorylinae), but molecular and other analyses suggest a close relationship. These ants evolved before the separation of Gondwana. Two widely distributed army ant species, Eciton burchelli and Labidus praedator, are prevalent in the Neotropics. In all, there are five genera and about 150 species of Neotropical army ants. They likely represent more biomass per unit area than all vertebrate predators combined (such as cats, weasels, coatis, raccoons). Eciton burchelli is one of the best-studied of Neotropical army ants, and its natural history is the focus of this section. Eciton varies in size and color. The largest individuals are soldiers, with extremely large and menacing mandibles, sharply hooked inward. The smallest workers are only about one-fifth the size of the soldiers. Color varies from orange and yellowish to dark red, brown, or black depending on subspecies. Eciton armies are immense, often containing in excess of a million ants. Armies are nomadic, moving through the forest, stopping at temporary bivouacs during their reproductive cycles. They may bivouac for only a night or for several weeks in the same area. When the entire mass moves, it is usually a nocturnal migration. Bivouacs are either underground or in hollow logs or trees and consist of massive clusters of the ants

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themselves. There is a single queen per colony, who remains in the bivouac except when the entire army is on the move, at which time an entourage of workers and soldiers transports her. Eciton raiders stream from the bivouac, making a dense column in search of prey. Soon the column begins to fan out widely, raiding parties moving in different directions. Ants move over and through the forest litter. Though virtually blind, the ants effectively communicate by chemical signals, and once prey is discovered, ants quickly converge upon it. Small prey is killed and taken to the nest, large prey is killed, dismembered, and carried to the nest, each task carried out by a specific worker caste. The raiders do not restrict their plundering to animals on the ground. They sometimes climb trees, even ascending into the canopy. They will enter human dwellings and attack cockroaches and other small animals. Eciton burchelli is a generalist predator. Prey consists of anything alive and small enough to subdue, most commonly arthropods such as caterpillars, spiders, millipedes, and other animals found among litter and leaves. Small vertebrates such as tree frogs, salamanders, lizards, and snakes are routinely attacked, and baby birds in the nest are frequent army ant victims. Note that humans are not included among the prey items of army ants. Many tropical visitors are concerned about possibly being attacked by army ants,

Plate 10-38. The Bicolored Antbird (Gymnopithys bicolor), here alertly looking for prey flushed by an army ant swarm, was recently split from the White-cheeked Antbird (G. leucapsis). This Photo by Kevin Zimmer.

but that worry is unfounded. The ants are easily spotted crossing a trail and thus easily avoided. Watching an army ant swam in action, with its attendant birds (discussed next), is a thrilling experience.

Here Come the Antbirds Raiding parties of army ants attract attention from diverse groups of birds specialized in following army ants. Birds typically and noisily accompany the ant swarms and capture prey exposed or attempting to flee from the horde of army ants. One of the easiest ways to find an army ant swarm is to listen for the bird sounds. Neotropical antbirds are members of two families, Thamnophilidae (206 species) and Formicariidae (62 species). These are discussed more in chapter 15. They are called antbirds because some follow and associate with army ant swarms. However, the vast majority of the species so designated do not follow army ants or attend ant swarms. Only 30 species from the two families combined are considered “professional” ant-following species, strongly associated with army ant swarms (plate 10-38). In addition, numerous other species of birds, including various woodcreepers, tanagers, motmots, and ground cuckoos join antbirds in attending ant swarms. The ant-following birds devour arthropods and small vertebrates (prey preference depending on the bird’s

Plate 10-39. The Ocellated Antbird (Phaenostictus mcleannani) and its feathered colleagues appear to be parasites of army ants, reducing their booty and paying them nothing in return. So much for mutualism, in this case. Photo by Kevin Zimmer.

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species) exposed by the ants. The relationship between army ants and ant-swarm birds has been puzzling. Scientists had reasoned that there were three possible types of association in action: the ever-active birds and ants may be mutualists, coevolved to help each other flush prey; the pair may be commensal, with the birds taking prey of no consequence to the ants; or the birds may be parasitic, taking prey away from the ants. A study performed at Soberania National Forest in Panama (near Barro Colorado Island) by P. H. Wrege and colleagues demonstrated that antbirds are actually parasites of army ants. The researchers, through a variety of creative techniques (one involved spraying persistent antbirds with a squirt gun to force them to flee), prevented antfollowing birds from attending swarms, while leaving other swarms with their attendant birds. They censused the arthropods and other animals captured by the ants, and at swarms where birds were permitted to remain they counted the prey items taken by birds. The results revealed the following: • The birds are highly dependent on ants to make prey available. Without the ants their foraging success would be greatly diminished. • The average nomadic ant colony consumes about 22 g (0.75 oz) of leaf-litter arthropods daily, plus an additional 22 g from social insects (other than the army ants). • The larger the flock size, the higher the cost of lost prey to the ants. • Each day antbirds take more than 200 prey items that otherwise, presumably, would have gone to the ants. This represents about 30% of the ants’ daily leaf-litter arthropod intake or 15% of the entire daily food requirement of a migrating ant colony.

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The relationship between army ants and ant-following birds is, at least if this study is typical, parasitic and not in any way mutualistic (plate 10-39).

So What Is Coevolution? The relationships among multitudes of species and their various roles in seed dispersal, pollination, and other interactions speak to the complexity and interdependencies evident in rain forest ecosystems. Biotic selection pressures prevail in the tropics. When one species exhibits a trait that acts as a selection pressure on another species, and the second species in turn evolves a trait that acts as a counter-selection pressure back upon the first, the evolutionary fates of both species may eventually become permanently interlocked. Should such interlocking occur, as we have seen throughout this chapter, it is an example of coevolution. Coevolutionary interactions may evolve from parasitic or predatory interactions, in which each species engages in a reciprocal arms race, as when both predator and prey evolve to be increasingly swifter. However, much focus on coevolution involves mutualistic relationships, when both species gain from the interaction. The majority of mutualisms, such as most seed dispersal, may be facultative, but others, such as fungus garden ants, are obligatory. But keep in mind, as is the case with the army ants and the ant-following birds, what might appear to be a mutualistic interaction may not be so in fact. Mutualism is not always easy to demonstrate. Lots of interactions remain antagonistic, as the next chapter will demonstrate.

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Plate 11-1. Boa Constrictor on forest floor demonstrating cryptic coloration. The photo was taken with flash, at night. Photo by Frederick Dodd.

Plate 11-2. Another cryptically patterned snake, this small anaconda (discussed in chapter 12) is partly revealed because it protrudes onto the road. Photo by John Kricher.

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Chapter 11 Evolutionary Arms Races: More Coevolution, More Complexity Predator-Prey Dynamics and Evolution Everything is food. Well, let’s say potential food. Rain forests abound in animal life and every animal, so it would seem, is potential sustenance for some other animal. Part of learning how to see when inside a rain forest, or any other habitat for that matter, is to realize that many creatures, ranging from various vertebrates to insects, spiders, and other invertebrates are adorned in colors and patterns that make them difficult to detect. Other creatures wear bold easy-to-see colors. Some even wear both types of colors. Why is this? Plants are not immune from predation either, which in their case is called herbivory. Why don’t all of the collective insect and other herbivores, such as sloths, just eat all of the plants? After all, the plants cannot run away. But perhaps they can fight back. It really is “a jungle out there,” an ongoing evolutionary arms race played out in ecological time. That’s what this chapter is mostly about.

Plate 11-3.

Cryptic Coloration: The Fine Art of Blending In The Neotropical boa constrictor (Boa constrictor), if placed on a plain table, appears boldly patterned, complexly colored in brown and gold, with stripes, diamonds, and other markings. Once on the rain forest floor resting on leaf litter, however, the snake seems to effectively blend into the background (plates 11-1–2). Some animals such as the blue morpho butterflies (Morpho spp.; plates 11-3–4) are very obvious in flight but not nearly so obvious when resting on a trunk or leaf with their wings closed. In essence, morphos have it both ways, being fairly cryptic when at rest and obvious when in flight. Crypsis, or cryptic coloration, pattern, behavior, or form, is nature’s camouflage. Thousands of species of tropical (and nontropical) insects, spiders, birds, mammals, and reptiles exhibit cryptic patterning and coloration to various degrees. It is a prevalent reality of nature both on land and in the seas. A sampling of cryptic creatures appears in plates 11-5–16.

Plate 11-4. Plates 11-3 and 11-4. A morpho butterfly with its wings closed (11-3) and another with wings opened (11-4). Photos by Andrew Whittaker.

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Plate 11-5. This large wolf spider (family Lycosidae) is pretty cryptic as it searches for prey on the forest floor. Photo by John Kricher.

Plate 11-6. The white spot reveals the wingtip of a helicopter damselfly (family Pseudostigmatidae) at rest on a vertical stick, very easy to overlook. The white wing spots are prominent when the insect is in its helicopter-like flight. Photo by John Kricher.

Plate 11-7. Stick insects (family Phasmatidae) are common in Neotropical forests. So are sticks—that’s the idea. Photo by Dennis Paulson.

Plate 11-8. Even large stick insects can be challenging to spot among the many real sticks to be encountered in a tropical forest. Photo by Dennis Paulson.

Plate 11-9. Many insects in the order Orthoptera are impressively cryptic. This is a leaf katydid (Stilpnochlora azteca). Photo by Dennis Paulson.

Plate 11-10. Meet Orophus conspersus, another katydid. Note that its wings resemble leaves with insect damage. Photo by Dennis Paulson.

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Plate 11-11. This katydid obviously bears a striking similarity to a small dead leaf. It is easy to see when the background coloration is different from the insect. Nonetheless, as dead leaves do occur among live leaves, this animal is easily overlooked. Photo by James Adams.

Plate 11-12. This one may take the prize for katydid camouflage. It looks like a decomposing leaf with only leaf veins remaining. Photo by Steve Bird.

Plate 11-13. Some katydids appear to rely on “thorns” to protect them as much as they do camouflage. This large and husky insect is from southwestern Amazonia. Photo by Sean Williams.

Plate 11-14. This grasshopper (Chromacris trogon) is yet another orthopteran insect that pretty much looks like the leaves of its habitat. Photo by Dennis Paulson.

Plate 11-15. Many insects besides katydids and grasshoppers have evolved to appear to be leaves. This is a stinkbug (family Pentatomidae). Photo by Dennis Paulson.

Plate 11-16. From a distance this tree frog (Hypsiboas semilineatus) would appear to be nothing more than a dangling dead leaf. Photo by Dennis Paulson.

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Plate 11-18. This mantis (family Mantidae) is a predator of insects and is normally cryptically positioned as it sits and waits for a potential prey insect. Photo by Dennis Paulson.

Plate 11-17. This is a Common Potoo (Nyctibius griseus) perched atop a tree snag, looking much like an extension of the snag. That’s the basic idea. All potoos exhibit such behavior during the day. They feed at night by capturing large insects in flight. Photo by John Kricher.

In the tropics, what appears at first to be a leaf may be a katydid; a twig may turn out to be a walkingstick or a mantis; a thorn may be a treehopper; a dead leaf may be a frog; bark may be a butterfly or moth; and a tree stump may be a bird. A bird? Yes. The Neotropical potoos (Nyctibiidae), a group consisting of seven species, are large nocturnal birds that feed on flying insects at night (chapter 15). When perched, they appear to be a combination of owl and nightjar. By day they sit very still atop a tree snag in plain sight, with the body positioned in such a manner as to closely resemble a branch (plate 11-17). In some species, if the tree snag sways with wind the potoo sways in synchrony with it. In many species cryptic coloration serves to reduce detection by predators, but in predators it acts to reduce detection by their prey (plate 11-18). Tropical cats also demonstrate cryptic coloration. The spotting and/or banding patterns of an Ocelot (Leopardus pardalis) or Jaguar (Panthera onca), so obvious when the animals are observed in zoos, aid in concealing the animals in nature (plates 11-19–20).

Plate 11-19. This Jaguar, photographed in the Pantanal of Brazil, demonstrates the cryptic nature of the animal’s coloration in the complex light and shade of forest. Photo by John Kricher.

Plate 11-20. When Jaguars are not hunting and are out in the open they still appear fairly cryptic. Take note of the second Jaguar sleeping in the shade to the left of the obvious one sunning on a riverbank. Photo by John Kricher.

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The stripes and spotted coat patterns break up the animal’s outline, rendering it less visible. Although cats are predators, cryptic coloration is no less an advantage to them, as it aids them in moving undetected toward their prey. Cryptic coloration evolves between an animal and its environment, but the selection pressures are actually based less on the physical environment than on the presence of other animals. Prey evolves to be concealed from predators, and predators evolve to be concealed from prey. The whole process is what evolutionary biologists term an evolutionary arms race. But the race is not always about concealment; it may take on a different look entirely. Some animals are pretty obvious. Why might that be?

Warning Coloration: Don’t Tread on Me

Plate 11-21.

Plate 11-22.

Cute Little Dangerous Frogs Although many animals are cryptic, some are exactly the opposite, standing out rather than blending in. Many groups of tropical butterflies and caterpillars as well as some snakes and frogs are brilliantly colored and stand out dramatically. There they are—you can’t miss them! Consider the small (5.5 cm/about 2.2 in) frogs of the family Dendrobatidae, the poison-dart frogs, which are common in many areas of Central America and northern South America. These colorful frogs hop nonchalantly in

Plate 11-23. Plate 11-24. Plates 11-21–11-24. These four photos illustrate some of the poison-dart frogs. Note how obvious they are, how easy to see. That characteristic serves to warn would-be predators of potential danger. Photos 11-21, 23, 24 by James Adams; photo 11-22 by Dennis Paulson.

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the open on the forest floor or are visible on leaves and branches, usually a short distance from the ground. They are a good subject for the axiom “look but do not touch.” There are about 30 species in the genus Dendrobates and five in the genus Phyllobates. All contain toxic alkaloids in their skin secretions. Each of these diminutive frogs is characterized by bold, often striped patterns of orange, red, yellow, blue, or green that glow like neon against a dark background. The Chocó tribes of western Colombia use toxic alkaloid compounds called batrachotoxins (a word that literally means “frog poisons”) extracted from the frogs’ skins as a potent arrow poison. One species, aptly named Phyllobates terribilis, is reputed to be potentially lethal to the touch. So don’t touch it. The others offer less risk, but you probably shouldn’t touch them either. A selection of poison-dart frogs appears in plates 11-21–24. Wow. Skin toxicity and bright coloration are evolutionarily linked. Poison-dart frogs represent a case of aposematic (or warning) coloration. Bright, bold patterning serves as a signal to potential predators that they should avoid the animal; it is a signal that they presumably either remember or have become innately attuned to recognize. After all, if a predator such as a bird (and birds see colors very well) were to eat the frog, sure, the predator would suffer from the frog toxin. But the frog would likely be killed by the would-be predator—not good for the frog. So there is a strong correlation between toxicity and frog obviousness. It is not an accident that frog obviousness takes the form of very bright, easy to remember colors. Almost 300 noxious or toxic alkaloids have been isolated from various species of amphibians. Batrachotoxins are considered to be the most toxic of the various alkaloid compounds (alkaloids are discussed further later in this chapter). The precursors of batrachotoxins are obtained in the insect diets of frogs, particularly from ants. Frogs kept in captivity show reduced levels of toxicity, suggesting that certain components of their natural diet are required to synthesize the skin toxins. For a bit more on poison-dart frogs see chapter 16.

Brightly Banded Snakes: Some of These Can Kill You, Some Are OK Neotropical coral snakes (54 species) are boldly patterned and colorful animals that are extremely venomous (plate 11-25). Coral snakes tend to be nonaggressive unless threatened (it is wise not to push this envelope). Why do they have such bright banding

Plate 11-25. This is a coral snake, highly venomous. Photo by James Adams.

Plate 11-26. This is a nonvenomous Honduran milk snake (Lampropeltis triangulum hondurensis). Many species of snakes in the tropics closely resemble coral snakes. Photo by James Adams.

Plate 11-27. Many coral snakes have a pattern in which red bands touch yellow, indicating that they can “kill a fellow.” This snake has that pattern. But it is a nonvenomous False Coral Snake (Erythrolamprus mimus). It is not fully clear whether it mimics coral snakes, they mimic it, or neither (though if neither, it would indeed be a striking coincidence). Photo by Dennis Paulson.

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patterns? Even though potentially lethal to any animal it happens to bite, a coral snake could still be killed or suffer extensive harm if attacked. Some bird species prey on snakes, and at least one, the Laughing Falcon (Herpetotheres cachinnans), has been observed to kill and devour coral snakes. A coral snake’s well-defined red, black, and often yellow pattern is presumably easy for birds (all of which see color) to recognize, remember, and avoid. Avoidance of coral snakes appears to be innate in some bird species. Both the Turquoisebrowed Motmot (Eumomota superciliosa) and the Great Kiskadee flycatcher (Pitangus sulphuratus) have been shown to instinctively avoid coral snake patterns. Others likely do as well. Certain nonvenomous snakes, including some king snakes, closely resemble coral snakes and are thought by many to be coral snake mimics (plates 11-26–27). Experiments have demonstrated that the avoidance of ringed patterns typical of both coral and king snakes is strong in areas where coral snakes are present, suggesting that the king snakes have evolved to mimic the coral snakes. But not everyone agrees. King snakes are aggressive when attacked, and thus it is not fully clear whether king snakes are mimicking coral snakes or coral snakes are mimicking king snakes—or both. The complexities of mimicry will be discussed later in this chapter. Coral snakes are discussed further in chapter 16. Bold patterning is common in some large caterpillars of the tropics. The larva of the False Sphinx Moth (Pseudosphinx tetrio), for instance, has a pattern somewhat suggestive of that of coral snakes (plates 11-28–29).

The Neotropical Pharmacy: Plant Chemical Defense Systems Do you like salads? Suppose you were somehow stranded inside a tropical rain forest. You are surrounded by tons of fresh greenery. Should you choose a few tender leaves and chow down? Maybe not. A look at any random sample of leaves in a rich tropical humid forest will usually reveal insect damage. Some leaves will show heavy damage, some little or none. Herbivore pressure on plants in the tropics is relatively constant because there is no cold winter (as in higher latitudes) when herbivores (at least most of them) become inactive. Plants cannot hide or run from potential herbivores. Their leaves are, in essence, always

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Plate 11-28. The large and colorful False Sphinx Moth caterpillar will writhe and twist violently when squeezed, such as would happen should a bird grab it. Photo by John Kricher.

Plate 11-29. This Ecuadorian caterpillar also represents an example of aposematic (warning) coloration, and then some. Note its bright coloration (it appears to have “headlights”) but also that it’s covered with dense spines. These are urticating hairs that, like nettles, cause extreme itching and discomfort if handled. Not only that, if you do pick this caterpillar up, it will, like the False Sphinx caterpillar, spasm so that you are likely to drop it immediately. Photo by John Kricher.

vulnerable. But in general, tropical herbivores take a notably small percentage of what is potentially available to them. That is why rain forests are always green. How do tropical plants defend against herbivorous hordes, not to mention invasive pathogenic bacteria and fungi? Let us count some of the ways. Leaves and stems may be covered with thorns of various sorts. Leaves grow to be thick and fibrous, with reduced nutritional value, difficult for herbivores to digest. Leaves of both tropical and temperate-zone plants are known to contain numerous chemicals that function in various ways to potentially defend the

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plant. Once known as secondary metabolites, they are now usually termed defense compounds and collectively called allelochemicals. Daniel Janzen (1975) put it well: “The world is not coloured green to the herbivore’s eyes, but rather is painted morphine, L-DOPA, calcium oxalate, cannabinol, caffeine, mustard oil, strychnine, rotenone, etc.” Many familiar drugs ranging from caffeine to curare to cocaine (chapter 17) are derived from the allelochemicals of plants. There really is a kind of “Neotropical pharmacy” in the rain forest. Defense compounds likely originated as genetically based accidental metabolic by-products or chemical wastes that, by chance, conveyed some measure of protection from attacks by microbes or herbivores. Such mutations would thus confer fitness, and natural selection would favor their rapid accumulation. Most plant species contain a pharmacopoeia of secondary metabolites that could function as potential defense compounds. Some defense compounds function principally to protect against herbivores, some to protect against bacteria and fungi. What follows is a brief introduction to some of the more prevalent groups of defense compounds. It is not meant to be comprehensive, but it should teach you enough that you will not be very tempted to make a salad composed of leaves taken randomly from tropical trees and shrubs. On the other hand, be aware that the science of ethnobotany is derived from the knowledge that humans began to acquire long ago when they realized the potency contained within the leaves, stems, and roots of numerous species of tropical plants and began to put plants to use. Ethnobotany is discussed more in chapter 17.

Alkaloids Alkaloids are a group of organic bases, all containing nitrogen. The alkaloid group includes some familiar and often addictive drugs. Some, such as the frog toxins described above, are highly toxic. Others are less so. Cocaine (from coca), morphine (from the opium poppy), cannabidiol (from hemp), caffeine (from teas and coffee), and nicotine (from tobacco) are each alkaloids. Taken together, there are more than 4,000 known alkaloids globally distributed among 300 plant families and over 7,500 species. A single plant species may contain nearly 50 different alkaloids. Alkaloids are found not only in leaves but almost anywhere in the plant, including seeds, roots, shoots, flowers, and fruits.

Most alkaloids taste bitter. In mammals, depending on dosage level, they may act as a stimulant (think about caffeine, for example) but they also may interfere with liver and cell-membrane function, as well as numerous other metabolic functions. The bitter taste combined with the potential negative effects on digestion and liver function may discourage animals from consuming alkaloid-rich vegetation, though the evidence for this is not widespread. Perhaps more significantly, alkaloids act to toughen leaves, and that alone acts to discourage herbivory, since it imposes an added cost to chewing and digestion. In general, alkaloid-containing plant species are more abundantly and disproportionally represented in tropical latitudes than in higher latitudes. This pattern suggests that there has been stronger selection pressure in the tropics to evolve alkaloids as plant protective compounds.

Phenolic Compounds, Including Tannins Phenolic compounds represent a diverse group of organic chemicals common in plants of all kinds. Some add pungency to spices. Some appear to function as defense compounds. Phenolics are compounds containing a hydroxyl group (−OH) directly bonded to an aromatic hydrocarbon group. The compound phenol (C6H5OH) is an example. Phenolics are stored in cell vacuoles, which break when an insect or other herbivore bites the leaf. Upon release, the phenolics combine with various proteins, including those enzymes necessary for splitting polypeptides (parts of proteins) in digestion. This makes it more difficult for the herbivore to digest protein. Leaf damage by insects or pathogens may stimulate production of phenolics. Tannins represent an important group of phenolic compounds that are structurally more complex. They are complex polyphenols with abundant hydroxyl and carboxyl groups that bond with proteins. Tannins are abundant in temperate and tropical oak leaves as well as in many other tropical plant species, including various mangroves. They provide the basic compounds used in tanning leather. Most people who enjoy wine know that tannic compounds are responsible for the astringency of certain red wines. Research by Phyllis Coley on Barro Colorado Island, Panama, that focused on the early successional tree Cecropia peltata showed that tannins are heavily concentrated in young trees of this species but decline in

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Wax-tail Hopper: Strange but True Meet the Wax-tail Hopper (Pterodictya reticularis; plate 11-30), an insect in the family Fulgoridae. At first glance it appears to be a disheveled katydid. It is not a true katydid, however, but it is relatively closely related to both the katydids and the treehoppers. This odd insect feeds on certain plant juices and metabolizes them in such a way that it creates its own thick wax. This wax composes the long white plumes that stream behind the abdomen. Apparently the wax functions in two ways: First, it coats the species’ eggs, helping protect them from parasites and from drying out. Second, it protects the adult insect by making it unpalatable to potential predators. At least that is our best guess for the moment. In any case, it is just another remarkable insect of the Neotropics for you to strive to observe.

Plate 11-30. The Wax-tail Hopper is easy to see but may not be so easy to eat. Photo by Dennis Paulson.

A Very Toxic Toad: Do Not Lick This Animal The Cane Toad (Rhinella marina, formerly Bufo marinus; plate 11-31), is a common resident on the forest floor throughout the Neotropics. It has been introduced in many places outside of its normal range, including south Florida, much of the Caribbean and as far away as Fiji and Australia, where it has become a serious pest species. When a Cane Toad reaches adulthood, it is somewhere between the size of a baseball and a softball. Even though its appearance is relatively cryptic, its large size makes it hard to miss. Once discovered, it does not hop very quickly. So it would appear vulnerable, a big fat toad, and a darned slow one. But it is well protected, and predators avoid it. Cane Toad skin contains a milky bufotoxin (toad toxin), secreted from the animal’s prominent parotoid glands, the “warts” that appear on its back and behind the head. This toxin, a kind of alkaloid called bufotenin, has been shown to produce hallucinations in humans—some of whom have apparently been known to lick toads just to have this occur. Should an animal ingest the toad or even just bite it, it risks illness and perhaps death. This is one dangerous toad.

concentration in older plants. This characteristic appears to be generally true for most tropical plants. Tannin levels are lower in plants grown in shade, indicating that tannin production may be metabolically costly, requiring full sunlight. In field experiments, low-tannin plants experienced twice the level of herbivory as those with high tannin levels. However, leaf production was inversely correlated with tannin levels. The more leaves on the tree, the lower the tannin per leaf, indicating that tannin production, though perhaps protective, is likely

Plate 11-31. This adult Cane Toad is well protected by its chemical defenses. The large parotoid glands posterior to the head, shown clearly in this image, secrete the toxin bufotenin. Photo by Dennis Paulson.

costly to the plant. Trees like Cecropia, experiencing intense competition for light, may have to limit tannin protection in favor of rapid growth, a situation termed an evolutionary trade-off. The role of phenolic compounds and tannins as anti-herbivore adaptations is unclear. Some insects have evolved enzymes that detoxify specific defense compounds. Leaf-cutter ants (chapter 10) are apparently undeterred by phenolic compounds, but of course they do not actually eat leaves. Instead they “feed” the leaves to

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Cassava: Staple Root Crop of the World Tropics Manioc (Manihot esculenta) is a ubiquitous Neotropical tree grown for its tuber, a carbohydrate-rich root usually referred to as cassava or yuca, which has become a staple food of humans throughout the region (plates 11-32–33). A native of South America, Manioc has long been grown throughout the tropical world. A perennial, it will grow annually without replanting. It is typically planted from cuttings taken from mature plants. For consumption, the tuber is usually ground into a paste and made into a hard bread, though it can also be fermented into a kind of beer. Whole recipe books have been written about the use Plate 11-32. Manioc cutting, recently planted, will of cassava. The plant itself is a small, spindly tree, with palmate, grow into a full-size plant; its root is sold under the compound leaves, most unpretentious in appearance. The root, name cassava. Photo by John Kricher. however, is thick and often more than 1 m (39 in) in length. On nutrient-poor soils, Manioc contains prussic acid, a powerful cyanogenic glycoside that defends the root from herbivore attack. Indigenous people have developed various methods for removal of the prussic acid, an absolute necessity before further preparation. In some cultures toxic cassava-root paste is soaked in water and repeatedly squeezed and compressed— literally wrung out; this washes the water-soluble cyanogenic compounds from the paste, rendering the root safe to consume. Many varieties of Manioc exist with variable levels of prussic acid concentration. There are sweet varieties of cassava, with essentially no prussic acid, and bitter cassava, which has high concentrations of cyanide compounds. Sweet-tasting varieties grow only in the most fertile soils, while the bitter strains are found in soils of low fertility, where herbivore damage would be more costly to the plant.

Plate 11-33. Cassava (manioc root) for sale at a market in Manaus, Brazil. Photo by John Kricher.

The Cyanogenic Millipede: What’s That Almond Smell? Plants are not the only organisms to utilize cyanogenic compounds. Millipedes, members of the huge phylum Arthropoda, are harmless ambling herbivores of the forest floor (plate 11-34); they should not be confused with swift-moving carnivorous centipedes, which inject toxin when they bite (chapter 16). Neotropical millipedes in the genus Nyssodesmus appear armored with a flattened shiny carapace protecting their delicate undersides. One of these creatures may reach 10 cm (4 in) in length and is readily visible as it slowly makes its way about on the forest floor. These millipedes are common throughout the Neotropics, and there is a probable reason as to why—they are well protected. When threatened, these millipedes roll up in a ball and tough it out (plate 11-35). Some have an impressive array of chemicals at their command. The hindgut can squirt a volley of noxious liquid, containing both hydrogen cyanide and benzaldehyde. You’ll notice this behavior if you handle one of these creatures, and your hands will smell distinctly like almonds, from the cyanide. Be sure to wash your hands afterward.

Plate 11-34. Millipede on forest floor. Photo by John Kricher.

Plate 11-35. Millipede in the hand, curling into a ball. Photo by John Kricher.

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the fungus they cultivate. Many tannins retard microbes and pathogens, and therefore presence of tannin may affect rates of decomposition and nutrient cycling.

Cyanogenic Glycosides Many species of tropical plants contain compounds called cyanogenic glycosides, which consist of cyanide (a potentially deadly compound) linked with a sugar molecule. When combined with enzymes from either the plant or an herbivore’s digestive system, the sugar is released, leaving hydrogen cyanide. Cyanogenic glycosides, as well as alkaloids, tannins, and other defense compounds, are well represented in passionflowers (Passiflora spp.). Very few insect herbivores feed upon passionflower leaves or stems. The defense compounds apparently do act to discourage most herbivores, though not all. The caterpillars of Heliconius butterflies feed on Passiflora species. This group of lepidopterans has evolved resistance to the Passiflora defense compounds. Much will be said of them later in this chapter.

Terpenoids Terpenoids are a complex group of fat-soluble compounds in plants. Some are used in the synthesis of compounds that may mimic insect growth hormones (preventing rather than promoting growth of the insect); others are modified into cardiac glycosides, which are well-known medicinal chemicals, such as digitalis, that act to stimulate the heart. Some terpenoids discourage both insects and fungi. One terpenoid in particular, caryophyllene epoxide, has been shown to repel the fungus garden (leaf-cutter) ant Atta cephalotes from clipping leaves of Hymenaea courbaril. This terpenoid was shown to be toxic to the fungus that the ants culture. In a survey by Stephen Hubbell and colleagues of 42 plant species from a Costa Rican dry forest, 75% contained terpenoids, steroids, and waxes that repelled leaf-cutter ants.

Toxic Amino Acids Some tropical plants, especially members of the legume, or bean and pea, family (Fabaceae), contain amino acids that do not build protein but instead interfere with normal protein synthesis. Canavanine, for example, mimics the essential amino acid arginine.

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Perhaps the best known of the toxic amino acids is LDOPA, a strong hallucinogen. Both canavanine and LDOPA are concentrated in the seeds of some tropical plants. In general, the major function of nonprotein amino acids, at least in legumes, seems to be to discourage herbivores. Taken together, the groups of potential defense compounds just described present an image of a tropical forest that suggests a chemical complexity every bit as impressive as its structural complexity and equally important.

Other Types of Plant Defenses We drive on a defensive adaptation of tropical plants— namely, rubber. The Rubber Tree (Hevea brasiliensis), which can reach heights of 36.5 m (120 ft), is one of many tropical trees that produce latex, resins, and gums, substances that render the trees less edible. Rubber Tree sap is a milky suspension in watery liquid contained in ducts just below the bark, external to the cambium and phloem. It congeals upon exposure to air and may aid in closing wounds to the plant, protection against microbial invasion, and hindering herbivores. Latex is present in plants of many families (Euphorbiaceae, Moraceae, Apocynaceae, Caricaceae, Sapotaceae, and others), a case of a convergent defensive adaptation among distantly related species of tropical plants. The Chicle Tree (Manilkara zapota), which grows in rain forests throughout Central America, produces latex called chicle from which chewing gum is made. Some insect herbivores have adapted to latex defense. One caterpillar species clips leaves of Papaya (Carica papaya) in such a way as to cause the defensive latex to flow away from where the insect is feeding. Tropical trees may be spiny, thorny, or have leaves coated with diminutive “beds of nails,” called trichomes, that literally impale caterpillars. Experiments have shown that sharply toothed leaf edges reduce caterpillar grazing. When teeth are experimentally removed, caterpillars inflict much greater damage to the leaf. Many palm species have spines lining the lower trunk (see plate 3-34). Some palms also have long, sharp spines on the undersides of leaf midribs. Wood of many tropical trees is hard, a possible adaptation to discourage termites and wood-decaying fungi.

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High Fiber Content Is an Adaptation Leaf toughness, nutrition value, and fiber content strongly contribute to herbivore resistance. Phyllis Coley (1983) examined rates of herbivory and defense characteristics of 46 canopy tree species on Barro Colorado Island. She compared young leaves with mature leaves and gap-colonizing species with shadetolerant species. In general, young leaves were grazed much more than mature leaves, even though many contained phenols (indicating that phenols do not prevent herbivory, though some forms may discourage it). In another study Coley and her colleagues (2005) learned that although leaves of shade-tolerant species may live for several years, 75% of the lifetime damage occurs during the early weeks when the leaves have opened and are expanding, before they have added essential fiber.

Soil Quality Affects Defense Compound Abundance Defense compounds are particularly abundant in plants of lowland forest occurring on nutrient-poor white, sandy soils, such as are found in the northern Amazon region (chapter 6). Because of scarce soil nutrients, leaves are metabolically costly to replace. These leaves are longlived (several years) and have such high concentrations of defense compounds that when a leaf finally drops, it must be leached of these compounds by rainfall before it can be broken down and its minerals recycled. Recall from chapter 6 that water from blackwater rivers characteristic of white, sandy soil regions appears dark and tea-like because of the concentration of leached phenolics (e.g., tannins). Plants have greater fitness if they manufacture enduring leaves with concentrated defense compounds than replace leaves ravaged by microbial pathogens, fungi, or herbivores. Given the shortage of minerals in the soil, the replacement of leaves is more costly than synthesis of defense compounds. Most plant species in sunlit disturbed areas and roadsides are adapted to maximize growth rates. They synthesize alkaloids, phenolic glycosides, and cyanogenic glycosides, all present in low concentration, collectively representing a relatively low metabolic cost. In contrast, plants on nutrient-poor soils invest in metabolically more costly defenses such as polyphenols and fiber (e.g., lignin), retaining them in leaves and bark. The trees grow more slowly but are better protected. These contrasting patterns in plant defenses appear to be a function of

Plate 11-36. Cecropia showing leaf damage by herbivorous insects. Photo by John Kricher.

resource availability. On sites where resources are poor, “expensive,” long-lasting defense compounds are favored. On resource-rich sites, “cheaper,” shorter-lasting defense compounds are favored, because the tree is able to both devote sufficient energy to rapid growth and replace defense compounds as needed. Many species of disturbed areas are subject to significant herbivore damage. Cecropias, for example, are fast growing but routinely show extensively damaged leaves (plate 11-36).

Ant-Plants and Plant Ants: Let the Ants Do the Work (but Pay Them) Nectar is a rich, sugary substance strongly associated with flowers. Recall from chapter 10 that it is the “bribe” that is paid by the plant to pollinating animals: “Come to the flower, have some nectar, but take along some pollen and deliver it to another flower.” However, nectar is not confined to flowers. Many tropical plant species possess nectar-secreting glands, called extrafloral nectaries (EFN), as well as other structures that attract ants. Extrafloral nectaries are found in 90 plant families and 330 genera. Some of these plants, which include ferns, epiphytes, vines, and trees, are called myrmecophytes, or ant-plants, because of their ant-attractant properties. Ant-plants occur widely in the Old World tropics, especially Southeast Asia, and in the Neotropics. They are also present in areas such as the Sonoran Desert in the southwestern United States. Ant-plants normally have some form of shelter for ants (domatia) in addition to providing nutrition.

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Domatia range from hollow stems to more sophisticated shelters such as specialized pouches or swollen thorns. Extrafloral nectaries are present on leaf blades, leaf petioles, stems, or other locations on the plant. These glands manufacture various energyrich sugary compounds as well as certain amino acids. In addition, some plants have bead bodies, which are modified hairs rich in oil. Extrafloral nectaries were initially puzzling (why do plants have them?), but it was quickly learned that plants with such bodies are populated by various aggressive ant species. This observation led to the protectionist hypothesis, which asserts that the relationship between plants and ants is fundamentally mutualistic. The alternative idea, called the exploitationist hypothesis, argued that the ants fed on the sugary nectaries but provided no actual service to the plants. That seemed to suggest an odd evolutionary blind alley, at least as far as the plants were concerned. Extensive research has strongly supported the protectionist hypothesis. Here are some examples. Cecropia trees (chapter 7) have glycogen-rich structures called Müllerian bodies (a form of extrafloral nectary) located at the base of the leaf petiole, where the large leaf attaches to the stem. Ants of the genus Azteca live in domatia within modified hollow pith of the stem and feed on the Müllerian bodies (plate 11-37). I have frequently encountered the ants of a cecropia, and they are pugnacious and appear to behave protectively of their tree. The underside of the wide, palmate cecropia leaf is velvet-like, with a carpet of tiny hairs and hooks that allow ants to gain purchase and move easily across the leaf. Cecropia species that normally lack ants have leaves with smooth undersides. In a now-classic study Daniel Janzen documented the protectionist activities of Pseudomyrmex ferruginea, an ant species found on five species of Acacia tree. Commonly called the bull’s horn or swollen-thorn acacias, these trees have pairs of large hollow thorns on the stem that shelter the ants (plates 11-38–39). A single queen ant burrows into a thorn of a sapling acacia to begin a colony that may grow to 12,000 ants by the time the tree matures. By the time the tree is seven months old, 150 worker ants are patrolling the stem. The acacia ants attack other insects that land or climb on the tree, including beetles, hemipterans (true bugs), caterpillars, and other ants. Ants also clip plants that begin to grow nearby or that overtop and shade the acacia (thus taking its sunlight), and attack mammals,

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Plate 11-37. Azteca ants on the bole of a cecropia. The brown areas beneath the leaf axils periodically produce food for the ants. Photo by Scott Shumway.

Plate 11-38. The branches of this understory acacia look innocent enough, until you get close and meet the ants that guard the plant. Photo by John Kricher.

Plate 11-39. The swollen, paired, hollow thorns of this acacia tree house small but aggressive Pseudomyrmex ants, seen here swarming over the branch. Photo by John Kricher.

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including people, if they should brush against the tree (a personal experience not easily forgotten). Ants appear agitated, swarming out of the thorns and over the foliage, at any disturbance. The ants obtain shelter within the thorns as well as nutrition from two kinds of extrafloral nectaries. One type is termed Beltian bodies, small orange globules growing from the tips of the leaflets of the compound leaves; the other type is the foliar nectaries, located on the petioles. Janzen performed a field experiment that discriminated between the protectionist and exploitationist hypotheses. He treated some acacias with the insecticide parathion, and he clipped thorns to remove all ants from the treated trees. The antless trees did not survive nearly as well as the control trees, which were permitted to keep their ants. Janzen estimated that antless acacias were not likely to survive beyond one year, either falling prey to herbivores or being overtopped by other, competing species of plants. He concluded that the ants and acacias are obligate symbionts, depending entirely upon each other. The relationship between plants and ants is thus one of obligate mutualism. More recent research has shown that the acacias attract protectionist ants in a biochemical manner. They synthesize the enzyme invertase, which cleaves the disaccharide sucrose in the EFN, rendering it to glucose and fructose. Protectionist ants avoid sucrose but are attracted to glucose and fructose. Researchers manipulated the sucrose concentrations in EFNs of acacias and were able to attract or repel Pseudomyrmex ants on the basis of presence (repel) or absence (attract) of sucrose. Extrafloral nectaries are known from some temperate-zone plants but are far more abundantly represented among tropical plant species. Though many plants with EFNs house ants, the degree to which the ants act to protect their hosts may vary considerably among species. But in the case of swollen-thorn acacias and some cecropia species, ants have clearly assumed the function of defense compounds.

Extrafloral Nectaries Promote Multispecies Interactions Because they represent an energy resource, it should not be surprising to learn that extrafloral nectaries attract numerous arthropods, not merely ants. There is constant selection pressure operating in any ecosystem to screen

arthropods as antagonists or otherwise. Ant defenders are subject to selection pressures by organisms other than plants. Philip DeVries documented a remarkable example in Panama, observing that caterpillars of the butterfly Thisbe irenea entice ants to protect them rather than their host plant (Croton), and the caterpillars then eat the leaves from the very plant the ants were once protecting. These caterpillars, termed myrmecophilous, for their “ant-loving” habits, have evolved at least three separate organs that act to attract and satisfy ants: nectary organs that produce protein-rich ant food; tentacles that release chemicals mimicking those of the ants themselves and signaling them to defend; and vibratory papilla that, when the caterpillar moves its head vigorously, make sounds that travel only through solid objects, but which immediately attract ants. The ants appear to have a stronger preference for the protein-rich caterpillar nectar droplets than for the carbohydrate-rich food supplied by the Croton nectaries. The ants are essential in protecting the otherwise vulnerable caterpillars from predatory wasps. By providing nectar for the ants, the caterpillars have succeeded both in averting the main protective adaptation of the plant and in ensuring their own relative safety from their major predators, wasps. Amazing. The ecological significance of extrafloral nectaries remains an area of active study. Because EFNs are so widespread among tropical tree species, they may be a widely utilized resource responsible for significant energy movement through tropical food webs.

The Evolutionary Arms Race Given that so many species of tropical plants possess numerous defense compounds as well as mechanical defenses, it may seem surprising that any kind of herbivore is able to consume them. But evolution is never static. Once a defense compound evolves, it in turn acts to exert a counter-selection pressure on herbivores and pathogens to evolve some form of adaptation that circumvents the plant defense. Once again vulnerable, the plant is then under enhanced selection pressures to evolve yet another defensive adaptation, which, should that occur, merely acts as yet another selection pressure on the herbivore, an evolutionary arms race of sorts. There are numerous examples of this chain of events. Here are a few of the most noteworthy.

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Plants vs. Insects Ecologists debate the degree to which insect communities in the tropics exhibit greater host specificity and specialization compared with those at higher latitudes. Some data suggest that lepidopteran (butterfly and moth) species are proportionally more host-specific in the tropics. Is increased insect specialization a general characteristic of tropical ecosystems, particularly rain forests? The answer is equivocal. It depends on how specialization is defined. Further complicating the question is that the exact magnitude of insect species richness is still relatively poorly documented for rain forests. Defense compounds, protective ants, and tough leaves all provide selection pressures affecting the evolution of insect herbivores. Those insects that evolve enzyme systems that detoxify defense compounds or somehow sequester them are able to specialize on specific plant species. Plant compounds may be repellent but not actually be toxic. Insects may overcome the repellency and adapt to recognize a host plant by its repellent compounds. Insects may evolve behaviors that minimize exposure to defense compounds. For example, the caterpillars of the butterflies of the genus Melinaea feed on plants in the nightshade family (Solanaceae). Philip DeVries and Irene Baker showed that the caterpillars cut the leaf veins of their host plants, preventing the defense compounds from reaching the leaf blade, where the caterpillars feed.

Plate 11-40. Mantled Howler Monkeys are folivores, but they do not eat just any leaves in any tree. They appear to pick and choose in order to avoid plants’ defense compounds. Photo by John Kricher.

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If you want to understand what goes on routinely in nature think of the fight against computer hacking as an analogy. Operating systems come with virus protection and various firewalls, and hackers figure out away around them. Then the programmers develop more protective software, and the hackers in turn hack that. Nature has been doing that sort of thing ever since there has been nature.

Plants vs. Howler Monkeys Primates are largely herbivorous, and many eat mostly fruit. Some, however, such as howler monkeys, are primarily leaf eaters, or folivores. Thus they are exposed to plants’ defense compounds. In a famous study by Ken Glander in Costa Rica, Mantled Howler Monkeys (Alouatta palliata) were observed to occasionally appear disoriented and even to fall from trees. Further observations showed that the howlers were apparently sickened by consuming toxic leaves and that affected their equilibrium in the trees. Howlers must learn to be extremely selective in exactly which trees they dine upon (plate 11-40). Within one tree species, Gliricidia sepium, represented by 149 individual trees in the howlers’ range, the troop fed on only three of the trees and always the same three. The leaves of these trees were less difficult to digest than those of their conspecifics. Mantled Howlers favor young leaves, which are relatively high in nutritional value but not yet concentrated with defense compounds. When

Plate 11-41. Spider monkeys are mostly frugivores, not folivores, and their intestinal system is adapted accordingly. Photo by Jill Lapato.

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only mature leaves are available, the monkeys eat just a little on one tree and then move to a different tree, minimizing their exposure to various arrays of defense compounds. Sometimes they eat only the leafstalk, or petiole, ignoring the blade; the petiole has lower alkaloid content. Ecologist Katherine Milton showed that protein and fiber content are also important factors affecting leaf choice in howler monkeys. Fiber, as noted earlier in the chapter, makes leaves difficult to digest. Monkeys prefer to eat young leaves, which have less fiber. Protein is also proportionally higher in young leaves. The greater the ratio of protein to fiber, the more desirable the leaf is to howlers. Howlers have long intestinal systems, especially the hindgut. It takes food up to 20 hours to pass through a howler’s digestive system. Geoffroy’s Spider Monkeys (Ateles geoffroyi) eat mostly fruits, which, because they contain more protein and fewer defense compounds than leaves, are much easier to digest (plate 11-41). It takes food only about 4.4 hours to move through the shorter gut of a spider monkey. Howlers, with their long hindguts, are able to more efficiently digest leaves, coping to a reasonable degree with both the high fiber and the defense compounds.

Plants vs. Butterflies To plant species, butterflies, with their complete metamorphosis, are evolutionary examples of Dr. Jekyll and Mr. Hyde. As adult sexually reproducing insects, butterflies play the role of benevolent Dr. Jekyll, dispersing pollen essential to the plants’ reproduction. As voracious caterpillars they become malevolent Mr. Hyde, devouring leaf tissue and reducing plant fitness. How do these scenarios play out in tropical ecology? Various lepidopterans in temperate and tropical areas have strong affinities for feeding on specific plant families. Caterpillars are much more strongly affiliated with particular plants than butterflies, their “adult” form. Butterflies feed on nectar, aiding in pollen dispersion, and their interactions with plants are fundamentally mutualistic. They tend to feed on a wider range of plants than larval lepidopterans, which have by natural selection evolved defenses against specific plant defense compounds. Caterpillars are voracious herbivores, and being folivores, they harm plants. Of course they encounter plant defenses, including defense compounds, as they chew on leaves.

Since different families of plants produce different combinations of defense compounds, natural selection has acted on caterpillars in such a way that various caterpillar species have evolved tolerance for defense compounds associated with different and specific plant families. In other words, they have tended to specialize. Heliconid Butterflies and Passionflowers A note of clarification to the reader: Please be aware that Heliconius butterflies have no coevolutionary relationship to plants in the genus Heliconia. The similarity in their names is coincidental. Adult heliconid butterflies may feed on Heliconia nectar, but they feed on nectar of many other kinds of flowering plants too. Heliconid butterflies, as will be explained below, are associated as caterpillars only with passionflowers, genus Passiflora. The names Heliconia and Heliconius are often points of confusion among visitors to the Neotropics.

Heliconius butterflies and their kin in the subfamily Heliconiinae, collectively known as heliconids and commonly called the longwing butterflies, are a diverse and colorful group of multiple genera and species, almost all of which are Neotropical (plate 11-42). They belong to the brush-footed butterfly family (Nymphalidae), which numbers nearly 3,000 species globally. The Heliconiinae is represented by about 50 species, which have many local races throughout tropical America. Only three species of longwings, Heliconius charithonia, H. erato, and Dryas iulia, regularly reach the United States, ranging through southern Texas and the Southeast, especially southern Florida. It is important to point out that caterpillars, the larval stage of lepidopterans, as well as adult lepidopterans (the butterflies and moths) are heavily preyed upon, particularly by birds (plate 11-43). This dynamic of nature sets up a potential evolutionary arms race between lepidopterans and birds that plays out constantly in the tropics. Heliconid adults feed on a variety of plant species, but the caterpillars feed virtually exclusively on species of Passiflora, or passionflower (family Passifloraceae), a common vine genus numbering approximately 500 species, a few of which reach North America (plate 11-44). Like heliconids, passionflowers are largely Neotropical. Very few herbivores other than heliconid caterpillars dine on passionflower vines, and another name for heliconids is “passionflower butterflies.” Most passionflowers contain a smorgasbord of cyanogenic

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glycosides and cyanohydrins. The high diversity of cyanogens among passionflower species could be an evolutionary response to herbivory by heliconids. Heliconids, however, apparently adapt to the everchanging cyanogen regime by evolutionary changes in their hydrolytic enzymes and by sequestration of cyanogens. Heliconid caterpillars have obviously coevolved with passionflower. They are pretty good passionflower hackers. Heliconid butterflies have adapted to a life cycle on their host plant. Females lay small numbers of eggs in globular yellow clusters directly on passionflower leaves, favoring young shoots. When eggs hatch, the caterpillars are conveniently sitting on their food source. The plant is therefore under selection pressure to somehow prevent the adult female butterfly from locating, selecting, and laying eggs on its leaves. Detailed studies by Lawrence Gilbert and W. W. Benson and colleagues have demonstrated diverse passionflower defenses that extend beyond defense compounds. Passionflower produces extrafloral nectaries that attract various species of ants and wasps. These insects help repel heliconid caterpillars. Some passionflower species are protected exclusively by ants, some by wasps, and some by both. At least one study has shown that caterpillar survival is much lower on Passiflora with attending ants: caterpillar mortality rate was 70% on ant-attended plants, compared with 45% on non-ant plants. Some Passiflora extrafloral nectaries appear, to the human eye, to mimic heliconid egg clusters. Perhaps that is also how they appear to the Heliconius butterfly eye. These passionflower vines typically have young leaves spotted with a few conspicuous yellow globs, the egg mimics. Female heliconids will not lay eggs on a leaf already containing egg masses, and the mimic egg masses presumably prompt the female to continue searching. Lawrence Gilbert believes the mimic eggs to be a recent evolutionary development in the plantinsect arms race, because only 2% of passionflower species have them. Leaf shape varies within a species of passionflower, and passionflower leaves often resemble those of other common plant species growing nearby, showing leaf mimicry. Perhaps heliconids may be tricked by the similarity of appearance and thus overlook a passionflower. This speculation depends, of course, on the butterfly using visual cues to locate passionflower vines. If the insect depends principally on scent, such leaf mimicry would seem to be useless.

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Plate 11-42. Heliconid butterflies (this one is Heliconius doris) are found throughout the Neotropics and have been the object of much coevolutionary study. Photo by John Kricher.

Plate 11-43. A Broad-billed Motmot (Electron platyrhynchum) with prey, a large caterpillar. Birds are strong predators of caterpillars and butterflies and exert strong selection pressures on the evolution of these insects. Photo by Nancy Norman.

Plate 11-44. Passionflower vines (Passiflora) are the only plants the caterpillars (larvae) of heliconid butterflies feed on. This photo shows a plant and its inflorescence. Photo by John Kricher.

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Plate 11-45. Even from a considerable distance, Heliconius butterflies are obvious. This one is either H. melpomene or H. erato; they are very difficult to distinguish. Notice how the wing pattern seems to focus the eye on the most vulnerable part of the insect, seemingly daring a predatory bird to attack it. Photo by John Kricher.

Plate 11-46. The bright orange Monarch Butterfly (Danaus plexippus), here feeding on aster flowers, is the best-known of the milkweed butterflies and the one Lincoln Brower used in his experiments to demonstrate that Blue Jays (Cyanocitta cristata) avoid Monarchs after being sickened by eating them. Photo by John Kricher.

For the time being, at least one passionflower species, Passiflora adenopoda, may have a firm advantage in the coevolutionary arms race. Its leaves have a dense covering of minute, hooked spines, called trichomes, resembling a bed of nails. The trichomes impale the soft-skinned caterpillars, and once a caterpillar is stuck, it starves. Score one for the plant. Trichomes occur on other plant species, and at least one butterfly species, Mechanitis isthmia (an ithomiine, not a heliconid), has adapted to thwart trichome defense. Mechanitis caterpillars, which feed on plants of the nightshade family, avoid impalement by spinning a fine web to cover the trichomes, so they can safely move over the leaf surface to feed on the leaf edges. The arms race continues.

butterflies are distasteful to would-be predators, a selection pressure favoring aposematic coloration becomes likely. Once a bird has eaten an unpalatable insect, bright coloration would tend to facilitate its learning avoidance behavior. It has been demonstrated that birds are capable of remembering butterfly warning coloration and will avoid unpalatable butterflies once they have experienced them. Lincoln Brower demonstrated that birds avoid eating milkweed-feeding butterflies, all of which are bright orange, once they have experienced the indigestion that follows (plate 11-46). Milkweeds contain high volumes of cardiac glycosides that obviously help protect the plants. Heliconid butterflies are likely to store the plant defense compounds they take in as caterpillars (or to use them as precursors to synthesizing their own unique defense compounds) and thus become unpalatable to predators. In other words, the chemical defense of the plant becomes, in turn, the chemical defense of the insect. In an experiment conducted by W. W. Benson in Costa Rica, the wing coloration pattern of the unpalatable butterfly Heliconius erato was altered, and the new patterning was one that predatory birds would not have seen before. A control group identical to normally occurring specimens was also established. Equal numbers were released of the altered, uniquely patterned individuals and the normal butterflies of the control group. Significantly fewer of the altered individuals were recaptured by the researchers, an indication that fewer had survived. Some altered

Why Are Heliconid Butterflies Obvious? Heliconid butterflies are among the most obvious, strikingly patterned butterflies of the tropics (plate 1145). They fly slowly, almost delicately, and are very easy to see along forest edges as well as in interior rain forest. When atop a plant, many of these butterflies glow brilliantly, as if lit up. Why are they so conspicuous? Consider the potential risk to the insect. Most tropical bird species feed heavily on insects. For a butterfly group to be colored like neon signs, practically saying “eat me,” seems like a death wish. But being conspicuous serves as a warning. Recall that coral snakes are dangerous and obvious. If heliconid

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butterflies that were recaptured showed wing damage from bird attacks. Benson was even able to identify one bird species, the Rufous-tailed Jacamar (Galbula ruficauda; plate 11-47; jacamars are discussed in chapter 15), by the shape of wounds it left in a butterfly’s wing (plate 11-48). The experiment showed that wing pattern does confer protection once predators learn the pattern and associate it with unpalatability (plate 11-49).

Mimicry Systems: Look-alikes Win Although heliconids and many other tropical butterflies are striking in appearance, species are often difficult to identify because different species evolve to look alike: they mimic one another. But why?

Plate 11-47. This Rufous-tailed Jacamar in the shaded forest understory is hunting for flying insects. Photo by Gina Nichol.

Batesian Mimicry Henry Walter Bates, a Victorian naturalist who explored Amazonia in the mid-19th century, was amazed to discover that some unrelated species of butterflies look alike. He suggested that a palatable species gains protection from predators if it closely resembles a noxious unpalatable species, a phenomenon now termed Batesian mimicry. The calculus of Batesian mimicry is complex. The unpalatable species, the model, would seem to be parasitized by the palatable species, the mimic. Because it closely resembles an unpalatable species, the mimic enjoys the umbrella of protection provided by the presence of the model. For the model, the presence of the palatable mimics makes the education of predators more difficult. Suppose a predator encounters one or even two palatable mimics as its first experience. It may be subsequently more difficult for the predator to “learn” that the noxious model is, indeed, noxious. If the mimic were as abundant as its model, the entire system would be relatively unprotected, because predators would encounter palatable mimics as readily as unpalatable models. But there is an alternative possibility. By sheer numbers, even palatable mimics could act as mutualists with models. If there is more overall food available to predators because of the presence of mimics, predation pressure on models will be relaxed. Butterflies exhibit numerous examples of Batesian mimicry throughout the tropics. However, they are not the only Batesian mimics. Many other insect species have evolved mimicry. Even in the temperate zone

Plate 11-48. This caligo butterfly (Caligo eurilochus) shows substantial damage along the lower edge of its wings. The outlines of bird beaks, likely those of motmots, are clearly visible. Photo by John Kricher.

Plate 11-49. Heliconius doris adult on a milkweed flower. There is little subtlety in the coloration patterns of heliconid butterflies. Photo by John Kricher.

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Figure 11–1. Comparison of distributions of Heliconius erato and H. melpomene. Note the divergence within each species’ convergence over its range, but the convergence in pattern between the two species wherever they co-occur. Reprinted with permission from Turner, J.R.G. 1975. “A Tale of Two Butterflies.” Natural History. 84: 29–37.

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some fly species have evolved to look similar to bees and wasps, presumably gaining protection from their similarity to aggressive insects.

Müllerian Mimicry Although Batesian mimicry is well represented in the tropics, recall that most tropical plant species contain defense compounds. Therefore, any caterpillar species will likely have to cope with defense compounds in adapting to a food source. Various degrees of unpalatability among caterpillars should be expected in the tropics, because so many of the food plants encountered by the larval insects have defense compounds that, if stored or metabolically modified by the insect, could render the creature unpalatable. Such secondary metabolites represent strong selection pressures on lepidopterans. In 1879, Fritz Müller suggested that two or more unpalatable species would benefit in evolutionary fitness by close resemblance. If two unpalatable species look alike, the would-be predator needs to be educated only once, not twice. The greater the resemblance, the greater the advantage would be to each species. This concept of convergent patterns among unpalatable species is termed Müllerian mimicry. Müllerian mimicry is in theory mutualistic, because individuals of both species benefit from the mimicry. But there may be many cases in which species show varying degrees of palatability. Nonetheless, simulations have demonstrated that when predators have an array of prey from which to choose, any resemblance to one another among prey can induce intense selection for mimicry. Both Heliconius erato and H. melpomene are unpalatable; both are brilliantly colored, and they look remarkably alike. What is even more remarkable is that there are 11 distinct morphs (or races) of H. melpomene in the American tropics, ranging from Mexico to southern Brazil. These morphs do not look the same. John Turner learned that for every local morph of H. melpomene, there is a virtually identical local morph of H. erato. Both species have converged in morphological variation throughout their ranges (fig. 11-1). Only one morph of H. erato, which is restricted to a small range in northern South America, lacks a H. melpomene counterpart. Fieldwork in which wing patterns are manipulated has demonstrated selection for Müllerian mimicry. For example, in a study performed in western Ecuador

using local morphs of Heliconius erato, H. cydno, and H. eleuchia, those butterfly morphs that were most distinctive, whose wing coloration or pattern did not match the predominant model, consistently suffered higher rates of predation. More recent genetic studies on heliconid butterflies by the Heliconius Genome Consortium (2012) included the sequencing of the genome of Heliconius melpomene. Using the genome sequences as a baseline, researchers compared gene sequences and chromosomal evolution among other heliconid species with those of H. melpomene. What was learned is that gene exchange through hybridization is clearly implicated among H. melpomene, H. timareta, and H. elevatus, which are all co-mimics. Furthermore, the hybridization is most apparent in the gene sequences controlling the mimicry patterning. The study concluded that hybridization among the various species, which has promoted exchange of gene sequences, has had a profound effect on rapid evolution of the present mimicry patterns. Given the level of potential protection afforded by mimicry, it is likely that any negative effects of hybridization are offset.

Aposematic Insects as Guides for Bioprospecting The presence of numerous plant defense compounds in sweeping numbers of tropical plant species has led to the concept of bioprospecting, the attempt to discover compounds of potential medical use in plants. It has long been appreciated that tropical peoples are often keenly aware of the medicinal and other uses of plants (ethnobotany); this topic is discussed in greater detail in chapter 17. Bioprospecting attempts to screen plant species for potential efficacy as drugs for use in treating a wide range of human diseases. Thus far bioprospecting has yielded some promising drugs for use in cancer treatment as well as for treating severe parasitic agents such as those that cause leishmaniasis (see Appendix: Words of Caution). In a unique approach to bioprospecting, Julie Helson and colleagues looked at the presence of aposematic insects as potential indicators of plants with active chemicals that could prove useful against disease. The logic was straightforward applied evolutionary theory. Plants with potent compounds exert a selection pressure such that only a few insect types evolve to

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utilize the plant (such as heliconid caterpillars gaining evolutionary access to Passiflora). In turn, these insect herbivores should be under selection pressure to evolve aposematic coloration. Thus the more aposematic insects associated with plants, the more likely the plants are to be biochemically active with regard to potential drugs. Plant species for the study were chosen from among 1,380 species. Bioassays of the various species were tested for activity against various cancers and parasites. The species tested were taken from six plant families and were chosen based on consistent activity or inactivity in bioassays, accessibility in the field, and abundance in the field. Active (meaning that it had been determined that medically active compounds were present in the plant) and inactive plant species were paired and examined for presence of aposematic insect

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species. Twenty plant species (10 active, 10 inactive) were examined. The results showed that aposematic insect species were present on both active and nonactive plants but were proportionally more represented on active plants. The researchers concluded, “The presence of aposematic insects can therefore indicate that a particular tropical plant may contain biologically active compounds. As non-aposematic insects are more equally associated with active and inactive plants, using all the insects collected on plants may not be as informative as using only aposematic insects.” It was also observed that aposematic insects were common on plants with non-active compounds, but the possibility exists that these insects are mimics of other species. Perhaps future bioprospecting research will begin with an insect survey.

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Plate 12-1. Rivers offer visitors wonderful opportunities to see Neotropical nature. Photo by John Kricher.

Plate 12-2. There is much to be seen by cruising rivers. This caiman has attracted several butterflies to its face. The insects are likely obtaining minerals from the secretions around the caiman’s eyes. The exposed river sediment suggests that the photo was taken in dry season. Photo by Sean Williams.

Plate 12-3. Marshes add to habitat complexity along rivers and host numerous species of animals. Photo by John Kricher.

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Cruising the Rivers to the Sea

Neotropical River Ecosystems: Orinoco and Amazon

(riverine) forests. In addition, rivers are bordered by numerous ecosystems, including swamps, marshes, streams, oxbows, and river islands. Each of these habitats contains species that otherwise would not be seen along the main rivers, adding significantly to regional diversity and the satisfaction of river travel (plate 12-3).

One of the most enjoyable ways to explore Amazonia is to take a river cruise. Excellent well-apportioned boats specifically designed for ecotourism on the Amazon River launch from Iquitos, Peru, and Manaus, Brazil. Wonderful travel is also available along the Río Napo in Ecuador and in numerous other wetlands, including the Pantanal floodplain of Brazil and the seasonally inundated Llanos (Plains) of Venezuela. Similar trips can be booked in Central America, particularly Belize, Costa Rica, and Panama. As you ride along the various Neotropical rivers you will see not only the sights and hear the sounds from the forest along the river itself, but you will also likely have the opportunity for exploration of backwaters and inlets, where even more wildlife is found (plates 12-1–2). Because of wet-dry seasonality, tropical rivers experience an annual flood cycle that exerts a significant impact on bordering ecosystems, especially gallery Valle de la Pascua

Rio Apure Arauca

The Orinoco River The Orinoco River is 2,140 km (1,330 mi) long, flowing northeast from the Río Guaviare in eastern Colombia and bisecting Venezuela before exiting to the Atlantic Ocean (fig. 12-1). Considering average annual discharge, it ranks as the third-largest river in the world. The Orinoco Basin, though large, is but one-sixth the area of the Amazon Basin, to which it connects via the Río Casiquiare, which flows into the Río Negro, which itself is part of the Amazon Basin. Much of the Orinoco Basin drains the geologically ancient Guiana Shield, located southeast of the main river (discussed below). EI Tigre

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The Unique Tepuis The smooth terrain that prevails in much of southeastern Venezuela, part of the geologically ancient Guiana Shield, is sharply punctuated by about 100 scattered, flat-topped mountains called tepuis (plate 12-4) that together occupy an area of about 500,000 km2 (200,000 mi2). Tepuis are not part of the Andes, but are much older. Were they located in the United States, tepuis would be called mesas or table mountains, in reference to their characteristic flattened summits. The word tepui, taken from the Peñon Indian language, means mountain. Rising abruptly from the flattened lowlands of the Gran Sabana and its surrounding tropical rain forests, tepuis rise from their forest-enshrouded bases as vertically steep, rocky escarpments to heights of over 1,500 m (5,000 ft). The tallest, Mt. Roraima, is 2,810 m (9,220 ft). The tepui region, located approximately 650 km (400 mi) south of the coastal city of Caracas, is home to the world’s highest waterfall, Angel Falls, which plummets 979 m (3,212 ft) from atop Auyan-tepui. Angel Falls (named for the bush pilot Jimmy Angel, who “discovered” it in 1935), is one of hundreds of waterfalls spilling from various tepuis, continuing the ancient process of erosion. Tepuis are of interest not only for their obvious stark beauty but also for their intriguing geological history. They are ancient and eroded. If one could project oneself back through time, to somewhere between 400 and 250 million years ago, the tepui region would be in close proximity to what would eventually become the division between South America and Africa, an area of lowlands in proximity to the sea. Between 180 and 70 million years ago, during the Mesozoic era, when dinosaurs were abundant, the future tepui region began to take shape as tectonic activity was separating the continents. At this time the Andes were being uplifted to the west and the Roraima Plateau was being eroded by a combination of tectonic and meteorological activity. Evidence for continental drift is seen in the sandstone of the tepuis,

virtually identical to that found in the mountains of the western Sahara. Erosion continued throughout the Cenozoic era and the flattened tops of today’s tepuis are all that remains of the once extensive Roraima Plateau. Most of the mass of sandstone that once composed the plateau has long since found its way to the oceans through the continuous process of erosion. Today’s tepuis represent but a fraction of that sandstone. The flattened, eroded tops of the tepuis represent “sky islands,” an archipelago of isolated mountaintops. Receiving as much as 400 cm (157 in) of rain annually, much of it in the form of deluges from thunderstorms, the plants and animals that tenant each tepui have evolved essentially in isolation from populations in the surrounding lowlands and, for that matter, on other tepuis. Sir Arthur Conan Doyle was so inspired by the splendid isolation of the wet, cloud-enshrouded tepuis that he chose the region as the setting for his 1912 science-fiction novel The Lost World, about a land where dinosaurs could still be found. No dinosaurs have as yet been located on any of the tepuis, nor are they likely to be, but the biota is nonetheless of great interest. At least half of the tepuis’ approximately 10,000 plant species are endemic, a clear example of the effect of evolution on isolated populations. Orchids abound, with 61 species found on Auyan-tepui alone. Also common are various plants that consume insects, such as pitcher plants and sundews. The soil atop the tepuis is poor, mostly eroded rock. Insectivorous plants are advantaged in such a soil-impoverished habitat, because they can supply their need for such nutrients as nitrogen and phosphorus by digesting insect bodies. If you want to visit a tepui you are more or less out of luck. I know of no tours that will drop you atop one. It is, however, possible to arrange a flight that will take you very close to them, in range of outstanding views of Angel Falls.

Plate 12-4. The “sky islands” in the distance are tepuis, ancient table mountains of Venezuela. Photo by John Kricher.

cruising the rivers to the sea

The Orinoco begins at an elevation of 1,074 m (3,523 ft) in the Parima Mountains close to the border between Venezuela and Brazil. It soon bifurcates into the southern and northern streams, the former of which flows southward, eventually joining the Río Negro and flowing into the Amazon, the latter flowing north and east, joining major tributaries such as the Río Meta, Río Arauca, and Río Apure. The major city located along the Orinoco is Ciudad Bolívar, in Venezuela, where the river is typically about 244 m (800 ft) wide. Ships can navigate the Orinoco for about 1,120 km (700 mi), from its mouth to the Cariben rapids, 9.6 km (6 mi) from the Río Meta. Like the Amazon and its tributaries, the Orinoco is strongly seasonal. At Ciudad Bolívar the annual variation between high and low water level is between 15 and 18 m (approx. 50–60 ft.). Rainy season in the Orinoco Basin is from April to October; dry season extends from November through March. Discharge rate varies with seasonality; the lowest flow during dry season is only 1/25 to 1/30 of the highest flow during wet season. The Orinoco River bisects two distinct geological areas. The right (southern) bank of the Orinoco borders Precambrian bedrock from the Guiana Shield, at 1.7 billion years old one of the oldest geological formations on Earth. In contrast, the land bordering the left (northern) bank of the main river is geologically recent, formed only a few centuries ago from sediments washed from the Andes and transported across the flattened Llanos. The effect of these differing geological histories is reflected in the differing characteristics of the tributary rivers that drain into the main Orinoco. The right-side tributaries typically are stable, constrained by crystalline bedrock and, especially within the Guiana Shield, abundantly supplied with rapids and waterfalls. The left side tributaries are unstable, with shifting channels formed by alluvial deposits from the river. The Orinoco flows west, then north, before beginning its major eastward flow. The river itself has had a strong influence on the geology of the region, having helped cut channels through parts of the Guiana Shield, thus contributing to the isolation of a unique series of flattopped table mountains called tepuis, some over a mile high (see “The Unique Tepuis” sidebar). The highest waterfall on the planet, Angel Falls (Kerepakupai Merú), drops from the top of one of these tepuis. Much of the Orinoco flows quietly and slowly through the vast marshy Llanos region of Venezuela (chapter 14), a region of relatively flat plains and marshes that supports abundant wildlife.

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The Orinoco meets the Atlantic Ocean at the Amacuro Delta and Gulf of Paria, an area of extensive mangrove forests that Columbus explored in 1498, calling it a “gateway of the Celestial Paradise.”

The Amazon River The Amazon River, or Río Amazonas, is a vast river that forms at the confluence of the Marañón and Ucayali rivers just west of Iquitos, Peru, flowing eastward 6,437 km (4,000 mi) to the sea (fig. 12-2). In Brazil the name Amazon is formally used from Manaus, Brazil, eastward, but west of Manaus the river is called the Río Solimões. As mentioned, the main river first takes shape as a confluence of several major Andean tributaries, principally the Ucayali, the Marañón, and, to a lesser degree, the Tigre, all just west of Iquitos, Peru. The headwaters of the Amazon were difficult to discover because of the challenging climatic conditions that prevail at high elevations in the Andes. But the river was eventually traced to a small, unremarkable tributary, the Carruhasanta, at an elevation of 5,598 m (18,363 ft) in the cold, windswept Peruvian Andes, only about 192 km (120 mi) from the Pacific Ocean. The Carruhasanta flows into the Hornillos, which in turn joins the Apurímac, a major tributary that eventually joins the Ene, the Tambo, and finally the Ucayali. The Amazon system plunges in elevation initially but drops only about 5 cm per 1.6 km (2 in/mi) once outside the Andes, eventually flowing to the Atlantic Ocean. The Amazon is the world’s longest river, measuring 6,993 km (4,345 mi), just surpassing the Nile River in length. However, the Amazon carries the world’s largest volume of water by a wide margin. About 16% of all river water in the world passes through the 320 km (200 mi) wide delta of the Amazon, which daily discharges about 17 trillion liters (4.5 trillion gal), or about 200,000 cubic meters of water per second (7.4 million ft3/sec). This represents a discharge of about 4.4 times that of the Congo (Zaire) River, the next most voluminous river. The plume of sediment-laden water from the Amazon can be seen as far as 100 km (about 60 mi) out to sea and has been traced by NASA’s Coastal Zone Color Scanner (CZCS) as it moves toward Africa between June and January and toward the Caribbean from February through May. The river itself is over 10 km (about 6 mi) wide as far as 1,600 km (1,000 mi) upriver, and large ships can navigate for over 3,700 km (2,300 mi), eventually docking at Iquitos,

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Peru. Two Amazonian tributary rivers, the Negro and the Madeira, rank as the fifth- and sixth-largest rivers in the world with regard to annual discharge. By comparison, the Mississippi River ranks about 10th and has only about 1/12 the annual discharge of the Amazon. To the surprise of many, the Amazon River originally flowed in the opposite direction, draining into the Pacific Ocean near what is today the port city of Guayaquil, Ecuador. The river changed to its present west-to-east course as recently as 10–15 million years ago, when the Andean uplift profoundly altered the river’s course, as well as patterns of biogeography, creating the Amazon Basin. Initially the uplift of the Andes created a gigantic lake, bordered on the west by the newly arisen mountain chain and to the east by the extensive Guiana and

Brazilian Shields. The Amazon finally made its way to the Atlantic during the Pleistocene, cutting through its eastern barrier in the vicinity of Obidos, Brazil. Many widespread trees were probably dispersed eastward by the altered course of the river water. The Amazon Basin, drained by the Amazon River and its gigantic tributaries, covers an area of about 6.92 million km2 (about 2.67 million mi2) essentially 40% of the total area of South America. Approximately 1,100 tributaries service the main river, and some of them, like the Negro, Napo, Madeira, Tapajós, Tocantins, and Xingu, rank as major rivers. Amazon tributaries vary in color from cloudy mocha to clear black depending upon where they originate and their geological and chemical properties (chapter 6).

Caracas VENEZUELA

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Brasilia Santa Cruz BRAZIL

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Figure 12–2. Map of the Amazon River and its major tributaries. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

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Examples of major blackwater rivers include the Río Negro and Río Urubu. Clearwater rivers include the Río Tapajós, Río Trombetas, Río Xingu, and Río Curuá Una. Whitewater rivers, abundant with sediment, include the Río Jutaí, Río Juruá, Río Madeira, Río Purús, Río Napo, and the upper Amazon itself. Before the ever-increasing numbers of roads and airstrips, these tributaries served as the only access to the interior. Cities such as Iquitos, Peru, are, even now, accessible only by boat or airplane.

The Amazonian Flood Cycle Standing in the downpour watching the trails turn into mud, I was surprised at first to discover that the level of the Amazon itself, near were I stood, was dropping nearly 1 m (3.3 ft) a day, even as it was raining heavily throughout the region. But the river’s depth was not closely tied to the rain falling on this rain forest near Iquitos, Peru. The river was dropping because it had stopped snowing in the Andes, the meltwater had already drained, absorbed by the Amazon. Now the huge river was receding from its peak flood. The timing of floods and the distribution of floodwaters result from a complex pattern of seasonal precipitation, much of it in distant mountains. Because of the vast area of the Amazon Basin, at any given time some regions will be experiencing flood while others are at low water. This is because the equator divides Amazonia (though it is north of the river itself) and many of the major Amazonian tributary rivers are either partly north or entirely south of the equator. Rainy season generally occurs in southern Amazonia from October to April. Rainy season in Manaus, in the middle of the basin, is from November to May, and rainfall is highest in the northern part of the basin from April through June. The wettest months in Iquitos, Peru, which receives between 300 and 400 cm (118–157 in) of annual rainfall, are February through May, though there is much variability. In fact, according to meteorological records kept at Iquitos Airport, every month of the year except May has, at one year or another, been the low water month. Seasonality in Iquitos is rather variable. In general, flooding in the northern waters occurs as southern waters are low and vice versa. In areas fed by one major tributary, there is a single annual flood. But in those regions fed by both southern and northern tributaries, there are two annual flood periods, which may differ from one another in intensity. As rainy

Plate 12-5. These houses on stilts are part of the city of Iquitos, Peru, which is subject to strong flooding by the Amazon River during the peak of the annual flood cycle. Photo by John Kricher.

season proceeds, floodwaters build such that the peak of the flood cycle usually occurs at the onset of dry season. Because some parts of the Amazon are at flood while other parts are at low water, there is little difference between the minimum and maximum annual discharge rates, which vary by only a factor of two or three. This is in marked contrast to the Orinoco River, all of which lies north of the equator (discussed above). The low, flat geomorphology of the Amazon Basin is conducive to flooding (plate 12-5). Though sediment has a strong tendency to build up along riverbanks, forming levees, Amazonian rivers will routinely overflow their banks at full flood. The general floodplain is characterized by land that is not uniformly flat, creating habitats such as temporary lakes and swamps. Floodplain forest is estimated to occupy approximately 100,000 km2 (38,610 mi2) within the total Amazon Basin. The ecological importance of the flood cycle should not be underestimated. Amazonian rivers experience an annual fluctuation that averages between 7 and 13 m (23–43 ft), which can result in a floodplain forest inundated to a depth of 10 m (33 ft) annually, a water fluctuation that can bring river water as far as 20 km (12.5 mi) into the neighboring forest. Flooding is essential in dispersing sediment, fertilizing várzea floodplain forests, and enabling fish and other organisms to make use of gallery forest during high water (and act as seed dispersers, as described in chapter 10). Zooplankton reproduction peaks during high water, and this resource, which washes into neighboring rivers as the flood recedes, provides an invaluable resource for fish, especially, but not exclusively, during their juvenile

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life-cycle stages. Until recently, the extensive damming activities routinely seen in countries such as the United States were unknown in South America. Damming changes the flood cycle, isolating previously flooded areas from the annual flooding. Doing so throughout much of Amazonia would cause a substantial disruption of many ecological relationships and interdependencies. This topic is discussed more in chapter 18.

Diverse Riverine Habitats In the ecological sense, rivers are really part of the terrestrial ecosystems that border them. A river is dynamic: it varies seasonally and, with time, turns and twists within its floodplain, creating a diversity of habitats.

Open River From a ship sailing upriver on the Amazon, the width of the vast river can take on the appearance of a small inland sea (plate 12-6). Strong currents and continuously changing underwater sediment bars make navigation challenging, and large ships sometimes run aground. There is not much wildlife to be seen on the open river (though there is much in it). In the central and lower Amazon, skies are typically clear above the widest stretches of the river, while neighboring forests have clouds above, the result of forest transpiration. But along the upper Amazon the humidity is often such that the river itself is cloud-covered and subject to intense cloudbursts.

Beaches and Sandbars The vast tonnage of sediment washed from the Andes and carried by the tributaries and the Amazon itself is often deposited along the river edge or as bars in the river itself (plates 12-7–8). Along the várzea forests of the upper Amazon the sediment is deep blackish gray, the rich volcanic soil transported from the high Andes. Altered annually by the flood cycle, sediment deposits form extensive beaches and sandbars that provide habitat for birds such as plovers, Black Skimmer, and various herons and egrets, as well as good resting places for caiman. Swallows of various species, mostly seen in flight over the river, can often be seen perched on small snags and bushes along beaches and sandbars.

Sandbar Scrub Andean sediment is rich in nutrients and does not go uninhabited for very long. Once sediment is deposited from the action of riverine dynamics, the area is subject to colonization by pioneer plant species. Various plants, including those of such familiar temperate genera as Salix, the willows, quickly invade and often become sufficiently dense to stabilize the soil. Sandbar scrub is typically dense, composed of a low diversity of fast-growing, colonizing plant species (plate 12-9).

River Islands From the riverside walk at Iquitos, Peru, you cannot see across to the far side of the Amazon River, but that’s not because the river is too wide. It is because the far bank is usually blocked from view by huge sediment islands. Padre Island is the main island visible from Iquitos, though just to the west of the city one finds Timarca and Tarapoto islands. River islands can be of all sizes, but the big ones are stable, composed of years of sediment deposit stabilized by vegetation invasion (plate 12-10). Forests grow on the river islands and can be managed for sustained yield of various products. Many humans inhabit and farm the river islands (as well as várzea floodplain bordering rivers), planting rice, corn, peppers, beans, and bananas. Whole towns can be found on the larger islands. The riverine people, called ribereños in western Amazonia and caboclos in Brazil, have long inhabited riverine areas, and actively alter the species composition of the forest in order to achieve economic gain. A study from the southeastern portion of the Amazon estuary in the vicinity of Belém, Brazil, and the Río Tocantins demonstrated that the local people employ several management techniques, including the active removal of unwanted plant species (such as certain spiny palms), removal of firewood species, cultivation of such species as cacao, avocado, and mango, and maintenance of potentially useful species such as rubber trees. The result of such management activities is that the forest is altered in species composition but is nonetheless maintained as forest in a sustainable manner. Ribereños also are active agriculturalists, planting maize, rice, manioc, bananas, and other crops. Fish are the major protein source for most river inhabitants. River islands, beaches, sandbars, and sandbar scrub are all related in a process that ecologists term point bar ecological succession. In this process, when a sandbar forms it provides habitat for plants, and through seed

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Plate 12-6. Near the mouth of the Amazon River, one of its wider areas. Photo by John Kricher.

Plate 12-7. Beaches forming from sediment deposit in the Río Napo, Ecuador. Vegetation is beginning to colonize the deposit. Photo by John Kricher.

Plate 12-8. Grasses quickly colonize exposed beach along the Río Napo. Photo by John Kricher.

Plate 12-9. Sandbar scrub has stabilized this island in the Río Napo. Photo by John Kricher.

Plate 12-10. River island in the Río Napo. Photo by John Kricher.

Plate 12-11. The point bar shown in this image is already being colonized by plants that will eventually stabilize it, contributing to its expansion. Photo by John Kricher.

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dispersal, plants quickly colonize (plate 12-11). As the colonizers stabilize the sandbar, it builds, forming a point bar and eventually supporting a sandbar scrub community that replaces the original colonizers. But by then more sand has been added, so the colonizers persist as the bar grows ever larger. It may, depending upon the dynamics of the river, become sufficiently large to form a substantial river island. The dynamic nature of tropical rivers is evident in the ever-changing pattern of point bars and riverine island distribution.

Oxbows Where the flow dynamics of the river become unstable (typically during the high water period), the river may cut a new channel, effectively isolating a meander and creating what is called an oxbow lake, a habitat of essentially standing water. Oxbows are common in rivers subject to a variable flood cycle and they provide yet another kind of riverine habitat, where water stagnates rather than flows rapidly. Such still water supports vast growth of water hyacinth, as well as the giant Victoria Water-lilies (Victoria amazonica; chapter 10). It is here that the peculiar Hoatzin can be found (see “Hoatzin: Bizarre Bird of the Riverbanks,” below).

Floating Meadows Entire islands of floating grasses can be encountered along the Amazon and within Amazonian lakes. Along the main rivers, some of these grassy islands occasionally reach a size at which they can be a hazard to navigation. Two grasses, Paspalum repens and Echinochloa polystachya, are abundant components of the floating meadows and together make up about 80–90% of all the floating grass species of Amazonia. Paspalum is adapted to float, forming dense, floating mats for the four- to five-month rainy season, when the river is high. The plants grow and spread asexually during this time, but also flower and make seeds, so that during dry season multitudes of seeds fall on the newly exposed ground, to quickly germinate. Thus Paspalum is adapted to be both a floating and terrestrial plant. Terrestrial Paspalum has a distinctly different morphology from the aquatic form, even though they are the same species. Unlike Paspalum, Echinochloa has no floating morph, but remains rooted throughout the flood cycle. This species is most common in lakes.

Moriche Specialists: Birds and Moriche Palms Stands of Moriche Palm are prime feeding areas for various large macaw species whose powerful bills are sufficiently strong to crack the hard palm nuts that occur in dense clusters below the fronds. Other bird species have become Moriche specialists, rarely if ever found away from Moriche stands. These species provide examples of an important component of Neotropical species diversity, the tendency toward extreme habitat specialization. The Moriche Oriole (Icterus chrysocephalus), a small, striking black oriole with bright yellow crown, shoulders, rump, and thighs, feeds and nests within Moriche fronds. The Sulphury Flycatcher (Tyrannopsis sulphurea) is a gray-headed, yellow-bellied bird, easily confused with the widespread Tropical Kingbird (Tyrannus melancholicus). Both species can be difficult to see well in the dense palm fronds. More obvious, the Fork-tailed Palm-Swift (Tachornis squamata) is a common aerial feeder, streaking through the skies in the vicinity of Moriche stands in search of insect prey. This pale swift with a deeply forked tail builds its nest on the underside of a dead Moriche Palm leaf. Finally, the Point-tailed Palmcreeper (Berlepschia rikeri), a member of the Furnariidae, or ovenbird family, is entirely confined to Moriche Palm stands in Amazonia, and is nowhere really common. It is difficult to spot among the dense, fanlike palm fronds, but its presence can be known from its song, a loud series of ringing notes. The bird is bright cinnamon on the wings and tail and streaked boldly with black and white on its head and breast. View it really, really well, and you’ll see its bright red eyes.

Plate 12-12. Moriche Palm swamp. Photo by John Kricher.

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Swamps A swamp is generally an area of woody vegetation that is inundated by standing water for a significant part of the year. Swamps are typically much lower in tree species richness than less wet sites, and some swamps are made up mostly of a single species. Many swamp tree species have stilt root systems, and buttressing of the trunk is extremely common as well (chapter 3). Along the coast, where saltwater incursion is normal, swamps are composed of various combinations of mangrove species (mangroves are discussed later in this chapter). Throughout interior Amazonia the most characteristic swamp forests are composed of palms, notably the Moriche Palm (Mauritia flexuosa; plate 1212). Commonly called buriti in Brazil, the Moriche is one of the most distinctive, abundant, and widespread Neotropical palms, growing in swamps and along wet areas, often forming pure stands. A Moriche Palm swamp forest is termed an aguajale. Moriche Palms are tall and slender, their fronds appearing as spike-tipped fans on elongate stalks that radiate from a common base atop the trunk.

Flooded Forests Floodplain forests within the Amazon Basin cover an area of approximately 150,000 km2 (approx. 58,000 mi2). Overall, floodplain forest comprises only about 4% of the total Amazon Basin, the remaining forest all being terra firme. Floodplain forests are so named, of course, because they are inundated by the annual flood cycle. Depending upon location, floodplain forests may be inundated for anywhere from two to 10 months out of the year. Flooded forests have lower tree species richness than terra firme forests. A few are largely dominated by a single species. Thus far it is unclear how physical conditions influence the relative species richness of trees occupying flooded forests. Perhaps dry-season effects and wet-season effects combine to affect survival of swamp-inhabiting species. The ability of root systems to grow deeply in flooded forests may be essential in the trees’ surviving drought stress during dry season as well as inundation in wet season. Flooded forests may border whitewater, clearwater, or blackwater rivers (chapter 6). Whitewater flooded forests, where soil nutrients are abundant, are typically higher in stature and biomass (and probably species richness) than clearwater rivers. Flooded forests of

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blackwater rivers are typically low in stature, and species richness tends to be a bit lower and to vary less from site to site as compared with whitewater rivers; many species of these forests are important fruit and seed consumers as well as seed dispersers. There is no simple explanation for how plant species that may be flooded for most of the year are able to survive such conditions. Their roots lack access to oxygen for much of the year, and yet there are no obvious physiological or anatomical adaptations that explain how they endure such immersion. Certain monkey species are restricted to floodplain forest, as are many species of birds and arthropods. Some plant species are unique to flooded forests, though many have closely related species in dry forests, suggesting a recent speciation between dry and floodplain species. Perhaps most important, many fish species are active consumers of fallen fruit during the wet season when the forests are flooded, and in some cases are important seed dispersers. One in particular, the Tambaqui (Colossoma macropomum), is considered uniquely important in this regard (chapter 10). Floodplain forest is not an absolute term. Some forested areas are located immediately adjacent to the river and flood frequently, while areas further from the river may be flooded infrequently.

Observing Wildlife along the Rivers and Tributaries Two Dolphins and Two Manatees There are two well-known species of freshwater dolphins found in the Amazon and its major tributaries, and both are relatively common and frequently observed. The largest and most widespread is the Pink River Dolphin, or Boto (Inia geoffrensis; plate 12-13). In Spanish-speaking areas it is usually called bufeo or tonina, while boto is its name in Portuguese-speaking Brazil. Pink River Dolphins hunt for fish and other aquatic animals (turtles, crabs) in muddy waters of the Amazon and Orinoco Basins, and they forage among the trees of flooded forests. They are pale in color, often distinctly pinkish, and range in length from about 2 to 2.5 m (6.5–8.2 ft) and have a long, slender snout, bulbous head, and a modest dorsal fin. Botos are usually in small groups of two to four animals, often at the mouth of a tributary or stream. Unlike the majority of dolphins, Botos have a flexible neck, put

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Plate 12-13. The Pink River Dolphin often allows close approach from boats. Photo by Andrew Whittaker.

Plate 12-14. West Indian Manatees reach as far north as the central Florida coast. Photo by John Kricher.

to good use as they search for food among the trees of the flooded forests. They do not have keen eyesight but have effective sonar, permitting them to navigate among the dense trunks of the forest. The second dolphin species is Sotalia fluviatilis, the Tucuxi (pronounced too-coo-she) or Gray Dolphin. Tucuxis are smaller and darker than Botos, reaching no more than 1.5 m (5 ft) in length. They have a shorter snout, much less bulbous head, and a more distinctive triangular dorsal fin. They normally show much of the head when they surface, and they often leap from the water. Tucuxis are found in larger groups than Botos, of from two to nine. Tucuxis are scarce or absent in most of the Orinoco Basin, probably due to seasonal changes in water depth. In the Amazon, Tucuxis are found typically in deeper waters than Botos. Tucuxis are so characteristic of deeper waters that river pilots observe them for navigational aids. A manatee more or less resembles a huge sausage with a small, puffy-looking head adorned with a wide, blunt snout and short whiskers. The body tapers into a fan-shaped tail used to swim. The forelimbs, adapted as flippers, are small. Manatees are in the mammalian order Sirenia (the name refers to the fact that these odd, homely animals were allegedly once mistaken for mermaids, or sirens). There are only three extant species, though some authorities argue that there are four. The Amazonian Manatee (Trichechus inunguis) is a close relative of the larger West Indian Manatee (T. manatus; plate 12-14). The Amazonian Manatee reaches a length of about 2.8 m (approx. 9 ft) and can weigh up to 500 kg (1,100 lb). It ranges throughout

much of the Amazon and its major tributary rivers, but it takes luck to see it, as it has been reduced throughout its range to the status of endangered species. Hunted for meat, oil, and hide, this once abundant creature, though now protected, still suffers persecution. The similar West Indian Manatee fares a bit better, enjoying protection, especially where it occurs along Florida’s coast and rivers. Manatees are strict vegetarians, harvesting plant material such as water lettuce and water hyacinth. They are social animals, usually in small groups. The only time they tend to be aggressive is when they are attempting to mate and tensions mount.

Capybara: Master of the Grasses The Capybara (Hydrochoeris hydrochaeris; plates 12-15–16), growing to 1.3 m (4 ft) long and 100 kg (about 220 lb), holds the title of the world’s largest extant rodent. A slightly smaller species, the Lesser Capybara (H. isthmius), occurs in northern South America, from eastern Panama through parts of Colombia and Venezuela. Both Capybara and Lesser Capybara are essentially identical in their ecologies. This account focuses on the larger Capybara. Ranging throughout most of lowland South America, from Panama to northeastern Argentina, the Capybara is aquatic, ecologically similar to the much larger African hippopotamus. A stocky, essentially tailless, caviomorph rodent (thus related to guinea pigs), the Capybara has a pale tan coat and short, thick legs. The toes are partially webbed, and the eyes, ears, and nostrils are located on

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the upper part of the squarish head, all adaptations to the animal’s aquatic lifestyle. Capybara vocalizations sound strikingly like those of guinea pigs, though you must have the luck to approach a contented one closely to hear its charming little squeaks, twitters, and grunts, which sound far more delicate than one might expect from a couple hundred pounds of rodent. Though capybaras are usually found in small family groups, herds can grow to 50 or a 100, especially in the Venezuelan Llanos or Brazilian Pantanal, where the animals remain abundant. Capybara groups typically spend most of their time in and along watercourses feeding on water-lilies, water hyacinth, leaves, and sedges that line Amazonian rivers, lakes, and swamps (plate 12-17). The name capybara translates as “master of the grasses,” a reference to the animal’s abundance on wet savannas. The species’ natural enemies, as might be expected, are caimans, Jaguars, and anacondas. In many places humans have hunted capybaras, and populations have been drastically reduced. In other areas, however, such as the vast ranches on the Venezuelan Llanos (chapter 14), capybara populations, when properly managed, provide a sustained yield of meat and leather.

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Plate 12-15. Capybaras have an air of quiet dignity about them, at least for large rodents. Photo by John Kricher.

A Really Big Otter The largest member of the weasel family (Mustelidae) is the Giant Otter (Pteronura brasiliensis; plate 1218), found throughout Amazonia but uncommon in many areas. The adult measures almost 1.5 m (5 ft) in length, not counting its meter-long (3.3 ft) tail. The species is identified by its large size (a really good field mark), fully webbed feet, and semi-flattened tail, somewhat like an elongate beaver’s tail. Giant Otters are social, and groups forage diurnally in the quiet waters of the Amazonian tributaries, especially around oxbow lakes (plate 12-19). Carnivorous, they feed on fish, mammals, birds, and other vertebrate prey, some sizable (plate 12-20). Giant Otters are common and seen well where they are protected, as in some areas of the Brazilian Pantanal. Unfortunately, in other areas they are much reduced by hunting (taken for their skins and because they are perceived as competitors with humans for fish) and are listed as endangered by CITES (Convention for International Trade in Endangered Species; https:// cites.org/eng) and IUCN (International Union for Conservation of Nature; http://www.iucnredlist.org).

Plate 12-16. Young capybaras are tended by parents, and groups are organized in various-size herds. They are preyed upon by caimans, anacondas, and Jaguars. Photo by John Kricher.

Plate 12-17. Food, namely plants, is abundant for capybaras, which often spend much of the day lounging in marshes and along riverbanks. Photo by John Kricher.

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Should you see an otter that is not really giant, you are looking at a Southern River Otter (Lontra longicaudis), a species that ranges throughout the Neotropics as far south as Uruguay, and to elevations as high as 3,000 m (9,843 ft). The Southern River Otter is but half the size of the Giant Otter and can be identified by its all-white throat and belly and non-flattened tail. Though widely ranging, this species, like its larger cousin, sadly, has been reduced by overhunting and is also placed on the CITES list.

A Stupendous Serpent The largest of all the New World snakes are the magnificent anacondas, which range throughout Amazonia. There are four anaconda species, including the Yellow Anaconda (Eunectes notaeus; plate 1221) and the largest of the four, the Green Anaconda (E. murinus). Anacondas do not grow to quite the lengths of some of the Old World python species. Male Green Anacondas usually reach about 3 m (9.8 ft) and females reach 4.6 m (15 ft), though some individuals have attained greater lengths, to nearly 9 m (approx. 29 ft.). Anacondas are wider in body than pythons and are considered to be the bulkiest of the world’s snakes. One 5.8 m (19 ft) specimen, photographed with seven men holding it, weighed 107 kg (236 lb). Some have been reputed to exceed 227 kg (500 lb). Anacondas are constrictors and are nonvenomous. They feed on agoutis, capybaras, peccaries, tapirs, large birds, and even crocodiles and caiman. They do not eat people and will avoid humans by taking shelter under water. Nonetheless, it’s not a good idea to disturb a 3 m long anaconda, as the animal might, understandably, react aggressively. Not particularly skilled swimmers, anacondas normally capture prey by lying in wait along quiet, muddy, marshy riverbanks, where even an immense snake can look remarkably camouflaged when coiled at the water’s edge. Anacondas, like most snakes, are prolific breeders. One recorded birth yielded 72 baby snakes.

Plate 12-18. With a long and lithe body and flattened tail, the Giant Otter is a surprisingly fast swimmer. These otters frequently are seen along riverbanks as well as in the water. Photo by John Kricher.

Plate 12-19. Giant Otters frolicking along a riverbank. Photo by John Kricher.

Crocodilians Crocodilians are venerable survivors from the reptilian dominance of the Mesozoic era. Today’s crocodiles and caimans look scarcely different from their ancestors, whose menacing eyes beheld such equally menacing creatures as Tyrannosaurus rex (plate 12-22). The exact

Plate 12-20. Giant Otters are carnivores, enjoying a fish-heavy diet. Photo by Nancy Norman.

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Plate 12-21. Though not the longest of the anacondas, the Yellow Anaconda is thought by most observers to be the most beautiful of these remarkable serpents. Photo by Andrew Whittaker.

number of extant species in the family Crocodylidae is unclear, though the most commonly cited figures are 22 or 23. Eleven species occur in the Neotropics. The majority of the world’s crocodilian species are threatened or endangered, including some from the Neotropics, and are on the CITES list. Crocodilians eat fish and other water-dwelling animals, including capybaras, snakes, and birds. They typically are most active at night, spending the day basking, easy to see, especially in the Llanos and Pantanal, where they are abundant. A handheld flashlight during a nighttime boat trip should reveal the red eyeshine of caimans and crocodiles as they search for a meal. Crocodilians perform an aquatic mating ritual, after which females build a nest mound and lay up to 60 eggs, depending on species. Parent animals, especially the female, aid the

newly hatched young in moving from the nest to the water and remain with them for some weeks. Juveniles have many predators, including storks, egrets, raccoons, and anacondas. Adults have fewer predators, but have been severely overhunted by people. Two subfamilies of crocodilians inhabit the Neotropics, the true crocodiles (Crocodylinae; plate 12-23) and the alligators and caimans (Alligatorinae; plate 12-24). They are similar in appearance and behavior, but crocodiles have more sharply pointed snouts than alligators and caimans, and the upper fourth tooth is visible on the outside when the jaws are closed. Alligators and caimans have rather blunt and rounded snouts and do not show the upper fourth tooth when the jaws are shut. The crocodile subfamily includes the Old World Nile Crocodile (Crocodylus niloticus) and the large and

Plate 12-22. Caimans do not exhibit complex social behavior, but they do not seem to mind one another’s company when lounging on a riverbank. Photo by John Kricher.

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Plate 12-23. Morelet’s Crocodile, a Central American species. Photo by John Kricher.

Plate 12-24. The Yacare Caiman is common in southern Amazonia. Photo by John Kricher.

Plate 12-25. The American Crocodile is the only crocodile species to reach the United States, occurring in southern Florida. Photo by John Kricher.

Plate 12-26. The Black Caiman sometimes reaches a length of 6 m (20 ft), making it one of the largest of the crocodilians and the largest predator of Amazonian waters. Photo by Sean Williams.

dangerous Indo-Pacific Crocodile (C. porosus). There are four Neotropical species of crocodiles. The American Crocodile (C. acutus, plate 12-25) ranges from the Florida Keys and western Mexico southward to Ecuador, inhabiting coastal swamps. In eastern Central America the Morelet’s Crocodile (C. moreletii; plate 12-23) inhabits coastal mangroves and inland riverine habitats and is most common in Belize. The Orinoco Crocodile (C. intermedius), as the name suggests, is found in the Orinoco river basin, in Venezuela and eastern Colombia in northern South America. Finally, the Cuban Crocodile (C. rhombifer) is found in only a very limited range, the Zapata swamp in Matanzas Province on Cuba. Caimans and alligators are generally more abundant than crocodiles. They avoid salt water, occurring

instead along riverine areas. The American Alligator (Alligator mississippiensis; plate 1.7) has, thanks to protection, established healthy populations throughout most of its range in North America. This success story is not generally repeated with South American caiman species. The Common Caiman (Caiman crocodilus), which is also called the Spectacled Caiman, can be found from southern Mexico southward, all the way to parts of northern Argentina. It grows to lengths of 2.5 m (8.2 ft), occasionally larger, though very large individuals are rare. The Black Caiman (Melanosuchus niger; plate 12-26), which can grow to lengths of nearly 6 m (20 ft), is by far the largest of any Neotropical crocodilian. It inhabits the central Amazon Basin, from the mouth

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Plate 12-27. This Yellow-spotted River Turtle has a hood ornament of sorts. Photo by Sean Williams.

of the Amazon westward as far as northeastern Peru and Bolivia. The species has suffered serious population reduction throughout most of its range and is today probably most numerous in the eastern part of its range. The other caiman species are the Cuvier’s Dwarf Caiman (Paleosuchus palpebrosus), and Schneider’s Dwarf Caiman (P. trigonatus), both of which are found in the Orinoco and Amazon Basins; the Yacare, or Paraguayan, Caiman (Caiman yacare; plate 12-24), common in southern Amazonia and southward to Argentina and Uruguay; and the Broad-snouted Caiman (C. latirostris), found in southeastern South America.

Turtles Turtles are evolutionarily ancient animals; the turtle body is a unique anatomical assemblage that has impressively stood the test of deep time. The largest known fossil turtle, appropriately named Stupendemys, with a carapace (upper shell) in excess of 2 m (6.5 ft) long, is known from the Pliocene in Venezuela. You may not see many turtles when you visit Amazonia. There are only about 20 species, considerably fewer than inhabit the Mississippi River and its tributaries. Here are some examples. Amazonian turtles belong to a relatively ancient group, called side-necked turtles (Pelomedusidae), that dates back to the Cretaceous period. Side-necks do not pull their heads directly back under their shells but rather tuck them sideways. Otherwise, side-necked turtles look similar to other freshwater turtles. The prehistoric-looking Matamata (Chelus fimbriata) is an imposing turtle with a highly ridged shell and flattened head that somewhat resembles a snapping turtle. It is

a bottom dweller that is frequently caught in fishing nets but, because it does not emerge to sun itself, is not often observed by ecotourists. Riverbanks, at least in some areas, are often lined with basking Arran Turtles (Podocnemis expansa). A giant turtle species that reaches 1 m (3.3 ft) in length and can weigh in excess of 45 kg (100 lb), it was at one time vastly abundant. When Henry Walter Bates explored Amazonia in the late 19th century, he commented on the abundance of this huge turtle and how good it tasted: “Roasted in the shell they form a most appetizing dish.” Bates also said he was “astonished” at the skills of the Amazonian indigenous people in shooting turtles as well as collecting eggs. They not only hunted the turtles, they kept many captured individuals penned for later use as food. Unfortunately, Arran Turtles have been seriously reduced by hunting for both their meat and their eggs. The species is now considered endangered and is seen in only a few protected reserves. The most commonly seen turtle along Amazonian rivers today is the Yellow-spotted River Turtle (Podocnemis unifilis; plate 12-27). This species reaches a length of about 68 cm (about 27 in), and is thus far smaller than the giant Arran.

Birding along Rivers and Streams As rivers cut through rain forests and flow along marshes, as they intertwine with streams and oxbows, they provide excellent opportunities and vantage points for observing bird activity. There are numerous birding-dedicated trips that are based entirely on

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Plate 12-28. The Gray-lined Hawk (Buteo nitidus), like other raptors, is often seen perched along a river as it searches for possible prey. Photo by John Kricher.

Plate 12-29. Kingfishers, up to six species of them, are commonly seen along rivers and streams. This one is a male Amazon Kingfisher (Chloroceryle amazona). Photo by John Kricher.

Plate 12-30. Swallows are graceful, sleek fliers that capture all of their insect food in the air. This Gray-breasted Martin (Progne chalybea) is typical of swallows in flight. Photo by John Kricher.

Plate 12-31. Like other swallows, the Gray-breasted Martin often perches in the open between aerial sorties. This species is widely distributed and not confined to riverine areas, though it is common in such habitats. Photo by John Kricher.

Plate 12-32. The Southern Roughwinged Swallow (Stelgidopteryx ruficollis) is common on most tropical rivers. It builds a tunnel nest in embankments. Photo by John Kricher.

Plate 12-33. The White-winged Swallow (Tachycineta albiventer) is widely distributed and common throughout the riverine areas of Amazonia. Photo by John Kricher.

Plate 12-34. The banana-colored, oversize bill of the Largebilled Tern makes it easy to recognize. Photo by John Kricher.

Plate 12-35. The Yellow-billed Tern in the foreground is markedly smaller than the Large-billed Tern standing behind it on this sandbar. Photo by John Kricher.

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Plate 12-36. Black Skimmers, such as these skimming for dinner, often forage in small flocks. Photo by John Kricher.

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Plate 12-37. The Black-collared Hawk, a dedicated fish eater, is commonly found throughout Amazonia along rivers and in marshes and swamps. Photo by John Kricher.

river travel. From a boat lazily moving downriver you can watch three and occasionally four species of vultures soaring overhead, observe hawks (plate 1228), caracaras, and falcons perched in riverside trees, and see parrots, ranging from frantic flocks of small, screeching parakeets to the larger, more sedate macaws. Kingfishers (discussed in chapter 9) are conspicuous (plate 12-29), and various species of swallows skim above the water pursuing insects.

Swallows Swallows of various species are found on all continents except Antarctica. One familiar species, the Barn Swallow (Hirundo rustica), ranks as one of the most widely distributed bird species on Earth. There are 27 swallow and martin species (family Hirundinidae) in the Neotropics, including some, such as the Barn Swallow and the Purple Martin (chapter 15), that migrate to breed in North America. Many swallow species are partial to rivers and marshes, but others are found in drier habitats. None are forest specialists. Travelers along rivers are apt to see the swallows and martin illustrated in plates 12-30–33.

Two Terns and a Skimmer Two species of terns are commonly seen along Amazonian rivers. One is the large (39 cm/15 in), unmistakable, and aptly named Large-billed Tern (Phaetusa simplex; plate 12-34). Its bill appears to be disproportionally large, an adaptation to its diet of various-size fish. Like all terns it dives to capture its piscine prey. The much smaller (24 cm/9.5 in) Yellowbilled Tern (Sternula superciliaris; plate 12-35) shares

Plate 12-38. This Black-collared Hawk is swooping toward the river, talons ready, to grab an unsuspecting fish. Photo by John Kricher.

the same broad range as the Large-billed, and both species are found throughout the rivers of South America. The Black Skimmer (Rynchops niger; plate 12-36), familiar to many birders in North America, is also common throughout Amazonia. This large (46 cm/18 in) species feeds both day and night by dropping its long lower mandible into the water, “skimming” the surface as it flies. When its lower mandible feels a prey item, such as a small fish, its upper mandible snaps shut, and it has its food.

A Fish-eating Hawk (Not an Osprey) Perched conspicuously in a riverside tree is a big rufous-colored hawk with a pale head. Binoculars show clearly that it has a black band, or collar, across the front of its throat and neck. Meet the Blackcollared Hawk (Busarellus nigricollis; plate 12-37). The hawk is searching for fish. Like the widespread Osprey

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Some Other Birds of Riverbanks, Sandbars, and Marshes You will likely see a wide variety of bird species on any Neotropical wetland tour. A sampling of some of the most iconic representatives of this remarkable assemblage is presented in plates 12-39–44. Plate 12-39. The Greater Ani (Crotophaga major), a member of the cuckoo family (chapter 15), is the largest of the anis (45 cm/18 in) and the most specialized. It is never far from riverbanks or marshes. Photo by John Kricher.

Plate 12-39.

Plate 12-40.

Plate 12-40. The Muscovy Duck (Cairina moschata) is found throughout Amazonia and much of Central America. It is a large duck (85 cm/33.5 in) of wooded riverine areas, often seen flying along the river with its large white wing patches evident, and is normally wary. The species has been widely domesticated throughout the tropics and beyond. Photo by John Kricher. Plate 12-41. Common along virtually all Neotropical rivers and ranging into Texas, the Neotropic Cormorant (Phalacrocorax brasilianus) is easy to recognize. It swims like a duck and dives like a loon to capture fish. Photo by John Kricher.

Plate 12-41.

Plate 12-42.

Plate 12-42. No, it isn’t a funky chicken. This is a Gray-necked Wood-Rail (Aramides cajaneus). The species may be found in wet, swampy wooded areas, but it is also common along riverbanks. It is widely distributed throughout the Neotropics. Photo by Jill Lapato. Plate 12-43. The unmistakable Pied Lapwing (Vanellus [Hoploxypterus] cayanus) is partial to beaches and riverbanks and is widespread throughout Amazonia. Photo by John Kricher.

Plate 12-43.

Plate 12-44.

Plate 12-44. The cardinal-size Blackcapped Donacobius (Donacobius atricapilla) is a taxonomic enigma, now placed in its own family, the Donacobiidae. Once believed to be related to mockingbirds and/or wrens, it is kin to neither. The bird is common and often conspicuous in marshy areas and river edges in much of Amazonia, extending north to southern Panama. Photo by Bruce Hallett.

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Herons and Ibises River edges and marshes support a diversity of wading birds of the families Ardeidae (herons and egrets) and Threskiornithidae (ibises). Plates 12-45–51 represent a few, but by no means all. Two other, more unusual herons are discussed in the sections that follow. Plate 12-45. The Cocoi Heron (Ardea cocoi), seen here flying over a lake, is a large wader common throughout the Neotropics. It is similar to the Great Blue Heron (Ardea herodias), which is widespread in North America but also a resident of the Neotropics. Photo by John Kricher.

Plate 12-45.

Plate 12-46.

Plate 12-46. The elegant Whistling Heron (Syrigma sibilatrix) has a disjunct range, occurring in northeastern South America and more extensively in central and southeastern South America. Photo by John Kricher. Plate 12-47. The Capped Heron (Pilherodius pileatus) is partial to quiet pools. It is widespread from Panama through Amazonia. Photo by Andrew Whittaker.

Plate 12-48.

Plate 12-49. Three species of tigerherons occur in the Neotropics, and each is found in marshes and along shaded riverine areas. This is the Rufescent Tiger-Heron (Tigrisoma lineatum). Photo by John Kricher.

Plate 12-47.

Plate 12-50.

Plate 12-49.

Plate 12-48. Once thought to be extremely rare, the small Zigzag Heron (Zebrilus undulatus) is a skulker and rarely observed. But it is not nearly as rare as it was once thought to be. Photo by Edison Buenaño.

Plate 12-51.

Plate 12-50. The Green Ibis (Mesembrinibis cayennensis), unlike many ibis species, is solitary, not found in flocks. It probes for food along riverbanks and swamps. Photo by John Kricher. Plate 12-51. The handsome Buffnecked Ibis (Theristicus caudatus), though it is certainly common around lakes, ponds, and rivers, is often found away from rivers in open fields. Photo by John Kricher.

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(Pandion haliaetus), which winters in Amazonia and is a permanent resident throughout much of Central America and the Caribbean, the Black-collared Hawk plunges feet-first into Amazonian rivers to capture its scaly prey. The Black-collared Hawk, like the Osprey, has talons with rough scaling, adapted to holding slippery fish. Watching it swoop down and capture a fish is a memorable experience (plate 12-38).

The Odd Boat-billed Heron The Boat-billed Heron (Cochlearius cochlearius) is an inhabitant of mangrove swamps and riverbanks, named for its extraordinarily wide, flattened bill (plates 12-52– 53). Colonies of Boat-billed Herons leave their roosts at night to feed individually along rivers and marshes. The function of this heron’s seemingly oversize bill remains largely unknown, though the bill is likely to be touch-sensitive (many bird bills are highly touch sensitive), aiding the bird in searching for frogs, fish, crustaceans, and various creatures inhabiting mud.

heron and a long neck to match, it commands a significant striking distance as it captures fish with a quick jab of its beak. Surprisingly little is known about the Agami Heron because it has been so difficult to observe. With more ecotourism and a plethora of talented guides it has, like the Zigzag Heron (plate 12-48), become easier to find in recent years. I was once on a trip to the Venezuelan Llanos (chapter 14) with an outstanding guide who found an Agami Heron virtually next to a Zigzag Heron. Wow. We happily clambered under some riverside trees to observe the stunning combination. The Agami Heron is widely distributed from Belize through most of Amazonia. Yet so little is known about this solitary species that it was only in 2015 that detailed photographs documented its rather elaborate courtship behavior.

Hoatzin: Bizarre Bird of the Riverbanks

Methodically skulking along banks of quiet streams and rivers as well as wooded swamps and mangroves, the Agami Heron (Agamia agami; plate 12-54) is a prized sighting for any birder or ecotourist. A bird of deep shade, typically hidden from easy viewing, it is hard to see. With the longest bill of any Neotropical

Unique among bird species, the Hoatzin (Opisthocomus hoazin; plate 12-55) is found along slow meandering streams and oxbows within the Amazon and Orinoco Basins. Hoatzins resemble chickens in size and shape and were once thought to be related to them. Their overall appearance suggests a primitive, almost prehistoric, bird. A Hoatzin is somewhat gangly, its body chunky, its neck slender, its head small. The face is not fully feathered but rather consists of bright blue bare skin surrounding brilliant red eyes. A conspicuous, ragged crest of feathers adorns the bird’s

Plate 12-52. This is a Boat-billed Heron. Unique is a good word for it. Photo by Andrew Whittaker.

Plate 12-53. Face to face with a Boat-billed Heron. Photo by Gina Nichol.

The Shade-loving Agami Heron

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Plate 12-54. The Agami Heron in a typical posture as it quietly stalks fish to capture. Photo by Kevin Zimmer.

Plate 12-55. The ever-so-odd Hoatzin. Photo by Gina Nichol.

head. Its plumage is a combination of soft browns, with rich buff on breast and wings. Hoatzins are weak fliers, a feature that contributes to their primitive appearance. They live in noisy groups that occupy dense riverine vegetation. Their nonmusical, guttural vocalizations add to the auditory experience at Neotropical oxbow lakes. Though originally considered taxonomically related to chickens, Hoatzins have proven difficult to classify. For a while they were linked with the cuckoos, but the most recent genetic analyses suggest that Hoatzins are related more closely to cranes and shorebirds. The species is placed in its own family, Opisthocomidae, and order, Opisthocomiformes. It has an unusual diet, unusual breeding system, and unusual juvenile behavior. Hoatzins are among the few avian folivores, feeding mostly on leaves (over 80% of the diet), often from plants that are typically loaded with secondary compounds, such as plants of the arum family, including philodendrons. (Recall the discussion of folivory in chapter 11.) Leaves are bitten off, swallowed, and ground into a large bolus in the bird’s oversize crop (the anterior of the digestive tract). With the aid of a diverse and abundant microflora housed within the expanded crop and esophagus, the bolus slowly ferments and is digested. The birds benefit not only from some of the digestive products of their microflora, but the bacteria, which are as concentrated in Hoatzins as they are in bovines, also help detoxify secondary compounds. The odd amalgamation of partially decomposed leaves gives the bird an unpleasant odor (rather like cow manure), a beneficial characteristic, since it renders

the flesh distasteful to human hunters. Though a few other bird species are known to eat leaves, Hoatzins represent the only known case of a bird species that exhibits foregut fermentation, a unique adaptation resulting from coevolution with microorganisms that enables the birds to survive on a diet of normally indigestible leaves from numerous plant species. Hoatzins are communal breeders, and between two and seven birds cooperate in a single nesting. Nonbreeding birds called helpers typically assist the pair responsible for the eggs. Nests with helpers are considerably more successful at fledging young than nests lacking helpers. The helpers aid in incubation and feeding young, enabling the juvenile birds to grow more quickly and thus reduce their vulnerability to predators. The streamside nest is a cluster of thin sticks so loosely constructed that the eggs are usually visible from beneath. Juvenile Hoatzins bear a superficial resemblance to Archaeopteryx, one of the first birds, whose fossilized remains established that birds evolved approximately 150 million years ago during the Mesozoic era, when dinosaurs flourished. Young Hoatzins possess claws on their first and second digits that enable them to climb about in riverside vegetation. Should they be faced with danger, they escape by dropping from the vegetation into the water; they swim and dive efficiently. When danger passes they use their wing claws to help in climbing back onto the vegetation. Wing claws were also present on Archaeopteryx, though no one suggests that the resemblance between the modern Hoatzin and the first bird is other than coincidental. Young Hoatzins lose their wing claws as they become adults.

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The Sunbittern Stalking along quiet riverbanks on bright red legs, the Sunbittern (Eurypyga helias; plate 12-56) hunts fish, amphibians, crustaceans, and insects, which it captures by striking quickly, using its long neck and spear-like bill. With a sharply defined white line above and below the eye, and complexly patterned plumage, the Sunbittern blends well in the sun-flecked forest interior. When displaying, it spreads its wings, revealing bright chestnut, yellow, black, and white “sunbursts” that give the bird its name (plate 12-57). Like the Hoatzin, the Sunbittern is the only species in its family, Eurypygidae, and its order, Eurypygiformes. Its low whistled call is commonly heard at dawn and dusk along stream edges.

The Sungrebe Swimming inconspicuously beneath shaded roots along quiet, slow-moving streams, the Sungrebe (Heliornis fulica; plate 12-58) goes about its business of seeking food. Its diet comprises mostly insects, fish, and various crustaceans. It is a challenge to spot a Sungrebe, as it is usually solitary and unobtrusive and often stays in deep shade. Like the Sunbittern, the Sungrebe is found throughout appropriate riverine habitats in Central America and all of Amazonia. It is the single Neotropical species of the finfoot family (Heliornithidae), comprised of three species; one species occurs in much of Africa and the third is found in tropical Asia.

Plate 12-56. The elegant Sunbittern is easily overlooked as it skulks along shaded edges of quiet streams and slow rivers. Photo by James Adams.

Screamers

Plate 12-57. Sunbittern displaying its remarkable wing patterning. Photo by Gina Nichol.

Three species of screamers (family Anhimidae, order Anseriformes) are found along slow rivers, swamps, and marshes throughout South America. Screamers are most closely related to ducks and geese. The name screamer comes from their characteristic loud, piercing calls. Screamers, though bulky birds, are excellent fliers and frequently perch in riverside trees. They are unique in their possession of a layer of air between their skin and muscle, and the buoyancy provided by this “inner tube” may aid them in soaring. Look closely at the vultures overhead. There may be a screamer or two soaring among them. The Horned Screamer (Anhima cornuta; plate 12-59) occurs throughout northeastern South America and is common in the Venezuelan Llanos and throughout

Plate 12-58. Sungrebe male. Females look similar but have a buffy rather than white cheek patch. Photo by John Kricher.

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much of Amazonia. Nearly the size of a turkey (which it vaguely resembles), it is a shiny black bird with thick legs, large unwebbed feet, and a smallish chickenlike head. The Horned Screamer is named for the long feather quill that tops off its head. The Southern Screamer (Chauna torquata; plate 12-60) has a gray head with a small, dapper crest and has a somewhat more confined range than the Horned Screamer. The Northern Screamer (C. chavaria) has the most limited range, confined to northernmost South America.

The Long-toed Jacanas

Plate 12-59. A pair of Horned Screamers. The one on the right shows its “horn” well. Photo by Sean Williams.

Eight species of jacanas (family Jacanidae, order Charadriiformes) use their elongate, unwebbed toes to delicately walk atop lily pads while searching for arthropod food throughout the world’s tropical marshlands and riversides. Two species, the Northern Jacana (Jacana spinosa) and the Wattled Jacana (J. jacana; plate 12-61), are Neotropical. Both are chickensize, blackish birds with dark rufous wings that reveal bright yellow patches when the birds fly. The Northern Jacana is one of the few birds of which only males incubate the eggs and any female will mate with several males. The role reversal is complete in that females establish territories and court males.

Plate 12-60. A Southern Screamer perched, as screamers often are, atop a tree along a river. Photo by John Kricher.

Plate 12-61. Note the long toes on the lifted right foot of this Wattled Jacana. Photo by John Kricher.

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Plate 12-62. The characins, a group to which this fish belongs, are among the most species-rich fish groups of Amazonia. Photo by John Kricher.

Plate 12-63. Not a particularly large specimen, this 1 m (39 in) long Arapaima is readily visible in clear water. Photo by John Kricher.

Amazonian Fish Diversity

sometimes increase to such abundance that their collective predatory habits may act to deplete some local fish species. Along parts of the Brazilian Amazon, a plant known locally as Timbo (Lonchocarpus utilis) is used to reduce numbers of piranha and piranha eggs. The plant contains rotenone, a toxin often used throughout Amazonia by indigenous people to temporarily paralyze fish and thus make them easy to catch. The rotenone, at the concentration used, is lethal to piranha and their eggs but does little if any harm to other fish. Electric Eels (Electrophorus electris) attain lengths of up to 1.8 m (6 ft). With their uniquely specialized skeletal muscles, they are capable of emitting a jolt of 650 volts. To make matters worse, they are fairly common in Amazon waters. They are generally considered to be far more dangerous than piranhas, as accidental contact with an Electric Eel can lead to a debilitating shock. The huge Arapaima, also called Pirarucu (Arapaima arapaima; plate 12-63), is an important protein source for people who live along the Amazon, and in many areas it is in decline from overfishing. It reaches weights of 150 kg (about 335 lb) and lengths of up to 3 m (9.8 ft), but such colossal sizes are now rarely seen, due to intense fishing pressure from people. The Arapaima is in a group called the bony-tongue fishes. It occurs in quiet lakes throughout Amazonia, where it preys on many other fish species. A relative of the Arapaima, the smaller Arowana (Osteoglossum bicirrhosum), is one of many Amazonian fish species that commonly show up in the tanks of aquarium fanciers, but it is also an important food fish for Amazonian people.

There are more than 2,400 species of fish known to inhabit the waters of the Amazon and its tributaries, and additional species may remain yet to be formally described. Approximately 40% of the species thus far described are members of two groups, the characins (plate 12-62) and the catfish. These multitudes include many favorites of the aquarist such as the Neon Tetra (Paracheirodon innesi), Cardinal Tetra (P. axelrodi), Pearl Headstander (Chilodus punctatus), Silver Hatchetfish (Gasteropelecus levis), Oscar (Astronotus ocellatus), and various species of catfish such as the many Corydoras species. Many Amazonian fish species are small. It has been hypothesized that small size evolved in response to a diet of tiny arthropods obtained during the flood cycle from within the flooded forest. Thus, when the tiny Neon Tetras gather at the surface to grab up miniscule morsels of tropical fish food, they may be exhibiting a behavior originally evolved as they massed around flooded forest trees, gathering up the displaced insects and spiders. The Amazon Basin is home for the infamous Red Piranha (Pygocentrus nattereri; plate 10-25) and its relatives, a group of fish whose reputation for collective ferocity is rarely merited. Though widespread and abundant, piranhas, which reach 35 cm (approx. 14 in) in length, are potentially dangerous only when water levels are low and food supply is poor, concentrating the already hungry predatory fish and putting any potential protein source at risk of attack. Piranha do

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Among the more unusual piscine species is the South American Lungfish (Lepidosiren paradoxa). This eel-like fish with large scales and thin ribbonlike fins can gulp air in the manner of its ancestors that swam in stagnant lakes 350 million years ago. There are two other lungfish species, one in Africa and one in Australia. The curious distribution of these three species of ancient freshwater fish on three widely separated continents is almost surely the result of plate tectonics and the breakup of Gondwana. Catfish (plate 10-26) are abundant and diverse in the Amazon and its tributaries. Some get to be very large, but not all. Vandellia cirrhosa, one member of a group of bizarre catfish collectively called candirus, is potentially irksome. Slimmer than a pencil, this tiny fish is normally a parasite of other fish, attaching to gills. However, it allegedly has the disconcerting habit of (presumably) mistakenly swimming into the human urethral, vaginal, or anal opening, whereupon it lodges itself with an array of sharp fin spines. Though candirus are widely reputed to have this unfortunate mistaken sense of direction, I have been unable to locate any evidence other than anecdotal accounts of attempted or actual invasion. Nonetheless, candirus do have the potential to be truly dangerous, to say nothing of painful, and it is worth being aware in areas where these fish are known to occur.

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Plate 12-64. The leaves of this Red Mangrove (Rhizophora mangle) are thick and waxy, resistant to salt spray and water loss. Note the seedling that will drop from the branch and float, perhaps reaching a sandbar to colonize. Photo by Dennis Paulson.

Coastal Mangroves: Saltwater Forests that Protect Coast and Enrich Seas Mangrove forest, sometimes termed mangal, lines tropical coasts, lagoons, and offshore islands throughout the global tropics. The term mangrove is not taxonomic but rather refers to a series of characteristics that mangrove trees have in common. In other words, the designation mangrove is based on physiological adaptations, most specifically the collective ability of mangrove trees to tolerate immersion in salty water (plates 12-64–65). Mangroves are not diverse and thus tend to form pure stands or stands of low species richness. They often have aerial roots of some sort. Many mangroves, though distinct from their nearest terrestrial relatives at the species level, have fairly close relatives on terra firme. Mangrove forests form essential habitat for many kinds of marine animals. Frigatebirds (Fregata spp.; see

Plate 12-65. The prop roots of this Red Mangrove cluster help protect inland vegetation and thus act to stabilize coastal ecosystems, buffering them from hurricanes and other coastal storms. Photo by Dennis Paulson.

plates 12-68–69) as well as many other species of birds commonly nest among mangroves. Migrant birds use mangroves as valuable wintering areas, because mangrove forests are rich in arthropod food. Perhaps most important, mangroves capture a great deal of energy that supports a rich marine ecosystem and contributes to the health of offshore marine ecosystems such as coral reefs. Mangrove leaves that drop decompose slowly, and numerous invertebrates and microbial organisms use them as a food source. As microbial communities cover the decomposing mangrove leaf, the carbon-

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to-nitrogen ratio declines, because more nitrogen is added by the decomposer community. Small fish and invertebrates feed on the leaf fragments, now rich in both carbon and nitrogen. Thus the energy captured by the mangrove leaf is slowly released in little pulses, supporting a diverse animal and microbial community. Mangroves are “nurseries” for many fish and invertebrate species that will later enter the coral reef or pelagic food web. In many areas of the tropics, mangrove forests are being removed, and the essential function of coastal mangrove forests in supporting marine diversity is being destroyed. Mangrove forests are being replaced by such operations as shrimp aquaculture, a change that eliminates the energy pulses that mangroves otherwise supply. Mangroves are woody plants tolerant of high internal concentrations of salt. These plants respond to the physiological challenges of high temperature and concentrated salt exposure with a variety of adaptations. For example, some have salt glands on their leaves that effectively remove excess sodium and chloride. Others accumulate salt in special areas in their leaves, and still others filter salt from the root system. Mangroves are also tolerant of soils low in oxygen. The thick, odorous, muddy substrate that anchors them is virtually anaerobic, or devoid of any gaseous oxygen. But some mangroves have roots that extend above the soil, modified to obtain oxygen from air. Mangrove leaves are similar to leaves of many rain forest tree species in that they are simple, unlobed, and very thick, with a heavy waxy cuticle—characteristics that aid in the storing of water and prevention of excess water loss through transpiration. The plants’ major control of gas exchange, as in leaves of all land plants, is through stomatal openings on the leaves. About 34 mangrove species occur globally in tropics and subtropics. Southeast Asia has the greatest diversity of mangrove species, whereas the Neotropics have the least, with only eight species, some of which are relatively uncommon. Some mangroves are adapted to colonize shallow sand flats, trapping sediment and gradually building a dense, muddy, organic soil. As mangroves are far more salt tolerant than other tree species, they tend to line tropical coasts, and their abundance extends inland along tidal rivers. Though subject to disturbance (especially from hurricanes and monsoons), they typically rebound, though recovery is often protracted. Mangroves range in form from short

Plate 12-66. Red Mangrove propagules attach to sediment, and the plant begins to grow quickly, forming prop roots. Photo by John Kricher.

and shrub-like to trees from 10 to 20 m (approx. 33–66 ft) in height, occasionally taller.

Types of Mangroves Red Mangrove (Rhizophora mangle; plates 12-64–66) is an abundant species that can grow as a bushy shrub, a stunted tree, or a full 20 m (66 ft) tall tree. It has reddish bark and numerous aerial prop roots, some of which are firmly anchored to the substrate and some of which grow downward toward it. Prop roots provide a firm anchor for the plant. The broadly spreading roots help assure stability against winds, tides, and shifting sands. Prop roots contain openings, called lenticels, important in transporting air to the oxygenstarved deep roots. Leaves are oval and thick, dark green above, yellowish below. Flowers are pale yellow with four petals. Fruits are reddish brown and produce elongate green seeds that actually germinate while still attached to the parent plant. Seedlings resemble green pods and are about the length of a pencil. They drop from the plant and initially float horizontally in the sea, becoming flotsam in the tropical ocean. Seedlings eventually absorb sufficient water that they reorient vertically. Should the tide carry the vertically floating seedling to a shallow area, once it touches substrate it will anchor and begin to put out roots. Dispersal is effective, and Red Mangrove has populated coasts of all tropical seas around the world. Black Mangrove (Avicennia germinans) is abundant throughout the Neotropics, often forming pure stands in anoxic substrate. Black Mangroves tend to grow in

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less exposed areas than Reds, but are able to thrive in oxygen-starved sediment. They are bushy-topped trees that can reach heights of up to 20 m (66 ft). Leaves are oval, leathery, and downy white underneath. The flower is yellow and tubular, the fruit green and ovate. Seedlings float and, like adult trees, are tolerant of low oxygen levels. The most notable feature of Black Mangrove is its root system. Shallow horizontal roots anchor it in thick, smelly, anaerobic mud, but these roots send up vertical aboveground shoots, called pneumatophores. Lenticels on the pneumatophores feed into wide air passages connecting with the underground roots, providing a means for air transport to the oxygen-starved root system. Two other common mangrove species are White Mangrove (Laguncularia racemosa) and Buttonwood

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(Conocarpus erectus). White Mangrove is less tolerant of prolonged immersion in the sea and tends to grow at slightly higher elevations than Red and Black Mangroves. White Mangrove has scaly reddish-brown bark and greenish-white flowers that turn into small (less than 2.5 cm/1 in) reddish-brown fruits with longitudinal ridges. It grows from about 9 to 18 m (approx. 30–60 ft) tall. Buttonwood resembles White Mangrove but occurs only well away from daily flooding by salt water. It is the least salt tolerant of any of the four common mangroves and was once not considered to be a mangrove. As salinity declines, such as at higher elevations or with distance from the coast, pure stands of Red or Black Mangroves give way to mixed stands of several species, not all of which are mangroves. The transition from mangal community to upland community is generally gradual.

Plate 12-67. The interior of a mangrove swamp is dense with roots that stabilize sediment and help expand the forest. Photo by John Kricher.

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How a Mangrove Cay Develops A careful look at the pattern of coastal mangrove species distribution in a mangrove cay suggests zonation among the various species. Red Mangroves line the outermost edges of a cay, and in the sea just beyond the cay pioneer Red Mangrove saplings grow. Black Mangroves lie inland of the Reds, and innermost are White Mangroves and an occasional Buttonwood. This zonation pattern was once thought to correlate with the tolerance each species has for saltwater immersion, but in fact Black Mangrove is the most salt tolerant, so the pattern is not a simple case of response to salt exposure. The cay appears to be expanding outward. Red Mangroves continuously colonize the outermost edges of the cay, but as sediment builds and the cay rises, Black Mangroves in turn expand their range outward, mixing with the Reds. Whites and Buttonwoods likewise expand their ranges as the sediment builds higher ground, as these species are most sensitive to immersion in salt water. Such a pattern has also been described for mainland coastal mangrove communities: Reds are outermost, Blacks intermediate, Whites and Buttonwoods innermost. Mangrove cay ecology is a topic of debate. Some ecologists dispute the idea that mangroves are sharply zoned and represent a successional sequence of the sort just described. Further, there is doubt about how routinely mangroves build up cays by trapping sediment (plate 12-67). Geological evidence suggests that mangrove cays originate from coral deposition, not sediment accumulation by colonizing mangroves. Not all mangrove areas seem to accumulate sediment, and changing conditions caused by storms and tides certainly influence the pattern of mangrove distribution. Some mangrove cays have remained stable for many years, without significantly expanding or contracting. Disturbance history has a strong influence on zonation patterns. Mangrove and coral reef ecosystems bear the brunt of tropical hurricanes and monsoons (plates 12-68– 69). But these ecosystems rebound. It is clear that coral reefs and mangrove forests provide a strong degree of protection from coastal erosion and damage from major storms. In addition, mangroves, by their high productivity, act as key species in nutrient flux in coastal tropical ecosystems. Mangrove forests are deserving of protection throughout their range, as they are essential assets.

Plate 12-68. This is Bird Caye off Dangriga, Belize, in 1978, some 17 years after Hurricane Hattie, which had a major impact on coastal Belize. Mangrove forests help buffer the coast and inland areas from the ravages of hurricanes. The birds are Magnificent Frigatebirds (Fregata magnificens), attempting to nest on the decimated cay. Photo by John Kricher.

Plate 12-69. This male frigatebird has its throat pouch fully expanded, an attempt to attract a female. Photo by John Kricher.

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The Coconut Palm Perhaps the most iconic of coastal tropical plants is the Coconut Palm (Cocos nucifera; plate 12-70). Some of these trees attain heights of nearly 30 m (98 ft), though most are smaller. Coconut seeds float and easily colonize tropical areas around the world, and most authorities believe Coconut Palms are not native to the New World but colonized the region from the tropical Pacific. As is well known, the “meat” from the nuts is very tasty.

Plate 12-70. Coconut Palms add considerable ambience to tropical sunsets throughout the coastal Torrid Zone. Photo by John Kricher.

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Plate 13-1. The Andes Mountains, viewed from Tierra del Fuego, at the southern tip of South America. Photo by John Kricher.

Plate 13-2. Mosses and various other plants characterize higher elevations in the Andes, where snow is common. Photo by John Kricher.

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Scaling the Andes

Montane (Mountain) Forests When visiting the Neotropics make sure you include a segment in the magnificent Andes Mountains. Don’t just settle for lowland rain forest. Do some climbing. The ecology is different up in the mountains, and the views are great. The Andes mountain chain extends from Trinidad and Venezuela all the way down the western part of the continent of South America to Tierra del Fuego (plate 13-1; fig. 13-1). The mountains in Central America, as well as those of islands such as Puerto Rico, are not as tall as the Andes but are nonetheless rich with cloud forests, and there is much to be seen in them.

Elevational Changes: An Overview

Plate 13-3. Alexander von Humboldt was the first to carefully document how elevational change in the Andes Mountains alters plant community structure; we call this the life-zone concept. Photo by John Kricher.

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With increasing elevation up an Andean mountainside, temperature decreases and condensation and Caribbean Sea Venezuela precipitation both increase, conditions supporting NORTH Guyana AMERICA Atlantic cooler and humid forests rich with trees often densely s Suriname Pacific no a Ocean l L Gu laden with epiphytes. Temperature gradientsOcean can French Hig iana Colombia Guiana be steep, and it is often surprisingly cool at higher hla (France) Ecuador nd s elevations. In the upper montane forests, trees are Galápagos Islands gnarled and small in stature, forming a kind of elfin n (Ecuador) azo forest. In high-elevation Andean zones, conditions Am asin Brazil B become colder and increasingly windy, too severe Brazilian for trees to survive, so only grass and shrubs prevail.SOUTH Shield Depending upon conditions, these alpine grassy and AMERICA Peru shrubby areas are called either páramo or puna (both Bolivia Atacama Paraguay discussed below). Snow is typical at high elevations, Desert even in equatorial regions (plate 13-2). Conditions above tree line are frequently foggy and bog-like, with Chile extensive areas of soft peat and mossy groundcover. As airborne moisture from the lowland tropical forest 600 miles Pacific meets the Andes it rises and cools, and mid-elevation 600 kilometers Ocean Uruguay montane forest becomes enshrouded in dense mist Argentina and fog—a cloud forest—for at least part of each day. Clear morning skies yield to afternoon fog that persists Falkland through nightfall. Cloud forests look and feel overcast Islands (UK) and damp, because you are literally walking in a cloud Atlantic Strait of Magellan Scotia Ocean when you traverse such areas. Cape Sea Tierra del Fuego Horn Alexander von Humboldt, who explored the Neotropics from 1799 to 1804, first described the Figure 13–1. General map showing the extensive range of the ecological zonation that is evident along tropical Andes Mountains. Reprinted with permission from Kricher, elevation gradients (plate 13-3). He documented how John. Tropical Ecology. Princeton, NJ: Princeton University lowland moist forests grade into cloud (or fog) forests, Press, 2011. Pa

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which, if elevation is sufficiently high, transition to elfin forests, páramo, or puna, depending on elevation and exposure. The changes observed by Humboldt and his associate, A. G. Bonpland, form the backbone of what became the concept of plant associations or ecological life zones. Humboldt clearly understood how changes in physical conditions resulted in changes in ecosystem characteristics.

Cloud Forests Tropical cloud forests vary from one site to another, but all share general characteristics. Here is a checklist of what to look for as you ascend into these unique ecosystems. • Various species inhabit distinct elevation zones. Species richness typically diminishes with elevation, because conditions become harsher, but groups such a ferns and orchids may exhibit higher diversities than in lowland rain forests. • Moisture-seeking plants such as mosses and ferns form abundant components of the vegetation community. Tree ferns are particularly distinctive of cloud forests. • Most species of plants and animals found in cloud forests have strong taxonomic affinities with species found in low-elevation rain forests, and some groups, such as tanagers and hummingbirds, are better represented in the mountains than in the lowlands (plate 13-4). • The stature of trees diminishes at high elevation, sometimes resulting in dwarf trees. At Monteverde Cloud Forest in Costa Rica, a place visited by many ecotourists, canopy height varies from 20 to 40 m (66–131 ft) in sheltered sites but decreases to 5–10 m (16.5–33 ft), forming elfin forest, on exposed sites such as ridges and peaks. • Sunlight is reduced due to the presence of fog, a characteristic that also acts to reduce plant productivity. • Precipitation is usually high. At Monteverde Cloud Forest annual rainfall is between 250 and 350 cm (98–138 in), and dry season is characterized by mist and cloud cover much of the day. Expect to get wet. Certain other montane forests in parts of Central America and those in the Chocó (along the western coast of Colombia and Ecuador) experience higher precipitation. Precipitation and mist keep these forests moist, even during dry season.

Plate 13-4. The widespread Bay-headed Tanager (Tangara gyrola) frequents low- to mid-elevation cloud forests and is often one of several tanager species traveling in mixedspecies foraging flocks. Photo by Jill Lapato.

• The saturated air inhibits evapotranspiration, making it more difficult for plants to obtain mineral nutrients from soil, a factor that also limits plant productivity. In other words, if the air is cool and highly saturated with water, the physical conditions necessary for effective uptake of water by plants are limited. • In addition to rainfall, precipitation occurs as fogdrip, wherein water from fog condenses on leaf and bark surfaces and drips on to the forest floor, saturating the soil. At Monteverde Cloud Forest 22% of the annual hydrologic input is due to wind-driven water from fog. • Soil tends to become water-saturated and acidic, creating bog-like conditions in some areas, where decomposition is slowed by the high soil acidity. When you walk in high-elevation areas the plant cover and litter layer will feel spongy beneath your feet.

Neotropical Montane Forest Distribution Cloud forests are the dominant kind of ecosystem along a narrow altitudinal belt, from 1,400 to 3,500 m (4,590–11,480 ft) along the eastern slope of the Andes. Cloud forests occur in Venezuela, Colombia, Ecuador, Peru, and Bolivia, and also in parts of southeastern Brazil. Cloud forests also occur at higher elevations in the Greater and Lesser Antilles, and in parts of Nicaragua, Guatemala, Panama, and Costa Rica in Central America. At Monteverde in Costa Rica, cloud

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forest occurs above 1,500 m (4,920 ft) on the Pacific slope but extends to between 1,300 and 1,400 m (4,265–4,590 ft) along the Atlantic slope.

A Closer Look inside Cloud Forest At Monteverde Cloud Forest in Costa Rica, three seasons are recognized: wet season, from May to October; transition season, from November to January; and dry season, from February to April. Wet season typically has clear morning skies followed by cumulus cloud formation and precipitation in afternoon and early evening (plates 13-5–6). Transition season features strong trade winds from the northeast, stratus and stratocumulus clouds, and wind-driven precipitation and mist throughout much of the day and night. Dry season features moderate trade winds, stratus clouds or clear sky part of the day but also wind-driven mist and cloud water, particularly in the evening hours. Neotropical cloud forests are lush, with high biomass (at low and mid elevations), and obvious abundance of epiphytic orchids, bromeliads, ferns, and mosses densely covering and draping branches and tree trunks. Vines are present but are relatively less well represented than in many lowland forests. Shrubs are often abundant. Trees, which at high and exposed elevations exhibit gnarled trunks and branches, are from 25 to 30 m (82–98 ft) in height, not as tall as in lowland rain forest. Both a tree canopy and understory of small trees are typically evident. Buttressing is common among trees at lower elevations. Bark characteristics are often difficult to discern, as bark is typically covered by epiphytic vegetation. Tree crowns are usually compact and most do not spread, parasollike, as is typical of lowland forest trees. Leaves are small, hard, waxy, and usually thick. In some places there are numerous pine trees. There are many montane palm species, and understory palms are sometimes abundant. Tree ferns (especially Cyathea), true ferns that grow to the size of small trees, are often common, adding an almost prehistoric look to the landscape (plate 13-7). Small ferns, including may epiphytic species, are also often abundant. Bamboos thrive in humid montane forests, and one genus, Chusquea, is often abundant. The cloud forest at Monteverde, Costa Rica, has been intensively studied for many years and is likely the bestknown and most visited cloud forest in the Neotropics. It has excellent trails and good nearby lodging, and skilled guides are readily available.

Plate 13-5. Clouds are beginning to close in on this Ecuadorian cloud forest as afternoon approaches. Photo by John Kricher.

Plate 13-6. This cloud forest in Venezuela contains numerous conifers (foreground). Fog has fully engulfed the forest. Photo by John Kricher.

Plate 13-7. Tree ferns are common in cloud forests. Photo by John Kricher.

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Plate 13-8. Cloud forests, with their continuous atmospheric moisture, host an abundance of epiphytes, as is evident in this image. Photo by John Kricher.

Plate 13-9. The Long-whiskered Owlet (Xenoglaux loweryi) was first described in 1977. It occurs in cloud forests at elevations of between 1,890 and 2,200 m (6,200–7,220 ft), in the Andes Mountains of northern Peru. Photo by Andrew Whittaker.

Plate 13-10. Cloud forests in Colombia and Ecuador are habitat for the Giant Antpitta (Grallaria gigantea). By far the largest member of its family, this species attains lengths of up to 28 cm (11 in). Because of extensive deforestation in many parts of its range, it is considered a vulnerable species by the IUCN (International Union for Conservation of Nature). Photo by Jill Lapato.

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Plate 13-11. This is a male Andean Cock-of-the-rock. These birds really light up a misty cloud forest. Photo by Nancy Norman.

Plate 13-12. The Plate-billed Mountain-Toucan (Andigena laminirostris). Photo by Clayton Taylor.

A total of 3,021 plant species, including 755 tree species, have been identified in the Monteverde forest. The most species-rich component is epiphytes, with 878 species (plate 13-8). More than 450 species of orchids occur. The most abundant families of trees in Monteverde are Lauraceae (laurels), Rubiaceae (the madder family, which includes coffee and Cinchona, the plant from which quinine, used to treat malaria, is extracted), Fabaceae (legumes), Moraceae (figs), and Euphorbiaceae (spurges). At La Selva Biological Station, a lowland rain forest site in Costa Rica, the five most abundant tree families are Fabaceae, Lauraceae, Rubiaceae, Annonaceae (custard apples, pawpaws), and Euphorbiaceae. The overlap between dominant tree families in montane and lowland forest is obvious. High endemism is characteristic of tropical montane cloud forests. The tropical Andes and the Amazon Basin each contain approximately the same number of bird species (791 and 788, respectively) but the Andes have more than twice as many endemic species as the lowland area (318, compared with 152). Some cloud forests are so remote and difficult to reach that new species of birds, all endemics, have been discovered even relatively recently. Intrepid ornithologists have described a new species of cotinga, a wren, two antpittas, and an owl (plate 139), all from northern and central Andean cloud forests. Monteverde Cloud Forest in Costa Rica has five endemic salamanders and 19 endemic frogs and toads (anurans), for a total of 24 endemic amphibian species. Monteverde also has 14 endemic reptiles (four lizards and 10 snakes).

Though most Caribbean islands contain some endemic species, they are often not confined only to cloud forest, thus endemism of birds is less pronounced in Caribbean cloud forests than in those of the Andes. Nonetheless, it is interesting that the Elfin-woods Warbler (Setophaga angelae), an endemic strictly confined to small areas of Puerto Rican cloud forest, was discovered only as recently as 1971.

Birds and a Bear, Oh My The most conspicuous vertebrates of cloud forests are birds. Numerous species, many endemic, are restricted to various elevation zones (plate 13-10). One of the most spectacular Neotropical birds, the Resplendent Quetzal (Pharomachrus mocinno; plate 15-19), nests in Central American cloud forests. Other quetzal species are found in South America. Along with some other cloud forest bird species, quetzals, which are fundamentally fruit eaters, migrate seasonally to lower elevations as fruit abundances change. The Andean Cock-of-the-rock (Rupicola peruvianus; plate 13-11), a large cotinga and close relative of the lowland Guianan Cock-of-the-rock (R. rupicola; chapter 10), nests in rocky ravines near streams at lowand mid-elevation montane forests. Males gather at subcanopy leks at daybreak to court females. Unlike Guianan Cock-of-the-Rocks, Andean males seem to cooperate, in groups of two, to court females, though, within the pair only one, the dominant male, will

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Plate 13-13. The Scarlet-bellied Mountain-Tanager occurs along the Andes at mid elevations from Colombia to Bolivia. Photo by Andrew Whittaker.

Plate 13-14. The Grass-green Tanager is found in wet cloud forests. Photo by Edward Harper.

actually mate. Like the quetzals, Andean Cock-of-therocks are fruit eaters and are often seen gathered in all their collective gaudiness in richly fruiting trees. Among the more elegant Andean cloud forest birds are the four species of mountain-toucans (Andigena spp.; plate 13-12). Mostly blue-gray with yellow rumps and long, variously colored bills, these elegant-looking birds are restricted to the epiphyte-laden trees of cloud forests. Many of the most colorful tanagers (particularly species in the genus Tangara) and bush-tanagers (Chlorospingus) are unique to cloud forests. Mixed flocks of various tanagers and other species may be found as they collectively go about their foraging. These include such gaudy species as the Scarlet-bellied Mountain-Tanager (Anisognathus igniventris; plate 1313) and the Grass-green Tanager (Chlorornis riefferii; plate 13-14). Many of the montane bird species are relatively easy to observe, but not all. One that gives birders fits is the Ocellated Tapaculo (Acropternis orthonyx; plate 13-15). Tapaculos are in the family Rhinocryptidae, a group of 58 species entirely confined to South America. As a group they pose challenges to anyone who wishes to get a good look at them. They sing with gusto but appear with great reluctance. The Ocellated Tapaculo is found generally between 2,300 and 3,500 m (7,550– 11,480 ft) elevation in Colombia, Ecuador, and Peru. It usually requires considerable patience to see it well. Of all of the various birds found in montane areas,

Plate 13-15. The ever shy and reclusive Ocellated Tapaculo. Photo by Andrew Whittaker.

perhaps no family is better represented than the hummingbirds (family Trochilidae; plate 13-16). On a visit to Ecuador, for example, if you are inclined to visit both the eastern and western slopes of the Andes at various elevations, you are quite likely to encounter over 50 hummingbird species. Many lodges have hummingbird feeders that make it easy to obtain wonderful looks at these hyperactive birds. Hummingbirds are remarkable for many reasons and are discussed more in chapters 10 and 15. Hummingbirds feed mostly on nectar and supplement their diet with arthropod food. Body sizes, bill lengths, and bill shapes vary among species, a reflection

Plate 13-16. This stunning Collared (or Gould’s) Inca (Coeligena torquata inca) was photographed as it was approaching a feeder. Photo by Andrew Whittaker.

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of coevolution between hummingbirds and their principal food plants. Numerous hummingbird species have exquisitely adapted to the harsh conditions of montane and highelevation ecosystems. These tiny, hyperactive birds endure cold winds and sweeping rain—and appear to thrive. Many species are found throughout the Andes Mountains and routinely survive the cold nights by entering a state of torpor, lowering body temperature and reducing their heart rate and body metabolism to conserve energy. In the morning they awaken and rapidly regain their normal metabolic rate and go about feeding as the temperature warms. Some, such as the Ecuadorian Hillstar (Oreotrochilus chimborazo), which lives at elevations of 3,600–4,600 m (11,810– 15,090 ft) in the windswept puna (described below) of the Ecuadorian Andes, will roost in holes in rocks, protected from wind. The 13.5 cm (5.3 in) long Sword-billed Hummingbird (Ensifera ensifera; plate 13-17) is remarkable for its extraordinarily long bill, measuring 9–10 cm (3.5–4 in). The uniquely long bill is adapted to obtain nectar from large, elongate tubular flowers, particularly in the genus Datura, though the species also feeds on other flowers with long corollas. Swordbills are uncommon, as their flowers are relatively widely scattered, but they may be seen coming to hummingbird feeders around ecotourism lodges at mid elevations in the central Andes, particularly near Quito, Ecuador. The Giant Hummingbird (Patagona gigas; plate 1318) is well named, being by far the largest member of its huge family. It measures about 23 cm (9 in) in length, and its wingspread is about 21.5 cm (about 8.5 in). Hummingbirds are closely related to swifts, and indeed the Giant Hummingbird is sometimes mistaken for a swift, given its large size. It is the only hummingbird that occasionally glides in flight, rather than constantly beating its wings. But in all respects it is a hummingbird, and a relatively common one along the Andes. It occupies mid to relatively high elevations along both slopes, feeding on a variety of flowers but often relatively focused on flowers of the genus Puya. The helmetcrests of the genus Oxypogon form a group of four species that have adapted their behavior to cope with the cold realities of high-elevation living (plate 1319). They are found among the tall, shrubby Espeletia plants (described later in the chapter) that abound in the high páramo (3,600–4,500 m/11,810–14,760 ft) of Venezuela and Colombia. All are small (11.4 cm/4.5

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Plate 13-17. Sword-billed Hummingbird. Photo by Edison Buenaño.

Plate 13-18. Giant Hummingbird. Photo by Andrew Whittaker.

Plate 13-19. Helmetcrest. Photo by Edison Buenaño.

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in long) hummingbirds and they conserve energy by actually walking on the ground and only briefly flying up to capture an insect or to feed on low flowers. Unlike other hummingbirds, helmetcrests rarely hover at flowers. Instead they perch, methodically plucking insects and obtaining nectar from within Espeletia and other favored nectar plants.

A Bear in the Andes? You Bet! The Spectacled Bear (Tremarctos ornatus; plate 13-20) is named for its facial pattern of beige lines surrounding its eyes and cheeks. Otherwise, the creature is black. It is a medium-size bear, weighing about 200 kg (approx. 440 lb). The only species of bear found in South America, it inhabits low-elevation montane cloud forests from Panama through Peru and Bolivia. The species is considered a relict, as it once ranged from the southern United States (California to the eastern seaboard) and throughout Central America. Like most bear species, it is omnivorous, feeding on a wide variety of vegetation (including hearts of bromeliads) as well as small vertebrates and invertebrates. Mostly solitary, Spectacled Bears have been reduced in population in many areas by hunting, and are among the most difficult large Neotropical mammals to observe in the wild.

Elevational Migrants: Follow the Food The Resplendent Quetzal is one of many bird species to engage in elevational (also called altitudinal) migration. Nesting from January to June in mid-elevation cloud forests, such as Monteverde (1,500–1,800 m/4,920–5,900 ft) in Costa Rica, these quetzals eventually migrate to lower elevations (1,100–1,300 m/3,610–4,265 ft) along the Pacific slope of Costa Rica, where they remain until October. At that time they move back to the nesting areas, where they remain for a few weeks. Then they fly to the Caribbean slope (700–1,100 m/2,300–3,610 ft) until returning upslope to nest. This complex pattern, discovered by attaching small radio transmitters to the birds, describes their general movement, but there is much annual variability, suggesting that the birds are seeking fruiting plant species in the family Lauraceae, their principal food. The migration pattern of the quetzal demonstrates strong ecological connectivity between

high- and low-elevational areas on both slopes. Other frugivorous bird species also have complex elevational migrations. Most hummingbird species at Monteverde move upslope to breed during wet season and migrate to lower elevations during dry season. Insectivorous bird species do not engage in elevational migration, suggesting that the driving force for these migrations is fruit availability, not factors such as seasonal changes in weather. Butterflies are also elevational migrants. At Monteverde, more than half of the 658 butterfly species undergo seasonal elevational migration. Butterflies’ migration patterns vary among families and species, but in general, most migrating butterflies depart lowlands at the end of wet season, moving higher in elevation, into the cloud forest life zones. At one location, Windy Corner (the entrance to Monteverde Cloud Forest Biological Reserve), on December 16, 1994, about 6,000 migrating butterflies were observed over a five-hour period. Other insects, such as certain dragonflies, flies, beetles, bugs, parasitic wasps, and moths, are also known to be elevational migrants. Some bat species, as well as Baird’s Tapir (Tapirus bairdii) and the White-lipped Peccary (Tayassu pecari), are also suspected to be elevational migrants, at least at Monteverde Cloud Forest Reserve. The existence of elevational migration in such diverse groups of animals has strong ecological and conservation significance. Elevational migration is a clear example of ecological linkages among life zones. Many frugivorous birds, for example, are important seed dispersers (chapter 10), and their elevational migratory movements may prove to be an important influence on the distribution of various plant species whose seeds they disperse. Ecological corridors that preserve suitable habitat for elevational migrants permit the movement of animals among various life zones. It is essential to recognize the need to preserve contiguous habitats that form elevational migratory corridors. At Monteverde Cloud Forest, the evidence of elevational migration helped in the creation of the Children’s Eternal Rainforest and the establishment of Arenal Volcano National Park to protect pre-montane rain forest essential to elevational migrants (as well as nonmigrants). Elsewhere in Costa Rica, a contiguous corridor has been established linking high-elevation Braulio Carrillo National Park with lowland La Selva Biological Station, a corridor that represents an elevational range of 2,871 m (9,419 ft). This corridor crosses six ecological life zones

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and transitional zones. In some places the corridor is only 4–6 km (2.5–3.7 mi) wide, rather narrow to assure sufficient usage by migrant species. Areas outside the corridor are heavily used by humans and therefore do not represent suitable habitats for elevational migrants and most other tropical forest species.

Scaling the Andes: High-Elevation Ecology You can’t miss them, especially as you gaze out from a comfortable cruising altitude of perhaps 10,000 m (33,000 ft) aboard a jetliner flying north from Lima, Peru, to Quito, Ecuador. The Andes are the dominant topographic feature throughout all of western South America. The ancient Incan city of Machu Picchu, at an elevation of 2,430 m (7,972 ft), is a World Heritage Site near the city of Cuzco, Peru, visited annually by thousands of tourists (plate 13-21). Approaching Quito, which itself is at an elevation of 2,858 m (9,375 ft), you hope the clouds will lift sufficiently that you can see Cotopaxi, the currently quiescent volcano that looms above the city at an elevation of 5,897 m (19,344 ft), one of many potentially turbulent mountains along the Andes chain. The youthful mountain range stretches from Cape Horn, the southernmost tip of South America, all the way north to the Caribbean Sea, finally terminating in the gentle, densely forested Northern Range on the island of Trinidad. The Andes are the longest continental mountain chain in the world, stretching about 7,000 km (4,300 mi) from end to end. The width ranges from about 200 to 700 km (120 to 430 mi). The Andes Mountains began forming after dinosaurs became extinct and are still growing and changing. Some of the snow-covered peaks are geologically recent. The Andes form an immense chain of granite stretching below your plane as far as you can see in either direction. To the east, over the high peaks, lies the vastness of the Amazon Basin, while to the west is a narrow belt of coastline, much of it Atacama Desert, one of the most arid regions in the world. In between, within the complex peaks and valleys of the mountains, are the high puna, the páramo, and the flat altiplano of the high Andes. The puffy cumulus clouds that sometimes obscure the view of the mountains below owe their existence to the presence of the mountains, which force moisture-laden air over the peaks, causing condensation into clouds (plate 13-22).

Plate 13-20. Spectacled Bear, relaxing. Photo by Andrew Whittaker.

Plate 13-21. Machu Picchu, near Cuzco, Peru, is one of the archaeological wonders of the world, a major city during the Incan Empire. Photo by David Clapp.

Plate 13-22. The Andes Mountains are extensive, complex, and active. The chain has numerous snow-capped peaks, including those here, partly enshrouded in clouds. Photo by John Kricher.

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The Andes Mountains, known in South America as Cordilleras de los Andes, define western and northern South America, running from Tierra del Fuego to Trinidad, the major ridges bending northeast when they reach Colombia and continuing into Venezuela, while one ridge continues northward into Panama. The Andes form a complex series of parallel chains divided by a flat tableland area, called altiplano, normally at about 4,000 m (13,120 ft) elevation. This tableland is the site of several isolated high-elevation lakes, the largest being Lake Titicaca, which sits on the border between Peru and Bolivia. Characteristic of young, geologically active mountains, the Andes are ruggedly tall peaks routinely ranging from 2,000 m (6,560 ft) to 6,000 m (19,680 ft) tall. There are over a dozen peaks in excess of 6,100 m (20,000 ft), the tallest being Mt. Aconcagua in Argentina, at 6,962 m (22,834 ft). You must go trekking in the Himalayas or Pamirs of Asia to find mountains of similar stature (Mt. Everest is about a mile higher than Aconcagua). Where the Andes cross the equator, the snowline begins at elevations between about 4,500 and 5,000 m (14,760–16,400 ft). As you move progressively north or south of the equator, the climate becomes more severe and snowline occurs at increasingly lower elevations. Approaching the southernmost part of the Andes, snowline is at only 1,000 m (3,280 ft).

Geography of the Cordilleras The Andes Mountains extend well beyond the climatic zone of the Neotropics, beginning at the frigid southern tip of South America, at Tierra del Fuego (Land of Fire). This land was once inhabited by the indigenous Yahgan (Yámana) Indians, a people known to Charles Darwin, who encountered them when the Beagle visited the region. The Yahgan inhabited an extremely harsh climate but were apparently physiologically capable of sleeping on snow, exposed to the open environment. Ships rounding Cape Horn face continually strong westerlies, gale-force winds that create among the roughest seas known. It is here that Captain FitzRoy of the hms Beagle discovered the Beagle Channel; as he sailed through the channel, FitzRoy noted a mountain, which he named Mt. Darwin (2,438 m/7,996 ft), after the Beagle’s most distinguished passenger.

The Andes stretch northward, a relatively narrow ridge along the border between Chile and Argentina. Some of the tallest peaks occur east of the Chilean cities of Valparaíso and Santiago, near the mountain city of Mendoza, Argentina, south of the Tropic of Capricorn. Here, in close proximity, one finds Mt. Aconcagua (6,962 m/22,834 ft), Mt. Tupungato (6,802 m/22,310 ft), and Mt. Mercedario (6,772 m/22,211 ft), and the Andes begin to widen into a series of ridges with extensive tracts of altiplano in between. The lower mountain slopes are temperate in climate, not yet tropical, and precipitation varies, depending on elevation, from between 25 and 102 cm (approx. 10–40 in) annually. West of the mountain ridge, in northern Chile near the city of Copaipó, the Atacama Desert begins, an arid coastal region extending northward almost 3,218 km (2,000 mi), finally becoming the Sechura Desert on the border between Peru and Ecuador. Where the countries of Chile, Peru, and Bolivia meet, the topography of the Andes becomes increasingly complex, as the mountain range diversifies into a series of ridges with vast area of intervening highelevation altiplano. It is here that there was once an extensive inland sea, the legacy of which remains as salt flats (Salar de Uyuni and Salar de Coipasa), as well as Lake Titicaca and a few other scattered, small lakes. The main chain of the Andes, the Western Cordillera, continues west of the salt lakes and Lake Titicaca toward Machu Picchu (the great city of the Inca) and Cusco, Peru. East of Titicaca, the Cordillera Real and Cordillera de Carabaya gradually descend on their eastern slopes through zones of humid montane forest, eventually terminating as tropical lowland rain forest in western Bolivia and eastern Peru. Throughout the Andes Mountains, modern descendants of the Inca continue to thrive in the high elevations (plate 13-23). In Ecuador and Colombia, the Andes diverge into three major ridges, the Western, Central, and Eastern Cordilleras. The Western Cordillera extends north to Central America. The Central Cordillera extends roughly 800 km (approx. 500 mi) northeastward through Colombia. The Eastern Cordillera passes through Bogotá toward the northeast, dividing into two ridges, the Cordillera de Perijá and the Cordillera de Mérida. The former continues northeastward in Colombia and terminates on the Guajira Peninsula bordering the Caribbean Sea, while the latter bends further northeast, passing into Venezuela, terminating

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finally in the Northern Range in Trinidad (an island today but once part of Venezuela; it became isolated only when the sea level rose after the melting of the glaciers several thousand years ago). The complex topography of the Andes exerts strong effects on the distribution and evolution of plants and animals. The immensity of the overall range coupled with the divisions of ridges and intervening altiplano, plus the elevational differences along the mountain slopes, have provided ideal conditions for evolutionary divergence among many taxa. The fact that countries such as Colombia, Ecuador, and Peru have so many species is due in no small measure to the vicariance potential (chapter 8) constantly present because of the Andes.

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Plate 13-23. Modern descendants of the Inca celebrating traditions linked to the once great Incan Empire. Photo by David Clapp.

Elfin Forests Trees and shrubs at high elevations (exact elevation varies with latitude) are noticeably shorter in stature, often very gnarled, and more heavily laden with epiphytes, especially mosses, lichens, and bromeliads, than those at lower elevations. Tree line, the elevation above which trees no longer grow (also called timberline), varies depending upon the location of the mountain relative to other mountains. Tree line is typically higher on mountains in close proximity with other mountains, whereas tree line is lower (meaning the climate is more severe) on isolated mountains. The explanation for such distribution is the climatic influence of the mountains themselves. Mountains in close proximity moderate the influence of wind and retain heat better than isolated, more exposed mountains. This pattern is called the Massenerhebung effect. At higher elevations, you will find elfin forests of twisted and stunted trees barely 3 m (9.8 ft) tall. An abundance of lichens, green algae, and bryophytes (mosses and their relatives) cover the trees’ branches, along with larger epiphytes such as ferns and orchids. These often dense, diminutive forests thrive in a climate of near perpetual mist. Tree growth is slowed by a shortage of sunlight as well as low temperatures. Elfin forests have a lower species richness of trees than lower elevation forests, probably due to greater climatic stress. Prominent plant genera include Podocarpus, Clusia, and Gynoxys.

Plate 13-24. Polylepis forest enshrouded, as it usually is, in mist. Photo by John Kricher.

Plate 13-25. Giant Conebill. Photo by Edison Buenaño.

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Plate 13-26. This combination of grasses, shrubs, and forbs characterizes páramo at high elevations in the Ecuadorian Andes. Photo by John Kricher.

Plate 13-27. See it? The Tawny Antpitta (Grallaria quitensis) occurs at elevations between 2,200 and 4,500 m (7,220– 14,760 ft) in páramo. More than 50 species of antpittas range from lowland rain forest to montane forests, but this species reaches the highest elevation of any. Because its habitat is relatively open, it is easy to see. Photo by Gina Nichol.

Plate 13-28. Much sought after by birders, the Rufous-bellied Seedsnipe (Attagis gayi) is one of four seedsnipe species (family Thinocoridae) found in the Andes. It favors wet páramo. Photo by Steve Bird.

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Plate 13-29. Espeletia dominates the landscape high in the Venezuelan Andes. Photo by John Kricher.

Plate 13-30. Espeletia in flower. Note the thick leaves. Photo by Bruce Hallett.

Unique and Endangered Polylepis Woods

Cold, Windy, Wet, Wonderful Páramo

At elevations between 3,500 and 4,500 m (11,480– 14,760 ft) in the Andes, above timberline, islands of gnarled trees dominated by the genus Polylepis (about 20 species, family Rosaceae) are found scattered in a landscape of wet páramo (see below for more on páramo). Polylepis trees are typical of wind-protected, rocky slopes (plate 13-24). Though Polylepis can be found mixed among other species in lower-elevation cloud forests, the genus occurs in pure stands at higher elevations. Polylepis is evergreen, its leaves drought resistant. The largest trees reach heights of about 18 m (60 ft), but most are of smaller stature. Studies in central Ecuador have shown that seedlings survive best when deep within the Polylepis stand, where wind conditions are far less severe. However, vegetative propagation by shoots and ramets (a ramet is a stem that arises from an underground root), a form of asexual reproduction, is highest at the boundary of the woodland. This suggests that with protection, stands of Polylepis could increase in area. Several specialized bird species are found in Polylepis woods, including the Giant Conebill (Oreomanes fraseri; plate 13-25). Conebills belong to the huge tanager family (Thraupidae), and most occur at lower elevations. This species is unique to Polylepis woods, occurring at 3,500–4,200 m (11,480–13,780 ft) in Ecuador, Peru, and Bolivia. Though Polylepis woodlands range from Venezuela to northern Argentina and Chile, this ecosystem type has been much reduced by cutting and is threatened throughout most of its range.

Páramo is a shrub and grass ecosystem occurring from Costa Rica south to Bolivia at elevations above those that support cloud and elfin forest, generally above 3,800 m (12,470 ft). The climate is wet and cool (often cold), and nightly frosts are frequent throughout the year. Approximately 5,000 plant species, including numerous endemic species, are known from páramo ecosystems, which are characterized by large areas of wet grass often interrupted by peat bogs. Dominant vegetation consists of large, clumped tussock grasses, which have sharp, yellowish blades, along with a scattering of terrestrial bromeliads and ferns (plate 13-26). Shrubs, most in the genus Espeletia, grow among the tussock grasses, some reaching heights of 4–5 m (approx. 13–16.5 ft), so they resemble small trees. Leaves grow from the base of the stem, surrounding it in a pattern termed a rosette. A number of bird species make their home in páramo; two are shown in plates 13-27–28. Espeletias are some of the oddest-appearing members of the immense sunflower or composite family (Asteraceae or Compositae), to which daisies, asters, and goldenrods belong. Espeletias have short, thickly woolly trunks densely surrounded by withered dead leaves and topped by a rosette of thick, elongate green leaves, each covered by soft hairs that help minimize evaporative water and heat loss (plates 13-29–30). Espeletias are indicator species of South American páramo. (Similar high-elevation ecosystems in Central America lack espeletias.) Scattered among the tussock grasses on the cold, windy Andean slopes, espeletias attract many hummingbirds and bees to feed on the nectar of their yellow flowers.

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Puna: The High Grassland of the Andes Puna is defined as cold alpine grassland where conditions are severe. The essential difference between puna and páramo is that puna is more arid. Windswept and cold, puna at higher elevations is sometimes snowcovered. Wind seems to be constant, and billowing fog clouds are commonplace. Tussock grasses are abundant (plate 13-31), as are various succulents, such as cacti. Wet puna (overlapping with páramo) occurs in the northern and western Andes (Colombia, Ecuador, Peru, Bolivia). Dry puna predominates to the south (Chile and Argentina). Globally, puna-like alpine grassland occurs in African mountains and in high elevations in New Guinea. Tussock grasses of higher elevations in New Zealand also form a similar alpine grassland ecosystem. The most striking of dry puna plants is Puya raimondii, the world’s largest bromeliad, characterized by a huge and dense basal cluster of thick swordlike leaves. Puya flowers relatively infrequently. When it does, its hundreds of flowers cluster on a stalk that protrudes well above the leaves, rising as high as 8–9 m (26.25–29.5 ft). Puya, as well as other puna plants, is visited by numerous hummingbird species. Puna is habitat for many mammal species, including the Vicuña (Vicugna vicugna), a South American member of the camel family. Herds made up of a dominant male and up to 10 females roam about the barren puna. Another wild camel of the Andes, somewhat larger than the Vicuña, is the Guanaco (Lama guanicoe; plate 13-32). It is perhaps ancestral to the domesticated llama (Lama guanicoe glama) and alpaca (L. g. pacos), whose origins date back to domestication by pre-Columbian peoples. Llamas are the beasts of burden for the mountain Indians, the modern Inca. The husky Mountain Viscacha (Lagidium peruanum), a member of the rodent family, is a close relative of the chinchillas (Chinchilla spp.), two Andean species now quite local due to overtrapping.

High above the puna and páramo, look for the immense Andean Condor (Vultur gryphus; plate 13-33) as it soars on heat currents rising from the surrounding valleys. The condor soars almost effortlessly, flying from mountaintop to seacoast. Twice the size of a Turkey Vulture, the condor has a 3 m (9.8 ft) wingspread (surpassed, but only barely, by the largest albatrosses) and can weigh as much as 15 kg (about 33 lb), making it one of the most massive birds. Vultures are scavengers, and historically the Andean Condor was dependent on Vicuña and other mammals for its food source. Condors are now known to rely on carcasses of sheep and cattle in some areas. Located in the puna, high elevation Andean salt lakes are habitat for several flamingo species as well as other birds rarely encountered at lower elevations. The James’s Flamingo (Phoenicoparrus jamesi) was considered extinct until rediscovered on a lake 4,400 m (14,450 ft) high in the Bolivian Andes in 1957. More common are the Andean (P. andinus) and Chilean (Phoenicopterus chilensis) Flamingos (plate 13-34). All flamingos feed on brine shrimp and other small crustaceans skimmed from the water with their peculiar hatchet-shaped bills. The Puna Teal (Anas puna; plate 13-35) is another species of puna lakes. Fast-flowing Andean rivers are habitat for the Torrent Duck (Merganetta armata; plate 13-36) and Whitecapped Dipper (Cinclus leucocephalus). The sleek male Torrent Duck has a white head boldly patterned with black lines and a sharply pointed tail. The female is rich brown. Both sexes have bright red bills. Six subspecies of Torrent Duck occur from the northern Andes to the extreme southern Andes. Torrent Ducks brave the most rapid rivers, swimming submerged with only their heads above water. The White-capped Dipper is a chunky bird suggesting a large wren in shape. Like the Torrent Duck, it favors clear, cold mountain rivers, submerging itself in search of aquatic insects and crustaceans. From condors to Torrent Ducks, from Guanacos to espeletias, the high Andes offer so much. This chapter has touched on just a few of the reasons to start climbing.

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Plate 13-31. Puna is windswept and dominated by tussock grass, as shown here. Photo by John Kricher.

Plate 13-32. Guanaco, at home in the high puna. Photo by Andrew Whittaker.

Plate 13-33. The Andean Condor, an iconic species of the high Andes, is huge and distinctive. Photo by Edison Buenaño.

Plate 13-34. This is a mixed flock of Chilean and Andean Flamingos in the high Andes. Photo by Andrew Whittaker.

Plate 13-35. High Andean lakes are habitat for the endemic Puna Teal. Photo by Sean Williams.

Plate 13-36. This Torrent Duck is a male. Females have rufous coloring on the underside. Photo by Gina Nichol.

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Chapter 14

Don’t Miss the Savannas and Dry Forests

What Is a Savanna? Tropical savanna is grassland that has a rich scattering of trees. Savanna forms part of an ecological gradient from grassland (little or no trees) to dry forest (mostly trees and not so much grass). Savanna ecosystems are estimated to cover approximately one-fifth of the land surface of Earth, including extensive areas within the tropics, particularly in eastern and southern Africa. J. S. Beard (1953) was among the first researchers to define tropical savanna, calling it “a natural and stable ecosystem occurring under a tropical climate, having a relatively continuous layer of xeromorphic grasses and sedges, and often with a discontinuous layer of low trees and shrubs.” In Beard’s definition, xeromorphic refers to plants adapted to withstand periodic dryness, and a strong dry season typifies savanna ecosystems. These xeromorphic characteristics are structural (and by implication, physiological) adaptations such as tough fibrous leaves that enable a plant to endure high temperatures and periodic drought and not lose water. Many savanna species are uniquely adapted to thrive under hot and sunny conditions (plate 14-1). Though Beard’s definition states that savannas are stable, they do experience changes in the relative amount of grass cover and woody vegetation, for reasons such as fire frequency and severity of dry season. Wherever savannas are found, there is a gradient evident: patches of grasslands grade into savannas and savannas grade into dry forests.

Plate 14-1. Burrowing Owls (Athene cunicularia) are common residents of grasslands and savannas throughout Central and South America, and their range extends well into North America. Photo by John Kricher.

Wet tropical savannas are found in tropical and subtropical areas that have strong rainy and strong dry seasons. One familiar example is the Florida Everglades, a wet seasonal subtropical savanna in extreme southern Florida (plate 14-2). In South America the extensive Llanos in the northeastern part of the continent and the vast Pantanal of southern Brazil and portions of Bolivia and Paraguay (both ecosystems are described below) are splendid examples of wet seasonal savannas. Each forms an ideal place to visit to see a true abundance, indeed a spectacle, of South American wildlife.

Savanna Distribution In South America, combinations of grassland, savanna, and dry forest are estimated to occupy about 250 million ha (618 million ac), principally in Brazil (cerrado, caatinga, campo rupestre, and Pantanal), Colombia (Llanos), and Venezuela (Llanos). Large tracts are also found in eastern Bolivia (Pantanal), and in northern Argentina and Paraguay (Chaco). Broad expanses of savanna and dry forest also occur in Central America particularly in the northern Yucatán Peninsula and in parts of Belize, Honduras, and Nicaragua. Savanna is common in many Caribbean areas, too, particularly in the Bahamas and West Indies (plate 14-3). Numerous tree species populate savannas throughout Central America, the Caribbean islands, and equatorial South America, including acacias, palmettos, palms,

Plate 14-2. The Florida Everglades has been called a “river of grass.” It is a seasonal wet savanna that is dependent on floodwaters from Lake Okeechobee to maintain the wet savanna ecosystem. Photo by John Kricher.

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cecropias, and others, depending upon location. Local plant species composition varies widely. In much of Central America and the Caribbean, the most abundant savanna tree species is Caribbean Pine (Pinus caribaea; plate 14-4), which is often adorned with bromeliads and orchids. Several species of oaks are common in Central American savannas, though no oaks are found in South American savannas. Fire-resistant tree species such as Byrsonima crassifolia, Casearia sylvestris, and Curatella americana are abundant on South American savannas, as are large stands of Moriche Palm (Mauritia flexuosa), typically found along wet areas. Grasses and (in wetter areas) sedges form much of the ground vegetation. Soil ranges widely, from sandy to claylike, but is typically described as poor.

What Causes Savanna Formation? There is no single environmental factor that determines that a given site will be savanna. Savannas are found on a wide variety of soil types and experience extremes of tropical climate. Rainfall, while usually strongly seasonal, may in some cases be relatively nonseasonal. Water drainage may be rapid or slow. Fire is an important influence, and savannas tolerate fire well, rebounding quickly after burning. Grazing by large animals may exert strong effects on some savannas, particularly in Africa, but grazing is not generally a factor in the Neotropics, except where there is extensive and prolonged cattle ranching.

Plate 14-3. Pinewoods characterize savannas in the Bahamas and much of the savanna habitat in Central America. Photo by John Kricher.

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Though climate has a major influence on savanna formation, it cannot be the only influence, because tracts of savanna frequently occur in the midst of otherwise wet forest areas, where rainfall is evenly distributed throughout the year. For this reason, local soil type (edaphic factors) as well as other factors must also influence savanna formation. Soil and climate strongly interact. In the central Llanos in northeastern South America, heavy rains result in soil forming a hardened crust of lateritic ferric hydroxide, usually at some depth in the soil but occasionally on the surface. This crust, termed arecife, is sufficiently hard to impede the growth of tree roots, except where the roots encounter channels through the crust. In essence, the area becomes permanent savanna. Lightning-set fire is a normal component of savanna climate and is of major importance in savanna formation and propagation. Natural fires may be common during dry season when brief but heavy thunderstorms are typical. Some savannas have formed on sites where rain forest has been repeatedly cut and burned, suggesting that human activity can alter conditions on the site such that savanna takes over when the site is abandoned.

Climate Savannas and moist forests share relatively few species, and moist forests are typically richer in species. However, savannas of various sorts, such as cerrado, host numerous endemic plant species and all savannas offer opportunities to see many animal species (plate 14-5), as discussed later in the chapter. Savannas typically

Plate 14-4. Savanna ecosystem on Abaco Island in the Bahamas. The foreground is mostly grass and palmettos; the background trees are Caribbean Pine. Photo by John Kricher.

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ways to withstand occasional burning. Grass is an outstanding example. Grasses have dense underground root systems that are protected from surface fire and allow rapid aboveground growth following fires. A fire burns the plants’ aboveground vegetation, releasing minerals, fertilizing the upper soil layer, and enhancing regrowth. Trees are less adaptable to fire, though ancient charcoal remains from Amazon forest soils dated prior to human invasion suggest that even moist forests also occasionally burn. Experiments in which fire is suppressed suggest that if fire did not occur in savannas, plant species composition would significantly change. When burning occurs, it prevents competition among plant species from progressing to the point where some species exclude others. Frequent fire generally favors grasses and selects against woody vegetation. Plate 14-5. The Campo Flicker (Colaptes campestris) ranges throughout southeastern South America. It frequents open areas, cerrado, dry woodland, and savannas, where it is often on the ground, searching for ants. Photo by Nancy Norman.

experience an annual rainfall of between 50 and 200 cm (about 20–80 in), most of it falling in a five- to eightmonth wet season. Rainfall varies among years, and periodic droughts occur, some of which may be severe. Though annual precipitation on a savanna may be substantial, for at least part of the year there is drought stress, which ultimately favors grasses and dry-adapted trees. In most areas, rainfall is the most critical variable in determining whether an area is essentially grassland (low rain), savanna, or dry woodland (moderate rain). Though savannas throughout Venezuela, Colombia, Bolivia, Suriname, Brazil, and Cuba all experience a significant dry season exceeding three months, savannas in Central America (Nicaragua, Honduras, Belize) as well as in coastal areas of Brazil and the island of Trinidad do not have protracted dry seasons. For only three months at the most is rainfall below 10 cm (4 in) per month. Additional factors, particularly soil quality, contribute to savanna formation in these areas.

Fire Fire frequency is an important variable upon which many savannas depend. Savannas typically experience frequent mild fires, but there may be major burns every few years or so. Many savanna and dry-forest plant species are pyrophytes, plants that are adapted in various

Soil Characteristics Many savanna soils, like many rain forest soils, are typically oxisols and ultisols (chapter 6), with a low pH (4–4.8) and notably low concentrations of phosphorus, calcium, magnesium, and potassium. Aluminum levels are high. Some savannas occur on waterlogged soils, others on dry, sandy, well-drained soils. Waterlogged soils occur in areas of flat topography or poor drainage. Because these soils usually contain large amounts of clay they become water-saturated. Air cannot penetrate between the soil particles, making the soil oxygen poor. In extreme cases, hardened pans form, as in the case of lateritic arecife soil and caliche soil, which is hardened with calcium carbonate. By contrast, dry soils are sandy and porous, their coarse texture permitting water to drain rapidly. Sandy soils are prone to the leaching of nutrients and minerals and so tend to be nutritionally poor. Though most savannas are found on sites with poor soils (either because of moisture conditions or nutrient levels or both), poor soils can and do support lush rain forest. The white, sandy soils of the upper Amazon (chapters 6 and 12) support such forests, unless the forest is cut and burned. This wide range of soil characteristics may seem unusual, but it really means that extreme soil conditions, either too wet or too dry for forests, are satisfactory for savannas. More moderate soil conditions support moist forests. Indeed, soil degradation is blamed for promoting savanna formation in sites that once supported moist forest.

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Herbivory Historically most savanna ecosystems have supported significant levels of herbivory by large animals. This was apparently true of South America until the Pleistocene extinctions. Today only Africa still retains its megafauna. The collective influence of over 40 species of hoofed mammals, some grazers (feeding on grass), some browsers (feeding on leaves from woody plants), and some generalists that both browse and graze, has had a significant influence on African savanna ecology. Presumably that was also the case when a diversity of large animals occupied Neotropical savannas.

Human Influence On certain sites savanna formation correlates with frequent cutting and burning of moist forests by humans. Increase in pastureland and subsequent overgrazing (mostly by cattle) has resulted in an expansion of savanna (plate 14-6). Cutting and burning, if too frequent, destroys the thin, upper layer of humus necessary for rapid decomposition of leaves by bacteria and fungi and recycling by surface roots. Once the humus layer is lost, nutrients cannot be efficiently recycled and more rapidly leach from the soil, converting soil from fertile to infertile and making it more suitable for savanna vegetation. In some areas in South America deep-rooted grasses imported from Africa to furnish fodder for cattle have come to dominate savannas, replacing native species. These grasses, in particular Andropogon gayanus and Brachiaria humidicola (often called African elephant grasses), now are estimated to cover about 35 million ha (86.5 million ac) of savanna.

Are All Savannas “Natural”? Some ecologists have suggested that Neotropical savannas have essentially resulted from human activity rather than environmental causes. This claim is unsubstantiated by historical evidence, however. The fossil record of South American megafauna shows that savanna and open woodland were present in many areas throughout much of the Cenozoic era. Evidence exists that savanna vegetation grew in parts of the Amazon Basin as recently as 13,000 to 30,000 years ago. What remains controversial is just how much savanna was present. Neotropical savannas demonstrate the highest plant species richness of any savanna ecosystems, including

Plate 14-6. Savannas have expanded in some areas because of intensive grazing by introduced cattle. The flying birds here are Blue-and-yellow Macaws (Ara ararauna). Photo by John Kricher.

those of Africa. In numbers of both herbaceous and woody species, Neotropical savannas rank first. This high species richness suggests that evolution of savanna species has been occurring throughout much of the Cenozoic era, particularly in the late Miocene. Savanna is as distinctive and intrinsic to the Neotropics as it is to Africa and other regions. There is a dynamic, temporal interface among grasslands, savannas, and dry forests. One expands as the others contract in a climatically driven, edaphically influenced, long-term process that has produced and continues to produce far-reaching effects on evolutionary patterns of both plants and animals.

Neotropical Savannas and Dry Forests: Some Examples Dry Pine Savanna of Belize The savannas of Nicaragua, Honduras, and Belize are populated abundantly by Caribbean Pine. Riding through miles of savanna along the Southern Highway in Belize, one notices that many of the pines have dark fire scars on their trunks. Lightning strikes cause fires during dry season, and the effects of dryness and periodic fires combine to preserve savanna. Caribbean Pines tolerate occasional mild fires better than other tree species in Belize. Grasses also thrive in an environment with periodic fire. Throughout much of southern Belize east of the Maya Mountains, the dominant ecosystem type is savanna, abounding in Caribbean Pine but also supporting many

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Plate 14-7. Pine savanna in southern Belize. Photo by John Kricher.

Plate 14-8. Dense dry woodland of low-stature trees characterizes areas of natural cerrado. Note the tall cactus plants. Photo by John Kricher.

Plate 14-9. Terrestrial bromeliads, shown here in the foreground, are common plants on cerrado. Photo by John Kricher.

Plate 14-10. The Purplish Jay (Cyanocorax cyanomelas) may be seen in dry cerrado woodland, especially near rivers. Photo by John Kricher.

other species, ranging from grasses, palms, and palmettos to Cecropia and Miconia species (plate 14-7). Compared with the nearby tropical moist forest nestled within the protective (and moister) Maya Mountains, the pine savanna is an area of low species richness and a simpler, more arid and rugged-looking ecosystem. During the dry season, which extends from about February through most of May, the pine savanna is subject to occasional fires, the evidence of which can be seen as charred stumps and burned bark on many of the pines throughout the region. In this area, fire is an important ecological influence, a factor that provides the key ingredient in maintaining the dominance of savanna. Wildlife is less diverse in this savanna than in the interior lowland moist forest, but many animal species typical of forest occasionally range into savanna, including boa constrictors and Jaguars. The pine savanna

is inhabited by Gray Fox (Urocyon cinereoargenteus), Tayra (Eira barbara), and White-tailed Deer (Odocoileus virginianus), as well as numerous bird species.

The Brazilian Cerrado The largest area of Neotropical savanna vegetation, the cerrado, occurs in central Brazil, forming a wide belt across the country from northeast to southwest. Cerrado occurs on acidic, deep, sandy soil and is characterized by small, often widely spaced trees and shrubs on grassland. Vegetation includes numerous endemic plant species, and the structure ranges from open woodlands with a 4–8 m (14–27 ft) tall canopy to dense scrub thicket (plate 14-8). Cerrado soils are nutrient poor, and crop yields are dramatically increased when soil is fertilized with trace elements.

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Plate 14-11. Maned Wolf, after dark. Photo by Andrew Whittaker.

Plate 14-12. Red-legged Seriema atop a mound, calling. Photo by John Kricher.

Plate 14-13. Greater Rhea. Photo by John Kricher.

Plate 14-14. This is a cattle pasture in converted cerrado. Note the flock of Greater Rheas occupying the pasture in dry cerrado woodland. Photo by John Kricher.

Dry woodland is part of cerrado. It consists of shrubs and scattered semi-deciduous trees typically no taller than 8 m (26.25 ft). The small, stocky trees have dense, twisted branching patterns and thick bark. Bromeliads (plate 14-9), many of them terrestrial rather than epiphytic, are common plants, and many bird species not found in moist forest inhabit cerrado (plate 14-10). Cerrado areas are highly seasonal and experience frequent natural fires, and their soil is typically very sandy. The cerrado ecosystem, which is a combination of savanna and dry forest and includes some 4,000 endemic species, is one of the most threatened ecoregions in the Neotropics. It is being widely cut to make room for crops, particularly soybeans. In the last 35 years approximately 2 million km2 (772,200 mi2) have been converted to agriculture, an area that represents about half of the original cerrado. A total of 137 cerrado species

are now listed as threatened, including the Maned Wolf (Chrysocyon brachyurus; plate 14-11). A large canine with a sharply pointed snout, strongly reddish coat, whitetipped tail, and long legs, the Maned Wolf, should you be so fortunate as to see one, is unmistakable. It reaches a length of about 1.5 m (5 ft). It is generally solitary and most often observed after dark, but daytime sightings are also possible, especially in areas (increasingly featured in ecotours) where the animal is know to occur. The cerrado provides habitat for some of the most interesting South American bird species. One is the Red-legged Seriema (Cariama cristata; plate 14-12), a large ground-dwelling bird. There are two species of seriemas in the family Cariamidae, once considered part of the order Gruiformes, which includes cranes, rails, and bustards, among others. Seriemas feed on insects, snakes, and rodents. They walk as they stalk, often

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using their powerful legs and talons to subdue snakes and small mammals. Besides their unique ecology, perhaps the most distinctive aspect of the seriemas is their ancestry. Anatomical and genetic analyses strongly indicate that they are direct descendants of the flightless so-called terror birds (Phorusrhacidae), which were top carnivores in savanna ecosystems throughout much of South America during most of the Cenozoic era. The largest birds of the cerrado are the flightless rheas, relatives of the ostriches. There are two species, the widely distributed Greater Rhea (Rhea americana; plates 14-13–14) and the more southerly and less widely distributed Lesser (once referred to as Darwin’s) Rhea (Rhea pennata). The Greater Rhea is the larger and more abundant of the two. Rheas have the unusual habit of laying eggs in a communal nest. Several females mate with one male, and each hen deposits two to three eggs in the same nest. Only the male incubates. Rheas have adapted well to human agricultural ecosystems in cerrado areas and are commonly observed as roadside birds.

Caatinga Caatinga is a more desertlike ecosystem scattered throughout parts of Brazil, consisting of highly seasonal (with prolonged dry season) deciduous forest dominated by spiny trees and shrubs with thick leaves and thick bark, their branches covered with an abundance of lichens and mosses. Various cactus species occur in caatinga, and many plants are widely spaced on the dry soil. Caatinga occurs in climate that could support forest were it not for the nutrient-poor, sandy soil plus a marked seasonality in precipitation. This ecosystem is not nearly as diverse as moist forest but nonetheless is characterized by a unique array of trees, grasses, and sedges, many of them endemic to the region.

Thornwoods Thornwoods occur in semidesert areas from Mexico through Patagonia (plate 14-15). Dominant trees are usually Acacia species and other leguminous trees, of short stature, spaced well apart, and often interspersed with succulents such as cacti and agave. In many areas of thornwood, large herds of goats can be seen wandering about. Thornwood is very common along the Pan-American Highway throughout Peru, as well as in central Mexico and many West Indian islands.

Plate 14-15. Thornwoods are common in more arid areas in the Neotropics. Photo by John Kricher.

Examples of Tropical Wet Savanna Los Llanos: Seasonal Savannas of Venezuela and Colombia The wide floodplain of the Orinoco River extends over an area of grassy savanna interrupted by riparian forest and hammocks of woodland (raised areas in otherwise marshy areas). This habitat is called the Llanos (plate 14-16). It bears a strong physical resemblance and ecological similarity to the Florida Everglades, being essentially wet tall-grass prairie with grasses growing up to 1 m (3.3 ft) in height. The Llanos extends for an area of approximately 100,000 km2 (38,610 mi2) throughout southern Venezuela and into parts of Colombia. Grasses and sedges, especially those in the genera Panicum, Leersia, Eleocharis, Luziola, and Hymenachne, dominate much of the landscape. Trees and shrubs are widely scattered, often occurring as “island” woodlots called matas or bancos. These small and scattered woodlots are also known as hammocks, especially in the Florida Everglades. The Llanos is seasonal wet savanna, with pronounced dry season extending through most of the northern winter. Approximately 100 cm (39 in) of rain is received over the seven-month rainy season. But for nearly five months, rainfall is quite low. It is then when natural fires are common. During dry season, vast flocks of wading birds such as ibises, storks, herons, and egrets are concentrated in the relatively limited remaining wet areas. These birds, plus the added presence of such species as the Capybara (Hydrochoeris hydrochaeris;

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Plate 14-16. Large flocks of birds mass on the Llanos, including spoonbills, egrets, and ibises, shown here. Photo by John Kricher.

Plate 14-17. Capybaras are abundant on the Llanos. Photo by John Kricher.

Plate 14-18. The Purple Gallinule (Porphyrio martinicus), which is related to rails, is commonly seen in marshy areas in the Llanos and Pantanal. Photo by John Kricher.

Plate 14-19. The Roseate Spoonbill (Platalea ajaja) ranges from the Georgia and Florida coasts and the Gulf coast states to Amazonia, where large populations are found in the Llanos and Pantanal. Photo by John Kricher.

plate 14-17), Giant Anteater (Myrmecophaga tridactyla), Green Anaconda (Eunectes murinus), Spectacled Caiman (Caiman crocodilus), and Jaguar (Panthera onca), make the Llanos one of the best areas in the Neotropics for observing wildlife. Rainy season usually peaks in July (and you should not go there then, as it is difficult to get around). On average, rainfall exceeds 120 cm (47 in) per year and can exceed 150 cm (59 in) annually. At peak rainy season, the Llanos is in full flood, though higher areas, such as hammocks of palms and other trees and shrubs, remain above water. Because of the strong degree of seasonality, plant and animal species must be generally adapted to endure both drought and flood. Many large cattle ranches are scattered throughout the Llanos, some of which also

serve to host ecotourist groups who wish to see the birds and other animals. The Llanos wet grassland savanna supports a diverse assemblage of waterbirds (plate 14-18). James Kushlan and colleagues studied the wading bird community of the Venezuelan Llanos and found 22 species of large wading birds, including seven ibis species, one spoonbill (plate 14-19), 11 herons and egrets, and three storks. In comparison, the Florida Everglades supports only 15 species of large waders. Stork species, including the huge Jabiru (Jabiru mycteria (plate 14-20), the Maguari Stork (Ciconia maguari; plate 14-21), and the Wood Stork (Mycteria americana; plate 14-22), are common on the Llanos, probably because large fish, their principal prey items,

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Plate 14-20. The Jabiru is, at 140 cm (55 in) tall, the largest of the New World storks. Photo by John Kricher.

Plate 14-21. The Maguari Stork is the second largest (120 cm/47 in tall) and the least common of the region’s three stork species. Photo by Nancy Norman.

Plate 14-22. Wood Storks are common throughout the Neotropics, particularly in the Llanos and Pantanal regions. They range as far north as Georgia. Photo by John Kricher.

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are abundant. Only the Wood Stork reaches North America. It is best to visit the Llanos in dry season. Animals, particularly waterbirds, are then concentrated in and around standing pools where fish are also concentrated, thus make wildlife viewing quite easy and pleasurable.

The Pantanal of Southern Brazil and Bolivia The vast Pantanal, a name that means “swamp,” is a more southerly ecological equivalent of the Llanos, sharing many of the same species (plate 14-25). Larger in area than the Llanos, the Pantanal covers approximately 200,000 km2 (77,220 mi2), of which about 70% is within the state of Mato Grosso do Sul in Brazil, with the remaining area in eastern Bolivia. It is a region of low elevation, only about 150 m (500 ft) above sea level, a vast, flattened basin created by deposited sediment eroded from the surrounding highlands. Eventually all of the many Pantanal rivers flow into the Río Paraguay, the Pantanal equivalent

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of the Orinoco in the Llanos. Dry season ranges from May through October (essentially the opposite pattern from the Llanos). During rainy season, which peaks from late January through mid-February, water levels can rise as much as 3 m (9.8 ft), and much of the lowlying grasses and sedges are in full flood. In general, the human population is low in this hyperseasonal wet savanna, concentrated in but a few large cattle ranches and scattered small towns and villages. Consequently, the wildlife diversity becomes a spectacle (plates 14-26–27). Riverbanks are lined with myriad caiman kept well fed by the bountiful populations of piranha, tetras, catfish, and other fish. Giant Otters (Pteronura brasiliensis) make dens along riverine embankments. Marsh Deer (Blastocerus dichotomus) and Red Brocket Deer (Mazama americana) can be seen among the tall Pantanal grasses, as can the Giant Anteater, Brazilian Tapir (Tapirus terrestris), Crabeating Fox (Cerdocyon thous), and Crab-eating Raccoon (Procyon cancrivorus). The Pantanal abounds with Capybara and vast hosts of wading birds, including

Escargot: Connoisseurs of the Marshes Snails in the genus Pomacea, along with a few other genera, are commonly called apple snails, presumably for their rotund shape and the fact that they approach the size of an apple. They are commonly kept in aquaria. Some are large, up to 15 cm (5.9 in) long. Apple snails are always present and often abundant in the Llanos and Pantanal as well as parts of the Florida Everglades. Not surprisingly these large mollusks represent a potentially good food source, and three bird species have specialized to feed on them. The Limpkin (Aramus guarauna; plate 14-23), a large wading bird, is the only member of the family Aramidae. It appears to be most closely related to rails and cranes. Limpkins make loud and wailing calls that have earned them the name “crying bird.” They specialize in feeding on apple snails, adeptly removing the fleshy animals from their shells. While relatively dependent on apple snails as a food source, Limpkins do feed on frogs and large insects, especially when snails are reduced in population. Two raptors, the Snail Kite (Rostrhamus sociabilis; plate 14-24) and the Slender-billed Kite (Helicolestes hamatus), both devour Pomacea snails by employing their sharply hooked upper mandibles to pluck the snail from its shell. The Snail Kite is widely distributed and common in the Llanos and Pantanal and extends its range to southern Florida (where it is sometimes called the Everglades Kite). The Slender-billed Kite is more restricted in range, occurring only in parts of Amazonia.

Plate 14-23. A Limpkin, with an apple snail in its bill. Photo by Andrew Whittaker.

Plate 14-24. A male Snail Kite hunts near dusk over the Pantanal marshes. Photo by John Kricher.

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Plate 14-25. Large wading birds such as the Great Egret (Ardea alba) are abundant in the Llanos and Pantanal during dry season, when they congregate in marshes. Photo by John Kricher.

Plate 14-26. Large numbers of wading birds frequent Pantanal marshes. Most of these birds are Great Egrets, but there is one Jabiru stork among them. Photo by John Kricher.

Plate 14-27. Pantanal reedbeds are habitat for the unmistakable Scarlet-headed Blackbird (Amblyramphus holosericeus). Males and females look alike. Photo by John Kricher.

Plate 14-28. Jabirus nest on the Pantanal. Photo by John Kricher.

three stork species (plate 14-28), four ibis species, and a dozen species of herons and egrets, most of which can be found on any given day. Among the copses of palms, the huge Hyacinth Macaw (Anodorhynchus hyacinthinus) can be seen, the Pantanal being the final stronghold for this once abundant and majestic parrot (chapter 15). Saving the best for last, the Pantanal is, in my opinion, the best and most reliable place to see the Jaguar

(plate 14-29). Ecotourist facilities provide boats with experienced spotters, and a slow ride along the various river tributaries in early morning (but really any time of day) often results in a sighting of a Jaguar lounging in the sun on the riverbank or even swimming across a river. Sometimes you get fortunate enough to watch one actually hunting a Capybara or caiman. Jaguars are discussed more in chapter 16.

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Plate 14-29. Feeling lucky? Jaguars do swim and sometimes afford memorable looks as they swim past your boat. Photo by Andrew Whittaker.

The Pampas In extreme southern Brazil continuing southward through Patagonia is a region termed the pampas. In human history, this is the land of the gauchos, talented horsemen indeed. The pampas are a vast expanse of mostly grassland that is part of the southern temperate zone. The pampas are essentially south of the Tropic of Capricorn and thus not part of the Torrid Zone but will be treated briefly here because of their intrinsic interest as well as the fact that they are frequently included in various ecotours, such as those increasingly popular tours combining nature watching with wine tasting. The pampas consist of extensive stands of tussock grasses (Stipa brachychaeta, S. trichotoma). In areas of sandy soil and decreased rainfall, dry woodland occurs, consisting mostly of a single legume species, Prosopis caldenia. The windswept, barren pampas host a diversity of unique animals. The Pampas Deer (Ozotoceros bezoarticus) is endemic. Rodents are abundant, including the Mara (Dolichotis patagonum), sometimes called the Patagonian Cavy or the Patagonian Hare. Superficially resembling a hare (including the long ears), this rodent can leap a distance of 1.8 m (6 ft). Charles Darwin was fascinated by a group of burrowing rodents of the pampas collectively called the tucotucos (Ctenomys spp.). Darwin wrote, in The Voyage of the Beagle: This animal is universally known by a very peculiar noise which it makes when beneath the ground. A person, the first time he hears it, is much surprised; for it is not easy to tell whence it comes, nor is it possible to guess what kind of creature utters it. The noise consists in a short, but not rough, nasal grunt, which is monotonously repeated about four times in quick succession; the name Tucutuco is given in imitation of the sound.

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Neotropical Birds: The Bustling Crowd

Plate 15-1. The Harpy Eagle (Harpia harpyja) is found throughout Amazonia, but each bird occupies a large territory. Seeing one is every tropical birder’s wish. Photo by Gina Nichol.

Plate 15-2. The widespread and familiar Bananaquit (Coereba flaveola) is one of the species that has usually been placed among the incertae sedis, at least in some authoritative lists. The American Ornithologists’ Union’s South American checklist currently considers it in the Thraupidae, among the tanagers. Photo by Nancy Norman.

Birds draw many visitors to the Neotropics. Many come to augment their life lists, wanting to add more parrot species, more tanagers, more hummingbirds, and hoping for an encounter with the majestic Harpy Eagle (plate 15-1). Others do research on birds in the hopes of adding knowledge about avian ecology and evolution in this richest of ecosystems. This chapter makes an attempt to convey the uniqueness and diversity of the Neotropical avifauna, whose continued welfare faces an uncertain future (chapter 18). Be aware that this account is in no way meant to be comprehensive and that birds, as you know by now, are featured in numerous chapters throughout the book. The International Ornithological Congress lists a total of 10,637 species of birds currently inhabiting the world. More than one third of these are found in the Neotropics. No one knows exactly how many species of birds inhabit the region, because avian taxonomy is in a current state of flux, and numbers of species in various groups change annually as decisions are made about lumping or splitting species. Incredibly there is no single list of bird species of the Neotropics, because most lists are confined either to South America or Middle America or the West Indies or individual countries, and authorities differ in assigning species status. The American Ornithologists’ Union (AOU) has compiled a current taxonomic bird species list for South America that totals 3,368 species (readily available on the AOU website; http:// www.americanornithology.org), but this list (which includes one extinct species) omits all the numerous species of Central America (such as the Resplendent Quetzal), as well as Cuba and the West Indies, because those areas are included in the North American AOU checklist, which, of course, includes numerous species that never occur in the Neotropics. In this chapter I have used both the AOU’s South American and North American checklists to cite current numbers or recognized species. As well, I have relied on Bird Families of the World (Winkler, Billerman, and Lovette, 2015). Other checklists to the world’s birds exist as well, including the comprehensive list published by the International Ornithological Congress (http://www. worldbirdnames.org). What is important to note is that these various authoritative sources do not agree in some cases on species designation, as well as species names, both common and scientific. Older field guides to birds will not reflect much of what has emerged with

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the new classification and taxonomy, so if you have a keen interest in birds, try to obtain the most recent field guides and checklists to wherever you are traveling. To reiterate, avian classification is changing rapidly as DNA analysis and dedicated field research together continue to reveal that birds once considered to form a single species are best split into several species (and vice versa). These decisions are often debated. Whole groups of Neotropical bird species are being reclassified, and the taxonomy of birds changes annually (almost daily) with continuing research and analysis. For some species, it is not yet possible to be certain about evolutionary affinities, and they are thus considered to be in a taxonomic category termed incertae sedis, and even species assigned to this category are placed in other categories by some authorities (plate 15-2). Without question the Neotropical region is the most bird-rich zoological realm on Earth, as more than one out of every three bird species can be found in Central and/or South America. But there is a catch. When Henry Walter Bates (1863) was exploring Amazonia he was moved to comment on the actual difficulty of observing birds in the dense Neotropical rain forest: The first thing that would strike a new-comer in the forests of the Upper Amazons would be the general scarcity of birds: indeed, it often happened that I did not meet with a single bird during a whole day’s ramble in the richest and most varied parts of the woods. Yet the country is tenanted by many hundred species, many of which are, in reality, abundant, and some of them conspicuous from their brilliant plumages. The apparent (but misleading) “scarcity” of birds in Neotropical lowland forests, evident particularly to many first-time visitors who walk trails for hours to tally relatively few species, seems surprising, because more species of birds occur there than in any other kind of ecosystem. Entire families, including cotingas, manakins, toucans, tapaculos, ovenbirds and woodcreepers, antbirds, antpittas, antthrushes, screamers, and trumpeters, are all essentially confined to the Neotropics, as are such unique species as the Sunbittern (Eurypyga helias), the Hoatzin (Opisthocomus hoazin), and the Boat-billed Heron (Cochlearius cochlearius), which were discussed in chapter 12. Bates put his finger on the irony of birding in the tropics. Even birds with glamorous plumages can be remarkably silent, still, and difficult to spot

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in the dense, shaded foliage. Patience, persistence, keen eyes, and a measure of luck are required of the tropical birder. Birds often appear suddenly, a dozen or more species moving together in a mixed-species foraging flock. Thus the birder may face a “feast or famine” situation. One minute birds seem absent. Then suddenly they are everywhere. And just as quickly they move on. Bates described just such an encounter: There are scores, probably hundreds of birds, all moving about with the greatest activity— woodpeckers and Dendrocolaptidae (from species no larger than a sparrow to others the size of a crow) running up the treetrunks; tanagers, antthrushes, hummingbirds, flycatchers, and barbets flitting about the leaves and lower branches. The bustling crowd loses no time, and although moving in concert, each bird is occupied, on its own account, in searching bark or leaf or twig; the barbets visiting every clayey nest of termites on the trees which lie in the line of march. In a few minutes the host is gone, and the forest path remains deserted and silent as before. The dark, complex foliage of interior rain forest hosts the majority of tropical bird species, a diversity that increases markedly from Central America into equatorial Amazonia. From forest floor to canopy, hundreds of different species probe bark, twigs, and epiphytes for insects and spiders. Others swoop at aerial insects, follow army ants as they scare up prey, search for the sweet rewards of fruit and flowers, or capture and devour other birds, mammals, and reptiles. One bird, the 96 cm (38 in) long Harpy Eagle (see “Hawks, HawkEagles, and Eagles,” below), preys on monkeys, sloths, and other large prey. Even with such an abundance of diversity, patience and luck are needed to see birds well.

Large Ground Dwellers Tinamous Though treetop species are often a challenge to see, even ground dwellers can be elusive. Forty-eight species of tinamous compose the family Tinamidae, a peculiar and evolutionarily ancient group of birds endemic to the Neotropics. A tinamou is superficially chicken-like, a chunky bird with a short, slender neck, a small, dove-like head, and thin, gently down-turned beak. Plumage ranges among species from buffy to

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deep brown, russet, or gray, often with heavy black barring. Some tinamous inhabit savannas, pampas, and mountainsides, but most live secretive lives on the rain forest floor, searching for fallen fruits, seeds, and an occasional arthropod. Forest tinamous are much more often heard than seen, and many are amazing vocalists. One of the most moving sounds of the rain forest is the clear, ascending, flutelike whistle of the Great Tinamou (Tinamus major; plate 15-3), a haunting sound given at dusk that heralds the end of the tropical day. One bird begins and soon others join in chorus. Evening twilight is the hour of the Great Tinamou serenade— it rarely sings during full daylight or dawn. As these birds are basically solitary, the function of the tinamou chorus may be to signal one another as to their various whereabouts. The best way to see a tinamou is to quietly walk a forest trail, especially in the early morning hours. You may suddenly come upon one foraging along the trail, and it will probably stare blankly at you for a moment before scurrying into the undergrowth. Tinamous are generally reluctant to fly but may abruptly flush in a burst of wings, landing but a short distance away. They cannot sustain flight for long distances, because their flight muscles, even though well developed, are not well vascularized, and the limited blood flow greatly restricts their effectiveness. Though tinamous superficially resemble chickens, tinamou anatomy and DNA analysis show that they are closely related to ostriches, rheas, and other large flightless birds. Their rounded eggs are unusual for their highly glossed shells and range of colors, from turquoise blue and green, to purple, deep red, slate gray, or brown. Only the male incubates the eggs, another characteristic shared with ostriches and rheas.

“Tropical Chickens”: Chachalacas, Guans, Curassows, and Quail The 56 species of chachalacas, guans, and curassows are similar in appearance to chickens and turkeys, and are in the same order, Galliformes, but are in their own family, Cracidae. They are found in dense jungle, mature forest, montane forest, and cloud forest. Though individuals and sometimes pairs or small flocks are often observed on the forest floor, small flocks are often seen perched in trees. The 15 chachalaca species are all slender, brownish olive in color, and have long tails (plate 15-4). Each

species is about 51 cm (20 in) from beak to tail tip. A chachalaca has a chicken-like head, with a bare red throat, usually visible only at close range. Most species form flocks of up to 20 or more birds. Chachalacas are highly vocal. The Plain Chachalaca (Ortalis vetula) is among the noisiest of tropical birds. Dawn along a rain forest edge is often greeted by a host of chachalaca males, each enthusiastically calling its harsh and monotonous chacha-lac! cha-cha-lac! cha-cha-lac! The birds often remain in thick cover, even when vocalizing, but an individual may call from a bare limb, affording easy views. Twenty-five species of guans and 16 species of curassows occur in Neotropical lowland and montane forests. Larger than chachalacas—most are the size of a small, slender turkey—they have glossy, black plumage set off by varying amounts of white or rufous (plate 155). Some, like the Horned Guan (Oreophasis derbianus) and the Helmeted Curassow (Pauxi pauxi), have bright red “horns” or wattles on the head and/or beak. The Blue-throated Piping-Guan (Pipile cumanensis; plate 156) and the Red-throated Piping-Guan (P. cujubi; plate 15-7) have much white about the head and wings and a patch of colorful skin on the throat. Guans and curassows, though quite large, can be difficult to observe well (plate 15-8). Small flocks move within the canopy, defying you to get a satisfactory binocular view of them. Like chachalacas, guans and curassows are often vocal, especially in the early morning hours. There are 23 species of New World quail (family Odontophoridae) in the Neotropics, but seeing them requires a lot of searching and good luck. They are generally a secretive, cryptic group, rarely giving observers a good close look, as they scurry quietly along the shaded forest interior (plates 15-9–10). Most of these species have narrow ranges but a few are more widely ranging. Both New World turkey species occur in the Neotropics. The familiar Wild Turkey (Meleagris gallopavo), whose domesticated relative graces the Thanksgiving table with its cooked presence, once ranged south to Guatemala. Now only domesticated individuals are found throughout the tropical portion of its range. The spectacular Ocellated Turkey (Meleagris ocellata; plate 15-11) ranges, still wild, from the Yucatán south through Guatemala. Smaller than the common turkey, the Ocellated has a bright blue bare head with red tubercles. Its plumage is more colorful than that of its relative, particularly its tail feathers, which have

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Plate 15-3. A Great Tinamou quietly going about its business. Photo by Gina Nichol.

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Plate 15-4. The Rufous-vented Chachalaca (Ortalis ruficauda) is found along forest edges and brushy areas from Trinidad to northern South America. Photo by Jill Lapato.

Plate 15-5. Female Bare-faced Curassow (Crax fasciolata). Curassows frequently perch in trees. Photo by John Kricher.

Plate 15-6. Blue-throated Piping-Guan flying across a river. Photo by John Kricher.

Plate 15-7. Red-throated Piping-Guan. These birds are rarely observed as clearly on the forest floor as this one. Photo by Andrew Whittaker.

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Plate 15-8. Male (left) and female (right) Great Curassows (Crax rubra). Where they enjoy protection from hunting, such as around ecolodges, curassows become much easier to observe. Photo by Steve Bird.

Plate 15-9. The Spot-winged Wood-Quail (Odontophorus capueira) is found in southeastern Amazonia. This one is making haste within the shaded forest. Photo by Andrew Whittaker.

Plate 15-10. The Starred Wood-Quail (Odontophorus stellatus), in a rare clear view that any birder would envy, occurs in a relatively wide range in western Amazonia. Photo by Sean Williams.

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Plate 15-11. Ocellated Turkey at Chan Chich Lodge in Belize, perhaps the best place to see this remarkable species. Photo by John Kricher.

Plate 15-12. Gray-winged Trumpeter (Psophia crepitans) on a forest trail. Photo by John Kricher.

bright blue and gold eyelike markings that give the bird its name (from ocellus, or eyespot). Ocellated Turkeys are easy to see at Tikal National Park in northeastern Guatemala and Chan Chich Lodge in Belize.

a muffled hoot, rather like the sound of air blowing over the opening of a bottle. Trumpeters will occasionally run around in circles, strutting and prancing with wings outstretched, apparently a courtship or excitement display. They roost in trees and nest in tree cavities. They are generally considered to be weak fliers.

Trumpeters Nothing looks quite like a trumpeter, except another trumpeter. These oddly shaped, rooster-size birds of the rain forest floor are uniquely humpbacked, with long legs, slender necks, and a chicken-like head (plate 15-12). There are three trumpeter species (family Psophiidae) recognized by the AOU, though some authorities (BirdLife International Illustrated Checklist of Birds of the World, vol. 1, 2015) recognize six species, a typical example of the taxonomic flux that currently reigns in ornithology. Each species, regardless of which taxonomy you choose, is confined to a different region within Amazonia; since each species’ range is separated by Amazonian tributaries, this distribution is an example of vicariance (chapter 8). Species are distinguished by wing coloration, ranging from white to dusky. Otherwise the birds are blackish, showing iridescent violet and greenish colors when in direct sunlight. Trumpeters amble along the forest floor in small flocks, feeding on such diverse items as large arthropods and fallen fruits. They are reputed to chase snakes. The name trumpeter comes from their curious vocalization,

Doves and Pigeons Doves and pigeons (order Columbiformes) are much alike in anatomy, but in general, doves are birds of edges and open areas (with some notable exceptions such as the quail-doves), while pigeons are found mostly in closed forest. Doves and pigeons are well represented in the Neotropics, where they feed heavily on seeds and fruits. There are 351 species in the world, of which about 64 occur in the Neotropics. Some Old World doves, particularly in Asia and the South Pacific, are extraordinarily colorful, but Neotropical species tend toward a plumage of muted colors such as grays, tans, or rich brown. Some of the larger species make low, deep cooing vocalizations that suggest the hooting of an owl. Doves and pigeons of various species are relatively common throughout Neotropical habitats and act as seed dispersers. Ground-doves of various species are commonly observed throughout the Neotropics (plate 15-13).

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Plate 15-13. The Ruddy Ground-Dove (Columbina talpacoti) is common throughout all of the Neotropics and now reaches parts of southwestern North America. It is found in open fields and forest edges. Photo by John Kricher.

Plate 15-14. The large Picazuro Pigeon (Patagioenas [Columba] picazuro) is widely distributed throughout southern Amazonia. Pigeons of various species often sit atop snags. Photo by John Kricher.

Plate 15-15. This Scaled Pigeon (Patagioenas speciosa), high atop a tree and backlit, is still clearly identifiable by its distinctive spotted breast. It is rather common to see pigeons in this way. Photo by John Kricher.

Plate 15-16. The White-throated Quail-Dove (Zentrygon [Geotrygon] frenata) is found along the Andes in lowland forests as well as cloud forests. Quail-doves, never easy to see, are among the most strikingly colored of Neotropical doves and pigeons. Photo by Nancy Norman.

Large forest pigeons are most easily observed when they sit conspicuously atop a tree or tree snag (plate 15-14), though this often places them in poor light, silhouetted against a bright sky (plate 15-15). Otherwise they may be seen mostly as they fly swiftly through or over the forest. Quail-doves and other forest doves are more of a challenge to observe as, like wood-quail, they tend to be rather secretive denizens of the forest floor (plate 15-16).

The family is well represented in Middle America as well as South America. Two species are found in the Greater Antilles, and two reach the southwestern United States, specifically Arizona. A trogon is a chunky, large-headed bird with a long, rectangular tail and short, wide bill. Complexly colored, males have iridescent green or blue heads and backs, and bright red or yellow breasts (plate 15-17). Females resemble males but are duller in color, often quite grayish. The pattern of black, gray, and white on the tail and the color of the eye-ring (a patch of colorful skin circling the eye) are important field marks to identify various species. Trogons range in size from about 25 to 33 cm (9.8–13 in).

Trogons There are 43 species of trogons (Trogoniformes) in the world’s tropics and subtropics, and 27 are Neotropical.

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Plate 15-17. Male Masked Trogon (Trogon personatus), perched in typical trogon posture, upright on a branch. This species is found throughout northwestern South America. Photo by Gina Nichol.

Plate 15-18. The Gartered Trogon, is one of the yellowbreasted trogons. It ranges from Mexico through Central America and into northern South America. Also called the Northern Violaceous Trogon, it was formerly considered a subspecies of Violaceous Trogon (Trogon violaceus). A male is pictured. Photo by Gina Nichol.

Trogons tend to sit upright with tail pointed vertically downward. They remain still and so are often overlooked. The easiest way to spot one is to look for its swooping flight, during which the bird flashes its bright plumage, and note where it lands. Most trogons vocalize throughout the day, often a repetitive cow, cow, cow, or caow, caow, caow, varying, of course, from one species to another. Sometimes the note sounds harsh, but in some species it is softly whistled and melodious. A good way to see a trogon at close range is to try to imitate its call. If the imitation is accurate, trogons may come close, with their characteristic swooping flight, to investigate. Some species are common along rain forest edges or successional areas. Look for their characteristic upright shape perched in cecropia trees. Trogons are cavity nesters. Some species excavate nest holes in decaying trees; others dig into termite mounds. The Gartered Trogon (Trogon caligatus; plate 15-18) utilizes large wasp nests, after carefully removing and consuming the resident wasps. The species also utilizes termite mounds as nests.

Plate 15-19. Male Resplendent Quetzal, in all its splendor. Photo by Gina Nichol.

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Trogons feed on fruits from palms, cecropias, and many other species, which they take by hovering briefly at the tree, plucking the fruits. They also catch large insects and occasional lizards, swiftly swooping down on them or snatching them in flight. Trogon bills are finely serrated, permitting a tight grip on food items. Arguably the most spectacular member of the trogon family is the Central American Resplendent Quetzal (Pharomachrus mocinno; plate 15-19), which is said to be the inspiration for the legendary phoenix. Guatemala’s monetary unit is the quetzal, and the bird’s image appears on all currency. Quetzals inhabit the cloud forests of Middle America, migrating to lower elevations seasonally. Most striking about the quetzal’s plumage is the brilliant green male’s elongated upper tail coverts, graceful plumes that stream down well below the actual tail, making the bird’s total length fully 61 cm (24 in). Females are a duller green and lack the elaborate tail plumes. Four other quetzal species are found in South America, and all are worth a look, but none of them have the long plumes of their more northerly relative.

Motmots The motmot family (Momotidae) currently consists of 14 species (but the taxonomy is being debated), all Neotropical. They are evolutionarily closely related to the kingfishers (discussed in chapter 9; plates 9-8– 12) and the todies (Todidae), a group of five species of small, brilliantly colored kingfisher-like birds that inhabit various islands of the Greater Antilles (plates 86–7). All of these birds share an unusual foot structure, in which the outermost and middle toes are fused together for almost their entire lengths. Motmots are slender birds whose back and tail colors are mixtures of green, olive, and blue. They have various amounts of rufous on the breast and have a wide, black band through the eye; some species have metallic blue feathers at the top of the head. Motmots range in size from the 18 cm (7 in) Tody Motmot (Hylomanes momotula) to the 44 cm (17.3 in) Rufous Motmot (Baryphthengus martii). Two noteworthy features of motmots are a long, racket-shaped tail (present on most but not all species) and a heavily serrated bill. The tail, which in some species accounts for more than half the bird’s total length, develops two extraordinarily long central

feathers. As the bird preens, sections of feather barbs drop off, leaving the vane exposed. The intact feather tip forms the “racket head” (plate 15-20). One may first sight a motmot as it sits on a horizontal branch in the forest understory methodically swinging its tail back and forth like a feathered pendulum (plate 1521). Another distinctive motmot characteristic is its bill, which is long, heavy, and strong, with toothlike serrations. I have held motmots and can testify as to the strength of their bite. They feed on large arthropods such as cicadas, butterflies, and spiders and will often whack their prey against a branch before eating it. They also take small snakes and lizards and frequently accompany army ant swarms. Motmots also eat much fruit, especially palm nuts, which they skillfully snip off while hovering, in a manner similar to trogons. Motmots are burrow nesters, making nest holes in embankments, another characteristic they share with kingfishers and todies. They excavate a tunnel nest along watercourses or occasionally nest within a mammal burrow. Motmots are most vocal at dawn. The call of the common and widespread Blue-crowned Motmot (Momotus momota; plates 15-20–21) may have given the family its name. The bird makes a soft, monotonous, and easily imitated whoot whoot. Often the birds in a pair will call back and forth to each other.

Jacamars There are 19 species of jacamars (plates 15-22–24), family Galbulidae, all of which are found in the Neotropics. The family is relatively closely related to the woodpecker order, Piciformes. Jacamars are anatomically somewhat similar to the Old World beeeaters (family Meropidae). They have long slender bills and fly out from a perch to capture insects. Jacamars are typically found along forest edge or within forests, often along steams. They usually occur in pairs, though not always. Their acrobatic flight is an adaptation to capture flying insects, something they appear to do with considerable skill. They are typical sit-and-wait predators, perching and patiently waiting for a flying insect to come within capturing distance. At that point the jacamar will sally forth for the capture. Jacamars, like bee-eaters, excavate nests in embankments, though some use termite nests.

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Plate 15-22. This is a White-throated Jacamar (Brachygalba albogularis) after a successful sally. Photo by Sean Williams.

Plate 15-20. A Blue-crowned Motmot (Momotus momota) showing its racket-like tail. Photo by James Adams.

Plate 15-23. The Rufous-tailed Jacamar (Galbula ruficauda) is the most common and widespread of the jacamar species. It is generally common in the forest understory. Photo by Kevin Zimmer.

Plate 15-21. A motmot will swing its tail, pendulum-like, from side to side, as this Blue-crowned Motmot demonstrates. Photo by James Adams.

Plate 15-24. The Great Jacamar (Jacamerops aureus) is the largest jacamar species. Photo by Kevin Zimmer.

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Plate 15-25. Toco Toucan (Ramphastos toco) in flight. Photo by John Kricher.

Plate 15-26. The Toco Toucan of South America is the largest and one of the most well known of the toucans. Photo by John Kricher.

Plate 15-27. Tropical versatility is represented in the bill of this Toco Toucan; it is adept at both plucking and gulping seeds (chapter 10) and, because it is heavily vascularized, serving to radiate excess heat. Photo by John Kricher.

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Plate 15-28. Keel-billed Toucan. Photo by James Adams.

Toucans, Aracaris, and Toucanets Perhaps more than any other kind of bird, toucans (family Ramphastidae) symbolize the American tropics. With a prominent boat-shaped, colorful bill almost equal in length to the body, the toucan silhouette is instantly recognizable. As it flies with neck outstretched, a toucan appears to follow its own oversize bill (plate 1525). Toucan is derived from tucano, the name used by Topi Indians in Brazil. Altogether, there are 50 species in the family Ramphastidae, including toucans, aracaris, and toucanets, all Neotropical. Currently the taxonomy of ramphastids is under review, and more species changes may be designated in the future. Even now, some toucans are routinely named with not only genus and species names but also subspecies, as taxonomists try to decide between lumping or splitting populations. Be prepared for changes. Toucan anatomy and DNA indicate a close alliance with woodpeckers (and thus they are in the same order, Piciformes), and both groups share certain characteristics of foot anatomy (two toes face forward, two face to the rear) as well as the habit of

roosting and nesting in tree cavities. Ramphastids occur in lowland moist forests and montane cloud forests. Toucans, aracaris, and toucanets range in body length from 33 to 59 cm (13–23 in). Toucans’ seemingly oversize bills are actually lightweight. The bill is supported by bony fibers beneath the outer horny surface of keratin (which is not very different from a fingernail). The upper mandible is slightly down-curved, terminating in a sharp tip. Colorful patterns adorn most ramphastid bills; they may possibly be used for signaling in mate selection. Recent studies on the Toco Toucan (Ramphastos toco; plates 15-26–27) have demonstrated that the birds are able to radiate excess heat from their long, vascularized bills. Their bills thus also function for thermoregulation. In a paper by Glenn Tattersall and colleagues, the researchers conclude that the toucan bill is “relative to its size, one of the largest thermal windows in the animal kingdom, rivaling elephants’ ears in its ability to radiate body heat.” Toucan plumage is also colorful, including patches of green, yellow, red, and white. One major group has

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Plate 15-29. Toucanets are smaller than toucans and tend to be strongly green, blending well with the foliage they inhabit. This is the Crimson-rumped Toucanet (Aulacorhynchus haematopygus), found in northwestern South America. Photo by Gina Nichol.

Plate 15-30. The Spot-billed Toucanet (Selenidera maculirostris) is one of the most distinctive of the toucanets. It is found in parts of central and southeastern Amazonia. Photo by Andrew Whittaker.

Plate 15-31. The Collared Aracari (Pteroglossus torquatus) is the most common of the aracari species in Central America. This bird has just captured a large dragonfly. Photo by James Adams.

Plate 15-32. The Pale-mandibled Aracari (Pteroglossus erythropygius) has a range limited to a small part of Ecuador. However, some authorities do not consider it to be a separate species from the widespread Collared Aracari (Pteroglossus torquatus). Debates over taxonomy are extremely common in ornithology now. Photo by John Kricher.

ebony body feathers offset by white or yellow throats and scarlet on the rump or under the tail. Most species have a colorful patch of bare skin around each eye. The Keel-billed Toucan (Ramphastos sulfuratus; plate 15-28), at 51 cm (20 in), is one of the larger species; it ranges from tropical Mexico through the upper Amazon. Both male and female look alike, a characteristic of most ramphastids. The Keel-billed Toucan has a call remarkably like that of a tree frog: preep, preep, preep. Like most toucans, Keel-bills associate in flocks of up to a dozen or more individuals. Typically, when one toucan flies, another soon follows,

and then another. A loose “string” of toucans will move from one tree to the next. Toucans are primarily frugivores, taking a wide variety of fruits from many plant genera, including Cecropia and Ficus. They show a preference for the ripest fruits, selecting black over maroon and maroon over red, the precise order of ripest to least ripe. Toucans are relatively large, heavy birds and prefer to perch on strong branches, reaching out to snip food with their elongate bills. Toucans are gulpers (chapter 10). A toucan snips off a fruit and holds it near the bill tip. It then flips its head back, tossing the fruit into its throat. Though this may

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seem awkward, the birds seem to have little difficulty. The long bill may be adaptive in permitting the relatively heavy bird to reach out and clip fruits from branch tips, which its weight would otherwise prohibit. In addition to fruits and berries, toucans eat insects, spiders, lizards, snakes, and nestling birds and eggs, all of which contain more protein than fruit. Large birds, typically in groups, toucans and aracaris are intimidating to other bird species. They easily displace other species in fruiting trees, for example. Some species of toucans bear a close anatomical resemblance and are best identified by voice; some have yelping calls and others croak. Many ornithologists and birders have noted that where two large and similar toucans co-occur, one typically is a yelper while the other is a croaker. This vocalization pattern applies, for instance, in Panama, where the Keel-billed Toucan is a croaker, and the similar Yellow-throated (formerly Chestnut-mandibled) Toucan (R. ambiguus swainsonii) is a yelper. Toucanets, represented by several genera and 14 species, are small ramphastids, many of which are primarily greenish, with rufous tails (plate 15-29). Their bills are variable and may serve for species recognition. Some, such as the Spot-billed Toucanet (plate 15-30), have extremely bright skin coloration around the eye. Aracaris (genus Pteroglossus) are about 44 cm (17.3 in) long and mostly dark in color, with banded breasts highlighted by bright yellow or orange red (plates 15-31–32). Their bills also vary from species to species. They have longer pointed tails than typical toucans. Both aracaris and toucanets are gregarious and are primarily fruit eaters. Finally, there are the four species of mountaintoucans (Andigena spp.), which occur in cloud forests. These were mentioned in chapter 13 (plate 13-12).

Neotropical Barbets The barbets of the Neotropics fall into two families: New World barbets (family Capitonidae) and prongbilled barbets (Semnornithidae). Barbets are smaller than toucans but somewhat similar in that they are colorful, frugivorous birds with prominent wide bills. There are 14 species currently listed by the AOU in the Capitonidae (though other authorities recognize 18 species, and this is another case of taxonomic flux currently ongoing in ornithology). Barbets also are

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Plate 15-33. The Red-headed Barbet (Eubucco bourcierii) is found in lowland and transitional cloud forest as well as secondary growth in northwestern South America. Photo by Nancy Norman.

Plate 15-34. The Black-girdled Barbet (Capito dayi) occurs in central Amazonia. The female is at the top of the photo, the red-capped male at the bottom. Photo by John Kricher.

found in Africa and Asia, but analysis of DNA indicates that New World barbets, African barbets, and Asian barbets are each in distinct families. New World barbets are genetically most similar to toucans. There are two genera in the family, Eubucco and Capito (plates 15-33–34). Look for these barbets in small flocks in fruiting trees. A barbet flock can be extremely territorial when defending a fruit tree, driving away larger birds such as pigeons.

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Plate 15-35. The Toucan Barbet is relatively common throughout its rather limited range in northwestern South America. Photo by Edison Buenaño.

Plate 15-36. This male Crowned Woodnymph (Thalurania colombica) is in ideal light to bring out the brilliant coloring of the gorget. Photo by James Adams.

The Toucan Barbet (Semnornis ramphastinus; plate 15-35) and its close relative the Prong-billed Barbet (Semnornis frantzii) are now placed in their own family (Semnornithidae). The Prong-billed Barbet is found in montane cloud forests in Central America. The colorful Toucan Barbet is endemic to a small area east of the Andes in Ecuador and Colombia. Also a montane species, it is found along forest edge where trees are bearing fruit.

possible for several major bird groups to specialize and feed on one or the other (or both). More is said about fruit ecology in chapter 10.

Fruit and Nectar Feeders Because of the relatively constant availability of fruit and nectar in tropical forests, many bird species of several families concentrate their diets on these resources. Throughout the tropical year there is at least some availability of both. Though seasonality exerts important effects on animal communities, it is nonetheless generally true that some plants are fruiting or flowering every month of the year. In the temperate zone, fruits tend to be abundant only from midsummer through autumn. Many birds, including migrating species, switch over from predominantly insect to fruit diets at that time. In the tropics, however, no such dramatic switch need be made. The constant availability of at least some nectar and fruit has made it

Hummingbirds: Nectarivores Nectar feeders consist mostly of hummingbirds (family Trochilidae, order Apodiformes), though many other birds, such as flowerpiercers, tanagers, and orioles, also devour nectar to varying degrees. At the present time there is no agreement as to exactly how many hummingbird species exist because, again, authorities differ in how they lump or split species. Currently, there are somewhere between 325 and 350 accepted species, depending on the authority. These small, rapid fliers are all restricted to the New World (though interestingly enough, there are fossilized remains of a hummingbird from the Old World). Most species are tropical, but 14 species do migrate to breed in North America and several other species occur there as rarities. The iridescent beauty of hummingbird plumage is reflected in the species’ names: Berylline, Emerald-chinned, Magnificent, Garnet-throated, Sparkling-tailed, and Ruby-topaz Hummingbirds, for a few examples. Among them you’ll meet jewelfronts, blossomcrowns, trainbearers, sylphs, coronets, velvetbreasts, sapphires, hillstars, firecrowns, sabrewings, spatuletails, topazes, starthroats, fairies, mangos, and racket-tails.

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Hummingbirds are highly active and fly forward and backward and hover. Hummingbirds accomplish their remarkably controlled flight both by a unique rotation of their wings through an angle of 180° and by having an extremely high metabolism. Hummingbird heart rates reach 1,260 beats per minute, and some species beat their wings approximately 80 times per second. Hummingbird metabolisms require that the birds must eat many times per day to adequately fuel their tiny bodies. Some mountain and desert species undergo nightly torpor, an adaptation to the cold temperatures of the evening. High-elevation hummingbirds are discussed more in chapter 13. Hummingbirds are both thrilling and frustrating to watch because they move so quickly. Suddenly appearing at a flower, its long bill and tongue reaching deep within the blossom to sip nectar, a bird will briefly hover, move to a different flower, hover, and zoom off. Others will come and go, and some will occasionally perch. The best way to see hummingbirds well is to observe at a flowering tree or shrub with the sun to your back so that the metallic, iridescent reds, greens, and blues will glow. In those hummingbird species that are sexually dimorphic, the male has a glittering red, green, or violet-blue throat patch called a gorget (plate 15-36). The gorget is instrumental in the male’s display behavior when he is courting females. Depending on the sun’s angle relative to the bird and the observer, the gorget may appear dull, partially bright, or brilliant and sparkling. When a male is courting, he positions himself so that the female is exposed to the gorget at its utter brightest. All hummingbirds are small. The tiniest is the Bee Hummingbird (Mellisuga helenae), endemic to Cuba, which weighs about as much as a dime. The largest, at 23 cm (9 in) long, is the Giant Hummingbird (Patagona gigas; plate 13-18) of the Andean slopes. This bird is sometimes first mistaken for a swift as it zooms past. The diversity of bill anatomy, plumage, and tail characteristics among hummingbird species represents a fine example of adaptive radiation (chapter 8). The Andean Sword-billed Hummingbird (Ensifera ensifera; plate 13-17), which lives high among Andean dwarf forests, has a body length of 13 cm (5.1 in), plus a 10 cm (4 in) long bill! This extraordinary length is a probable case of coevolution with Passiflora mixta, a flower with a very long, tubelike corolla on which the Andean Swordbill feeds. The Booted Racket-tail (Ocreatus underwoodii; plate 15-37), also a cloud forest dweller,

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Plate 15-37. The Booted Racket-tail (Ocreatus underwoodii) is a hummingbird of the highlands, ranging from Venezuela, Colombia, and Bolivia to Ecuador and Peru. Here it hovers as it feeds at a flower cluster. Photo by Nancy Norman.

Plate 15-38. The male Crimson Topaz is one of showiest of the hummingbirds. Photo by Andrew Whittaker.

Plate 15-39. The 6.5 cm (2.5 in) Rufous-crested Coquette frequents forest edges and cleared areas in northwestern South America. Coquettes are among the smallest of the hummingbirds. This is a male. Photo by Andrew Whittaker.

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Plate 15-41. This Booted Racket-tail (Ocreatus underwoodii) has come to a feeder at a lodge in Ecuador. Photo by John Kricher.

Plate 15-40. Long-billed Hermit (Phaethornis longirostris). Photo by James Adams.

Plate 15-42. Even the spectacular Sword-billed Hummingbird is commonly attracted to feeders. Photo by Gina Nichol.

Plate 15-43. This Shining Sunbeam (Aglaeactis cupripennis) was attracted to clusters of hummingbird feeders situated at various places along a mountainside trail near Quito, Ecuador. Placement of such feeders makes it much easier to obtain good views of montane hummingbirds and, of course, supplies nutrition to the birds. Photo by John Kricher.

has two long central tail feathers with bare shafts but feathered tips, somewhat like those of a motmot. The Crimson Topaz (Topaza pella; plate 15-38), a rain forest species from northeastern Amazonia, often found along watercourses, is one of the most colorful examples of a very colorful group. The Rufous-crested Coquette (Lophornis delattrei; plate 15-39), another standout, is one of several species of very small hummingbirds. Though most hummingbirds are brilliantly colored, not all are. The subfamily Phaethornithinae includes

the 34 hermit and barbthroat species, some of the commonest hummingbirds of lowland forests. Most are greenish brown with grayish or rufous breasts. Unlike most hummingbirds, in which males are brighter than females, hermits have similar sexes. All hermits have a black line bordered by white through the eyes and a long, often down-curved bill (plate 15-40). Hermits inhabit the forest understory and edge, and their more subdued plumage seems to fit well with the dark forest interior. Male Long-tailed Hermits (Phaethornis

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Plate 15-44. The Red-crested Cardinal (Paroaria coronata) is representative of the difficulties currently arising in common name nomenclature of Neotropical bird species as classifications change due to genetic analysis. Once placed within the Cardinalidae, it is now classified within the family Thraupidae, the tanagers, along with five other species bearing the common name “cardinal.” Photo by Steve Bird.

Plate 15-45. There are 30 seedeater species in the genus Sporophila. This is a male Variable Seedeater (Sporophila corvina), a species that ranges from Central America to northwestern South America. Photo by John Kricher.

superciliosus) are both abundant and vocal throughout Central and South America. Males gather in courtship areas called leks (see “Manakins,” later in this chapter) and twitter vociferously at one another as each attempts to entice a passing female. Hummingbirds are attracted to red, orange, and yellow flowers, and a single flowering tree or shrub may be a food resource for several species. When a tree is abundant with flowers, it is neither economical nor practical for a single hummingbird to try to defend it from others. Nonetheless, hummingbirds are generally pugnacious, and it is easy to observe both intra- and interspecific aggression among hummingbirds as they jockey for a position at their favorite flower. This competition is exacerbated because, though a plant may have many flowers, very few may be nectar rich. Some hummingbirds are highly territorial, defending a favored feeding site. Others, including some of the hermits, seem to circulate along a regular route visiting several flowers; these are called trapliners. It is often possible to observe hummingbirds well at flowering plants that attract them. Just enjoy the ongoing show as various species come and go. You will likely observe lots of agonistic behavior as the various individuals contest for access to the flowers. Many tropical lodges and restaurants now put out hummingbird feeders, so it is possible to sit on a comfortable deck with some good coffee and enjoy the various species as they come around (plates 15-41–43).

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Tanagers are an evolutionarily diverse and taxonomically complex group of unusually colorful, small perching birds, many of which are the highlight of any visit to the Neotropics. Tanager, like the word toucan, comes from the Topi Indian language of Brazil. Tanagers are a huge and ongoing conundrum in avian taxonomy, often expressed tongue-in-cheek, even by the experts, with the question “What is a tanager?” They are part of a major, complex, recent, and rapid evolutionary diversification of passerine (perching) birds. Some species traditionally classified as tanagers are no longer considered part of the group, while other species that were never included have now been moved into the tanager family (Thraupidae). Older field guides to birds of the Neotropics do not reflect this new positioning. Many bird species now assigned to the Thraupidae are not “tanagers” in the traditional meaning of the word. Some are cardinals (plate 1544), dacnises, honeycreepers, conebills, flowerpiercers, bush-tanagers, sierra-finches, diuca-finches, warblingfinches, inca-finches, grass-finches, seedeaters (plate 15-45), and Darwin’s finches (the latter group confined to the Galápagos Islands). On the other hand, the four “tanager” species (and they are still thus named) that migrate to breed in North America (Scarlet, Summer, Western, and Hepatic) have recently been reclassified and are no longer considered to be actual tanagers.

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Plate 15-46. The well-named Silver-throated Tanager (Tangara icterocephala) is common along forest edges in montane areas in northwestern South America. Photo by Gina Nichol.

Plate 15-47. The Green-headed Tanager (Tangara seledon) is but one of many remarkably colorful tanager species in its genus. This species is often encountered in clearings and gardens while feeding on fruiting plants. Photo by Andrew Whittaker.

Plate 15-48. The striking and well-named Red-necked Tanager (Tangara cyanocephala) occurs in Brazil, Argentina, and Paraguay. Like other species of its genus, it is highly colorful. Photo by Andrew Whittaker.

Plate 15-49. The widely distributed Blue-gray Tanager has adapted to towns and is very common wherever there is some fruit to be had. This one likes bananas. Photo by Gina Nichol.

They are now placed in the family Cardinalidae. That means that all actual tanagers in the world are confined to the Neotropics. The family Thraupidae now conservatively consists of 300-plus species, about 150 of which are actually called, with current accuracy, “tanagers.” This section features them. Most tanager species are brilliantly colored and feed on fruit (they are mashers, chapter 10), nectar, and insects. Tanagers are found from lowland forests to high montane and cloud forests. They are particularly common around forest edge habitats and are often easy to see at fruiting figs, palms, cecropias, and other trees. The common names of tanager species reflect

their multicolored, exotic feather patterns. One may encounter the Crimson-collared, Saffron-crowned, Flame-colored, Blue-and-gold, Golden-hooded, Silverthroated, and Emerald Tanagers, a list that is far from exhaustive. In most, but not all, of the Neotropical tanager species, males and females are equally colorful. Many tanagers form mixed-species flocks and forage together, primarily in montane areas but also in lowlands. Tanager flocks seem to prefer forest edge. It is particularly satisfying to see groups of such colorful species mixed together. Indeed, the high species richness of tanagers, particularly in the genera Thraupis and Tangara (plates 15-46–48), is testimony

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to the uniqueness of avian evolution in the Neotropics. One of the most common and widely distributed birds of the tropics is the Blue-gray Tanager (Thraupis episcopus; plate 15-49), which is well described by its name. Tanagers devour both fruit and arthropods, and though the various species in a mixed foraging flock appear to the casual observer to be feeding in much the same manner, studies have suggested that species do specialize their foraging in various ways, perhaps reducing the potential for interspecific competition. For example, some species are most commonly observed in the canopy, while others forage lower. Even their various behaviors, as they glean insects or select fruit, vary among species. Nonetheless, many species forage heavily on various Miconia species (Melastomataceae) and mistletoes (Loranthaceae). Cloud forests provide habitat for a group of colorful and robust tanagers called mountain tanagers. They are often seen in mixed flocks with other tanagers and, like many tanager species, can be attracted to bird feeding trays that offer fruit. The Blue-winged Mountain Tanager (Anisognathus somptuosus; plate 15-50) is one representative of this group. Honeycreepers (plates 15-51–52), which include dacnises and conebills, are nectarivorous, though they also include ample amounts of fruit and arthropods in their diets. Warbler-size, they have fairly long, downcurved bills. Some tanagers, such as the ant-tanagers (genus Habia), are army ant followers, and many other tanagers, including honeycreepers, move with antbirds, woodcreepers, and other species in large mixed foraging flocks. Studies by Charles Munn and John Terborgh have revealed the high diversity and intriguing complexity of behavior within both canopy and understory mixed-species flocks in the Peruvian Amazon. Each flock type consists of a core of five to 10 different species, each represented by a single bird, a mated pair, or a family group. Up to 80 other species join flocks from time to time, including 23 tanager and honeycreeper species, a remarkably high diversity. Mixed foraging flocks occupy specific territories, and when another flock is encountered, the same species from each flock engage in “singing bouts” and displays as boundary lines are established. Adult birds tend to remain flock members for at least two years. Nesting occurs in the general territory of the flock, the nesting pair commuting back and forth from nest to flock.

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Plate 15-50. Blue-winged Mountain Tanager. Photo by Andrew Whittaker.

Plate 15-51. The Purple Honeycreeper (Cyanerpes caeruleus) is found from southern Central America (Panama) through Amazonia. This bird is a male. Photo by James Adams.

Plate 15-52. The Green Honeycreeper (Chlorophanes spiza) is widely distributed throughout the Neotropics and is common in open habitats and gardens. This bird is a male. Most honeycreepers are smaller than the Green. Photo by James Adams.

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Plate 15-53. A Hyacinth Macaw (Anodorhynchus hyacinthinus) pair from the Brazilian Pantanal, where this magnificent species remains relatively common. Photo by John Kricher.

Plate 15-54. The Yellow-chevroned Parakeet (Brotogeris chiriri), shown here, and the similar Canary-winged Parakeet (Brotogeris versicolurus) are commonly observed in sizeable flocks throughout Amazonia. Photo by Nancy Norman.

Plate 15-55. This White-eyed Parakeet (Psittacara [Aratinga] leucophthalma) is not alone in this mango tree. There are others deeper in the dense foliage. Observers are often surprised by how many more parrots than they think are in a fruiting tree will come flying out of it. Photo by John Kricher.

Plate 15-56. Red-fan Parrots (Deroptyus accipitrinus) allopreening each other. It is not possible to tell males from females by sight. These large and colorful parrots are fairly common in lowland forests in parts of northeastern and central Amazonia. The “fan” of feathers on the nape may be raised in display. Photo by Andrew Whittaker.

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Parrots Like toucans, parrots are quintessentially tropical, but they are global in distribution; 374 species occur mainly in tropical forests of the Southern Hemisphere. In the Neotropics, 136 species of the family Psittacidae (order Psittaciformes) can be found, ranging from the spectacular large macaws (genera Ara, Cyanoliseus, Anodorhynchus; plate 15-53) to the sparrow-size parrotlets (genus Forpus). Among the most commonly encountered of the New World parrots are the chunky, short-tailed amazons (most in the genus Amazona). There are also moderate-size, long-tailed parrots known collectively as parakeets (plates 15-54–55). Many parakeets are in the genus Aratinga. Parrots are mostly green (though there are some dramatic exceptions) and can be remarkably invisible when perched in the leafy forest canopy, quietly and methodically devouring fruits. Parrots often reveal their presence by vocalizing, usually a harsh screech or squawk. No parrot is naturally melodious. Indeed, the large macaws commit a bit of an assault on the ears, such is the harshness of their squawks. Often a parrot flock will suddenly and unexpectedly burst from a tree like shrieking banshees. With few exceptions, there is little or no difference in plumage between the sexes in parrots (plate 15-56). Parrots are gregarious; it is uncommon to find only one or two, though large macaws may occur in such numbers (plate 15-57). Flocks move about in forests and savannas searching out fruits (parrots are mainly frugivores), flowers, and occasionally roots and tubers. Parrots climb methodically around the tree branches, often hanging in awkward acrobatic positions as they attack their desired fruits. The sharply hooked, hinged upper mandible is used in climbing around in trees as well as in scraping and scooping out large fruits. Using their strong nutcracker-like bills, parrots can crack many of the toughest nuts and seeds, which they eat with equal relish as the pulpy fruit itself (plate 1558). Their tongues are muscular, and they are adept at scooping out pulp from fruit and nectar from flowers. Because of their ability to crush and digest seeds, parrots are primarily seed consumers rather than seed dispersers. Parrots, including some of the large macaws, often gather in large numbers along clay embankments called collpas (plate 15-59). They ingest the clay soil as an aid to digestion (discussed in chapter 6). Parrot gatherings of this sort provide a wonderful visual experience for ecotourists and birders.

Plate 15-57. The Blue-headed Parrot (Pionus menstruus) is widely distributed and common throughout the Neotropics. It is usually seen in groups. Photo by Andrew Whittaker.

Plate 15-58. Scarlet Macaw (Ara macao) methodically dismantling a fruit. Photo by Gina Nichol.

Plate 15-59. Dusky-headed Parakeets (Aratinga weddellii) at a collpa in Ecuador. Photo by John Kricher.

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Plate 15-60. Hyacinth Macaw, the largest species of flying parrot in the world. Photo by John Kricher.

Plate 15-61. A Scarlet Macaw pair in flight. Photo by Sean Williams.

Plate 15-62. Blue-and-yellow Macaws (Ara ararauna) allopreening. Photo by Andrew Whittaker.

Plate 15-63. Hyacinth Macaw emerging from nest cavity. Photo by John Kricher.

The most spectacular Neotropical parrots are the 19 macaw species, especially the larger species. These long-tailed parrots with bare skin on their faces range in plumage from the predominantly green Chestnutfronted (Ara severus), Military (A. militaris), and Great Green (A. ambiguus), to the bright red Scarlet (A. macao), and Red-and-green (A. chloropterus), to the brilliant Blue-and-yellow (A. ararauna), and the deep indigo blue of the Hyacinth (Anodorhynchus hyacinthinus; plate 15-60). Macaws are most commonly seen flying to and from their roosting and feeding sites. Their slow wing beats and long tails make them distinctive in flight (plate 15-61). Many macaws frequent gallery forests along watercourses or humid forests interrupted by open areas. They feed heavily on palm nuts, their huge bills being fully capable of crushing these dense fruits.

Parrots are exceedingly intelligent and social and live long lives, some surviving for 60 or more years. They form strong pair bonds and reinforce these bonds rather as primates do, by allopreening (plate 15-62). One bird will preen another and expect reciprocation. This behavior is similar to that of monkey and ape groups that practice constant mutual grooming. Social bonding in various parrot species is among the strongest exhibited by any group of animals. The vast majority of parrots are cavity nesters and require some sort of tree cavity in which to lay eggs (plate 15-63). Both parents are fully involved in tending the young birds to the point of fledging. Unfortunately, 42 species, or about 30% of the Neotropical parrot species, are considered to be at some risk of extinction, principally from habitat loss and/or the pet trade. One of the most threatened

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species is the Spix’s Macaw (Cyanopsitta spixii), now apparently extinct in the wild but still extant as captive populations. This species once ranged in eastern Brazil but was decimated by loss of habitat as well as human trapping. The Indigo Macaw (Anodorhynchus leari), which is very similar to the Hyacinth Macaw, is considered endangered, now found only in a very narrow range in eastern Brazil. The somewhat smaller Glaucous Macaw (Anodorhynchus glaucus) is now extinct, another victim of human persecution and habitat loss. It once ranged through southeastern Brazil, Paraguay, and Uruguay to northern Argentina. In addition to the parrots listed as threatened or endangered, many other species are in decline for the same reasons. Nest trees are cut to procure the nestlings for the pet trade. Deforestation eliminates still more nest trees. Mortality rates among parrots shipped from Latin America for the pet trade are staggering. Interest in preserving wild parrot species has increased, and it is hoped that species that have been negatively affected will rebound.

Cotingas Cotingas (family Cotingidae, order Passeriformes) are among the real glamour birds of the Neotropics (plate 15-64). With names such as bellbirds, umbrellabirds, cock-of-the-rocks, pihas, fruitcrows, and fruiteaters (plate 15-65), the 65 cotinga species make up a colorful and diverse family. Cotingas are birds of rain forests and, to a lesser extent, cloud forests, and are characterized as extreme fruit specialists. Large cotingids eat fruits of laurels (Lauraceae), incense (Burseraceae), and palms (Arecaceae, or Palmae), while smaller species eat smaller, sweeter fruits, sometimes plucking them while hovering. Cotingas typically have wide, flattened bills, shaped well for accommodating rounded fruits. Cotingas feed only on the flesh of the fruit and not the seeds and thus can be effective seed dispersal agents. Some species, such as the fruitcrows and pihas, mix insects among their fruits, but most cotingas feed exclusively on fruit. Cotingas are diverse. Some, such as the fruitcrows (plate 15-66), umbrellabirds and cock-of-the-rocks, are large and colorful or have ornate plumage, while others, such as the fruiteaters and pihas, are smaller and relatively drab. Some are sexually monomorphic, the males and females looking alike, while others represent extreme cases of sexual dimorphism. Some

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Plate 15-64. The Lovely Cotinga (Cotinga amabilis) is one of several species of cotingas of which males have strikingly blue and violet coloration. The species occurs from Mexico to Panama, and similar cotinga species are found elsewhere in lowland humid forest throughout much of the Neotropics. Photo by James Adams.

Plate 15-65. The Green-and-black Fruiteater (Pipreola riefferii) ranges over northern South America and is found in lowland forests and forest edges as it roams in search of fruit. This individual is a male. Females are more uniformly green. Photo by Edison Buenaño.

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Plate 15-66. The Red-ruffed Fruitcrow (Pyroderus scutatus) is generally uncommon but ranges widely in Amazonia and is one of the largest of the cotingas. Photo by Edison Buenaño.

Plate 15-67. The Bare-necked Umbrellabird (Cephalopterus glabricollis) of Costa Rica and Panama is a large cotinga often encountered along rivers sitting atop a high perch. This is a male. Photo by Gina Nichol.

form pairs and occupy territories, while others are highly polygynous, the cocks mating with many hens. In a few species, such as the cock-of-the-rocks (genus Rupicola), whose complex breeding behavior is detailed in chapter 10, and the Screaming Piha (discussed below), males gather to court females in mating areas called leks. Bellbirds (also discussed below) are known for their piercing bell-like call notes, pihas for their loud “screams,” cotingas for their shiny metallic plumage, cock-of-the-rocks for their golden-orange or orange-red coloration and fan of head feathers, and umbrellabirds (genus Cephalopterus; plate 15-67) for their extraordinary umbrella-like head plumes and inflatable air sac on the breast. Cotingas generally make small, inconspicuous nests, incubate but a single egg, and have a prolonged incubation period. Bellbirds typically incubate for approximately 30 days, and cockof-the-rocks for 40 or more days. This long incubation period is probably related to feeding nestlings almost exclusively fruit, which is low in protein but high in fat and carbohydrate.

rupicola), one of the “fanciest” of the cotingas, provided an example of how sexual selection may dominate a species’ evolution. But in discussing cotingas, it is worth adding a bit more about some of the most distinctively sounding birds in Neotropical forests. These include the various bellbird species and a rather nondescript cotinga with the name Screaming Piha (Lipaugus vociferans). We’ll start with the piha. The Screaming Piha is a common bird throughout much of Amazonia. Anyone walking in lowland forest will eventually be likely to hear it. Its courtship call is a short, demonstrative, ringing, loud WEE-WEEE-HAH! (with emphasis on the first two notes). Male Screaming Pihas select trees in which to display, but the display is essentially all in its voice (note its scientific name, vociferans). Male pihas distribute themselves in what are termed dispersed leks. Males do not see one another. A male will perch 5–8 m (16.4–26.25 ft) high in a tree, remain essentially motionless, and just explode with its voice. Females choose among the various calling males, presumably selecting the “voice” they like the best. Male and female Screaming Pihas look alike— nondescript, slender, robin-size birds, light gray on the face and breast and uniformly dark gray on wings, back, and tail. A piha is a far cry from a male cock-ofthe-rock. Screaming Pihas can be surprisingly hard to see, as they are so drab, and their voice is ventriloquial.

Screaming Pihas and Clanging Bellbirds Sexual selection has dominated the evolution of the cotingas. The description in chapter 10 of lekking behavior in the Guianan Cock-of-the-rock (Rupicola

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Because male and female Screaming Pihas look alike, this species would not seem to fit with Darwin’s concept of sexual selection, focused as it is on sexual dimorphism. It is with voice, however, and not looks, that a male Screaming Piha attracts a female and tells other males that he is so doing. Barbara Snow studied the Screaming Piha in Guyana and found that one male spent 77% of his time calling on the lek, usually from a thin horizontal branch well below the canopy. An excited male called at the rate of 12 times per minute. Calling clearly substitutes for plumage and display behavior as the signal to the females. Sexual selection has occurred, but for characteristics of voice, not appearance. There are numerous excellent YouTube videos of the Screaming Piha as well as other courting cotingas. Bellbirds (genus Procnias), like the Screaming Piha, rely heavily on voice as part of the courtship process. There are four species, each shaped generally like a starling, though larger in size. Bellbirds range throughout lush montane forests of Central America and northern South America. In montane populations, the birds migrate vertically, breeding in highland forests and moving downslope to lowland forests when not breeding. Unlike pihas, bellbirds are sexually dimorphic, the males having much white on the body along with ornate wattles about the head. In one species, the White Bellbird (P. albus), the male is entirely white with a fleshy wormlike wattle dangling from its face above the bill. The male Bare-throated Bellbird (P. nudicollis) is almost all white but has bare blue skin on the throat and face around the eyes. The male Bearded Bellbird (P. averano; plate 15-68) has black wings and a chestnut head with a heavy “beard” of black fleshy wattles hanging from its throat. The male Three-wattled Bellbird (P. tricarunculatus) is chestnut on body, tail, and wings but has a white head and neck and three fleshy wattles hanging from the base of the bill. Females of all four species are similar: greenish yellow, darkest on the head, with streaked breasts. Male bellbirds establish calling and mating territories in the forest understory. Though not true leks, bellbird courtship territories are closely spaced together. Each male spends most of his time in his territory vocalizing to attract females. Males take no part in nest building, incubation, or raising young. The Bearded Bellbird in Trinidad and the Three-wattled Bellbird in Panama are both well studied; they court in a generally similar manner.

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Male Bearded Bellbirds vocalizations are among the first sounds one hears upon entering the Arima Valley in Trinidad. David Snow aptly described their call as a loud bock! A muted clang with a bell-like quality, the call carries amazingly well, and most observers, including me, when first hearing them think the birds are nearby, though they may be half a kilometer (0.25 mi) or more away. Even when very close to a calling male, it can be frustratingly difficult to locate him in the forest understory. Males initially call from a perch above the canopy, often a dead limb, but will drop down into the understory to complete the courtship. Females never call, and it is clear that male vocalizations are an essential part of sexual selection in bellbirds. The object of calling is to attract a female to the male’s territory. Each male bellbird has his own courtship

Plate 15-68. This male Bearded Bellbird “bocks” (vocalizes) in the understory on its display perch. Photo by Jill Lapato.

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Plate 15-69. The multicolored male Pin-tailed Manakin (Ilicura militaris) is found in humid forests in southeastern Brazil. Photo by Andrew Whittaker.

Plate 15-70. The White-collared Manakin (Manacus candei) is found mostly in Central America. This is a male. Photo by James Adams.

site in the forest understory. The male “bocks” fairly continuously, mixing the bocking with a series of dry but loud tock, tock, tock notes. If successful in luring a female to his territory, the male initiates a series of courtship postures, performed from a horizontal branch upon which the female perches as his only audience. These postures include display of the beard wattles, a wing display, and a display in which a bare patch of skin on the male’s thigh is revealed. All bellbird species include a jump display as part of courtship. A cock Bearded Bellbird will leap from one perch to another, landing before the hen with his body crouched, tail spread, and eyes staring at her. You can guess what happens next, assuming the male has performed satisfactorily. Outstanding films of courting Bearded Bellbirds, many taken at the Asa Wright Nature Centre in Trinidad, are readily available on YouTube. Or you could just go to Trinidad.

not true manakins but are taxonomically somewhere between cotingas, tyrant flycatchers, and manakins. Manakins have short tails, rounded wings, and a short but wide bill with a slightly hooked tip (plates 15-69–70). Males of most species are colorful; females are drab, olive green and yellowish. Manakins pluck small fruits (often from Miconia species) on the wing, supplementing their largely frugivorous diets with occasional arthropods. Manakins are polygamous; as a result, only females build the nest, incubate, and feed young. Clutch sizes are typically small, one to two birds per nest. Manakins, like cock-of-the-rocks, exhibit elaborate courtship displays (described in chapter 10). Many manakin species are “arena birds,” meaning they court in concentrated areas called leks, assemblages of males that display to interested females. Others court in dispersed leks, while still others have a cooperative courtship behavior in which several males display together in an extraordinarily coordinated manner virtually unknown in other bird families.

Manakins There are 58 species in the manakin family (Pipridae), a group of small, chunky fruit-eating birds, most of which inhabit lowland forests. Manakins are endemic to the Neotropics and should not be confused with mannikins, an Old World group of birds of the estrildid finch family. Neotropical manakins are close evolutionary cousins of the cotingas and tyrant flycatchers, and recent taxonomic analysis has suggested that “manakins” of several genera (e.g., Schiffornis) are

Many Bugs, Many Bird Species One key factor leading to the diversity and adaptive radiation of some groups of Neotropical land birds is that they are arthropod feeders, and arthropods, particularly insects, are really diverse in the Neotropics.

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Indeed, the “bird supermarket” is well stocked with a wide range of chitin-covered choices. Arthropods range in size from tiny to noticeably large (think gnats compared with tarantulas). That expansive size range matters because it presents a broad food resource spectrum. Eating insects and other arthropods per se does not cause speciation, but it does accommodate increasing avian diversity, because such a broad resource spectrum promotes specialization. No species eats both gnats and tarantulas. Insects and other arthropods don’t want to be eaten by birds. These prey animals require finding, and that requires a search image. Arthropods require catching, and that requires a foraging technique. As described in chapter 11, arthropods are well adapted to avoid predation through either cryptic or warning coloration or escape behavior (plate 15-71). Each insecteating bird tends to develop a particular behavioral repertoire employed in finding, catching, and feeding, and the bird’s size, behavior, and bill shape evolve to focus on a particular size range and type of prey. Prey characteristics provide major selection pressures in shaping evolution among avian predators. Bird species compete against one another. The presence of many insect-eating species cohabiting a complex ecosystem generates continuous low-level (also called diffuse) competition within a species assemblage, keeping each species ecologically adapted to doing what it alone does best. Insect eaters can be roughly categorized by overall feeding method. These are: (1) fly-catching (tyrant flycatchers, puffbirds, and nunbirds), (2) bark probing and drilling (woodcreepers and woodpeckers), (3) foliage gleaning (ovenbirds and many antbirds), and (4) ant following (some antbirds and others).

Plate 15-71. This Peacock Katydid (Pterochroza ocellata), normally cryptic (its body mimics a leaf), is here in full display, not to attract a mate but rather to thwart a potential avian predator, nature’s version of “shock and awe.” Photo by Sean Williams.

Puffbirds and Nunbirds: Just Sit and Wait . . . and Wait Puffbirds and nunbirds make up the family Bucconidae, of which there are 35 species. They are most closely related to jacamars and woodpeckers, and all are exclusively Neotropical. They feed primarily on insects captured by darting from a perch and snatching the prey from a branch or the ground, a foraging behavior termed a sally strike. And they are patient about it, to the point of being called “lethargic” by some observers. These birds will perch (depending on species) from understory to canopy and remain essentially motionless as they patiently sit and wait for potential prey.

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Plate 15-72. The Black-fronted Nunbird. Photo by Sean Williams.

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Plate 15-73. Head of a Spotted Puffbird (Bucco tamatia) showing the long rictal bristles and formidable bill. Photo by Andrew Whittaker.

Plate 15-74. A pair of White-necked Puffbirds (Notharchus macrorhynchos). The species ranges from Mexico to Argentina. Photo by Kevin Zimmer.

Plate 15-76. The Semicollared Puffbird (Malacoptila semicincta) is a rain forest species of limited range in western Amazonia. Photo by Sean Williams.

Plate 15-75. The Collared Puffbird (Bucco capensis) is widespread in Amazonia. Photo by Sean Williams.

Plate 15-77. The Swallow-wing (also called Swallow-winged Puffbird) (Chelidoptera tenebrosa) is the only puffbird that is an aerial forager, catching flying insects in the air. It typically sits on an exposed perch and is easy to observe. The species occurs throughout Amazonia, usually in open clearings or forest edges. Photo by Sean Williams.

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The Black-fronted Nunbird (Monasa nigrifrons; plate 15-72) ranges throughout the Amazon Basin. This ubiquitous, robin-size, forest-dwelling bird is often revealed by its bright red bill as it perches on an understory branch. Nunbirds will form noisy groups and typically join large mixed-species foraging flocks. Some nunbird species follow army ant swarms. Puffbirds (plates 15-73–77), which feed like nunbirds, are large-headed, heavy-bodied birds so named for the puffed appearance of their feathers. Though some species are boldly patterned in black and white, most species, particularly those that inhabit shaded understory, are brownish or tan. Their cryptic plumage plus their stationary behavior when perched in the shaded forest understory makes them easy to overlook. Like flycatchers (chapter 8), puffbirds have large bills with prominent rictal bristles (hairlike feathers around the base of the bill; plate 15-73) that probably aid in capturing aerial insects). Nunbirds and puffbirds excavate nests in termite mounds or in the ground, depending upon species. Rather little is known about the details of their breeding biology, but they do form strong pair bonds, and many species are commonly observed in pairs.

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Plate 15-78. The House Wren is a common bird around houses and gardens throughout its extensive range. This one was in a hotel garden in Panama. Photo by John Kricher.

Wrens There are 85 species of wrens in the world and 84 of them are found only in the New World. Wrens (family Troglodytidae) obviously evolved in the New World and they have an impressive diversity, occurring in all major terrestrial habitats other than arctic tundra. Wrens include the familiar House Wren (Troglodytes aedon; plate 15-78), the most broadly distributed species of wren in the Americas, ranging from Canada to southern Chile and Argentina. Wrens are fundamentally insectivorous and many species are skulkers, remaining in the well-shaded forest understory, a challenge to observe. Wrens are well known for their remarkable ability to sing highly complex songs. There are 48 wren species in South America, and several among them are simply amazing singers. One of those is the wellnamed Musician Wren (Cyphorhinus arada; plate 1579). Often part of mixed-species flocks and always in the understory, the Musician Wren will spontaneously begin to sing its complex song, which seems to oscillate in pitch. You just have to hear it (which you can do on YouTube).

Plate 15-79. Though rather nondescript in plumage, the Musician Wren is anything but dull in its singing ability. This one is upright and singing; it is difficult to get such a clear look as this. Photo by Andrew Whittaker.

Plate 15-80. The songs of the White-breasted Wood-Wren and other similar wren species are among the most often heard sounds in Neotropical rain forests. Photo by Dennis Paulson.

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Plate 15-81. The White Woodpecker (Melanerpes candidus) is one of many distinctive woodpecker species found in the Neotropics. Social groups of White Woodpeckers can be observed in the Brazilian Pantanal as well as other areas in southern Amazonia. Photo by John Kricher.

Plate 15-82. The Crimson-crested Woodpecker (Campephilus melanoleucos), which ranges throughout Amazonia, shows the typical woodpecker foraging posture while it clings vertically to the tree. At 36 cm (14 in) long, it is the secondlargest woodpecker species in South America. The largest is the Magellanic Woodpecker (C. magellanicus), which reaches 43 cm (17 in). But the Magellanic is found only in temperate Nothofagus (southern beech) forests in southernmost areas of Chile and Argentina, near Tierra del Fuego. The bird in the photo is a female. Photo by Nancy Norman.

Plate 15-83. Piculets are chickadee-size woodpeckers that often assume acrobatic postures as they forage. This is the Grayish Piculet (Picumnus granadensis), found in northwestern South America. Most piculet species occupy limited ranges. Photo by Gina Nichol.

Plate 15-84. The Spotted Piculet (Picumnus pygmaeus) of eastern Amazonia is one of 25 piculet species found in South America. Photo by Andrew Whittaker.

The White-breasted Wood-Wren (Henicorhina leucosticta; plate 15-80) is another species often heard in the Neotropics. Some tropical wren species are duetting singers, males and females both singing in close proximity so that the sound appears to be one song. Wrens forage in pairs and usually remain close together in the understory, and duetting presumably helps the two remain aware of each other’s location. Some wrens are rather large, reaching lengths of up to 22 cm (8.6 in), and some of these are found along forest edge or arid scrub and around cultivated areas. They are much easier to observe than the forest skulkers. Some, like the Striped-backed Wren (Campylorhynchus nuchalis), are extensively striped with black. The most distinctive of the large wrens may be the White-headed Wren (C. albobrunneus). It has a white head, breast, and belly, and black wings, back, and tail, making it quite unmistakable.

Bark Drillers: Woodpeckers There is a lot of wood available in a tropical forest, so it is little surprise that the Neotropics host nearly 100 species of woodpeckers (family Picidae, order Piciformes). These birds probe and drill bark, extracting insects, mostly larval, by using their long, barbed tongues. They

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hitch vertically up tree trunks, their bodies supported by stiff tail feathers that act as a prop (plate 15-81). Woodpeckers, of which there are 254 species, occur globally (except Australia and Antarctica) wherever there are trees, and, thus many are temperate-zone species. However, both the size range and the species richness of woodpeckers are highest in the tropics, where they vary in size from the 36 cm (14 in) ivorybilled types (Campephilus spp.; plate 15-82) to the diminutive, 9 cm (3.5 in) piculets (Picumnus spp.; plates 15-83–84). Neotropical woodpeckers range in color from bold black with a red crest, to greenish olive, to soft browns and chestnut (plates 15-85–86). Some species have horizontal black and white “zebra” stripes on their backs and varying amounts of red on the head. Neotropical woodpeckers excavate roosting and nesting cavities that are sometimes usurped by other species. Alexander Skutch, famous for his detailed accounts of nesting tropical bird species, observed a group of Collared Aracaris (Pteroglossus torquatus) evict a pair of Pale-billed Woodpeckers (Campephilus guatemalensis) from their nest cavity.

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Plate 15-85.

Anis and Cuckoos Anis and Cuckoos (family Cuculidae) are, like woodpeckers, globally distributed, occurring on all continents except Antarctica. Most of the 149 species are found in the tropics, and most of those are in the Australasian tropics. The 23 species found in South America are an interesting and diverse lot. All cuckoos feed on various animals, ranging from arthropods to small vertebrates. Anis are easy to see, but many species of forest cuckoos tend to be furtive. They vocalize often but are difficult to locate in the foliage. It is difficult to visit the tropics without seeing groups of anis, iridescent black birds with long, loosely held tails and prominent, hawklike black beaks. Three species occur, each widely distributed. The Smoothbilled Ani (Crotophaga ani; plate 15-87) and the Groove-Billed Ani (C. sulcirostris) are typically found in disturbed roadside habitats and farmland, and the Greater Ani (C. major), the largest, is characteristic of wetland areas and river edges. Anis nest cooperatively in groups, and several females contribute their eggs to the same nest. Among the most social birds of the family is the Guira Cuckoo (Guira guira; plate 15-88), which typically associates in groups of about 10 or more

Plate 15-86. Plates 15-85 and 15-86. Two richly colored members of the tropical genus Celeus. The Chestnut Woodpecker (C. elegans; 15-85) is widely distributed throughout Amazonia, usually in várzea and gallery forests. The Waved Woodpecker (C. undatus; 15-86) occurs in northeastern South America. Females are shown. Photos by Andrew Whittaker.

Plate 15-87. Two Smooth-billed Anis. Photo by John Kricher.

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Plate 15-88. Guira Cuckoos are known for their sociality. Photo by John Kricher.

Plate 15-89. A Squirrel Cuckoo in the open. Photo by Jill Lapato.

Plate 15-90. The Rufous-vented Ground-Cuckoo (Neomorphus geoffroyi) is not an easy bird to observe, but here, at an ant swarm in Panama, it stood for its portrait with its prominent tail cocked. Photo by Kevin Zimmer.

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Plate 15-91. The Nacunda Nighthawk, which measures 30 cm (12 in) long and has a white belly and prominent white wing patterning, is one of the largest and most distinctive of the South American nighthawks. It often flies during the day and roosts in the open. Photo by John Kricher.

Plate 15-92. The 35 cm (14 in) Common Potoo (Nyctibius griseus) in daytime “tree snag” posture. Note that its offspring instinctively adopts the same posture. Both birds are sleeping. Photo by James Adams.

Plate 15-93. The Great Potoo (Nyctibius grandis), here photographed at night from its song and hunting perch, is 52 cm (20.5 in) long. Both the Common and Great Potoos are widely distributed in Central and South America. Photo by Andrew Whittaker.

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birds. The species, easily observed, occurs in savanna habitats and open areas and is common around human habitations. It is found in eastern and south-central Amazonia and is common on the Brazilian Pantanal. This brown, shaggy-crested bird with bright orangy eyes has a somewhat primeval look to it. With luck, most birders get to see the large (47 cm/18.5 in) and colorful Squirrel Cuckoo (Piaya cayana; plate 15-89). The species ranges throughout the Neotropics and inhabits various kinds of forests and edge habitats. Like other cuckoos it tends to stay hidden, but with patience and luck it is possible to get a good look at it nonetheless. The largest of the Neotropical cuckoos are the five species of ground-cuckoos (plate 15-90). Each is about 50 cm (nearly 20 in) in length. Ground-cuckoos do occasionally fly but the name is well chosen as they spend the majority of their time on the shaded forest floor, often accompanying army ant swarms. They are notoriously difficult to find and to see well.

Potoos, Nighthawks, and Nightjars Many insects, particularly moths, are nocturnal. Two closely related groups of birds, the potoos (family Nyctibiidae) and the nighthawks and nightjars (family Caprimulgidae), have each adapted to catching and consuming nocturnal insects. (Also recall that these

Plate 15-94. The cryptic plumage of the Ladder-tailed Nightjar (Hydropsalis climacocerca) is typical of nightjars. Males of this and several other nightjar species have elongated central tail feathers, a sexually selected characteristic. Photo by Sean Williams.

birds are closely related to the Oilbird, described in chapter 10.) Five potoo species and 30 nighthawk and nightjar species occur in South America. All are cryptically colored birds, and most nest and roost on the forest floor, where they are difficult to spot because of their crypsis. All species have large eyes and large mouths with long rictal bristles that enable them to find, capture, and eat their nocturnal flying prey. Various species are sometimes seen around streetlamps and other lights where flying insects are apt to congregate. The Nacunda Nighthawk (Chordeiles nacunda; plate 15-91) is unusual in that it is often seen flying in daylight. Potoos (also discussed in chapters 4 and 11) roost and nest in tree branches, and due to their plumage and posture, bear a remarkable resemblance to a tree snag when roosting (plates 15-92–93). Potoos, like nightjars, vocalize at night, and show an amazing range of “song,” from a haunting whistle-like series of notes to extremely loud, harsh growling snarls, depending upon species. Nighthawks and nightjars may be found in a wide range of habitats from interior forest to savanna to sandbars in rivers (plates 15-94–95). But one way to see these birds is to go out at night and look on and along roads, particularly gravel roads. Active birds will often land on or beside roads and the birds will display prominent eyeshine. Close approach is often possible.

Plate 15-95. A Nacunda Nighthawk relaxing on the Brazilian Pantanal and seemingly unconcerned about being rather obvious on the green grass. Photo by John Kricher.

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Suboscine and Oscine Birds: Neotropical Uniqueness By far the largest bird order is the Passeriformes, perching birds, of which there are 5,899 species, representing about 60% of all extant bird species. Of this assemblage, 1,263 are within a group classified taxonomically as suboscines. This is of interest because there are 1,213 species of suboscine birds in the Neotropics and only 50 suboscine species in all of the rest of the world. Thus the Neotropics are unusual in harboring so many members of this group. Most passerines in the world are true oscines, or songbirds, which have a complex musculature of the syrinx (the avian voice box, located in the bronchial area), the part of the trachea that produces elaborate, complex sounds, such as the flutelike songs of various thrushes (plate 15-96) and solitaires and the sweet whistle of an oriole. Suboscines are different. These birds have a much less complex syringeal musculature and thus have far more limited singing abilities than true oscines. In addition, true oscines typically learn and refine their songs, whereas the simple vocalizations of most suboscine species (except for some cotingas) are not learned—they are innate. Neotropical suboscines have undergone two major adaptive radiations, with the tyrant flycatchers, cotingas, and manakins representing one, and the ovenbirds (including woodcreepers), antbirds, antthrushes, antpittas (plate 15-97), gnateaters, and tapaculos representing the other. No one knows why suboscines have fared so well in the Neotropics, but the reason simply may be historical. The tyrant flycatchers are discussed in chapter 8, and the cotingas and manakins are discussed earlier in this chapter. Now it is time to look at some other suboscines. There are 296 species of ovenbirds and woodcreepers (Furnariidae), 217 species of typical antbirds (Thamnophilidae), 12 species of antthrushes (Formicariidae) and 51 species of antpittas (Grallariidae), as well as 410 species of tyrant flycatchers (Tyrannidae). Of the above groups, only a few of the tyrannids venture to North America to nest. All others are entirely Neotropical.

Plate 15-96. The Rufous-bellied Thrush (Turdus rufiventris), which happens to be the national bird of Brazil, is a fine example of an oscine passerine. Like all thrushes, it has an excellent singing voice (and often sings in early morning before first light), a reason it is much loved by Brazilians. Photo by John Kricher.

Plate 15-97. The Chestnut-naped Antpitta (Grallaria nuchalis) is a suboscine that ranges from Colombia to Peru. It has a simple and short song. Like other antpittas, it is a forest understory species that feeds heavily on insects and other arthropods. Photo by Steve Bird.

Furnariids: Ovenbirds and Woodcreepers Ovenbirds (family Furnariidae, order Passeriformes) are the “little brown birds” of the American tropics, their plumage typically a mixture of brown, tan, buffy,

Plate 15-98. The plumage of the Rufous-fronted Thornbird (Phacellodomus rufifrons) is, like that of virtually all members of the large family Furnariidae, a study in brown. Photo by John Kricher.

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or grayish (plate 15-98). Identification of individual species can be a challenge since differences among species are often subtle. This highly diverse family occurs not only in lowland forests but also, like the tyrant flycatchers, in all types of habitat ranging through cloud forest, Patagonian pampas, Andean páramo and puna, and coastal deserts and seacoast. Many kinds of furnariids, especially the spinetails, are common along forest edge and disturbed areas, and many are found in dry forests. The family takes its common name, ovenbird, from several species (most notably the horneros, genus Furnarius; plates 15-99–100) that construct oven-like, dome-shaped mud nests, but by no means do all furnariids build such structures. Some species nest in natural cavities or in mud banks, and some make basket-like structures of twigs and grass. The thornbirds (genus Phacellodomus) construct large and conspicuous globular nests of sticks that are easy to see in dry forest (plate 15-101). Ovenbird species have among the oddest common names of any birds. One may encounter a xenops, a recurvebill, a foliage-gleaner, and a leaftosser. There are also woodhaunters, treehunters, treerunners, palmcreepers, and earthcreepers (not to be confused with streamcreepers). There are barbtails, spinetails, titspinetails, softtails, and thistletails (not to be confused with prickletails). Finally, there are thornbirds, miners, cinclodes, horneros, canasteros, and more. Birders need patience and skill to sort out ovenbirds, as they are a challenging group. All ovenbird species are basically insectivorous. Species tend to be habitat and range specific and develop specialized feeding behaviors. Some, like the groundfeeding leaftossers, systematically probe among the litter. Others, like the slender foliage-gleaners, search actively among the leaves, ranging throughout canopy and understory (plate 15-102). Spinetails, often hidden in dense vegetation, dart quickly from bush to bush (plate 15-103). The small xenopses hang chickadeelike while searching the underside of a leaf. Ovenbirds of various species are often members of mixed foraging flocks. Woodcreepers were once placed in their own family, the Dendrocolaptidae, but are now grouped as a subfamily within the Furnariidae. They look superficially like woodpeckers, particularly their vertical posture supported by rigid tail feathers, but the two groups share no close evolutionary relationship (plate 15-104). The anatomical similarity between woodcreepers and

Plate 15-99.

Plate 15-100. Plates 15-99 and 15-100. Rufous Hornero (Furnarius rufus; 15-99) and a hornero nest (15-100). This type of nest gives the Furnariidae family its common name, the ovenbirds. Photos by John Kricher.

Plate 15-101. The large nest of the Rufous-fronted Thornbird. The thornbird pair is seen to the upper left. Photo by John Kricher.

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Plate 15-102. The small (16.5 cm/6.5 in) Scaly-throated Foliagegleaner (Anabacerthia variegaticeps) occurs in low-elevation forests on the western slope of the Andes. Here it is shown doing what foliage-gleaners do, methodically searching epiphytes for potential food items. Photo by Jill Lapato.

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Plate 15-103. Spinetails are frequently difficult to observe, as they inhabit thick foliage, but they are worth the patience and effort it takes to see them well. This is the White-whiskered Spinetail (Synallaxis candei) of northern South America. Photo by Andrew Whittaker.

Plate 15-105. A Wedge-billed Woodcreeper being held for bird banding. The species occurs in lowland humid forests throughout Central America and much of Amazonia. Photo by John Kricher.

Plate 15-104. The 30 cm (12 in) long Great Rufous Woodcreeper (Xiphocolaptes major) is one of the largest of the woodcreeper species and shows clearly the anatomical resemblance between this group and the woodpeckers. It is found in gallery and dry forests in central Amazonia. Photo by Andrew Whittaker.

Plate 15-106. The Brown-billed Scythebill (Campylorhamphus pusillus) is found in parts of Central America and northwestern South America. Photo by Bruce Hallett.

Plate 15-107. The Narrow-billed Woodcreeper (Lepidocolaptes angustirostris) is not a bird of humid forests but rather is found in dry forests and cerrado in much of southeastern South America. Photo by John Kricher.

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woodpeckers is an example of evolutionary convergence brought about by similar foraging ecologies. All woodcreepers have become bark-probing specialists, but their feeding behavior is different from that of woodpeckers. A woodcreeper moves methodically up and around a trunk, probing into crevices, poking its bill into epiphytes, and generally removing insects, spiders, and even an occasional tree frog. Woodcreepers rarely peck into the trunk, instead using their long bills as forceps to pick off prey. They may also join mixed flocks that follow army ant swarms. Like other furnariids, woodcreepers are soft shades of brown and rufous. Many have various amounts of yellowish-white streaking on the breast, head, and back. Overall body size, bill size and shape, and streaking patterns vary with species. The smallest is the 14 cm (5.5 in) Wedge-billed Woodcreeper (Glyphorynchus spirurus; plate 15-105), which has a very short but sharply pointed bill. Several species reach about 30 cm (just over 12 in) in length, and the largest, the Longbilled Woodcreeper (Nasica longirostris; plate 9-14), a sensational-looking inhabitant of várzea forests, reaches just over 35 cm (14 in). Among the oddest of the group are the five species of scythebills (genus Campylorhamphus; plate 15-106), whose extremely long, downward curving bills are used to probe deeply into bromeliads and other epiphytes. Many woodcreepers are ant followers, joining antbirds and other species to feed on insects and other animals disturbed by oncoming army ants. Because they have differing body sizes and bill shapes, several species of woodcreepers coexist and feed with little or no apparent competition. At one army ant swarm in Belize, I observed six woodcreeper species. Two were large, three were medium-size, and one was small. Woodcreepers are common not only in rain forests but also along forest edges, disturbed jungle, and dry forests (plate 15-107). Although they are suboscines, many species have songs consisting of pleasant, if simple, melodious, whistled trills.

Antbirds, Antthrushes, and Antpittas (Some of Which Do Follow Ant Swarms, Most of Which Do Not) The families Thamnophilidae, Formicariidae, and Grallariidae (order Passeriformes) include the antbirds, antshrikes, antwrens (plates 15-108–110), antvireos, antthrushes, and antpittas—all generally referred to as

Plate 15-108. The Dot-winged Antwren (Microrhopias quixensis) is one of the most widespread and commonly encountered typical antbirds, ranging from southeastern Mexico through Central America to Amazonian Ecuador, Brazil, and Bolivia. Photo by Andrew Whittaker.

Plates 15-109.

Plates 15-110. Plates 15-109 and 15-110. The 9.5 cm (3.75 in) Amazonian Streaked Antwren (Myrmotherula multostriata) is a typical antbird; it is not an ant follower. It is found along the edges of lakes and streams throughout Amazonia. A male (15-109) and female (15-110) are shown. Most typical antbird species are sexually dimorphic. Photos by Sean Williams.

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“antbirds.” All antbirds were once placed in the family Formicariidae, but analysis of DNA patterns in the group resulted in the splitting of the family. About 75% of the antbird species are placed in Thamnophilidae, referred to as typical antbirds, while the other 25% are in either the antthrushes (Formicariidae) or the antpittas (Grallariidae). Antbirds reach their peak species richness in Amazonia, where up to 30 or 40 species may occur together. The name antbird, or formicariid, comes from the army-ant-following behavior of some species. However, most antbirds do not follow army ant swarms. Some never do, some occasionally do, and some virtually always do. This latter group, comprises both typical antbird species and antthrushes (plate 15111). Thamnophilid antbirds are more boldly patterned than ovenbirds, and many are sexually dimorphic. Males are often black and white. Some, like the widely distributed and common Barred Antshrike (Thamnophilus doliatus; plate 15-112), are zebrastriped. Others are grayish black with varying amounts of white patterning on wings, breast, and flanks. Still others are chestnut or brown. Females tend to be rich brown, tan, or chestnut. Some antbirds have an area of bare blue or red skin around the eye, and in some species the iris is bright red (plate 15-113). Most antbirds are foliage gleaners, picking and snatching arthropods from foliage, and some capture insects on the wing. They forage at all levels, from the canopy to the litter on the forest floor, and various antbird species tend to feed at specific heights above the forest floor. Antbirds typically form mixed-species flocks with other birds. Mixed flocks of up to 50 bird species move through Amazonian lowland forests, of which 20 to 30 species may be antbirds. Certain species, such as the fly-catching antshrikes (genus Thamnomanes), occupy the role of central species in the flock. These antshrikes are highly vocal and act as sentinels, warning the others of impending danger should they spot a forest-falcon or other potential predator. There are about 30 species of professional antfollowing birds, each of which makes its livelihood by capturing arthropods scattered by advancing fronts of army ants (chapter 10). In addition, other bird species frequently, but not always, can be found accompanying the ants. The Spotted Antbird (Hylophylax naevioides), the Bicolored Antbird (Gymnopithys bicolor; plate 15114), and the Black-faced Antthrush (discussed below)

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Plate 15-111. The 19 cm (7.5 in) Rufous-breasted Antthrush (Formicarius rufipectus) is occasionally found at ant swarms, but it is not a “professional” ant-follower. It is a lower montane species found along the Andes from Venezuela to Peru. Photo by Edison Buenaño.

Plate 15-112. Male Barred Antshrike. (Thamnophilus doliatus) Photo by Kevin Zimmer.

Plate 15-113. This is an unusually good view of the Great Antshrike (Taraba major), one of the larger and most widely distributed of the antshrikes. It is normally a skulker and is more often heard than seen. This bird is a male. Females are brown where the male is black. Photo by John Kricher.

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Plate 15-114. Bicolored Antbird (Gymnopithys bicolor). The species was recently split from G. leucaspis, which is now known as the White-cheeked Antbird. Photo by Kevin Zimmer.

Plate 15-115. Black-faced Antthrush. Photo by Kevin Zimmer.

Plate 15-116. Streak-chested Antpitta (Hylopezus perspicillatus) is largely a Central American species, though it ranges well into Colombia and Ecuador. Photo by Kevin Zimmer.

Plate 15-117. The Chestnut-crowned Antpitta (Grallaria ruficapilla) ranges from Venezuela to Peru. Photo by Edison Buenaño.

are among the most devoted ant followers in Central America. Where these three are found together, there are surely army ants about. Ant followers rarely feed directly on army ants. It is suspected that the high formic acid content of these insects deters birds from eating them. Instead, antbirds feed on anything from insects to small lizards scared up by the oncoming ant columns. Two army ant species, Eciton burchelli and Labidus praedator, are the ants most frequently followed. Birds such as woodcreepers, ovenbirds, motmots, certain tanagers, and other “less professional” antbirds come and go as part of the ant-following avian assemblage, but the professional antbirds always stay with the ants. Only when breeding

do they become territorial and cease to follow ants for a time. Even then, they will quickly orient to army ant swarms within their territories. Species such as the Spotted and Bicolored Antbirds feed actively in trees and undergrowth, while the Blackfaced Antthrush (Formicarius analis; plate 15-115) walks sedately on the forest floor. With the stature of a small rail, walking with its short tail cocked upward and head held up and alert, the Black-faced Antthrush can be found throughout lowland forests in Central America and much of South America. It is easy to imitate its whistled, descending chew, chew, chew, chew call. In Trinidad, I called one almost to my feet, as I whistled and it answered.

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Antbirds tend to mate for life. Both male and female are active nest builders. One species, the Ocellated Antbird (Phaenostictus mcleannani; plate 10-39), forms clans. Sons and grandsons of a pair return to the breeding territory with mates to form clans, and a clan will occasionally attack an intruding clan. Antbirds also sometimes intimidate migrant thrushes that attempt to gather at ant swarms. Antpittas (family Grallariidae) usually present a challenge for observation, though they sing from their oft-hidden perches with gusto. These birds anatomically resemble the Old World pittas (family Pittidae) but lack the vibrant colors that typify this group. Antpittas all have chunky bodies and stand upright on long legs (plates 15-116–117). They hop along the forest floor in the understory shade.

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Plate 15-118. The Great-tailed Grackle is hard to miss among Neotropical bird species. This is a male. Photo by John Kricher.

Blackbirds, Oropendolas, Caciques, and Orioles The large avian family Icteridae, the New World blackbirds, includes the blackbirds and their relatives, such as orioles and meadowlarks. There are 112 species, most living in the Neotropics, but some, like the familiar Red-winged Blackbird (Agelaius phoeniceus), inhabiting North America. Some icterids are very colorful, and all are interesting. One of the most common birds of much of Central America is a large (46 cm/18 in) blackbird, the Greattailed Grackle (Quiscalus mexicanus; plate 15-118). It is common in urban areas as well as open habitats but prefers to be relatively near the coast. It ranges from the Gulf Coast in North America to coastal areas of Ecuador. It sometimes roosts in large numbers around towns, and flocks can be very noisy. Males are sleek iridescent black, with long tails and bright yellow eyes. Females are somewhat smaller and rich brown. Other grackle and blackbird species are locally distributed throughout the Neotropics. Two of the most striking are the Red-breasted Blackbird (Sturnella militaris; plate 15-119), found in open agricultural areas, and the Oriole Blackbird (Gymnomystax mexicanus; plate 15-120), common in grasslands, savannas, and marshes of northern Amazonia. Not all Neotropical blackbirds are so colorful. The aptly named Unicolored Blackbird (Agelasticus cyanopus; plate 15-121) occurs mostly in southern Amazonia and the Pantanal south to Argentina.

Plate 15-119. The male Red-breasted Blackbird is obvious as it perches atop a shrub to defend its territory during breeding season. Photo by John Kricher.

Plate 15-120. The Oriole Blackbird is found in open areas near water and is frequently seen along the Amazon and its tributaries. Photo by Andrew Whittaker.

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The Grayish Baywing (Agelaioides badius; plate 15122) has a disjunct range, with one population in southern Amazonia and the Pantanal and the other in northeastern South America. Both species frequent open savanna and agricultural areas. Oropendolas and caciques are colonial and make long, hanging, basketlike nests. An oropendola nest tree is easy to spot because it is out in the open and adorned with numerous pendulous nests (plate 15123). The isolation of the nest tree affords some protection against predation by monkeys, since the simians are usually loath to leave the canopy and cross open ground. Oropendolas are large birds (some almost crow-size), and caciques are robin-size. In shape, both caciques and oropendolas are relatively slender and have long tails and sharply pointed bills. Oropendolas come in two color types. One group of species is mostly black and chestnut, with yellow on the bill and tail, and the other is much more uniformly greenish (plates 15-124–125). Caciques are mostly sleek black but with bright red or yellow rumps and/or wing patches, and yellow bills. Both caciques and oropendolas tend to locate their colonies near bee or wasp nests (plate 15-126). Because these colonial insects can be very aggressive toward intruders, this behavior helps reduce the probability of nest predation by mammals. Scott Robinson learned that Yellow-rumped Caciques (Cacicus cela; plate 15-127) employ other “strategies” that would also seem to protect the colony. These caciques often nest on islands in a river or lake, affording added security from both mammals and snakes, for would-be predators would have to cross a water body patrolled by otters and caimans. Furthermore, the caciques tend to mob potential avian predators. Their unused abandoned nests remain in the nest tree along with active nests. The presence of the unused nests may confuse a predator. Not surprisingly, each cacique attempts to locate its nest in the center (where protection is maximized), rather than the riskier periphery of the colony. For caciques, colonial nesting and group defense is a significant adaptation against nest predation. Robinson documented, however, that Yellowrumped Caciques are occasional victims of nest piracy by other bird species. One, appropriately named the Piratic Flycatcher (Legatus leucophaius), harassed caciques until they abandoned their nests to the flycatchers. Russet-backed Oropendolas (Psarocolius

Plate 15-121. Unicolored Blackbird. Photo by John Kricher.

Plate 15-122. Grayish Baywing, in early morning light at a pasture in the Brazilian Pantanal. Photo by John Kricher.

Plate 15-123. Nests of the Montezuma Oropendola (Psarocolius montezuma) hang in a cluster from branch tips. Photo by Bruce Hallett.

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Plate 15-124. The Montezuma Oropendola is one of the largest of the oropendola species and is an example of the so-called black oropendolas. It occurs in Central America. Photo by Gina Nichol.

Plate 15-125. The Dusky-green Oropendola (Psarocolius atrovirens) is one of several green oropendolas. This species is found in montane forests along the eastern slope of the Andes. Photo by Andrew Whittaker.

Plate 15-126. A cluster of cacique nests (in shadows) located close to a large wasp colony (left). The density of wasps presumably provides protection for the cacique nests. Photo by John Kricher.

Plate 15-127. Yellow-rumped Cacique. Photo by Nancy Norman.

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Plate 15-128. Giant Cowbirds (37 cm/14.5 in), here bathing in a pasture, are brood parasites that frequently lay their eggs in oropendola and cacique nests. Photo by John Kricher.

angustifrons) destroyed cacique eggs and killed young, leaving nests empty. Finally, Venezuelan Troupials (Icterus icterus), which are large, aggressive orioles, both destroyed cacique eggs and young and took over their nests. Robinson hypothesized that the piracy is not related to competition for food, because each of the nest pirate species has a diet different from that of caciques. Instead, the presence of many nearby empty cacique nests serves to confuse potential predators and confer protection on the nest pirate species. Oropendolas and caciques are also routinely parasitized by Giant Cowbirds (Molothrus oryzivorus; plate 15-128), which are brood parasites. A female cowbird will surreptitiously (and quickly) lay an egg in an oropendola or cacique nest, and the oropendolas and caciques (which do not know the egg is not one of theirs) actually raise and fledge the young cowbird. Of course, if they catch the cowbird in the act, the nest owners usually evict the egg. Orioles are among colorful blackbird species, their plumage usually various combinations of orange, yellow, and black (plate 15-129–130). They are not colonial, like the oropendolas or caciques, but nest as territorial pairs. Several oriole species migrate to North America to nest, but most remain in the tropics. Orioles, oropendolas, and caciques feed on fruit and nectar, mixing various arthropods into an otherwise vegetarian diet.

Plate 15-129. The well-known Baltimore Oriole (Icterus galbula), a migrant that breeds in eastern and central North America, shows the strikingly colorful plumage pattern typical of most orioles. Baltimore Orioles winter in the Neotropics. Photo by John Kricher.

Finches, Seedeaters, and Others: Taxonomy in Flux

Plate 15-130. Look for the Yellow-hooded Blackbird (Chrysomus icterocephalus) along marshes and wet areas from Central America to northern South America and along the Amazon River. Photo by Jill Lapato.

There are many species of Neotropical birds with thick, strong, seed-cracking bills. Typically seed-eating birds inhabit areas such as grassy, disturbed sites and forest edges. They also occur in marshes and around human habitations. Some inhabit forests. The classification of birds has become increasingly complex, and taxonomic sequences have changed as more molecular-based data have been analyzed. Such complexity is illustrated, for example, with a subfamily of common birds that comprises the genera Euphonia and Chlorophonia. Euphonias (plate 15-131), long believed to be allied with the tanagers, are a group of 27 small, multicolored species. On the basis of DNA studies, they have been reclassified and placed in the large family Fringillidae, with the so-called true finches, such as goldfinches and

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Plate 15-131. The Violaceous Euphonia (Euphonia violacea) is widely distributed in much of the Neotropics. The bird shown is a male. Photo by Andrew Whittaker.

Plate 15-132. The Blue-naped Chlorophonia (Chlorophonia cyanea) is found along montane forest edges. It was once considered a tanager but is currently placed in the Fringillidae along with siskins and goldfinches. Photo by Andrew Whittaker.

Plate 15-133. The Summer Tanager (Piranga rubra) is now considered to belong within the Cardinalidae and is thus is no longer a “tanager.” It winters widely in Central America and northwestern South America and migrates to North America to breed. Photo by John Kricher.

Plate 15-134. The Chestnut-capped Brushfinch (Arremon brunneinucha) is found in northwestern South America. Though in the open in this photo, it typically is found in forest understory and forest edge. Photo by Gina Nichol.

siskins, birds that feed primarily on seeds. Euphonias feed heavily on mistletoe (family Loranthaceae), mashing up the berries in their beaks, and are important dispersers of mistletoe seed, as their sticky droppings, deposited on branches, contain the seeds that begin life as epiphytes before becoming parasitic. Euphonias often nest in bromeliads (Bromeliaceae). Chlorophonias are a group of five small (sparrowsize), bright green and yellow highland birds also traditionally thought to be tanagers. They too have, on the basis of DNA analysis, been reclassified and placed within the Fringillidae. Regardless of their pedigree,

chlorophonias are really worth a look (plate 15-132). Two other major families of seed-eating birds are represented in the Neotropics. One is the Cardinalidae, the cardinals and grosbeaks, which now includes the North American tanagers (plate 15-133). The other, more diverse family is the Emberizidae, the buntings and New World sparrows. As currently recognized by avian systematists, the Emberizidae is composed of various sparrows and brushfinches (plate 15-134), plus a few others that occur mostly in montane areas or in southern South America. All told, 59 species of Emberizidae occur in South America.

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Plate 15-135. The widespread Turkey Vulture, showing its typical soaring pattern of wings held slightly upward, in a dihedral. Photo by John Kricher.

Plate 15-136. In the air Black Vultures demonstrate a different flapping pattern from Turkey Vultures and also have white on the ventral surface of the primary feathers of the wing. Photo by John Kricher.

Birds of Prey

prey. Turkey and Black Vultures are among the most ubiquitous birds in Neotropical skies. The Black Vulture ranges from Argentina into southern and central North America. Black Vultures commonly congregate in vast numbers around garbage dumps and are thus common city dwellers, urbanite birds that work as sanitary engineers throughout much of Latin America. Turkey Vultures are named for their red heads, which give them a superficial resemblance to the heads of turkeys. Turkey Vultures fly with wings distinctly upraised, in a dihedral pattern, a behavior that provides them with outstanding soaring ability (plate 15-135). Turkey Vultures are permanent residents in the Neotropics, but their population is augmented in winter months as thousands migrate, mostly from western North America, southward, along with large numbers of Swainson’s (Buteo swainsoni) and Broadwinged (B. platypterus) Hawks. Because vultures and hawks migrate diurnally by soaring on daily thermal currents rising from the ground, they must migrate over land. Thus thousands may be seen in the fall migration in places such as Veracruz in Mexico and in Panama, particularly as they converge over the narrow Isthmus of Panama (plate 15-139). Two other species, the Greater Yellow-headed and Lesser Yellow-headed Vultures, are less widespread and generally less common than Turkey and Black

Birds of prey are diverse and abundant in the Neotropics. They range in size from the tiny Bat Falcon and Pearl Kite to the majestic Harpy Eagle (all three species are covered further below). Open areas, such as savannas, are excellent places for searching out many of the larger species, since some habitually soar on thermal currents rising from the hot ground. Inside forests, birds of prey can be elusive. Many, such as the forest-falcons (genus Micrastur), sit motionless on a branch waiting for an opportunity to attack would-be prey.

New World Vultures Five vulture species (family Cathartidae), the Black (Coragyps atratus), Turkey (Cathartes aura), Lesser Yellow-headed (Cathartes burrovianus), Greater Yellow-headed (Cathartes melambrotus), and King (Sarcoramphus papa) Vultures, occur in various combinations soaring over rain forests and savannas (plates 15-135–136). Not really raptors, these birds are strictly carrion feeders (though Black Vultures occasionally kill small animals), devouring carcasses (plates 15-137–138). Unlike typical raptors, vultures have naked heads, a probable adaptation to reduce feather contamination from carcass eating, and weak feet lacking the typical strong talons of birds of

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Plate 15-137. Turkey Vultures at a deer carcass. They may have located it either by olfaction or by sight—or both. Photo by John Kricher.

Plate 15-138. Black and Turkey Vultures on a deer carcass. Tensions often mount among the birds as they compete for access to the food resource. Photo by John Kricher.

Vultures. Each of these two species has a yellowish head. The Greater Yellow-headed is most commonly seen flying over forests and along watercourses. It occurs throughout most of Amazonia. The Lesser Yellow-headed (plate 15-140) avoids closed forests and inhabits savannas and open areas. Ornithologists have shown that Turkey Vultures locate their carrion using both keen senses of olfaction (detecting the odor of ethyl mercaptan, emitted by putrefying flesh) and vision. Greater Yellow-headed Vultures and King Vultures are suspected of also having

a keen olfactory sense. Both species are forest vultures, and many carcasses lying within closed forest would not be visible from the air. Black Vultures and Lesser Yellow-headed Vultures are savanna foragers and detect carrion visually. Black Vultures also routinely observe Turkey Vultures and follow them when the Turkey Vultures descend on newly discovered carrion. The King Vulture (plate 15-141) is the largest and most spectacularly plumaged Neotropical vulture. It is black and white, and its head is adorned with bright (but bizarre-looking) orange wattles. King Vultures are

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Plate 15-139. The photo shows but a small part of an extensive “aerial river” of Turkey Vultures soaring as they migrate. Photo by John Kricher.

Plate 15-140. Lesser Yellow-headed Vulture. Photo by John Kricher.

never abundant but occur throughout forested areas of Central America and Amazonia. In addition to the vultures there are two New World condor species, the California (Gymnogyps californianus) and Andean (Vultur gryphus). Only the Andean Condor occurs in South America; it is discussed in chapter 13.

Hawks, Hawk-Eagles, and Eagles

Kites Eleven species of kites gracefully skim Neotropical skies searching out small animals such as mice, birds, lizards, and arthropods. Kites have sharply hooked bills, a trait particularly evident in the Snail Kite (Rostrhamus sociabilis) and the Hook-billed Kite (Chondrohierax uncinatus). The Snail Kite and the Slender-billed Kite (Helicolestes hamatus) both specialize on large marsh snails, which they adeptly remove from the protective shell with their sharply hooked bills (discussed in chapter 14). Another common kite is the White-tailed (Elanus leucurus), often seen hovering over open fields and savannas seeking its small animal prey. The most graceful flier among the kites is the Swallow-tailed (Elanoides forficatus), a slender black-and-white bird with a deeply forked tail. At 23 cm (9 in) long, the Pearl Kite (Gampsonyx swainsonii; plate 15-142) is one of the smallest tropical birds of prey. Mostly black, with white underparts, it has a buffy forehead and face, and a white or rufous neck. Like most kites it frequents savannas.

There are just over 50 species of hawks and allies (family Accipitridae, order Accipitriformes) to be found in the Neotropics. Those briefly described and shown here are but a mere sample. The well-named and widely distributed Savanna Hawk (Buteogallus meridionalis; plate 15-143), tends to be seen perched on a fence or a bare limb or walking about on the open ground. It is largely rufous, with black tail and wing tips and dark barring across its breast. The splendid White Hawk (Pseudastur [Leucopternis] albicollis; plate 15-144) is apt to be seen soaring on warm thermals over forests. As its name implies, it is virtually all white but for a black band across the tail and black on the wings and around the eyes. Other soaring hawks include the Common Black Hawk (Buteogallus anthracinus) and Great Black Hawk (B. urubitinga; plate 15-145). Both of these birds are almost all black but for white tail bands. The wide-ranging Roadside Hawk (Buteo magnirostris; plate 15-146) is well named. The relatively small, grayish-rufous hawk can be seen perched on cecropias, palm trees, ceibas, and utility poles all along tropical roads. This abundant and widely distributed species is also variable in plumage, and multiple subspecies have been recognized. The largest Neotropical birds of prey are eagles and hawk-eagles. There are three species of hawk-eagles,

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Plate 15-141. King Vulture. Photo by Steve Bird.

Plate 15-142. Pearl Kite. Photo by John Kricher.

Plate 15-143. Savanna Hawk. Photo by John Kricher.

Plate 15-144. White Hawk soaring, a typical behavior. Photo by John Kricher.

Plate 15-145. The Great Black Hawk often is found perched along streams and rivers, where it searches for potential prey items. Photo by John Kricher.

Plate 15-146. The Roadside Hawk is perhaps the most commonly sighted raptor throughout the Neotropics. Photo by John Kricher.

each of which has a crest atop its head. The Ornate Hawk-Eagle (Spizaetus ornatus; plate 15-147) has a bright orange neck and a tall black crest. The Black Hawk-Eagle (S. tyrannus) is uniformly dark, and the Black-and-white Hawk-Eagle (S. melanoleucus) is black above and white below. Hawk-eagles are soaring hawks, usually seen above the canopy making circles high overhead. The Harpy Eagle (Harpia harpyja; plate 15-148) ranks among the most magnificent of Neotropical birds

and is arguably the largest bird of prey in the world. Nonetheless, it is secretive, tending not to soar and thus is hard to see well. It ranges from southern Central America throughout Amazonia but is difficult to find over most of that vast territory. However, many birding tour operators now have reasonable success at showing their clients this remarkable raptor because they monitor where the birds are nesting. This huge predator is just over 1 m (3.3 ft) tall and has extraordinarily thick, powerful legs and feet. As with all birds of prey, females

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are larger than males. It is mostly gray on the face and belly, and the wings, back, and upper breast are black. The head sports a tall blackish-gray crest. Harpy Eagles feed mostly on monkeys and sloths, including the largest species, capturing them in a swift pass, legs extended, by grabbing the prey from its tree. The Crested Eagle (Morphnus guianensis; plate 15149), which resembles the Harpy Eagle and has similar habits, is somewhat smaller (a female Crested is about the size of a male Harpy). It shares much of the range of the Harpy Eagle, occurring in rain forest and along riverine areas throughout Amazonia.

Falcons and Caracaras Falcons (family Falconidae, order Falconiformes) are speedy birds of prey known for their aerial agility. With long tails and sharply pointed wings, falcons are quick to pursue and capture rodents, small birds, and insects. One species, the diminutive Bat Falcon (Falco rufigularis), specializes in capturing bats at dawn and dusk, but is often observed perched in the open in daylight. It is largely dark blue, with a white throat and orange on the thighs and lower belly. Recent genetic analysis has resulted in a major revision of falcon and caracara classification. The group, family Falconidae, is now recognized as its own order, the Falconiformes, and placed between the woodpeckers (Piciformes) and the parrots (Psittaciformes). Such a change suggests that the characteristics of falcons as birds of prey are convergent rather than derivative of such birds of prey as hawks and eagles. The Laughing Falcon (Herpetotheres cachinnans; plate 15-150) is often seen perched atop a snag along a forest edge, cleared field, or savanna. Very buffy on the head, neck and breast, the Laughing Falcon has dark brown wings, back, and tail, with a black band through the eyes and around the back of the neck. Named for its penetrating loud call, these birds prey on snakes and other animals spotted by patiently sitting for long periods. This is one of the few raptors, perhaps the only species, to have been documented (in film) to prey on highly venomous coral snakes. Forest-falcons (genus Micrastur; plate 15-151) are grayish falcons that skulk inside forests and are generally difficult to find. They are typically inconspicuous, perching motionless in the deep forest shade until they fly swiftly through the forest to capture prey, mostly birds. Researchers who band birds by

Plate 15-147. Ornate Hawk-Eagle. Photo by Sean Williams.

capturing them in long inconspicuous mist nets have often observed that a forest-falcon will learn that birds are being netted and come to the net to prey on the bird as soon as it is captured. The Yellow-headed Caracara (Milvago chimachima; plate 15-152) is a common and conspicuous falcon, often seen in groups along rivers and forest edges. Caracaras, like vultures, feed on carrion and hence are frequently encountered along roadsides. Yellow-headed Caracaras are slender birds, buffy yellow on head, breast, and belly, with blackish brown wings and tail. Three closely related species of crested caracaras (Caracara; plate 15-153) range from the southern United States throughout Central and South America. Similar in appearance and ecology, crested caracaras frequent open grasslands and savannas.

Owls Owls (order Strigiformes, families Tytonidae [barn owls] and Strigidae [typical owls]) are nocturnal birds of prey. Approximately 50 species of owls, screechowls, and pygmy-owls occur in the Neotropics. Several of the most wide-ranging are discussed below. Owls prey mostly on vertebrates, particularly small mammals and birds. The Spectacled Owl (Pulsatrix perspicillata; plate 15-154) is the largest Neotropical owl, reaching 50 cm (19.7 in) in length. It is buffy yellow on the lower breast and belly, a dark brown band crosses its upper breast, and it has a dark brown back, wings, tail, and head. The bright yellow eyes highlighted by white give the bird its name. Spectacled Owls make a deep hooting sound.

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Plate 15-148. Nirvana for birders: a pair of Harpy Eagles at a nest. Photo by Gina Nichol.

Plate 15-149. The majestic Crested Eagle in flight. Photo by Andrew Whittaker.

Plate 15-150. Laughing Falcon. Photo by Jill Lapato.

Plate 15-151. Most visitors to tropical rain forests never get this good of a look at a Lined Forest-Falcon (Micrastur gilvicollis). Photo by Andrew Whittaker.

Plate 15-152. Yellow-headed Caracara. Photo by John Kricher.

Plate 15-153. Southern Crested Caracara (Caracara plancus), photographed in the Pantanal of Brazil. Photo by John Kricher.

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Plate 15-154. Spectacled Owl. Photo by Kevin Zimmer.

Plate 15-155. Mottled Owl. Photo by John Kricher.

Plate 15-156. Crested Owl. Photo by Kevin Zimmer.

Plate 15-157. Ferruginous Pygmy-Owl. Photo by John Kricher.

The Mottled Owl (Ciccaba virgata; plate 15-155) is warm brown and tan with dark brown eyes. It is often found near dwellings and is one of the most frequently encountered of the Neotropical forest owls. The Crested Owl (Lophostrix cristata; plate 15-156) is found both in dense forest and in secondary forest. It is somewhat less frequently encountered than the other species shown here, but it is certainly worth the effort to find it. Its call is described as a rolling note somewhat similar to the sounds of a toad.

During the daytime, it is not uncommon to encounter a small pygmy-owl (genus Glaucidium), staring with its bright eyes from its perch atop a snag. Several species of these 15.2 cm (6 in) owls occur in the tropics, but the most common is the Ferruginous Pygmy-Owl (G. brasilianum; plate 15-157), so named for its reddish-brown plumage. Imitating the call of a pygmy-owl will frequently result in exciting numerous passerine birds to come close, call, and investigate the perceived nearby predator.

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North American–Neotropical LongDistance Migrant Birds Various species of orioles, tanagers, flycatchers, grosbeaks, thrushes, buntings, and wood warblers (plate 15-158), along with numerous other birds, nest in North America, migrating north in spring and returning to subtropical and tropical habitats after breeding season concludes. While the breeding ecology of most of these species has been well understood, their wintering ecology and migratory stopover sites have only recently been investigated, with fascinating results. During autumn, 338 species (including shorebirds, raptors, and numerous passerines), or about 52% of all North American migrant bird species, fly to wintering areas somewhere within Central or South America, as far south as southern Chile and Argentina. This influx may total somewhere between 5 and 10 billion birds, but no one really knows with any certainty. The majority of long-distance migrant passerines winter in Central America, but many also winter in South America and the Caribbean Islands, especially the Greater Antilles. The density of North American migrants is high in the Neotropics from November through March. Not only are there innumerable birds—yearlings in addition to adults—but the actual land area of Central America, where many migrant species winter, is smaller, by about a factor of eight, than available nesting area in North America. Migrants ranging from Swainson’s Hawks to Least Flycatchers (Empidonax minimus) are packed into tropical America for the winter months. Many North American migrants are from families that evolved in the Neotropics. Tyrant flycatchers, hummingbirds, tanagers, orioles, and wood warblers all originated in the Neotropics, though their speciation patterns may have been much affected by their breeding ranges in North America. Longdistance migrant species represent the relatively few that ventured northward into the temperate zone, extending their ranges, perhaps because the northern summer presents an abundance of protein-rich insect resources for the rearing of young, longer days in which to feed, fewer predators, and the availability of abundant nesting sites. Evidence suggests that during the Pleistocene glaciation, speciation events occurred in the northern breeding areas that added to the diversity of long-distance migrant birds. Neotropical migrant land bird species, when on their tropical wintering grounds, use virtually all available

Plate 15-158. The Bay-breasted Warbler (Setophaga castanea) breeds in the boreal forests of North America and winters in the humid forests of Colombia and western Venezuela, occasionally to Peru and Brazil. This bird, which flies thousands of miles annually, weighs a mere 12.5 g (about 0.44 oz)—and thus you could mail two of them anywhere in the United States for the price of a first-class postage stamp. The bird in the photo is a male. Photo by John Kricher.

Plate 15-159. Kentucky Warblers typically winter within tropical forests throughout Central America and into northern South America. Photo by John Kricher.

Plate 15-160. Male Black-and-white Warbler in a typical feeding posture along a limb, searching for arthropod food. Photo by John Kricher.

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habitat types. They can be found, often abundantly, in dry forest, mangrove forest, montane forest, and rain forest. Brushy successional areas are habitat for many species, such as Gray Catbird (Dumetella carolinensis), Common Yellowthroat (Geothlypis trichas), and Yellowbreasted Chat (Icteria virens). Rain forests provide habitat for Wood Thrushes (Hylocichla mustelina), Kentucky Warblers (Geothlypis formosa; plate 15-159), American Redstarts (Setophaga ruticilla), and other wood warblers. Many of these species also utilize successional areas. Some Neotropical migrants—the Black-and-white Warbler (Mniotilta varia; plate 15-160), for example— range widely in the Neotropics, occupying many kinds of wintering habitat. Black-and-white Warblers, unique among wood warblers for their habit of foraging for arthropods on bark, somewhat like nuthatches, are extraordinary in their inclination to range widely and frequent virtually any terrestrial habitat. They can be found in oak-pine forests, in mangroves, in plantations, along any kind of forest edge and successional scrub, in dry forests, and in interior rain forests anywhere from western Mexico, the Antilles and West Indies, and all parts of Central America through northern South America. In general, other migrants are more restricted (some much more so), which puts them at risk should they suffer from habitat loss. An example is the Cerulean Warbler (Setophaga cerulea), which winters along a narrow elevational belt at between 620 and 1300 m (2,030–4,265 ft) in the eastern Andean foothills of Colombia, Ecuador, and Peru. Unfortunately, this area has been and continues to be heavily deforested and converted to agriculture, including cocaine fields, putting the future of this species at some risk. Many North American migrants eat a diet high in fruit while in the tropics. Baltimore and Orchard Orioles (Icterus galbula and I. spurius) and Scarlet and Summer Tanagers (Piranga olivacea and P. rubra) feed in cecropia and fig trees among mixed flocks of euphonias, Neotropical tanagers, and honeycreepers. Many researchers have noted that abundance of migrants is high in successional areas and young forests. Fruit availability may be one reason migrants favor such areas. North American migrants are believed to be important fruit consumers and seed dispersers, especially for plants that typically grow in disturbed areas. Some Neotropical migrant species, such as the Orchard Oriole and Tennessee Warbler (Oreothlypis peregrina), feed on nectar and are recognized as

potential pollinators while on their wintering grounds. Given that North American migrants spend perhaps the majority of their year in the Neotropics, it is not surprising to learn that some are relatively specialized when on their wintering grounds. The degree to which North American migrants interact with Neotropical resident birds is a subject of ongoing research. Neotropical migrants are often observed accompanying mixed flocks of resident birds and have also been documented to attend army ant swarms. This is hardly surprising given the advantages that could be gained from watching experienced resident birds as they forage. Many if not most Neotropical migrant species are territorial on their wintering ground and have a strong tendency to return to the same wintering site annually. Species as the Wood Thrush, Ovenbird (Seiurus aurocapilla), Kentucky Warbler, and Gray Catbird usually occupy exactly the same locations from one winter to the next. Although these birds migrate north to nest, they return in the fall to precisely the same local wintering area used the previous year, a behavior called winter site fidelity. As one might expect, winter site fidelity often means that the birds are territorial, defending those winter sites. Wood Thrushes for example, establish and defend winter territories, using subtle vocalizations and body posturing. Each Wood Thrush has its own turf within the rain forest. Survivorship among “floater” Wood Thrushes, birds that have not succeeding in acquiring and holding a winter territory, is very likely diminished. In another example, male Hooded Warblers (Setophaga citrina) obtain territories inside interior forest, while females are territorial in disturbed, successional habitats. Through a combination of techniques ranging from banding to analysis of stable isotopes (such as carbon-13) contained in the feathers and blood of birds, it has been learned that habitats vary in value to birds, and this results in differences in overall robustness of the birds and the timing of their return migration northward. American Redstarts and Black-throated Blue Warblers (Setophaga caerulescens; plate 15-161) wintering in marginal scrubby habitats where food is less abundant than in interior forests do not tend to gain weight in winter and do not reach nesting sites nearly as early as healthier birds that winter in richer forest. A relatively new research technique uses geolocating devices, which are attached to the backs of birds and measure daily day length as the bird moves through

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Plate 15-161. Black-throated Blue Warblers fare better in forests than scrubby habitats. A male is shown. Photo by John Kricher.

Plate 15-162. The Purple Martin (Progne subis) is a colonial swallow that winters throughout much of South America, including Amazonia. It was among the first species whose breeding and wintering range connectivity was established by use of geolocators. The bird in the photo is a male. Photo by John Kricher.

Plate 15-163. Male Blackpoll Warbler in spring plumage heading north to its boreal forest breeding grounds. It follows an entirely different route than it does in its fall migration. Photo by John Kricher.

Plate 15-164. The true wintering range of the Veery is poorly documented but may be in areas where deforestation has been accelerating and much habitat is already lost. Photo by John Kricher.

Plate 15-165. A Kirtland’s Warbler on its highly restricted wintering grounds in the Bahamas. Photo by Bruce Hallett.

Plate 15-166. The Chestnut-sided Warbler may be a species that has benefited from increasing successional habitats created as a result of forest clearance. The bird in the photo is a male. Photo by John Kricher.

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its migration cycle (plate 15-162). The bird is given a geolocator on its breeding grounds and that device (which weighs very little and does not impede the bird) is removed when the bird returns to its nesting area in the following spring (many bird species are highly site faithful to their breeding grounds). Analysis of the geolocator data will show the researcher exactly where and for how long the bird wintered and will track its migratory routes south and north. This technique represents a major breakthrough in establishing the connectivity between breeding and wintering areas and the routes of travel to and from. The majority of passerine migrant bird species are nocturnal migrants. Their call notes may be heard on clear nights both in spring and fall as they make their journeys. Most migrant bird species move south to the Gulf states in late summer and autumn and then cross the Gulf of Mexico, a journey of about 965 km (600 mi) over water, which is subsequently repeated as they come north in the spring. Some species, however, migrate mostly overland, moving into northern Central America and continuing south. This route is typical of migrants that breed in the central and western United States and also of groups such as swallows, which are diurnal migrants and feed while on the wing. One unique migratory route is that of the Blackpoll Warbler (Setophaga striata; plate 15-163). In the fall, on its boreal North American breeding grounds, it responds to cold fronts that bring strong northwesterly winds and migrates southeast across the Atlantic Ocean to eventually encounter the equatorial trade winds that help move it southwest toward its wintering grounds in Amazonia. This flight, which usually is accomplished nonstop, requires about four days on the wing to complete. In spring Blackpolls use an entirely different route, migrating across the Gulf of Mexico

and overland to their breeding grounds in boreal forests. If it tried to repeat the route of its fall migration it would fly into head winds for its entire journey. Many North American migrant species may be subject to ongoing human-caused reduction in wintering sites, an increasing concern. For example, the Veery (Catharus fuscescens; plate 15-164) has, based on specimen records, been thought to winter in northern Amazonia, where much forest remains. However, most of those specimens were taken during the active migratory period. It appears that Veeries actually winter farther south, in south-central and southeastern Brazil, areas that have been subject to intensive habitat loss. Thus the species could be in decline. Some migrant species are now rare in North America, possibly due to a combination of nesting site specialization and loss of their Neotropical wintering areas. The Kirtland’s Warbler (Setophaga kirtlandii; plate 15-165) nests only in successional Jack Pine forests in Michigan. The bird was once probably more widely spread and could possibly occupy a larger nesting area today, but loss of winter habitat in the Bahamas may have restricted its population. The Bachman’s Warbler (Vermivora bachmanii) is now considered to be extinct but was once an inhabitant of dense canebrake areas in southern hardwood swamps. Loss of cane habitat in Cuba, where the bird wintered, as well as habitat reduction in North America is thought to have been responsible for its population demise. On the other hand, increase in second-growth habitat could actually favor such species as Chestnut-sided Warbler (Setophaga pensylvanica; plate 15-166) and Indigo Bunting (Passerina cyanea). As with virtually all tropical ecology puzzles, questions about the effects of tropical deforestation on migrants are complicated and elude simple answers.

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Chapter 16 From Monkeys to Tarantulas: Endless Eccentricities Alfred Russel Wallace (1895) was deeply impressed by the animals he observed in the tropics:

Mammals

In this chapter I will try to convey some of the wonder Wallace felt and introduce you to some of the “eccentric” creatures that dwell within rain forests. As noted in the previous chapter, on the region’s birdlife, no single book can offer anything other than a sampling of the diverse creatures of the rain forest. So, here I present here an array of Neotropical mammals (plate 16-1), reptiles, amphibians, and invertebrates, by no means intended to be inclusive (what a foolish idea that would be), but rather with the focus of the discussion on those that the visitor is likely to see or at least hope to see.

As a group, rain forest mammals tend to be secretive and mostly nocturnal, making it a challenge to see them well. Unlike the diverse herds of large mammals that inhabit the African plains, rain forest mammals do not occupy open areas that allow for easy viewing but rather scurry through the leafy canopy or over the forest floor, often well ahead of the naturalist. Still, by careful stalking or quiet sitting, especially in preserves where the animals enjoy protection from hunting, it is often possible to obtain excellent views of mammals. In some places mammals, particularly monkeys, have become relatively habituated to the presence of humans and are easy to see and photograph. Many mammals are primarily nocturnal, and a walk at night with a good flashlight can be rewarding. It is essential to understand two things about Neotropical mammals and other animals as you move through this chapter. First, as has occurred with bird classification, mammal classification is an active work in progress, and there have been numerous changes since the 1998 edition of A Neotropical Companion. Many splits have occurred, thus recognizing “new” species, especially within the primates (as you will see

Plate 16-1. Jaguar (Panthera onca), the Neotropical “king of beasts.” Photo by Dennis Paulson.

Plate 16-2. Greater Tent-making Bat (Uroderma bilobatum). Photo by Dennis Paulson.

Animal life is, on the whole, far more abundant and more varied within the tropics than in any other part of the globe, and a great number of peculiar groups are found there which never extend into temperate regions. Endless eccentricities of form and extreme richness of colour are its most prominent features, and these are manifested in the highest degree in those equatorial lands where the vegetation acquires its greatest beauty and its fullest development.

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below). Second, many mammalian species (as well as other animals) are declining for various reasons. The conservation status of mammals as well as other animals is evaluated by two organizations, the International Union for the Conservation of Nature (IUCN) and the Convention on International Trade in Endangered Species (CITES). These organizations will be cited throughout this chapter as I discuss recent changes in taxonomy as well as the apparent declines of some species. The order Chiroptera, the bats (plate 16-2), is second only to rodents (order Rodentia) in mammalian Neotropical species richness. Nearly 40% of Neotropical rain forest mammal species are bats, and 236 species occur in the Neotropics. An account of bats and their remarkable adaptive radiation is described and illustrated in chapter 8, and thus bats are not discussed here.

The Simians of the Rain Forest: New World Monkeys Neotropical monkeys all belong to a group named the platyrrhines, a word that refers to the position of the nostrils. New World monkeys’ nostrils open at the sides (plate 16-3). This is in contrast with Old World monkeys, the catarrhines, whose nostrils are more closely spaced and point downward (humans, having evolved from apes in Africa, have a similar nostril position). Some New World monkeys are known less for their nostrils, however, than for their tails. Some common and widely distributed platyrrhines, such as the capuchins, spider monkeys, woolly monkeys, and howler monkeys, have prehensile tails, which they skillfully use as a one-fingered fifth limb (chapter 8). When the previous edition of this book was published in 1998, authoritative accounts listed approximately 60 species of New World Monkeys, but the number of New World monkey species is now considered to be 141. The upward spike has come about mostly because of a strong recent trend in splitting, mostly by elevating subspecies to species level. In 2011 an expedition in Brazil discovered a new monkey species, which has been named Milton’s Titi Monkey (Callicebus miltoni), after Milton Thiago de Mello, a famous Brazilian primatologist. Yet another new species, the Urubamba Brown Titi Monkey (C. urubambensis), was described in 2015 from a remote area along the Urubamba River in Peru. This newly described titi monkey is a

Plate 16-3. Note how the nostrils open to the sides of the nose on this Mantled Howler Monkey (Alouatta palliata). That is typical of the platyrrhines, or New World monkeys. Photo by John Kricher.

taxonomic split from the Brazilian Brown Titi Monkey (C. brunneus). It may seem amazing that a group as well known as the primates is still presenting us with new species. However, Amazonian primate diversity has historically presented taxonomic problems; recently, more study combined with new information about the genetics and ecology of Neotropical monkeys has clarified the status of various previously problematic examples. Nonetheless New World monkeys remain a taxonomic work in progress and more changes in classification are likely. Even as more is learned about the classification of New World monkeys, more species are considered threatened or endangered. The IUCN currently lists 58 monkey species as threatened and 33 as endangered (of which 12 are considered critically endangered). The reason for loss of primates has to do with extensive forest clearance and fragmentation as well as local hunting pressure (chapter 18). Platyrrhines have not only extensively speciated but also adaptively radiated to occupy many ecological niches in various kinds of Neotropical forest. There are large apelike monkeys (spider, woolly, and howler monkeys), medium-size “typical” monkeys (capuchins and squirrel monkeys), monkeys with bald faces (uakaris), monkeys with long, shaggy fur (sakis), nocturnal monkeys (night monkeys or douroucoulis), small, lemur-like monkeys (marmosets), and squirrellike monkeys (tamarins). New World monkeys are forest animals, avoiding savannas. There are no Neotropical equivalents of the mostly terrestrial baboons that roam the African plains.

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Plate 16-4. The Black-striped Capuchin (Sapajus [Cebus] libidinosus), sometimes called Bearded Capuchin, is typical of the capuchins. It has been observed to crack nuts using a stone, an example of tool use. Photo by Andrew Whittaker.

Plate 16-5. Humboldt’s White-fronted Capuchin (Cebus albifrons) feeding on a large, nutlike fruit. Photo by Andrew Whittaker.

Plate 16-6. Humboldt’s White-fronted Capuchins are known to be generalized foragers. This one is eating what appears to be a frozen treat normally eaten only by humans, particularly children. Feeding wild monkeys is not recommended. Photo by Andrew Whittaker.

Plate 16-7. The Brown Capuchin (Sapajus [Cebus] apella) ranges throughout Amazonia and is one of the most often sighted of the capuchins. Photo by John Kricher.

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Plate 16-8. Common Squirrel Monkey. Look closely, as there is a baby on its back. Photo by Andrew Whittaker.

Plate 16-9. A group of Spix’s Night Monkeys (Aotus vociferans) peering out of their shared tree cavity. Photo by Andrew Whittaker.

Monkeys occupy interior forest, disturbed forest edge, gallery forests, and dry forests. They are most diverse and abundant in lowlands, but some occur in humid montane forests. All are arboreal, and most species rarely come to the ground, though some, such as the capuchins and uakaris, occasionally do so to feed. Taxonomically, the platyrrhines are divided into the “typical” monkeys, placed in the family Cebidae; and the tamarins and marmosets, sometimes called the “squirrel-like” monkeys, in the family Callitrichidae. Goeldi’s Monkey (discussed below), formerly placed in its own family (Callimiconidae), is now placed in Callitrichidae. Marmosets and tamarins are small, and the group includes some of the world’s smallest primates, such as the 15 cm (6 in), 85 g (3oz) Pygmy Marmoset (discussed below). The largest Neotropical monkeys are cebids, the biggest of which are the 9 kg (20 lb) howlers. There are no Neotropical equivalents of the great apes (the orangutan, gorilla, and chimpanzees), though spider monkeys are ecologically and anatomically similar to gibbons (small apes). Among the more commonly seen monkeys are the capuchins (plates 16-4–7), which range from Amazonia through southern Central America. There are currently 16 species, listed in the genera Cebus and Sapajus. Capuchins are 30–60 cm (1–2 ft) in length, excluding the 46 cm (18 in) prehensile tail, and weigh from 0.9 to 4 kg

(2–9 lb). They vary from pale brown to black, and each species has a pale face surrounded with whitish hair. Troops, typically numbering from five to 30 or more (depending on species), move quickly through forests foraging for fruits, leaves, and arthropods. Some also take birds’ eggs, baby birds, and even small mammals. Capuchins are found in a wide variety of forest habitats, and one is apt to encounter a capuchin group anywhere from low tangle along the forest edge to the canopy of interior forest. They also frequent gallery forests, dry forests, and mangrove forests, as well as disturbed and mature rain forest. Capuchins feed heavily on palm nuts and thus are frequently seen among the fronds in palm stands. They often function as seed dispersers. Capuchin troops are noisy, and their vocalizations sometimes attract agoutis and Collared Peccaries, which feed on fruits dropped by the simians. Titi monkeys (Callicebus spp.) are smaller than capuchins. They have small faces and are thickly furred, body color ranging from gray to black, with nonprehensile, hairy tails. Titis are found in small groups of two to six. Diurnal and highly active, they are very skilled treetop jumpers. They feed on a wide variety of fruits, buds, and various arthropods (including spiders and millipedes), though one species, the widespread Dusky Titi (C. moloch), feeds especially on leaves. Titis seem to seek out thick jungle growth in which to feed

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Plate 16-10. This Panamanian Night Monkey (Aotus zonalis) clearly displays its thickly furred, non-prehensile tail. Photo by Dennis Paulson.

Plate 16-11. White Uakari (Cacajao calvus calvus). In 2008 this subspecies was listed by the IUCN (International Union for Conservation of Nature) as vulnerable, due to hunting pressure and habitat loss. Photo by John Kricher.

and rest, often frequenting bamboo thickets. Titis are known for their dawn chorus, a loud, ringing duet performed by pairs. They are confined to Amazonia. Squirrel monkeys (genus Saimiri) are widely spread in Amazonia and into Central America. The Common Squirrel Monkey (S. sciureus; plate 16-8) is found throughout much of upper Amazonia. The Central American Squirrel Monkey (S. oerstedii) is an endangered species whose range is restricted to a small area along the Pacific coast of Costa Rica and Panama. Taxonomists are not in full agreement about the systematics of this group. A squirrel monkey does not resemble a squirrel. It is a bit smaller than a capuchin, but its tail is equally long, which gives it the appearance of a slender little animal with an immensely long, thin, black-tipped tail. The appealing eyes are dark, appearing quite large, and surrounded by white “spectacles” that are contrasted by a black nose and mouth. Ears are white. Body hair is grayish, with rich rusty coloration on the back, arms, and tail. The Central American species is rustier in color than the species in South America. Squirrel monkeys favor gallery forests, lowland rain forest, and successional areas. They are usually obvious, as their troops number anywhere from 20 to over 100 animals, and they tend to be highly active among the trees’ outer branches. They sometimes come around villages to

feed on bananas, plantains, and citrus. They eat many kinds of fruits, as well as numerous insects. Night monkeys, or douroucouli (Aotus spp.; plates 16-9–10), are well named, as they are the only genuinely nocturnal species. These smallish (0.9 kg/2 lb) monkeys with soft grayish-brown pelage range from northern Argentina and Paraguay throughout the Amazon Basin and north into Panama. One look at the somewhat owl-like, rounded head, with immense dark eyes surrounded by white fur, is enough to discern the creature’s nocturnal way of life. Groups of two to five night monkeys spend the daytime hours cuddled together in a hollow tree or among dense vines and other vegetation. At night they forage anywhere from almost ground level to the top of the canopy. They search for fruits, buds, insects, and occasionally nestling birds. Their densely furred, black-tipped tails are not prehensile. Their loud calls, heard at night, keep the foraging troop together. Taxonomists do not agree as to how many species there are, but up to 12 species have been recognized, all very similar in appearance. Uakaris (Cacajao spp.) are medium-size to large monkeys of gallery forests along the upper Amazon. Two species are currently recognized by IUCN. Cacajao calvus, found in várzea forests, has two subspecies, the Red Uakari, with long, thick reddish body hair, and the White Uakari (plate 16-11), with silvery-white body

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Plate 16-12. Brown Bearded Saki (Chiropotes chiropotes). The red testicles of this mature male are evident in the photo. Photo by Andrew Whittaker.

Plate 16-13. The White-bellied Spider Monkey of northwestern Amazonia is now considered to be an endangered species. Photo by Andrew Whittaker.

hair. In both subspecies, the head is both bald and bright red, making the animal unmistakable. The other species, the Black Uakari (C. hosomi), found in igapo forests, is entirely black, and the face (but not the entire head) is bald. Uakaris (pronounced WOK-a-rees) have short, hairy, non-prehensile tails. Groups of 10 to 30 or more animals feed on fruits, leaves, flowers, and arthropods, especially caterpillars. They sometimes descend to the ground to forage on seedlings and fruits. Unfortunately, both species of uakaris are considered endangered due to hunting pressure and loss of forest to logging. The sakis (Pithecia spp.; plate 1-22) and bearded sakis (Chiropotes spp.; plate 16-12) resemble uakaris in general body shape and in having long hair, but they have dense hair on their heads and faces, and their thick, bushy non-prehensile tails are longer than those of uakaris. Most are brownish gray or black. One species, the Guianan Saki (Pithecia pithecia), is strongly sexually dimorphic, the male black with a white face, the female gray-brown. There are, debatably, six saki species and four bearded saki species found

in various places throughout Amazonia. Sakis, rather like the lemurs of Madagascar, are skilled at leaping from tree to tree, which has earned them the Spanish name volador, or “flier.” Small groups, rarely exceeding five animals, feed primarily on fruits and are found mostly in well-developed rain forest. Sakis are not nearly as uncommon as uakaris. Bearded sakis also feed primarily on fruits but are found in larger troops, numbering up to 25 to 30 individuals. Spider monkeys occur from Mexico southward through the lower Amazon. There are seven species in the genus Ateles and two in the genus Brachyteles. They are generally geographically separated, though there are many areas where the ranges of two species are parapatric (sharing a common border but not significantly overlapping). Because there is much variation in color within some of the species, spider monkeys are more easily identified by range than by appearance. The three common and wide-ranging species are the Central American Spider Monkey (Ateles geoffroyi), which ranges throughout Central America

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Scared Monkeys and Angry Monkeys It is insightful to contrast primate behavior in areas where the animals are hunted regularly to behavior in areas in which they enjoy complete protection. Where they are hunted, monkeys become fearful and wary, attempting to remain out of sight in the canopy when humans approach. Near Manaus, Brazil, capuchins have apparently learned to descend to the ground so as to run through underbrush and avoid hunters. In unprotected forests where monkeys are regularly shot for food, I have seen troops of spider monkeys frantically dash through the canopy, apparently attempting to avoid the humans below. However, in a protected forest near Alta Floresta, Brazil, south of the Amazon, the presence of my group actually attracted a troop of White-bellied Spider Monkeys, which behaved belligerently, approaching us quite closely in the forest, climbing into the understory and lower canopy, vigorously shaking branches, loudly vocalizing, and eventually urinating and defecating on us. These monkeys do not normally encounter humans and apparently regarded us as invaders into their territory. Similar accounts are common where monkeys and humans infrequently meet. It was a fulfilling experience to see these animals so closely—though prudent to wear a hat. In places where monkeys and humans do frequently meet, but where monkeys are protected, the monkeys do not act aggressively toward humans but seem to view us as we view them, curiosities of nature (plate 16-14).

into southern Mexico; the Black Spider Monkey (A. paniscus), which has two population centers, one east of the Río Negro and north of the Amazon and one in western Amazonia west of the Rio Madeira; and the White-bellied Spider Monkey (A. belzebuth; plate 1613), once found widely southeast of the Amazon as well as northwest of it in parts of Peru, Colombia, and Venezuela, but now listed by the IUCN as endangered. Spider monkeys are large but slender (hence the name), generally weighing about 6.4 kg (14 lb). Their prehensile tails range up to 90 cm (35 in) in length. They vary in color from black to pale brown to reddish. Troops of spiders typically consist of about eight adult males, 15 adult females, and 10 babies and juveniles. At any given time, four females will be either pregnant or in estrus. Bachelor male troops also occur. Often fewer animals are seen together, because troops frequently fractionate in a given area during the day, reassembling at their sleeping

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Monkey species are hunted to varying degrees throughout Amazonia, where several of the larger species are important food sources for indigenous people. In general, where human populations are low, monkey hunting is usually not so severe as to markedly deplete the primate populations. Where human populations are dense, local monkey populations may be significantly reduced, and monkeys try hard to avoid humans. It is obvious that the most important considerations in maintaining primate populations is to assure the presence of large tracts of natural forest accompanied by freedom from hunting pressure.

Plate 16-14. These two—note the face at the bottom of the photo—Mantled Howler Monkeys show no fear of our group. They occupy an area in Panama where they are free from local hunting pressure and are also frequently exposed to people, so they do not act aggressively. Photo by John Kricher.

tree at night. Spiders forage together in the treetops, often quite actively. Their slender bodies adapt them well for graceful movement through the canopy, and they seem to prefer mature forest. Spider monkeys often move by brachiation, swinging arm over arm from branch to branch in a manner similar to Old World gibbons. As discussed in chapter 11, spider monkeys feed heavily on fruits, though they also consume some leaves. One of the most endangered Neotropical monkeys is the Southern Woolly Spider Monkey, or Muriqui (Brachyteles arachnoides), an inhabitant of the threatened coastal forest of southeastern Brazil. It is estimated that only 300 to 400 of these creatures remain, scattered widely in fragments of what was at one time continuous forest. As is the case with some other endangered species, this animal was initially hunted for food and is now mostly threatened by habitat loss.

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Woolly monkeys are a group of six species (genera Lagothrix and Oreonax; plates 8-13 and 16-15) named for their thick woolly fur, which may be black, brown, grayish, or reddish, depending both upon species and geographic location (there is much variation). The Common Woolly Monkey (Lagothrix lagothricha) ranges throughout western Amazonia. Woollies are larger than spider monkeys, weighing up to 10 kg (22 lb), and in body shape they more closely resemble howler monkeys (discussed below). Like howlers and spiders, woolly monkeys have prehensile tails and are highly skilled arboreal acrobats. They prefer mature forest, where groups of between two and 60 monkeys feed on fruits, palm nuts, seeds, foliage, and some arthropods. They feed at varying heights, not being confined to the canopy, and can be found in both seasonally flooded and terra firme forests. Woollies are intensively hunted, because the meat is tasty and the animals themselves are large. They have a generally low reproduction rate and cannot maintain their populations against strong hunting pressure. Howler monkeys (Alouatta spp.) are as large or larger than woolly monkeys and are the most well studied Neotropical monkeys. Many primatologists have focused on howlers, including studies of their various behaviors, troop sizes, communications, territoriality, vocalizations, and feeding habits. Howlers are large and robust monkeys with prehensile tails and bearded faces. They are widespread, distributed from the Amazon Basin south to Argentina and Paraguay and north to Trinidad, Central America, and the Yucatán Peninsula. There are 11 species, two of which are considered endangered. The most widespread is the Red Howler Monkey, historically known as A. seniculus and the subject of much fieldwork. Recently the IUCN has split it into the Guianan Red Howler Monkey (A. mcconnelli) and the Bolivian Red Howler Monkey (A. sara), but be aware that most of the descriptions in the literature were written prior to the split and thus refer to it as the Red Howler Monkey and A. seniculus. Red howlers of either species are recognized by bright reddish fur, hence the common name (plate 16-16). Red howler species occur throughout northern South America north of the Amazon and east of the Andes, including Trinidad. They are replaced south of the Amazon and throughout central and eastern Brazil by the Red-handed Howler (A. belzebul), which has all-black fur except on the hands, feet, tail, and (on males) scrotum, where it is

Plate 16-15. The Yellow-tailed Woolly Monkey (Oreonax [Lagothrix] flavicauda) is found only in Andean humid montane forests in Peru and is considered an endangered species. Photo by Andrew Whittaker.

rusty red. The Black Howler (A. caraya; plates 16-17–18) is found in extreme southern Amazonia into Paraguay and Argentina. It is sexually dimorphic in coat color, the males being all black, the females tan. The Brown Howler (A. guariba), whose coat color is uniformly warm brown, is found in southeastern Brazilian coastal forests and in northeastern Argentina, and, though not yet considered endangered, it is experiencing rapid loss of habitat. Both species of endangered howlers occur largely (one entirely) in Middle America. The Mexican Black Howler (A. pigra), an all-black species quite similar in appearance to the Black Howler, is found only on the Yucatán Peninsula, in Mexico, Belize, and Guatemala. The Mantled Howler (A. palliata; plate 16-14), essentially black but tan-brown on its sides and back, is found west of the Andes from northern Peru to Colombia and throughout Central America to southern Mexico. Though this range is extensive (and does not overlap with that of the Mexican Black Howler), the populations have been reduced in some places due to forest fragmentation. Howlers are named for their loud and intimidating vocalization, which echoes through the rain forest mostly at sunrise and sunset (plate 16-19). The sound is more like a roar than a howl. Males have an enlarged

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Plate 16-16. A family of red howler monkeys (Alouatta sp.). Mothers are very protective of their offspring. Photo by Andrew Whittaker.

Plate 16-17. Male Black Howler Monkey grasping a branch with its prehensile tail. Photo by Andrew Whittaker.

Plate 16-18. This female Black Howler Monkey had given birth in this tree just minutes before this photo was taken. Her infant is clinging to her underside. Female Black Howlers are tawnycolored; only the males are black. Photo by John Kricher.

Plate 16-19. This red howler monkey is sounding off, making his troop’s territory well known. Photo by Gina Nichol.

throat sac and huge tracheal cartilages that act as a resonator, dramatically amplifying their calls. Howling serves to mark the troop territory; because the howling carries for nearly 1.5 km (1 mi) through rain forest, two troops can come to a mutual agreement about realestate boundaries without necessarily ever meeting one another. Male howlers are approximately 30% larger in body size than females, and this difference, plus the unique male vocal apparatus, suggests strong sexual selection in this species complex. An average howler clan consists of three adult males, seven to eight females, and varying numbers of juveniles. Clans vary in size, however, ranging from four to 35. Males are dominant over females, and young animals tend to be dominant

over older animals. Monkey troops frequently engage in mutual grooming behavior, an important behavior in maintaining troop cohesiveness. Howlers live in many forest types (mature and disturbed forests, gallery forests, semi-deciduous forests, lowland and lower montane forests) and, wherever they occur, specialize on a diet of leaves, with fruit and flowers making up only about 30% of their diet. Because they rely so heavily on leaves, they tend to have fairly small territories. Why small? Well, leaves are pretty abundant in rain forests, so for howlers food is pretty much everywhere. This is not to say that all leaves are equally tasty or even equally safe—far from it (recall chapter 11). But leaf biomass assures sufficient palatability to allow territories to be small, and that means howlers

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Plate 16-20. The Emperor Tamarin (Saguinus imperator) sports a prominent moustache. The species occurs widely in western Amazonia. Photo by Sean Williams.

Plate 16-21. The Black Tufted-ear Marmoset (Callithrix penicillata) is one of six closely related and similar species that were until recently considered subspecies. It inhabits dry and upland forests in much of east-central Brazil. Photo by Kevin Zimmer.

are particularly abundant and frequently encountered. Their diet, a mixture of mature and young leaves as well as flowers, leaf petioles, and some fruit, affords sufficient protein (mostly from mature leaves) and minimizes the amount of indigestible fiber and potentially toxic defense compounds ingested. Howlers are more often heard than seen, as they tend to remain well up in the canopy of mature rain forest and, as mentioned earlier, their howling carries long distances. Nonetheless, there are numerous areas where howler monkeys are easy to observe. Howlers and other monkeys on Barro Colorado Island, Panama, are apt to suffer a high natural mortality rate. Katherine Milton, in a now-classic study focused on howler monkeys, found that seasonal changes in food availability, plus periodic unpredictable shortages of high-quality foods, placed major stresses on the population. Years of severe El Niño events, such as 2015–16, may result in significant increases in mortality (recall discussion in chapter 2). In addition, monkeys are commonly parasitized by botflies (see the Appendix), though most monkeys appear to survive their botfly wounds. Still, such parasitic afflictions can’t be pleasant for the simians. Marmosets and tamarins (plate 16-20), are diminutive monkeys, the gnomes of the rain forest, scurrying through the branches, peeking out from behind leaves often larger than they are. They resemble hyperactive squirrels as they scatter about in the low tangles of branches, constantly scanning in all directions. They share the habit of leaping from one branch to another, landing vertically. Their tails, while used for balance, are non-prehensile. These small monkeys may be found in interior forest but also favor gaps and disturbed areas, where insects and small fruits are abundant. Many feed in the lower story of forest as well as forest edge. Marmosets comprise 22 species, all of which are confined to South America. Among them are the Black-tufted Marmoset (Callithrix penicillata; plate 16-21), found in cerrado forests from central and southeastern Amazonia to coastal Brazil; and the tiny Pygmy Marmoset (Cebuella pygmaea), which ranges throughout much of western Amazonia. The Pygmy Marmoset is yellowish-brown, with thick fur surrounding its tiny face. Marmosets of the genus Callithrix have somewhat shaggy fur, ranging in color from nearly white to grizzled gray and black, and long tails. Their faces are small but accentuated by prominent tufts of fur about the ears.

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Plate 16-22. Geoffroy’s Tamarin. Photo by Nancy Norman.

Plate 16-23. Goeldi’s Monkey is listed by CITES (Convention for International Trade in Endangered Species) as endangered. Photo by Andrew Whittaker.

Marmosets are too small to be regularly hunted, thus many often occur near human habitations and often are found in and around fruiting trees. They feed on berries, buds, fruits such as bananas, and various arthropods. Some have the odd habit of “sap-sucking,” which involves gnawing holes into a favorite tree trunk and drinking the oozing sap. Their lower incisors are long, an aid in chewing holes to harvest sap There are 15 species of tamarins in the genus Saguinus and four in the genus Leontopithecus. As a group tamarins are fairly similar in general appearance to marmosets. They have long tails, shaggy fur, often with striking coloration patterns, and their small faces are accentuated by topknots, moustaches, or ruffs. Like marmosets, tamarins search mostly for insects and other arthropods, as well as fruits, but they do not drill holes in search of sap. Tamarins are essentially confined to South America, though one species, Geoffroy’s Tamarin (Saguinus geoffroyi; plate 16-22), ranges into Central America as far north as southern Costa Rica. The most widely distributed species are the Midas Tamarin (S. midas) of northeastern Amazonia and the Saddleback Tamarin (S. fuscicollis), found in western Amazonia. Other species have much narrower ranges. Goeldi’s Monkey (Callimico goeldii; plate 1623) is a unique, tamarin-like monkey found in terra firme forests east of the Andes from Colombia to Bolivia, Brazil, and Peru.

Twenty-two marmoset and tamarin species are listed by IUCN as currently declining and some of these have declined to the point where they are considered endangered. The Golden Lion Tamarin (Leontopithecus rosalia; plate 1-26) arguably the most beautiful of the group, is the most endangered of any Neotropical monkey, considered to be in extreme danger of extinction. Found in southeastern Brazil, the species has lost over 90% of its habitat, and its total population is estimated at about 1,000 individuals. Tamarins and marmosets are unusual among primates for their flexible breeding systems. In some ways they seem to exhibit the reverse of the normal primate pattern. A single female tamarin may mate with several males (polyandry), without creating aggression among the males. Tamarin groups normally consist of four to six adults, typically two or more females and several males. Females are aggressive toward one another, and one female does all of the breeding in the group. Several males mate with the alpha female, and males devote much energy, more so than females, to parental care.

Rodents: Agouti, Paca, and Others Rodents, in the order Rodentia, are distinct among mammals in having a large pair of continuously growing, chisel-like incisors, with which they gnaw all manner of food. There are approximately 2,000 rodent

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species in the world, and that number represents about 40% of all mammal species. By far and away the most diverse order of mammals, Rodentia is rivaled in diversity only by Chiroptera, the bats (see chapter 8), but globally bats have only about half of the species represented by rodents. The Neotropics harbor some of the most ecologically interesting species, as well as the largest, of the vast assemblage of rodents. Several are aquatic, others arboreal, and still others are burrowers. Some are familiar, similar to those found away from the tropics. These include such groups as tree squirrels, pocket mice, rice rats, and the familiar House Mouse (Mus musculus), each of which descended from ancestors that colonized the Neotropics from elsewhere. Others, like the porcupines, spiny rats, agoutis, pacas, and capybaras, members of what is known as the Caviomorpha (or Hystricognathi) rodents, are evolutionarily unique to the Neotropics, having originated there. Caviomorph rodents include the familiar domestic guinea pig (Cavia porcellus), chinchillas (Chinchilla chinchilla), and the North American Porcupine (Erethizon dorsatum). Agoutis (Dasyprocta spp.; plate 16-24) are among the most common of the larger rodents, represented by 11 species that range from tropical Mexico to northern Argentina and Paraguay. Each species has a similar ecology. Primarily diurnal, agoutis are apt to be encountered anywhere inside forests. One of my students described an agouti (as well as its close relative the paca) rather well by asking me, “What are those little piggy things running across the trail?” Agoutis do not look like “little piggy things” when seen close up, but from a distance their chunky, 64–75 cm (25–30 in) bodies, long legs, and delicate prancing gait give an impression of a small, tailless (though they have very short tails), hoofed animal with the head of a mouse. Depending mostly upon species, they range in coat color from buffy reddish brown to grizzled gray and black. They eat by sitting upright on their hind legs, holding their food (usually a fruit or seed) with their front paws in a manner suggestive of mice and squirrels. Agoutis are often important seed dispersers, collecting more seeds than they can consume at once and burying the remainder in a widely scattered pattern. The wide-pattern burial behavior, termed scatter hoarding, is possibly adaptive in protecting the agouti’s cache from discovery by other seed consumers, such as peccaries. During times of shortage, agoutis dig up their buried seeds. Agoutis are vocal, and when

Plate 16-24. The Central American Agouti (Dasyprocta punctata) is a member of a New World branch of the rodents known as the caviomorphs. Photo by Dennis Paulson.

Plate 16-25. This is a rare sighting of a Lowland Paca during the daylight hours, scurrying through the deeply shadowed forest floor. Photo by Andrew Whittaker.

Plate 16-26. The world’s largest rodent, the Capybara can be up to 1.2 m (4 ft) long and weigh as much as 54.4 kg (120 lb). Photo by John Kricher.

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Plate 16-27. The Mexican Hairy Dwarf Porcupine (Sphiggurus [Coendou] mexicanus) is common throughout much of southern Mexico and Central America. It is not found in South America. Photo by James Adams.

Plate 16-28. A rare sighting of a Brazilian Porcupine on the ground, wandering across an open stretch of the Llanos in Venezuela. Sometimes also called the Prehensile-tailed Porcupine, it tends not to leave the safety of trees. Photo by John Kricher.

frightened by a predator they often emit a high-pitched alarm bark. An acouchy is another type of rodent, represented by two species in the genus Myoprocta. Acouchys look very much like smaller versions of agoutis but have short, yet obvious tails. Both species are found in northern Amazonia and are ecologically similar to agoutis. When agoutis retire for the evening, the Lowland Paca (Cuniculus paca; plate 16-25) comes out. There are two paca species, one in the Neotropical lowlands that ranges from tropical Mexico to northern Paraguay, the other, the Mountain Paca (C. taczanowskii), is found in higher elevation forests in northern South America, from Peru to Venezuela. Pacas are common but are less frequently seen than agoutis because of their nocturnal habits. Pacas seem to prefer to be near water, and daytime hours are typically spent resting in a burrow along a stream bank. Monogamous, males and females share a single territory but nonetheless forage alone and occupy separate dens. Pacas resemble agoutis in shape but have larger eyes and longitudinal white stripes and spots along the sides of their reddish-brown coat. Their bodies are larger and legs proportionally shorter than those of agoutis, and pacas weigh more, up to 10 kg (22 lb). When threatened by a predator, a paca will retreat to water and remain immersed until out of danger (or air). Pacas, like agoutis, feed on fruit but also take leaves and other plant materials, including certain tubers. Unfortunately, paca meat is considered to be highly tasty by humans, and pacas have been overhunted in various regions.

A more easily seen Neotropical rodent is the enormous Capybara (Hydrochoeris hydrochaeris; plate 16-26). It is discussed in chapter 12. Seventeen species of New World porcupines and dwarf porcupines (Erethizontidae; plate 16-27) are found in the Neotropics, and one species, the North American Porcupine, is a well known resident in northern and mountainous North American forests. All porcupines bear stiff hairs that often form sharp quills, but they differ from the familiar and related North American species in that they have prehensile tails. All porcupines have short faces with large, bulbous noses and rather small eyes and ears. One of the most wide-ranging and frequently encountered species is the Brazilian Porcupine (Coendou prehensilis; plate 16-28), which ranges throughout Amazonia, from extreme northern South America to southeastern Brazil. Nocturnal and almost entirely arboreal (aided by a strong prehensile tail), it climbs through the trees like either a slow monkey or a fast sloth, depending upon your frame of reference. Neotropical porcupines feed on a combination of fruits (including those of palms), bark, and leaves, though the diets of some species are not well studied. Spiny rats and tree rats (family Echimyidae) are the most diverse group of caviomorph rodents, with as many as 100 species ranging throughout the Neotropics. Spiny rats (Proechimys spp.) are common but are solitary and nocturnal and thus not often observed unless one searches at night. The fur has spines, particularly in the region of the lower back and

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hind legs, but the spines lack barbs. Spiny rats, like some lizards, have tails that can break off with a minor tug, an adaptation that permits escape from a predator, though with the cost of a tail. Spiny rats are found on the forest floor but the closely related tree rats (Echimys spp.) are arboreal. Trees provide habitat for approximately 20 species of Neotropical tree squirrels (mostly in the genus Sciurus), which are similar in appearance to North American tree squirrels (also Sciurus). The ancestors of these animals ventured southward during the great faunal interchange of the Pleistocene (chapter 8). Some Neotropical sciurids are reddish, including the Amazonian Red-tailed Squirrel (S. granatensis). One particularly striking species is the Central American Variegated Squirrel (S. variegatoides), which ranges in color from white with a black back, to reddish black, to blackish gray, depending upon range. To my eyes, the most wonderful of the lot is the diminutive Amazon Dwarf Squirrel (Microsciurus flaviventer), an adorable and hyperactive little brownish rodent with a thin, straight tail and big, curious eyes. This largely solitary creature, undersize for a squirrel, lives most of its life in the canopy. Finally, there is a group of rodents collectively called spiny pocket mice (genera Heteromys and Liomys). These little mice look very much like North American deer mice and white-footed mice (genus Peromyscus). They feed mostly on seeds.

Plate 16-29. Collared Peccaries remain in family groups and are usually not aggressive. Photo by Andrew Whittaker.

Plate 16-30. White-lipped Peccaries are greater in body size than Collared Peccaries. They form larger herds and have a reputation for being aggressive on occasion. Photo by Andrew Whittaker.

Collared and White-lipped Peccaries Peccaries are members of the huge even-toed ungulate order, the Artiodactyla. They closely resemble wild pigs but are in their own family, the Tayassuidae. They differ from pigs in that their upper canine teeth are extremely sharp and point straight downward, whereas in pigs these teeth curve outward as tusks. Peccaries also have a dorsal scent gland, located toward the posterior of their backs. This gland exits through a large and conspicuous opening that was once mistaken for the animal’s navel! The secretion from the gland is quite musky, and the animals rub their faces vigorously against one another’s scent gland as a means of recognition and solidification of the herd. Peccaries are highly social animals and are rarely seen singly. The most common, and also the smaller, of the two peccary species is the 22.7–29.5 kg (50–65 lb) Collared Peccary (Pecari tajacu; plate 16-29). This species is

Plate 16-31. This White-lipped Peccary is exhibiting aggressive behavior, staring directly ahead, with its bristly upper back fur erect. It’s time to move away. Photo by Andrew Whittaker.

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abundant in forests and savannas throughout tropical America as far south as Argentina and ranges northward through the Mexican deserts into the American Southwest. Collared Peccaries form herds of any number from three to 30 or more. Their bristly hair is a mixture of black and gray in adults, but it is quite brownish as juveniles. The name Collared is a reference to a band of whitish hair that separates neck from shoulder. The Collared Peccary’s face is unmistakably pig-like; its snout has a hard fingernail-like rhinarium, which acts as a trowel in rooting up vegetation. Herds of peccaries forage, in the manner of pigs, for roots, bulbs, and underground stems, as well as leaves and fruits. They also eat arthropods and small vertebrates, if they can catch them. Loose soil from their rooting efforts is a common sight in rain forests, along with the prints of their small cloven hooves. During dry season they often congregate at favored watering places. As they forage, peccaries communicate with soft continuous grunts, but should danger threaten they emit a loud deep Woof! reminiscent of a large dog’s bark. When cornered, they erect their bristles, chatter their teeth, and display their large canines. They put on quite an impressive show of threat but will not charge (usually) unless no escape is possible. Collared Peccaries are fundamentally peaceful, highly social animals, though they have an undeserved reputation for aggression. Should you encounter a band of them, give them a wide berth, and they will go about their business, leaving you totally intact. The larger White-lipped Peccary (Tayassu pecari; plates 16-30–31), identified by the white hair around its mouth, congregates in herds of 50 to 300 individuals and is essentially confined to rain forest, its range limited to the lowland forests of South America and southern Central America. White-lipped Peccary herds range widely in search of fruits. The species’ odor is distinct from that of the Collared Peccary. White-lipped Peccaries have been shown to be capable of cracking tougher fruits and seeds than Collared Peccaries and thus can make use of food items unavailable to their smaller cousins. The typically large herd size of White-lipped Peccaries may be related to the fruit crop: some of the trees with the hardest fruits, such as palms, drop many fruits at once, representing a temporarily abundant but highly patchy resource. In large herds, White-lips can find and exploit such a resource effectively. White-lips have a narrower rhinarium (the toughened end of the snout) than

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Collared Peccaries and do not dig as deeply for roots. They probably depend more heavily on hard fruits. Both Collared and White-lipped Peccaries are extensively hunted, and the White-lipped is currently considered vulnerable by the IUCN. White-lipped Peccaries have for many years been reputed to be unpredictably aggressive. Charles Waterton, in his classic volume Wanderings in South America (1825), describes peccary aggression thusly: There is scarcely a hunter who has not been forced to climb into the branches of trees in order to escape a herd of Peccaries, and even when they have driven him into a tree, they will sit round it, gnashing their tusks in anger. The sound of the clashing tusks is well known to hunters, and warns them to prepare for a charge. While peccaries are certainly capable of selfdefense and some strong offense, modern accounts of aggressive behavior by herds of White-lipped Peccaries are uncommon.

Neotropical Deer Like peccaries, deer (Cervidae) are artiodactyls, even-toed (also called cloven-hoofed) ungulates. The familiar White-tailed Deer (Odocoileus virginianus; plate 16-32), common throughout most of North America, also ranges throughout Central America and well into South America. The species adapts to

Plate 16-32. White-tailed Deer range widely and are found throughout the Neotropics, including within rain forest. Photo by John Kricher.

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numerous kinds of habitats, ranging from interior rain forest (in Central America) to savannas, successional areas, and montane areas (in South America). The Marsh Deer (Blastocerus dichotomus; plate 1633) is found only in South America and is the largest of the Neotropical deer. True to its name, it is found only in marshes and is perhaps best observed in the Brazilian Pantanal, where it is considered relatively common. It is believed that the marsh itself helps protect these deer, reputed to be excellent swimmers, from the Jaguar and the Puma, their principal predators. But the primary threats to Marsh Deer now are habitat loss and hunting by people, principally for antlers. The IUCN lists the species as vulnerable. Two small deer species, called brocket deer, are also found in the Neotropics. The Red Brocket Deer (Mazama americana; plate 16-34) occurs in much of Central America, where it is found mostly in areas of dense vegetation and forest. It also ranges widely throughout Amazonia, where it is relatively common, particularly in dry forests. The other species, the Gray Brocket Deer (M. gouazoubira), occurs only in South America. The small size—they are only about 1 m (3.3 ft) long and weigh no more than 22 kg (48 lb)—makes it easy for brocket deer to move quietly and efficiently through dense understory. Antlers (on males only) are short and straight, with no branching. Brocket deer are in many ways ecological equivalents of the chevrotains or mouse deer (family Tragulidae) of Southeast Asian and African rain forests.

Plate 16-33. A buck Marsh Deer on the Brazilian Pantanal. Photo by John Kricher.

Plate 16-34. Red Brocket Deer. Photo by Sean Williams.

Tapirs Tapirs (genus Tapirus) are odd-toed ungulates (order Perissodactyla), evolutionary relatives of rhinoceroses and horses. Only four species of tapirs occur in the world, and three of them are in the American tropics (the fourth is in the Asian tropics). Tapirs are stocky, almost hairless animals, brownish to black, depending upon species, with a short elephantine proboscis and a dense but short mane of stiff hairs on their upper neck. The mane probably aids the animal in making its way through dense undergrowth. Tapirs have an acute sense of smell and select food plants at least in part on the basis of odor. They eat only vegetable matter, including leaves and fruits of various species. Research on a captive tapir at Barro Colorado Island, Panama, has suggested that tapirs may be a bit finicky about what plants they devour.

Plate 16-35. The Brazilian Tapir occurs within forests but also forages in more open areas, particularly at night. Photo by Steve Bird.

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The three Neotropical tapir species are separated by range and habitat, as discussed in chapter 8. The most widespread is the Brazilian Tapir (Tapirus terrestris; plate 16-35), which can be found east of the Andes from northern South America throughout Amazonia as far south as Paraguay. The Baird’s Tapir (T. bairdii) ranges throughout Central America and northern South America west of the Andes. The Mountain Tapir (T. pinchaque) has the most restricted range and is, as the name implies, essentially confined to higher elevations. It inhabits the páramos of the Central and Eastern Cordilleras of the Andes, from Colombia to Ecuador. Tapirs (and peccaries) are widely hunted, often with dogs, and thus tend to be wary. Hunting pressure throughout the range of the various tapir species has seriously reduced populations. Both Baird’s and Mountain Tapirs are listed as endangered by CITES and IUCN. The Brazilian Tapir is listed as locally endangered by CITES and vulnerable by IUCN. Tapirs are most active at night, and you will be very lucky if you manage to see one well. Look for tapirs along watercourses. They are frequent and excellent swimmers.

Sloths, Anteaters, and Armadillos Sloths and anteaters are among the most characteristic (and “must-see”) animals of Neotropical rain forests. Along with the armadillos, one species of which ranges into North America, they compose the magnaorder Xenarthra (also called Edentata), creatures united by a number of anatomical characteristics. Anteaters, with

Plate 16-36. This Brown-throated Three-toed Sloth has adopted a typical lethargic posture in a cecropia tree. Photo by Nancy Norman.

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their skulls modified for ingesting ants, are toothless, but sloths and armadillos have peg-like teeth on the sides of their mouths (front teeth are lacking). The term sloth, when applied to a person, has come to mean sluggish, lethargic, dull, and dim-witted. Real sloths (families Bradypodidae and Megalonychidae) are probably all of these things. These traits offer a tremendous advantage to you, however, because it means they do stick around once you find them. If you care to watch a sloth move from one tree to another, a distance that might take a few seconds for a monkey, plan to spend about a day or so. Sloths lead slowmotion lives. The three-toed sloths (genus Bradypus), the favorites of Charles Waterton, are the most commonly observed. Four species range throughout Neotropical forests, the most common of which is the Brown-throated Three-toed Sloth (B. variegatus; plates 16-36–37). A three-toed sloth looks somewhat like a deformed monkey. It has shaggy, tan-colored fur, long forearms and hind legs (but no tail), and a rounded face with very appealing eyes. Its sad, vacuous expression gives the impression that the gleam in its eyes is but the reflection off the back of its skull. The common name derives from the three sharp, curved claws on each of its four feet, which serve as hooks as the animal hangs upside down from a branch, like an odd mammalian Christmas tree ornament. The easiest way to find a three-toed sloth is to scan a cecropia, a favorite resting and feeding tree for sloths. Sloths frequent trees along riverbanks and disturbed areas and are much easier to locate in such habitats than in closed forest.

Plate 16-37. A Brown-throated Three-toed Sloth enjoying some cecropia fruits. For many years ecologists thought sloths ate only cecropia leaves, but they are much more diverse in their vegetarian diets. Photo by Dennis Paulson.

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Sloths and Moths As you know by now, tropical forests abound in unusual species relationships. The sloth discussion mentioned, for example, that numerous arthropods inhabit the fur of sloths. These include moths. Yes, moths. At least five moth species commonly inhabit sloth fur, presumably feeding upon the algae that grow liberally within the coarse, dense coat. The sloth-moth relationship is commensal. The sluggish mammals do not appear to gain any enhancement of probable survival and reproduction from hosting the lepidopterans. But the moths do gain fitness from inhabiting the sloth. They have access to food—but that’s not all. Sloth moths fly from the sloth’s fur when it descends from the tree and defecates. The moths lay their eggs directly on the sloth excrement. The moth larvae, or caterpillars, feed on the sloth dung before pupating.

Once they metamorphose into moths, where do they go? Why up into the canopy, of course, in search of a sloth to inhabit. And not just any sloth will do. The relationship has, at least in some cases, become evolutionarily tight. For example, the moth Cryptoses choloepi is only found in the fur of three-toed sloths, not two-toed. The sloth’s habitat is forest, but to the sloth moth, that is beside the point. Its habitat is a sloth or a sloth dropping, depending upon whether it is an adult or a larva. When you stop to think of the diverse bacterial community within the sloth’s gut, indeed the community that allows it to digest and thus to function, and add to that the diverse community of algae and animals that inhabit its fur, estimated to be in the hundreds of species, the sloth, sluggish as it is, is one impressive ecosystem.

Plate 16-38. Hoffmann’s Two-toed Sloth (Choloepus hoffmanni). Photo by Gina Nichol.

Plate 16-39. This three-toed sloth is holding its baby as it sleeps on a branch. Sloth hair grows in a reverse direction from the growth pattern in most mammals. Notice also the distinctive green tinge to the mother’s fur, indicative of the algal community that inhabits it. The baby has yet to acquire its algae and thus is much browner. Photo by Dennis Paulson.

Because three-toed sloths are usually observed in cecropia trees, and clearly devour the leaves, for years it was assumed that they ate only cecropia leaves. But detailed studies in which radio transmitters were used to follow sloths showed that they feed on leaves of numerous tree species, moving to a different tree about every day and a half. The problem is, when sloths are not in cecropias, which offer easy views of the animals, they are nigh impossible to spot. Sloth populations are estimated to be five to eight per hectare (2.5 acres) in Panama. This is considered

a high population density and is likely attributable to their ability to ingest many kinds of leaves and tolerate the defense compounds contained therein. Because sloths have an extraordinarily low metabolic rate, they do not eat as much as their numbers and body size (61 cm/24 in long, up to 4.5 kg/10 lb) might suggest. They are relatively efficient digesters, owing their prowess to a complex and long digestive tube and multitudes of gut bacteria that process, ferment, and digest the leaves. There are two species of two-toed sloths (genus Choloepus; plate 16-38). The two-toed is similar in

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habits to its better-known relative but distinguished by its larger size (it weighs up to 9 kg/20 lb) and two, rather than three, prominent claws on the front feet and four, rather than three, on the hind feet. Two-toed sloths are more confined to primary forest than three-toed species. Although the two kinds of sloths look similar, the three-toed and two-toed families are only distantly related. The two-toed sloths are considered more closely related to the extinct giant ground sloths (chapter 8). Because sloths spend so much time upside down, hanging by all fours from a tree branch, their fur has adapted, by natural selection, an orientation from the belly to the back, the opposite of the usual direction in mammals. The hairs of their coats are grooved and serve as habitat for numerous insects, mites, ticks, and algae. The algae are so abundant that sloths take on a greenish tinge (plate 16-39). It has been suggested (but not demonstrated) that the greenish appearance of an algal-dense sloth may serve to camouflage the animal in the foliage. Sloths are reputed to become browner in the dry season, when lack of rain results in fewer algae inhabiting their fur. Sloths come to the ground about once a week to defecate at the base of a tree. Three-toed sloths dig a small depression and cover their excrement, an operation that takes about 30 minutes. Two-toed slots do not dig. Descending to the ground to take care of business is undeniably an odd behavior, and ecologists have yet to explain it to everyone’s satisfaction. Should you wish to look into why sloths choose to descend to the ground to poop, at last check there were about 83,500 hits on Google to this profound and vexing question. Or see the sidebar “Sloths and Moths.” The most commonly seen of the anteaters (Myrmecophagidae) are the 60 cm (2 ft) long tamanduas. Two species occur, the Northern Tamandua (Tamandua mexicana; plate 16-40), in Central America and northern South America west of the Andes, and the Southern or Collared Tamandua (T. tetradactyla), in Amazonia as far south as northern Argentina. Both species are similar, with extended pointed snouts, formidable curved claws on the forelegs, prominent ears, and a long, prehensile tail. The coat color is variable, depending upon range. Some animals may be pure blond, others “vested” with black. Tamanduas are largely solitary and are active day or night. They are equally at home digging up ant nests in the ground or sampling the delicacies of termitaria in trees. They excavate with their sharp front claws and extract the insects using their extensible sticky tongues.

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Plate 16-40. The unmistakable Northern Tamandua is a frequently encountered anteater species, one that few forget. Photo by James Adams.

Plate 16-41. Bring it on. This tamandua is in threat posture. Those sharp claws provide it with considerable measure of protection. Photo by James Adams.

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Tamanduas eat many kinds of ants, as well as termites and bees. They tend to shy away from army ants and ponerine ants, both of which give nasty stings. When threatened, a tamandua may sit up on its hind legs and brandish its sharply curved claws (plate 16-41). Be aware that such behavior forecasts a potentially dangerous encounter for anything or anyone that bothers this anteater. Its forearms are strong, and the claws are formidable. The animal my look innocuous, but it isn’t. The ground-dwelling Giant Anteater (Myrmecophaga tridactyla; plate 16-42) is much larger than the tamandua anteaters. Its body measures about 1.2 m (4 ft) in length, and its huge bushy tail adds almost another meter (3.3 ft). Its head is shaped like a long funnel, with eyes and ears placed well back of the small mouth, from which can protrude a 51 cm (20 in) sticky tongue. The grayish-black coat color is marked on each side by a broad black stripe lined with white. The body terminates in an immensely thick, ragged tail. Like those of the tamandua, the front claws are curved and sharp, an adaptation to digging into the hardened ant and termite nests that contain the anteater’s dinner. The Giant Anteater ranges through Amazonia and southern Central America, though it is now rare throughout much of its range. The animal remains common along forest edge and in savanna areas such as the Llanos of Venezuela and the Pantanal of Brazil. Like the tamandua, the Giant Anteater will rear up and brandish its sickle-shaped, sharpened front claws if danger threatens. A fourth anteater species is the Silky or Pygmy Anteater (Cyclopes didactylus; plate 16-43). Smallest of the four, it reaches only 46 cm (18 in) in length. Don’t count on finding one of these little creatures, for they are nocturnal and arboreal, climbing about in thick lianas. They have soft golden-buffy fur, short snouts and claws, and a prehensile tail. Their large black eyes testify to their nocturnal habits. They are known to eat only ants. The other members of the Xenarthra are the ubiquitous armadillos (Dasypodidae), of which there are several species. One, the Nine-banded Armadillo (Dasypus novemcinctus; plate 8-43), ranges into southeastern North America and is expanding its range northward. Armadillos are slow-moving ground dwellers, whose hard bony skin protects them from most predators. When attacked, they curl up in a tight ball with their vulnerable soft parts tucked in. Mostly nocturnal, they are quite common, especially in savannas, and they feed on a variety of insects and other arthropods. The largest species is the Giant Armadillo (Priodontes maximus) a

Plate 16-42. The Giant Anteater is quite simply one of the most remarkable-looking animals on Earth. This one hastens across a road in Brazil. Photo by John Kricher.

Plate 16-43. Silky Anteater. Photo by James Adams.

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huge creature that ranges throughout South America as far south as Argentina. It is listed by CITES as rare and endangered over much of its range, and is extinct from some parts of it, all due to overhunting.

Neotropical Raccoons and Weasels The familiar Northern Raccoon (Procyon lotor; plate 1644), raider of garbage cans throughout much of North America, ranges southward as far as Panama. Should you be driving along a Central American road at night or camping inside a rain forest, do not be shocked if this black-masked, ring-tailed beast makes an appearance. Raccoons are members of the family Procyonidae, which also includes the coatis (or coatimundi), the Kinkajou, and the Olingo (discussed below). In addition to the Northern Raccoon, the Neotropics host another Procyon species, the Crab-eating Raccoon (P. cancrivorus), which ranges throughout Central and South America as far south as northeastern Argentina. This animal is similar in appearance to the Northern Raccoon, but its legs and feet are darker and its body is more slender. Crab-eaters frequent swamps and other aquatic areas and are generally nocturnal. Northern Raccoons overlap in range with Crab-eating Raccoons in Central America. However, where these two similar species overlap, Northern Raccoons frequent coastal mangrove swamps, while Crab-eating Raccoons are more partial to interior riverine areas. Coatis (Nasua spp.), sometimes called coatimundis, are pointy-nosed, familiar diurnal denizens of forests throughout the Neotropics. There are two species, the White-nosed Coati (N. narica; plate 16-45), which ranges from southern Arizona and New Mexico through Central America and into northern South America along the western side of the Andes, and the South American Coati (N. nasua; plate 16-46), found throughout Amazonia east of the Andes as far south as northern Argentina. Coatis have broad habitat tolerances, and can be found in the Andes, in deserts, and in savannas, as well as rain forest. Coatis usually travel in small bands mostly comprising females and young. The males tend to be solitary, except during breeding time. Coatis typically shuffle along, resembling streamlined raccoons with sharply pointed snouts, slender, grayish-brown bodies, and a long slim tail, usually with faint rings (you must be close to see this) and typically held upright, the way a cat holds its tail. Though their tails are not prehensile, coatis are

Plate 16-44. Northern Raccoon. Photo by John Kricher.

Plate 16-45. The White-nosed Coati has extensive white around its snout; it is common in Central America. Photo by Jill Lapato.

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Plate 16-47. Kinkajous are sometimes encountered during the day, but they are more commonly nocturnal. Photo by Gina Nichol.

Plate 16-46. The South American Coati has a dark snout and white chin. Photo by Sean Williams.

Plate 16-48. Kinkajous travel in family groups and typically forage at night. Photo by Sean Williams.

adept at tree climbing and are as apt to be seen in trees as on the ground. They feed on all manner of things, including fruits, ground-dwelling invertebrates, and lizards and mice. When they are not hunted, they become easy to observe. The Kinkajou (Potos flavus; plate 16-47) is smaller than a coati and uniformly grayish tan, and has an extremely long prehensile tail. The species ranges throughout forests of Central and South America. Kinkajous are as nocturnal as coatis are diurnal. They scurry about the tree branches at night, often making loud squeaking vocalizations, the banshees of the rain forest canopy. They can often be seen if you search by shining a flashlight with a strong beam that will penetrate the canopy at night (plate 16-48). Kinkajous have forwardplaced large eyes and wide, rounded ears and thus look a bit like monkeys. They feed mostly on fruits (look for Kinkajous in fig trees) but also take small animals.

The Olingo (Bassaricyon gabbii; plate 16-49) resembles a Kinkajou in face and body shape, but it has a grayer-brown coat color and a faintly ringed, non-prehensile tail. Olingos range less widely than Kinkajous, occurring mostly in humid forests of western Amazonia and much of Central America. They are not well studied and are seen far less often than Kinkajous, with which they share similar habits. They are nocturnal, rarely leave the trees, and feed on fruits and small animals. Some taxonomists have suggested that there are as many as six olingo species, all geographically separated. The weasel family (Mustelidae) is represented in the tropics by several noteworthy animals. The most common is the 60 cm (2 ft) long Tayra (Eira barbara; plate 16-50). Resembling a large mink or marten, the Tayra is a sleek, blackish-brown animal with a buffy face (which may be more black than buffy on some

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individuals) and a long, black bushy tail. It occurs throughout the Neotropics and, because it is diurnal as well as nocturnal, is observed frequently. Tayras lack prehensile tails but are good tree climbers. They are omnivorous, feeding on rodents, nestling birds, and lizards, as well as eggs, fruits, and honey. They occupy many different habitats, including rain forests, savannas, and coastal areas. They raise young in a den usually located in a hollow tree trunk. The Greater Grison (Galictis vittata), another mustelid, resembles a sleek badger. Smaller than the Tayra, the Greater Grison is a short-legged, slinkylooking animal with a grizzled gray back, black legs and throat, and a prominent white stripe behind the eyes. Its gray tail is short and thick. This grison ranges throughout lowland areas of the Neotropics. Like the Tayra, it is not confined to forests but can be spotted in savannas and other open areas, and it is commonly encountered near human habitations where chickens and other tempting morsels are present. Strictly carnivorous, it feeds on rodents and other small vertebrates. A second, similar species, the Lesser Grison (G. cuja), is found at higher elevations. Another Neotropical mustelid is the Giant Otter (Pteronura brasiliensis; plate 16-51), described in chapter 12. If you think you see or smell a skunk in the tropics, chances are you are right. The Eastern Spotted Skunk (Spilogale putorius) occurs as far south as Costa Rica, the Hooded Skunk (Mephitis macroura) gets into Nicaragua, and the hog-nosed skunk (genus Conepatus), of which there are several species, ranges as far south as Patagonia and up into the Andes. Skunks were once considered mustelids but are now usually placed in the family Mephitidae.

Plate 16-49. The Olingo, like the Kinkajou, is related to the raccoons. Photo by Sean Williams.

Plate 16-50. The Tayra is member of the weasel family, Mustelidae. Photo by Gina Nichol.

Neotropical Felines Most people who travel to the American tropics for the thrills of seeing wildlife, when asked which animal they would most like to see, would probably name El Tigre, the Jaguar (plate 16-52). The Lion may reign supreme on the African savanna, the Tiger in India, but in the Neotropical rain forest, Panthera onca is the top cat. Though this cat ranges from northern Mexico through Patagonia, it is now rare over much of its range and is listed by IUCN as near threatened. Only in the interior Amazon, remote montane forests, the Pantanal region of Brazil, and other areas out of the immediate reach of hunters’ gunfire, does the “Leopard of the New World”

Plate 16-51. The largest of the Neotropical mustelids is the Giant Otter. Photo by John Kricher.

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Plate 16-52. Jaguar resting on a riverbank in the Brazilian Pantanal. Photo by John Kricher.

Plate 16-53. This male Jaguar was photographed just as it was about to pounce on a caiman. It killed the caiman and carried it away. Photo by John Kricher.

Plate 16-54. Jaguar attacking a caiman. Photo by Nancy Norman.

remain unmolested. In the Cockscomb area of central Belize a reserve, the first of its kind, has been created specifically to preserve Jaguars. Jaguars resemble Leopards in spotting pattern but are generally heavier. Size varies considerably among individuals, but some individuals reach 160 kg (about 350 lb). An adult Jaguar has no nonhuman predators,

with perhaps the rare exception of the anaconda, the serpentine giant of the Amazon (chapter 12). Jaguars are ecological generalists. These cats are found in lowland rain forests, montane forests, savannas, wetlands, coastal mangroves, and along rivers. They feed on many kinds of animals, including deer, tapirs, peccaries, sloths, capybaras, Giant Otters,

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fish, birds, reptiles, and caiman (plates 16-53–54). A jaguar attacks its prey with a vigorous leap, quickly attempting to sever the neck vertebrae. The name jaguar derives from the South American Indian word yaguar, meaning “he who kills with one leap.” The Jaguar is largely solitary and basically nocturnal, and its footprints are seen more often than the beast itself. The best place to reliably see Jaguars is the Brazilian Pantanal, where ecotourism has proliferated in recent years. Ecotours to the Pantanal focus on seeing these large wildcats, which are not molested by humans here and are easily seen from a boat as they bask along riverbanks. Much smaller and considerably more common than the Jaguar are the Ocelot (Leopardus pardalis; plate 1655) and its close relative the Margay (L. wiedii; plate 1656), both of which range throughout the Neotropics. The big-eared, bright-eyed Ocelot is about 105 cm (3.4 ft) in length, including the long, thick tail. A large individual weighs about 11.3 kg (25 lb). The Margay is similar in appearance but slightly smaller. It is difficult to separate these species on the basis of a quick look, because their spotting patterns are similar. However, Ocelots tend to look more striped, with their spots run together, whereas the Margay’s spots do not tend to merge. Both small cats are essentially nocturnal, though Ocelots can sometimes be seen during the day, usually in dense cover. Margays are believed to be more nocturnal than Ocelots. As mentioned in chapter 9, Ocelots are terrestrial, but Margays are skilled tree climbers. Both animals are carnivores, feeding on anything from monkeys to insects. Like their domestic brethren, they spray to mark their territories. Jaguars, Ocelots, and Margays are the unfortunate victims of pelt seekers, who make profits from killing these magnificent cats. There is another Neotropical Leopardus, the Oncilla (L. tigrina), a small cat only about half the size of a Margay, which it otherwise resembles. Oncillas are poorly studied, and much about their ecology and even their range (from southern Central America through Amazonia) is uncertain. Of the various Neotropical cats, the Jaguarundi (Puma yagouaroundi) is probably the most frequently seen. It is common and diurnal, often found in savannas as well as forest. The Jaguarundi is also the most frequently misidentified cat; many who are unfamiliar with it assume it to be a large weasel and not a cat at all. It indeed looks superficially weasel-like, with its long and sleek body and long tail. It is 0.9–1.4 m (3–5 ft) in length,

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Plate 16-55. Ocelots are most commonly observed at night, while they are hunting. Photo by Sean Williams.

Plate 16-56. Margays can sometimes be seen during the day, as they rest in trees. Photo by James Adams.

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including the 0.3–0.6 m (1–2 ft) tail. Its coat color varies from dark brown to gray to black, depending on the individual. The Jaguarundi is totally terrestrial. Like the other cats, it is essentially solitary. The other large cat of the Neotropics is the Puma (Puma concolor; plate 16-57), also called the Cougar or the Mountain Lion. Pumas range widely in size; the largest individuals reach weights of up to 120 kg (265 lb). The species is widespread, ranging in North America as far north as parts of Canada and through Central and South America as far south as Tierra del Fuego. It is remarkably adaptable, an animal of open savannas, rain forest, windswept mountains, and many other habitats. Perhaps the most reliable place to see Pumas in the Neotropics is along the Andean slopes, where the cats feed on animals such as the Guanaco (Lama guanicoe; plate 16-58), which was discussed in chapter 13.

Plate 16-57. Female Puma aware that she is being observed. Photo by Andrew Whittaker.

Neotropical Canids The family Canidae (dogs, wolves, and foxes) is not diverse in the Neotropics, and only a few species are found either in or around rain forest. The Bush Dog (Speothos venaticus) and the Short-eared Dog (Atelocynus microtis) are forest species, and both are infrequently seen. The Crab-eating Fox (Cerdocyon thous; plate 16-59) is an animal of savannas and dry forest and is relatively common and easily seen. In addition, Coyotes (Canis latrans) occur in the Neotropics, though not in humid forest, as does the Gray Fox (Urocyon cinereoargenteus). The largest canid in South America is the Maned Wolf (Chrysocyon brachyurus; plate 14-11). It is found in the open pampas areas of southeastern Brazil.

Plate 16-58. Male Puma feasting on a kill, a Guanaco (plate 1332), in the Andes Mountains. Photo by Andrew Whittaker.

Neotropical Marsupials Most people associate marsupials—kangaroos, wallabies, wombats, bandicoots—with Australia. Marsupials are mammals that give birth to premature young, which migrate to a pouch on the mother’s abdomen, where they attach to a teat and complete their development. Almost everyone has seen pictures of a mother kangaroo with a joey in her pouch. Mammals that bring young to term in utero are called placental mammals. Though Australia is the world’s undisputed marsupial capital, until relatively recently in geologic time, South

Plate 16-59. Two Crab-eating Foxes strolling along in the Brazilian Pantanal. Photo by John Kricher.

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Plate 16-60. It is easy to see why this tiny animal is called a mouse opossum. The species pictured is Mexican Mouse Opossum (Marmosa mexicana). Photo by James Adams.

Plate 16-61. Like other opossums, the Central American Woolly Opossum (Caluromys derbianus) is fundamentally arboreal and active mostly at night. Photo by James Adams.

America also boasted a diverse marsupial community. Today, though, just over 40 species of opossums are found in the Neotropics, most of the original South American marsupial fauna is extinct. During the Pleistocene faunal exchange (chapter 8) a few species migrated northward, including the durable Virginia Opossum (Didelphis virginiana; plate 8-46), which continues to expand its population in North America today. However, many placental mammals emigrated from the north into South America, and their arrival coincides to a degree with a decline in richness of marsupials. South America’s marsupial fauna is but a remnant of what it once was. The Common Opossum (D. marsupialis), found throughout Central America and Amazonia, has hardly changed in appearance from its ancestors who roamed the planet 65 million years ago. The fossil record indicates that the opossum family (Didelphidae) dates back to the Late Cretaceous period, while the Common Opossum species arose about 35 million years ago. That means, of course, that early opossums were contemporary with the last of the dinosaurs. Superficially rat-like, with a pointed snout and scaly naked tail, the Common Opossum weighs between 2.3 and 4.5 kg (5–10 lb) and is largely gray, with some

black. It inhabits almost any kind of terrestrial habitat other than desert and high mountains. Opossums are excellent tree climbers and often hang upside down, clinging by their prehensile tails. Totally omnivorous, the opossum will try eating almost anything. Its most remarkable behavior, “playing possum,” is an act in which the animal feigns death when it is threatened. In addition to the Common Opossum, the Neotropics host numerous other opossums. Most are nocturnal, but many are common and seen relatively often in daytime. There are tiny mouse opossums (Marmosops, Micoureus, Gracilinanus, Marmosa; plate 16-60), furry little woolly opossums (Caluromys; plate 16-61), bushy-tailed opossums (Glironia), foureyed opossums (Philander, Metachirus), which are four-eyed in name only, short bare-tailed opossums (Monodelphis), and the Yapok, or Water Opossum (Chironectes minimus). Though these species are different sizes, they are all basically similar in anatomy, and the group ranges throughout the various habitats of Central and South America. What this diversity indicates is that opossums have undergone a successful adaptive radiation throughout the American tropics and are the survivors of what was, for other marsupials, a bygone era.

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Plate 16-62. Encountering snakes is a common concern among visitors to rain forests. This beautiful snake is Chironius exoletus, a species of vine snake, or sipo, as the group is known locally. It is nonvenomous, as are most Neotropical snakes, and should be a welcome sight for any naturalist. Photo by Sean Williams.

Plate 16-63. The Mato Grosso Lancehead (Bothrops matogrossensis) is a typical Neotropical pitviper. Photo by Nancy Norman.

Plate 16-64. This Fer-de-lance is coiled, a typical defensive position that may also signal aggression (venomous snakes seem to believe that the best defense is a strong offense). Photo by James Adams.

Plate 16-65. This is closer than one ought to get to a Fer-delance. Photo by James Adams.

Reptiles and Amphibians

once they conquered their initial fears of serpents, develop intense curiosity about them, followed by admiration of their beauty. This section addresses that curiosity and focuses on a few other reptiles and amphibians as well. But let’s start with snakes—and venomous snakes at that. Between northern Mexico and southern Patagonia, there are 145 species of venomous snakes to be found. These include 54 species of coral snakes, one sea snake, the Cantil, the Copperhead, seven species of palmpitvipers, eight species of forest-pitvipers, 31 species of lancehead pitvipers (plate 16-63), 14 species of hognosed and montane pitvipers, 26 species of rattlesnakes

People always seem to associate the tropics with snakes. The fear of snake-infested trails and trees taints many folks’ views about the allure of rain forest. How can you admire the scenery when you always have to be looking out for venomous snakes? In reality, venomous snakes are not frequently encountered. They tend to be secretive and nocturnal, and it’s actually not easy to find them, even when you search diligently. There are, however, many species of snakes in the tropics, both venomous and (most) nonvenomous, and as a group they are fascinating (plate 16-62). I have seen people,

from monkeys to tarantulas: endless eccentricities

and pygmy rattlesnakes, the Mexican Horned Pitviper, and, largest of the lot, the Bushmaster. Maybe it is a good idea to keep an eye on your feet as you walk the rain forest trails.

Snakes: The Pitvipers All pitvipers (subfamily Crotalinae), which range throughout both the tropics and the temperate zone, are venomous. North American rattlesnakes, plus the well-known Copperhead (Agkistrodon contortrix) and Cottonmouth, or Water Moccasin (A. piscivorus), are pitvipers. The “pits” referred to in the name are sensory depressions located between the nostrils and eyes. They sense heat and aid the snake in locating warm-blooded prey. Like other serpents and some lizards, pitvipers use their forked tongues to detect odors. The tongues, flicked in and out frequently, are highly sensitive to molecules in the air. Pitvipers have long hypodermic fangs in which a venom duct from modified salivary glands can deliver a lethal dose of a biochemically complex toxin that attacks blood cells and vessels, surrounding tissue, and sometimes nerve tissue. Pitvipers tend to rest in a coiled position, which they also assume when danger threatens (plate 16-64). Any pitviper may be aggressive in display, raising its head high and vibrating its tail. Rattlesnakes enhance this position by shaking their noisy rattles. Pitvipers normally have large, triangle-shaped heads, and catlike eyes with vertical, slit-like, elliptical pupils, helpful features in recognizing them. The most well known Neotropical pitviper is the Fer-de-lance (Bothrops asper; plate 16-65), one of 31 species of lanceheads, all in the genus Bothrops. Lanceheads are mostly lowland species found at elevations below 1,500 m (approx. 5,000 ft). They tend to bear a close resemblance to one another, and it is often not possible to identify them to the species level without a careful in-hand examination of the animal (not recommended). The Fer-de-lance will serve to introduce you to the group. Known variously as the Yellow-tail, Yellow-jaw, or Tommygoff, as well as by many Spanish and Portuguese names, it is best known by its Trinidadian name, Fer-de-lance, though its English name is actually Terciopelo. The name ferde-lance refers to the lancelike shape suggested by the long, serpentine body and conspicuously large, triangular head. In Brazil a very similar species is called the Jararaca, a name meaning “arrowhead.” The Fer-

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Are Fer-de-lances Very Common? Well, to speak the plain truth, yes. In a somewhat courageous study performed at La Selva Biological Station in Costa Rica, researchers D. K. Wasko and M. Sasa used radiotelemetry to study the spatial ecology, activity patterns, and habitat selection of 11 female and five male Fer-de-lances. They brought captured snakes to the lab, anesthetized them, and implanted radio transmitters. They released the snakes back where they were initially taken and monitored their movements, attempting to relocate each animal at least once a day, either during the day or at night. They documented the snakes’ activity patterns, recording them as inactive if lying coiled, active if moving, ambushing if lying coiled and alert, head raised. The study was performed over a two-year period. Each of the snakes had a relatively small home range, and that, of course, allows for numerous snakes to inhabit a forest tract. Habitat preference was focused on swamps, although the snakes were also commonly present in primary and secondary forest—so they could show up pretty much anywhere. The good news was that they generally avoided developed areas, presumably to the relief of humans who occupy such areas. However, I have seen Fer-de-lances rather often around field stations and lodges located within forest (plate 16-66). So be vigilant. Fer-de-lances and most other snakes are primarily nocturnal in their activity patterns, spending most of the daytime hours coiled and inactive. Remember though, they are out there.

Plate 16-66. This small and deceased Fer-de-lance was apparently the victim of an automobile. It was lying on a gravel road adjacent to an ecotourist lodge. Even the small ones are highly venomous. Photo by John Kricher.

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de-lance, like most Bothrops, is a tan snake with dark brown diamond patterning along its sides (intensity of body color and blotching patterns are quite variable). The creature averages a length of 1.2–1.8 m (approx. 4–6 ft), with some individuals reaching 2.5 m (8.2 ft). Regardless of size, a Fer-de-lance is a potentially lethal snake (as are all Bothrops). Even the juveniles are highly venomous, and up to 50 young are born at a time (so take care to look around if you should encounter a juvenile— its siblings may be lurking about). Campbell and Lamar (1989) note that Bothrops species “are responsible for more human morbidity in the New World than any other group of venomous snakes.” The venom is fast acting and painful. It rapidly destroys blood cells and vessels and produces extensive necrosis (decomposition) of tissue around the bite site. Infection can follow and can be massive. Mortality without treatment is about 7%, but it is reduced to between 0.5% and 3% with proper treatment. A person bitten by a Bothrops should receive antivenin quickly, and even then recovery is usually an ordeal. Occasionally a Bothrops will bite in self-defense but not inject venom. It may have exhausted its venom on a recent catch or may simply not discharge it. Note that most Bothrops are inactive during the day, as they tend to hunt at night. However, these snakes can be quick and aggressive if disturbed. Heed the words of Campbell and Lamar: “Specimens can (and often do) move very rapidly, reversing directions abruptly, and defending themselves vigorously. An adult B. asper, if cornered and fully aroused, is a redoubtable adversary and must be regarded as extremely dangerous.” Remember that, and don’t mess with a Fer-de-lance.

The Fer-de-lance feeds on various mammals and some birds. The species ranges mostly throughout Central America to northern South America, and throughout the Orinoco Basin. To the south, throughout Amazonia, it is largely replaced by the similar B. atrox, B. brazili, and B. jararaca, as well as numerous other Bothrops species, including one just described in 2010. The eight species of forest-pitvipers (genus Bothriopsis), which are similar to Bothrops species, have restricted ranges in northern South America, but two species, B. bilineata (Two-striped Forest-Pitviper) and B. taeniata (Speckled Forest-Pitviper) are widely distributed throughout Amazonia. Forest-pitvipers tend to be slender and may exceed lengths of 1.5 m (5 ft). They have prehensile tails, which allow them to climb trees, and all are found in interior forest. There are 10 species of palm-pitvipers (genus Bothriechis), which tend to grow to shorter lengths than other pitvipers, to 60–80 cm/2–2.5 ft). Any palmpitviper is potentially dangerous, as these snakes are arboreal and usually cryptic (often greenish), coiled among palm fronds. Most species are Central American and found in montane areas. However, one species, B. schlegelii, is common in lowland rain forest and ranges throughout Central America and as far south as central Ecuador. Called the Eyelash PalmPitviper (plate 16-67) because of enlarged scales that grow outward over each eye, it is generally considered abundant throughout its range. The species is highly variable in color, but most specimens are some shade of green, finely suffused with black, though some are bright yellowish gold. A good climber, with a prehensile

Plate 16-67. This attentive and attractive Eyelash Palm-Pitviper is showing its “eyelashes” well. Photo by James Adams.

Plate 16-68. The Bushmaster, the largest of the world’s pitvipers. Photo by Sean Williams.

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tail, the Eyelash Palm-Pitviper feeds on small rodents as well as tree frogs and anole lizards. There are 14 species of montane or hog-nosed pitvipers (genera Porthidium and Atropoides). One, the Jumping Pitviper (A. nummifer), which ranges from southern Mexico through Panama, is alleged to sometimes hurl itself at a perceived attacker, a claim that is apparently exaggerated, though it sounds exciting. A short snake with a very thick body, it is gray-brown with black diamonds. Its venom is apparently not as potent as that of other pitvipers. Rattlesnakes are mostly North American, with the majority of species found in northern and central Mexico. However, one species, the Neotropical Rattlesnake (Crotalus durissus), occurs from Central America to Brazil and Paraguay, mainly in dry forests and uplands. It is a regionally variable species, but as it is basically the only rattler in South America, if a scary-looking coiled serpent rattles at you, be assured it’s this one—and be careful. The snake has an elaborate threat display, and it is not bluffing. The bite of this animal results in progressive paralysis of muscles due to nerve paralysis, accompanied by destruction of red blood cells and kidney failure. This cascade results in a mortality rate of 72% without treatment. The Bushmaster (Lachesis muta; plate 16-68) is the giant of the pitvipers. Not only is it the largest pitviper in the Neotropics, it is the world’s largest, reaching lengths of between 2 and 3.3 m (6.5–11.7 ft). My group and I encountered a Bushmaster as it was slowly crossing a road at night in Trinidad and estimated the snake to be approximately 2.7–3 m (9–10 ft) in length (it seemed prudent not to try for a more precise measurement). As its head was descending into the gully on the right side of the road, its tail had yet to emerge from the gully on the left side of the road. It was a truly magnificent creature to behold, seen to advantage in the headlights of our van, as my group remained at a respectable, safe distance. The Bushmaster is generally yellowish tan, reddish brown, or pinkish tan, patterned with dark brown diamond-shaped splotches, the broadest splotches on its back, not its sides, as is typical in Bothrops pitvipers. The Bushmaster is reputed to strike without audible warning, though it usually does vibrate its tail, and that action can be audible when done in dry leaves. It is also known to threaten with its neck inflated when coiled. Because of its length, a Bushmaster can strike over a long distance. It has large fangs and can deliver a high dose of venom.

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There are not a great many reports of Bushmaster strikes on people, but those that exist are peppered with the word “fatality.” This snake is an inhabitant of lowland rain forest throughout lower Central America, Amazonia, and the southeastern coastal forest of Brazil, and is reportedly often seen coiled within buttresses of large trees. It is most active at dawn and dusk, as well as throughout the night. The snake feeds primarily on mammals and birds. Careful now.

Pitviper Wannabes On a trip to Peru, several of us encountered a small, slender, emerald green snake resting in the middle of the trail, looking innocuous, even for a serpent. I could see no pits, its eyes were not vertically slit, and its head was slender, not triangular. I decided that it was nonvenomous, as are most Neotropical snake species. Nonetheless, always erring on the side of caution, I fetched a small stick and gently (I thought) prodded the creature’s tail end to encourage it to vacate the trail. I assumed it would hasten along. It didn’t. It apparently took offense, coiled, lifted its head high, opened its mouth very wide, and vigorously struck (though it came nowhere near me—I am no stranger to evasive action). As it continued with this aggressive behavior, its head seemed to actually flatten and become increasingly triangular. It put on a good act, in line with the notion that the best defense is a strong offense. Many Neotropical nonvenomous snake species have evolved a behavior when threatened that is similar to that of venomous species, especially pitvipers. In effect, they are pitviper behavioral mimics. Given that nonvenomous snakes may become Neotropical thespians, how do you know for sure when you are dealing with the real thing, an actual venomous snake? Just assume you are, and you’ll be fine.

Coral Snakes “Red and yellow, kill a fellow; red and black, friend of Jack.” This is a little rhyme to help remember the distinction between potentially lethal North American coral snakes and nonvenomous, harmless king snakes (if red bands touch yellow bands, it’s a coral snake, but if red bands touch black bands, it’s not). But be advised that this lyrical distinction does not work in the Neotropics. There are just over 50 species of coral snakes in the Neotropics, and many (probably most)

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Plate 16-69. “Red and black, friend of Jack”? Nope. This is Micrurus ibiboboca, one of the Brazilian coral snake species. Beware. Photo by Andrew Whittaker.

do not have red bands touching yellow (plates 16-69– 70). It’s safest just to avoid colorful snakes with any combination of red, black, and/or yellow rings. They may be coral snakes, and you don’t want to be holding a coral snake. Coral snakes are members of the global family Elapidae, to which the deadly cobras and mambas belong. Their powerful venom is a neurotoxin (a venom affecting the nervous system) that quickly produces paralysis and death by suffocation. Lengths vary among species, but coral snakes typically reach between 0.6 and 1.2 m (2–4 ft), though some species can be more than 1.6 m (5.25 ft). Unlike pitvipers, coral snakes have short fangs and must bite with force to inject their lethal venom. Coral snakes are active both day and night and are most often found beneath leaves, logs, or rocks in habitats ranging from deserts to lowland rain forest. They eat mostly lizards and other snakes. Recall that the bright patterning, which typifies all coral snake species, is considered to be warning coloration (described in detail in chapter 11). But warning goes only so far, and so coral snakes exhibit various escape behaviors, such as raising the tail and moving it in tandem with the head, possibly making the animal appear as two snakes rather than one. When threatened, a coral snake will actively thrash its body, wave its tail, and may try to bite. Handling one is therefore dangerous, because its narrow head can easily slip through fingers, giving the snake an opportunity to strike, and you don’t want that to happen. Many species of nonvenomous snakes, often collectively called “false coral snakes” (see chapter 11 and plates 11-25–27),

Plate 16-70. The Bicolored Coral Snake (Micrurus nigrocinctus) is a Central American species. Photo by James Adams.

converge in color pattern with coral snakes wherever their ranges overlap. For example, coral snake mimicry is shown by the nonvenomous Lampropeltis triangulum hondurensis, which, in Honduras, looks similar to the coral snake Micrurus nigrocinctus divaricatus. In both, wide, bright red bands alternate with thinner black bands, and the snout is black. If you should encounter a coral snake, or any serpent that looks like it could be one, you are wise to avoid touching it.

More Snakes: The Constrictors The world’s largest snakes are constrictors (family Boidae). In the Old World, these snakes are called pythons, but in the Neotropics they are the boas and anacondas. A few boas are found in Madagascar and the Indo-Pacific islands, but most are in the Americas. Boas are nonvenomous, though their teeth are needlesharp, and their bite can be nasty. With wide heads, wide bodies, and elaborate patterning, they are sometimes confused with pitvipers. Boas capture and kill prey through constriction, a process whereby the serpent coils around its victim tightly enough to prevent it from breathing, eventually killing it by suffocation. Following death of the victim, constrictors, like all snakes, swallow their prey whole, opening their mouths widely, due to jaws attached only by elastic ligaments. The Rainbow Boa (Epicrates cenchria; plate 16-71) is one of the smaller boids, normally growing to about 1 m (39 in.) long. To be appreciated, this little constrictor must be observed in full sunlight, which makes its dull blackish-brown scales sparkle with the iridescent colors that give the snake its popular name. Rainbow Boas are

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skilled tree climbers and often prey on bats. They range from Central America all the way south to Patagonia. Perhaps the best known of the group is the Boa Constrictor (Boa constrictor; plate 16-72), common throughout the Neotropics. Boa Constrictors are warm tan, with dark brown, diamond-shaped patterning, but variable in color pattern. Those found in South America are generally lighter-colored and more sharply marked than their Central American counterparts. Their heads, like those of all Boidae species, are long and taper to a pointed snout. Boas average about 1.5 to 1.8 m (5–6 ft) in length. The largest Boa Constrictor on record was 5.64 m (18.5 ft), most extraordinary for this species. Boas can be aggressive and will coil, hiss, and bite if attacked. In captivity they can become docile (but they don’t belong in captivity, regardless of disposition). They are mostly nocturnal, feeding on all manner of mammals, including small cats. They also take birds and lizards. Boa Constrictors inhabit a wide range of habitats, from wet lowland forests to dry savanna. The Emerald Tree Boa (Corallus canina) is one of the most beautiful of Neotropical boids. Deep green above, yellow green below, with a dorsal white line and scattered white spots, it has burning yellow eyes with catlike, slitted pupils. Confined to South America, this 1.8 m (6 ft) boa can be cryptic, said to resemble a bunch of bananas when coiled in a tree. Small individuals have been found on banana boats among the bunches. The tail is prehensile, and these snakes are skilled at moving about in the trees, preying on squirrels, opossums, birds, and lizards. Both the Emerald Tree Boa and Boa Constrictor become tame when handled frequently by humans. The largest of the Neotropical constrictors is the Green Anaconda (Eunectes murinus), most common along rivers and in marshes (discussed in chapter 12).

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Plate 16-71. The Rainbow Boa (Epicrates cenchria) is one of the most beautifully patterned of the boas. It occurs in both Central and South America. Photo by Sean Williams.

Plate 16-72. Boa Constrictor. Photo by James Adams.

A Few More Nonvenomous Snakes There are many additional species of nonvenomous snakes in the Neotropics. They include the various vine snakes (genus Oxybelis), thin brown, gray, or green snakes that climb about the foliage capturing and feeding on lizards. The beautiful Indigo Snake (Drymarchon corais) can reach lengths of 3 m (9.8 ft), eating virtually any kind of animal from fish to birds. The large-eyed, extraordinarily thin Blunthead Tree Snake (Imantodes cenchoa; plate 16-73) may be spotted coiling in outer branches, where it preys on small tree frogs and lizards.

Plate 16-73. The Blunthead Tree Snake is a common nonvenomous snake species ranging from Mexico through Amazonia. It is typically encountered in understory vegetation. Photo by Dennis Paulson.

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Iguanas and Other Lizards

Plate 16-74. Green Iguanas, which are not always green, look prehistoric. Photo by Gina Nichol.

Plate 16-75. This young Green Iguana is indeed green. Its color will change as it ages. Photo by Dennis Paulson.

Plate 16-76. The dewlap is readily visible on this Green Iguana. Photo by Steve Bird.

The Green Iguana (Iguana iguana; plate 16-74) is a ubiquitous inhabitant of Neotropical humid forests. These lizards are among the largest of the Neotropical lizards. They are green when small but become grayish brown as they grow larger and mature (plate 16-75). A mature iguana can exceed 1.8 m (6 ft) in length, but much of it is tail, which tapers into a slender tip. The face, with large mouth and wide, staring eyes, atop the primordial reptilian body presents a dinosaurlike countenance. (Indeed, iguanas have played the role of dinosaurs in several very old B movies.) Two short spines adorn the nose above the nostrils, and a loose membrane of skin called a dewlap hangs below the throat (plate 16-76). The head is flat and covered by heavy tubercle-like scaling, and the neck and back are lined with short, flexible spines. The legs sprawl alligator-like to the sides, and the feet have long toes with sharp claws. Iguanas do not often hurry, but they are capable of moving quickly if necessary. They spend most of their time in trees, usually along a stream or river, into which they jump should danger threaten. Excellent swimmers, they can remain underwater for considerable time. When small they concentrate on insect food but when full-size feed more heavily on fruits and leaves. Should you encounter an iguana, even a large one, you have nothing to fear. They usually do not bite unless thoroughly harassed, they are not particularly effective scratchers, and they are nonvenomous. The most aggressive iguana I ever encountered was directing its hostility at a rat. Both the mammal and the reptile were contesting access to garbage dumped alongside the Amazon River in Iquitos, Peru. The iguana lost. Adult iguanas feed heavily on fruits and leaves and thus, because they are near the base of the food chain, are apt to be abundant in rain forests. They are a potentially important protein source for humans. Iguanas are members of the large family Iguanidae, which includes the many anole lizards, basilisk lizards, and ctenosaurs. Anoles (genera Anolis and Norops; plates 16-77–78) are generally abundant lizards. Some are bright green, some are brown, and some are mixtures of both. Some can change color, rather like chameleons, to which they are not closely related. During the heat of the day the sounds of these and other small lizards scurrying over dry leaves precedes you as you walk along. Anoles have sharply

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Plate 16-77. This Green Tree Anole (Norops biporcatus) has changed color from green to mottled brown, a characteristic behavior of the species that indicates it is likely stressed. Photo by Dennis Paulson.

pointed noses and large conspicuous dewlaps, which males distend during courtship. They are skilled tree climbers and are often seen facing downward on a tree trunk with the neck stretched out horizontally. They are also common on foliage. Small arthropods make up their diet. Basilisk lizards (Basiliscus spp.; plate 16-79) are commonly called “Jesus Christ lizards” because of their ability to scurry at high speed (not walk!) across water. With long toes on the hind feet, lined with skin flaps, these odd lizards run full tilt on their hind legs across small streams and puddles. They look even more like dinosaurs than iguanas do because they are adorned with elongate spiny fins on the back and tail. They feed on invertebrates, vertebrates, and various fruits and flowers. Basilisks are found primarily in Central America and are common and easily seen. The Helmeted Iguana (Corytophanes cristatus; plate 16-80), also called the Helmeted Basilisk, may be mistaken for a basilisk. Ctenosaurs (genus Ctenosaura; plate 16-81), or black iguanas, are among the larger iguanid lizards. Ctenosaurs closely resemble iguanas but have more of a banded pattern (though they can change pigmentation easily, and pattern varies widely from animal to animal: some are dark, some light), and they tend to frequent drier areas such as open fields, farmyards, savannas, roadside edges, and coastal areas. They are adept burrowers and skilled tree climbers. As with iguanas, larger ctenosaurs concentrate on vegetable food,

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Plate 16-78. The Slender Anole (Norops limifrons) is one of the most abundant and frequently encountered of the anole lizards. Another, similar species, also called Slender Anole (N. fuscoauratus), occurs widely in South American humid forests. Photo by Dennis Paulson.

Plate 16-79. Green Basilisk (Basiliscus plumifrons). Photo by Steve Bird.

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Plate 16-80. This is a Helmeted Iguana. It is much more closely related to basilisks, which it resembles, than to iguanas. Photo by James Adams.

Plate 16-81. This is a ctenosaur known as the Black Spinytailed Iguana or Black Iguana (Ctenosaura similis). Like iguanas, ctenosaurs are adept at climbing trees. Photo by Scott Shumway.

Plate 16-82. No, it’s not a T. rex. It is an Argentine Black-andwhite Tegu, found from southeastern Brazil through Uruguay and Paraguay to Argentina. Photo by Dennis Paulson.

Plate 16-83. The Common Tegu is called the Matte in Trinidad, where this photo was taken. Photo by John Kricher.

though they are not averse to sampling such delicacies as bats, baby birds, and one another’s eggs. Iguanas and ctenosaurs shift their diets from primarily arthropods to primarily vegetation as they increase in body size, a diet shift that may be related to reptilian energetics and constraints of large size. Small lizards can be active and successful in catching small but scurrying prey, such as beetles and spiders. Large lizards require more energy (simply because they are larger) but actually need less energy per gram of body weight (because large animals have slower metabolisms). Perhaps they are not as well served by spending time and energy trying to capture fast-moving insects, none of which individually contain much energy. Plants don’t move and they require little energy to “capture,” and

though plant material is harder to digest, more can be swallowed at a single sitting. Thus, a vegetarian diet is more optimal for a large lizard, presuming digestion of the plant matter is not problematic to the creature. Even some of the medium-size and large carnivorous lizards do not pursue prey, perhaps because such pursuit would expend more energy than would be contained in the prey item. These animals sit and wait and then capture any slow-moving arthropod (such as a caterpillar or grub) that happens to blunder past. The lizard family Teiidae includes the largest of the South American lizards, the tegus (genus Tupinambis). They superficially resemble Old World monitor lizards. Four species range through South America. The Argentine Black-and-white Tegu (T. merianae; plate

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16-82) reaches a length of 145 cm (57 in); it and its close relative the Red Tegu (T. rufescens), are the two largest lizard species of the Americas. The Common Tegu (T. teguixin; plate 16-83), which sometimes reaches 1 m (39 in) in length, is perhaps the most commonly encountered species. Tegus live in forested areas and forest borders, but may also frequent savannas and even beaches. They feed on small animals, including chickens and their eggs, and local farmers hunt them as a protein source. Gekkonidae, the geckos, is a major lizard family of the world’s tropics. Geckos are usually pale colored with dark splotches (plate 16-84). With adhesive scales on their feet, geckos cling comfortably to smooth walls. They feed exclusively on arthropods and are nocturnal. Some species inhabit dwellings, living in harmony with humans. Geckos are considered valuable for their ability to keep numbers of cockroaches and other vermin within tolerable limits. The name gecko comes from their loud calls, given only at night, often while hanging on a wall rather near where you’re sleeping. It takes some getting used to. Many more species of snakes and lizards (plate 1685) inhabit the Neotropics, but the ones discussed and shown here ought to give you the general idea of the remarkable biodiversity and beauty.

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Plate 16-84. The Yellow-headed Gecko (Gonatodes albogularis) is widely distributed and common in Central and South American humid forests. Photo by Dennis Paulson.

Anurans: Tree Frogs, True Frogs, and Toads Amphibians are vertebrates that do not lay eggs in protective shells. Instead, they require water to reproduce. Typically, gelatinous eggs are laid in ponds or streams, either as floating masses or attached to rocks or debris. Larval animals (referred to as a tadpoles in frogs and toads) hatch and pass through a developmental stage in water. During this aquatic phase the animal breathes by external gill tufts, but these are resorbed when the larva passes through metamorphosis to adulthood. Adult amphibians usually require moisture for their skins, though toads are able to survive with dry skins. Salamanders are not diverse in the tropics. They represent an exception to the general tendency for taxonomic groups to show high species richness in the tropics. By far the most abundant, diverse, and interesting amphibians are the anurans, the frogs, tree frogs, and toads. There are approximately 4,000 species of anurans in the world, and some 1,600 occur in the Neotropics

Plate 16-85. Berthold’s Bush Anole (Polychrus gutturosus), also popularly called the Forest Iguana, occurs from Honduras to Ecuador. It shows the remarkable beauty typical of many snakes and lizards. Photo by Dennis Paulson.

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Anuran Defenses As discussed in this section, anurans exhibit warning coloration (poison-dart frogs) and toxic irritating chemicals as defenses. They have two other defense tricks. Some species that are normally cryptic display flash colors when threatened. The flash color is revealed when the frog raises a foot or other body part, revealing a bright patch of color, usually red, orange, yellow, or blue. The sudden appearance of the bright coloration may momentarily confuse a predator, interrupting its search image long enough for the frog to use its most obvious defense tactic, its jumping ability.

(plate 16-86). In some areas in western Amazonia there can be as many as 80 species of anurans at single sites within lowland rain forest. Although many species of anurans reproduce in the manner described above, many also show dramatic departures. In Costa Rica, where 119 anuran species are found, some have live birth, bearing fully formed miniature adults (skipping the egg and larval phases); others lay eggs on plants, from which larvae hatch and drop into water; and some lay eggs in nests of foam on land, in bromeliads, or in tree cavities. The speciesrich genus Eleutherodactylus (plate 16-87) reproduces by direct development, laying eggs that hatch into tiny but fully formed frogs. Courtship patterns are also sophisticated. Frogs and toads vocalize, the males emitting a specific call that serves to attract the females. Many species are territorial. Anuran reproductive behavior has undergone an impressive adaptive radiation in the tropics. This is largely possible because the tropical rain forest maintains a constantly high humidity that facilitates keeping an anuran’s skin constantly moist, a prerequisite to its survival. Tree Frogs

Plate 16-86. The Small-headed Tree Frog (Dendropsophus microcephalus) ranges from Central America to Brazil. It demonstrates the expanded throat that enhances the loud vocalization of these animals as well as the flattened toes adapted to attach to vertical surfaces, such as leaves and stems. Photo by Dennis Paulson.

Plate 16-87. The 2.5 cm (1 in) long Central American Common Tink Frog (Eleutherodactylus [Diasporus] diastema) is named for its tink call. This species brings forth fully formed adults from the gelatinous egg, with no free-swimming tadpole stage of the life cycle. Photo by Dennis Paulson.

Tree frogs of the family Hylidae are arboreal, attaching to leaves and stems by tiny suction disks on their feet. Most are small and cryptic, though some are brightly colored. One of the most common is the Red-eyed Tree Frog (Agalychnis callidryas; plate 16-88). This Central American species has bulging, blazing red eyes, a bright green upper body with a scattering of white spots, bluish marks on the sides, white on the belly, and orange on the hands and feet! Males and females have a prolonged mating ritual, in which the female, with the male clinging to her, attaches eggs to a leaf as the male fertilizes them. Hatching occurs in approximately five days, and the larval tadpoles drop off the leaf into water. One of the most intriguing examples of the complexity of frog life cycles is provided by the Strawberry Poisondart Frog (Oophaga pumilio). In this species, whose life history has been painstakingly documented, both male and female parents are involved in caring for the eggs and tadpoles. The male guards the eggs for 10 to 12 days. Once the eggs hatch into tadpoles, the female takes over, transporting each tadpole to a bromeliad containing water. Each tadpole is placed in a different bromeliad plant, to which the female returns regularly

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to deposit an unfertilized egg to serve as food for the developing frog. Poison-dart frogs (Dendrobatidae) are the most colorful, and dangerous, of the tree frogs (plates 11-21– 24). Some are shiny black with red or orange markings, some bright green. Indigenous people utilize the poisonous alkaloids from the frogs’ skins in making potent darts for hunting. The poison affects nerves and muscles, producing paralysis and respiratory failure. These colorful frogs hunt by day, feeding on termites and ants, and it has been suggested that their warning coloration evolved in response to their long feeding periods, when they would otherwise be vulnerable to predators. Poison-dart frogs are discussed in more detail in chapter 11. Glass frogs are small green tree frogs, most with transparent belly skin that reveals the beating heart and intestinal system (plate 16-89). They attach eggs to leaves over streams, and larvae hatch and drop into the water. Eggs tend to hatch in heavy rain, facilitating the release of tadpoles into the water below. Tadpoles become bright red and burrow in stagnant litter in slow pools. Their color is the result of a concentrated blood supply, an adaptation to low oxygen levels in the mud.

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Plate 16-88. Red-eyed Tree Frog. Photo by Steve Bird.

Typical Frogs Numerous species of typical frogs inhabit swamps, marshes, wet forests, and other suitable habitats throughout the Neotropics. The genus Leptodactylus (plate 16-90) is well represented by about 75 species, but there are many others as well.

Plate 16-89. Fleischmann’s Glass Frog (Hyalinobatrachium fleischmanni) calling on a leaf. Photo by James Adams.

Toads The Cane Toad (Rhinella marina [Bufo marinus]; discussed in chapter 11; plate 11-31), largest of the New World anurans, is common in many areas of the Neotropics and has become a pest species in southern Florida and Australia. It secretes irritating fluid from its skin and is toxic if eaten. The large, nearly softball-size animal would make a tempting target for predators, but its toxic integument is so dangerous that dogs and cats have reportedly died just from picking up the toad in their mouths. One curious human application of toad toxin has been studied in Haiti. Along with extract from puffer fish and two plant species, toad toxin is used to induce the deathlike trance observed in victims of voodoo rituals.

Plate 16-90. Savage’s Thin-toed Frog (Leptodactylus savagei) is one of many species of its genus. It occurs in much of Central America and in northern South America. Photo by Dennis Paulson.

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A Few Select Invertebrates Bugs. Beetles. Spiders. Scorpions. Things that creep and crawl and look scary and noxious occur by the thousands in the Neotropics. They come in petite, small, medium, large, extra large, double extra large, and outrageous. They abound from treetops to leaf litter, in closed forests and successional gaps, in field stations and tents, and occasionally in shoes. They are out by day, dusk, night, and dawn, and some of them even glow in the dark. Myriad animals without backbones—insects, centipedes, millipedes, various arachnids, worms—are at home in the Neotropics. Seemingly innumerable invertebrate creatures crawl, hop, slither, climb, burrow, and fly through rain forests. In no way can this book provide a representative sample of the invertebrate life forms that can be found by diligently searching rain forests and other Neotropical habitats. Many invertebrate examples have been discussed in previous chapters, and those included below are a mere sample of some of the other most interesting and frequently encountered members of this vast horde.

Social Insects Two great insect orders, Hymenoptera (the bees, wasps, ants) and Isoptera (the termites), have evolved species that display complex social systems in which societies of close relatives (genetic sisters) support a fertile queen. Both orders are abundantly represented in the world’s tropics and are of vast ecological influence. Workers are usually separated into differing morphological castes, consisting of various-size workers and soldiers. Sterile animals are

Plate 16-91. This is a Bullet Ant. Do not pick one of these up. Photo by Alex Wild.

usually females, all sisters, but male workers occur in termites. In other cases males are produced only during mating of the queen and are otherwise superfluous. Termites are described in chapter 6, fungus-garden ants and army ants in chapter 10. A Mean and Nasty Giant Tropical Ant Beware of the Giant Tropical Ant, which is also called the Bullet Ant (Paraponera clavata; plate 16-91). It is in a subfamily of its own (Paraponerinae), and represents a kind of relict species, as its last common ancestor with other ants lived about 90 million years ago. This 2.5 cm (1 in) long black ant can both bite and sting. This creature’s normal mode of attack is to bite hard, then, once attached by its jaws, to twist its abdomen around and deliver a very painful wasplike sting of substantial potency. This unpleasant experience is reputed to be rather similar to being struck by a bullet (hence the common name). Bullet Ants occur throughout Central and South America and are both terrestrial and arboreal. They are usually seen on the forest floor but may be in the understory, too. Not surprisingly, such a formidable ant has its mimics. A beetle species (order Coleoptera) resembles the giant ant when at rest, but the deceptive coleopteran looks like a wasp when in flight. Bullet Ants tend to be solitary, but one is quite enough.

Cockroaches It is hard to imagine a trip to the Neotropics that does not include a sighting of la cucaracha. Most of the world’s 4,000-plus cockroach species live in the tropics, and the Neotropics can certainly lay claim to its share. Most

Plate 16-92. Meet Megaloblatta blaberoides, a name that translates as “big cockroach.” This species, from Honduras, is not as large as the Giant Cockroach but, as is clear from the photo, it is sizable. Photo by James Adams.

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people can identify cockroaches easily (plate 16-92), as they routinely cohabit human dwellings, much to the dismay of the primate occupants. But such an attitude is wrong-headed. You ought to be willing to share with them. Their evolutionary lineage reaches well back into deep time. Cockroaches have resided on the planet for over 300 million years, and they are a wonderful evolutionary success story. They do not bite or sting, nor do they carry vile diseases. So relax and enjoy them. You might as well. In the Neotropics, at least, they are always close by. Cockroaches are oval in shape, are covered on the dorsal side by a pair of large wings, and sport a pair of very long antennae on the head. Excellent fliers and basically nocturnal, they are often seen fluttering around lights at night. They are remarkably fast runners and have an uncanny ability to squeeze between floorboards and into other tight places. One of the most striking tropical species is the Giant Cockroach (Blaberus giganteus). At full size, this insect behemoth easily fills the palm of your hand and then some. It lives in hollow trees and other reclusive places during the day and scurries about in search of food at night. Blaberus is a good cockroach mother. I came upon one on the forest floor, near an outhouse (cockroaches like outhouses) in Amazonian Peru. I noticed lots of odd little white things around the animal. Closer inspection revealed that the little white things were unpigmented baby cockroaches. The adult was brooding, and was very protective about getting the pale little animals under the protection of her wings. With such devoted parental care, it’s no wonder they have been around for so many millions of years.

Harlequin Longhorn Beetle

Plate 16-93. The Harlequin Longhorn Beetle. Photo by James Adams.

Plate 16-94. Rhinoceros beetle, male. Photo by Gina Nichol.

There are many thousands of Neotropical coleopterans (beetle biodiversity was discussed in chapter 9). Acrocinus longimanus, commonly called the Harlequin Longhorn Beetle (plate 16-93), is both large (to 7.5 cm/ 3 in) and colorful (complexly patterned in red, black, and yellow) and sports very long antennae. Males have extremely long and thick front legs, used during mating. Larvae live inside bark, forming galleries inside the wood, and heavy infestations may kill the tree. Adults inhabit a variety of trees, including figs, and are strongly attracted to sap. If you are fortunate enough to find one of these large insects, look carefully under its thick outer wings (elytra). Don’t worry; it won’t bite you, at least not to the degree that you ought to care about it. Beneath the wings you can usually find a tiny pseudoscorpion (not a real scorpion, so don’t worry about being stung). The pseudoscorpion uses the harlequin beetle as a host. The host gains no benefit from the pseudoscorpion, but the little hitchhiker does no harm, so this is an example of commensalism.

Rhinoceros and Hercules Beetles These beetles, as the names imply, are formidable in size. They are members of the Lamellicornia, a beetle group that includes the scarab and stag beetles. The rhinoceros beetles (Megasoma spp.; plate 16-94) are scarabs named for the long up-curved, hornlike projection possessed by the males. Megasoma elephas, commonly called the Elephant Beetle, is a huge and bulky rhinoceros beetle that can exceed 8 cm (3 in) in length. It is mostly brownish, its elytra (thick outer wings) covered by tiny hairs. The combination of large size, long horns, and hairy surface

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makes it extremely distinctive. If you see one, you’ll recognize it. Females are similar to males in size but lack the long horns, a characteristic true of all scarabs. The Hercules Beetle (Dynastes hercules) of Central America is similar but even larger, reaching lengths of 17 cm (6.7 in). Its long horns project forward, unlike those of the Rhinoceros Beetle, which curve upward. Charles Darwin (1871) hypothesized that these large male scarab beetles evolved their horns by sexual selection (chapter 10). The horns, thought Darwin, would aid the males in combat for female scarabs. Males do use the horns in combat. Scarabs and stag beetles all over the world, from Costa Rica to Africa to the Solomon Islands, jostle like wrestlers, locking horns until the victor lifts the loser and tosses him out of the tree. What is not abundantly clear is the degree to which females care about all this pugilism. Males seem more oriented to fighting for favored feeding sites in the trees than for females. Females may “care” about the battles insofar as victorious males have access to good sources of nutrition. From a female’s viewpoint, these would be the males to get to know. There are many scarab species in the Neotropics, most very beautiful. Some species, such as those in the genus Megasoma, require mature lowland rain forest, because the larvae must live in large decaying logs. The cutting of rain forest and the conversion from forest to brushy areas may significantly reduce the beetle’s reproductive success. Already Megasoma are considered to be rare in many places.

is large, with a 12.5 cm (5 in) wingspan, and when oriented vertically along a tree trunk vaguely resembles a lizard. The reason for the resemblance is its long head, whose shape and markings make it look like a cross between a lizard head and an alligator head. One Spanish name for it is mariposa caiman, meaning “alligator butterfly.” A member of the Homoptera, or sucking insects, the Lantern Fly is unusual in almost every way. The English name Lantern Fly comes from the mistaken belief that the huge head is bioluminescent (able to glow in the dark). It isn’t. Its alternative common name, is Peanut-headed Bug, another reference to the odd shape of its head. The Lantern Fly comes equipped with several survival strategies. When oriented on a tree trunk, it is highly cryptic, its soft mottled grays making it appear as part of the bark. If disturbed, it will climb away or drum its head against the tree, making a rapping sound. If the disturbance persists, the insect discharges a skunky odor and flies to another tree. When it takes flight, it reveals bright yellow eyespots on its hind wings, rather like those of the Owl Butterfly (discussed below). These spots, which may also be revealed by a quick flash of the wings when the animal is not in flight, may act to temporarily confuse a would-be predator.

A Lepidopteran Sampler

The remarkable Lantern Fly, or Peanut-headed Bug (Fulgora laternaria; plate 16-95), is really worth seeing. It

In this section are some noteworthy butterflies and moths (order Lepidoptera) that almost every visitor to the lowland rain forests notices. I’ve previously discussed the butterflies of the genus Heliconius (plate 16-96), their relationship with plants of the genus Passiflora, and their mimicry complexes (chapter 11).

Plate 16-95. A Lantern Fly with its wings open, showing its distinctive eyespots. Photo by James Adams.

Plate 16-96. Heliconius butterflies shine like beacons in the forest understory. Photo by John Kricher.

Lantern Fly (Peanut-headed Bug)

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Plate 16-97. An Owl Butterfly resting in the shade of the forest understory during the day. Photo by John Kricher.

Plate 16-98. A swarm of butterflies at a urine site, including many pierids (whites and sulphurs) and swallowtails. Photo by Dennis Paulson.

Owls and Witches

Ant-following Butterflies

Put out a few overripe bananas at night in the Neotropics, and soon both a large brownish butterfly and a big dark moth will appear. The Owl Butterfly (Caligo memnon; plate 16-97) and the Black Witch (Ascalapha odorata) are among the largest of the tropical lepidopterans, and they tend to be strongly crepuscular (active at dusk and dawn), though adults fly during the day in deep rain forest shade. They feed on rotting fruits, hence their orientation to bananas. Black Witches are occasionally mistaken for bats in the evening twilight as they flutter about a banana bunch, and this species is frequently flushed from shaded sites such as hollow trees during the day, again giving rise to the mistaken notion that it is a bat.

There is a group of butterfly species that accompany army ant swarms, especially the swarms of Eciton burchelli (chapter 10). These so-called ant-butterflies or army ant butterflies are all members of the large family Nymphalidae and the subfamily Ithomiinae. They generally resemble Heliconius species. Only female army ant butterflies actually orient to the army ant swarms. Anywhere from eight to 12 females may fly about the swarm (researchers captured as many as 30 within a few hours at some swarms). The butterflies are feeding on the droppings of ant-following birds, probably using the droppings as a nitrogen source, necessary in forming eggs.

Morphos

The Urine Butterflies

The blue morphos (genus Morpho; plates 4-19 and 113–4) are among the most spectacular of Neotropical butterflies. Large, with brilliant deep blue upper wings that seem to glow in sunlight, morphos are deceptively swift fliers able to elude the most persistent wielder of an insect net. Common along streams and other sunlit areas, they feed on a wide variety of plant species. When on the ground or on a tree with their upper wings hidden, morphos are cryptic, but they are (to put it mildly) obvious in the air. Their striking patterning and color, visible only in flight, has been termed the “flash and dazzle” strategy of capture avoidance. There are about 80 species of blue morphos, all members of the family Morphidae.

One common sight throughout the Neotropics is the massing of butterflies along exposed riverbanks and other areas where cattle, or other creatures, have recently urinated (plate 16-98). Most of these are yellow, gold, or white butterflies, often in the genus Phoebis in the whites and sulphurs family, Pieridae. Males are bright yellow, with orange on the forepart of the wing, and females are more uniformly orange, with black lining the outer part of the wings. Sulphurs range from the United States through the Neotropics and are inhabitants of open areas and forest edges. They feed on many of the flowers, such as Lantana, that are common tropical roadside weeds. They aggregate at pools containing urine from cattle or humans. The urine supplies them with sodium

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Plate 16-99. Malachite with wings open, showing its upper wings. Photo by John Kricher.

Plate 16-100. Malachite with wings closed, resting beneath a leaf. Photo by John Kricher.

Plate 16-101. A clearwing satyr of the species Cithaerias pireta. Photo by John Kricher.

Plate 16-102. Urania moth stopping temporarily on a grassy lawn. Photo by John Kricher.

and nitrogen, just as bird droppings do for army ant butterflies. Other butterflies, especially swallowtails, may be present at a urine site as well.

often on a log along a forest trail (plate 16-101). Their wings are highly transparent, most obvious when they are flying. Several species look very much alike but are separated by range.

What’s That Gorgeous Green Butterfly? Most visitors to Neotropical forests and forest edges from Central America through northern Amazonia have the visual thrill of seeing a Malachite (Siproeta stelenes; plate 16-99). A member of the huge brushfooted butterflies family (Nymphalidae), the Malachite is both distinctive and common. Adults feed on flower nectar but are often attracted to dung, rotting fruit, or even animal carcasses. They fly slowly and often perch with wings shut (plate 16-100). Look, That Butterfly Has Transparent Wings The forest butterflies called the clearwing satyrs (Cithaerias spp., subfamily Satyrinae) are often seen in the understory and around light gaps. These butterflies have a bouncy flight and are apt to perch frequently,

That’s a Moth? At first glance, moths in the genus Urania are easily mistaken for species of swallowtail butterflies (plate 16102). They are true moths, though unlike most of their kin, they commonly fly during daylight hours. Various species occur, ranging from Central America through Amazonia, and all look similar. Some populations are migratory, and their perambulations have been linked to increasing toxicity of their host plant, Omphalea, a genus of lianas. It has been suggested that when urania moths become so abundant that their caterpillars are having a strong negative impact, the local population of Omphalea increases its defense compound concentration, driving the moths away, to find less toxic lianas. Adult urania moths feed mostly on nectar and tree sap.

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Plate 16-103. This centipede is best observed and not touched. Photo by Dennis Paulson.

Plate 16-104. This is not a scorpion. It is a tailless whipscorpion, a member of the arachnid order Amblypygi. Whipscorpions are widely distributed from deserts to rain forests and are common in the Neotropics. They do not have the stinging capacity of true scorpions and are thus quite harmless. Photo by Dennis Paulson.

Some Scary-looking Invertebrates You are apt to see some large and rather intimidatinglooking creatures scurrying about the rain forest floor or tending webs along the trail. Here are just a few of them. Centipedes You might recall the millipedes, discussed in chapter 11. They are slow and cannot really harm you. This is not true of centipedes, which belong to the arthropod class Chilopoda and are not closely related to millipedes (plate 16-103). Centipedes are fast and can bite you, and the bite is not pleasant. They are well equipped with poison glands, and they use them. So be careful. Not convinced? Well, there is one species, the Amazonian Giant Centipede (Scolopendra gigantea) that reach lengths of up

Plate 16-105. Scorpions are arachnids that vary from large (just over 10 cm/4 in) to very small (2.5cm/1 in). They occupy all habitats from deserts to forests and sometimes enter dwellings. All scorpions have a poison gland at the tail tip and are adept at using it. Potency varies—some species have much more powerful venom than others—and large scorpions are not necessarily more venomous than small species. Indeed, some of the smallest species pack the greatest wallop. Scorpion stings can be life threatening, and though such severity is rare, it is best to leave all scorpions alone. Photo by Sean Williams.

to 35 cm (nearly 14 in). That gets your attention. Usually most active at night, the giant centipede chows down on sleeping birds, mice, frogs, and lizards. It is reputed to enter bat caves, climb the walls, and capture and devour bats. But that is the good news, so to speak. Centipedes are normally nocturnal and so do not present serious threats to humans. But if you do get bitten by a centipede, you will suffer intense pain at the site of the bite accompanied by considerable swelling, plus the possibility of nausea and fever. Centipedes are best avoided. Whipscorpions and True Scorpions It is common in the Neotropics to come upon a creature with a wide and somewhat flattened body and long legs (plate 16-104). It looks scary. Many people take it to be some sort of scorpion. But it isn’t. It is

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one of the whipscorpions, common and innocuous animals that belong to an entirely different arthropod order (Amblypygi) than true scorpions (Scorpiones). On the other hand, it is also common to come upon real scorpions, the ones with poison glands at the tip of their dexterous abdomen (plates 16-105–106). Scorpions have imposing claws, rather like those of lobsters, but it is the poison-packed stinger on the abdomen of which to beware. Scorpions reside in leaf litter and decaying logs. They also enter dwellings, so be aware that you should not leave clothes lying on the floor—and it is not a bad idea in some areas to check your shoes or boots before putting them on, lest a scorpion be occupying your footwear. Many scorpions give painful but nonlethal stings, but some are rather more dangerous, and some of these tend to be among the smallest in body size. So do not assume that the bigger the scorpion, the more dangerous it must be.

Plate 16-107. The Spiny Orb Weaver (Gasteracantha cancriformis) is a widespread spider, not only throughout the Neotropics but throughout much of southern North America, as well as Australia, South Africa, and many other areas. It is seen frequently in the forest understory. Photo by Dennis Paulson.

Spiders There are many spider species in the Neotropics, and a few, such as the orb weavers, are spectacular in appearance, so take the time to enjoy them (plate 16107). Orb weavers are discussed in chapter 8. Tarantulas Tarantulas are essentially big, hairy, scary-looking spiders. But in reality they are rather docile if not harassed and are fascinating to see (plate 16-108). Tarantulas belong to a group of spiders called megalomorphs, in the family Theraphosidae, and there are reputed to be approximately 900 species throughout the world. Tarantulas are typically active at night, emerging from burrows to hunt. The largest of the Neotropical tarantulas are the so-called bird-eating spiders of Amazonia. The largest is the Goliath Birdeater (Theraphosa blondi). Its leg span reaches up to 30 cm (12 in). That’s a big spider. All tarantulas are covered with hairlike spines, and they move quickly if bothered. Their bite, like all spider bites, contains poison, but they usually seek escape rather than exhibit aggression, and most people are not inclined to pick them up and risk a bite. Tarantulas of various species are found in a wide variety of habitats ranging from deserts to rain forest. They are reclusive, staying in burrows during daylight hours and exploring for food at night. Look for them anywhere.

Plate 16-108. This tarantula was photographed during a night walk, as it happened to be wandering about on a dusty road. Photo by John Kricher.

Plate 16-106. Scorpions have the characteristic of reflecting ultraviolet light, as shown in this image. Photo by James Adams.

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Human Ecology in the Tropics

Humans in all tropical regions have had millennia in which to learn about and adapt to their environments. Indigenous knowledge, passed down orally over generations, is deeply ingrained in local tribal populations (plate 17-1). For example, Amerindian peoples make diverse use of Moriche Palm (Mauritia flexuosa) throughout its extensive range. Called the koi in Suriname and the buriti in Brazil, this species, which has been called the “tree of life,” provides wood for canoes and houses, thatch, and material for weaving. It is also used for making bow staves, spears, arrow shafts, and manioc strainers. Its unopened flowers are used to make wine or for flavoring. Fruit from Moriche Palm, used for oil, is reported to be the third most important fruit, after bananas and plantains, sold at the markets in Iquitos, Peru. A long time ago, people figured out all of those uses. Some aboriginal groups have learned to extract and refine potent poisons, ranging from batrachotoxins in frog skin (chapter 11) to curare from various plants. The spiritual world is extremely important in many tribal cultures, hardly surprising when one considers how many hallucinogenic drugs are extracted from tropical plants and mushrooms. Consequently, one of the most important members of many traditional tribal societies is the village shaman, the person who holds the knowledge about the varied uses of local plants and animals and who, it is believed, is able to communicate with the spirit world. In addition to their local knowledge of plants, the hunting skills of tropical indigenous peoples have been widely documented, from the stealth and speed with which they move through the forest to their accuracy with a bow and arrow or blowgun. This chapter considers some of the aspects of how people successfully thrive in tropical rain forests and how they have adapted certain agricultural practices to sustain crops in the tropics.

Human Occupation of Amazonia The indigenous peoples of tropical America inhabited Amazonia for several millennia before the Spaniards arrived (usually dated to 1492, the first voyage of Columbus). Their total population number remains an open question (see more on this later in chapter). When Europeans began staking claims in Amazonia between

Plate 17-1. Humans live close to nature in most tropical regions and have learned how to extract resources and nutrition from the landscape. This is Blue Creek Village in the Toledo District of Belize. Photo by John Kricher.

1500 and 1600, the indigenous population crash began, largely due to the introduction of such diseases as smallpox, diphtheria, and influenza. Questions remain as to just how dense human populations were in pre-Columbian times and what their collective influence on the landscape was. Human prehistory in Amazonia remains uncertain, but archaeological data are being uncovered. Some evidence now suggests that widespread urbanization, population concentration, and agriculture thrived within parts of Amazonia. Várzea regions, where soil fertility is annually renewed during the flood cycle, may have supported large and permanent settlements from about A.D. 500 until the European conquest. Francisco de Orellana, European discoverer of the Amazon River, reported dense human populations along much of the river when he navigated it in 1542. However, many of Orellana’s observations (actually reported by his scribe, Friar Gaspar de Carvajal) are considered questionable as to veracity. It was Carvajal, for example, who reported an aggressive tribe of women, who became known as the Amazons, very likely a mythical tribe but one from which a sizeable river obtained its name. Until recently, it was generally believed that South American Amerindian civilization originated in the Andes and slowly spread eastward into Amazonia. That view has been challenged by the discovery of artifacts that may predate Andean artifacts. Middens have been uncovered in the Santarém region of Brazil, near the confluence of the Tapajós and Amazon rivers,

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Terra Preta del Indio In parts of Amazonia there are scattered patches of a unique latosol (or oxisol) soil (chapter 6) called terra preta del Indio. The name is from the Portuguese for “black soil” or “black earth,” for unlike most latosols, terra preta is dark, often black. The reason for its color is that it is rich in charcoal. It also contains pottery shards and organic material, including plant remains, animal waste, and bones from fish and other animals. In fact, terra preta soils have as much as 14% organic matter. Unlike most soils in Amazonia (particularly on terra firme), terra preta is nutrient rich, with high concentrations of nitrogen, potassium, calcium, and other essential elements. Terra preta is a type of soil that was made by humans, an anthropogenic soil dated to between A.D. 450 and about 950. Apparently, indigenous people developed the technology and knowledge to cut the forest and burn it at low temperature, allowing the accumulation of charcoal. Terra preta soils are sometimes 2 m (6.5 ft) deep indicating that people had been present in the same location over many years, steadily building up the nutrient-rich soil. The utility of terra preta was obviously to enhance local agriculture. These human-constructed soils were far greater in nutrient content than the normal oxisols that make up most of the substrate in Amazonia. Terra preta remains are found along river courses scattered throughout the Amazon Basin; these likely indicate locations of permanent human settlements in pre-Columbian times. The high organic content and overall nutrient richness of terra preta shows a sophisticated understanding of how to enhance agricultural production such that it could support relatively large human populations. It has been suggested that terra preta could be used to enhance agriculture in the present century.

containing pottery and other artifacts that date from about 8,000 to 7,000 years before the present. The pottery dates to about 1,000 years earlier than that found in northern South America and 3,000 years earlier than Andean and Mesoamerican pottery. Archaeologists investigating this site suggest that by 2,000 years ago, a large and agriculturally sophisticated population could have been supported on the rich alluvial soils deposited by the annual flood cycle along Amazonian floodplain forests (várzea). The discoveries of archaeological sites in various parts of Amazonia suggest that dense aggregations of people settled permanently, practiced efficient and sustained agriculture, and relied on rivers to supply needed animal protein.

Mayan Impact in Central America

Hill terracing permitted the Maya to cultivate a given plot for much longer than ordinary slash-and-burn techniques, because the soil fertility was preserved. Raised fields involve the excavation of drainage canals to reduce water levels and thus raise dry fields from what was previously swampland. Ancient Maya not only used the raised fields for agriculture, but also used the canals for keeping fish and turtles, both important protein sources. Imagine being in a small plane at low altitude, flying over the Mayan Yucatán during the height of the Classic Period. It would resemble the view from a flight over midwestern North America, where vast acreages of agriculture characterize the landscape. The Maya of Tikal (plate 17-3) cultivated the ramon, or Breadnut Tree (Brosimum alicastrum). The Breadnut is today abundant throughout Guatemala’s Petén region. A single tree has the potential to yield

There is much archaeological evidence in Central America suggesting that the Maya supported their dense population by employing techniques of intensive agriculture and silviculture. Such practices resulted in large-scale landscape alterations, including extensive forest clearance (see chapter 7). Intensive agriculture in Central America was accomplished largely by two methods, hill terracing and raised fields in swamps and marshland. Hill terracing, still used today in many tropical areas, involves the construction of walls along hillsides, the walls acting to retard erosion and trap soil washed by rains (plate 17-2). (This method was also widely practiced by the Inca in the Andes.)

Plate 17-2. Hill terracing is a pragmatic form of crop production employed throughout the global tropics. This photo is from Sabah, Malaysia, on Borneo. Photo by John Kricher.

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1,000 kg (2,200 lb) of edible nutritious seeds. The Breadnut Tree is tolerant of many soil types and grows rapidly, an ideal tree for cultivation. Its fruits and seeds would have been sources of nutrition for humans and domestic animals, its leaves used for animal forage, and its wood used for construction. The unique abundance of ramon throughout areas formerly densely populated by Mayan citizenry is likely due to Mayan silviculture. Maya apparently preserved ramon seeds in underground chambers called chultunob (singular, chultun). Breadnuts probably served as a “famine food,” to be used when times were difficult.

Hunting and Gathering in Tropical Forests For the vast majority of their history, humans survived by selective use of plants, as well as by hunting and scavenging various animals. Hunter-gatherer groups have very low population densities, often less than one person per square mile (2.6 km2), and thus do little in the way of manipulating or altering the ecosystem. The impact of hunter-gatherers is normally low but not negligible. Hunter-gatherer tribes still exist in some relatively remote parts of Amazonia today but are rarely if ever encountered by ecotourists. In most areas traditional hunter-gatherer groups have increasingly had interaction with elements of modernity. Hunter-gatherer groups are commonly egalitarian, sharing food and other resources within the tribe. Egalitarianism is a pragmatic social order in a society in which individual hunters experience variable biomass yields from one day to another. Should a hunter fail on any given day, he nonetheless eats. Should he succeed, he shares. Hunter-gatherers are typically nomadic, moving their settlements after having depleted essential resources, which could range from particular animal species to certain plant species. Because they are nomadic, there is normally wide birth spacing in hunter-gatherer groups, keeping populations low. The diets of hunter-gather peoples are heavily dependent on animal food, which usually makes up between 45 and 65% of the total daily energy intake. Protein makes up 19–35% of the daily energy intake. In this regard, hunter-gatherer societies take in considerably less carbohydrate in relation to protein than non-huntergatherer groups that rely more on agriculture.

Plate 17-3. Tikal, in eastern Guatemala, dates to the Classic Period of Mayan civilization, during which much of the surrounding forest was cleared for intensive agriculture. The archaic temples look nothing like they did when the civilization flourished, but they nonetheless are invaluable artifacts. Photo by John Kricher.

In ecological terms, humans in hunter-gatherer societies harvest few calories relative to what is present in the ecosystem as a whole. Most of the plants and animals in the forest are not used. For this reason, hunter-gatherer groups require large areas. Because hunter-gatherer groups remain small, inbreeding is a potential genetic problem. Human behaviors such as incest and tribal raids that procure females, who are then brought into the raiding group as wives, are sociological adaptations to this reality. So is tribal warfare among neighboring groups. Since settlements are not permanent, and because resources are ultimately limited, periodic warfare among huntergatherer groups is commonplace. Because of the variety of hunter-gatherer tribes throughout the Neotropics, as well as differences in habitat from one region to another, cultures vary. It is not possible to describe one tribal culture as typifying all. But all traditional Neotropical hunter-gatherers are relatively nomadic, living in a small temporary village or encampment for some time and eventually moving on when they have exhausted the game or essential plants from a given locality. Hunting is accomplished by careful, quiet stalking, using a blowgun, bow and arrow, or spear to bring down essential protein: large birds, monkeys, sloths, agoutis, pacas, tapirs, and other animals. Often, but not always, arrows or darts are tipped with poison. Protein is also supplied by certain arthropods, especially large grubs, and, among tribes living along rivers, by fish (sometimes captured using poison), turtles, capybara, and crocodilians.

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Some Neotropical hunter-gatherer tribes are territorial and have been known, at least in the past, for high levels of aggression (shrunken human heads are part of the cultural artifacts of some Amazonian aboriginal groups). Tribal warfare was probably a response to the need to protect areas of forest for the exclusive use of a single tribe. Tribal raids, as noted above, were also done to procure women, ensuring genetic outbreeding through aggression, a custom inculcated within the culture. There are few “pristine” hunter-gatherers in the Amazon Basin and essentially none in Central America. Most people now use agriculture of some sort to supplement their diets and most have direct contact with the modern world. Shotguns are rapidly replacing blowguns. When Europeans first arrived in South America around 1500, the estimated total population of aboriginal humans throughout Amazonia was as much as 6.8 million, though some estimates suggest a number half that size. By the early 1970s, the indigenous population was only 500,000, and in Brazil alone the number dropped precipitously from about a million to about 200,000 during the 20th century. By 1988, the estimate for all of Amazonia was only about 250,000, a 24-fold decrease from an estimated 6 million. Amerindian populations were reduced by a lethal combination of conquest and genocide, slavery, and, probably most significant, by the introduction of various European diseases, to which the Amerindians had little natural resistance. In Amazonia, tribes that inhabited várzea, who represented the largest Amerindian populations, fared worse than all others, being essentially decimated by Europeans. Only those tribes such as the Yanomami, the Javari, the Xingu, and others that inhabited remote and inaccessible forest survived the conquest period, and even they suffered reductions in population whenever there was European contact. Today, most Amerindian tribes live on anthropological reserves or “indigenous areas,” called resguardos, lands in which aboriginal groups are permitted to follow their traditional lifestyles. In Brazil, Indian lands are administered by the government agency Fundação Nacional do Indio (FUNAI), or National Indian Foundation. This agency governs a huge area representing 100.2 million ha (248 million ac) in 371 reservations in the Brazilian Amazon, representing roughly 20% of Brazilian Amazonia.

In the northern state of Roraima, about 42% of the land area is reserved for use by Indians, even though they represent only about 15% of the population of Roraima. Numerous issues face indigenous tribes. Amerindian populations continue to be forced into retreat in some areas, as people with different cultural backgrounds, often from overpopulated, extremely poor urban areas, migrate to the new frontier of the rain forest, some to begin subsistence farming, some in search of gold. This trend has greatly accelerated in Amazonian Brazil due to the continually expanding Trans-Amazonian highway system and, most recently, by the construction of major hydroelectric dams (chapter 18). In some areas aboriginal tribes (for example, the Nambikwara tribe of Mato Grosso, Brazil) have been exploiting their own lands for short-term profit, granting permission to outsiders for logging and gold mining.

Impact of Hunter-Gatherers Do hunter-gatherers eventually deplete local game populations? A study of the Siona-Secoya Indian community in terra firme rain forest of northeastern Ecuador, documented 1,300 kills representing 48 species, including various mammals, large birds, and reptiles. The average number of kills per 100 manhours of hunting was only about 21 (within a sample size of 802 man-days and 6,144 man-hours) and the mean number of kills per man-day of hunting was only 1.62. These figures do not suggest that hunting pressure was sufficient to deplete the animal populations and are consistent with other studies. In contrast, if one looks at the entire rural population of Amazonian Brazil, including colonists as well as aboriginals, subsistence hunting takes on far greater impact. There are numerous examples of hunting pressure being responsible for the local depletion of animals.

Agriculture in the Neotropics Agriculture, which developed about 10,000 years ago, differs from simple gathering (finding plants useful as food or fiber and then collecting them) in that the plants in question are selectively chosen and cultivated, increasing their population densities at the expense of cohabiting species. Humans use work energy to nurture and protect the plants chosen for agriculture

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Plate 17-4. This plot of cleared land, planted mostly with corn, is a milpa. It is typical of rotational agriculture in southern Belize (in this case) as well as much of the rest of the tropics. Photo by John Kricher.

Plate 17-5. The charred remains of trees are readily visible among the bananas growing in this agricultural plot on Trinidad cleared by slash and burn. Photo by John Kricher.

until it is time to harvest them, which requires more human labor. Agriculture requires work of a much different sort from that required of hunting and gathering. People alter the local ecology to redirect a significantly greater portion of the sun’s energy to themselves. This alteration or perturbation of the ecosystem, the conversion of a natural ecosystem to one containing only selected, harvestable species, forms the essence of agriculture. The Neotropics are the place of origin for: • Maize (corn), sometime between 9,000 and 8,000 B.P. (years before present). • Pumpkin and related squash, about 10,000 B.P. • Potato, about 7,000 B.P. • Peanut, about 8,500 B.P • Manioc, about 8,000 B.P. • Chile pepper, about 6,000 B.P. • Other important crops include cacao, tobacco, peach palm, and rubber. In order to support agriculture a plot of land must be cleared of all competing species. Desired species must be planted and continuously protected as they grow. This requires human labor. People are concentrated around relatively small agricultural plots, tending crops (plate 17-4). Because land can be farmed repeatedly, and because agricultural labor requires constant human effort, permanent or semipermanent villages form. Traditional agriculture supports somewhere between 10 and 100 persons per square mile, a one to two order-of-magnitude increase from that of hunter-gatherer societies.

Crop ecosystems are ecologically unstable, open to invasion by both competitors and herbivores. Thus energy input from human labor is fundamental to preserve the stability of crop ecosystems. What this means, of course, is that humans must reinvest some of the energy (in the form of human labor) they derive from the present growing season’s crops to ensure the success of crops in the forthcoming season. They must also devote some of the productivity of the crops to sustaining domestic animals. Work provided by animals includes not only pulling objects such as plows but also supplying essential fertilizer. Animals are also used as food.

Slash-and-Burn Agriculture Tropical peoples face a challenge in attempting to farm in rain forest, because the soils are nutrient- and mineral-poor. Most of the minerals and nutrients are not in the soil but in the biomass: the trees, lianas, and epiphytes. To clear an area for farming, it is obviously necessary to remove that mass of vegetation. But to do so seems to doom the farming effort, because the poor soil will not sustain very much in the way of crops. The way out of this dilemma is fire, applied in a practice that has come to be termed slash-and-burn agriculture. Slash-and-burn agriculture follows a typical pattern: A small plot of land (usually between 0.4 and 0.6 ha/1–1.5 ac) is chosen, and machetes and axes are used to cut down all of the vegetation. Trees too large to be cut are girdled, which kills them. The tangled pile of vegetation is then set on fire rather than removed.

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Plate 17-6. Subsistence farmers, such as the ones who live here, commonly practice slash-and-burn agriculture. Photo by John Kricher.

Plate 17-7. Young boy skillfully paddling a dugout canoe. Photo by John Kricher.

Fire eliminates the leaves and wood while at the same time releasing the nutrients and minerals contained within. The ash raises the pH, making the soil less acidic, so the soil surface, fertilized by the ash from the biomass, tends to be alkaline. The farmer plants crops for a few years on relatively fertile soil. Rainfall will still act to erode the now-exposed soil and leach minerals. The crops themselves are removed, of course, and with them go more of the minerals. The result is that fertility and yield decline steadily. Typically, staple crops include manioc (various varieties), plantains, bananas, sweet potato, pineapple, chile peppers, and others (plate 17-5). Plots are normally planted as polycultures rather than monocultures, a practice that helps with pest control and slows the rate of natural succession. Crop losses from predation by such creatures as agoutis are actually anticipated and extra sweet manioc is often planted for rodent consumption. As available soil minerals are depleted, crop yields typically decline sharply within the first four to five years of cultivation. Within a few years the plot will be abandoned, allowing natural succession to occur. The typical time sequence for slash-and-burn agriculture is to farm the plot for two to five years (sometimes only for one year, sometimes for as long as seven years) and then abandon it for at least 20 years. Ideally (but rarely), an area just abandoned will not be recut for nearly a hundred years or so, permitting substantial recovery of the system. Slash-and-burn agriculture requires constant rotation of sites and often results in a nomadic population that must move around in the

rain forest to find suitable plots to farm. Because of soil nutrient limitation and therefore the need to allow forest regeneration, the human population density remains generally low (plate 17-6).

Nonindigenous Farmers in Amazonia Should you travel anywhere along the Orinoco, Amazon, or the major river tributaries, you will notice immediately that areas along rivers are inhabited by people, particularly várzea areas. When Europeans colonized Amazonia they bred with Amerindians, and the descendants of those unions became the people who today make their living by farming and fishing the floodplains. The riverine peasantry is called caboclo, ribereño, mestizo, or campesino, depending upon region (plate 17-7). These people practice agriculture on the floodplain in a manner similar to those populations on terra firme, with the exception that they make much more use of a market economy rather than relying entirely on subsistence. Because they are on a river they have the ability to move goods. They grow rice as a cash crop, for instance, and sell fish at market. Indeed, the largest and most diverse fish market in Amazonia is at Manaus, Brazil, where between 30,000 and 50,000 tons of fish are marketed annually. Riverine people also harvest such things as Brazil nuts, palm fruits, and rubber for commercial sale. Note that such usage is not necessarily environmentally damaging, unless overharvesting occurs (and it often does with game animals, including creatures such as tapirs, manatees, turtles, and capybara, though not so much with plants).

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Agroforestry: Focus on Coffee Coffee and Cacao are each widely cultivated in the tropics and each is fundamentally an understory plant (plates 17-8–9). Coffee is a shrub, the Cacao is a small tree. Agroforestry is the practice of crop cultivation within a forest. Only the planting of the understory crop alters the forest. The canopy and other attributes of the forest remain more or less unaltered (but see below). Agroforests are floristically less complex than other forests, often with a dominant canopy species, such as the widespread tree Inga. Structural complexity varies considerably, depending upon how much the forests are manipulated. There is, for example, a gradient of shade coffee agroforests, ranging from rustic, where there has been essentially no canopy alteration, to various degrees of plantation forests, where select species such as Inga are planted to varying densities. Coffee is in the Rubiaceae, a large plant family of some 550 genera and 9,000 species. Two species, Coffea arabica and C. canephora (also known as C. robusta) are cultivated. Caffeine averages from 0.8 to 1.4% in C. arabica and 1.7 to 4.0% in canephora. Many varieties, called cultivars, have been developed within each species. C. arabica is endemic to Ethiopia, southeastern Sudan, and northern Kenya, but today it is planted over 10 million ha (25 million ac) within more than 50 countries, representing about 70% of the world’s coffee crop. In the Neotropics, about 95% of the coffee grown is C. arabica. In 2006, the countries producing the most coffee were Brazil, Vietnam, and Colombia. While coffee is genetically adapted to grow in shade, cultivars have been produced that thrive in full sunlight. This has resulted in the progressive replacement of traditionally shade-grown coffee with high-intensity agriculturally grown coffee, a trend that has caused concern among those interesting in conserving tropical biodiversity through more traditional agroforestry. Traditional coffee production, in what are called rustic coffee plantations, involves replacement of understory species with coffee plants. Forests remain relatively unchanged, aside from the dominance of coffee plants throughout the understory (plate 17-10). But coffee plants grow more rapidly with more sun, so in many cases some canopy trees are taken out to open the forest and permit much more light, reducing the biodiversity value of the rustic coffee plantation

Plate 17-8. Coffee beans ripening on the plant. Photo by John Kricher.

Plate 17-9. Cacao fruits grow from cauliflorous flowers (chapter 3) on understory trees. Photo by John Kricher.

(plate 17-11). Sometimes the coffee is combined with other crop plants, such as various fruits, vegetables, and medicinal plants to form a complex polyculture. A more focused approach, usually called commercial polyculture, requires additional manipulation and simplification of the ecosystem to permit greater sunlight and faster growth of coffee. This approach may be extended to create reduced or specialized shade by replacing canopy tree species with select species of Inga, Erythrina, Gliricidia, or other genera. Inga is a canopy-level species, but the others are small trees that allow far more sunlight to penetrate. Finally, there is the full-sun coffee plantation, a monoculture that appears identical to those of traditional large-scale agriculture. Sun-coffee plantations have been simplified to the

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Plate 17-10. This rustic coffee plantation near Gallon Jug, in western Belize, is representative of a traditional coffeegrowing approach. There is a dense canopy of indigenous trees, and the biodiversity of this plantation is high. Photo by John Kricher.

Plate 17-11. This is the same area in Belize some years later, when some of the canopy trees were removed to permit more sunlight for coffee growth. The dense coffee understory is readily evident, but the forest’s biodiversity has been reduced. Photo by John Kricher.

degree that they no longer support forest biodiversity and thus represent a form of habitat loss, just as the cutting of forest for soybean production does. It has been long recognized that rustic coffee production acts to preserve local biodiversity. But as noted above, some plantations are not rustic, but instead utilize a single species of canopy tree, in many cases Inga. Studies have demonstrated that rustic coffee plantations act to maintain high species richness of birds, essentially the same as that of any local forest. In plantations that have an overstory of purely Inga or Gliricidia, considerably fewer species occur than in mature forests. In other words, as coffee plantations are structurally simplified, bird species richness declines, especially in sun-grown coffee plantations. As forests are converted to grow increasingly sunadapted cultivars of coffee, biodiversity is lost. It is clearly possible to continue to grow coffee in a manner in which that outcome is prevented. Shade coffee is not the same as undisturbed forest, but it has clearly demonstrated the potential to maintain a reasonably high biodiversity. Efforts by conservationists to promote the use of shade coffee and develop a market for a coffee product that does not deplete biodiversity are ongoing. But problems exist with the pragmatics and economics of shade coffee. Typically, it is considered to be premium coffee and costs more at the store. There is also the matter of certification. How does one know that the coffee is really shade coffee? There must be some form of enforcement in the field to assure that the coffee really is shade coffee.

Certification programs differ, so “certified” for one brand of shade coffee may mean something different from that label to another. For example, some certification programs exclude shaded monocultures while others do not. Nonetheless, if the challenges of social and economic factors are met successfully, there is little question of the potential value of shade coffee production to sustain much biodiversity. To that end, if you are eager to support conservation efforts in the Neotropics, switch to consuming shade-grown coffee. Be aware that most commonly sold coffee brands (including coffee served in various restaurant outlets specializing in coffee products) are not shade grown. But there are organic shade-grown coffee dealers and a quick check on the Internet will take you to several websites. Various brands of shade-grown coffee are sold on Amazon.

Ethnobotany Native peoples in the tropics have generations of experience with plant and animal defense compounds. It is not surprising that indigenous people have found multiple uses for the diverse array of chemicals contained within the many species of native flora and fauna. Chemicals have been extracted for use in arrow (dart) poisons, hallucinogens, fish poisons, drugs for medical and related use, stimulants and spices, essential oils, and pigments.

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Ethnobotany is the study of how indigenous people have learned how to use ambient vegetation for a diversity of pragmatic purposes. It is broader in scope than merely the extraction and subsequent usage of chemicals contained within the plants. Ethnobotany also includes a consideration of all uses of plants, including for food and fiber. It is an interdisciplinary field involving botany, anthropology, archaeology, plant chemistry, pharmacology, history, and geography. Ethnobotany is not confined to the tropics. A perusal of old herbal manuals will quickly reveal that numerous North American plant species were relied upon for pharmaceutical applications in years past, until the advent of modern medicines. Some still are used. As one example, resin from the Mayapple (Podophyllum peltatum), a common understory spring wildflower throughout eastern forests, was commonly employed by Native Americans to remove warts. It is still used today to treat venereal warts. In the Neotropics, many make the assumption that ethnobotany applies only to isolated indigenous tribes, but this is false. Modern populations of mixed heritage, such as the mestizos and ribereños of Peru or the caboclos of Brazil, all of which are linked to native Amerindian cultures but also under strong Western influence, make heavy use of ethnobotanical knowledge. Ethnobotanical insight is gained through generations essentially by trial and error. Not all indigenous groups possess equally sophisticated ethnobotanical understanding. With regard to extraction and preparation of various drugs and drug combinations, the knowledge is often housed in the mind of but one revered individual, the shaman of the village. Nothing is ever written down but is instead passed on from one generation to the next by the shaman, who is both a teacher and a practitioner, a person of substantial power in the community. Illnesses are rarely if ever blamed on organic causes but are usually assigned to evil spirits or curses. It is the shaman who communicates with the spirit world—and who cures headaches, back pain, bug bites, and constipation. Unfortunately, a shaman may die of old age before passing his knowledge to the next generation. There is widespread fear among ethnobotanists that much knowledge is currently being lost, as traditional tribes experience the impact of Western culture, and fewer young people study to be shamans. Ethnobotanist Mark Plotkin, in his best-selling and now classic book Tales of a Shaman’s Apprentice (1993),

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describes how he studied with shamans in northeastern South America, relating many intriguing examples to demonstrate the sophisticated knowledge of local people in the use of tropical defense compounds. Alkaloid-containing sap from a common liana is used to help cure fever in children. Rotenone, a potent vasoconstrictor, is extracted from another common liana and employed to kill fish, a critical protein source. Plants that even a skilled botanist has difficulty telling apart are easily recognized as separate species by the shaman. Equally intriguing is Plotkin’s vivid descriptions of how he was tutored in this knowledge (including the use of hallucinogens) by various shamans whose trust and respect he patiently won. Many serious ailments may be helped by potent compounds from the tropics. For many years the alkaloid quinine (found in tonic water), from the Neotropical shrub/small tree genus Cinchona, has been reasonably effective in combating certain malarias. Resin extracted from plants of the genus Virola, used as a powerful hallucinogen, may also prove to be very effective in controlling or even curing chronic fungal infections, which currently can be suppressed only by Western medicines. The legendary ethnobotanist Richard Evans Schultes, often called the “father of ethnobotany,” spent a career documenting the diverse uses of numerous plant species by indigenous peoples of Amazonia. His classic book, The Plants of the Gods: Their Sacred, Healing, and Hallucinogenic Powers (1979), coauthored by A. Hoffmann, is required reading for anyone interested in ethnobotany. Mark Plotkin notes that at the time he was writing only about 5,000 of the world’s 250,000 species of plants had been thoroughly investigated as to pharmacological properties, and that the 120 plant-based prescription drugs on the market had been derived from only 95 species. Plotkin emphasizes the obligation to share any benefits that may be derived from ethnobotanical studies with the indigenous people who, in fact, obtained the knowledge in the first place. Such a policy is not only morally compelling, it has strong conservation potential. For example, the Terra Nova Rain Forest Reserve in Belize was established in 1993 by the Belize Association of Traditional Healers, an assemblage that includes people from most of the cultural and ethnic groups in Belize, a country in which about 75% of the people are estimated to be dependent on plant medicines for their primary healthcare needs. The reserve, a 2,400 ha (5,930 ac) area of

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lowland forest, is managed to accomplish the following: cultivation and documentation of medicinally useful plants; protection of the plants from overharvesting; conducting of ethnobotanical and ecological research; and encouragement of ecotourism, with walks and seminars designed to teach about the uses of the plants. Schultes and Robert Raffauf, in their book The Healing Forest (1990), discuss approximately 1,500 species and variants of plants from 596 genera and 145 families, all of which have medicinal or toxic uses by indigenous peoples in northwestern Amazonia. It is fascinating to see the range of symptoms that are treated as well as the diversity of plants that are applied to certain common ailments or conditions. For example, there are 38 plants that can be used for diarrhea, 25 for headache, 18 for muscular aches and pains, and 38 for toothache. There are many plants that can be used to treat various insect bites (including 16 for ant bites), 36 for intestinal parasites, and 29 for snakebites. Twenty-six plants are listed for use as contraceptives. In addition, there are plants alleged to have use in treating such conditions as sinusitis, stiff neck, bleeding gums, stomach ulcers, cataracts, asthma, swollen breasts, epilepsy, testicular swelling, tumors, boils, blisters, mange, and baldness, a selection that is by no means comprehensive. It is necessary to bear in mind that the degree to which these diverse applications achieve success is debatable. Besides medicinal uses, many plants are used to extract various poisons for hunting and many other plants are used for hallucinogenic or narcotic purposes. I will close this chapter with a brief look at some of the better known of these.

Curare Charles Waterton, whose first journey to Amazonia was in 1812, was undoubtedly a wonderfully entertaining dinner guest. What stories he must have told. This aristocratic, eccentric explorer of the Amazon demonstrated uncommon skill at taxidermy as well as intrepid drive for exploration and discovery. One of his discoveries was that indigenous people had found a very powerful drug, one now called curare. Waterton (1825) describes a vine, called wourali, which supplies the primary ingredient for arrow poison, and the “gloomy and mysterious operation” in which the poison is extracted and prepared, only by certain skilled individuals. He details how a large ox, estimated to weigh nearly 450 kg (1,000 lb), died

within 25 minutes after being shot in the thigh with three poisoned arrows. The poison, said Waterton, produced “death resembling sleep.” Curare has such a powerful effect of relaxing muscles that it induces paralysis. And that’s the basic idea. Curare is added to the tips of arrows and darts and then used by skilled hunters to bring down various species of mammals and birds. If you look at the small darts that are the ammunition of blowguns, you will see immediately that these weapons would do little more than make a pinprick in their intended prey were it not for the presence of the poison. The arrow or dart doesn’t bring the creature down—the curare does. Curare and its derivatives are well known by practitioners of Western medicine, as they are commonly employed during certain surgical procedures. Curare takes its name from the plant genus Curarea (sometimes known as Chondrodendron). Curarea plants are lianas, beginning as rooted shrubs that eventually become climbers. Curarea toxicofera is a species that is widely used by many tribes. The curare is extracted from the bark and wood of the stem and is often mixed with other species, particularly those in the genus Strychnos. Curares are extracted from many different kinds of plants from an array of different families. Indeed, over 75 plant species are utilized for this purpose in Amazonia. Most curares are mixtures of several plant species (often prepared specifically for the kind of animal sought), made with much variation, not only from tribe to tribe but from one shaman to another. The art of preparing curare requires careful attention to detail. It is a dangerous substance.

Cocaine Cocaine is an addictive and powerful narcotic, a powerful alkaloid extracted principally from a small, unpretentious shrub, Erythroxylum coca, var. ipadu, from western Amazonia. The substance extracted is commonly called coca. A second species, E. novogranatense, is cultivated along the eastern slopes of the Andes. Neither species is cultivated in lowland areas because alkaloid content is higher if cultivated at higher elevations. Coca contains numerous alkaloids, but cocaine is the one in greatest concentration. Though cocaine is considered a scourge of society in North American culture, it has important traditional uses by South American indigenous peoples: as medicine, in

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certain rituals, for chewing, and for nutrition. Studies show that ingestion of 100 g (3.5 oz) of coca leaves is sufficient to supply one’s daily needs for calcium, iron, phosphorus, and vitamins A, B2, and E. Chewing wads of coca leaves also suppresses fatigue, providing important added endurance for people in the rarefied air of the high Andes. It should be emphasized that a leaf contains only about 1% cocaine and the effects are modified by other compounds in the leaf, so chewing coca leaves is not the same as smoking crack cocaine (which affects the brain in as little as 5–10 seconds). Coca leaves are also applied to wounds or boiled to make a tea. Most coca that is grown to be used as a narcotic is from Peru and Bolivia, though it is purified and shipped from Colombia, which produces about 80% of the world’s cocaine. One area of cultivation is the Upper Huallaga Valley in Peru (along the eastern slopes of the Andes), where it is estimated that 60% of the world’s coca is grown. One historic note of interest is that the soft drink Coca Cola was at one time really coca cola. In 1903, based on the recommendations from a report by the US Commission on the Acquisition of the Drug Habit, the producers of Coca Cola eliminated the minute amount of cocaine that, up to that time, had been included in the recipe. The report asserted that mostly “bohemians, gamblers, prostitutes, burglars, racketeers, and pimps” were using cocaine.

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blown with great force, through an elongate pipe made from a plant stem, into the nostrils and sinuses. In some cases, however, the drug is administered orally, in the form of a pellet. A combination of strong indole alkaloids, the drug, once administered, causes immediate tearing and mucous discharge, soon followed by a restless sleep during which the person is subject to extreme visual hallucinations described as “nightmarish.” Details of this experience can be found in Schultes and Hoffmann (1992), Schultes and Raffauf (1990), and Plotkin (1993). Besides use as a hallucinogen, the Virola preparation is used for an array of medical problems. Aztec and Maya of Central America routinely used mushrooms and various “psychedelic” fungi in their religious rituals. Peyote, derived from the cactus (Lophophora spp.), is a widely used alkaloid hallucinogen throughout Middle America.

Looking to the Future Indigenous people as well as others who reside in the vast Neotropics face numerous issues ranging from the potential continued development of Amazonia to the growing impact of accelerating climate change (plate 17-12). The conservation of this unique biological realm is uncertain, and that is the subject of the concluding chapter.

Intoxicants and Hallucinogens Perhaps the best-known hallucinogen of the Neotropics comes from the genus Virola, in the nutmeg family (Myristicaceae). There are between 62 and 65 species of these understory trees throughout the Neotropics, and extracts from a few of them are widely used throughout western Amazonia and much of the Orinoco Basin to achieve rapid and extreme intoxication with subsequent hallucinations. This practice serves multiple functions, ranging from spiritual divination to ritualistic diagnosis and treatment of disease. In many tribes only the shaman takes epena, ebena, or nyakwana, as the Virola preparation is known, while in others, such as the Yanomami, for example, all male members of the group participate. The drug itself is obtained from cambial exudate on the inner bark of the tree, which is boiled, simmered, and refined into a reddish powder. In most cases the drug is taken as a powdered snuff,

Plate 17-12. This child with an orphaned howler monkey, its tail around her neck, likely will face some major ecological and societal changes over her lifetime in the tropics. Photo by John Kricher.

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Plate 18-1. Cattle ranching, fields of soybeans, teak plantations, continued logging, damming of major rivers, and climate change all portend accelerated changes for the ecology and biodiversity of the Neotropics. Photo by John Kricher.

Plate 18-2. This degraded forest in Amazonian Brazil (in Mato Grosso do Sul) has been cleared for logging and for conversion to agriculture. Perhaps ironically, the words mato grosso come from the Portuguese for “thick wood.” The color of the sky is due to heavy smoke created by the burning of wood (during the dry season) from the cleared forest. Photo by John Kricher.

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The Future of the Neotropics

Threats to Tropical Forests: Overview Ecologists have identified many potential threats to the integrity of tropical forests. These include continued deforestation, forest degradation, forest fragmentation, and increasing loss of biodiversity. Forest conservation is a complex topic, because it is not just a matter of forest clearance. Forests may not be fully cleared but nonetheless be significantly degraded. Forest degradation results from such activities as logging, agriculture, cattle ranching, prospecting for minerals, and building of hydroelectric dams (plate 18-1). Forests may be highly fragmented, which isolates small forest tracts from one another, causing severe ecological effects. Local hunting pressure may leave a forest essentially intact but lacking in animal species essential for seed dispersal. Another more subtle and complex threat is the effect of climate change, a reality that will likely alter forest dynamics, biotic interactions, trophic dynamics, carbon sequestration, recycling of nutrients, and land-use patterns.

Deforestation: How Much, How Bad? It is well known that there has been extensive deforestation throughout the global tropics, including the Neotropics. Rates of deforestation throughout the tropics are difficult to obtain and are constantly changing. Anyone who travels throughout a tropical region will bear witness to deforestation, but such observations are anecdotal and difficult to quantify. The method of choice for estimating large-scale regional deforestation rates has been satellite imagery, because it provides a large-scale look at forest changes over time. One study, which used 30 m resolution satellite imagery, concluded that from 1990 to 1997, a total of 5.8 million ha (14.3 million ac) of humid tropical forest had been lost annually (an area about the size of the state of Maryland) and that an additional 2.3 million ha (5.7 million ac) were visibly degraded. The once extensive Atlantic Forest of southeastern Brazil has been reduced and fragmented to a mere 10% of its original area. Approximately 70% of the animal species considered endangered in Brazil are confined to the Atlantic Forest. There are about 55 threatened bird species (each of which is endemic), and 21 threatened endemic mammal species. European colonists began

cutting the forest immediately upon their arrival, because they believed that the forests had to be cleared to allow for social progress (as did the European settlers who colonized North America). Deforestation in the global tropics is closely linked with growth of human population (plate 18-2). As rural populations have burgeoned, forest loss has increased. The United Nations Food and Agriculture Organization (FAO), using data generated from satellite observation, has documented that tropical deforestation usually occurs first in the more dry and open forests (which are easier for humans to access), rather than humid rain forests, and that about 2.2% of the potential closed-canopy tropical forest (all forest types combined) is being removed each decade. Forests are dynamic. If land that has been cleared is abandoned, secondary forest will normally grow on the site. So in some areas, such as areas cleared for logging and subsequently abandoned, forests are returning through the process of succession (chapter 7). But secondary forests are different from old-growth forests. The dynamic between forest loss and forest regrowth is complex, and it has major implications that are essential to understand in considering the future of tropical forests. It has become a topic of significant debate and will be discussed further below.

Fire, Degradation, and Deforestation Human-caused fire has been shown to have a strong impact on forest degradation, even to the point of gradually changing forest into savanna in some areas. Accidental fires are linked to road building, agriculture, mining, and pretty much any human intrusion into forest. Initially fires are of low intensity and travel along the forest floor, not reaching the canopy. But though the fires appear only to destroy leaf litter, they also kill tree stems, because many tropical trees have thin bark. A cascade of ecological effects ensues. The fire thins the forest, and subsequent windthrow adds debris to the litter layer. The increasingly open canopy permits greater solar heating, and the litter dries, making it more prone to fire. The greater openness results in growth of various vines and herbaceous species that add combustible fuel. Forests that have burned are therefore likely to burn again and with greater intensity. A positive feedback is established in which each subsequent fire is more severe than the previous one, and recurrent fires

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become more frequent. Forests become so degraded by fire that the land becomes, in effect, deforested. This forest fire feedback loop is exacerbated in El Niño years, when there is less rainfall. Indeed, heating and drought, both forecast to increase in the future due to climate change, are expected to greatly increase occurrence of serious fires in areas of humid tropical forest. Though natural fires do occur in Amazonia, the time between fires at a given location is historically in the hundreds or thousands of years. That has changed.

forest biomass, permit greater light penetration, create damage to soils, and increasing potential for serious fire. Conservation biologists distinguish between deforested areas, as are typical in areas of agriculture, and degraded forest, where logging is practiced. Another question focuses on the impact of logging on wildlife. Logging roads and skid trails permit hunters to penetrate areas that would otherwise be difficult to access and have therefore contributed to increasing wildlife harvest.

Logging

Deforestation in Amazonia

Logging is practiced routinely throughout the global tropics (plate 18-3). This activity may take various forms, ranging from clear-cutting to more selective removal. In many parts of the temperate zone, particularly in North America and Europe, sustainable logging is well established. In its most basic form, sustainable logging is based on removal of trees of economic value that have not yet reached senescence, which is the point at which plant growth is slowed essentially to a stop. Thus harvesting when the trees are still vigorously growing is, in the economic sense, logical. The logged area is reseeded or replanted with tree species that attain harvestable size relatively rapidly. In many cases, temperate-zone forests may be clear-cut in 40to 50-year (or shorter) cycles. Sustainable logging is, in a sense, much like basic agriculture, with trees as the crops. Debatably, sustainable logging in much of the temperate zone has not resulted in major species reductions or loss of ecosystem function, though this is not true in such places as Germany and Scandinavia. Logging in the tropics is not as straightforward as it is at higher latitudes. Some forests are largely clear-cut. But in many cases valuable trees must be removed individually because they are widely separated, a general characteristic of tropical forest tree distribution. Loggers make trails to access trees whose timber is deemed of value, and logging roads penetrate deeply into forests. Trees are cut and subsequently dragged over skid (also called snig) trails to the road to be loaded on to large trucks. Trucks carry logs from forest to central locations where they can be shipped to urban areas for further processing (plate 18-4). Intensive logging activity in the tropics results in forest degradation. Logging roads, skid trails, and human activities associated with logging impose damage to plants other than the target species, reduce

Extensive deforestation has occurred in many areas of the Amazon Basin, particularly in Brazil, which occupies the majority of the region. The Brazilian Amazon contains about 40% of all remaining tropical rain forest; because of this massive area, the future of the Brazilian Amazon has been a focus of concern for many years. Most deforestation has been associated with the growth of soybean production and cattle ranching (plate 18-5). Some years ago, for example, there was much discussion about the “hamburger connection,” having to do with the exportation of inexpensive South American beef, raised in pastures that were once rain forest, to North America for use in fast-food restaurants (plate 18-6). Brazil has been the focus of attention for many years, though other Amazonian countries have also experienced major deforestation of lowland forest. In Brazil, forest clearance has been most extensive in the states of Mato Grosso, Pará, and Rondônia. Much of the rest of the country remains deeply forested. While much of the forest clearance in Brazil has been for cattle ranching and soybean production, logging has also been a major activity. A comprehensive review of logging in the Brazilian Amazon by Greg Asner and colleagues showed that from the years 1999 to 2002 between 12,075 and 19,823 km2 (4,662–7,654 mi2) were logged per year, figures that were somewhere between 60% and 123% greater (depending upon which study it was compared with) than those that had been reported previously. The study employed large-scale, highresolution, automated sensing analysis, using Landsat Enhanced Thematic Mapper Plus satellite data, to detect previously undetectable logged areas. The researchers found that, in general, such protected areas as national parks, reserves, and lands belonging to indigenous people were not subject to illegal logging, with the

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Plate 18-3. Big logging trucks carrying huge logs from rain forest trees are commonplace in many areas of Amazonia. Photo by John Kricher.

Plate 18-4. Logs at a collection area in Mato Grosso, Brazil. Photo by John Kricher.

Plate 18-5. Large cattle ranches are found in many areas of the Neotropics. Photo by John Kricher.

Plate 18-6. Cattle ranching is a major enterprise throughout much of the Brazilian Amazon region. This is a herd of cattle coming down a road to go to pasture. Photo by John Kricher.

exception of areas in northern Mato Grosso. However, selective logging of the Brazilian Amazon had in effect doubled the total amount of forest degraded by human activities than previous estimates had shown. The researchers estimated that the total volume harvested equated to the removal of between 10 and 15 million metric tons of carbon (MtC). This did not count the masses of debris, such as stumps, branches, foliage, that will eventually decompose, adding carbon dioxide to the atmosphere. No one denies that logging may create significant collateral damage to ecosystems. But in global markets, demand remains high for wood from tropical trees. The limitations to sustained logging in Brazil are formidable: high species richness within the world’s most complex terrestrial ecosystem, slow growth and

regeneration of trees, and relatively few tree species of high economic value (such as Mahogany, Swietenia mahagoni, for example). Any logging will result, under the best of circumstances, in some collateral ecological damage.

Effects of Hunting on Species Hunting is widely practiced throughout tropical ecosystems. Indigenous people are expert hunters and have become increasingly skilled at using shotguns rather than traditional weapons. Hunting has had an impact on tropical forest dynamics, and hunting intensity is sometimes sufficient to drive local populations of large bird and mammal species to local extinction.

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Elimination of large animals by hunting affects forest function, as first described by Kent Redford in a paper with the evocative title “The Empty Forest” (1992). An “empty” forest may appear normal, but it is not, due to lack of key animal species that disperse seeds, for example. Large animals are often disproportionally depleted. At Manú National Park in the Peruvian Amazon, the loss of large and medium primates due to hunting negatively affected seed dispersal. Local hunting exterminated large primates (such as spider and woolly monkeys) and reduced medium-size primates (such as capuchins), many of which are critical seed dispersers, by up to 80%. As a consequence, tree species richness was 55% lower on the hunted sites than on sites where monkeys were not hunted. In a carefully controlled series of experiments done in Veracruz, Mexico, Rodolfo Dirzo and Eduardo Mendoza documented that in areas subject to strong hunting, the mammalian fauna is altered as the large animals are largely eliminated, the balance shifting in favor of small animals such as rodents. These small mammals preferentially devoured small-seeded species of plants, providing an advantage for large-seeded species whose seed predators had been eliminated by hunting. Hunting pressure is clearly sufficient to change the plant species composition of a tropical forest. Hunting will likely continue to be a problem throughout the tropics. Whatever balance there may have been between indigenous peoples and the animals they hunted is no longer equal, at least not in places where guns have replaced traditional forms of hunting (plates 18-7–8).

Forest Fragmentation Fragmentation, which is increasing throughout the Neotropics, occurs when forests are cut and divided into parcels of varying sizes, separated by non-forest habitat. A patchwork of semi-isolated forest fragments results. Fragmentation results in numerous ecological effects and in some cases may lead to eventual loss of species. Some of those effects come about as fragmentation increases the proportion of edge habitat in relation to total forest volume. Furthermore, isolation of forest fragments inhibits dispersal of many plant and animal species, a critical component of tropical ecology. Millions of hectares of tropical forest (ranging from lowland rain forest to tropical dry forest) are cleared annually and converted to pastures, agriculture, or some other use (plate 18-9). In many cases, forest

clearance leaves behind scattered remnant forest “islands.” That is fragmentation. Ecologists have investigated how fragmentation affects complex food webs typical of closed tropical forests. One of the most insightful projects has been the Biological Dynamics of Forest Fragments Project.

The Biological Dynamics of Forest Fragments Project Approximately 70–90 km north of Manaus, Brazil, on terra firme forest, there is an ongoing study that was established to evaluate the ecological effects of forest fragmentation, with the associated objective of learning how best to structure biological preserves (plate 18-10). The project was formerly known as the Minimum Critical Size of Ecosystems Project but has since been renamed the Biological Dynamics of Forest Fragments Project (BDFFP). It was initiated in 1979 with the support of INPA, the Brazil National Institute for Research in Amazonia, and the World Wildlife Fund. In 1989 the US National Museum of Natural History at the Smithsonian Institution assumed the administration of the project, and has worked in cooperation with INPA ever since. The study has had more than 25 principal investigators working with such groups as woody plants, birds, primates, bats, nonflying mammals, ants, butterflies, euglossine bees, and various beetles. As would be expected from such a comprehensive study, there have been numerous publications; general reviews can be found in Lovejoy et al. (1986); Lovejoy and Bierregaard (1990); Bierregaard et al. (1992); and Bierregaard et al. (2001a and 2001b). Researchers worked with cattle ranchers in designing the project. The ranchers were persuaded to clear forest in such a way as to create forest fragments of different sizes and distances from an undisturbed, protected 1,000 ha (2,470 ac) forest area that served as a control (analogous to the “mainland” or source). Fragments varied in area as follows: • 1 ha/2.47 ac (5 fragments) • 10 ha/24.7 ac (4 fragments) • 100 ha/247 ac (3 fragments) • 200 ha/494 ac (1 fragment) Fragments were separated by varying distances (100– 900 m/328–2,953 ft) from the 1,000 ha control forest. The researchers posed various questions: What, for instance, would be the differences in biodiversity between two 10 ha plots, one of which was 500 m

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Plate 18-7. The Crested Guan (Penelope purpurascens) is commonly hunted for meat in Central America. It is an important seed disperser for some tree species. Photo by John Kricher.

Plate 18-8. Skins for sale: two Ocelots, one red howler monkey, one Puma, and one Jaguar. They were killed by bushmeat hunters in Venezuela. Photo by John Kricher.

Plate 18-9. This photograph was taken near Alta Floresta, Brazil. The foreground shows essentially total deforestation. Fragmented forest remnants are visible in the distance. The dense haze is smoke from fires set to burn the slash. Photo by John Kricher.

Plate 18-10. Aerial image of a study fragment from the Biological Dynamics of Forest Fragments Project (BDFFP). Photo by Mark W. Moffett/Minden Pictures. Reprinted with permission from Kricher, John. Tropical Ecology. Princeton, NJ: Princeton University Press, 2011.

(1,640 ft) from the source and one of which was 100 m from it? What are the differences between a 1 ha plot and a 10 ha plot, both of which are 200 m (656 ft) from the source forest? Does the tree community change in fragmented patches, and if so, how? Are understory bird species more sensitive to differences in area than canopy species? Which species of monkeys are most sensitive to area and isolation? What species increase in density with fragmentation? Various researchers have shown that virtually all the taxonomic groups studied are sensitive in varying ways to both area and distance effects. Some species decline, others increase. For example, effects of isolation included the following:

• Isolated fragments experienced an influx of understory birds (presumably emigrating from the surrounding deforested area), but after about 200 days, the total number of birds dropped to below what it had been before the forest fragment was isolated. In other words, biodiversity plummeted. • Army-ant-following birds were negatively affected, declining and disappearing from fragments. This occurred because army ants require large areas in which to forage for prey, so they are among the species most likely excluded in small-area fragments. (A similar pattern was evident on Barro Colorado Island, Panama, after it became an island in 1913.) • Euglossine bees, which are important long-distance

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pollinators, were apparently reluctant to fly into fragments isolated by 80 m (262 ft) or more from other forest. • Primate species richness in four 10 ha fragments combined was less than the species richness in a single 100 ha fragment. • Small nonflying mammals such as various rodents increased in species richness, biomass, and abundance in 1 ha fragments compared with 10 ha fragments and continuous forest. • In areas where forest was cut but not burned, the rate of succession in the cut patch was faster, and the dense vegetation supported a larger community of butterflies than either isolated forest fragments or continuous forest. • Three species of Phyllomedusa frogs were lost from small fragments, probably because peccary wallows form the breeding pools for these small frogs, and peccaries had abandoned these areas. With the peccaries gone, the frogs could not breed. Fragmentation thus produces various ecological domino effects. Edge effects were also evident in isolated fragments. Many injured and dead trees were found along edges, and the overall turnover rate of trees was highest on edges. Rates of litter accumulation accelerated near edges. Seedling recruitment patterns varied as well. Edge effects have been a focus of study in relation to forest fragmentation and will be discussed in more detail below. Isolation is frequently problematic. Small, distantly isolated forest fragments become ecologically depauperate and function differently from normal continuous forest, sometimes resulting in what might be called ecological meltdowns. This should come as little surprise, given that so many species of Neotropical trees, for instance, are dependent on longdistance pollinators or seed dispersers or both. A tree isolated in a small fragment well over 100 m from other forest could, in effect, be made sterile for want of seed dispersers. Unfortunately, isolation due to the creation of forest fragments is occurring throughout Brazil and other tropical countries the world over. In general, fragmentation will exert its most severe impact on those species that require a large area but are reluctant to cross small gaps. There are many such species. A study directed by Gonçalo Ferraz of 55 bird species inhabiting the forest and forest fragments of the BDFFP demonstrated that bird species are sensitive to

Plate 18-11. Cecropia trees (chapter 7) are among the most aggressive colonizers along edges and normally increase in fragmented areas. Photo by Dennis Paulson.

varying degrees to patch area and to isolation. Many species were strongly affected by area, while the effect of isolation was more variable among species. For example, the Black-throated Antshrike (Frederickena viridis) is a typical forest-interior species. It is a poor colonizer that virtually never leaves the interior forest understory and is thus highly sensitive to area loss. Another species, the White-chinned Woodcreeper (Dendrocincla merula), is one of several species that typically follow army ant swarms. This behavior makes it particularly sensitive to isolation (because army ants are confined to forest) but less sensitive to area loss. However, bird species typically found in edge habitat or in canopy gaps are more tolerant of fragmentation. Because of varying ecological responses among species, it is clear that fragmentation alters community structure (plate 18-11). This makes predicting the outcome of fragmentation quite difficult. One way to mitigate the effects of fragmentation is to connect isolated fragments by corridors of uncut forest. Instead of islands of forest isolated by pasture and other hostile anthropogenic ecosystems, corridors permit the movement of species within ecosystems to which they are adapted. Fragments thus joined represent an interconnected matrix in which their respective areas are functionally additive, making for a much greater area and therefore sustaining a higher equilibrium point with regard to biodiversity. Even an uncut forest of 1,000 ha may not be sufficient to meet the ecological requirements of certain species. John Terborgh (1986) argues that national parks must have between 100,000 and 1 million ha (approx. 250,000–

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2.5 million ac) to assure that maximum biodiversity is maintained. This is particularly true for top carnivore species, each of which requires a large range.

Climate Change All ecosystems will be increasingly affected by global climate change throughout the present century. There is now an immense body of research ranging from climatology to ecology that documents the reality of ongoing and perhaps accelerating global climate change. The driver for climate change is global warming from additional greenhouse gases, in particular carbon dioxide. The terrestrial tropics have been a major source of added greenhouse gases, mostly due to deforestation, which releases carbon dioxide when forest remnants are burned to clear the brush. Ecologically speaking, climate change is the proverbial elephant in the room. Don’t think even for a minute that you can ignore it. In the tropics, climate change is currently happening fastest in areas such as flooded grasslands, deserts, and mangrove forests. The rate is more moderate for tropical and subtropical broad-leaved forests. What climate change ultimately means is that organisms within various ecosystems must essentially move to keep up with changing temperature. Distributions of organisms along various elevational zones will change, for example, as organisms from lower elevations will attempt to move higher, thus to remain within their thermal comfort zone. The ecosystems of the world are being reshuffled as organisms are increasingly affected by climate alteration, most particularly temperature change, a trend that will continue indefinitely. For species of the lowland tropics, the largest threat from climate change is biological attrition, which occurs when climate warms beyond a species’ thermal tolerances and there is no region to which to migrate (plate 18-12). Adaptation by natural selection is, of course, possible, but such a process is measured in generations and may never occur. Strong selection pressures may just as easily result in extinction as adaptation. And without question, climate change is likely to force the reassembly of ecological communities as species react individualistically to the impact of climate change. Given the intricate ecological relationships ongoing in tropical ecosystems, where biodiversity is the most essential attribute, it is

Plate 18-12. This Common Basilisk (Basiliscus basiliscus), photographed in in Belize, is resting in the shady undergrowth. The thermal world of lizards requires constant adjustment to maintain a suitable body temperature, making them susceptible to climate change. Photo by John Kricher.

impossible to predict the degree to which tropical food webs will unravel and realign. Tropical forests are huge ecosystems that are major centers of carbon cycling, which has an enormous global impact. It is not clear, given the complexities of climate change, whether tropical forests, particularly tropical moist forests, will ultimately act as carbon sinks or carbon sources. More years with excessive heat and drought are forecast with climate change. It is clear that when major events such as an El Niño/Southern Oscillation (ENSO) occur (associated with higher than usual temperatures as well as drought), many trees perish and subsequent decomposition liberates CO2 to the atmosphere; in becoming a carbon source to the atmosphere, the forest thus adds to greenhouse gas accumulation. Climate change is expected to exacerbate ENSO occurrences, and models of climate change predict much reduced rainfall in parts of the Amazon.

A Tipping Point? An unsettling scenario has been suggested by D. Nepstad and colleagues. The vast Amazon Basin to a large degree makes its own weather. The transpiration of water within the basin and its subsequent condensation into rainfall is a major factor in its hydrodynamics and ultimately its sustained productivity. With continuing logging and land clearance throughout Amazonia, forest degradation will continue. This trend toward

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deforestation will be forced by increasing global demand for meat, lumber, and biofuels (soybeans are used in biofuels). More greenhouse gases will be emitted by human activities associated with forest clearance, and accidental fires could increase, in particular, adding that much more greenhouse gas to the atmosphere and acting to reduce rainfall. The combination of forest fires, drought (expected from global climate change), and logging will combine to establish a positive feedback such that Amazonian forests may reach a tipping point beyond which forests cannot recover. At that point, large areas such as southeastern Brazil may convert from forest to savanna-type ecosystems. It has been estimated that the tipping point will occur with an added 4° C (7.2° F, within the range of some models of global warming (see Carlos Nobre, interview in Nature). It is not yet clear just how Amazonian forests are going to react to the various drivers that are now altering forest ecology.

Hydroelectric Dams: The Newest (and Worst?) Threat It is called the Belo Monte Dam and, as of this writing, it is scheduled to go into operation within the near future, though it continues to face court challenges for its potential effects on indigenous peoples. It is in the Brazilian state of Pará, and it will permanently alter the Rio Xingu, displace local populations of indigenous people, and change the ecology of the region. The Belo Monte Dam represents one of the largest of its kind in the world and was designed to provide hydrogenerated electricity, needed to support Brazil’s rapidly expanding economy. Plans for Amazon-powered hydroelectric dams such as Belo Monte have existed since the mid-1970s, and proposals for damming parts of the Amazon and its tributaries have continually generated controversy, including at the international level. Such dams require enormous capital investments. Belo Monte, for example, has been estimated to cost about $18 billion (US dollars), with another $2.5 billion for transmission lines to carry the power. The complexity of such a project is hard to understate, and its development and construction have generated many legal challenges, much debate, and international protests. But it is being built. Why should a hydroelectric dam cause such concern? The dam’s reservoir will flood 400 km2 (155 mi2) of

forest, and that represents about 0.01% of the Amazon Basin. It will initiate an ecological cascade of effects that will result in diminished biodiversity. There is also the claim that the dam will displace up to 20,000 indigenous people. For details and references on this immense undertaking, see https://en.wikipedia.org/wiki/Belo_ Monte_Dam. But there is more. Dams are also being planned for construction along the Madeira, Tapajós, and Teles Pires rivers. Many more Amazonian dam projects are now under consideration or in the planning stages. The subsequent loss of forest as well as alteration of the typical Amazonian flood cycle has the potential to significantly reduce the Amazon region’s recycling of water (chapter 2), affecting in particular its capacity to sustain its annual rainfall. When combined with climate change, the outlook is concerning, because the entire region could be subject to frequent and severe droughts. As the Amazon region becomes drier, it is likely that plant productivity will decline (chapter 5). If that occurs it will initiate a bottom-up effect that will reduce insect numbers, which in turn will reduce animals dependent on insects, and so on up the food chain. A friend who resides in Brazil has told me that Manaus, at the confluence of the Amazon and Negro rivers, has recently experienced humidity of below 20%, which is shockingly low. The effect of the dryness was evident in reduced flowering and fruiting and obvious changes in patterns of insects and birds. If such trends continue, and it appears that they will, the alteration and ecological degradation of the entire Amazonian region would seem to be inevitable. There are numerous websites devoted to the various aspects of Amazonian hydroelectric dam projects projected to occur in the near future. I have included some of them after the Further Reading section that accompanies the chapter. See also a paper by Philip M. Fearnside (2015) included in Further Reading.

Restoration and Rehabilitation of Tropical Forests: Hope for the Future? What is the outlook for tropical forests over the remainder of the 21st century? A research team led by Britaldo Soares-Filho constructed a model to compare various scenarios from the present to 2050 for the Amazon Basin. They examined eight scenarios and

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looked closely at the two extremes of the continuum. One was called the BAU model, as in “business as usual.” The other was termed the “governance” scenario, which assumes a best-case outlook involving much greater implementation of environmental legislation and more careful and sophisticated use of the land than presently occur. The BAU model predicts that by 2050 there will be a loss of 40% of Amazon forests, mostly due to expansion of agriculture. In this calculation, a current forest area of 5.3 million km2 (2.04 million mi2) would decline to 3.2 million km2 (1.2 million mi2), to about 53% of its original area, by 2050. This would include two-thirds of the forest cover in six major watersheds. An estimated total of 32 (+/−8) Pg (petagrams) of carbon would be released into the atmosphere. (A petagram is equal to 1 trillion kg, so the estimated release is 24–40 trillion kg/53–88 trillion lb of carbon.) To estimate the impact on biodiversity, the researchers used non-flying mammals as indicator taxa. Under the BAU projection, one-fourth of the 382 mammalian species would lose more than 40% of forest within their ranges. Thirty-five primate species would stand to lose 60–100% of their Amazonian ranges (100%, of course, means local extinction). Ecosystems most at risk include major watersheds, savanna, closed-canopy forest, and wetland forest, which taken together compose most of Amazonia. Most deforestation would be concentrated in the eastern Amazon. Under the governance model the projections suggest less severe impacts. The model predicts about a twothirds reduction compared with the BAU model in the numbers of threatened watersheds and mammal species, as well as far less carbon emission. The model assumes a planned expansion of protected areas (PAs) from 32% to 41% of the total forest area and that 100% of the forests within PAs are kept intact. Only 50% of the forests outside PAs would be subject to any form of deforestation. The researchers suggest that the governance model would be more likely if developed countries were willing to pay to make “frontier governance” more politically feasible. They urge consideration of sale of carbon credits as well as environmental certification (meaning close government oversight) of beef, soybean, and timber production. They also urge strong action to encourage conservation on private lands. Questions arise about the degree to which conservation goals, which typically focus on biodiversity preservation and maintenance of intact

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forests, are compatible with increasing human usage of the Amazon’s resources. As John Terborgh (2000) and many others have stated, there is a divide between what is perceived as good for people and what is good for nature. If biodiversity and ecosystem services are good for all of Earth’s people, why should a small percentage of Earth’s people (such as subsistence farmers in the tropics) bear the economic burden of biodiversity preservation? Acronyms have become popular in these discussions. REDD stands for “reducing emissions from deforestation and forest degradation.” PES stands for “payments for ecosystem services.” EEFD stands for “ecological-economic farm diversification.” The EEFD approach was investigated for local land use near Podocarpus National Park in southern Ecuador, as documented by Thomas Knoke and colleagues. More than 500 bird species and 40 mammal species have been documented to occur within the park and surrounding area. The park is located in a relatively high montane zone where there is extensive farming. This activity has led to overused, degraded, and abandoned land parcels. The high elevation of the park results in a slow process of secondary succession, exacerbating the problem of land recovery. Farmers near the park normally use pastures for only a few years and then abandon them, promoting degradation. The EEFD model examined a small, 30 ha (74 ac) farm that included 10 ha (24.7 ac) of previously degraded wastelands. The EEFD model focused on active reforestation of degraded land using a native tree species, Andean Alder (Alnus acuminata). It is worth noting that many reforestation projects do not rely on native species but instead use various eucalyptus and pine species that, because they are exotic species, have no value with regard to biodiversity. Andean Alder grows quickly and adds much nitrogen to the soil. Commercial harvesting of Andean Alder may commence as early as a decade past planting, but the model predicts peaks in revenue in years 20, 30, and 40, when various crops of Andean Alder are harvested. The model requires diversification in land use, combining limited logging with agriculture and restoration. A rotational and sustainable system is established that does not require encroachment on protected areas. The point was made that market values for agriculture and logging are uncoupled so that, for example, if the price of timber drops in a given year, the economic loss may be buffered by good crop

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production. Diversification hedges against market fluctuations. Reforestation acts as an investment against price fluctuations in agricultural products. The model has a major limitation in that natural forest, as such, has no tangible value to local farmers other than as potential “insurance” should they need to clear it. So if the reclamation of abandoned pasture fails, deforestation could result. The model suggests that economic advantages of good pasture management should normally buffer the possible need for deforestation. The conservation conundrum is that traditional monocultures (including exotic species) pay local benefits but result in biodiversity loss. Ecosystem restoration enhances biodiversity but is economically weak. And restoration is often difficult. Degradation following agriculture represents an ongoing challenge. Some areas that once supported forest have succeeded to grassland, sometimes because of invasion by exotic grass species (plate 18-13). One avenue toward forest restoration is with plantings that attempt to mimic ecological succession. Numbers of rapidly growing sun-adapted species of plants are introduced to shade out invasive weeds and grasses and reduce potential fire hazard. A variation of this approach is instead to introduce plant species more typical of mid-succession, essentially bypassing early succession. Both of these techniques require some proximity to established forest in order to encourage the fauna required by particular plant species, such as seed dispersers. One limitation of the restoration plantings method is that it is often costly. Another approach is plantation establishment, which is typically a monoculture but need not be. In the worst cases, plantations do not even consist of native plant species. Asian Teak plantations, for example, are thriving in parts of the Neotropics. Even when plantations do utilize native species, the structural and species diversity of the habitat pales in comparison with natural forest. Plantations have strong ecological limitations. They certainly are potentially profitable, but they are no solution to the biodiversity problem, quite the contrary. The closest harmonious relationship between a plantation approach and promotion of species diversity may be seen perhaps in the Inga overstory of shade-coffee plantations, as discussed in chapter 17. The use of many species rather than monocultures in plantations offers some hope toward encouraging biodiversity.

Plate 18-13. Exotic grass species have become established on what was once dry forest in Venezuela. Photo by John Kricher.

The Wright-Laurance Debate Conservation biologists have recently engaged in a debate about the future of tropical forests and biodiversity. The debate is fundamentally between William Laurance and Joseph Wright, both associated with the Smithsonian Tropical Research Institute in Panama. Many tropical ecologists have contributed to the discussion. The debate has sometimes been characterized as a “cup half full vs. cup half empty” argument. Wright and colleagues assert that demographic trends in human populations between now and mid-century will result in a net reduction in birthrate in most tropical regions and a large-scale movement from rural into urban areas. This projection, based on forecasts from the United Nations, will alleviate the trend toward increasing deforestation and forest degradation. Secondary forests will regenerate, and there will eventually be net increase in rate of regrowth of forests (similar to what has occurred in temperate nations when agriculture has been reduced and urbanization increased). Because the demographic trends cited above are already occurring, there will be little change in forest cover between now and 2030 and possibly after that time a net annual increase in forest cover throughout most of the tropics. The tropics will consist largely of secondary forests. While secondary forests are less species rich than primary forests, they will nonetheless serve well for most species. Most forest species would be generalists, but a few specialist species with rigid ecological requirements would be likely to survive as well. This is the “cup half full” view. The response by William Laurance and others is to question the assumptions underlying the Wright

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Plate 18-14. Many ecotourists, such as these people, who were part of a workshop taught by the author at the Canopy Tower and Canopy Lodge in Panama, strive to promote conservation goals and understanding with local people as their travels take them to various tropical countries. Photo by John Kricher.

Plate 18-15. In spite of the satellite dish atop the roof, it is obvious that many people of the tropics are of limited economic means. Winning them over to support conservation is essential. Photo by John Kricher.

position and assert that most deforestation has little to do with local populations and their impact on the landscape. Laurance argues that business interests supporting timber extraction, large-scale agriculture and cattle ranching, plantation growth, and other activities that have nothing directly to do with rural subsistence by local farmers will soon dominate much of the tropics. Even if large numbers of humans abandon the forests and move to the city, the industrialists will still invest in forest extraction industries and thus closed forest is unlikely to return. In short, there is no reason to assume that reduced population growth will do anything to reduce the economic pressure that results in deforestation. Another contentious issue in the debate revolves around extinction rates and loss of biodiversity. Critics of Wright’s model take issue with its extinction forecasts. Omitted from the model are such realities as effects of deforestation on centers of endemism as well as the collective effects of severe fragmentation of forests, both of which contribute to potential extinctions. Critics therefore contend that extinction rates will be considerably more severe than is forecast by Wright and colleagues. The Wright-Laurance debate is not a winner-takeall contest. There are strong elements of reality in both positions. All parties seem to agree that primary forest will continue to be degraded indefinitely and that secondary forest will come to prevail in many areas. No one doubts that extinction rates will accelerate.

A Final Word How much value should humanity place on the tropics, their exceptional biodiversity, and their ecosystem services, from which we all benefit? Ultimately the tropics and all of their varied ecosystems and biota will become what we humans make of them. The fate of the world’s biomes is ours to decide. There seems no room for doubt that biodiversity will decline during the current century, and most of the decline will occur in the global tropics. Extinction rates will rise too. It becomes a question of magnitude of loss. There is no doubt that climate is changing and that the long-term effects of that reality are not fully clear. But that said, there are numerous governmental and nongovernmental associations diligently and conscientiously working toward global conservation goals, including in the tropics. Throughout the world academicians from biology, ecology, conservation science, climatology, geology, economics, political science, anthropology, and other disciplines are focusing their research agendas on the tropics. Conservation agendas must also embrace another reality. Many millions of people are not permitted the luxury of concern over biodiversity. It is, in fact, admirable that in so many tropical areas people of limited economic means seem to be increasingly knowledgeable about and proud of the biodiversity in their nations. Most people in the tropics need to concern themselves over basic daily nutrition, their

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health, and simply having a place to live. For travelers and tourists, supporting local economies, hiring local guides, and doing what one can to support constructive conservation goals that work harmoniously with local people should be a priority (plate 18-14). There has never been a time when it has been so convenient to visit tropical destinations and experience

Plate 18-16. Sunset in the Torrid Zone. Photo by John Kricher.

the amazing ecosystems found there. If you have not done so, go and experience the Torrid Zone. Go back often. And when you do, listen and learn from the people you meet (plate 18-15). The more this type of interaction happens, the more the cup might appear half full. I hope this book has helped you to understand and embrace the remarkable Neotropics (plate 18-16).

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Appendix

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Words of Caution: Be Sure to Read This

Anyone visiting the Neotropics should be aware of the animals that have the potential to annoy you or even endanger you. I have discussed snakes in chapter 16, but it is time to talk a bit about some of the small invertebrates that you will likely meet—and likely dislike.

Mosquitoes Mosquitoes are ubiquitous in the Torrid Zone, and there are hordes of them in the temperate and polar zones as well. They have done really well since they evolved. You might be surprised by how few mosquitoes you encounter on a visit to the Neotropics. But then again, you might find a lot. Mosquito abundance depends partly on season. During the dry season there are fewer mosquitoes; during rainy season, they tend to peak. Mosquitoes are irritating and produce itchy bites, but more serious potential problems are associated with them. The mosquitoes in the genus Anopheles are well-known vectors of the various Plasmodium species (a kind of protozoan) that cause malaria. Other mosquitoes are vectors for yellow fever and dengue fever. The 2015 outbreak of Zika virus in Brazil has been linked to Aedes mosquitoes as vectors. Any visitor to the Neotropics should become familiar with the risks of mosquito-borne diseases in the region in which travel is planned (see the “Travelers’ Health” section of the Centers for Disease Control website: http://wwwnc.cdc.gov/travel) and consult with a physician about appropriate preventative medications. Some countries require certification of yellow fever vaccination as a requirement for entrance. It is advisable to use insect repellent when visiting mosquito habitats and to be diligent about avoiding mosquito bites. Dress accordingly. The more of you that is exposed, the more chance there is that a mosquito will dine on your blood. Mosquitoes are active at all times but are most active at dawn, dusk, and during the night.

Chiggers and Ticks Everyone who visits the tropics eventually will talk about chiggers, which, like ticks, are in the class Arachnida, along with spiders and scorpions. And many humans will serve, quite unwillingly, as ground zero for a host of chiggers. Chiggers are actually larval

mites of the family Trombiculidae, and they come in droves. You don’t see them on you because they are virtually microscopic. Instead, you see the little red spots they produce and you feel intense itching. Chiggers occur in forests but are far more numerous in sunny, grassy areas, including lawns. Chiggers clamber onto your body, go exploring, and tend to accumulate around areas on your person where garments have elastic bands or compress against you, such as tops of socks and underwear. They do not burrow into you but they do inject their teensy mouthparts into the skin and begin devouring it. That is what produces the itching reaction. Once that reaction begins, it continues regardless of whether you scratch or not (and you will want to scratch). There is little to do at that point but use standard anti-itch medication, such as over-thecounter Benadryl. The good news, such as it is, is that you can significantly reduce your exposure to chiggers (and ticks) by tucking your pant legs tightly into your socks (which looks geeky but sort of works) and, better yet, whack your ankles, shoes, and lower extremities with a sock containing sulfur powder, reputed to repel chiggers. Most field stations have such socks readily available and encourage their usage. And it works. Ticks act sort of like grown-up chiggers (they’re not really similar, as chiggers are mites). But they are potentially more dangerous, as there are numerous tick-borne illnesses in the world. So be careful of ticks and follow the advice to check yourself for ticks. Dry season seems to be the time ticks are most numerous. My group enjoyed a walk in a Brazilian várzea forest during dry season, but many of us emerged with dozens of tiny ticks the size of pinheads marching from ankle upward. When that occurs, get in the shower and, if possible, consider allopreening with a fellow human.

Botflies A fly is a fly is a fly. Well, not really. Some flies are best avoided. The ones that come around your peanut butter and jelly sandwich are likely harmless. But some that you encounter (even indirectly) in the field are not. Some are biting flies, related to the horse flies and deer flies that are familiar to most people. These are annoying but not dangerous. And then there is another group, the botflies, which offer another solid reason you should avoid mosquitoes.

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In what is perhaps a play on words, the botfly species Dermatobia hominis is called the Human Botfly. In spite of its name, the insect is known to infest many other mammals, including dogs, cattle, rabbits, and monkeys. When it is time to reproduce, the female botfly captures a female mosquito and, without harming it, lays her botfly eggs on it in a sticky substance she secretes. (It sounds incredible, but this actually happens.) The mosquito is released from the fly’s grip, and if it eventually lands on a human, a botfly egg hatches as the mosquito is feeding— so you get a mosquito bite and a botfly. A tiny larval botfly burrows into the skin of the human host. This is a condition called myiasis, a medical term that means “you have a maggot growing in you.” The subcutaneously growing maggot is covered with tiny spines and it has a propensity to move, creating intense irritation on the site. You soon become aware that something is amiss, and you will likely notice a raised and perhaps reddened lesion on your skin, signaling the home of the botfly larva. Local itching and occasional sharp pain continues, as the spine-infested larva moves and grows within you. If left untreated, the maggot will continue to grow, passing through several developmental stages called instars. This process requires anywhere from five to 12 weeks, a long time to play host to a maggot. But if the maggot matures, it emerges, drops from the host, and pupates in the soil. Once that happens an adult human botfly emerges and, using its superb olfactory sense, flies off to find another botfly with which to mate. I have personally experienced two bouts with human botflies and know many people who have had multiple bouts with them. So what to do? The maggots need air and breathe through two tubelike spiracles, openings at the tip of their abdomen. It is possible to deprive the maggot of air, thus killing it. Even if not killed it will come near the surface of the lesion where it can be removed with forceps or be gently and carefully squeezed out. This solution worked for me. Another solution is, believe it or not, to bribe it. Some folks claim to have taped a piece of bacon or other meat over the lesion area, and the maggot subsequently exited the human and entered the bacon. I cannot vouch for the efficacy or veracity of this approach. The most conventional approach is to have the maggot surgically removed. Or you could simply ignore the creature within you, let nature take its course, and watch as the remarkable insect eventually takes its leave of you. There you have it.

Sand Flies and Leishmaniasis Sand flies are tiny flies in the family Ceratopogonidae that are often abundant along sandy rivers and beaches in the tropics. They can be active throughout the day but are a most active at dawn, dusk, and at night. They are sometimes called no-see-ums, but there are biting midges that are also called no-see-ums. The two should not be confused. Sand fly bites, like mosquito bites, result in reddened itchy spots that are really annoying. But that is not what should concern you. Sand flies are vectors for various species of a protozoan that can produce a condition known as leishmaniasis. Weeks to months after the protozoan is introduced into the bloodstream via the bite of a sand fly, you may notice skin lesions around the face or arms and legs that appear without explanation. These lesions could be sensitive to touch, even outright painful. The lesions, caused by the leishmania protozoans take months to resolve and can reappear in the future. Worse yet, the condition may become severe, affecting the spleen and liver. Leishmaniasis is a serious medical condition that has the potential to be fatal and thus requires monitoring and treatment.

Bees and Wasps Bees and wasps abound in the Neotropics, and many are formidable stingers that become aggressive if disturbed. Wasp and bee nests are readily visible in trees (plate A1). Recall that oropendolas and other bird species often nest in proximity to a colony of wasps or bees, gaining

Plate A-1. Do not disturb. A colonial wasp nest in understory vegetation rather near the trail. Best to leave these alone. Photo by John Kricher.

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some measure of protection from the aggressive insects. The Africanized Honey Bee (also called the Killer Bee), a hybrid between the Western Honey Bee (Apis mellifera) and the African Honey Bee (A. m. scutellata), occurs in parts of South America. This is a potentially dangerous animal, especially when a swarm becomes agitated. Africanized Honey Bees were first introduced in Brazil over a half-century ago and have now spread throughout much of South and Central America and are moving north into the southwestern United States.

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The most serious problem with bees and wasps is the potential for an allergic reaction if stung. Persons prone to such allergies could face anaphylactic shock, and thus they need to take precautions, such as carrying (and knowing how to use) an epinephrine auto-injector (such as EpiPen).

***

The alarms that I have sounded here should not dissuade you from visiting the tropics. Forewarned is forearmed, so to speak.

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Further Reading Oldies but Goodies Popular, historical, and classical references: these books, all still available (at least in libraries or through the Internet), are strongly recommended as insightful, entertaining, and inspiring. Andrews, M. 1982. The Flight of the Condor. Boston: Little, Brown and Company. This well-illustrated book takes the reader from the high Andes to the rain forests. Bates, H. W. 1863. The Naturalist on the River Amazons. London: John Murray. Classic and important account of Amazonian natural history, and all of it is quite wonderful. Beebe, W. 1918. Jungle Peace. London: Witherby. ———. 1921. Edge of the Jungle. New York: Henry Holt. Both this and the previous volume contain short, delightful essays on tropical ecology written by one of the pioneers in the field. Classic. Belt, T. [1874] 1985. The Naturalist in Nicaragua. Chicago: Univ. of Chicago Press. One of the best of the classic exploratory accounts, focused entirely on Central America. Chapman, F. M. 1938. Life in an Air Castle. New York: Appleton-Century. Highly readable, offering much information, particularly on tropical birds. Chapman was an outstanding ornithologist. Darwin, C. R. 1859. On the Origin of Species. London: John Murray. Origin is available in many editions as well as online. I recommend a facsimile of the first edition annotated by James T. Costa (Cambridge, MA: Belknap Press of Harvard University Press, 2009). Though not focused on the tropics, Darwin’s stunning achievement in logic and science changed biology forever, as well as Western philosophy. It may surprise you how engaging it is and how easy to understand. ———. [1906] 1959. The Voyage of the Beagle. London: J. M. Dent and Sons. One of the best classic accounts of travel throughout South America. Many reprinted editions are available. A must-read. Forsythe, A., and K. Miyata. 1987. Tropical Nature: Life and Death in the Rain Forests of Central and South America. New York: Charles Scribner’s Sons. This book of essays captures the unique nature of the tropics and is the only book I know of that describes a botfly emerging during a Boston Red Sox game. That alone makes it well worth the price. Hilty, S. 2005. Birds of Tropical America: A Watcher’s Introduction to Behavior, Breeding, and Diversity. Austin: Univ. of Texas Press. Hilty is a first-class ornithologist and guide who has spent innumerable hours in the Neotropics watching and studying birds. And it shows. Linblad, J. 1966. Journey to Red Birds. New York: Hill and Wang. A wonderful tale of exploration on Trinidad, written by a 20th-century explorer, leading up to finding flocks of Scarlet Ibises, the “red birds” of the title.

Maslow, J. 1996. Footsteps in the Jungle: Adventures in the Scientific Exploration of the American Tropics. Chicago: Ivan R. Dee. Each chapter features a brief account of a major figure in the history of scientific exploration of Amazonia. Matthiessen, Peter. 1991. At Play in the Fields of the Lord. New York: Vintage. This is a novel set in the rain forest of Amazonia. Matthiessen is masterful at using the rain forest itself, the jungle, as a major player in this remarkable and rather dark story. Medina, J. T. (ed.). [1894] 1988. The Discovery of the Amazon. New York: Dover Publications. This is a reprint of a historic book about how the Amazon was discovered and the various controversies that have arisen since Francisco de Orellana took his most fateful voyage. Millard, C. 2006. The River of Doubt: Theodore Roosevelt’s Darkest Journey. New York: Broadway Books. Millard is a superb writer and in this best-selling book presents a spellbinding account of the difficulties Roosevelt faced on an Amazonian journey while converying his determination as an explorer. As you read, consider that ecotours now routinely visit the Amazon tributary known as the River of Doubt. Morrison, T. 1974. Land above the Clouds. London: Andre Deutsch LTD. This is one of the earlier and best accounts of the natural history of the Andes. O’Hanlon, R. 1990. In Trouble Again: A Journey between Orinoco and the Amazon. New York: Vintage. This book has attained classic status. O’Hanlon is never daunted and always amusing. Plotkin, M. J. 1993. Tales of a Shaman’s Apprentice: An Ethnobotanist Searches for New Medicines in the Amazon Rain Forest. New York: Viking. This was a best seller that is now a classic in modern writing about the Neotropics. Plotkin describes his experiences as he discovers firsthand the effects of hallucinogenic drugs concocted by shamans of indigenous tribes in Amazonia. Very engaging and informative. Roosevelt, T. [1914] 2009. Through the Brazilian Wilderness. New York: CreateSpace. This is a reprinted edition of Roosevelt’s classic account of his voyage down the River of Doubt. It reads in stark contrast to the drama of C. Millard’s recent book The River of Doubt. Roosevelt takes the tone of the objective explorer, describing what he sees and seemingly trivializing his difficulties. Royte, E. 2001. The Tapir’s Morning Bath. Boston, MA: Houghton Mifflin Company. A journalist attempts to and succeeds in gaining the trust of dedicated researchers at Barro Colorado Island and follows them into the forest to observe their often challenging work. Entertaining and informative and should be read by all would-be tropical researchers. Shoumatoff, A. 1978. The Rivers Amazon. San Francisco, CA: Sierra Club Books. This entertaining and detailed book follows the author’s journey from the mouth of the Amazon to deep within its various tributaries. He keeps it interesting.

further reading

Simpson, G. G. 1980. Splendid Isolation: The Curious History of South American Mammals. New Haven, CT: Yale Univ. Press. Somewhat dated but still engaging, this book, written by one of the most influential evolutionary biologists of the 20th-century, provides a readable account of the unique mammalian fauna that once dominated much of South America. Skutch, A. F. 1977. A Bird Watcher’s Adventures in Tropical America. Austin: Univ. of Texas Press. Skutch was a legendary ornithologist, a real pioneer of avian natural history studies. This book, which focuses on Skutch’s early years in the tropics, is more than just accounts of birds as evidenced in the chapter “Through Peruvian Amazon by Gunboat.” Wallace, A. R. 1895. Natural Selection and Tropical Nature. London: Macmillan. This delightful book contains vivid descriptions, in glorious Victorian prose, of Alfred Russel Wallace’s experiences in Amazonia. Waterton, C. [1825] 1983. Wanderings in South America. London: Century Publishing. A very engaging narrative by an eccentric but perceptive explorer. One of the best of the early travel narratives. Worth, C. B. 1967. A Naturalist in Trinidad. Philadelphia, PA: J. B. Lippincott Company. The title is explanatory and the writing is wonderful. The book is enhanced by the artistic mastery of Don R. Eckelberry.

General References: The Essentials Here I supply a list of book-length references, some of which are nontechnical, some of which are research-focused. Taken together they provide added understanding of Neotropical natural history, ecology, and research. Bridgewater, S. 2012. A Natural History of Belize: Inside the Maya Forest. Austin: Univ. of Texas Press. Bush, M. B., J. R. Flenley, and W. D. Gosling (eds.). 2011. Tropical Rainforest Responses to Climatic Change. Chichester, UK: Praxis Publishing and Springer. Chazdon, R. L., and T. C. Witmore. Foundations of Tropical Forest Biology: Classic Papers with Commentaries. Chicago: Univ. of Chicago Press. Fleming, T. H., and W. J. Kress. 2013. The Ornaments of Life: Coevolution and Conservation in the Tropics. Chicago: Univ. of Chicago Press. Gentry, A. H. (ed.). 1990. Four Neotropical Rainforests. New Haven, CT: Yale Univ. Press. Goulding, M. 1990. Amazon: The Flooded Forest. London: Guild Publishing. Goulding, M., N. J. H. Smith, and D. J. Mahar. 1996. Floods of Fortune: Ecology and Economy along the Amazon. New York: Columbia Univ. Press.

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Huston, M. A. Biological Diversity: The Coexistence of Species on Changing Landscapes. Cambridge, UK: Cambridge Univ. Press. Janzen, D. H. (ed.). 1983. Costa Rican Natural History. Chicago: Univ. of Chicago Press. Kricher, J. 2011. Tropical Ecology. Princeton, NJ: Princeton Univ. Press. Leigh, E. G. Jr. 1999. Tropical Forest Ecology: A View from Barro Colorado Island. Oxford, UK: Oxford Univ. Press. Leigh, E. G. Jr., A. S. Rand, and D. M. Windsor. 1982. The Ecology of a Tropical Forest: Seasonal Rhythms and Longterm Changes. Wash., DC: Smithsonian Inst. Press. Lovejoy, T. E., and L. Hannah (eds.). 2005. Climate Change and Biodiversity. New Haven, CT: Yale Univ. Press. McDade, L. A., K. S. Bawa, H. A. Hespendeide, and G. S. Hartshorn (eds.). 1994. La Selva: Ecology and Natural History of a Neotropical Rain Forest. Chicago: Univ. of Chicago Press. Nadkarni, N. M., and N. T. Wheelwright (eds.). 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. New York: Oxford Univ. Press. Primack, R., and R. Corlett. 2005. Tropical Rain Forests: An Ecological and Biogeographical Comparison. Malden, MA: Blackwell. Reddish, P. 1996. Spirit of the Jaguar: The Natural History and Ancient Civilization of the Caribbean and Central America. London: BBC Books. Sodhi, N. S., C. H. Sekercioglu, J. Barlow, and S. K. Robinson. 2011. Conservation of Tropical Birds. Oxford, UK: WileyBlackwell. Wilson, E. O. 1992. The Diversity of Life. New York: W. W. Norton & Co.

Chapter-by-Chapter Further Reading Lists Studies discussed in the chapter are in boldface. Others are included as additional reading suggestions.

Chapter 1: Further Reading Achard, F., H. D. Eva, H.-J. Stibig, P. Mayaux, J. Gallego, T. Richards, and J.-P. Malingreau. 2002. Determination of deforestation rates of the world’s humid tropical forests. Science 297: 999–1002. Chazdon, R.L., and T. C. Whitmore (eds.). 2002. Foundations of Tropical Biology: Classic Papers with Commentaries. Chicago: Univ. of Chicago Press. Clark, D. A. 2004. Tropical forest and global warming: slowing it down or speeding it up? Front. Ecol. Environ. 2: 73–80. Jackson, S. T. 2009. Alexander von Humboldt and the general physics of the Earth. Science 324: 596–597.

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further reading

Leigh, E. G. Jr. 1999. Tropical Forest Ecology: A View from Barro Colorado Island. New York: Oxford Univ. Press. Meyer-Abich, Adolf. 1969. Alexander von Humboldt. Bonn: Inter Nationes. Parker, G. G., A. P. Smith, and K. P. Hogan. 1992. Access to the upper forest canopy with a large tower crane. BioScience 42: 664–670. Primack, R., and R. Corlett. 2005. Tropical Rain Forests: An Ecological and Biogeographic Comparison. Malden, MA: Blackwell. Wright, S. J., and H. C. Muller-Landau. 2006b. The uncertain future of forest species. Biotropica 38: 443–445.

Chapter 2: Further Reading Bates, H. W. 1863. The Naturalist on the River Amazons. London: John Murray. Canby, T. Y. 1984. El Niño’s ill wind. Nat. Geog. 162: 143–183. Foster, R. B. 1982. Famine on Barro Colorado Island. In The Ecology of a Tropical Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press. Garwood, N. C. 1982. Seasonal rhythm of seed germination in a semi-deciduous tropical forest. In The Ecology of a Tropical Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press. Gillis, J. 2012a. A climate scientist battles time and mortality. The New York Times, Jul. 3, 2012. ———. 2012b. In sign of warming, 1,600 years of ice in Andes melted in 25 years. New York Times, Apr. 4, 2013. Graham, N. E., and W. B. White. 1988. The El Niño cycle: A natural oscillator of the Pacific Ocean–atmosphere system. Science 240: 1293–1301. Holdridge, L. R. 1947. Determination of world plant formations from simple climatic data. Science 105: 367– 368. Junk, W. J., and K. Furch. 1985. The physical and chemical properties of Amazonian waters and their relationships with the biota. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Salati, E., and P. B. Vose. 1984. Amazon Basin: A system in equilibrium. Science 225: 129–138. Suplee, C. 1999. El Niño–La Niña: Nature’s vicious cycle. Nat. Geog. 195: 72–95. Thompson, L. G. 2000. Ice core evidence for climate change in the tropics: Implications for our future. Quaternary Sci. Rev. 19: 19–35.

Chapter 3: Further Reading Clark, D. A. 1994. Plant demography. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press.

Darwin C. 1862. On the Various Contrivances by which British and Foreign Orchids Are Fertilised by Insects, and on the Good Effects of Intercrossing. London: John Murray. ———. [1906] 1959. The Voyage of the Beagle. London: J. M. Dent and Sons. Dressler R. L. 1981. The Orchids: Natural History and Classification. Cambridge, MA: Harvard Univ. Press. Gentry, A. H. 1991. The distribution and evolution of climbing plants. In The Biology of Vines, F. E. Putz and H. A. Mooney (eds.). Cambridge, UK: Cambridge Univ. Press. ———. 1993. A Field Guide to the Families and Genera of Woody Plants of Northwest South America. Wash., DC: Conservation International. Halle, F., R. A. A. Oldman, and P. B. Tomlinson. 1978. Tropical Trees and Forests: An Architectural Analysis. Berlin: Springer-Verlag. Hartshorn, G. S. 1980. Neotropical forest dynamics. In Tropical Succession, supplement to Biotropica 12: 23–30. ———. 1983. Plants. In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Henderson, A., G. Galeano, and R. Bernal. 1995. Field Guide to the Palms of the Americas. Princeton, NJ: Princeton Univ. Press. Horn, H. S. 1971. The Adaptive Geometry of Trees. Princeton, NJ: Princeton Univ. Press. King, D. A. 1990. Allometry of saplings and understorey trees in a Panamanian forest. Functional Ecology 5: 485–492. ———. 1996. The allometry and life history of tropical trees. Journal of Tropical Ecology 12: 25–44. Lotschert, W., and G. Beese. 1981. Collins Guide to Tropical Plants. London: Collins. Perry, D. R. 1978. Factors influencing arboreal epiphytic phytosociology in Central America. Biotropica 10: 235–237. Perry, R. D. 1984. The canopy of the tropical rain forest. Sci. Amer. 251: 138–147. Phillips, O. 1991. The ethnobotany and economic botany of tropical vines. In The Biology of Vines, F. E. Putz and H. A. Mooney (eds.). Cambridge, UK: Cambridge Univ. Press. Pires, J. M., and G. T. Prance. 1985. The vegetation types of the Brazilian Amazon. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Poorter, L., F. Bongers, F. J. Sterck, and H. Woll. 2003. Architecture of 53 rain forest tree species differing in adult stature and shade tolerance. Ecology 84: 602–608. Putz, F. E. 1984. The natural history of lianas on Barro Colorado Island, Panama. Ecology 65: 1713–1724. Putz, F. E., and H. A. Mooney (eds.). 1991. The Biology of Vines. Cambridge, UK: Cambridge Univ. Press. Schnitzer, S. A., and F. Bongers. 2002. The ecology of lianas and their role in forests. Trends in Ecol. Evol. 17: 223–230. Schnitzer, S. A., J. W. Dalling, and W. P. Carson. 2000. Lianas and gap-phased regeneration in a tropical forest. Jour. Ecol. 88: 655–666. Smith, N., S. A. Mori, A. Henderson, D. Wm. Stevenson,

further reading

and S. V. Heald. 2004. Flowering Plants of the Neotropics. Princeton, NJ: Princeton Univ. Press. Utley, J. F., and K. Burt-Utley. 1983. Bromeliads (Pina silvestre, pinuelas, chiras, wild pineapple). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Wallace, Alfred Russel (1853). Palm Trees of the Amazon and Their Uses. London: John Van Voorst. Walterm, K. S. 1983. Orchidaceae (orquideas, orchids). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Zahl, P. A. 1975. Hidden worlds in the heart of a plant. Nat. Geog. 147: 388–397. Zuchowski, W. 2007. Tropical Plants of Costa Rica: A Guide to Native and Exotic Flora. Ithaca, NY: Comstock.

{~?~DES: Note, there is no further reading list for chapter 4.}

Chapter 5: Further Reading Baker, D. F. 2007. Reassessing carbon sinks. Science 316: 1708– 1709. Brown, S., and A. E. Lugo. 1982. The storage and production of organic matter in tropical forests and their role in the global carbon cycle. Biotropica 14: 161–187. Bunker, D. E., F. DeClerck, J. C. Bradford, R. K. Colwell, I. Perfecto, O. L. Phillips, M. Sankaran, and S. Naeem. 2005. Species loss and aboveground carbon storage in a tropical forest. Science 310: 1029–1031. Chambers, J. Q., N. Higuchi, E. S. Tribuzy, and S. E. Trumbore. 2001. Carbon sink for a century. Nature 410: 429. Clark, D. A. 2004. Tropical forests and global warming: slowing it down or speeding it up? Front. Ecol. Environ. 2: 73–80. Clark, D. A., S. Brown, D. W. Kicklighter, J. Q. Chambers, J. R. Thomplinson, J. Ni, and E. A. Holland. 2001. Net primary productivity in tropical forests: An evaluation and synthesis of existing field data. Ecol. Appl. 11: 371–384. Clark, D. A., and D. B. Clark. 1994. Climate induced annual variation in canopy tree growth in a Costa Rican tropical rainforest. Jour. Ecol. 82: 865–872. Clark, D. L. 2002. Are tropical forests an important carbon sink? Reanalysis of the long-term plot data. Ecol. Appl. 12: 3–7. Cochrane, M. A. 2003. Fire science for rainforests. Nature 421: 913–919. Grace, J., and Y. Malhi. 2002. Carbon dioxide goes with the flow. Nature 416: 594–595. Graham, E. A., S. S. Mulkey, S. J. Wright, K. Kitajima, and N. G. Phillips. 2003. Cloud cover limits productivity in a rainforest tree during tropical rainy seasons. Proc. Nat. Acad. Sci. USA 100: 572–576.

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Holloway, M. 1993. Sustaining the Amazon. Sci. Amer. 269: 90–99. Hughen, K. A., T. I. Eglinton, L. Xu, and M. Makou. 2004. Abrupt tropical vegetation response to rapid climate changes. Science 304: 1955–1959. Malhi, Y., and J. Grace. 2000. Tropical forests and atmospheric carbon dioxide. Trends in Ecol. Evol. 15: 332–337. Mayorga, E., A. K. Aufdenkampe, C. A. Masiello, A. V. Krusche, J. I. Hedges, P. D. Quay, J. E. Richey, and T. A. Brown. 2005. Young organic matter as a source of carbon dioxide outgassing from Amazonian rivers. Nature 436: 538–541. Mellilo, J. M., A. D. McGuire, D. W. Kicklighter, B. I. Moore, C. J. Vorosmarty, and A. L. Schloss. 1993. Global climate change and terrestrial net primary production. Nature 363: 234–240. Moran, E. F., E. Brondizio, P. Mausel, and Y. Wu. 1994. Integrating Amazonian vegetation, land-use, and satellite data. Bioscience 44: 329–338. Page, S. E., F. Siegert, J. O. Rieley, H-D. V. Boehm, A. Jaya, and S. Limin. 2002. The amount of carbon released from peat and forest fires in Indonesia during 1997. Nature 420: 61–65. Phillips, O. L., and 10 other authors. 1998. Changes in the carbon balance of tropical forests: evidence from longterm plots. Science 282: 439–442. Phillips, O. L., and 18 other authors. 2002. Increasing dominance of large lianas in Amazonian forests. Nature 418: 770–774. Phillips, O. L., and 66 other authors. 2009. Drought sensitivity of the Amazon rainforest. Science 323: 1344–1347. Raich, J. W., E. B. Rastetter, J. M. Melillo, D. W. Kicklighter, P. A. Steudler, B. J. Peterson, A. L. Grace, B. Moore III, and C. J. Vorosmarty. 1991. Potential net primary productivity in South America: Application of a global model. Ecol. Appl. 1: 399–429. 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. Richey, J. E., J. M. Melack, A. K. Aufdenkampe, V. M. Ballester, and L. L. Hess. 2002. Outgassing from Amazonian rivers and wetlands as a large tropical source of atmospheric CO2. Nature 416: 617–620. Saleska, S. R., and 17 other authors. 2003. Carbon in Amazon forests: Unexpected seasonal fluxes and disturbance-induced losses. Science 302: 1554–1557. Saleska, S. R., K. Didan, A. R. Huete, and H. R. da Rocha. 2007. Amazon forests green-up during 2005 drought. Science 318: 612. Schiermeier, Q. 2006. Methane finding baffles scientists. Nature 439: 128. Schuur, E. A. G. 2003. Productivity and global climate revisited: The sensitivity of tropical forest growth to precipitation. Ecology 84: 1165–1170.

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further reading

Vitousek, P. M., P. R. Ehrlich, A. E. Ehrlich, and P. A. Matson. 1986. Human appropriation of the products of photosynthesis. Bioscience 36: 368–373. Vogt, K. A., C. C. Grier, and D. J. Vogt. 1986. Production, turnover, and nutrient dynamics of above- and belowground detritus of world forests. In Adv. Ecol. Res. 15: 303–377. A. Macfadyen and E. D. Ford (eds.). London: Academic Press.

Chapter 6: Further Reading Abe, T., and M. Higashi. 2001. Isoptera. In Encyclopedia of Biodiversity, vol. 3., Levin, S. A. (ed.). San Diego, CA: Academic Press. Ackerman, I. L., R. Constantino, H. G. Gauch Jr., J. Lehmann, S. J. Riha, and E. C. M. Fernandes. 2009. Termite (Insecta: Isoptera) species composition in a primary rain forest and agroforests in Central America. Biotropica 41: 226–233. Bates, H. W. 1862. Contributions of an insect fauna of the Amazon Valley. Trans. Linn. Soc. London 23: 495–566. Bentley, B. L., and E. J. Carpenter. 1984. Direct transfer of newly fixed nitrogen from free-living epiphyllus microorganisms to their host plant. Oecologia 63: 52–56. Brightsmith, D. J., J. Taylor, and T. D. Phillips. 2008. The roles of soil characteristics and toxin adsorption in avian geophagy. Biotropica 40: 766–774. Cleveland, C. C., S. C. Reed, and A. R. Townsend. 2006. Nutrient regulation of organic matter decomposition in a tropical rain forest. Ecology 87: 492–503. Cleveland, C. C., and 10 other authors. 1999. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Global Biogeochemical Cycles 13: 623–645. Davidson, E. A., and 11 other authors. 2007. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447: 995–998. Eichhorn, M. P., S. G. Compton, and S. E. Hartley. 2008. The influence of soil type on rain forest insect herbivore communities. Biotropica 40: 707–713. Falkowski, P. G., T. Fenchel, and E. F. Delong. 2008. The microbial engines that drive Earth’s biogeochemical cycles. Science 320: 1034–1039. Feeley, K. J., and J. W. Terborgh. 2005. The effects of herbivore density on soil nutrients and tree growth in tropical forest fragments. Ecology 86: 116–124. Forman, R. T. T. 1975. Canopy lichens with blue-green algae: A nitrogen source in a Colombian rain forest. Ecology 56: 1176–1184. Golly, F. B. 1975. Mineral Cycling in a Tropical Moist Forest Ecosystem. Athens: Univ. of Georgia Press. ———. 1983. Nutrient cycling and nutrient conservation. In Tropical Rain Forest Ecosystems: Structure and Function, F. B. Golley (ed.). Amsterdam: Elsevier Scientific. Herrera, R. 1985. Nutrient cycling in Amazonian forests. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press.

Irion, G. 1978. Soil infertility in the Amazonian rain forest. Naturwissenschaften 65: 515–519. Janos, D. P. 1980. Mycorrhizae influence tropical succession. Biotropica 12 (suppl.): 56–64. ———. 1983. Tropical mycorrhizae, nutrient cycles, and plant growth. In Tropical Rain Forest: Ecology and Management, S. L. Sutton, T. C. Whitmore, and A. C. Chadwick (eds.). Oxford, UK: Blackwell Scientific. Janos, D. P., C. T. Sahley, and L. H. Emmons. 1995. Rodent dispersal of vesicular-arbuscular mycorrhizal fungi in Amazonian Peru. Ecology 76: 1852–1858. Jordan, C. F. 1982. Amazon rain forests. Amer. Sci. 70: 394– 401. ———. 1985a. Nutrient Cycling in Tropical Forest Ecosystems. New York: J. Wiley. ———. 1985b. Soils of the Amazon rainforest. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Jordan, C. F., F. Golley, J. D. Hall, and J. Hall. 1979. Nutrient scavenging of rainfall by the canopy of an Amazonian rain forest. Biotropica 12: 61–66. Jordan, C. F., and R. Herrera. 1981. Tropical rain forests: Are nutrients really critical? Amer. Nat. 117: 167–180. Jordan, C. F., and J. R. Kline. 1972. Mineral cycling: Some basic concepts and their application in a tropical rain forest. Ann. Rev. Ecol. Syst. 3: 33–50. Lal, R. 1990. Tropical soils: Distribution, properties and management. In Tropical Resources: Ecology and Development, J. I. Furtado, W. B. Morgan, J. R. Pfafflin, and K. Ruddle (eds.). London: Harwood Assoc. Langley, J. A., and B. A. Hungate. 2003. Mycorrhizal controls on belowground litter quality. Ecology 84: 2302–2312. Lavelle, P., E. Blanchart, A. Martin, S. Martin, A. Spain, F. Toutain, I. Barois, and R. Schaefer. 1993. A hierarchical model for decomposition in terrestrial ecosystems: Application to soils of the humid tropics. Biotropica 25: 130–150. Lodge, D. J. 1996. Microorganisms. In The Food Web of a Tropical Rain Forest. D. P. Reagan and R. B. Waide (eds.). Chicago: Univ. of Chicago Press. Lubin, Y. D. 1983. Nasutitermes (Comején, hormiga blanca, nasute termite, arboreal termite). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Lubin, Y. D., and G. G. Montgomery. 1981. Defenses of Nasutitermes termites (Isoptera, Termitidae) against Tamandua anteaters (Edentata, Myrmecophagidae). Biotropica 13: 66–76. Lucas, Y., F. J. Luizao, A. Chauvel, J. Rouiller, and D. Nahon. 1993. The relation between biological activity of the rain forest and mineral composition of soils. Science 260: 521– 523. Martinelli, L. A., M. C. Piccolo, A. R. Townsend, P. M. Vitousek, E. Cuevas, W. McDowell, G. P. Robertson, O.

further reading

C. Santos, and K. Treseder. 1999. Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry 46: 45–65. Martius, C. 1994. Diversity and ecology of termites in Amazonian forests. Pedobiologia 38: 407–428. McGuire, K. L. 2007. Common ectomycorrhizal networks may maintain monodominance in a tropical rain forest. Ecology 88: 567–574. Meyer, J. L. 1990. A blackwater perspective on riverine ecosystem. Bioscience 40: 643–651. Nicholaides, J. J. III, D. E. Bandy, P. A. Sanchez, J. R. Benites, J. H. Villachica, A. J. Coutu, and C. S. Valverde. 1985. Agricultural alternatives for the Amazon Basin. Bioscience 35: 279–285. Parker, G. G. 1994. Soil fertility, nutrient acquisition, and nutrient cycling. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. Powell, L. L., T. U. Powell, G. V. N. Powell, and D. J. Brightsmith. 2009. Parrots take it with a grain of salt: Available sodium content may drive collpa (clay lick) selection in Southeastern Peru. Biotropica 41: 279–282. Prestwich, G. D., and B. L. Bentley. 1981. Nitrogen fixation by intact colonies of the termite Nasutitermes corniger. Oecologia 49: 249–251. Prestwich, G. D., B. L. Bentley, and E. J. Carpenter. 1980. Nitrogen sources for Neotropical nasute termites: Fixation and selective foraging. Oecologia 46: 397–401. Reed, S. C., C. C. Cleveland, and A. R. Townsend. 2007. Controls over leaf litter and soil nitrogen fixation in two lowland tropical rain forests. Biotropica 39: 585–592. ———. 2008. Tree species control rates of free-living nitrogen fixation in a tropical rain forest. Ecology 89: 2924–2934. St. John, T. V. 1985. Mycorrhizae. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Salati, E., and P. B. Vose. 1984. Amazon Basin: A system in equilibrium. Science 225: 129–138. Salick, J., R. Herrera, and C. F. Jordan. 1983 Termitaria: Nutrient patchiness in nutrient-deficient rain forests. Biotropica 15: 1–7. Sanford, R. L. Jr. 1987. Apogeotropic roots in an Amazon rain forest. Science 235: 1062–1064. Sollins, P., F. M. Sancho, R. Mata, and R. J. Sanford Jr. 1994. Soils and soil processes. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. Townsend, A. R., C. C. Cleveland, G. P. Asner, and M. M. C. Bustamante. 2007. Controls over foliar N:P ratios in tropical rain forests. Ecology 88: 107–118. Uhl, C., D. Nepstad, R. Buschbacher, K. Clark, B. Kauffman, and S. Subler. 1990. Studies of ecosystem response to natural and anthropogenic disturbances provide

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guidelines for designing sustainable land-use systems in Amazonia. In Alternatives to Deforestation: Steps toward Sustainable Use of the Amazon Rain Forest, A. B. Anderson (ed.). New York: Columbia Univ. Press. Vitousek, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65: 285–298. Vitousek, P. M., and R. L. Sanford. 1986. Nutrient cycling in moist tropical forest. Ann. Rev. Ecol. Syst. 17: 137–167. Whitfield, J. 2007. Underground networking. Nature 449: 136– 138. Wilson, E. O. 1971. The Insect Societies. Cambridge, MA: Belknap Press of Harvard Univ. Zimmerman, P. R., J. P. Greenberg, S. O. Wandiga, and P. J. Crutzen. 1982. Termites: A potentially large source of atmospheric methane, carbon dioxide, and molecular hydrogen. Science 218: 563–65.

Chapter 7: Further Reading Alvarez-Clare, S., and K. Kitajima. 2009. Susceptibility of tree seedlings to biotic and abiotic hazards in the understory of a moist tropical forest in Panama. Biotropica 41: 47–56. Baker, H. G. 1983. Ceiba pentandra (Ceyba, ceiba, Kapok tree). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Bazzaz, F. A., and S. T. A. Pickett. 1980. Physiological ecology of tropical succession: A comparative review. Ann. Rev. Ecol. Syst. 11: 287–310. Brokaw, N. V. L. 1982. Treefalls: Frequency, timing, and consequences. In The Ecology of a Tropical Rain Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press. ———. 1985. Gap-phase regeneration in a tropical forest. Ecology 66: 682–687. ———. 1987. Gap-phase regeneration of three pioneer tree species in a tropical forest. Jour. Ecol. 75: 9–19. Bush, M. B., and P. A. Colinvaux. 1994. Tropical forest disturbance: Paleoecological records from Darién, Panama. Ecology 75: 1761–1768. Chazdon, R. L., A. R. Brenes, and B. V. Alvarado. 2005. Effects of climate and stand age on annual tree dynamics in tropical second-growth rain forests. Ecology 86: 1808–1815. Chazdon, R. L., and N. Fetcher. 1984. Photosynthetic light environments in a lowland tropical rain forest in Costa Rica. Jour. Ecol. 72: 553–564. Clark, D. A. 1994. Plant demography. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. Clark, D. A., and D. B. Clark. 1987. Population ecology and microhabitat distribution of Dipteryx panamensis, a Neotropical rain forest emergent tree. Biotropica 19: 236–244. ———. 1992. Life history diversity of canopy and emergent trees in a Neotropical rain forest. Ecol. Monog. 62: 315–344.

398

further reading

Cochrane, M. A., A. Alencar, M. D. Schulze, C. M. Souza Jr., D. C. Nepstad, P. Lefebvre, and E. A. Davidson. 1999. Positive feedbacks in the fire dynamic of close canopy tropical forests. Science 284: 1832–1835. Condit, R., S. P. Hubbell, and R. B. Foster. 1992. Short-term dynamics of a Neotropical forest. Bioscience 42: 822–828. ———. 1993. Identifying fast-growing native trees from the neotropics using data from a large, permanent census plot. Forest Ecology and Management 62: 123–143. Dalling, J. W., and T. A. Brown. 2009. Long-term persistence of pioneer seeds in tropical rain forest soil seed banks. Amer. Nat. 173: 531–535. Dalling, J. W., and R. C. John. 2008. Recruitment limitation and coexistence of pioneer species. In Tropical Forest Community Ecology, W. P. Carson and S. A. Schnitzer (eds.). New York: Blackwell Science. Dalling, J. W., M. D. Swaine, and N. C. Garwood. 1998. Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79: 564–578. D’Antonio, C. M., and P. M. Vitousek. 1992. Biological invasions by exotic grasses, the grass/fire cycle, and global change. Ann. Rev. Ecol. Syst. 23: 63–87. Denslow, J. S., and G. S. Hartshorn. 1994. Tree-fall gap environments and forest dynamic processes. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. Diamond, J. 2004. Collapse: How Societies Choose to Fail or Succeed. New York: Viking. Engelbrecht, B. 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. Ewel, J. 1980. Tropical succession: Manifold routes to maturity. In Tropical Succession, supplement to Biotropica 12: 2–7. ———. 1983. Succession. In Tropical Rain Forest Ecosystems: Structure and Function, F. B. Golley (ed.). Amsterdam: Elsevier Scientific. Ewel, J., S. Gliessman, M. Amador, F. Benedict, C. Berish, R. Bermudez, B. Brown, A. Martinez, R. Miranda, and N. Price. 1982. Leaf area, light transmission, roots and leaf damage in nine tropical plant communities. AgroEcosystems 7: 305–326. Fichtler, E., D. A. Clark, and M. Worbes. 2003. Age and longterm growth of trees in an old-growth tropical rain forest, based on analyses of tree rings and 14C. Biotropica 35: 306– 317. Finegan, B. 1996. Pattern and process in neotropical secondary rain forests: The first 100 years of succession. Trends in Ecol. Evol. 11: 119–124. Flannery, K. V. (ed.). 1982. Maya Subsistence. New York: Academic Press.

Fleming, T. H. 1983. Piper (Candela, candelillos, piper). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. ———. 1985a. Coexistence of five sympatric Piper (Piperaceae) species in a tropical dry forest. Ecology 66: 688–700. ———. 1985b. A day in the life of a Piper-eating bat. Nat. Hist. 94: 52–59. Foster, R. B. 1990. Long-term change in the successional forest community of the Rio Manu floodplain. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Gentry, A. H., and J. Terborgh. 1990. Composition and dynamics of the Cocha Cashu “mature” floodplain forest. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Gilbert, G. S., K. E. Harms, D. N. Hamill, and S. P. Hubbell. 2001. Effects of seedling size, El Niño drought, seedling density, and distance to nearest conspecific adult on 6-year survival of Ocotea whitei seedlings in Panamá. Oecologia 127: 509–516. Greenberg, R. 1987a. Development of dead leaf foraging in a tropical migrant warbler. Ecology 68: 130–141. ———. 1987b. Seasonal foraging specialization in the Wormeating Warbler. Condor 89: 158–168. Hammond, N. 1982. Ancient Maya Civilization. New Brunswick, NJ: Rutgers Univ. Press. Hart, R. D. 1980. A natural ecosystem analog approach to the design of a successional crop system for tropical forest environments. In Tropical Succession, supplement to Biotropica 12: 73–82. Hartshorn, G. S. 1978. Tree falls and tropical forest dynamics. In Tropical Trees as Living Systems, P. B. Tomlinson and M. H. Zimmerman (eds.). London: Cambridge Univ. Press. Hooper, E. R., P. Legendre, and R. Condit. 2004. Factors affecting community composition of forest regeneration in deforested, abandoned land in Panama. Ecology 85: 3313–3326. Holthuijzen, A. M. A., and J. H. A. Boerboom. 1982. The Cecropia seedbank in the Surinam lowland rain forest. Biotropica 14: 62–67. Hubbell, S. P., and R. B. Foster. 1986a. Canopy gaps and the dynamics of a Neotropical forest. In Plant Ecology, M. J. Crawley (ed.). Oxford, UK: Blackwell Scientific. ———. 1986b. Commonness and rarity in a Neotropical forest: Implications for tropical tree conservation. In Conservation Biology: The Science of Scarcity and Diversity, M. E. Soule (ed.). Sunderland, MA: Sinauer. ———. 1986c. Biology, chance, and history and the structure of tropical rain forest tree communities. In Community Ecology, J. Diamond and T. J. Case (eds.). New York: Harper & Row. ———. 1990. Structure, dynamics, and equilibrium status of old-growth forest on Barro Colorado Island. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press.

further reading

———. 1992. Short-term dynamics of a Neotropical forest: Why ecological research matters to tropical conservation and management. Oikos 63: 48–61. Hubbell, S. P., R. B. Foster, S. T. O’Brien, K. E. Harms, R. Condit, B. Wechsler, S. J. Wright, and S. Loo de Lao. 1999. Light-gap disturbances, recruitment limitation, and tree diversity in a Neotropical forest. Science 283: 554–557. Janzen, D. H. 1969. Allelopathy by myrmecophytes: The ant Azteca as an allelopathic agent of Cecropia. Ecology 50: 147–153. ———. 1983. Mimosa pigra (Zarza, dormilona). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Klinge, H., W. A. Rodrigues, E. Brunig, and E. J. Fittkau. 1975. Biomass and structure in a central Amazonian rain forest. In Tropical Ecological Systems: Trends in Terrestrial and Aquatic Research, F. B. Golley and E. Medina (eds.). New York: Springer-Verlag. Knight, D. H. 1975. A phytosociological analysis of species rich tropical forest on Barro Colorado Island, Panama. Ecol. Monog. 45: 259–284. LaFay, H. 1975. The Maya: Children of time. Nat. Geog. 148: 728–767. Leigh, E. G. Jr. 1975. Structure and climate in tropical rain forest. Ann. Rev. Ecol. Syst. 6: 67–86. ———. 1999. Tropical Forest Ecology: A View from Barro Colorado Island. Oxford, UK: Oxford Univ. Press. 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. Jour. Ecol. 73: 915–924. McDade, L. A., K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn, eds. 1994. La Selva: Ecology and Natural History of a Neotropical Rain Forest. Chicago: Univ. of Chicago Press. Metcalf, C. J., C. C. Horvitz, S. Tuljapurkar, and D. A. Clark. 2009. A time to grow and a time to die: a new way to analyze the dynamics of size, light, age, and death of tropical trees. Ecology 90: 2766–2778. Nations, J. D. 1988. The Lacandon Maya. In People of the Tropical Rain Forest, J. S. Denslow and C. Padoch (eds.). Berkeley: Univ. of Calif. Press. Opler, P. A., H. G. Baker, and G. W. Frankie. 1980. Plant reproductive characteristics during secondary succession in Neotropical lowland forest ecosystems. In Tropical Succession, supplement to Biotropica 12: 40–46. Phillips, O. L., R. V. Martinez, A. M. Mendoza, T. R. Baker, and P. N. Vargas. 2005. Large lianas as hyperdynamic elements of the tropical forest canopy. Ecology 86: 1250– 1258. Pickett, S. T. A., and M. L. Cademasso. 2005. Vegetation dynamics. In Vegetation Ecology, pp. 238–264, E.v.d. Marrel (ed.). Malden, MA: Blackwell.

399

Putz, F. E. 1984. The natural history of lianas on Barro Colorado Island, Panama. Ecology 65: 1713–1724. Rankin-De-Merona, J. M., R. W. Hutchings, and T. E. Lovejoy. 1990. Tree mortality and recruitment over a five-year period in undisturbed upland rain forest in the Central Amazon. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Sanford, R. L. Jr., J. Saldarriaga, K. Clark, C. Uhl, and R. Herrera. 1985. Amazonian rain-forest fires. Science 227: 53–55. Stiles, F. G. 1983. Heliconia latispatha (Platanillo, wild plantain). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Titiz, B., and R. L. Sanford Jr. 2007. Soil charcoal in oldgrowth rain forests from sea level to the continental divide. Biotropica 39: 673–682. Uhl, C. 1988. Restoration of degraded lands in the Amazon Basin. In Biodiversity, E. O. Wilson (ed.). Wash., DC: National Academy Press. Uhl, C., R. Buschbacher, and E. A. S. Serrao. 1988c. Abandoned pastures in eastern Amazonia. I. Patterns of plant succession. Jour. Ecol. 76: 663–681. Uhl, C., K. Clark, N. Dezzeo, and P. Maquirino. 1988a. Vegetation dynamics in Amazonian treefall gaps. Ecology 69: 751–763. Uhl, C., J. B. Kauffman, and D. L. Cummings. 1988b. Fire in the Venezuelan Amazon 2: Environmental conditions necessary for forest fires in the evergreen rain forest of Venezuela. Oikos 53: 176–184. Uhl, C., D. Nepstad, R. Buschbacher, K. Clark, B. Kauffman, and S. Subler. 1990. Studies of ecosystem response to natural and anthropogenic disturbances provide guidelines for designing sustainable land-use systems in Amazonia. In Alternatives to Deforestation: Steps toward Sustainable Use of the Amazon Rain Forest, A. B. Anderson (ed.). New York: Columbia Univ. Press. Van Breugel, M., F. Bongers, and M. Martinez-Ramos. 2007. Species dynamics during early secondary forest succession: Mortality and species turnover. Biotropica 35: 610–619. Williams-Linera, G. 1983. Biomass and nutrient content in two successional stages of tropical wet forest in Uxpanapa, Mexico. Biotropica 15: 275–284. Wright, S. J., H. C. Muller-Landau, R. Condit, and S. P. Hubbell. 2003. Gap-dependent recruitment, realized vital rates, and size distributions of tropical trees. Ecology 84: 3174–3185.

Chapter 8: Further Reading Antonelli, A., J. A. A. Nylander, C. Persson, and I. Sanmartin. 2009. Tracing the impact of the Andean uplift on Neotropical plant evolution. Proc. Nat. Acad. Sci. USA 106 (no. 24): 9749–9754. doi: 10.1073/pnas.0811421106. Belt, T. [1874] 1985. The Naturalist in Nicaragua. Chicago: Univ. of Chicago Press.

400

further reading

Bush, M. B., and P. E. de Oliveira. 2006. The rise and fall of the refugial hypothesis of Amazonian speciation: A paleoecological perspective. Biota Neotropica 6. Online version. Colinvaux, P. A. 1989a. Ice-age Amazon revisited. Nature 340: 188–189. ———. 1989b. The past and future Amazon. Sci. Amer. 259: 102–108. Cracraft, J. 1983. Cladistic analysis and vicariance biogeography. Amer. Sci. 71: 273–281. Cracraft. J. 1985. Historical biogeography and patterns of differentiation within the South American avifauna: Centers of endemism. Ornithological Monographs, no. 36. P. A. Buckley et al. (eds.). Wash., DC: American Ornithologists’ Union. Craig, C. L. 1989. Alternative foraging modes of orb weaving spiders. Biotropica 21: 257–264. Eisner, T., and S. Nowicki. 1983. Spider web protection through visual advertisement: Role of the stabilimentum. Science 219: 185–186. Emmons, L. H. 1997. Neotropical Rainforest Mammals: A Field Guide, 2nd ed. Chicago: Univ. of Chicago Press. Fenton, M. B. 1992. Wounds and the origin of blood-feeding in bats. Biol. Jour. Linn. Soc. 47: 161. Fitzpatrick, J. W. 1980a. Foraging behavior of Neotropical tyrant flycatchers. Condor 82: 43–57. ———. 1980b. Wintering of North American tyrant flycatchers in the Neotropics. In Migrant Birds in the Neotropics: Ecology, Behavior, Distribution, and Conservation, A. Keast and E. S. Morton (eds.). Wash., DC: Smithsonian Inst. Press. ———. 1985. Foraging behavior and adaptive radiation in the Tyrannidae. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, E. S. Morton, R. S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union. Garzione, C. N., G. D. Hoke, J. C. Libarkin, S. Withers, B. MacFadden, J. Eiler, P. Ghosh, and A. Mulch. 2008. Rise of the Andes. Science 320: 1304–1308. Haffer, J. 1969. Speciation in Amazonian forest birds. Science 165: 131–137. ———. 1974. Avian Speciation in Tropical South America. Publication no. 14, R. A. Paynter (ed.). Cambridge, MA: Nuttall Ornithological Club. ———. 1985. Avian zoogeography of the Neotropical lowlands. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, E. S. Morton, R. S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union. ———. 1993. Time’s cycle and time’s arrow in the history of Amazonia. Biogeographica 69: 15–45. Haffer, J., and J. W. Fitzpatrick. 1985. Geographic variation in some Amazonian forest birds. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, E. S. Morton, R. S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union.

Haffer, J., and G. T. Prance. 2001. Climatic forcing of evolution in Amazonia during the Cenozoic: On the refuge theory of biotic differentiation Amazoniana 16 579–607. Heyer, W. R., and L. R. Maxon. 1982. Distributions, relationships, and zoogeography of lowland frogs: The Leptodactylus complex in South America, with special reference to Amazonia. In Biological Diversification in the Tropics, G. T. Prance (ed.). New York: Columbia Univ. Press. Irion, G. 1989. Quaternary geological history of the Amazon Lowlands. In Tropical Forests, L. B. Holm-Nielson, I. Neilson, and H. Basley (eds.). London: Academic Press. Janzen, D. H., and P. S. Martin. 1982. Neotropical anachronisms: The fruits the gomphotheres ate. Science 215: 19–27. Janzen, D. H., and D. E. Wilson. 1983. Mammals. In Costa Rican Natural History, D. E. Janzen (ed.). Chicago: Univ. of Chicago Press. Kinzey, W. G. 1982. Distribution of primates and forest refuges. In Biological Diversification in the Tropics, G. T. Prance (ed.). New York: Columbia Univ. Press. Lomolino, M. V., F. S. Dov, and J. H. Brown (eds.). 2004. Foundations of Biogeography: Classic Papers with Commentaries. Chicago: Univ. of Chicago Press. Marshall, L. G. 1988. Land mammals and the Great American Interchange. Amer. Sci. 76: 380–388. Marshall, L. G., S. D. Webb, J. J. Sepkowski, and D. M. Raup. 1982. Mammalian evolution and the great American interchange. Science 215: 1351–1357. Maxson, L. R., and W. R. Heyer. 1982. Leptodactylid frogs and the Brasilian Shield: An old and continuing adaptive relationship. Biotropica 14: 10–14. Mayle, F. E. 2004. Assessment of the Neotropical dry forest refugia hypothesis in the light of palaeoecological data and vegetation model simulations. Jour. Quaternary Science 19: 713–717. Miller, B. W. 2001a. Beyond mist-nets: What the rest of the bats can tell us about forests. The consequences of timber exploitation for bat communities in tropical America. in Cutting Edge: Conserving Wildlife in Logged Tropical Forests, pp. 154–156, A. Grajal and J. G. Robinson (eds.). New York: Columbia Univ. Press. ———. 2015. Annotated key to known bats of Belize with current taxonomic changes, pp. 1–39. http://www. academia.edu/15037926/. Miller, B. W., and C. M. Miller. 1999. Results of a survey of bats of the Cockscomb Basin Wildlife Sanctuary, pp. 1–16. WCS Technical Report Series: Tropical Forest and Reserve Planning Project, Belize. Pearson, D. L. 1977. A pantropical comparison of bird community structure on six lowland forest sites. Condor 79: 232–244. ———. 1982. Historical factors and bird species richness. In Biological Diversification in the Tropics, G. T. Prance (ed.). New York: Columbia Univ. Press.

further reading

Prance, G. T. (ed.). 1982a. Biological Diversification in the Tropics. New York: Columbia Univ. Press. ———. 1982b. Forest refuges: Evidence from woody angiosperms. In Biological Diversification in the Tropics, G. T. Prance (ed.). New York: Columbia Univ. Press. ———. 1985. The changing forests. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Price, T. 2008. Speciation in Birds. Greenwood Village, CO: Roberts and Company. Ridgely, R. S., and P. J. Greenfield. 2001. The Birds of Ecuador: Status, Distribution, and Taxonomy. Ithaca, NY: Cornell Univ. Press. Ridgely, R. S., and G. Tudor. 2009. Field Guide to the Songbirds of South America: The Passerines. Austin: Univ. of Texas Press. Schoener, T. W. 1971. Large-billed insectivorous birds: A precipitous diversity gradient. Condor 73: 154–161. Simpson, B. B., and J. Haffer. 1978. Speciation patterns in the Amazonian forest biota. Ann. Rev. Ecol. Syst. 9: 497–518. Simpson, G. G. 1980. Splendid Isolation: The Curious History of South American Mammals. New Haven, CT: Yale Univ. Press. Traylor, M. A. Jr., 1985. Species limits in the Ochthoeca diadema species-group (Tyrannidae). Ornithological Monographs, no. 36, P. A. Buckley et al. (eds.). Wash., DC: American Ornithologists’ Union. Waterton, C. [1825]. 1983. Wanderings in South America. London: Century Publishing. Webb, S. D. 1978. A history of savanna vertebrates in the new world. Part II: South America and the Great Interchange. Ann. Rev. Ecol. Syst. 9: 393–426. Wilf, P., N. R. Cúneo, K. R. Johnson, J. F. Hicks, S. L. Wing, and J. D. Obradovich JD. 2003. High plant diversity in Eocene South America: Evidence from Patagonia. Science 300: 122–125. Willis, K. J., and R. J. Whittaker. 2000. Paleoecology: the refugial debate. Science 25: 1406–1407.

Chapter 9: Further Reading Askins, R. A. 1983. Foraging ecology of temperate-zone and tropical woodpeckers. Ecology 64: 945–956. Bermingham, E., and C. Dick. 2001. The Inga—newcomer or museum antiquity? Science 293: 2214–2215. Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 199: 1302–1310. Connell, J. H., and E. Orias. 1964. The ecological regulation of species diversity. Amer. Nat. 98: 399–414. Connell, J. H., and R. O. Slatyer. 1977. Mechanisms of succession in natural communities and their role in community stability and organization. Amer. Nat. 111: 1119–1144. DeVries, P. J. 1987. The Butterflies of Costa Rica and Their Natural History, vol. 1. Princeton, NJ: Princeton Univ. Press.

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———. 1994. Patterns of butterfly diversity and promising topics in natural history and ecology. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. ———. 1997. The Butterflies of Costa Rica and Their Natural History, vol. 2. Princeton, NJ: Princeton Univ. Press. Dial, R., and J. Roughgarden. 1995. Experimental removal of insectivores from rain forest canopy: Direct and indirect effects. Ecology 76: 1821–1834. Dobzhansky, T. 1950. Evolution in the tropics. Amer. Sci. 38: 209–221. Duellman, W. E. 1992. Reproductive strategies of frogs. Sci. Amer. 267: 80–87. Emmons, L. H. 1984. Geographic variation in densities and diversities of non-flying mammals in Amazonia. Biotropica 16: 210–222. ———. 1987. Comparative feeding ecology of felids in a Neotropical rainforest. Behav. Ecol. Sociobiol. 20: 271–283. Erwin, T. L. 1982. Tropical forests: Their richness in Coleoptera and other arthropod species. Colleopterists’ Bull. 36: 74–75. ———. 1983. Beetles and other insects of tropical forest canopies at Manaus, Brazil, sampled by insecticidal fogging. In Tropical Rain Forest: Ecology and Management, S. L. Sutton, T. C. Whitmore, and A. C. Chadwick (eds.). London: Blackwell. ———. 1988. The tropical forest canopy: The heart of biotic diversity. In Biodiversity, E. O. Wilson (ed.). Wash., DC: National Academy Press. Fine, P. A. V., I. Mesones, and P. D. Coley. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305: 663–667. Foster, R. B., and S. P. Hubbell. 1990. The floristic composition of the Barro Colorado Island forest. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Foster, R. B., and 17 other authors. 1994. The TambopataCandamo Reserved Zone of Southeastern Peru: A Biological Assessment. Wash., DC: Conservation International. Gentry, A. H. 1982. Neotropical floristic diversity: Phytogeographical connections between Central and South America, Pleistocene climatic fluctuations, or an accident of Andean orogeny? Annals of the Missouri Botanical Garden 69: 557–593. ———. 1986. Species richness and floristic composition of Choco region plant communities. Caldasia 15: 71–91. ———. 1988. Tree species richness of upper Amazon forests. Proc. Nat. Acad. Sci. USA 85: 156–159. ———. 1990. Floristic similarities and differences between southern Central America and upper and central Amazonia. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press.

402

further reading

Hammel, B. 1990. The distribution of diversity among families, genera, and habit types in the La Selva flora. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Hartshorn, G. S., and B. E. Hammel. 1994. Vegetation types and floristic patterns. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. Hawkins, B. A., E. R. Porter, and J. A. F. Diniz-Filho. 2003a. Productivity and history as predictors of the latitudinal diversity gradient of terrestrial birds. Ecology 84: 1608– 1623. Hawkins, B. A., and 11 other authors. 2003b. Energy, water, and broad-scale geographic patterns of species richness. Ecology 84: 3105–3117. Heithaus, E. R., T. H. Fleming, and P. A. Opler. 1975. Foraging patterns and resource utilization in seven species of bats in a seasonal tropical forest. Ecology 56: 841–854. Hilty, S. L., and W. L. Brown. 1986. A Guide to the Birds of Colombia. Princeton, NJ: Princeton Univ. Press. Hubbell, S. P., and R. B. Foster. 1986a. Canopy gaps and the dynamics of a Neotropical forest. In Plant Ecology, M. J. Crawley (ed.). Oxford, UK: Blackwell Scientific. ———. 1986b. Commonness and rarity in a Neotropical forest: Implications for tropical tree conservation. In Conservation Biology: The Science of Scarcity and Diversity, M. E. Soule (ed.). Sunderland, MA: Sinauer. Huston, M. A. 1994. Biological Diversity: The Coexistence of Species on Changing Landscapes. Cambridge, UK: Cambridge Univ. Press. Jablonski, D., K. Roy, and J. W. Valentine. 2006. Out of the tropics: Evolutionary dynamics of the latitudinal diversity gradient. Science 314: 102–106. Janzen, D. H. 1976. Why are there so many species of insects? Proc. XV Int. Cong. Ent.: 84–94. Jaramillo, C., M. J. Rueda, and G. Mora. 2006. Cenozoic plant diversity in the Neotropics. Science 311: 1893–1896. Karr, J. R. 1975. Production, energy pathways and community diversity in forest birds. In Tropical Ecological Systems: Trends in Terrestrial and Aquatic Research, F. B. Golley and E. Medina (eds.). New York: Springer-Verlag. ———. 1976. Within- and between-habitat avian diversity in African and Neotropical lowland habitats. Ecol. Monog. 46: 457–481. Knight, D. H. 1975. A phytosociological analysis of species rich tropical forest on Barro Colorado Island, Panama. Ecol. Monog. 45: 259–284. Lovejoy, T. E. 1974. Bird diversity and abundance in Amazon forest communities. Living Bird 13: 127–192. MacArthur, R. H. 1965. Patterns of species diversity. Biol. Rev. 40: 510–533.

May, R. M. 1988. How many species are there on Earth? Science 241: 1441–1449. Novotny, V., P. Drozd, S. E. Miller, M. Kulfan, M. Janda, Y. Basset, and G. D. Weiblen. 2006. Why are there so many species of herbivorous insects in tropical rainforests? Sciencexpress, July 2006. Pianka, E. R. 1966. Latitudinal gradients in species diversity: A review of concepts. Amer. Nat. 100: 33–45. Prance, G. T. 1990. The floristic composition of the forests of Central Amazonian Brazil. In Four Neotropical Rainforests, pp. 112–140, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Prance, G. T., W. A. Rodrigues, and M. F. da Silva. 1976. Inventario florestal de um hectare de mata de terra firme, km 30 da Estrada Manaus-Itacoatiara. Acta Amazonica 6: 9–35. Remsen, J. V. 1990. Community Ecology of Neotropical Kingfishers. Univ. Calif. Pub. 124: 1–116. Remsen, J. V. Jr., and T. A. Parker III. 1983. Contribution of river-created habitats to bird species richness in Amazonia. Biotropica 15: 223–231. Richardson, J. E., R. T. Pennington, T. D. Pennington, and P. R. Hollingworth. 2001. Rapid diversification of a speciesrich genus of Neotropical rain forest trees. Science 293: 2242–2245. Robinson, S. K., and J. Terborgh. 1990. Bird communities of the Cocha Cashu Biological Station in Amazonian Peru. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Schoener, T. W. 1971. Large-billed insectivorous birds, a precipitous diversity gradient. Condor 73: 154–161. Sherry, T. W. 1984. Comparative dietary ecology of sympatric, insectivorous Neotropical flycatchers. Ecol. Monog. 54: 313–338. Skutch, A. F. 1981. New Studies of Tropical American Birds. Publication no. 19. Cambridge, MA: Nuttall Ornithological Club. Snow, D. W. 1966. A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos 15: 274–281. Stutchbury, B. J. M., and E. S. Morton. 2001. Behavioral Ecology of Tropical Birds. New York: Academic Press. Terborgh, J. 1992. Maintenance of diversity in tropical forests. Biotropica 24: 283–292. Terborgh, J., S. K. Robinson, T. A. Parker III, C. A. Munn, and N. Pierpont. 1990. Structure and organization of an Amazonian forest bird community. Ecol. Monog. 60: 213– 238. Terborgh, J., and J. S. Weske. 1975. The role of competition in the distribution of Andean birds. Ecology 56: 562– 576. Tramer, E. J. 1974. On latitudinal gradients in avian diversity. Condor 76: 123–130. Wallace, A. R. 1895. Natural Selection and Tropical Nature. London: Macmillan.

further reading

Weir, J. T., and D. Schluter. 2007. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315: 1574–1576. Wilson, E. O. 1987. The arboreal ant fauna of Peruvian Amazon forests: A first assessment. Biotropica 19: 245– 251.

Chapter 10: Further Reading Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton Univ. Press. Bascompte, J., P. Jordano, and J. M. Olesen. 2006. Asymmetric coevolutionary networks facilitiate biodiversity maintenance. Science 312: 431–433. Beehler, B. M., and M. S. Foster. 1988. Hotshots, hotspots, and female preference in the organization of lek mating sytems. Amer. Nat. 131: 203–219. Bradbury, J. W. 1981. The evolution of leks. In Natural Selection and Social Behavior: Research and New Theory, R. D. Alexander and D. W. Tinkle (eds.). New York: Chicago Press. Bradbury, J. W., and R. Gibson. 1983. Leks and mate choice. In Mate Choice, P. Bateson (ed.). Cambridge, UK: Cambridge Univ. Press. Chapela, I. H., S. A. Rehner, T. R. Schultz, and U. G. Mueller. 1994. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266: 1691– 1694. Clark, C. J., J. R. Poulsen, B. M. Bolker, E. F. Connor, and V. T. Parker. 2005. Comparative seed shadows of bird-, monkey-, and wind-dispersed trees. Ecology 86: 2684– 2694. Clark, J. S., M. Silman, R. Kern, E. Macklin, and J. HilleRisLambers. 1999. Seed dispersal near and far: Patterns across temperate and tropical forests. Ecology 80: 1475–1494. Feinsinger, P. 1978. Ecological interactions between plants and hummingbirds in a successional tropical community. Ecol. Monog. 48: 269–287. ———. 1983. Variable nectar secretion in a Heliconia species pollinated by hermit hummingbirds. Biotropica 15: 48–52. Fleming, T. H., R. Breitwisch, and G. H. Whitesides. 1987. Patterns of tropical vertebrate frugivore diversity. Ann. Rev. Ecol. Syst. 18: 91–109. Fleming, T. H., and W. J. Kress. 2013. The Ornaments of Life: Coevolution and Conservation in the Tropics. Chicago: Univ. of Chicago Press. Futuyma, D. J., and M. Slatkin (eds.). 1983. Coevolution. Sunderland, MA: Sinauer. Galetti, M., C. I. Donatti, M. A. Pizo, and H. C. Giacomini. 2008. Big fish are the best: Seed dispersal of Bactris glaucescens by the pacu fish (Piaractus mesopotamicus) in the Pantanal, Brazil. Biotropica 40: 386–389.

403

Goulding, M. 1980. The Fishes and the Forest: Explorations in Amazonian Natural History. Berkeley: Univ. of Calif. Press. ———. 1985. Forest fishes of the Amazon. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. ———. 1990. The Flooded Forest. London: Guild Publishing. ———. 1993. Flooded forests of the Amazon. Sci. Amer. 266: 114–120. Heithaus, E. R., P. A. Opler, and H. B. Baker. 1974. Bat activity and pollination of Bauhinia pauletia: Plantpollinator coevolution. Ecology 55: 412–419. Herz, H., W. Byeschlag, and B. Hölldobler. 2007. Herbivory rate of leaf-cutting ants in a tropical moist forest in Panama. Biotropica 39: 482–488. Hoglund, J., and R. V. Alatalo. 1995. Leks. Princeton, NJ: Princeton Univ. Press. Hölldobler, B., and E. O. Wilson. 1990. The Ants. Cambridge, MA: Belknap Press of Harvard Univ. Howe, H. F. 1977. Bird activity and seed dispersal of a tropical wet forest tree. Ecology 58: 539–550. ———. 1982. Fruit production and animal activity in two tropical trees. In The Ecology of a Tropical Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press. Howe, H. F., and G. F Estabrook. 1977. On intraspecific competition for avian dispersers in tropical trees. Amer. Nat. 111: 817–832. Howell, D. J. 1974. Bats and pollen: Physiological aspects of the syndrome of chiropterophily. Comparative Biochemistry and Physiology Part A: Physiology 48: 263–276. ———. 1976. Plant-loving bats, bat-loving plants. Nat. Hist. 85: 52–59. Hubbell, S. P., J. J. Howard, and D. F. Wiemer. 1984. Chemical leaf repellency to an attine ant: Seasonal distribution among potential host plant species. Ecology 65: 1067–1076. Hubbell, S. P., D. F. Wiemer, and A. Adejare. 1983. An antifungal terpenoid defends a Neotropical tree (Hymenaea) against attack by fungus-growing ants (Atta). Oecologia 60: 321–327. Janzen, D. H. 1970. Herbivores and the number of tree species in tropical forests. Amer. Nat. 104: 501–528. ———. 1971. Euglossine bees as long-distance pollinators of tropical plants. Science 171: 203–206. ———. 1975. Ecology of Plants in the Tropics. London: Edward Arnold. ———. 1980b. When is it coevolution? Evolution 34: 611–612. Johnsgard, P. A. 1994. Arena Birds: Sexual Selection and Behavior. Wash., DC: Smithsonian Inst. Press. Jordano, P. 1983. Fig-seed predation and dispersal by birds. Biotropica 15: 38–41. ———. 2000. Fruits and frugivory. In Seeds: The Ecology of Regeneration in Natural Plant Communities, M. Fenner (ed.). Wallingford, UK: Commonwealth Agricultural Bureau International.

404

further reading

Kubitzki, K. 1985. The dispersal of forest plants. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Leck, C. F. 1969. Observations of birds exploiting a Central American fruit tree. Wilson Bull. 81: 264–269. Levey, D. J. 1985. Two ways to be a fruit-eating bird: Mashers versus gulpers. Abstracts of the 103d American Ornithologists’ Union Meeting. Levey, D. J., T. C. Moermond, and J. S. Denslow. 1984. Fruit choice in Neotropical birds: The effect of distance between fruits on preference patterns. Ecology 65: 844–850. ———. 1994. Frugivory: An overview. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. Levey, D. J., and F. G. Stiles. 1994. Birds: Ecology, behavior, and taxonomic affinities. In La Selva: Ecology and Natural History of a Neotropical Rain Forest, L. A. McDade, K. S. Bawa, H. A. Hespenheide, and G. S. Hartshorn (eds.). Chicago: Univ. of Chicago Press. Lill, A. 1974. The evolution of clutch size and male “chauvinism” in the white-bearded manakin. Living Bird 13: 211–231. Little, A. E. F., and C. R. Currie. 2008. Black yeast symbionts compromise the efficiency of antibiotic defenses in fungusgrowing ants. Ecology 89: 1216–1222. Lowe-McConnell, R. H. 1987. Ecological Studies in Tropical Fish Communities. Cambridge, UK: Cambridge Univ. Press. Lucas, C. M. 2008. Within flood season variation in fruit consumption and seed dispersal by two characin fishes of the Amazon. Biotropica 40: 581–589. Martin, M. M. 1970. The biochemical basis of the fungusattine ant symbiosis. Science 169: 16–20. Moermond, T. C., and J. S. Denslow. 1985. Neotropical avian frugivores: Patterns of behavior, morphology, and nutrition, with consequences for fruit selection. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, E. S. Morton, R. S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union. Morton, E. S. 1973. On the evolutionary advantages and disadvantages of fruit eating in tropical birds. Amer. Nat. 107: 8–22. Mueller, U. G., S. A. Rehner, and T. R. Schultz. 1998. The evolution of agriculture in ants. Science 281: 2034–2038. Poulsen, M., and J. J. Boomsma. 2005. Mutualistic fungi control crop diversity in fungus-growing ants. Science 307: 741–744. Prance, G. T. 1985b. The pollination of Amazonian plants. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Prum, R. O. 1994. Phylogenetic analysis of the evolution of alternative social behavior in the manakins (Aves: Pipridae). Evolution 48: 1657–1675. Prum, R. O., and W. E. Lanyon. 1989. Monophyly and phylogeny of the Schiffornis group (Tyrannoidea). Condor 91: 444–461.

Roca, R. L. 1994. Oilbirds of Venezuela: Ecology and Conservation. Publication no. 24, R. A. Paynter Jr. (ed.). Cambridge, MA: Nuttall Ornithological Club. Rockwood, L. L. 1976. Plant selection and foraging patterns in two species of leaf-cutting ants (Atta). Ecology 57: 48–61. Sick, H. 1967. Courtship behavior in manakins (Pipridae): A review. Living Bird 6: 5–22. Silman, M. R., J. W. Terborgh, and R. A. Kiltie. 2003. Population regulation of a dominant rain forest tree by a major seed predator. Ecology 84: 431–438. Snow, B. K., and D. W. Snow. 1979. The ochre-bellied flycatcher and the evolution of lek behavior. Condor 81: 286–292. Snow, D. W. 1961 The natural history of the oilbird, Steatornis caripensis, in Trinidad, W. I. Part 1. General behavior and breeding habits. Zoologica 46: 27–48. ———. 1962. The natural history of the oilbird, Steatornis caripensis, in Trinidad, W. I. Part 2. Population, breeding ecology, food. Zoologica 47: 199–221. ———. 1971. Observations on the purple-throated fruitcrow in Guyana. Living Bird 10: 5–18. ———. 1976. The Web of Adaptation. Ithaca, NY: Cornell Univ. Press. ———. 1982. The Cotingas: Bellbirds, Umbrellabirds, and Other Species. Ithaca, NY: Cornell Univ. Press. Thompson, J. N. 2005. The Geographical Mosaic of Coevolution. Chicago: Univ. of Chicago Press. ———. 2006. Mutualistic webs of species. Science 312: 372–373. Trail, P. W. 1985a. Courtship disruption modifies mate choice in a lek-breeding bird. Science 227: 778–779. ———. 1985b. A lek’s icon: The courtship display of a Guianan cock-of-the-rock. Amer. Birds 39: 235–240. Weber, N. A. 1972. The attines: The fungus-culturing ants. Amer. Sci. 60: 448–456. Wheelwright, N. T. 1985. Fruit size, gape width, and the diets of fruit-eating birds. Ecology 66: 808–818. 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: 173–192. Wheelwright, N. T., and G. H. Orions. 1982. Seed dispersal by animals: Constraints with pollen dispersal, problems of terminology, and constraints on coevolution. Amer. Nat. 119: 402–413. Willis, E. O., and Y. Oniki. 1978. Birds and army ants. Ann. Rev. Ecol. Syst. 9: 243–263. Willson, S. K. 2004. Obligate army-ant-following birds: A study of ecology, spatial movement patterns, and behavior in Amazonian Peru. Ornithological Monographs 55: 1–67. Wrege, P. H., M. Wikelski, J. T. Mandel, T. Rassweiler, and I. D. Couzin. 2005. Antbirds parasitize foraging army ants. Ecology 86: 555–559. Youngsteadt, E. 2008. All that makes fungus gardens grow. Science 320: 1006–1007.

further reading

Chapter 11: Further Reading Bates, H. W. 1862. Contributions of an insect fauna of the Amazon Valley. Trans. Linn. Soc. London 23: 495–566. Beatty, C. D., K. Beirinckx, and T. N. Sherratt. 2004. The evolution of Müllerian mimicry in multispecies communities. Nature 431: 63–67. Benson, W. W. 1972. Natural selection for Müllerian mimicry in Heliconius erato in Costa Rica. Science 176: 936–939. ———. 1985. Amazon ant plants. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Benson, W. W., K. S. Brown, and L. E. Gilbert. 1976. Coevolution of plants and herbivores: Passion flower butterflies. Evolution 29: 659–680. Bentley, B. L. 1976. Plants bearing extrafloral nectaries and the associated ant community: Interhabitat differences in the reduction of herbivore damage. Ecology 54: 815–820. ———. 1977. Extrafloral nectaries and protection by pugnacious bodyguards. Ann. Rev. Ecol. Syst. 8: 407–427. Brower, L. P. 1969. Ecological chemistry. Sci. Amer. 220: 22– 29. Brower, L. P., and J. V. Z. Brower. 1964. Birds, butterflies, and plant poisons: A study in ecological chemistry. Zoologica 49: 137–159. Brower, L. P., J. V. Z. Brower, and C. T. Collins. 1963. Experimental studies of mimicry: 7. Relative palatability of Müllerian mimicry among Neotropical butterflies of the subfamily Heliconiinae. Zoologica 48: 65–84. Brown, B. J., and J. L. Ewel. 1987. Herbivory in complex and simple tropical successional ecosystems. Ecology 68: 108– 116. Chamberlain, S. A., and J. N. Holland. 2009. Quantitative synthesis of context dependency in ant-plant protectionist mutualisms. Ecology 90: 2384–2392. Coley, P. D. 1982. Rates of herbivory on different tropical trees. In The Ecology of a Tropical Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press. ———. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol. Monog. 53: 209–233. ———. 1984. Plasticity, costs, and anti-herbivore effects of tannins in a Neotropical tree, Cecropia peltata (Moraceae). Bull. Ecol. Soc. Amer. 65: 229. Coley, P. D., J. P. Bryant, and F. S. Chapin III. 1985. Resource availability and plant antiherbivore defense. Science 230: 895–899. Coley, P. D., and 14 other authors. 2003. Using ecological criteria to design plant collection strategies for drug discovery. Front. Ecol. Environ. 8: 421–428. Coley, P. D., and 12 other authors. 2005. Divergent defense strategies of young leaves in two species of Inga. Ecology 86: 2633–2643.

405

Crump, M. L. 1983. Dendrobates granuliferus and Dendrobates pumilio. In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Daly, J. W., H. M. Garraffo, and T. F. Spande. 1993. Amphibian alkaloids. In The Alkaloids, vol. 43, G. A. Cordell (ed.). San Diego, CA: Academic Press. DeVries, P. J. 1987. The Butterflies of Costa Rica and Their Natural History. Princeton, NJ: Princeton Univ. Press. ———. 1990. Enhancement of symbiosis between butterfly caterpillars and ants by vibrational communication. Science 248: 1104–1106. ———. 1992. Singing caterpillars, ants and symbiosis. Sci. Amer. 267: 76–82. DeVries, P. J., and I. Baker. 1989. Butterfly exploitation of an ant-plant mutualism: Adding insult to herbivory. Jour. New York Entomological Soc. 97: 332–340. DuVal, E. H., H. W. Greene, and K. L. Manno. 2006. Laughing falcon (Herpetotheres cachinnans) predation on coral snakes (Micrurus nigrocinctus). Biotropica 38: 566–568. Dyer, L. A., and 12 other authors. 2007. Host specificity of Lepidoptera in tropical and temperate forests. Nature 448: 696–699. Ehrlich, P. R., and P. H. Raven. 1964. Butterflies and plants: A study in coevolution. Evolution 18: 586–608. ———. 1967. Butterflies and plants. Sci. Amer. 216: 104–113. Futuyma, D. J. 1983. Evolutionary interaction among herbivorous insects and plants. In Coevolution, D. J. Futuyma and M. Slatkin (eds.). Sunderland, MA: Sinauer. Gilbert, G. S., and C. O. Webb. 2007. Phylogenetic signal in plant pathogen-host range. Proc. Nat. Acad. Sci. 104: 4979–4983. Gilbert, L. E. 1971. Butterfly-plant coevolution: Has Passiflora adenopoda won the selectional race with Heliconiine butterflies? Science 172: 585–586. ———. 1975 Ecological consequences of a coevolved mutualism between butterflies and plants. In Coevolution of Animals and Plants, L. E. Gilbert and P. H. Raven (eds.). Austin: Univ. of Texas Press. ———. 1982. The coevolution of a butterfly and a vine. Sci. Amer. 247: 110–121. ———. 1983. Coevolution and mimicry. In Coevolution, D. J. Futuyma and M. Slatkin (eds.). Sunderland, MA: Sinauer. Glander, K. E. 1977. Poison in a monkey’s Garden of Eden. Nat. Hist. 86: 35–41. ———. 1982. The impact of plant secondary compounds on primate foraging behavior. American Journal of Physical Anthropology 25: 1–18. Hansen, M. 1983b. Yuca (Yuca, cassava). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Harborne, J. B. 1982. Introduction to Ecological Biochemistry. New York: Academic Press. Heisler, I. L. 1983. Nyssodesmus python (Milpes, large forestfloor millipede). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press.

406

further reading

Heliconius Genome Consortium. 2012. Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94-98. Helson, J. E., T. L. Capson, T. Johns, A. Aiello, and D. M. Windsor. 2009. Ecological and evolutionary bioprospecting: Using aposematic insects as guides to rainforest plants active against disease. Front. Ecol. Environ. 7: 130–134. Herz, H., W. Beyschlag, and B. Hölldobler. 2007a. Assessing herbivory rates of leaf-cutting ant (Atta colombica) colonies through short-term refuse deposition counts. Biotropica 39: 476–481. ———. 2007b. Herbivory rate of leaf-cutting ants in a tropical moist forest in Panama at the population and ecosystem scales. Biotropica. 39: 482–488. Hölldobler, B., and E. O. Wilson. 1990. The Ants. Cambridge, MA: Belknap Press of Harvard Univ. Hubbell, S. P., J. J. Howard, and D. F. Wiemer. 1984. Chemical leaf repellency to an attine ant: Seasonal distribution among potential host plant species. Ecology 65: 1067–1076. Hubbell, S. P., D. F. Wiemer, and A. Adejare. 1983. An antifungal terpenoid defends a Neotropical tree (Hymenaea) against attack by fungus-growing ants (Atta). Oecologia 60: 321–327. Janzen, D. H. 1966. Coevolution and mutualism between ants and acacias in Central America. Evolution 20: 249–275. ———. 1975. Ecology of Plants in the Tropics. London: Edward Arnold. ———. 1980. Two potential coral snake mimics in a tropical deciduous forest. Biotropica 12: 77–78. ———. 1985. Plant defences against animals in the Amazonian rain forest. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Keeler, K. H. 1980. Distribution of plants with extrafloral nectaries in temperate communities. Amer. Midl. Nat. 104: 274–280. Krieger, R. I., L. P. Feeny, and C. F. Wilkinson. 1971. Detoxication enzymes in the guts of caterpillars: An evolutionary answer to plant defenses? Science 172: 579–581. Kursar, T. A., and Coley, P. D. 2003. Convergence in defense syndromes of young leaves in tropical rainforests. Biochemical Systematics and Ecology 31: 929–949. Kursar, T. A., and 10 other authors. 2008. Linking insights from basic research with bioprospecting in order to promote conservation, enhance research capacity and provide economic uses of biodiversity. In Tropical Forest Community Ecology, W. Carson and S. Schnitzer (eds.). New York: Wiley-Blackwell. Levin, D. A. 1971. Plant phenolics: An ecological perspective. Amer. Nat. 105: 157–181. ———. 1976. Alkaloid-bearing plants: An ecogeographic perspective. Amer. Nat. 110: 261–284. Marquis, R. J. 1984. Leaf herbivores decrease fitness of a tropical plant. Science 226: 537–539.

Maxson, L. R., and C. W. Myers. 1985. Albumin evolution in tropical poison frogs (Dendrobatidae): A preliminary report. Biotropica 17: 50–56. Milton, K. 1979. Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food selection by generalist herbivores. Amer. Nat. 114: 362–378. ———. 1981. Food choice and digestive strategies of two sympatric primate species. Amer. Nat. 117: 496–505. ———. 1982. Dietary quality and demographic regulation in a howler monkey population. In The Ecology of a Tropical Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press. Moffett, M. W. 1995a. Poison-dart frogs. Nat. Geog. 187: 98–111. Müller, F. 1879. Ituna and Thyridis: A remarkable case of mimicry in butterflies. Proc. Ent. Soc. London 1879: 20–29. Myers, C. W., and J. W. Daly. 1983. Dart-poison frogs. Sci. Amer. 248: 120–133. Nathanson, J. A. 1984. Caffeine and related methylxanthines: Possible naturally occurring pesticides. Science 226: 184–186. Ness, J. H., W. F. Morris, and J. L. Bronstein. 2009. For antprotected plants, the best defense is a hungry offense. Ecology 90: 2823–2831. Nijhout, H. 1994. Developmental perspectives on evolution of butterfly mimicry. Bioscience 44: 148–157. Oliveira, P. S., and H. F. Leitao-Filho. 1987. Extrafloral nectaries: Their taxonomic distribution and abundance in the woody flora of cerrado vegetation in southeast Brazil. Biotropica 19: 140–148. Pfennig, D. W., W. R. Harcombe, and K. S. Pfennig. 2001. Frequency-dependent Batesian mimicry. Nature 410: 323. Rathcke, B. J., and R. W. Poole. 1975. Coevolutionary race continues: Butterfly larval adaptation to plant trichomes. Science 187: 175–176. Rudgers, J. A., and M. C. Gardener. 2004. Extrafloral nectar as a resource mediating multispecies interactions. Ecology 85: 1495–1502. Smiley, J. T. 1985. Heliconius caterpillar mortality during establishment on plants with and without attending ants. Ecology 66: 845–849. Smith, S. M. 1975. Innate recognition of coral snake pattern by a possible avian predator. Science 187: 759–760. ———. 1977. Coral snake pattern rejection and stimulus generalisation by naive great kiskadees (Aves: Tyrannidae). Nature 265: 535–536. Steppuhn, A., K. Gase, B. Krock, R. Halitschke, and I. T. Baldwin. 2004. Nicotine’s defensive function in nature. PLoS Biology 2(8): 217. Turner, J. R. G. 1971. Studies of Müllerian mimicry and its evolution in burnet moths and heliconid butterfiies. In Ecological Genetics and Evolution, R. Creed (ed.). Oxford, UK: Blackwell Scientific. ———. 1975. A tale of two butterflies. Nat. Hist. 84: 29–37. ———. 1981. Adaptation and evolution in Heliconius: A defense of neo-Darwinism. Ann. Rev. Ecol. Syst. 12: 99–121.

further reading

Whittaker, R. H., and P. P. Feeny. 1971. Allelochemics: Chemical interactions between species. Science 171: 757–770. Zucker, W. V. 1983. Tannins. Does structure determine function? An ecological perspective. Amer. Nat. 121: 355–365.

Chapter 12: Further Reading Alongi, D. M. 2009. The Energetics of Mangrove Forests. New York: Springer. Bates, H. W. 1863. The Naturalist on the River Amazons. London: John Murray. Dyk, J. V. 1995. The Amazon. Nat. Geo. 187: 2–39. Ellison, A. M., and E. L. Farnsworth. 1993. Seedling survivorship, growth, and response to disturbance in Belizean mangal. Amer. Jour. Botany 80: 1137–1145. Goulding, M. 1980. The Fishes and the Forest: Explorations in Amazonian Natural History. Berkeley: Univ. of Calif. Press. ———. 1993. Flooded forests of the Amazon. Sci. Amer. 266: 114–120. Goulding, M., N. J. H. Smith, and D. J. Mahar. 1996. Floods of Fortune: Ecology and Economy along the Amazon. New York: Columbia Univ. Press. Grajal, A., S. D. Strahl, R. Parra, M. G. Dominguez, and A. Neher. 1989. Foregut fementation in the Hoatzin, a Neotropical leaf-eating bird. Science 245: 1236–1238. Junk, W. J. 1970. Investigations on the ecology and production-biology of the “floating meadows” (PaspaloEchinochloetum) on the middle Amazon. Amazonia 2: 449–495. Junk, W. J., and K. Furch. 1985. The physical and chemical properties of Amazonian waters and their relationships with the biota. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Kalliola, R., J. Salo, M. Puhakka, and M. Rajasilta. 1991. New site formation and colonizing vegetation in primary succession on the western Amazon floodplains. Jour. Ecol. 79: 877–901. Lopez, O. R., and T. A. Kursar. 1999. Flood tolerance of four tropical tree species. Tree Physiology 19: 925–932. ———. 2003. Does flood tolerance explain tree species distribution in tropically seasonally flooded habitats? Oecologia 136: 193–204. Lowe-McConnell, R. H. 1987. Ecological Studies in Tropical Fish Communities. Cambridge, UK: Cambridge Univ. Press. Lugo, A. E., and S. C. Snedaker. 1974. The ecology of mangroves. Ann. Rev. Ecol. Syst. 5: 39–64. Meade, R. H., and L. Koehnken. 1991. Distribution of the river dophin, tonina Inia geoffrensis, in the Orinoco River Basin of Venezuela and Colombia. Interciencia 16: 300–312. Meade, R. H., J. M. Rayol, S. C. Da Conceicao, and J. R. G. Natividade. 1991. Backwater effects in the Amazon River Basin of Brazil. Environ. Geol. Water Sci. 18: 105–114.

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Muller-Karger, F. E., C. R. McClain, and P. L. Richardson. 1988. The dispersal of the Amazon’s water. Nature 333: 56–59. Nordin, C. F. Jr., and R. H. Meade. 1982. Deforestation and increased flooding in the upper Amazon. Science 215: 426–427. ———. 1985. The Amazon and the Orinoco. McGraw-Hill Yearbook of Science and Technology 1986, pp. 385–390. New York: McGraw-Hill. Ojasti, J. 1991. Human exploitation of capybara. In Neotropical Wildlife Use and Conservation, J. G. Robinson and K. H. Redford (eds.). Chicago: Univ. of Chicago Press. Piou, C., I. C. Feller, U. Berger, and F. Chi. 2006. Zonation patterns of Belizean offshore mangrove forests 41 years after a catastrophic hurricane. Biotropica 38: 365–374. Rodriguez, G. 1987. Structure and production in Neotropical mangroves. Trends in Ecol. Evol. 2: 264–267. Rutzler, K., and I. C. Feller. 1987. Mangrove swamp communities. Oceanus 30: 16–24. ———. 1996. Caribbean mangrove swamps. Sci. Amer. 274: 94–99. Saenger, P. 2009. Mangrove Ecology, Silviculture, and Conservation. Heidelberg: Springer Netherlands. Salati, E., and P. B. Vose. 1984. Amazon Basin: A system in equilibrium. Science 225: 129–138. Spalding, M., M. Kainuma, and L. Collins. 2010. World Atlas of Mangroves. London: Earthscan Publications. Strahl, S. D. 1985. Correlates of reproductive success in communal Hoatzins (Opisthocomus hoazin). Abstracts of the 103d American Ornithologists’ Union Meeting. Strahl, S. D., and A. Schmitz. 1990. Hoatzins: Cooperative breeding in a folivorous Neotropical bird. In Cooperative Breeding in Birds, P. B. Stacey and W. D. Koenig (eds.). Cambridge, UK: Cambridge Univ. Press. Tomlinson, P. B. 1995. The Botany of Mangroves. Cambridge, UK: Cambridge Univ. Press. Walsh, G. E. 1974. Mangroves: A review. In Ecology of Halophytes, R. J. Reimold and W. H. Queens (eds.). New York: Academic Press.

Chapter 13: Further Reading Andrews, M. 1982. Flight of the Condor. Boston: Little, Brown. Bridges, E. L. 1949. Uttermost Part of the Earth: Indians of Tierra del Fuego. New York: E. P. Dutton. [Reprinted by Dover Publications, NY, 1988.] Chazdon, R. L., and D.F.R.P. Burslem, the Earl of Cranbrook. 2002. Tropical naturalists of the sixteenth through nineteenth centuries. In Foundations of Tropical Forest Biology, R. L. Chazdon and T. C. Whitmore (eds.). Chicago: Univ. of Chicago Press. Clerjacks, A., K. Wesche, and I. Hensen. 2007. Lateral expansion of Polylepis forest fragments in central Ecuador. Forest Ecology and Management 242: 477–486.

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further reading

De Barcellos Falkenberg, D., and J. C. Voltilini. 1995. The montane cloud forest in southern Brazil. In Tropical Montane Cloud Forests: Ecological Studies 110, L. S. Hamilton, J. O. Juvik, and F. N. Scatena (eds.). New York: Springer-Verlag. Doumenge, C., D. Gilmour, M. R. Perez, and J. Blockhus. 1995. Tropical montane cloud forests: conservation status and management issues. In Tropical Montane Cloud Forests: Ecological Studies 110, L. S. Hamilton, J. O. Juvik, and F. N. Scatena (eds.). New York: Springer-Verlag. Graves, G. R., J. P. O’Neill, and T. A. Parker III. 1983. Grallaricula ochraceifrons, a new species of antpitta from northern Peru. Wilson Bull. 95: 1–6. Grubb, P. J. 1971. Interpretation of the “Massenerhebung” effect on tropical mountains. Nature 229: 44–45. ———. 1977. Control of forest growth and distribution on wet tropical mountains. Ann. Rev. Ecol. Syst. 8: 83–107. Haber, W. A. 2000. Plants and vegetation. Chapter 3 in Monteverde: Ecology and Conservation of a Tropical Cloud Forest, N. M. Nadkarni and N. T. Wheelright (eds.). New York: Oxford Univ. Press. Hamilton, L. S., J. O. Juvik, and F. N. Scatena (eds.). 1995. Tropical Montane Cloud Forests: Ecological Studies 110. New York: Springer-Verlag. Hilty, S. L. 2003. Birds of Venezuela, 2nd ed. Princeton, NJ: Princeton Univ. Press. Isler, M. L., and P. R. Isler. 1987. The Tanagers: Natural History, Distribution, and Identification. Wash., DC: Smithsonian Inst. Press. Leo, M. 1995. The importance of tropical montane cloud forest for preserving vertebrate endemism in Peru: The Rio Abiseo National Park as a case study. In Tropical Montane Cloud Forests: Ecological Studies 110, L. S. Hamilton, J. O. Juvik, and F. N. Scatena (eds.). New York: Springer-Verlag. Long, A. J. 1995. The importance of tropical montane cloud forests for endemic and threatened birds. In Tropical Montane Cloud Forests: Ecological Studies 110, L. S. Hamilton, J. O. Juvik, and F. N. Scatena (eds.). New York: Springer-Verlag. Morrison, T. 1974. Land above the Clouds. London: Andre Deutsch. ———. 1976. The Andes. Amsterdam: Time-Life International. Murray, K. G., S. Kinsman, and J. L. Bronstein. 2000. Plantanimal interactions. Chapter 8 in Monteverde: Ecology and Conservation of a Tropical Cloud Forest, N. M. Nadkarni and N. T. Wheelright (eds.). New York: Oxford Univ. Press. Nadkarni, N. M., and N. T. Wheelright (eds.). 2000. Monteverde: Ecology and Conservation of a Tropical Cloud Forest. New York: Oxford Univ. Press. O’Neill, J. P., and G. R. Graves. 1977. A new genus and species of owl (Aves: Strigidae) from Peru. Auk 94: 409–416. Parker, T. A. III, and J. P. O’Neill. 1985. A new species and new subspecies of Thryothorus wren from Peru. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, E. S. Morton, R.

S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union. 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 Monteverde: Ecology and Conservation of a Tropical Cloud Forest, pp. 439–442, N. M. Nadkarni and N. T. Wheelright (eds.). New York: Oxford Univ. Press. Pringle, C. M. 1988. History of conservation efforts and initial exploration of the lower extension of Parque Nacional Braulio Carrillo, Costa Rica. In Tropical Rain Forests, pp. 131–142, F. Almeda and C. M. Pringle (eds). San Francisco: Calif. Acad. of Sci. and AAAS Pacific Division. Pringle, C. M., I. Chacón, M. H. Grayum, H. W. Greene, G. S. Hartshorn, G. E. Schatz, F. G. Stiles, C. Gómez, and M. Rodríguez. 1984. Natural history observations and ecological evaluation of the La Selva Protection Zone, Costa Rica. Brenesia 22: 189–206. Ridgely, R. S., and P. J. Greenfield. 2001. The Birds of Ecuador Field Guide. Ithaca: Cornell Univ. Press. Ridgely, R. S., and G. Tudor. 1994. The Birds of South America, vol. 2. Austin: Univ. of Texas Press. Robbins, M. B., G. H. Rosenberg, and F. S. Molina. 1994. A new species of cotinga (Cotingidae: Doliornis) from the Ecuadorian Andes, with comments on plumage sequences in Doliornis and Ampelion. Auk 111: 1–7. Schulenberg, T. S., and M. D. Williams. 1982. A new species of antpitta (Grallaria) from northern Peru. Wilson Bull. 94: 105–113. Stevenson, R., and W. A. Haber. 2000. Migration of butterflies through Monteverde. In Monteverde: Ecology and Conservation of a Tropical Cloud Forest, pp. 118–119, N. M. Nadkarni and N. T. Wheelright (eds.). New York: Oxford Univ. Press. Stiles, F. G. 1988. Altitudinal movements of birds on the Caribbean slope of Costa Rica: Implications for conservation. In Tropical Rain Forests, pp. 243–258, F. Almeda and C. M. Pringle (eds). San Francisco: Calif. Acad. of Sci. and AAAS Pacific Division. Stotz, D. F., J. W. Fitzpatrick, T. A. Parker III, and D. K. Moskovits. 1996. Neotropical Birds: Ecology and Conservation. Chicago: Univ. of Chicago Press. Timm, R. M., and R. K. LaVal. 2000. Mammals. Chapter 7 in Monteverde: Ecology and Conservation of a Tropical Cloud Forest, N. M. Nadkarni and N. T. Wheelright (eds.). New York: Oxford Univ. Press. Wheelwright, N. T. 1983. Fruits and the ecology of resplendent quetzals. Auk 100: 286–301. Young, B. E., and D. B. McDonald. 2000. Birds. Chapter 6 in Monteverde: Ecology and Conservation of a Tropical Cloud Forest, N. M. Nadkarni and N. T. Wheelright (eds.). New York: Oxford Univ. Press.

further reading

409

Chapter 14: Further Reading

Chapter 15: Further Reading

Beard, J. S. 1953. The savanna vegetation of northern tropical America. Ecol. Monog. 23: 149–215. Blydenstein, J. 1967. Tropical savanna vegetation of the llanos of Colombia. Ecology 48: 1–15. Boulière, F., and H. Hadley. 1970. The ecology of tropical savannas. Ann. Rev. Ecol. Syst. 1: 125–152. Hoffman, W. A., R. Adasme, M. Haridasan, M. T. de Carvalho, E. L. Geiger, M. A. B. Pereira, S. B. Gotch, and A. C. Franco. 2009. Tree topkill, not mortality, governs the dynamics of savanna-forest boundaries under frequent fire in central Brazil. Ecology 90: 1326–1337 Huber, O. 1982. Significance of savanna vegetation in the Amazon territory of Venezuela. In Biological Diversification in the Tropics, G. T. Prance (ed.). New York: Columbia Univ. Press. ———. 1987. Neotropical savannas: Their flora and vegetation. Trends in Ecol. Evol. 2: 67–71. Kauffman, J. B., D. L. Cummings, and D. E. Ward. 1994. Relationships of fire, biomass, and nutrient dynamics along a vegetation gradient in the Brazilian cerrado. Jour. Ecol. 82: 519–531. Kushlan, J. A., G. Morales, and P. C. Frohring. 1985. Foraging niche relations of wading birds in tropical wet savannas. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, E. S. Morton, R. S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union. Marris, E. 2005. The forgotten ecosystem. Nature 437: 944–945. Pires, J. M., and G. T. Prance. 1985. The vegetation types of the Brazilian Amazon. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Riginos, C., and J. B. Grace. 2008. Savanna tree density, herbivores, and the herbaceous community: Bottom-up vs. top-down effects. Ecology 89: 2228–2238. Salgado-Labouriau, M. L. 1998. Late quaternary palaeoclimate in the savannas of South America. Jour. Quaternary Science 12: 371–379. Sarmiento, G. 1983. The savannas of tropical America. In Tropical Savannas, F. Boulière (ed.). New York: Elsevier. Sarmiento, G., and M. Monasterio. 1975. A critical consideration of the environmental conditions associated with the occurrence of savanna ecosystems in tropical America. In Tropical Ecological Systems: Trends in Terrestrial and Aquatic Research, F. B. Golley and E. Medina (eds.). New York: Springer-Verlag. Walter, H. 1971. Ecology of Tropical and Subtropical Vegetation. New York: Van Nostrand Reinhold. ———. 1973. Vegetation of the Earth in Relation to Climate and the Ecophysiological Conditions. London: English Universities Press.

Note: Field guides, as well as papers described in the chapter, are in boldface. Angehr, G. R., and R. Dean. 2010. The Birds of Panama: A Field Guide. Ithaca, NY: Comstock. Askins, R. A., J. F. Lynch, and R. Greenberg. 1990. Population declines in migratory birds in eastern North America. In Current Ornithology, vol. 7, D. M. Power (ed.). New York: Plenum Press. Bates, H. W. 1863. The Naturalist on the River Amazons. London: John Murray. Buckley, P. A., M. S. Foster, E. S. Morton, R. S. Ridgely, and F. G. Buckley (eds.). 1985. Neotropical Ornithology. Wash., DC: American Ornithologists’ Union. Collar, N. J., L. P. Gonzaga, N. Krabbe, A. Madrono Nietro, L. G. Naranjo, T. A. Parker III, and D. C. Wedge. 1992. Threatened Birds of the Americas: The ICBP/IUCN Red Data Book. Wash., DC: Smithsonian Inst. Press. DeGraaf, R. M., and J. H. Rappole. 1995. Neotropical Migratory Birds: Natural History, Distribution, and Population change. Ithaca, NY: Cornell Univ. Press. Delacour, J., and D. Amadon. 1973. Curassows and Related Birds. New York: American Museum of Natural History. Del Hoyo, J., and N. J. Collar. 2015. HBW and BirdLife International Illustrated Checklist of Birds of the World, vol. 1. Barcelona: Lynx Edicions. Erize, F., J. R. Rodriguez Mata, and M. Rumboll. 2006. Birds of South America: Non-Passerines: Rheas to Woodpeckers. Princeton, NJ: Princeton Univ. Press. Fjelda, J., and N. Krabbe. 1990. Birds of the High Andes. Svendborg, Denmark: Zoological Museum, Univ. of Copenhagen, and Apollo Books. Garrigues, R., and R. Dean. 2007. The Birds of Costa Rica. Ithaca, NY: Comstock. Greenberg, R., and P. P. Marra (eds.). 2005. Birds of Two Worlds: The Ecology and Evolution of Migration. Baltimore, MD: Johns Hopkins Univ. Press. Gwynne, J. A., R. S. Ridgely, G. Tudor, and M. Argel. 2010. Birds of Brazil: The Pantanal and Cerrado of Central Brazil. Ithaca, NY: Comstock. Hagan, J. M. III, and D. W. Johnston. 1992. Ecology and Conservation of Neotropical Migrant Landbirds. Wash., DC: Smithsonian Inst. Press. Hallett, B. 2006. Birds of the Bahamas and the Turks & Caicos Islands. Oxford, UK: Macmillan Caribbean. Hilty, S. L. 2003. Birds of Venezuela, 2nd ed. Princeton, NJ: Princeton Univ. Press. Hilty, S. L., and W. L. Brown. 1986. A Guide to the Birds of Colombia. Princeton, NJ: Princeton Univ. Press. Isler, M. L., and P. R. Isler. 1987. The Tanagers: Natural History, Distribution, and Identification. Wash., DC: Smithsonian Inst. Press.

410

further reading

Jones, H. L. 2003. Birds of Belize. Austin: Univ. of Texas Press. Keast, A., and E. S. Morton (eds.). 1980. Migrant Birds in the Neotropics: Ecology, Behavior, Distribution, and Conservation. Wash., DC: Smithsonian Inst. Press. Kricher, J. C. 1995. Black-and-white warbler. In The Birds of North America, no. 158, A. Poole and F. Gill (eds.). Philadelphia, PA: Academy of Natural Sciences / Wash., DC: American Ornithologists’ Union. Kricher, J. C., and W. E. Davis Jr. 1986. Returns and winter site fidelity of North American migrants banded in Belize, Central America. Jour. Field Ornithol. 57: 48–52. ———. 1987. No place like home. Living Bird Quarterly 6: 24–27. ———. 1992. Patterns of avian species richness in disturbed and undisturbed habitats in Belize. In Ecology and Conservation of Neotropical Migrant Landbirds, J. M. Hagan III and D. W. Johnston (eds.). Wash., D. C.: Smithsonian Inst. Press. Land, H. 1970. Birds of Guatemala. Wynnewood, PA: Livingston. Lovejoy, T. E. 1974. Bird diversity and abundance in Amazon forest communities. Living Bird 13: 127–192. Marra, P. P., K. A. Hobson, and R. T. Holmes. 1998. Linking winter and summer events in a migratory bird by using stable-carbon isotopes. Science 282: 1884–1886. Meyer de Schauensee, R. 1966. The Species of Birds of South America. Wynnewood, PA: Livingston, for the Academy of Natural Sciences, Philadelphia. Moynihan, M. 1962. The organization and probable evolution of some mixed species flocks of Neotropical birds. Smithsonian Misc. Coll. 143: 1–140. Munn, C. A. 1985. Permanent canopy and understory flocks in Amazonia: Species composition and population density. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, E. S Morton, R. S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union. Munn, C. A., and J. W. Terborgh. 1979. Multi-species territoriality in Neotropical foraging flocks. Condor 81: 338–347. Pearson, D. L. 1977. A pantropical comparison of bird community structure on six lowland forest sites. Condor 79: 232–244. ———. 1982. Historical factors and bird species richness. In Biological Diversification in the Tropics, G. T. Prance, ed. New York: Columbia Univ. Press. Peterson, R. T., and E. L. Chaliff. 1973. A Field Guide to Mexican Birds. Boston: Houghton Mifflin. Pimm, S. L., and R. A. Askins. 1995. Forest losses predict bird extinctions in eastern North America. Proc. Nat. Acad. Sci. 92: 9343–9347. Raffaele, H., J. Wiley, O. Garrido, A. Keith, and J. Raffaele. 1998. A Guide to the Birds of the West Indies. Princeton, NJ: Princeton Univ. Press. Rappole, J. H. 1995. The Ecology of Migrant Birds: A Neotropical Perspective. Wash., DC: Smithsonian Inst. Press.

Rappole, J. H., E. S. Morton, T. E. Lovejoy III, and J. L. Ruos. 1983. Nearctic Avian Migrants in the Neotropics. Wash., DC: US Dept. of Interior, Fish and Wildlife Service. Rappole, J. H., M. A. Ramos, and K. Winkler. 1989. Wintering Wood Thrush mortality in southern Veracruz. Auk 106: 402–410. Rappole, J. H., and D. H. Warner. 1980. Ecological aspects of avian migrant behavior in Veracruz, Mexico. In Migrant Birds in the Neotropics, A. Keast and E. S. Morton (eds.). Wash., DC: Smithonian Inst. Press. Remsen, J. V. Jr. 2001. True winter range of the veery (Catharus fascensens): Lessons for determining winter ranges of species that winter in the tropics. Auk: 118, 838–848. Restall, R. 2006. Birds of Northern South America: An Identification Guide, vol. 1. New Haven, CT: Yale Univ. Press. ———. 2006. Birds of Northern South America: An Identification Guide, vol. 2. New Haven, CT: Yale Univ. Press. Ricklefs, R. E. 1969a. The nesting cycle of songbirds in tropical and temperate regions. Living Bird 8: 165–175. ———. 1969b. Natural selection and the development of mortality rates in young birds. Nature 223: 422–425. Ridgely, R. S., and P. J. Greenfield. 2001. The Birds of Ecuador: Status, Distribution, and Taxonomy. Ithaca, NY: Comstock. ———. 2001. The Birds of Ecuador: Field Guide. Ithaca, NY: Comstock. Ridgely, R. S., and J. A. Gwynne. 1989. A Guide to the Birds of Panama with Costa Rica, Nicaragua, and Honduras, 2nd ed. Princeton, NJ: Princeton Univ. Press. Ridgely, R. S., and G. Tudor. 1989. The Birds of South America, vol. 1. Austin: Univ. of Texas Press. ———. 1994. The Birds of South America, vol. 2. Austin: Univ. of Texas Press. ———. 2009. Field Guide to the Songbirds of South America. Austin: Univ. of Texas Press. Robbins, C. S., J. W. Fitzpatrick, and P. B. Hamel. 1992. A warbler in trouble: Dendroica cerulea. In Ecology and Conservation of Neotropical Migrant Landbirds, J. M. Hagan III and D. W. Johnston (eds.). Wash., DC: Smithsonian Inst. Press. Robinson S. K. 1985a. Coloniality in the yellow-rumped cacique as a defense against nest predators. Auk 102: 506–519. ———. 1985b. The yellow-rumped cacique and its associated nest pirates. In Neotropical Ornithology, P. A. Buckley, M. S. Foster, L. S. Morton, R. S. Ridgely, and F. G. Buckley (eds.). Wash., DC: American Ornithologists’ Union. ———. 1986. Social security for birds. Nat. Hist. 95(3): 39–47. Robinson, S. K., and J. Terborgh. 1990. Bird communities of the Cocha Cashu Biological Station in Amazonian Peru. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press.

further reading

Schulenberg, T. S., D. F. Stotz, D. F. Lane, J. P. O’Neill, and T. A. Parker III. 2007. Birds of Peru. Princeton, NJ: Princeton Univ. Press. Sick, H. 1993. Birds in Brazil: A Natural History. Princeton, NJ: Princeton Univ. Press. Skutch, A. F. 1954. Life Histories of Central American Birds. Pacific Coast Avifauna, no. 31. Berkeley, CA: Cooper Ornithological Society. ———. 1960. Life Histories of Central American Birds II. Pacific Coast Avifauna, no. 34. Berkeley, CA: Cooper Ornithological Society. ———. 1967. Life Histories of Central American Highland Birds. Publication no. 7. Cambridge, MA: Nuttall Ornithological Club. ———. 1969. Life Histories of Central American Birds III. Pacific Coast Avifauna, no. 35. Berkeley, CA: Cooper Ornithological Society. ———. 1972. Studies of Tropical American Birds. Publication no. 10. Cambridge, MA: Nuttall Ornithological Club. ———. 1973 The Life of the Humminghird. New York: Crown. ———. 1981. New Studies of Tropical American Birds. Publication no. 19. Cambridge, MA: Nuttall Ornithological Club. ———. 1983. Birds of Tropical America. Austin: Univ. of Texas Press. ———. 1985. The Life of the Woodpecker. Ithaca, NY: Cornell Univ. Press. ———. 1989. The Life of the Tanager. Ithaca, NY: Cornell Univ. Press. ———. 1991. The Life of the Pigeon. Ithaca, NY: Cornell Univ. Press. ———. 1996. Antbirds and Ovenbirds. Austin: Univ. of Texas Press. Snow, B. K., and D. W. Snow. 1979. The ochre-bellied flycatcher and the evolution of lek behavior. Condor 81: 286–292. Snow, D. W. 1961 The natural history of the oilbird, Steatornis caripensis, in Trinidad, W. I. Part 1. General behavior and breeding habits. Zoologica 46: 27–48. ———. 1962. A field study of the black-and-white manakin, Manacus manacus, Trinidad. Zoologica 47: 65–104. ———. 1966. A possible selective factor in the evolution of fruiting seasons in tropical forest. Oikos 15: 274–281 ———. 1976. The Web of Adaptation. Ithaca, NY: Cornell Univ. Press. ———. 1982. The Cotingas: Bellbirds, Umbrellabirds, and Other Species. Ithaca, NY: Cornell Univ. Press. Stiles, F. G. 1975. Ecology, flowering phenology and hummingbird pollination of some Costa Rican Heliconia species. Ecology 56: 285–301. ———. 1977. Coadapted competitors: The flowering seasons of hummingbird-pollinated plants in a tropical forest. Science 198: 1177–1178. Stotz, D. F., J. W. Fitzpatrick, T. A. Parker III, and D. K. Moskovits. 1996. Neotropical Birds: Ecology and Conservation. Chicago: Univ. of Chicago Press.

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Stutchbury, B. 2007. Silence of the Songbirds. New York: Walker and Company. Stutchbury, B., S. A. Tarof, T. Done, E. Gow, P. M. Kramer, J. Tautin, J. W. Fox, and V. Afanasyev. 2009. Tracking long-distance songbird migration by using geolocators. Science 323: 896. Tattersall, G. J., D. V. Andrade, and A. S. Abe. 2012. Heat exchange from the toucan bill reveals a controllable vascular thermal radiator. Science 325: 468–470. Terborgh, J. 1989. Where Have All the Birds Gone? Princeton, NJ: Princeton Univ. Press. Terborgh, J., S. K. Robinson, T. A. Parker III, C. A. Munn, and N. Pierpont. 1990. Structure and organization of an Amazonian forest bird community. Ecol. Monog. 60: 213–238. Van Perlo, B. 2015. Birds of South America: Passerines. Princeton, NJ: Princeton Univ. Press. Winkler, D. W., S. M. Billerman, and I. J. Lovette. 2015. Bird Families of the World: An Invitation to the Spectacular Diversity of Birds. Barcelona: Lynx Edicions. Zuccon, D., R. Prŷs-Jones, P. C. Rasmussen, P. G. P. Ericson, 2012. The phylogenetic relationships and generic limits of finches (Fringillidae). Molecular Phylogenetics and Evolution 62 (2): 581–596. doi:10.1016/j. ympev.2011.10.002.

Chapter 16: Further Reading Abrahamson, D. 1985. Tamarins in the Amazon. Science 85: 58–63. Bates, H. W. 1862. Contributions of an insect fauna of the Amazon Valley. Trans. Linn. Soc. London 23: 495–566. Boulière, F. 1983. Animal species diversity in tropical forests. In Tropical Rain Forest Ecosystems: Structure and Function, F. B. Golley (ed.). Amsterdam: Elsevier Scientific. Brown, L., and L. L. Rockwood. 1986. On the dilemma of horns. Nat. Hist. 95: 54–62. Campbell, J. A., and W. W. Lamar. 1989. The Venomous Reptiles of Latin America. Ithaca, NY: Comstock. Castner, J. L. 2000. Amazon Insects: A Photo Guide. Gainesville, FL: Feline Press. Colwell, R. K. 1985b. A bite to remember. Nat. Hist. 94: 2–8. Conniff, R. 1996. Tarantulas: Earth tigers and bird spiders. Nat. Geog. 190: 98–115. Crump, M. L. 1983. Dendrobates granuliferus and Dendrobates pumilio. In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. D’Abrera, B. 1984. The Butterflies of South America. Victoria, Australia: Hill House. Darwin, C. R. 1871. The Descent of Man and Selection in Relation to Sex. London: John Murray. Davis, E. W. 1983. Preparation of the Haitian zombie poison. Harvard Univ. Botanical Museum Leaflets 29: 139–149. DeVries, P. J. 1983. Caligo memnon (Buhito pardo, caligo, cream owl butterfly). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press.

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further reading

———. 1987. The Butterflies of Costa Rica and Their Natural History, vol. 1. Princeton, NJ: Princeton Univ. Press. ———. 1997. The Butterflies of Costa Rica and Their Natural History, vol. 2. Princeton, NJ: Princeton Univ. Press. Duellman, W. E. 1992. Reproductive strategies of frogs. Sci. Amer. 267: 80–87. Eisenberg, J. F. 1989. Mammals of the Neotropics, vol. 1, The Northern Neotropics. Chicago: Univ. of Chicago Press. Emmons, L. H. 1984. Geographic variation in densities and diversities of non-flying mammals in Amazonia. Biotropica 16: 210–222. ———. 1987. Comparative feeding ecology of felids in a Neotropical rainforest. Behav. Ecol. Sociobiol. 20: 271–283. ———. 1997. Neotropical Rainforest Mammals: A Field Guide, 2nd ed. Chicago: Univ. of Chicago Press. Goldizen, A. W. 1988. Tamarin and marmoset mating systems: Unusual flexibility. Trends in Ecol. Evol. 3: 36–40. Hardy, D. L. Sr. 1994. Bothrops asper (Viperidae) snakebite and field researchers in Middle America. Biotropica 26: 198–207. Heyer, W. R., and L. R. Maxon. 1982. Distributions, relationships, and zoogeography of lowland frogs: The Leptodactylus complex in South America, with special reference to Amazonia. In Biological Diversification in the Tropics, G. T. Prance (ed.). New York: Columbia Univ. Press. Janzen, D. H., and C. R. Carroll. 1983. Paraponera clavata (Bala, giant tropical ant). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Janzen, D. H., and C. C. Hogue. 1983. Fulgora latenaria (Machaca, peanuthead bug, lantern fly). In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Janzen, D. H., and D. E. Wilson. 1983. Mammals. In Costa Rican Natural History, D. H. Janzen (ed.). Chicago: Univ. of Chicago Press. Milton, K. 1979. Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food selection by generalist herbivores. Amer. Nat. 114: 362–378. ———. 1981 Food choice and digestive strategies of two sympatric primate species. Amer. Nat. 117: 496–505. ———. 1982. Dietary quality and demographic regulation in a howler monkey population. In The Ecology of a Tropical Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press. Montgomery, G. G., and M. E. Sunquist. 1975. Impact of sloths on Neotropical forest energy flow and nutrient cycling. In Ecological Studies 11, Tropical Ecological Systems, F. B. Golley and E. Medina (eds.). Heidelberg: Springer-Verlag. Oppenheimer, J. R. 1982. Cebus capucinus: Home range, population dynamics, and interspecific relationships. In The Ecology of a Tropical Forest, E. G. Leigh Jr., A. S. Rand, and D. M. Windsor (eds.). Wash., DC: Smithsonian Inst. Press.

Pearson, D. L., and L. Beletsky. 2010. Brazil: Amazon and Pantanal, Travellers’ Wildlife Guides. Northampton, MA: Interlink Publishing Group. Penny, N. D., and J. R. Arias. 1982. Insects of an Amazonian Forest. New York: Columbia Univ. Press. Ray, T. S., and C. C. Andrews. 1980. Antbutterflies: Butterflies that follow army ants to feed on antbird droppings. Science 210: 1147–1148. Redford, K. H., and J. F. Eisenberg. 1992. Mammals of the Neotropics, vol. 2, The Southern Cone. Chicago: Univ. of Chicago Press. Reid, F. A. 1997. A Field Guide to the Mammals of Central America and Southeast Mexico. New York: Oxford Univ. Press. Reid, F. A., T. Leenders, J. Zook, and R. Dean. 2010. The Wildlife of Costa Rica: A Field Guide. Ithaca, NY: Comstock. Sowls, L. K. 1984. The Peccaries. Tucson: Univ. of Arizona Press. Wallace, A. R. 1895. Natural Selection and Tropical Nature. London: Macmillan. Wasko, D. K., and M. Sasa. 2009. Activity patterns of a Neotropical ambush predator: Spatial ecology of the Ferde-lance (Bothrops asper, Serpentes: Viperidae) in Costa Rica. Biotropica 41: 241–249. Waterton, C. [1825] 1983. Wanderings in South America. London: Century Publishing.

Chapter 17: Further Reading Ayensu, E. S. (ed.). 1980. The Life and Mysteries of the Jungle. New York: Crescent Books. Balick, M. J. 1985. Useful plants of Amazonia: A resource of global importance. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Balick, M. J., and P. A. Cox. 1997. Plants, People, and Culture: The Science of Ethnobotany. San Francisco, CA: W. H. Freeman. Balter, M. 2007. Seeking agriculture’s ancient roots. Science 316: 1830–1835. Beckerman, S. 1987. Swidden in Amazonia and the Amazon rim. In Comparative Farming Systems, B. L. Turner and S. B. Brush (eds.). New York: Guilford Press. Boucher, D. H. 1991. Cocaine and the coca plant: Traditional and illegal uses. Bioscience 41: 72–76. Carneiro, R. L. 1988. Indians of the Amazonian forest. In People of the Tropical Rain Forest, J. S. Denslow and C. Padoch (eds.). Berkeley: Univ. of Calif. Press. Collins, M. (ed.). 1990. The Last Rain Forests. New York: Oxford Univ. Press. Cox, P. A., and M. J. Balick. 1994. The ethnobotanical approach to drug discovery. Sci. Amer. 270: 82–87. Cruz-Angon, A., T. S. Sillett, and R. Greenberg. 2008. An experimental study of habitat selection by birds in a coffee plantation. Ecology 89: 921–927.

further reading

Denevan, W. M. 1976. The aboriginal population of Amazonia. In The Native Population of the Americas in 1492, W. M. Denevan (ed.). Madison: Univ. of Wisconsin Press. ———. 2003. The native population of Amazonia in 1492 reconsidered. Revista Indias 62: 175–188. Dufour, D. L. 1990. Use of tropical rain forests by native Amazonians. Bioscience 40: 652–659. Ewel, J., C. Berish, B. Brown, N. Price, and J. Raich. 1981. Slash and burn impacts on a Costa Rican wet forest site. Ecology 62: 816–829. Fedick, S. L., and A. Ford. 1990. The prehistoric agricultural landscape of the Central Maya Lowlands: An examination of local variability in a regional context. World Archaelogy 22: 18–33. Gibbons, A. 1990. New view of early Amazonia. Science 248: 1488–1490. Glaser, B. 2007. Prehistorically modified soils in central Amazonia: A model for sustainable agriculture in the twenty-first century. Phil. Trans. R. Soc. B 362: 187–196. Gomez-Pompa, A., and A. Kaus. 1990. Traditional management of tropical forests in Mexico. In Alternatives to Deforestation: Steps toward Sustainable Use of the Amazonian Rain Forest, A. B. Anderson (ed.). New York: Columbia Univ. Press. Gomez-Pompa, A., H. L. Morales, E. J. Avilla, and J. J. Avilla. 1982. Experiences in traditional hyraulic agriculture. In Maya Subsistence, K. V. Flannery (ed.). New York: Academic Press. Gottlieb, O. R. 1985. The chemical uses and chemical geography of Amazon plants. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. Greenberg, R., P. Bichier, A. Cruz-Angon, and R. Reitsma. 1997a. Bird populations in shade and sun coffee plantations in Central Guatemala. Cons. Biol. 11: 448– 459. Greenberg, R., P. Bichier, and J. Sterling. 1997b. Bird populations in rustic and planted shade coffee plantations of eastern Chiapas, Mexico. Biotropica 29: 501–514. Greenberg, R., I. Perfecto, and S. M. Philpott. 2008. Agroforests as model systems in tropical ecology. Ecology 89: 913–914. Hammond, N. 1982. Ancient Maya Civilization. New Brunswick, NJ: Rutgers Univ. Press. 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: 1710–1714. Heckenberger, M. J., J. C. Russell, C. Fausto, J. R. Toney, M. J. Schmidt, E. Pereira, B. Franchetto, and A. Kuikuro. 2008. Pre-Columbian urbanism, anthropogenic landscapes, and the future of the Amazon. Science 321: 1214–1217. Hill, K., and A. M. Hurtado. 1989. Hunter-gatherers of the New World. Amer. Sci. 77: 436–443.

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Horn, S. P. 1993. Postglacial vegetation and fire history in the Chirripó Páramo of Costa Rica. Quaternary Res. 40: 107– 116. Horn, S. P., and R. L. Sanford Jr. 1992. Holocene fires in Costa Rica. Biotropica 24: 354–361. Kellman, M., and R. Tackberry. 1997. Tropical Environments: The Functioning and Management of Tropical Ecosystems. London, UK: Routledge. Kricher, J. 2000. Evaluating shade-grown coffee and its importance to birds. Birding 32: 57–60. McLean, J. 2000. Status of shade grown coffee. Birding 32: 61–65. Mann, C. C. 2008. Ancient earthmovers of the Amazon. Science 321: 1148–1152. Mas, A. H., and T. V. Dietsch. 2004. Linking shade coffee certification and biodiversity conservation: Butterflies and birds in Chiapas, Mexico. Ecol. Appl. 14: 642–654. Meggars, B. J. 1985. Aboriginal adaptations to Amazonia. In Amazonia, G. T. Prance and T. E. Lovejoy (eds.). Oxford, UK: Pergamon Press. ———. 1988. The prehistory of Amazonia. In People of the Tropical Rain Forest, J. S. Denslow and C. Padoch (eds.). Berkeley: Univ. of Calif. Press. ———. 2003. Natural versus anthropogenic sources of Amazonian biodiversity: The continuing quest for El Dorado. In How Landscapes Change, G. A. Bradshaw and P. A. Marquet (eds). Berlin, Germany: Springer. Padoch, C. 1988. People of the floodplain and forest. In People of the Tropical Rain Forest, J. S. Denslow and C. Padoch (eds.). Berkeley: Univ. of Calif. Press. Peres, C. A. 1994. Indigenous reserves and nature conservation in Amazonian forests. Cons. Biol. 8: 586–588. Perfecto, I., R. A. Rice, R. Greenberg, and M. E. Van der Voort. 1996. Shade coffee: A disappearing refuge for biodiversity. Bioscience 46: 598–608. Perfecto, I., J. H. Vandermeer, G. López Bautista, G. I. Nuñez, R. Greenberg, P. Bichier, and S. Landgridge. 2004. Greater predation in shaded coffee farms: The role of resident neotropical birds. Ecology 85: 2677–2681. Perfecto, I., J. Vandermeer, A. Mas, and L. S. Pinto. 2005. Biodiversity, yield, and shade coffee certification. Ecological Economics 54: 435–446. Perry, L., D. H. Sandweiss, D. R. Piperno, K. Rademaker, M. A. Malpass, A. Umire, and P. de la Vera. 2006. Early maize agriculture and interzonal interaction in southern Peru. Nature 440: 76–79. Phillips, O., A. H. Gentry, C. Reynel, P. Wilkin, and C. GalvezDurand B. 1994. Quantitative ethnobotany and Amazonian conservation. Cons. Biol. 8: 225–248. Piperno, D. R., and D. M. Pearsall. 1998. The Origin of Agriculture in the Lowland Neotropics. New York: Academic Press. Plotkin, M. J. 1993. Tales of a Shaman’s Apprentice: An Ethnobotanist Searches for New Medicines in the Amazon Rain Forest. New York: Viking.

414

further reading

Plotkin, M., and L. Famolare (eds.). 1992. Sustainable Harvest and Marketing of Rain Forest Products. Wash., DC: Island Press. Redford, K. H. 1992. The empty forest. Bioscience 42: 412– 422. Redford, K. H., and J. G. Robinson. 1987. The game of choice: Patterns of Indian and colonial hunting in the Neotropics. Amer. Anthropol. 89: 650–667. Robinson, J. G., and K. H. Redford (eds.). 1991. Neotropical Wildlife Use and Conservation. Chicago: Univ. of Chicago Press. Roosevelt, A. C. 1989. Lost civilizations of the lower Amazon. Nat. Hist. 98: 75–83. Roosevelt, A. C., R. A. Housley, M. Imazio da Silveira, S. Maranca, and R. Johnson. 1991. Eighth millennium pottery from a prehistoric shell midden in the Brazilian Amazon. Science 254: 1621–1624. Shultes, R. E. 1992. Ethnobotany and technology in the northwest Amazon: A partnership. In Sustainable Harvest and Marketing of Rain Forest Products, M. Plotkin and L. Famolare (eds.). Wash., DC: Island Press. Schultes, R. E., and A. Hoffmann. 1992. Plants of the Gods: Their Sacred, Healing, and Hallucinogenic Powers. Rochester, VT: Healing Arts Press. Schultes, R. E., and R. F. Raffauf. 1990. The Healing Forest: Medicinal and Toxic Plants of the Northwest Amazonia. Portland, OR: Dioscorides Press. Schultes, R.E., and S. von Reis. 2008. Ethnobotany: Evolution of a Discipline. Portland, OR: Timber Press. Siemans, A. H. 1982. Prehispanic agricultural use of the wetlands of northern Belize. In Maya Subsistence, F. V. Fleming (ed.). New York: Academic Press. Tejada-Cruz, C., E. Silva-Rivera, J. R. Barton, and W. J. Sutherland. 2010. Why shade coffee does not guarantee biodiversity conservation. Ecology and Society 15: 13. http://www.ecologyandsociety.org/vol15/iss1/art13/ Turner, B. L. II, and P. D. Harrison. 1981. Prehistoric raisedfield agriculture in the Maya lowlands. Science 213: 339– 405. Turner, B. L. II, and P. D. Harrison (eds.). 1983. Pulltrouser Swamp: Ancient Maya Habitat, Agriculture, and Settlement in Northern Belize. Austin: Univ. of Texas Press. Uhl, C. 1987. Factors controlling succession following slash and burn agriculture in Amazonia. Ecology 75: 377–407. Vega, F. E. 2008. The rise of coffee. Amer. Sci. 96: 138–145. Vickers, W. T. 1988. Game depletion hypothesis of Amazonian adaptation: Data from a native community. Science 239: 1521–1522. ———. 1991. Hunting yields and game composition over ten years in an Amazon Indian territory. In Wildlife Use and Conservation, J. G. Robinson and K. H. Redford (eds.). Chicago: Univ. of Chicago Press. Waterton, C. [1825] 1983. Wanderings in South America. London: Century Publishing.

Wunderle, J. M. Jr. 1999. Avian distribution in Dominican shade coffee plantations: Area and habitat relationships. Jour. of Field Ornithol. 70: 58–70. Wunderle, J. M. Jr., and S. C. Latta. 1998. Avian resource use in Dominican shade coffee plantations. Wilson Bull. 110: 271–281. ———. 2000. Winter site fidelity of Nearctic migrants in shade coffee plantations of different sizes in the Dominican Republic. Auk 117: 596–614.

Chapter 18: Further Reading Aragão, L. E. O., and Y. E. Shimabukuro. 2010. The incidence of fire in Amazonian forests with implications for REDD. Science 328: 1275–1278. Archard, F., H. D. Eva, H. J. Stibig, P. Mayaux, J. Gallego, T. Richards, and J. P. Malingreau. 2002. Determination of deforestation rates of the world’s humid tropical forests. Science 297: 999–1002. Asner, G. P., D. E. Knapp, E. N. Broadbent, P. J. C. Oliveira, M. Keller, and J. N. Silva. 2005. Selective logging in the Brazilian Amazon. Science 310: 480–482. Bierregaard, R. O. Jr., C. Gascon, T. E. Lovejoy, and R. Mesquita (eds.). 2001a. Lessons from Amazonia: The Ecology and Conservation of a Fragmented Forest. New Haven, CT: Yale Univ. Press. Bierregaard, R. O. Jr., T. E. Lovejoy, V. Kapos, A. Augusto de Santos, and R. W. Hutchings. 1992. The biological dynamics of tropical rain forest fragments. Bioscience 42: 859–866. Bierregaard, R. O. Jr., and 14 other authors. 2001b. Principles of forest fragmentation and conservation in the Amazon. In Lessons from Amazonia: The Ecology and Conservation of a Fragmented Forest, R. O. Bierregaard et al. (eds.). New Haven, CT: Yale Univ. Press. Brown, K. S. Jr., and G. G. Brown. 1992. Habitat alteration and species loss in Brazilian forests. In Tropical Deforestation and Species Extinction, T. C. Whitmore and J. A. Sayer (eds.). London: Chapman & Hall. Bruna, E. M. 1999. Seed germination in rain forest fragments. Nature 402: 139. ———. 2003. Are plant populations in fragmented habitats recruitment limited? Tests with an Amazonian herb. Ecology 84: 932–947. Bruna, E. M., and M. K. Oli. 2005. Demographic effects of habitat fragmentation on a tropical herb: Life-table response experiments. Ecology 86: 1816–1824. Bush, M. B., J. R. Flenley, and W. D. Gosling (eds.). 2011. Tropical Rainforest Responses to Climatic Change. Chichester, UK: Praxis and Springer. Bush, M. B., and H. Hooghiemstra. 2005. Tropical biotic responses to climate change. In Climate Change and Biodiversity, T. E. Lovejoy and L. Hannah (eds.). New Haven, CT: Yale Univ. Press.

further reading

Butchart, S. H. M., and 44 TK# {AU: Please fill in # (or name if fewer than 10} other authors. 2010. Global biodiversity: Indicators of recent decline. Science 328: 1164–1168. Butler, R. A. 2007. Just how bad is the biodiversity extinction crisis? A debate erupts in the halls of conservation science. Mongabay, Feb. 6, 2007. https://news.mongabay.com/2007/02/ just-how-bad-is-the-biodiversity-extinction-crisis/. Chazdon, R. L. 2003. Tropical forest recovery: Legacies of human impact and natural disturbances. Perspectives in Plant Ecology and Evolutionary Systematics 6: 51–71. Clark, D. A. 2004. Tropical forests and global warming: Slowing it down or speeding it up? Front. Ecol. Environ. 2: 73–80. Cochrane, M. A., A. Alencar, M. D. Schulze, C. M. Souza Jr., D. C. Nepstad, P. Lefebvre, E. A. Davidson. 1999. Positive feedbacks in the fire dynamic of closed canopy tropical forests. Science 284: 1832–1835. Costanza, R., and 12 other authors. 1997. The value of the world’s ecosystem services and natural capital. Nature 387: 253–260. Dean, W. 1995. With Broadax and Firebrand: The Destruction of the Brazilian Atlantic Forest. Los Angeles: Univ. of Calif. Press. Desouza, O., J. H. Schoereder, V. Brown, and R. O. Bierregaard Jr. 2001. The theoretical overview of the processes determining species richness in forest fragments. In Lessons from Amazonia: The Ecology and Conservation of a Fragmented Forest, R. O. Bierregaard et al. (eds.). New Haven, CT: Yale Univ. Press. Dirzo, R., and E. Mendoza. 2007. Size-related differential seed predation in a heavily defaunated Neotropical rain forest. Biotropica 39: 355–362. FAO. 2000. Global forest resource assessment 2000—main report. FAO Forestry Paper 140, United Nations Food and Agriculture Organization, New York. Fearnside, P. M. 2015. Brazil’s São Luiz do Tapajós dam: The art of cosmetic environmental impact assessments. Water Alternatives 8 (3): 373–396. Feeley, K. J., and J. W. Terborgh. 2006. Habitat fragmentation and effects of herbivore (howler monkey) abundances on bird species richness. Ecology 87: 144–150. Ferraz, G., J. D. Nichols, J. E. Hines, P. C. Stouffer, R. O. Bierregaard Jr., and T. E. Lovejoy. 2007. A large-scale deforestation experiment: Effects of patch area and isolation on Amazon birds. Science 315: 238–241. Foley, J. A., and 10 other authors. 2007. Amazonia revealed: forest degradation and loss of ecosystem goods and services in the Amazon Basin. Front. Ecol. Environ. 5: 25–32. Galindo-Leal, C., and I. de Gusmao Camara. 2003. The Atlantic Forest of South America: Biodiversity Status, Threats, and Outlook. State of the Hotspots series. Wash., DC: Island Press. Gardner, T. A., J. Barlow, L. W. Parry, and C. A. Peres. 2006. Predicting the uncertain future of tropical forest species in a data vacuum. Biotropica 39: 25–30. Gullison, R. E., and 11 other authors. 2007. Tropical forests and climate policy. Science 316: 985.

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Houghton, R. A., D. L. Skole, Carlos A. Nobre, J. L. Hackler, K. T. Lawrence, and W. H. Chomentowski. 2000. Annual fluxes of carbon from deforestation and regrowth in the Brazilian Amazon. Nature 403: 301–304. Kaimowitz, D., and D. Shell. 2007. Conserving what and for whom? Why conservation should help meet basic human needs in the tropics. Biotropica 39: 567–574. Keller, M., G. A. Asner, G. Blate, J. McGlocklin, F. Merry, M. Pena-Claros, and J. Zweede. 2007. Timber production in selectively logged tropical forests in South America. Front. Ecol. Environ. 5: 213–216. Koellner, T., and O. J. Schmitz. 2006. Biodiversity, ecosystem function, and investment risk. BioScience 56: 977–985. Knoke, T., B. Calvas, N. Aguirre, R. M. Roman-Cuesta, S. Gunter, B. Stimm, M. Weber, and R. M. Mosandl. 2009. Can tropical farmers reconcile subsistence needs with forest conservation? Front. Ecol. Environ. 7: 548–554. Lamb. D., P. D. Erskine, and J. A. Parotta. 2005. Restoration of degraded tropical forest landscapes. Science 310: 1628–1632. Laurance, S. G. W. 2006. Rainforest roads and the future of forest dependent wildlife: A case study of understory birds. In Emerging Threats to Tropical Forests, W. F. Laurance and C. A. Peres (eds.). Chicago: Univ. of Chicago Press. Laurance, W. F. 1999. Reflections on the tropical deforestation crisis. Biol. Cons. 91: 109–117. ———. 2001. Fragmentation and plant communities. In Lessons from Amazonia: The Ecology and Conservation of a Fragmented Forest, R. O. Bierregaard et al. (eds.). New Haven, CT: Yale Univ. Press. ———. 2006. Have we overstated the tropical biodiversity crisis? Trends in Ecol. Evol. 22: 65–70. Laurance, W. F., M. A. Cochrane, S. Bergen, P. M. Fearnside, P. Delamõnica, C. Barber, S. D’Angelo, and T. Fernandes. 2001. The future of the Brazilian Amazon. Science 291: 438–439. Laurance, W. F., H. E. M. Nascimento, S. G. Laurance, A. C. Andrade, P. E. Fearnside, J. E. L. Ribeiro, and R. L. Carpretz. 2006. Rain forest fragmentation and the proliferation of successional trees. Ecology 87: 469–482. Laurance, W. F., and C. A. Peres (eds.). 2006. Emerging Threats to Tropical Forests. Chicago: Univ. of Chicago Press. Loarie, S. R., P. B. Duffy, H. Hamilton, G. P. Asner, C. B. Field, D. D. Ackerly. 2009. The velocity of climate change. Nature 462: 1052–1055. Lovejoy, T. E., and R. O. Bierregaard Jr. 1990. Central Amazonian forests and the minimum critical size of ecosystems project. In Four Neotropical Rainforests, A. H. Gentry (ed.). New Haven, CT: Yale Univ. Press. Lovejoy, T. E., R. O. Bierregaard Jr., A. B. Rylands, J. R. Malcolm, C. E. Quintela, L. H. Harper, K. S. Brown Jr., A. H. Powell, G. V. N. Powell, H. O. R. Schubart, and M. B. Hays. 1986. Edge and other effects of isolation on Amazon forest fragments. In Conservation Biology: The Science of Scarcity and Diversity, M. E. Soule (ed.). Sunderland, MA: Sinauer.

416

further reading

Lovejoy, T. E., and L. Hannah (eds.). 2005. Climate Change and Biodiversity. New Haven, CT: Yale Univ. Press. Muller-Landau, H. C. 2007. Predicting the long-term effects of hunting on plant species composition and diversity in tropical forests. Biotropica 39: 372–384. Nepstad, D. C., C. M. Stickler, B. Soares-Filho, and F. Merry. 2008. Interactions among Amazon land use, forests and climate: Prospects for a near-term forest tipping point. Phil. Trans. R. Soc. B. 27: 1737–1746. Ninan, K. N. (ed.). 2009. Conserving and Valuing Ecosystem Services and Biodiversity: Economic, Institutional, and Social Challenges. London: Earthscan Publications. Nobre, C. 2008. Interview, “All Eyes on the Amazon.” Nature 452, no. 7184 (March 12, 2008): 137 Parmesan, C., and G. Yohe. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42. Pearce, D., F. E. Putz, and J. K. Vanclay. 2003. Sustainable forestry in the tropics: Panacea or folly? Forest Ecology and Management 172: 229–247. Peres, C. A., and E. Palacios. 2007. Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: Implications for animal-mediated seed dispersal. Biotropica 39: 304–315. Putz, F. E., and K. H. Redford. 2010. The importance of defining “forest”: Tropical forest degradation, deforestation, long-term phase shifts, and further transitions. Biotropica 42: 10–20. Redford, K. H. 1992. The empty forest. Bioscience 42: 412– 422. Redford, K. H., and J. G. Robinson. 1991. Neotropical Wildlife Use and Conservation. Chicago: Univ. of Chicago Press. Robinson, J. G., K. H. Redford, and E. L. Bennett. 1999. Wildlife harvest in logged tropical forests. Science 284: 595–596. Rodrigues, A. S. L., R. M. Ewers, L. Parry, C. Souza Jr., A. Verissimo, and A. Balmford. 2009. Boom-and-bust development patterns across the Amazon deforestation frontier. Science 324: 1435–1437. Rudel, T. K. 2005. Tropical Forests. New York: Columbia Univ. Press. Silva Dias, M. A. F., and 19 other authors. 2002. Cloud and rain processes in a biosphere-atmosphere interaction context in the Amazon region. Jour. Geophys. Res. 107: LBA 39-1–LBA 39-18. doi:10.1029/2001JD000335. Soares-Filho, B. S., D. C. Nepstad, L. M. Curran, G. C. Cerqueira, R. A. Garcia, C. A. Ramos,E. Voll, A. McDonald, P. Lefebvre, and Peter Schlesinger. 2006. Modelling conservation in the Amazon basin. Nature 440: 520–523. Sodhi, N. S., C. H. Sekercioglu, J. Barlow, and S. K. Robinson. 2011. Conservation of Tropical Birds. Oxford, UK: Wiley-Blackwell.

Spray, S. L., and M. D. Moran (eds.). 2006. Tropical Deforestation. New York: Rowman and Littlefield. Stoner, K. E., P. Riba-Hernández, K. Vulinec, and J. E. Lambert. 2007. The role of mammals in creating and modifying seedshadows in tropical forests and some possible consequences of their elimination. Biotropica 39: 316–327. Stoner, K. E., K. Vulinec, S. J. Wright, and C. A. Peres. 2007. Hunting and plant community dynamics in tropical forests: A synthesis and future directions. Biotropica 39: 385–392. Terborgh, J. 1974. Preservation of natural diversity: The problem of extinction prone species. Bioscience 24: 715– 722. ———. 1986. Keystone plant resources in the tropical forest. In Conservation Biology: The Science of Scarcity and Diversity, M. E. Soule (ed.). Sunderland, MA: Sinauer. ———. 2000. The fate of tropical forests: A matter of stewardship. Cons. Biol. 14: 1358–1361. Tollefson, J. 2008. Brazil goes to war against logging. Nature 452: 134–135. ———. 2010. Amazon drought raises research doubts. Nature 466: 423. Wood, C. H., and R. Porro (eds.). 2002. Deforestation and Land Use in the Amazon. Gainesville: Univ. of Florida Press. Wright, S. J., A. Hernandez, and R. Condit. 2007. The bushmeat harvest alters seedling banks by favoring lianas, large seeds, and seeds dispersed by bats, birds, and wind. Biotropica 39: 363–371. Wright, S. J., and H. C. Muller-Landau. 2006a. The future of tropical forest species. Biotropica 38: 287–301. ———. 2006b. The uncertain future of forest species. Biotropica 38: 443–445. Wright, S. J., K. E. Stoner, N. Beckman, R. T. Corlett, R. Dirzo, H. C. Muller-Landau, G. Nuñez-Iturri, C. A. Peres, and B. C. Wang. 2007. The plight of large animals in tropical forests and the consequences for plant regeneration. Biotropica 39: 289–291. Zahawi, R. A., and K. D. Holl. 2010. Bridging the gap between scientific research and tropical forest restoration: A multifaceted research, conservation, education, and outreach program in southern Costa Rica. Ecological Restoration 28: 143–146.

Website Articles about Hydroelectric Dam Projects in Amazonia https://en.wikipedia.org/wiki/Belo_Monte_Dam http://www.theguardian.com/world/2016/jan/15/brazil-belos-monte-dam-delay-court-indigenous-people http://www.economist.com/news/americas/21577073-having-spent-heavily-make-worlds-third-biggest-hydroelectric-project-greener-brazil http://news.nationalgeographic.com/2015/04/150419-amazon-dams-hydroelectric-deforestation-rivers-brazil-peru/

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Index A acacia (Acacia spp.): 193–4, 250, 256; bull’s horn, 193; swollenthorn, 193 acouchy (Myroprocta spp.): 331 adaptation: 88, 96, 117–9, 121, 157, 161, 173, 189, 213, 215, 229–30, 250, 367 adaptive radiation: 120–5, 172, 277, 288, 297, 320, 345, 356 agave: 256 agouti: 37, 39, 48, 58, 62–3, 102, 144, 150, 156, 163, 216, 322, 329–31, 367, 370; Central American (Dasyprocta punctata), 62–3, 330. See also rodent agriculture: 27, 75, 87, 95, 97, 102, 255, 316, 365–71, 376–8, 380, 385–7; crops, 369–70; large-scale, 366, 371, 387; nonindigenous farmers, 370; slash-and-burn (swidden), 111, 366, 369–70; tropical soils and, 87; successional crop system, 111 aguajale: 213. See also palm, Moriche air plant: 33, 40, 50, 52–3. See also epiphyte Alder, Andean (Alnus acuminata): 385 alfisols: 85–6 algae: 56, 88, 169, 245, 336–7 algae: 56, 88, 169, 245, 336–7, alkaloid: 83, 90, 186, 188–9, 191–2, 196, 357, 373–5 alligator: 217–8; American (Alligator mississippiensis), 17, 218. See also crocodile Alpaca (Lama guanicoe pacos): 248 Alta Floresta, Brazil: 325, 381 altiplano: 129, 243–5 Amacuro Delta: 207 Amazon (River): 23, 25, 34, 83, 90, 93, 115, 129–30, 205, 207–10, 213 amazon [bird]: 283. See also parrot Amazon Center for Environmental Education and Research (ACEER): 23–4 Amazon(ia): 9, 12, 18, 20, 23, 27, 65, 86–7, 93, 129, 131, 205, 212–3, 384; Basin, 9, 18, 30–1, 130, 205, 208, 213, 239, 243, 383; Basin: climate in, 30, 32–3, 83; deforestation in, 27, 378–80, 383–5; drought, 78–9; fire in, 103; fish in, 169, 228; forests, 39, 76–7, 87, 169; human occupation of, 365–8; Planalto, 86: precipitation (rainfall), 27, 30–3, 78, 83, 383; primates in, 380, 385; soils, 83, 85–8, 103, 252; species richness in, 134–6; succession, 98, 102–3 amino acid: 47, 174, 176, 191, 193; canavanine, 191, L-DOPA, 191; proline, 174; tyrosine, 174 amphibian: 133, 136, 138, 150, 186, 346, 355–7 anaconda: 180, 215–6, 342, 350; Green (Eunectes murinus), 216, 257, 351; Yellow (Eunectes notaeus), 216–7 Andagoya, Colombia: 33 Andes (Mountains): 19, 37, 102, 115, 128–31, 141, 208–10, 235–6, 243–8, 365–6, 375; and geographic isolation, 129; soils in, 85, 90; source of Amazon, 207 Angel Falls: 206–7 Angel, J.: 206 Ani: Greater (Crotophaga major), 222, 293; Smooth-billed (Crotophaga ani), 293. See also cuckoo

anole: 352–3; Anolis, 150–1, 352; Berthold’s Bush (Polychrus gutturosus), 355; Green Anole (Anolis carolinensis), 151; Green Tree (Norops biporcatus), 353; Slender (Norops limifrons; N. fuscoauratus), 353. See also lizard; iguana ant followers: 281, 300, 302. See also antbird ant-plants (myrmecophytes): 192 ant: Acromyrmex, 175; army (Eciton burchelli; Labidus praedator), 26, 145, 177–9; Atta, 175–7, 191; Azteca, 109–10, 193; fungus garden (Atta cephalotes), 62, 174–7, 179, 191; Giant Tropical or Bullet (Paraponera clavata), 358; leaf-cutter, 24, 39–40, 62, 110, 174–7, 189; Pseudomyrmex ferruginea, 193–4 antbird: 145,177–9, 263, 281, 289, 297, 300–3; Bicolored (Gymnopithys bicolor), 301–2; Blackish (Cercomacra nigrescens), 129–30; Chestnut-backed (Poliocrania [Myrmeciza] exsul), 66; Dusky (Cercomacra tyrannina), 129–30; Formicariidae, 178, 297, 300–1; Myrmotherula, 300; Ocellated (Phaenostictus mcleannani), 178, 303; Spotted (Hylophylax naevioides), 144, 301; typical (Thamnophilidae), 178, 297, 300–1; White-cheeked (Gymnopithys leucapsis), 178, 302 anteater: 92, 150, 335, 337–8; Giant (Myrmecophaga tridactyla), 159–60, 257, 338; Silky or Pygmy (Cyclopes didactylus), 338. See also tamandua antpitta: 239, 263, 297, 300–3; Chestnut-crowned (Grallaria ruficapilla), 302; Chestnut-naped (Grallaria nuchalis), 297; Giant (Grallaria gigantea), 238; Jocotoco (Grallaria ridgelyi), 136; Streak-chested (Hylopezus perspicillatus), 302; Tawny (Grallaria quitensis), 246 antshrike: 300; Barred (Thamnophilus doliatus), 301; Black-throated (Frederickena viridis), 382; Castelnau’s (Thamnophilus cryptoleucus), 146; fly-catching (Thamnomanes), 301; Great (Taraba major), 301 antthrush: 263, 297, 300–1; Black-faced (Formicarius analis), 301–2; Rufous-breasted (Formicarius rufipectus), 301 antvireo, 300 antwren: 300; Amazonian Streaked (Myrmotherula multostriata), 300; Dot-winged (Microrhopias quixensis), 300. See also antbird anuran: 60, 136, 239, 355–7. See also frog; toad aposematic (warning) coloration: 185–7, 198, 202–3 aracari (Pteroglossus): 16, 24, 62, 109, 163, 186, 273, 275; Collared (Pteroglossus torquatus), 274, 293; Pale-mandibled (Pteroglossus erythropygius), 274. See also toucan; toucanet Arapaima or Pirarucu (Arapaima arapaima): 228 arecife: 251 Argentina: 18, 244, 247–8, 250, 292 Arima Valley, Trinidad: 22, 72, 149, 287 armadillo: 37, 131–2, 335, 338; Giant (Priodontes maximus), 338; Nine-banded (Dasypus novemcinctus), 131, 338 Arowana (Osteoglossum bicirrhosum): 228 arrested litter: 88 arrow poison: 186, 357, 367, 372, 374 arthropod: 26, 81, 110, 137–8, 143, 150, 190, 194, 213, 228, 288–9, 322, 324, 326, 336, 363–4, 367

418

index

arum: 39, 53; ornamental (Monstera deliciosa), 52. See also philodendron Asa Wright Nature Centre, Trinidad: 21–2, 25, 288 Askins, Robert A.: 146–7 Asner, G.: 378, Atacama Desert: 20, 115, 243–4 Atlantic Forest: 27, 377 avocado: 102, 210 B bacteria: 50, 56, 75, 77, 79, 81–2, 88–9, 93, 176, 187–8, 225, 253, 336 Baker, I: 195 bamboo: 143, 145, 237 Banana (Musa sapientum): 86–7, 93, 96, 111, 210, 361, 365, 369–70 Bananaquit (Coereba flaveola): 262. See also tanager bancos (tree grove): 256 barbet: 263, 275; Black-girdled (Capito dayi), 275; Prong-billed (Semnornis frantzii), 276; Red-headed (Eubucco bourcierii), 275; Toucan (Semnornis ramphastinus), 276 barbtail: 298 barbthroat: 278. See also hummingbird Barro Colorado Island (BCI), Panama: 36, 99–100, 106, 134–6, 177, 188, 192, 381 basilisk: 149, 352–3; Common Basilisk (Basiliscus basiliscus), 383; Green Basilisk (Basiliscus plumifrons), 353; Helmeted Basilisk (Corytophanes cristatus). See also iguana bat: 61, 123–4, 148, 150, 156, 159–61, 242, 320, 330; adaptive radiation in, 121–3, 146; Bulldog (Noctilio leporinus), 122–3; Chestnut Short-tailed (Carollia castanea), 122; Vampire (Desmodus rotundus), 123; echolocation by, 121–2; False Vampire (Vampyrum spectrum), 122; fruit dispersal by, 163; fruit-eating, 48; ghost (Diclidurus spp.), 123; Greater Tent-making (Uroderma bilobatum), 319; Greater White-lined (Saccopteryx bilineata), 122; Honduran White Bat (Ectophylla alba), 124; kapok pollinating, 171; leaf-nosed (Phyllostomidae), 156; Long-nosed or Proboscis (Rhynchonycteris naso), 124; microchiroptera, 121, 161; nectarivorous, 174; Neotropical Pygmy Fruiteating (Dermanura phaeotis), 121; pollination by, 45–6, 107, 170–1, 173–4; as seed disperser, 108; small leaf-nosed (Phyllostomidae), 123; Sucker-footed (Thyroptera tricolor), 124; Vampire (Desmodus rotundus), 12; Wrinklefaced (Centurio senex), 121 Bates, Henry Walter: 34, 87, 199, 219, 263 batrachotoxins: 186, 365 Baywing, Grayish (Agelaioides badius): 304 Bazzaz, F.: 99 BCI (Barro Colorado Island, Panama): 36, 99–100, 106, 134–6, 177, 188, 192, 381 Beagle, hms: 120, 132, 244, 261 bean: 102, 111, 210; common (Phaseolus vulgaris), 111 Bear, Spectacled (Tremarctos ornatus): 242–3 Beard, J. S.: 250 bee: 171, 390–1; African Honey (Apis mellifera scutellata), 391; euglossine, 56, 171, 380–1; Eulaema polychroma, 171;

Western Honey (Apis mellifera), 391 beech: 134, 292; southern (Nothofagus), 292 beetle: 46, 108, 134, 137, 150, 171, 174, 242, 358, 380; Cyclocephala spp., 174; Elephant (Megasoma elephas), 359–60; Harlequin Longhorn (Acrocinus longimanus), 359; Hercules (Dynastes hercules), 359–60; leaf(Chrysomelidae), 137; Rhinoceros (Megasoma spp.), 359–60; scarab, 360; stag, 360 Belém, Brazil: 31, 33, 210 Belize Association of Traditional Healers: 373 Belize City, Belize: 34 Belize, 18, 85, 121, 205, 250, 252; savanna in, 253–4 bellbird: 169, 286–8; Bare-throated (Procnias nudicollis), 287; Bearded (Procnias averano), 159, 287; Three-wattled (Procnias tricarunculata), 287; White (Procnias alba), 287 Belo Monte Dam: 384 Belt, Thomas: 130 Beltian bodies: 194 Benson, W. W.: 197–9 bentbill: 126; Southern (Oncostoma olivaceum), 126. See also flycatcher Bermingham, E.: 140 Bierregaard, R. O.: 380 biodiversity: 21, 27, 50, 73, 75, 81, 84, 88, 104, 117, 133–6, 371–2, 377, 380–8. See also species richness biogeochemical cycling: 79, 81–5, 91 biogeography: 29, 113–6, 130, 208 Biological Dynamics of Forest Fragments Project (BDFFP): 380–2 Biological Species Concept (BSC): 113, 119–20 Biome: 21, 29, 32–3, 387 bioprospecting: 202 Bird Caye, Belize: 232 birds: 262–318 blackbird: 303, 306; Oriole (Gymnomystax mexicanus), 303; Redbreasted (Sturnella militaris), 303; Red-winged (Agelaius phoeniceus), 303; Scarlet-headed (Amblyramphus holosericeus), 260; Unicolored (Agelasticus cyanopus), 303–4; Yellow-hooded (Chrysomus icterocephalus), 306 blossomcrown: 276. See also hummingbird Blue Creek Village, Belize: 365 Bolivia: 18, 236, 244, 252, 259. See also Pantanal borhyaenoids: 133 botfly: 328, 389–90; Human (Dermatobia hominis), 390 Boto: 213. See dolphin Bottlebrush, Common (Melaleuca citrina): 46 Brazil National Institute for Research in Amazonia (INPA): 380 Brazil: 18, 20, 25, 27, 30–1, 77, 105, 113, 131, 134, 138, 236, 250, 252, 254, 256, 259, 261, 297, 365, 368, 370–1, 373, 376–81, 384. See also Manaus; Pantanal Brazilian Shield: 87, 208 Brightsmith, FD.: 91 bromeliad (Bromeliaceae): 24, 39, 53–5, 57, 71, 119, 146, 237, 242, 245, 247–8, 251, 254–5, 300, 307, 356. See also pineapple Brower, L.: 198

index

brushfinch: 307; Chestnut-capped (Arremon brunneinucha), 307 bug: 26, 193, 242, 288–9, 373; Peanut-headed (Fulgora laternaria), 360 bunting: 307, 315; Indigo (Passerina cyanea), 318 buriti. See palm, Moriche koi. See palm, Moriche business as usual (BAU) model: 385 butterfly: 360–2; ant-butterfly, 361; Batesian mimicry by, 199–202; Blue Morpho (Morpho didius), 64; brush-footed (Nymphalidae), 362; Caligo eurilochus, 199; clearwing satyr (Cithaerias spp.), 362; cracker (Hamadryas spp.), 64–5; Dryas iulia, 196; heliconid 130, 196–9, 202–3; Heliconius spp. 18, 64–5, 119, 191, 196–7, 198–9, 202, 360–1; Heliconius cydno, 202; Heliconius doris, 197, 199; Heliconius eleuchia, 202; Heliconius elevatus, 202; Heliconius erato, 119, 196, 198, 200, 202; Heliconius melpomene, 119, 198, 200, 202; Heliconius timareta, 202; Malachite (Siproeta stelenes), 362; Mechanitis isthmia, 198; Melinaea spp., 195; migration in, 242; Monarch (Danaus plexippus), 198; morpho (Morpho spp.), 64, 181, 361; Owl (Caligo memnon), 361; Phoebis spp., 361; swallowtail, 361–2; Thisbe irenea, 194; whites and sulphurs (Pieridae), 361; Zebra Longwing (Heliconius charithonia), 18, 196. See also caterpillar; moth Byrsonima crassifolia: 251 C caatinga: 99, 250, 256 caboclo: 210, 370, 373 cacao (Theobroma cacao): 22, 44, 111, 210, 369, 371 cacique: 303–7; Yellow-rumped (Cacicus cela), 304–5 cactus: 39, 53, 248, 254, 256; Lophophora spp., 375 caffeine: 188, 371 caiman: 17, 204, 210, 215–9, 259, 304; Black (Melanosuchus niger), 218; Broad-snouted (Caiman latirostris), 219; Common or Spectacled (Caiman crocodilus), 218, 257; Cuvier’s Dwarf (Paleosuchus palpebrosus), 219; Schneider’s Dwarf (Paleosuchus trigonatus), 219; Yacare or Paraguayan (Caiman yacare), 218–9, See also crocodile calcium oxalate: 188 calcium: 53, 73–4, 82–5, 87, 93, 252, 366 Campbell, J. A.: 348, campesino: 373 campo rupestre: 250 Canaima Falls, Venezuela: 89 canastero: 298 candela or candellillo. See piper canid: 344. See also dog; fox; wolf cannabidiol: 188 Canopy Tower, Panama: 21, 23, 25, 387 canopy walkway: 23–5 capuchin. See monkey Capybara (Hydrochaeris hydrochaeris): 131–2, 214–5, 257, 260, 330–1, 367, 370; Lesser (Hydrochaeris isthmius), 214. See also rodent caracara: 221, 312; crested (Caracara spp.), 312; Southern Crested (Caracara plancus), 313; Yellow-headed (Milvago chimachima), 312–3

419

Carbon Dioxide: 73–7, 93, 379, 383 carbon: 73–8, 229–30, 379, 383, 385; credit, 385; cycling, 383; fixation, 73; loss from deforestation and fire, 77; loss from river outgassing, 77; seasonal flux and loss of, 76–7; sequestration, 28, 377; sink, 74–9, 383; source, 76, 79, 81, 383 cardinal: 279, 307; Red-crested (Paroaria coronata), 279 Caribbean: 16–8, 37, 100, 207, 239, 242–4, 250–1 Carvajal, Gaspar de: 365 Casearia corymbosa, 163; Casearia sylvestris: 251 cassava. See manioc cat: 132–3, 150, 148, 184–5, 341–4 Catbird, Gray (Dumetella carolinensis): 316 caterpillar: 80–1, 149, 185, 187, 191, 194–8, 202–3, 336; False Sphinx Moth (Pseudosphinx tetrio), 187; myrmecophilous, 194. See also butterfly; moth catfish (order Siluriformes): 169–70, 228–9, 259; Corydoras spp. 228; Vandellia cirrhosa, 229 cattle ranching: 251, 376–9, 387 cauliflory: 44–5, 174 Cavy, Patagonian: 261 cecropia (Cecropia spp.): 67, 108–10, 189, 192–4, 251, 254, 269–70, 274, 280, 310, 316, 335–6, 382; Cecropia obtusifolia, 104, 110; Cecropia peltata, 188 Cenozoic era: 128, 206, 253, 256 centipede: 138, 190, 358, 363; Amazonian Giant (Scolopendra gigantea), 363 Central America: 90, 100, 102, 110–11, 135–6, 159, 205, 235–6, 244, 247, 250–2, 366, 368 cerrado: 20, 27, 250–1, 254–6 chachalaca: 264–5; Plain (Ortalis vetula), 264; Rufous-vented (Ortalis ruficauda), 265. See also curassow; guan Chaco: 250 Chan Chich Lodge, Belize: 25, 267 characins (family Characidae): 169–70, 228 Chat, Yellow-breasted (Icteria virens): 316 chiggers: 389 Children’s Eternal Rainforest, Costa Rica: 242 Chile: 18, 20, 25, 115, 244, 247–8, 292, chinchilla (Chinchilla spp.): 132, 248, 330. See also rodent chiropterophily: 173–4 chlorophonia: 306–7; Blue-naped (Chlorophonia cyanea), 307. See also tanager Chocó: 135, 186, 236 cicada (order Hemiptera): 60–1 Cinchona: 239, 373 cinclodes: 298 Ciudad Bolívar, Venezuela: 207 Clark, D.: 57 climate change: 28, 37, 74, 78–9, 93, 107, 128, 140, 375–8, 383–4, 387 climate: 16–21, 28–32, 48, 85, 106, 138, 140–2, 150, 153, 244–5, 247, 250–2, 256. See also climate change Clusia: 245 coati / coatimundi: 36–7, 58, 102, 159, 177, 339–40; South American coati (Nasua nasua), 339; White-nosed coati (Nasua narica), 339

420

index

coca / cocaine: 188, 316, 374–5 Coca Cola: 375 Cocha Cashu Biological Station, Peru: 105, 135–6, 160 cock-of-the-rock: 166, 168–9, 189, 285–6, 288; Andean (Rupicola peruvianus), 239–40; Guianan (Rupicola rupicola), 164–5, 239, 286 cockroach: 91, 150, 358–9; Giant (Blaberus giganteus), 359; Megaloblatta blaberoides, 358 Cockscomb, Belize: 342 coevolution: 155–79, 181–203 coffee (Coffea spp.): 188, 239, 371–2 Coley, P.: 188, 192 Colinvaux, P. A.: 130 collpa: 90–1, 283 Colombia: 18, 25, 135, 141, 205, 236, 244, 246, 250, 252, 256, 371, 375; bird species richness in, 136, 138. See also llanos commensalism: 155, 359 competition: 42, 53, 96, 106, 108–9, 116, 125, 133, 141, 146–50, 153, 155, 157–8, 160, 163–5, 168, 189, 252, 279, 281, 289, 300, 306; interspecific, 96, 125, 141, 146–9, 153, 160, 281. See also interspecific competition hypothesis competitive exclusion: 146 Condor: Andean (Vultur gryphus), 248–9, 310; California (Gymnogyps californianus), 310 conebill: 279, 281; Giant Conebill (Oreomanes fraseri), 245, 247. See also tanager Connell, J. H.: 153 Convention for International Trade in Endangered Species (CITES): 215–7, 320, 329, 335, 339 convergence: 200, 300 cooperative behavior: 158, 288, 293 Coquette, Rufous-crested (Lophornis delattrei): 277–8. See also hummingbird coral reef: 153, 229–30, 232 cordillera: 244–5 Cormorant, Neotropic (Phalacrocorax brasilianus): 222 corn: 73, 102, 111, 210, 369 coronet: 276. See also hummingbird Costa Rica: 12, 18, 39, 55, 85, 90, 111, 118–9, 134, 136, 148–9, 152, 158, 163, 172, 175, 191, 195, 198, 205, 236–7, 242, 247, 356; bats in, 122. See also La Selva Biological Station cotinga: 285–6; Lovely (Cotinga amabilis), 144, 285; Spangled (Cotinga cayana), 24. See also bellbird; cock-of-the-rock; fruitcrow; fruiteater; piha; umbrellabird Cowbird, Giant (Molothrus oryzivorus): 306 Coyote (Canis latrans): 344 crab: 55 Cracraft, J.: 115–6 Cretaceous: 141, 177, 219, 345 crocodile (crocodilian): 150; 216–9; American (Crocodylus acutus), 17, 218; Cuban (Crocodylus rhombifer), 218; Morelet’s (Crocodylus moreletii), 218; Orinoco (Crocodylus intermedius), 218. See also alligator; caiman crop: 36, 55, 87, 111, 169, 190, 210, 254–5, 365–6, 369–71, 378, 385 Croton: 194

cryptic coloration (crypsis): 180–5, 296 ctenosaur (Ctenosaura spp.): 352–4. See also iguana Cuba: 115, 252, 318 cuckoo: 178, 225, 222, 293–4, Guira (Guira guira), 293–4; Rufous-vented Ground- (Neomorphus geoffroyi), 294; Squirrel (Piaya cayana), 294, 296. See also ani Cueva del Guácharo, Venezuela: 162 Cuipo (Cavanillesia platanifolia): 34 curare (Curarea spp. [Chondrodendron spp.]): 188, 365, 374 curassow: 48, 130, 144, 156, 163, 166, 264–5; Bare-faced (Crax fasciolata), 265; Great (Crax rubra), 166; Helmeted (Pauxi pauxi), 264. See also chachalaca; guan Curatella americana: 251 cyanohydrins: 197 Cypress, Bald (Taxodium distichum): 18 Cypress, Montezuma: 42 D dacnis: 279, 281. See also tanager damselfly, helicopter (family Pseudostigmatidae): 182 Darién, Panama: 25, 102 Darwin, C.: 12, 21, 39, 56, 115–7, 120, 132, 134, 138, 163, 164, 171, 244, 261, 287, 360 decomposer food web: 75, 80–1 decomposition: 41, 43, 76, 79, 81–2, 84–5, 87–9, 93, 131, 191, 236, 253, 348, 383 deer: 132, 157, 177, 333; Gray Brocket (Mazama gouazoubira), 334; Marsh (Blastocerus dichotomus), 259, 334; Pampas (Ozotoceros bezoarticus), 261; Red Brocket (Mazama americana), 259, 334; White-tailed (Odocoileus virginianus), 254, 333 defense compounds (allelochemicals): 89, 177, 188–9, 191–2, 194–8, 202, 328, 336, 372–3; benzaldehyde, 190; hydrogen cyanide, 190. See also alkaloid; amino acid; calcium oxalate; glycoside; mimicry; phenolic; tannins; terpenoids deforestation: 27, 32, 74, 102, 318, 377–9, 381, 383–7; carbon loss from, 77 DeVries, P. J.: 136, 194–5 Dial, R.: 150 Dick, C.: 140 Dieffenbachia spp.: 39 Dipper: White-capped (Cinclus leucocephalus), 248 Dirzo, R,: 380 disease: 123, 202, 359, 365, 368, 375, 389 disturbance: 21, 37, 40–1, 94–112, 153, 230 diversity gradient: 13, 138, 140, 150; latitudinal (LDG), 138 DNA: 81, 116, 120, 139, 263–4, 273, 275, 301, 306–7; mitochondrial, 120; nuclear, 120 Dobzhansky, T.: 138–41 dog: 132, 335, 344, 390; Bush (Speothos venaticus), 344; Shorteared (Atelocynus microtis), 344 Dogwood, Flowering: 40 Dolphin: Pink River or Boto (Inia geoffrensis), 213–4; Gray or Tucuxi (Sotalia fluviatilis), 214 domatia: 192–3

index

Donacobius, Black-capped (Donacobius atricapilla): 222 dove (Columbiformes): 48, 156, 267–8; Ruddy Ground(Columbina talpacoti), 268; White-throated Quail(Zentrygon [Geotrygon] frenata). See also pigeon Doyle, Sir A. C.: 206 drought: 27, 35–6, 75, 78–9, 100, 102–4, 106–7, 213, 250, 252, 257, 378, 383–4 Duck: Muscovy (Cairina moschata), 222; Torrent (Merganetta armata), 248–9 Duellman, W.: 136 E eagle: Black Hawk- (Spizaetus tyrannus), 311; Black-and-white Hawk- (Spizaetus melanoleucus), 311; Crested (Morphnus guianensis), 312; Harpy (Harpia harpyja), 116, 262, 308, 311–3; Ornate Hawk- (Spizaetus ornatus), 311–2 earthcreeper: 298 echolocation: 121–2, 160, 162 ecological life zone: 19–20, 29–30, 236, 242 ecosystem, noanalog: 28 ecotourism (ecotourist): 21, 23, 136, 205, 219, 224, 236, 241, 257, 260, 283, 343, 367, 374, 387 Ecuador: 12, 18–9, 25, 39, 89, 115, 130–1, 136, 140, 202, 205, 208, 236, 244–8, 368; bird species richness in, 136 edaphic: 30, 85, 251, 253 edge effects: 382 Eel, Electric (Electrophorus electris): 228 egret (Ardeidae): 210, 217, 223, 257, 260; Great (Ardea alba), 260. See also heron El Niño/Southern Oscillation (ENSO): 35–7, 78, 103, 106, 328, 378, 383 El Salvador: 18 Emmons, L. H.: 121, 150 Empty Forest, The (Redford): 380 endangered species: 27–8, 214–5, 217, 219, 285, 320, 323–6, 329, 335, 338–9, 377 endemic species: 27, 115, 239, 247, 251, 254–6, 263, 276–7, 288, 371, 377 endemism: 27, 115–6, 128, 130–1, 139, 239, 387; regional, 115; taxonomic, 115 Eocene: 121, 131, 141 epiphyll: 44, 56, 88 epiphyte: 18, 33, 39–40, 50–7, 67, 88, 98, 100, 102, 110, 135, 143, 155, 192, 235, 238–9, 245, 307. See also air plant Erwin, T.: 136–8 Erythroxylum coca: 374; Erythroxylum novogranatense, 364 Espeletia: 241–2, 247 ethnobotany: 188, 202, 372–5 euphonia: 54–5, 69, 306–7, 316; White-vented (Euphonia minuta), 54; Violaceous (Euphonia violacea), 307. See also tanager evapotranspiration: 29, 31–2, 140, 236, Everglades: 17, 250, 256–7, 259 Evolution in the Tropics (Dobzhansky): 138 evolution: 59, 93, 110, 113–33, 138, 140–1, 144–5, 147–9,

421

157, 164, 206, 245, 253; convergent, 113, 133, 177; and speciation, 120. See also coevolution; evolutionary arms races; speciation; species richness evolutionary: arms races: 181–203; fitness, 117; tradeoff, 189 Ewel, J.: 111 exploitationist hypothesis: 193 Explorama, Peru: 25 Explorer’s Inn Reserve, Peru: 136 extinction: 27, 117, 119, 130, 133, 138–9, 141, 149–50, 153, 253, 284, 379, 383, 385, 387 extrafloral nectaries (EFN): 110, 173, 192–4, 197 F fairy: 276. See also hummingbird falcon: 221, 312; Bat (Falco rufigularis), 145, 308, 312; forest(Micrastur spp.), 301, 308, 312; Laughing (Herpetotheres cachinnans), 187, 312–3; Lined Forest- (Micrastur gilvicollis), 313 Fearnside, P. M.: 384 Feinsinger, P.: 172 feline: 148, 341–4. See also cat female preference model: 168 fern: 39–41, 53, 57, 134, 138, 192, 236–7, 245, 247; tree, 236–7 ferralsols: 85 Ferraz, G.: 382 fig (Ficus spp.): 52, 140, 157–8, 176, 274; strangler, 52, 113, finch: Darwin’s: 120–1, 279; diuca-, 279; grass-, 279; inca-, 279; Large Ground (Geospiza magnirostris), 121; sierra-, 279, warbling-, 279 fire: 20, 77, 95, 98, 102–4, 250–5, 257, 369–70, 377–8, 381, 384, 386 firecrown: 276. See also hummingbird fish: 228–9, as seed dispersers, 169–70; fruit-consuming, 170 FitzRoy, Captain: 244 flagelliflory: 174 flamingo: 248; Andean (Phoenicoparrus andinus), 248–9; Chilean (Phoenicopterus ruber), 248–9; James’s (Phoenicoparrus jamesi), 248 flash colors: 356 flatworm: 55 Fleming, T. H.: 159 Flicker, Campo (Colaptes campestris): 252. See also woodpecker floating meadows: 212 flood cycle: 87, 89, 169–70, 205, 209–13, 228, 365–6, 384 flowerpiercer: 144, 173, 276, 279; Indigo (Diglossa indigotica), 173. See also tanager flowers: 46–7 fly: Lantern (Fulgora laternaria): 360; sand (family Ceratopogonidae), 390. See also botfly; leishmaniasis flycatcher: tyrant, 12, 120, 124–9, 159, 263, 288–9, 297–8, 304, 315; Amazonian Royal (Onychorhynchus coronatus), 128. Black-capped Pygmy- (Myiornis atricapillus), 126; Boat-billed (Megarynchus pitangua), 125–6; Common Tody- (Todirostrum cinereum), 126; flatbill, 148; Forktailed (Tyrannus savana), 128, Gray-capped (Myiozetetes granadensis), 126; Least (Empidonax minimimus), 319;

422

index

Ochre-bellied (Mionectes oleagineus), 127, 159; Piratic (Legatus leucophaius), 304; Rusty-margined (Myiozetetes cayanensis), 126; Short-crested (Myiarchus ferox), 124; Social (Myiozetetes similis), 126; Streaked (Myiodynastes maculatus), 66; Sulphury (Tyrannopsis sulphurea), 212; Yellow-throated (Conopias parvus), 126. See also bentbill; kiskadee; spadebill; tyrant flying fox (megachiroptera): 161 foliage-gleaner: 298; Scaly-throated (Anabacerthia variegaticeps), 299 foliar nectaries: 194 food chain, grazing: 81 food web: 75, 81, 101, 194, 230, 380, 383; decomposer, 81 forest: cloud, 19, 235–7, 239, 247; dry, 20, 27, 33, 130, 191, 250, 253, 380; degradation of, 377–8, 383, 385–6; deciduous, 30, 32–3, 157, 256; demographics of, 104; elfin, 235–6, 245; equilibrium, 100, 153, 382; extreme rain, 33; flooded, 48, 169–70, 213, 228; fragmentation of, 27, 109, 320, 326, 377, 380–3, 387; gallery (igapo), 87, 89–90, 134, 205, 209; gaps in, 40, 56–7, 98, 100–1, 145; monsoon, 33; plantation, 371; rain, 29–34, 39–41, 73–9, 95; regeneration of, 98, 102, 370, 379; restoration of, 384–6; tropical seasonal or moist, 30, 33–5. See also jungle; mangrove; várzea Foster, R. B.: 36–7, 100, 106, 134–5 fox: 344; Crab-eating (Cerdocyon thous), 260, 344; Gray (Urocyon cinereoargenteus), 254, 344 frangipani (Plumeria spp.): 46 French Guiana: 18 frequency-dependent selection: 150 frigatebird: 229, 232; Magnificent (Fregata magnificens), 232 frog: 60, 119, 131, 136, 184–6, 188, 239, 355–7, 365, 382; Canal Zone Tree (Hypsiboas rufitelus), 137; Central American Common Tink (Eleutherodactylus [Diasporus] diastema), 356; Dendrobates spp., 186; Eleutherodactylus spp, 356; Fleischmann’s Glass (Hyalinobatrachium fleischmanni), 357; glass, 357; Leptodactylus spp., 131, 357; Phyllobates spp., 186; Phyllobates terribilis, 186; Phyllomedusa spp., 382; poisondart, 185–6, 356–7; Red-eyed Tree (Agalychnis callidryas), 356–7; Savage’s Thin-toed (Leptodactylus savagei), 357; Small-headed Tree (Dendropsophus microcephalus), 356; Strawberry Poison-dart (Oophaga pumilio), 356; tree, 55, 60, 119, 136–7, 183, 355–7; tree (Hypsiboas semilineatus), 183. See also anuran; toad frugivore: 157, 159–60, 165, 195, 274, 283 fruitcrow: 285; Purple-throated (Querula purpurata), 158; Redruffed (Pyroderus scutatus), 286 Fruiteater, Green-and-black (Pipreola riefferii): 285. See also cotinga fruits: 47–9; 163–4 Fundação Nacional do Indio (FUNAI): 368 fungi: 53, 55–6, 62, 75, 79, 81–4, 87, 93, 106, 174–7, 179, 187–8, 191–2, 253, 375. See also mycorrhizae G Galápagos: 114–5, 120, 279 gallery forest. See forest

Gallinule, Purple (Porphyrio martinicus): 257 Gallon Jug, Belize: 372 Garwood, N, C.: 35 gecko: 355; Yellow-headed (Gonatodes albogularis), 355 gene flow: 120, 128 genes: 116–8, 128 Gentry, A. H.: 134–5 Gilbert, L. E.: 197 Glander, K. E.: 195 glycosides: cardiac 191, 198; cyanogenic, 190–2, 196–7; phenolic, 192 glyptodont: 131–2 gnateater: 297 goldfinch: 306–7 gomphotheres: 48, 119, 132 Gondwana: 177, 229 Goulding, M.: 169 gourd: 102 Gran Sabana: 206 grasses: 19, 103–4, 171, 211–2, 246–54, 256, 259, 261, 386; Andropogon gayanus, 253; Brachiaria humidicola, 253; Echinochloa polystachya, 212; Hymenachne spp., 256; Leersia spp., 256; Luziola spp., 256; Panicum spp., 256; Paspalum repens, 212; Saccharum spontaneum, 104; Stipa brachychaeta, 261; Stipa trichotoma, 261; tussock, 19, 247–9 grasshopper: Chromacris trogon, 183 grassland: 20, 27, 30, 32, 73, 91, 176, 248, 250, 252–4, 257, 261, 303, 312, 383, 386. See also pampas; paramo; puna; savanna Great American Faunal Interchange: 131–3 Greater Antilles: 17, 37, 236, 268, 270 greenhouse effect / gas: 76, 93, 383–4. See also Carbon Dioxide Grison: Greater (Galictis vittata): 341; Lesser Grison (Galictis cuja), 341 grosbeak: 307, 315 ground-dove. See dove Guácharo, See oilbird guan: 48, 144, 156, 163, 264; Blue-throated Piping- (Pipile cumanensis), 264–5; Chestnut-bellied (Penelope ochrogaster), 156; Crested (Penelope purpurascens), 381; Horned (Oreophasis derbianus), 264; Red-throated Piping(Piplie cujubi), 264–5. See also chachalaca; curassow Guanacaste (Enterolobium cyclocarpum): 119 Guanacaste, Costa Rica: 175 Guanaco (Lama guanacoe): 248–9, 344 Guatemala: 18, 102–3, 138, 146, 236, 267, 270, 366–7; bird species richness in, 138 Guiana Shield: 85, 87, 90, 206–7 Guinea Pig (Cavia aperea): 132, 214–5, 330 Gulf of Paria: 207 Gynoxys: 245 H Hadley cells: 31 Haffer, J.: 116, 129–30, Haiti: 357

index

hallucinogens: 50, 191, 365, 372–5 Hammel, B.: 135 hammock (tree grove): 256–7 Hare, Patagonian: 261 Hart, Robert: 111 Hartshorn, G.: 101, 135 Hatchetfish, Silver (Gasteropelecus levis): 228 hawk-eagle. See eagle hawk: 310–2, 221, 312; Black-collared (Busarellus nigricollis), 221, 224; Broad-winged (Buteo platypterus), 308; Common Black (Buteogallus anthracinus), 310; Great Black (Buteogallus urubitinga), 308, 311; Gray-lined (Buteo nitidus), 220; Roadside (Buteo magnirostris), 310–11; Savanna (Buteogallus meridionalis), 310–11; Swainson’s (Buteo swainsoni), 308, 315; White (Pseudastur [Leucopternis] albicollis), 310–11 Hawkins, B.: 140 Headstander, Pearl (Chilodus punctatus): 228 Healing Forest, The (Schultes and Raffauf): 374 Heithaus, E. R.: 149 heliconia (Heliconia spp.): 46–7, 57, 67, 96, 107, 111, 172, 196; Heliconia psittacorum, 172; Lobster Claw (Heliconia rostrata), 47 Heliconius Genome Consortium: 202 Heliconius. See butterfly helmetcrest (Oxypogon spp.): 241. See also hummingbird Helson, J.: 202 hemiepiphyte: 51–2 herbivore / herbivory: 74, 80, 83, 89, 93, 106, 111, 132, 149, 177, 181, 187–97, 203, 253, 369 hermit: 47, 67, 107, 165, 172–3, 278–9; Long-billed (Phaethornis longirostris), 66–7, 278; Long-tailed (Phaethornis superciliosus), 278–9. Pale-bellied (Phaethornis anthophilus), 47; Saw-billed (Ramphodon naevius), 173. See also hummingbird heron (Ardeidae): 210, 223, 257, 260; Agami (Agamia agami), 224–5; Boat-billed (Cochlearius cochlearius), 224, 263; Cocoi (Ardea cocoi), 223; Capped (Pilherodius pileatus), 223; Great Blue (Ardea herodias), 223; Rufescent Tiger- (Tigrisoma lineatum), 93, 223; Whistling (Syrigma sibilatrix), 223; Zigzag (Zebrilus undulatus), 223–4. See also egret Herrera, R.: 84 Herz, H.: 177 hickory: 32, 85 hillstar: 241, 276; Ecuadorian (Oreotrochilus chimborazo), 241. See also hummingbird Hoatzin (Opisthocomus hoatzin): 212, 224–6, 263 Hoffmann, A.: 373, 375 Holdridge, L. R.: 29–30, 33 Holloway, M.: 77 Honduras: 18, 25, 118, 250, 252–3, 355, 358 honeycreeper: 69, 279, 281, 316; Green (Chlorophanes spiza), 281, Purple (Cyanerpes caeruleus), 281. See also tanager Hopper, Waxtail (Pterodictya reticularis), 189 hornbill: 16, 113; Rhinoceros (Buceros rhinoceros), 113

423

hornero: 298; Rufous (Furnarius rufus), 114, 298 hotshot model: 168 hotspot model: 168 Howe, H.: 163 Hubbell, S. P.: 100, 106, 134–5, 191 human settlement: 365–7 Humboldt, Alexander von: 19, 138, 235–6 humification: 92, 93 hummingbird: 12, 46–7, 54–5, 65–9, 107, 110, 144, 165, 168, 171–3, 236, 240–2, 247–8, 262, 276–9, 315; Bee (Mellisuga helenae) 277; Berylline, 276; Emerald-chinned, 276; Garnet-throated, 276; Giant (Patagonia gigas), 241, 277; Magnificent, 276; Ruby-topaz, 276; Rufous-tailed (Amazilia tzacatl), 172; Sparkling-tailed, 276; Sword-billed (Ensifera ensifera), 241, 277–8. See also barbthroat; blossomcrown; coquette; coronet; fairy; firecrown; helmetcrest; hermit; hillstar; inca; jewelfront; mango; racket-tail; sabrewing; sapphire; spatuletail; starthroat; sunbeam; sylph; topaz; trainbearer; velvetbreast; woodnymph humus: 82–4, 87, 253 hunting and gathering: 367–8 hunting: 27, 215–6, 219, 242, 266, 319–20, 323–6, 334–5, 339, 357, 365, 367–8, 377, 379–80 hurricane: 32, 37, 95, 98, 100, 153, 229–30, 232 hydroelectric dam: 27, 368, 377, 384 hyperdiversity: 138, 141 I ibis: 223, 257, 260; Buff-necked (Theristicus caudatus), 223; Green (Mesembrinibis cayennensis), 223; Scarlet (Eudocimus ruber), 117 ice age: 131 Icteridae: 303–6 igapo. See forest, gallery iguana: 60, 64, 110, 144, 163, 352–5; black, 353; Black Spinytailed or Black (Ctenosaura similis), 354; Forest (Polychrus gutturosus), 355; Galápagos Marine (Amblyrhynchus cristatus), 114; Green (Iguana iguana), 63–4, 352–3; Helmeted (Corytophanes cristatus), 353–4 Inca, Collared (or Gould’s) (Coeligena torquata inca): 240. See also hummingbird insect, stick (or walkingstick) (family Phasmatidae): 182, 184 intermediate disturbance hypothesis (IDH): 153 International Union for Conservation of Nature (IUCN): 215, 238, 320, 323, 325–6, 329, 333–5, 341 interspecific competition hypothesis: 146–50 Intertropical Convergence (ITC): 31–2, 36 intoxicants: 375 invertebrates: 358–64 Iquitos, Peru: 23, 30, 33, 205, 207–10, 365 Irion, G.: 87, 131 isolation: allopatric, 113, 115, 120; geographic (vicariance), 113, 115, 120, 128, 130–1, 245, 267; reproductive, 120 Ivy, Poison (Toxicodendron radicans): 51

424

index

J Jablonski, D.: 139 jacamar: 270, 289; Great (Jacamerops aureus), 271; Rufoustailed (Galbula ruficauda), 199, 271; White-throated (Brachygalba albogularis), 271 jacana: Northern (Jacana spinosa), 227; Wattled (Jacana jacana), 227 Jacaranda mimosifolia: 46 Jaguar (Panthera onca): 14–5, 61, 150, 184, 215, 254, 257, 260–1, 341–4 Jaguarundi (Puma yagouaroundi): 343–4 Janzen, D. H.: 118, 122, 143, 171, 188, 193–4 Jaramillo, C.: 141 Jay: Blue (Cyanocitta cristata), 198; Purplish (Cyanocorax cyanomelas), 254 jewelfront: 276. See also hummingbird Jordan, C. F.: 87, 89 Jordano, P: 158 jungle: 20–1, 97, K Karr, J.: 143 katydid: 150, 182–4, 189; leaf (Stilpnochlora azteca), 182; Orophus conspersus, 182; Peacock (Pterochroza ocellata), 289 Kingbird: Eastern (Tyrannus tyrannus), 126; Tropical (Tyrannus melancholicus), 124–5, 212. See also flycatcher kingfisher: 64, 141–2, 148, 221, 270; American Pygmy (Chloroceryle aenea), 64, 142, 148; Amazon (Chloroceryle amazona), 142, 148, 220; Belted (Megaceryle alcyon), 141; Green (Chloroceryle americana), 142; Green-and-rufous (Chloroceryle inda), 142; Ringed (Megaceryle torquata), 143, 148 Kinkajou (Potos flavus): 36, 61, 117, 119, 339–40 Kiskadee: Great (Pitangus sulphuratus), 125–6, 187; Lesser (Pitangus lictor), 125–6. See also flycatcher Kite: Hook-billed (Chondrohierax uncinatus), 310; Pearl (Gampsonyx swainsonii), 308, 310–11; Slender-billed (Helicolestes hamatus), 259, 310; Snail (Rostrhamus sociabilis), 259, 310; Swallow-tailed (Elanoides forficatus), 310; White-tailed (Elanus leucurus), 310 Knight, D. H.: 99–100, 134 Knoke, T.: 385 Kushlan. J.: 257 L L-DOPA. See amino acid La Niña: 36 La Selva Biological Station, Costa Rica: 57, 100–1, 104, 106, 135–6, 163, 239, 242, 347 Lake Titicaca: 244 Lamar, W. W.: 348 Landsat Enhanced Thematic Mapper Plus: 378 Lantana: 361 Lapwing, Pied (Vanellus [Hoploxypterus] cayanus): 222 laterization: 86

latex: 44, 191 Laurance, W.: 386–7 laurel (Lauraceae): 160, 162, 239, 242, 285; Mountain, 40 Leaching: 79, 83, 86, 89, 252 leaf area index (LAI): 99 leaf litter: 85 leaf: characteristics, 45; drip tip, 40, 45, 83; leaf drop, 34, 40, 110, 112, 152; trichomes on, 55, 191, 198 leaftosser: 298 legume (Fabaceae): 40, 45, 47–9, 88, 111, 136, 139, 176, 191, 239, 261 leishmaniasis: 202, 390. See also fly, sand lek: 164–9, 239, 279, 286–8; concentrated, 164; dispersed, 286 lepidoptera. 360–2. See also butterfy; moth Lesser Antilles: 17, 37, 236 Leuhea seemannii: xx liana: 35, 39, 41, 48, 50–1, 100, 104, 110, 135, 362, 369, 373–4 lichen: 32, 41, 44, 53, 56, 88, 245 Lill, A.: 165 litopterns: 133 liverwort: 53, 56, 88 lizard: 60, 147, 149–51, 239, 332, 347, 352–5, 383; Anolis, 150–1, 352. See also anole; basilisk; gecko; iguana; tegu llama (Lama guanicoe glama): 248 Llanos: 205, 207, 215, 217, 224, 226, 250–1, 256–60, 331, 338 logging: 27, 95, 324, 368, 376–9, 383–5 Lost World, The (Doyle): 206 Lovejoy, T. E.: 143, 380 lowland species attrition: 28 Luchea seemannii: 137 Lungfish, South American (Lepidosiren paradoxa): 229 M macaw: 156, 260, 282–5; Blue-and-yellow (Ara araraura), 253, 284; Chestnut-fronted (Ara severus), 284; Glaucous (Anodorhynchus glaucus), 285; Great Green (Ara ambiguus), 284; Hyacinth (Anodorhynchus hyacinthinus), 156, 260, 282, 284–5; Indigo (Anodorhynchus leari), 285; Military (Ara militaris), 284; Red-and-green (Ara chloropterus), 284; Scarlet (Ara macao), 283–84. Spix’s (Cyanopsitta spixii), 285. See also parrot Machu Picchu: 102, 243–4 Macrauchenia: 133 magnesium: 82–4, 252 maize (Zea mays): 87, 201, 111, 210, 369 malaria: 26, 239, 373, 389 manakin: 62, 148, 152, 156, 159, 162–9, 263, 288, 297; blue (Chiroxiphia spp.), 166–7; Club-winged (Machaeropterus deliciosus), 168; Golden-collared (Manacus vitellinus) 62–3; Golden-headed (Ceratopipra erythrocephala), 159, 167; Pin-tailed (Ilicura militaris), 288; Red-capped (Ceratopipra mentalis), 148; Swallow-tailed (Chiroxiphia caudata), 166; White-bearded (Manacus manacus), 159, 166–8; White-collared (Manacus candei), 288; Wire-tailed (Pipra filicauda), 167, 169

index

manatee: 213–4, 370; Amazonian (Trichechus inunguis), 214; West Indian (Trichechus manatus), 214 Manaus, Brazil: 25, 30, 33, 89–90, 105, 135, 169, 205, 207, 209, 325, 370, 380, 384 mango [hummingbird]: 276; Black-throated (Anthracothorax nigricollis), 172. See also hummingbird mango [plant]: 210, 282 mangrove: 17, 188, 213, 229–32, 383; Black (Avicennia germinans), 230–32; Buttonwood (Conocarpus erectus), 231; forest (or mangal), 43, 91, 207, 229–30, 322, 383; Red (Rhizophora mangle), 229–32; White (Laguncularia racemosa), 231–2 manioc or sweet potato (Manihot esculenta): 111, 190, 210, 365, 369–70 mantis (family Mantidae): 91, 184 Manú National Park: 380, maple: 32, 40, 45, 85, 134, Mara (Dolichotis patagonum): 261. See also rodent Margay (Leopardus wiedii): 147–8, 343 marsupial. See opossum Martin, M. M., 176 Martin, P., 118 martin: 221; Gray-breasted (Progne chalybea), 220; Purple (Progne subis), 221, 317. See also swallow Massenerhebung effect: 245 mata (tree grove): 256 Matamata (Chelus fimbriata): 219 Mato Grosso, Brazil: 376, 378–9 Matte. See Tegu, Common Maya / Mayan: 37, 47, 102–3, 123, 366–7, 375 Mayapple (Podophyllum peltatum): 373 Mendoza, Argentina: 244 Mendoza, E.: 380 Mesozoic era: 128, 206, 216, 225 mestizo: 370, 373 Mexico: 16–8, 26, 32, 102, 110, 256, Miconia (Melasomataceae): 57, 108, 148–9, 254, 281, 288 migration: 156–7, 177, 308, 316, 318; elevational or altitudinal, 242 milkweed: 198–9 Miller, B.: 121 millipede: 138, 190, 358, 363; Nyssodesmus spp., 190 milpa: 369 Milton, K.: 196, 328, mimicry: 64, 187, 197, 199–202, 350, 360; Batesian, 199–202; Müllerian, 202. See also cryptic coloration miner: 298 mineral cycling: 87 minerals: 53, 55, 73, 81–8, 90, 99, 111, 192, 192, 204, 252, 369–70, 377 Minimum Critical Size of Ecosystems Project: 380. See Biological Dynamics of Forest Fragments Project (BDFFP) mining: 377; gold, 368 Miocene: 139, 141, 253, mistletoe (Loranthaceae): 54, 281, 307

425

mite: 337, 389, See also chiggers mollusk: 138–9, 259. See also bivalve; snail monkey: 320–9; Bearded Capuchin, 321; bearded saki (Chiropotes spp.), 324; Black Howler (Alouatta caraya), 326–7; Black Spider (Ateles paniscus), 325; Black-striped Capuchin (Sapajus [Cebus] libidinosus), 321; Black Tuftedear Marmoset (Callithrix penicillata), 328; Black Uakari (Cacajao hosomi), 324; Bolivian Red Howler (Alouatta sara), 326; Brazilian Brown Titi (Callicebus brunneus), 320; Brown Bearded Saki (Chiropotes chiropotes), 324; Brown Howler (Alouatta guariba), 326; Brown Capuchin (Sapajus [Cebus] apella), 321; Brown Titi (Callicebus urubambensis), 320; capuchin (Cebus spp.), 65, 151, 320, 322, 325, 380; Central American Spider (Ateles geoffroyi), 324; Central American Squirrel (Saimiri oerstedii), 323; Common Squirrel (Saimiri sciureus), 322–3; Common Woolly (Lagothrix lagothricha), 326; Dusky Titi (Callicebus moloch), 322; Emperor Tamarin (Saguinus imperator), 328; Geoffroy’s Spider (Ateles geoffroyi), 196; Geoffroy’s Tamarin (Saguinus geoffroyi), 65, 329; Goeldi’s (Callimico goeldii), 322, 329; Golden Lion Tamarin (Leontopithecus rosalia), 27, 329; Guianan Red Howler (Alouatta mcconnelli), 326; Guianan Saki (Pithecia pithecia), 324; howler (Alouatta spp.), 195–6, 320, 322, 326–7; Humboldt’s White-fronted Capuchin (Cebus albifrons), 16, 321; Mantled Howler (Alouatta palliata), 195, 326; marmoset (Callithrix spp.), 15, 65, 320, 322, 328–9; Mexican Black Howler (Alouatta pigra), 326; Midas Tamarin (Saguinus midas), 329; Milton’s Titi (Callicebus miltoni), 320; night or douroucouli (Aotes spp.), 100, 320, 323; Panamanian Night (Aotus zonalis), 323; Pygmy Marmoset (Cebuella pygmaea) 328; Red-handed Howler (Alouatta belzebul), 326; Red Howler (Alouatta seniculus), 326–7; Red Uakari, 323; Saddleback Tamarin (Saguinus fusciocollis), 329; saki (Pithecia spp.), 24–5, 65, 118, 320, 322, 324; Southern Woolly Spider or Muriqui (Brachyteles arachnoides), 325; spider (Ateles; Brachyteles spp.), 324–5; Spix’s Night (Aotus vociferans), 322; squirrel (Saimiri spp.), 323; tamarin (Saguinus; Leontopithecus spp.), 15, 65, 322, 328–9; titi (Callicebus spp.), 322; uakari (Cacajao spp.), 320, 322–4; White Uakari (Cacajao c. calvus), 323; White-bellied Spider (Ateles belzebuth), 324–5; woolly (Lagothrix; Oreonax spp.), 326; Yellow-tailed Woolly (Oreonax [Lagothrix] flavicauda), 326 Monteverde Cloud Forest, Costa Rica: 25, 162, 172, 236–7, 239, 242 Mora excelsa: 134 Moran, E.: 77 morphine: 188 Morton, E.: 152, 157 mosquito: 26, 55, 389–90. See also malaria mosses: 32, 53, 56, 234, 236–7, 245, 256 moth: 13, 46, 64, 119, 171, 184, 195, 242, 296, 336, 360–2; Black Witch (Ascalapha odorata), 361; False Sphinx (Pseudosphinx tetrio), 187; Saffron Playboy (Xanthiris flaveolata), 13; Sloth (Cryptoses choloepi), 336; urania (Urania spp.), 362 motmot: 59, 178, 199, 270–1, 278, 302; Blue-crowned (Momotus momota), 270–1; Broad-billed (Electron

426

index

platyrhynchum), 197; Rufous (Baryphthengus martii), 270; Tody (Hylomanes momotula), 270; Turquoise-browed (Eumomota superciliosa), 187; Whooping (Momotus subrufescens), 60–1 mountains: 115; Maya 253–4; Parima, 207. See also Andes Mountains; tepui mouse: field, 132; House (Mus musculus), 330; spiny pocket (Heteromys; Liomys), 332. See also rodent Mt. Aconcagua: 244 Mt. Cotopaxi: 243 Mt. Darwin: 244 Mt. Mercedario: 244 Mt. Roraima: 206 Mt. Tupungato: 244 Müller, F.: 202 Müllerian bodies: 110, 193 Munn: C. A.: 281 mushroom: 84, 176, 365, 375 mutualism: 93, 155, 178–9; obligate, 88, 93, 176, 194 mycorrhizae: 53, 55, 82, 84, 87. See also fungi myiasis: 390 N National Indian Foundation: 368. See Fundação Nacional do Indio (FUNAI) National Museum of Natural History at the Smithsonian Institution: 380 national parks: 378–9, 382–3 natural selection: 104, 113, 116–7, 120, 134, 188, 196, 337, 383 Naturalist on the River Amazons, The (Bates): 34 nectarivorous species: 122, 174, 281 Nepstad, D.: 383 net ecosystem productivity (NEP): 75–6 Nicaragua: 18, 236, 250, 252–3, 339 niche: ecological, 122, 145–50, 320; fundamental, 147; partitioning, 146–7; realized, 147 Nicholaides, J. J.: 83, 87 nicotine: 188, nighthawk: 296; Nacunda (Chordeiles nacunda), 295–6 nightjar: 125, 161–2, 184, 296; Laddertailed (Hydropsalis climacocerca), 145, 296 nitrogen: 28, 74, 82, 88–9, 93, 176, 188, 206, 230, 361–2, 385; fixation: 88–9 noanalog ecosystem: 28 Nobre, C.: 384 notoungulates: 132–3 nunbird: 289; Black-fronted (Monasa nigrifrons), 289–90, See also puffbird nutrient cycling: 79, 82–3, 87, 89, 93, 191 O oak: 32, 35, 40, 45, 251; Southern Live (Quercus virginiana), 18 Ocelot (Leopardus pardalis): 61, 147–8, 150, 184, 343, 381 Oilbird (Steatornis caripensis): 22, 160–2, 165, 296 Oligocene: 141

Olingo (Bassaricyon gabbii): 339, 340–1 Omphalea spp.: 362 Oncilla (Leopardus tigrina): 343 opossum: 117, 119, 132, 345; bare-tailed (Monodelphis spp.) 335; bushy-tailed (Glironia spp.), 345; Central American Woolly (Caluromys derbianus), 345; Common (Didelphis marsupialis), 345; four-eyed (Philander, Metachirus spp.), 345; Mexican Mouse (Marmosa mexicana), 345; mouse (Gracilinanus, Marmosa, Marmosops, Micoureus spp.), 345; Virginia (Didelphis virginiana), 132; woolly (Caluromys spp.), 345; Yapok or Water (Chironectes minimus), 345; orchid (Orchidaceae): 24, 39, 41, 49, 53, 55–6, 171, 206, 236–7, 239, 245, 251; Sobralia, 55; Cattleya, 56; Vanilla, 56 Orellana, Francisco de: 365 Origin of Species, On the (Darwin): 12, 116, 138, 171 Orinoco River: 205–7, 209, 213, 256, 259, 270, 275, 348 oriole: 158, 171, 276, 297, 303, 306, 315–6; Baltimore (Icterus galbula), 306, 316; Moriche (Icterus chrysocephalus), 212; Orange-crowned (Icterus auricapillus), 59; Orchard (Icterus spurius), 316. See also troupial oropendola: 303–6; Dusky-green (Psarocolius atrovirens), 305; Montezuma (Psarocolius montezuma), 304–5; Russetbacked (Psarocolius angustifrons), 304–6 Oscar (Astronotus ocellatus): 228 oscine birds: 297 Osprey (Pandion haliaetus): 221–4 otter: 215–6, 304; Giant (Pteronura brasiliensis), 215–6, 259, 341; Southern River (Lontra longicaudis), 216 Ovenbird (Seiurus aurocapilla): 316 ovenbirds: 12, 67, 114–5, 144, 212, 263, 289, 297–9, 301–2. owl: 239, 267, 312, 314; Black-and-white (Ciccaba nigrolineata), 145; Burrowing (Athene cunicularia), 250; Crested (Lophostrix cristata), 314; Ferruginous Pygmy- (Glaucidium brasilianum), 314; Mottled (Ciccaba virgata), 314; pygmy(Glaucidium spp.), 314; Spectacled (Pulsatrix perspicillata), 312, 314. See also owlet Owlet, Long-whiskered (Xenoglaux loweryi): 238. See also owl oxbow: 205, 212, 215, 219, oxisol: 85–6, 252, 266 P paca: 37, 61, 144, 150, 159, 329–31, 367; Lowland (Cuniculus paca), 69, 330–31; Mountain (Cuniculus taczanowskii), 331. See also rodent Pachystachys spp.: 46 Padre Island, Peru: 210 Paleocene: 141 Paleozoic era: 15 palm-swift, fork-tailed (Tachornis squamata): 212 palm: 39–40, 47, 49–50, 57, 88, 96, 101–2, 106, 111, 113, 156, 160, 162, 169, 191, 210, 213, 237, 250–1, 254, 257, 260, 270, 280, 284–5, 310, 326, 331, 333, 348, 369–70; Astrocaryum jauari, 169; Astrocaryum murumura, 160; Coconut (Cocos nucifera), 233; Moriche (Mauritia flexuosa), 212–3, 251, 365 palmcreeper: 298; Point-tailed (Berlepschia rikeri), 212 palmetto: 250–1, 254

index

pampas: 261 Panama: 18, 34, 36, 62, 78, 99, 104, 138, 140, 236; bird species richness in, 138; land bridge or Isthmus, 131, 140, 308. See also Barro Colorado Island Pantanal: 184, 205, 215, 217, 250, 257–60, 282, 292, 296, 303–4, 313, 334, 338, 341–4 Papaya (Carica papaya): 102, 191 Pará, Brazil: 378, 384 Paraguay: 18, 55, 250 parakeet: 221, 282–3; Dusky-headed (Aratinga weddellii), 283; White-eyed (Psittacara [Aratinga] leucophthalma), 282; Yellow-chevroned (Brotogeris chiriri), 282. See also parrot páramo: 19, 124, 235–6, 241, 243, 246–8, 298, 335, parasite / parasitism: 52–4, 84, 90, 112, 116, 155, 164, 178–9, 189, 199, 202–3, 229, 242, 306–7, 328, 374; brood, 306; territory, 172 parasite: 90, 116, 155, 164, 178–9, 189, 203, 229, 374; brood, 306; territory, 172 Parker, T. A. III: 145 parrot: 23, 48–9, 60, 90–1, 102, 144, 156, 158–9, 221, 260, 262, 282–5, 312; Blue-headed (Pionus menstruus), 60, 283; Redfan (Deroptyus accipitrinus), 282. See also amazon; macaw; parakeet; parrotlet parrotlet (Forpus spp.), 283. See also parrot passionflower (Passiflora spp.): 46, 191, 196–8, 203, 360; Passiflora adenopoda, 198; Passiflora mixta, 277 pasture: 75, 94–5, 102–3, 110, 253, 255, 378, 380, 382, 385–6 Patagonia: 256, 261, 298 peanut: 369 peccary: 60–1, 123, 132, 150, 156, 159–60, 330, 332–3, 335, 382; Collared (Tayassu tajacu), 36, 151, 332–3; White-lipped (Tayassu pecari), 160, 242, 332–3 penduliflory: 174 pepper: 107, 111, 210; chile, 102, 369–70. See also piper Periwinkle, Mangrove (Littorina angulifera): xxx Permian period: 15 Peru: 18, 20, 25, 37, 91, 115, 207, 236, 243–5, 373, 375; bird species richness in, 136. See also Iquitos Petén, Guatemala: 102, 366 peyote: 375 phenolics / phenols: 88–9, 90, 188–9, 192 Phillips, O.: 78 philodendron (e.g. Monstera spp.): 39, 52–3 phorusrhacoid (terror bird): 131–3, 256 phosphorus: 28, 53, 73–4, 82–5, 87, 89, 93, 206, 252 photosynthesis: 28, 34, 55, 73–4, 78, 81–2, 99, 101, 155 Pianka, E.: 141 Pickett, S. T. A.: 99 Pico Bonito, Honduras: 25 piculet: 292–3; Grayish (Picumnus granadensis), 292; Spotted (Picumnus pygmaeus), 292; See also woodpecker pigeon (Columbiformes): 48, 156, 162, 267–8, 275; Picazuro (Patagioenas [Columba] picazuro), 268; Scaled (Patagioenas speciosa), 268. See also dove piha: 285; Screaming (Lipaugus vociferans), 286–7

427

pine: 32, 35, 39, 171, 176, 237, 251, 253–4, 316, 385; Bristlecone (Pinus longaeva), 42, 104; Caribbean (Pinus caribaea), 251, 253; Jack, 318; Norfolk Island (Araucaria heterophylla), 46 Pineapple (Ananas comosus): 53, 55, 370, See also bromeliad piper (Piperaceae) (Piper spp.): 57, 107–8, 140; Piper nigrum, 107 piranha: 170, 228, 259; Red (Pygocentrus nattereri), 170, 228 pitcher plant: 206 pitviper. See snake Planalto: 86 plant chemical defense: 187–4 plate tectonics: 15, 115, 229 platyrrhines: 320, 322. See also monkey Pleistocene: 119, 130–1, 133, 139–41, 208, 253, 315, 332, 345 Pliocene: 139, 219 Plotkin, M.: 373, 375 plover: 210. See also lapwing Podocarpus National Park, Ecuador: 385 Podocarpus: 245 point bar: 211–2. See also river island; sandbar pollen profile: 131, 141 pollination: 35, 40, 45–7, 55–6, 107–8, 110, 149, 155, 157, 170–4, 192, 316, 382 Polylepis: 245, 247 polyphenols: 188, 192 porcupine: 37, 117, 131, 330–1; Brazilian Porcupine (Coendou prehensilis), 331; dwarf (Erethizontidae), 331; Mexican Hairy Dwarf (Sphiggurus [Coendou] mexicanus), 331; New World, 331; North American (Erethizon dorsatum), 330. See also rodent potassium: 53, 73–4, 82–4, 93, 252, 366 potato: 369; sweet, 87, 111, 370. See also manioc potoo: 184, 296; Common (Nyctibius griseus), 184, 295; Great (Nyctibius grandis), 59, 295 Poui, Pink (Tabebuia pentaphylla): 46 Prance, G.: 130, 135, 174 precipitation (rainfall): 20, 27, 29–33, 35–6, 40, 76–9, 82–3, 88–9, 90, 98, 113, 138, 192, 209, 235–7, 244, 251–2, 256–7, 370, 378, 383–4 predation hypothesis: 149–50 predation: 116, 141, 149–50, 152, 155, 158, 165, 181, 199, 202, 289, 304, 370; hypothesis, 149–50; nest, 152, 165, 30 predator-prey dynamics: 181 prickletail: 298 primary productivity: 73; gross (GPP), 73–4, 76; net (NPP): 72–6, 78–9, 81, 89, 99, 140 productivity-resources hypothesis: 142–6 Prosopis caldenia: 261. See also legume protectionist hypothesis: 193 Prum, R. O.: 168–9 prussic acid: 190 pseudoscorpion: 359 Psychotria (Rubiaceae): 57, 140 Puerto Rico: 46, 90, 100, 150, 235 puffbird: 289–91; Collared (Bucco capensis), 290; Semi-collared (Malacoptila semicincta), 290; Spotted (Bucco tamatia), 290;

428

index

Swallow-winged (Chelidoptera tenebrosa), 290; Whitenecked (Notharchus macrorhynchos), 290; White-whiskered (Malacoptila panamensis), 66, See also nunbird Puma (Mountain Lion; Cougar) (Puma concolor): 150, 344, 381 pumpkin: 102, 369 puna: 124, 235–6, 241, 243, 248–9, 298 Putz, F.: 51 Puya: 241 pyrophyte: 252 quail-dove. See dove quail: 58, 156, 264, 268; Spot-winged Wood- (Odontophorus capueira), 266; Starred Wood- (Odontophorus stellatus), 266 Q Quelccaya: 37, Quetzal, Resplendent (Pharomachrus mocinno): 157, 239–40, 242, 262, 269–70. See also trogon quinine: 91, 239, 373 Quito, Ecuador: 19, 241, 243 R rabbit: 132, 390 rabies: 123 raccoon: 177, 217, 339; Crab-eating (Procyon cancrivorus): 260, 339; Northern (Procyon lotor), 339 racket-tail: 276–8; Booted (Ocreatus underwoodii), 277–8. See also hummingbird Raffauf, R.: 374–5 rainfall. See precipiation rat: rice, 330; spiny (Proechimys spp.), 330–2; tree (Echimys spp.), 331–2. See also rodent recurvebill: 298 Redford, K. H.: 380 Redstart, American (Setophaga ruticilla): 316 reductionoxidation reaction: 81 refuges (refugia): 128–31, 142 Remsen, J. V.: 141, 145 reptile: 133, 138, 150, 181, 239, 346–55, 368. See also anole; basilisk; gecko; iguana; lizard; snake; tegu Reserva Ducke, Brazil: 135–6 resguardo (reserve): 368 resin: 44, 191, 373 rhea: 256, 264; Greater (Rhea americana), 255–6; Lesser or Darwin’s (Rhea pennata), 256 ribereño: 210, 373 rice: 210, 370 Richardson, J. E.: 139–40 Richey, J.: 77 Río Apure: 207 Río Apurímac: 207 Río Arauca: 207 Río Casiquiare: 205 Río Curuá Una: 209 Río Ene: 207 Río Juruá: 209

Río Jutaí: 209 Río Madeira: 135, 169, 208–9, 384 Río Manú: 135 Río Marañón: 207 Río Meta: 207 Río Napo: 89, 205, 208–9, 211 Río Negro: 84, 89–90, 103, 105, 134, 205, 207–9, 325, 384, Río Paraguay: 259 Río Purús: 209 Río Solimoes: 207 Río Tambo: 207 Río Tapajós: 208–9, 365, 384 Rio Teles Pires: 384 Río Tigre: 207 Río Tocantins: 208, 210 Río Trombetas: 209 Río Ucayali: 207 Río Urubu: 209 Río Xingu: 208–9, 384 river island: 145, 205, 210–12 river: blackwater, 88–90, 169–70, 192, 209, 213; clearwater, 209, 213; whitewater, 89–90, 135, 170, 209, 213 riverine ecosystem: 77 RNA: 82 Robin, American (Turdus migratorius): 152 Robinson, Scott: 304–6 Roca, R. L.: 162 rodent: 48, 62–3, 121, 132, 150, 214, 248, 261, 320, 329–32, 370, 380, 382; cricetid: 132. See also agouti; caypbara; chinchilla; mara; mouse; paca; porcupine; rat; squirrel Rondônia, Brazil: 378 root: apogeotropic, 88; basket, 56; buttressed, 17–8, 39–40, 42–3, 110, 113; canopy, 88; epiphyte mat, 53; prop, 39–43, 229–31; stilt, 40, 43, 109, 213; surface, 41–3 Roraima, Brazil: 206, 368 rotenone: 188, 228, 373 Roughgarden, J.: 150 rubber: 191, 369–70. See also Tree, Rubber S sabrewing: 276; Violet (Campylopterus hemileucurus), 68–9. See also hummingbird Sacha Lodge, Ecuador: 23, 25 salamander: 55, 178, 239, 355 Salar de Coipasa: 244 Salar de Uyuni: 244 Saleska, S.: 76, 78 sally gleaning: 125 salt flats: 244 Saltator, Grayish (Saltator coerulescens): 163 San Carlos de Río Negro: Venezuela: 84, 105 sandbar: 146, 210, 212, 222, 229 Santarém, Brazil: 76, 365 sapphire: 276. See also hummingbird Sassafras: 40

index

satellite imagery: 377 savanna: 30, 39, 49, 73, 86–7, 91, 103, 124–5, 128–31, 138, 171, 175, 215, 250–9, 264, 283, 296, 303–4, 308–12, 338, 377, 384–5 Schoener, T.: 144 Schultes, R. E.: 373–5 scorpion: 26, 358, 363–4, 389 screamer: 226–7, 263; Horned (Anhima cornuta), 226–7; Northern (Chauna chavaria), 227; Southern (Chauna torquata), 227 scrub: 254; sandbar, 210–12, 145 scythebill: 300; Brown-billed (Campylorhamphus pusillus), 299. See also woodcreeper search image: 59, 289, 356 season: 20, 30–7, 40, 74–8, 83, 86, 100, 104, 106–7, 110, 135, 138, 140, 205, 207, 209, 212–3, 236–7, 250–4, 256–7, 259, 389 Sechura Desert: 244 sedges: 171, 215, 250–1, 256, 259; Eleocharis spp., 256 seed bank: 96, 98, 104, 109 seed shadow: 157–8, 162 seed: 47–9; dispersal of, 35, 48, 54, 96–7, 104, 107–9, 118, 149, 155–8, 162–3, 169–70, 179, 209, 213, 242, 267, 285, 318, 322, 330, 377, 380–2, 386; predator of, 47, 106, 156, 158, 160, 170, 380 seedeater: 279, 306; Variable (Sporophila corvina), 279 Seedsnipe, Rufous-bellied (Attagis gayi): 246 Selaginella: 57 selection pressure: 93, 116, 125, 128, 138, 148–9, 152, 163, 169, 171, 173, 179, 185, 188, 194–5, 197–8, 202–3, 289, 383 Selva Verde, Costa Rica: 25 Seriema, Red-legged (Cariama cristata): 255–6 sexual dichromatism: 163 sexual selection: 159, 163–5, 168, 286–7, 327, 360 shaman: 365, 373–5 shifting mosaic: 40, 95 Silman, M.: 160 Siona-Secoya Indian community: 368 siskin: 307 Skimmer, Black (Rynchops niger): 210, 221 skunk: 132, 341; Eastern Spotted (Spilogale putorius), 341; hognosed (Conepatus spp.), 341; Hooded (Mephitis macroura), 341 Skutch, A. F.: 152, 293 Slatyer, R. O.: 153 sloth: 110, 119, 131–2, 150, 177, 181, 263, 335–7; Brownthroated Three-toed (Bradypus variegatus), 67–8, 119, 335; Hoffmann’s Two-toed (Choloepus hoffmanni), 58, 336; giant ground, 48, 132; ground, 119, 131–2 Smilodon: 133 Smithsonian Institution: 380 snail: 55, 138, 310; apple (Pomacea spp.), 259 snake: 26–7, 43, 59–60, 69, 113, 117, 138, 181, 185–6, 216–7, 346–51; anaconda, 180, 215–7, 350; Bicolored Coral (Micrurus nigrocinctus), 350; Blunthead Tree (Imantodes cenchoa), 60, 351; boa constrictor (Boa constrictor),

429

68–9, 180–1, 254, 351; Bushmaster (Lachesis muta), 347–9; Cantil, 346; constrictors, 350–1; Cope’s Parrot (Leptophis depressirostris), 26; Copperhead (Agkistrodon contortrix), 346–7; coral (Micrurus spp.), 186–7, 198, 346, 349–50; Cottonmouth (Agkistrodon piscivorus), 347; Emerald Tree Boa (Corallus canina), 351; Eyelash Palm-Pitviper (Bothriopsis schlegelii), 348–9; False Coral (Erythrolamprus mimus), 186, 350; fer-de-lance (Bothrops spp.), 26, 346–8; forest-pitviper (Bothriopsis spp.), 346, 348; Green Anaconda (Eunectes murinus), 216, 351; hognosed pitviper (Porthidium; Atropoides spp.), 346, 349; Indigo (Drymarchon corais), 351; Jararaca, 347–8; Jumping Pitviper (Atropoides nummifer), 349; king, 186–7, 349; lancehead (Bothrops spp.), 346–8; Lampropeltis triangulum hondurensis, 350; Mato Grosso Lancehead (Bothrops matogrossensis), 346; lancehead pitviper, 346; Mexican Horned Pitviper, 347; montane pitviper (Porthidium; Atropoides spp.), 346, 349; Neotropical Rattlesnake (Crotalus durissus), 349; palm-pitviper (Bothriechis spp.), 346, 348–9; pitviper (Bothropis spp.), 347, 349; pygmy rattlesnake, 347; Rainbow Boa (Epicrates cenchria), 350–1; rattlesnake, 346–7; Speckled Forest-Pitviper (Bothrops taeniata), 348; Terciopelo, 347; Two-striped Forest-Pitviper (Bothrops bilineata), 348; vine (Chironius exoletus), 346; vine (Oxybelis spp.), 351; Water Moccasin (Agkistrodon piscivorus), 347; Yellow Anaconda (Eunectes notaeus), 216–7 snakebite: 364, Snow, B.: 159, 287 Snow, D: 149, 157–62, 164–6, 287 Soares-Filho, Britaldo: 384 Soberania National Forest/Park, Panama: 21, 179. See also Canopy Tower sociality: 158–9, 161, 294 sodium: 82–3, 91, 230, 361 softtail: 298 soil: 81–93, 99, 111, 190, 206, 251–6, 283, 365–6, 369–70, 378, 385; caliche; 252; lateritic arecife, 252 Southern Oscillation. See El Niño/Southern Oscillation (ENSO) soybean: 27, 254, 372, 376, 378, 384–5 spadebill (Platyrinchus spp.): 126 sparrow, New World: 307 spatuletail: 276. See also hummingbird specialization: 125, 145–8, 150, 195, 212, 289, 318 speciation: 114–5, 120, 127–31, 138–42, 213, 289, 315 species richness: 56, 103, 119, 130–1, 134–43, 149–50, 153, 195, 213, 229, 236, 245, 253–4, 280, 293, 301, 320, 355, 372, 379, 380, 382 species: 119–20 spider: 26, 109, 118, 136–8, 143, 181–2, 364; Goliath Birdeater (Theraphosa blondi), 364; Golden Orb or Banana Spider (Nephila clavipes), 26; orb-weaving, 118; Spiny Orb Weaver (Gasteracantha cancriformis), 264; tarantula, 264; wolf, 182 spinetail: 298; Parker’s (Cranioleuca vulpecula), 146; tit-, 298; White-bellied (Synallaxis propinqua), 146; White-whiskered (Synallaxis candei), 299 Spoonbill, Roseate (Platalea ajaja): 257

430

index

squash: 102, 369 squirrel: 330, 332; Amazon Dwarf (Microsciurus flaviventer), 24, 332; Amazonian Red-tailed (Sciurus granatensis), 332; Central American Variegated (Sciurus variegatoides), 332; tree (Sciurus spp.), 332. See also rodent stabilimenta: 118 stability-time hypothesis: 141–2 starthroat: 276. See also hummingbird stinkbug (family Pentatomidae): 183 stork: 257, 259–60; Jabiru (Jabiru mycteria), 258–60; Maguari (Ciconia maguari), 258–9; Wood (Mycteria americana), 258–9 streamcreeper: 298 Stutchbury, B.: 152 suboscine birds: 297 succession(al): 94–100, 102–4, 107–8, 110–12, 145, 172, 175, 188, 210, 232, 289, 316, 318, 323, 358, 370, 377, 382, 386; point bar ecological, 210; secondary, 103, 106, 385 Sunbeam, Shining (Aglaeactis cupripennis): 278. See also hummingbird Sunbittern (Eurypyga helias): 226, 263 sundew: 206 Sungrebe (Heliornis fulica): 226 Suriname: 18, 109, 165, 252 survival of the fittest: 116 Swallow-wing (Chelidoptera tenebrosa): 290 swallow: 210, 220–1, 317–8; Barn (Hirundo rustica), 221; Southern Rough-winged (Stelgidopteryx ruficollis), 220; White-winged (Tachycineta albiventer), 220. See also martin swamp: 49, 205, 209, 213, 231, 259, 366; Caroni, 117; Zapata, 218 sycamore: 32 sylph: 276. See also hummingbird sympodial construction:, 42 T table mountain. See tepui: 206–7 tamandua: 92, 337–8; Northern (Tamandua mexicana), 337; Southern or Collared (Tamandua tetradactyla), 337. See also anteater tamarin. See monkey Tambaqui (Colossoma macropomum): 169–70, 213 Tambopata Reserve, Peru: 136 tanager: 23–4, 59, 69, 113, 144, 156, 158–9, 162–3, 171, 173, 178, 236, 240, 247, 262–3, 276, 279–81, 302, 306–7, 315–6; ant- (Habia spp.), 281; Bay-headed (Tangara gyrola), 236; Blue-and-gold, 280; Blue-gray (Thraupis episcopus), 280–1; Blue-winged Mountain- (Anisognathus somptuosus), 281; bush- (Chlorospingus spp.), 240, 279; Cone-billed (Conothraupis mesoleuca), 28; Crimson-collared, 280; Emerald, 280; Flame-colored, 280; Golden-hooded, 280; Grass-green Tanager (Chlorornis riefferii), 240; Greenheaded (Tangara seledon), 280; Hepatic, 279; Palm Tanager (Thraupis palmarum), 152; Paradise (Tangara chilensis), 113; Red-necked (Tangara cyanocephala), 280; Saffron-crowned, 280; Scarlet, 279; Scarlet-bellied Mountain- (Anisognathus

igniventris), 240; Silver-throated (Tangara icterocephala), 280; Summer (Piranga rubra), 279, 307; Swallow (Tersina viridis), 70–1; Western, 279. See also Bananquit; dacnis; chlorophonia; conebill; eupohnia; flowerpiercer; honeycreeper tannins: 88–9, 188–92 tapaculo: 240, 263, 297; Ocellated (Acropternis orthonyx), 240 Tapajós National Forest, Santarém, Brazil: 76 tapir (Tapiridae): 48, 61, 81, 123, 132, 157, 344–5, 367; Baird’s (Tapirus bairdii), 36, 129, 242, 335; Brazilian (Tapirus terrestris), 61, 128–9, 260, 224, 334–5; Mountain (Tapirus pinchaque), 129, 335 Tarapoto Island, Peru: 210 Tattersall, G.: 273 Tayra (Eira barbara), 254, 340–1 Teak, Asian (Tectona grandis): 27 Teal, Puna (Anas puna): 248–9 Tegu: Argentine Black-and-white (Tupinambis merianae), 354– 5; Common (Tupinambis teguixin), 354–5; Red (Tupinambis rufescens), 355 temperature: 20, 28–31, 33, 36, 79, 82–3, 90, 97, 100, 113, 116, 130, 138, 140–1, 150, 174, 230, 235, 241, 245, 250, 277, 383; mean annual (MAT), 29–30, 79. See also climate; climate change tepui: 206–7 Terborgh, J.: 149–50, 281, 382, 385 termite: 39, 44, 81, 86, 88, 91–3, 338, 358; Nasutitermes spp. (family Termitidae), 92; ecological importance of, 91–3 Tern: Large-billed (Phaetusa simplex), 220–1; Yellow-billed (Sternula superciliaris), 220–1 terpenoids: 83, 176, 191 terra firme: 39, 87, 130–1, 135, 213, 229, 326, 329, 366, 368, 370 Terra Nova Rain Forest Reserve, Belize: 373 terra preta: 366 terror bird (Phorusrhacidae): 131–3, 256 tetra: 259; Cardinal (Paracheirodon axelrodi), 228; Neon (Paracheirodon innesi), 228 thistletail: 298 Thompson, L.: 37 thornbird: 298. Rufous-fronted (Phacellodomus rufifrons), 297–8 thornwoods: 256 thrush: 162, 297, 303, 315; Clay-colored (Turdus grayi), 152; Rufous-bellied (Turdus rufiventris), 297; Wood (Hylocichla mustelina),316 Thylacosmilus: 133 tick: 26, 337, 389 Tierra del Fuego: 19, 128, 234–5, 244 tiger-heron. See heron Tikal, Guatemala: 47, 102–3, 366–7; National Park, 267 Timarca Island, Peru: 210 timberline: 245, 247 Timbo (Lonchocarpus utilis): 228 tinamou: 39, 48, 58, 69, 156, 263–5; Great (Tinamus major), 68, 264 Tityra, Masked (Tityra semifasciata): 162–3

index

toad: 60, 136, 189, 239, 355–7; Cane (Rhinella marina [Bufo marinus]), 189, 357; Leaf Litter (Rhaebo haematiticus), 60 tobacco: 188, 369 Tody: Cuban (Todus multicolor), 144; Puerto Rican (Todus mexicanus), 144 tomato: 102, 111 topaz: 276. Crimson (Topaza pella), 277–8. Ruby-, 276. See also hummingbird topography: 85, 114, 129, 243–5, 252 Torrid Zone: 14–20. 32, 388–9 toucan: 16, 23, 39, 48, 62, 100, 102, 113, 156, 159–60, 162, 170, 263, 273–5, 279; Chestnut-mandibled (Ramphastos ambiguus swainsonii), 275; Keel-billed (Ramphastos sulfuratus), 273–4; mountain- (Andigena spp.), 240, 275; Toco (Ramphastos toco), 163, 272–3; Yellow-throated (or Black-mandibled) (Ramphastos ambiguus), 62–3. See also aracari; toucanet toucanet: 16, 24, 62, 120, 163, 273–5; Crimson-rumped (Aulacorhynchus haematopygus), 274; Emerald (Aulacorhynchus prasinus), 120; Saffron (Pteroglossus bailloni), 16; Spot-billed (Selenidera maculirostris), 274–5. See also aracari; toucan toxicity: 170, 186, 362 toxodon: 132–3 trade winds: 31–2, 34–6, 237, 318 trail etiquette: 69–70 Trail, P.: 164–5 trainbearer: 276. See also hummingbird Tramer, E.: 136 transpiration: 29, 73, 82–3, 210, 230 trapliner/traplining: 66, 172–3, 279 tree line: 235, 245 Tree: Almendro (Dipteryx panamensis), 104; Brazil Nut (Bertholletia excelsa), 43, 47–8, 370; Breadnut or ramon (Brosimum alicastrum), 102, 366–7; California Redwood, 42; Cannonball (Couroupita guianensis), 46; Chicle (Manilkara zapota), 44, 102, 191; Cochlospermum spp. 47; coral (Erythrina spp.), 46, 371; Flamboyant (Delonix regia), 46; Gliricidia spp., 195, 371–2; Gumbo Limbo (Bursera simaruba), 17; Hevea spruceana, 169; Inga, 139–40, 371–2, 386; Kapok or Silk-cotton (Ceiba pentandra), 46, 48, 110, 112, 134, 171; mahogany (Swietenia spp.), 49, 102, 379; Milk (Brosimum utile), 47; Monkey Pot (Lecythis ampla), 47; Morning-glory (Ipomoea arborescens), 46; Rubber (Hevea brasiliensis), 111, 169, 191, 210; Stinking Toe (Hymenaea courbaril), 48, 176, 191. See also cecropia; cypress; oak; pine treehopper: 184, 189; Membracis bucktoni, 137 treehunter: 298 treerunner: 298 trees: boles of, 39, 52, 95; buttresses of, 42–3; canopy, 42, 47, 51–3, 88, 98, 101, 105, 157, 192, 371–2; emergent, 40–2, 100, 104, 106, 134, 171; falls of, 40, 51, 57, 62–3, 95–6, 100; pioneer species of, 104–5; species richness of, 103, 119, 135, 213, 245, 379–80; stature of, 236, 245. See also leaf, root Treeswift, Whiskered (Hemiprocne comata): 113 tribal warfare: 367–8

431

tribe: Javari, 368; Nambikwara, 368; Xingu, 368; Yanomami, 368, 375 Trinidad: 19, 22, 128, 134, 159, 235, 243–5, 252 trogon (Trogoniformes): 48, 59, 158, 163, 268–70; Bluecrowned (Trogon curucui), 158; Collared (Trogon collaris), 24; Gartered (Trogon caligatus), 269; Masked (Trogon personatus), 269; Northern Violaceous, 269; Slaty-tailed (Trogon massena), 59; Violaceous (Trogon violaceus) 269. See also quetzal Troupial, Venezuelan (Icterus icterus): 306. See also oriole trumpeter: 263, 267; Gray-winged (Psophia crepitans), 267 tucotuco (Ctenomys spp.): 261 Tucuxi. See dolphin turkey: 264; Ocellated (Meleagris ocellata), 156, 264, 267; Wild (Meleagris gallopavo), 264 Turner, J. R. G.: 202 turtle: 219, 366–7, 370; Arran (Podocnemis expansa), 219; Matamata (Chelus fimbriata), 219; side-necked (Pelomedusidae), 219; Stupendemys, 219; Yellow-bellied Slider (Trachemys scripta), 17; Yellow-spotted River (Podocnemis unifilis), 219 tyrant: Brown-backed Chat- (Ochthoeca fumicolor), 128; Cattle (Machetornis rixosa), 127; chat- (Ochthoeca spp.) 129; Pied Water- (Fluvicola picapiratic), 127; White-headed Marsh(Arundinicola leucocephala), 127. See also flycatcher U uakari. See monkey Uhl, C.: 87, 98, 103 ultisols: 85–6, 252 umbrellabird: 285–6; Bare-necked (Cephalopterus glabricollis), 286 upwelling: 35–6 V várzea: 86, 90, 130, 135, 169, 170, 209–10, 300, 323, 365–6, 368, 370 Veery (Catharus fuscescens): 317–8. See also thrush velvetbreast: 276. See also hummingbird Venezuela: 18–9, 39, 84, 87, 89, 93, 103, 105, 128, 141, 162, 205–7, 219, 235–7, 241, 244–5, 250, 252, 256–7, 381, 386. See also llanos Veracruz, Mexico: 18, 308, 380 viburnum: 40 vicariance. See isolation Vicuña (Vicogna vicugna): 248 vine(s): 33, 39, 41, 48, 50–2, 55, 95–7, 100, 110, 113, 118, 157, 174, 192, 196–7, 237, 377; wourali, 374. See also liana; passionflower Virola spp.: 373, 375 virus: rabies, 123; yellow fever, 26; Zika, 389 Viscacha, Mountain (Lagidium peruanum): 248 voice: 60–1, 69, 120, 275, 286–7, 297 voodoo: 357 Voyage of the Beagle, The: 120, 261 vulture: 81, 221, 226, 248, 308, 312; Black (Coragyps

432

index

atratus), 37, 70, 308–9; Greater Yellow-headed (Cathartes melambrotus), 308–9; King (Sarcoamphus papa), 70–1, 308–9, 311; Lesser Yellow-headed (Cathartes burrovianus), 308–9; Turkey (Cathartes aura), 37, 70, 248, 308–10 W Wallace, A. R.: 21, 49, 116, 117, 134, 319 Wanderings in South America (Waterton): 119, 333 warbler: 315–6; Bachman’s (Vermivora bachmanii), 318; Baybreasted (Setophaga castanea), 315; Black-and-white (Mniotilta varia), 315–6; Black-throated Blue (Setophaga caerulescens), 316–7; Blackpoll (Setophaga striata), 317–8; Cerulean (Setophaga cerulea), 316; Chestnut-sided (Setophaga pensylvanica), 317–8; Elfin-woods (Setophaga angelae), 239; Hooded (Setophaga citrina), 316; Kentucky (Geothlypis formosa), 315–6; Kirtland’s (Setophaga kirtlandii), 317–8; Tennessee (Oreothlypis peregrina), 316; Worm-eating (Helmitheros vermivorum), 110 warning (aposematic) coloration: 185–7, 198, 202–3 wasp: 91, 158, 176, 194, 197, 202, 242, 305, 358, 390–1 Water-lily, Victoria or Royal (Victoria amazonica): 174, 212 Waterton, C.: 119, 333, 335, 374 waxwing: 156 weevil: 48, 137 Weske, J.: 149 West Indies: 17, 250 Wheelwright, N. T:, 162–3 Whip-poor-will, Eastern (Caprimulgus vociferus): 161. See also nightjar whipscorpion: 363–4 Why Are There So Many Species of Insects? (Janzen): 143 willow (Salix spp.): 163, 210 Wilson, D. E.: 122 Wilson, E. O.: 136 winter site fidelity, 316 Wolf, Maned (Chrysocyon brachyurus): 255, 344 Wood-rail, Gray-necked (Aramides cajaneus): 222 woodcreeper: 12, 115, 144, 178, 263, 281, 289, 297–300, 302; Great Rufous (Xiphocolaptes major), 299; Long-billed (Nasica longirostris), 144, 300; Narrow-billed (Lepidocolaptes

angustirostris), 299; Northern Barred (Dendrocolaptes sanctithomae), 66; Wedge-billed (Glyphorynchus spirurus), 299–300; White-chinned (Dendrocincla merula), 382. See also scythebill woodhaunter: 298 woodland: 130, 247, 252–7, 261 Woodnymph, Crowned (Thalurania colombica): 276. See also hummingbird woodpecker: 65, 67, 100, 146–7, 162–3, 263, 270, 273, 289, 292–3, 300, 312; Black-cheeked (Melanerpes pucherani), 146; Chestnut (Celeus elegans), 293; Crimson-crested (Campephilus melanoleucos), 292; Golden-olive (Colaptes rubiginosus), 146; ivory-billed (Campephilus spp.), 293; Lineated (Dryocopus lineatus), 65, 71; Magellanic (Campephilus magellanicus), 292, Pale-billed (Campephilus guatemalensis), 293; Waved (Celeus undatus), 293; White (Melanerpes candidus), 292. See also flicker; piculet World Wildlife Fund: 380 Wrege, P. H.: 179 wren: 222, 239, 291–2; House (Troglodytes aedon), 291; Musician (Cyphorhinus arada), 291, Striped-backed (Campylorhynchus nuchalis), 292; White-breasted Wood- (Henicorhina leucosticta), 291–2; White-headed (Campylorhynchus albobrunneus), 292. See also donacobius Wright, J.: 386–7 X xenops: 298 xeromorphic: 250 Y Yahgan (Yámana) Indians: 244 yellow fever: 26, 389 Yellowthroat: Bahama (Geothlypis rostrata), 114; Common (Geothlypis trichas): 316 Ygapos: 87 Yucatán, Mexico: 102, 250, 264, 326, 366 Z zooplankton: 169–70, 209