Marine Ecology: Processes, Systems, and Impacts [2 ed.] 0199227020, 9780199227020

Table of contents :
Binder1
1600~ (1)
1600~ (2)
1600~ (3)
1600~ (4)
1600~ (5)
1600~ (6)
1600~ (7)
1600~ (8)
1600~ (10)
1600~ (12)
1600~ (13)
1600~ (14)
1600~ (15)
1600~ (17)
1600~ (18)
1600~ (19)
1600~ (20)_1
1600~ (21)
1600~ (22)
1600~ (23)
1600~ (24)
1600~ (26)
1600~ (27)
1600~ (28)
1600~ (29)
1600~ (30)
1600~ (31)
1600~ (32)
1600~ (33)
1600~ (34)
1600~ (35)
1600~ (36)
1600~ (37)
1600~ (38)
1600~ (39)
1600~ (40)
1600~ (41)
1600~ (42)
1600~ (43)
1600~ (45)
1600~ (46)
1600~ (47)
1600~ (49)
1600~ (50)
1600~ (51)
1600~ (52)
1600~ (53)
1600~ (54)
1600~ (55)
1600~ (56)
1600~ (57)
1600~ (58)
1600~ (59)
1600~ (60)
1600~ (61)
1600~ (62)
1600~ (63)
1600~ (64)
1600~ (65)
1600~ (66)
1600~ (67)
1600~ (68)
1600~ (70)
1600~ (71)
1600~ (72)
1600~ (73)
1600~ (74)
1600~ (75)
1600~ (76)
1600~ (78)
1600~ (80)
1600~ (81)
1600~ (82)
1600~ (84)
1600~ (85)
1600~ (86)
1600~ (87)
1600~ (89)
1600~ (91)
1600~ (93)
1600~ (94)
1600~ (95)
1600~ (96)
1600~ (97)
1600~ (98)
1600~ (99)
1600~ (100)
1600~ (101)
1600~ (103)
1600~ (104)
1600~ (105)
1600~ (107)
1600~ (108)
1600~ (109)
1600~ (110)
1600~ (111)
1600~ (112)
1600~ (113)
1600~ (114)
1600~ (115)
1600~ (116)
1600~ (117)
1600~ (118)
1600~ (119)
1600~ (120)
1600~ (121)
1600~ (122)
1600~ (123)
1600~ (124)
1600~ (125)
1600~ (126)
1600~ (127)
1600~ (128)
1600~ (129)
1600~ (130)
1600~ (131)
1600~ (132)
1600~ (133)
1600~ (135)
1600~ (136)
1600~ (137)
1600~ (138)
1600~ (139)
1600~ (141)
1600~ (143)
1600~ (144)
1600~ (145)
1600~ (146)
1600~ (147)
1600~ (148)
1600~ (149)
1600~ (150)
1600~ (152)
1600~ (154)
1600~ (155)
1600~ (156)
1600~ (157)
1600~ (158)
1600~ (159)
1600~ (160)
1600~ (161)
1600~ (162)
1600~ (163)
1600~ (164)
1600~ (166)
1600~ (167)
1600~ (168)
1600~ (169)
1600~ (170)
1600~ (171)
1600~ (172)
1600~ (173)
1600~ (174)
1600~ (175)
1600~ (176)
1600~ (178)
1600~ (179)
1600~ (180)
1600~ (181)
1600~ (182)
1600~ (183)
1600~ (184)
1600~ (185)
1600~ (186)
1600~ (187)
1600~ (188)
1600~ (190)
1600~ (191)
1600~ (192)
1600~ (193)
1600~ (194)
1600~ (195)
1600~ (196)
1600~ (197)
1600~ (198)
1600~ (199)
1600~ (200)
1600~ (201)
1600~ (202)
1600~ (203)
1600~ (204)
1600~ (205)
1600~ (206)
1600~ (207)
1600~ (208)
1600~ (209)
1600~ (210)
1600~ (211)
1600~ (212)
1600~ (213)
1600~ (214)
1600~ (215)
1600~ (216)
1600~ (217)
1600~ (218)
1600~ (219)
1600~ (220)
1600~ (221)
1600~ (222)
1600~ (223)
1600~ (224)
1600~ (225)
1600~ (226)
1600~ (227)
1600~ (228)
1600~ (229)
1600~ (230)
1600~ (231)
1600~ (232)
1600~ (233)
1600~ (234)
1600~ (235)
1600~ (236)
1600~ (237)
1600~ (238)
1600~ (240)
1600~ (241)
1600~ (242)
1600~ (243)
1600~ (244)
1600~ (245)
1600~ (246)
1600~ (247)
1600~ (248)
1600~ (249)
1600~ (250)
1600~ (251)
1600~ (252)
1600~ (253)
1600~ (254)
1600~ (255)
1600~ (256)
1600~ (257)
1600~ (258)
1600~ (259)
1600~ (260)
1600~ (261)
1600~ (262)
1600~ (263)
1600~ (264)
1600~ (265)
1600~ (266)
1600~ (267)
1600~ (268)
1600~ (269)
1600~ (270)
1600~ (271)
1600~ (272)
1600~ (273)
1600~ (274)
1600~ (275)
1600~ (276)
1600~ (277)
1600~ (278)
1600~ (279)
1600~ (280)
1600~ (281)
1600~ (282)
1600~ (283)
1600~ (284)
1600~ (285)
1600~ (286)
1600~ (287)
1600~ (288)
1600~ (289)._270
Binder2
1600~ (1)_271
1600~ (2)
1600~ (4)
1600~ (5)
1600~ (6)
1600~ (7)
1600~ (8)
1600~ (9)
1600~ (10)
1600~ (11)
1600~ (12)
1600~ (13)
1600~ (14)
1600~ (15)
1600~ (16)
1600~ (17)
1600~ (18)
1600~ (19)
1600~ (20)
1600~ (21)
1600~ (22)
1600~ (23)
1600~ (24)
1600~ (25)
1600~ (26)
1600~ (27)
1600~ (28)
1600~ (29)
1600~ (30)
1600~ (31)
1600~ (32)
1600~ (33)
1600~ (34)
1600~ (35)
1600~ (36)
1600~ (37)
1600~ (38)
1600~ (39)
1600~ (40)
1600~ (41)
1600~ (42)
1600~ (43)
1600~ (44)
1600~ (45)
1600~ (46)
1600~ (47)
1600~ (48)
1600~ (49)
1600~ (50)
1600~ (51)
1600~ (52)
1600~ (53)
1600~ (54)
1600~ (55)
1600~ (56)
1600~ (57)
1600~ (58)
1600~ (59)
1600~ (60)
1600~ (61)
1600~ (62)
1600~ (63)
1600~ (64)
1600~ (65)
1600~ (66)
1600~ (67)
1600~ (68)
1600~ (69)
1600~ (70)
1600~ (71)
1600~ (72)
1600~ (73)
1600~ (74)
1600~ (75)
1600~ (76)
1600~ (77)
1600~ (78)
1600~ (79)
1600~ (80)
1600~ (81)
1600~ (82)
1600~ (83)
1600~ (84)
1600~ (85)
1600~ (86)
1600~ (87)
1600~ (88)
1600~ (89)
1600~ (90)
1600~ (91)
1600~ (92)
1600~ (93)
1600~ (94)
1600~ (95)
1600~ (96)
1600~ (97)
1600~ (98)
1600~ (99)
1600~ (100)
1600~ (101)
1600~ (102)
1600~ (103)
1600~ (104)
1600~ (105)
1600~ (106)
1600~ (107)
1600~ (109)
1600~ (110)
1600~ (111)
1600~ (112)
1600~ (113)
1600~ (114)
1600~ (115)
1600~ (116)
1600~ (117)
1600~ (118)
1600~ (119)
1600~ (120)
1600~ (121)
1600~ (122)
1600~ (123)
1600~ (124)
1600~ (125)
1600~ (126)
1600~ (127)
1600~ (128)
1600~ (129)
1600~ (130)
1600~ (131)
1600~ (132)
1600~ (133)
1600~ (134)
1600~ (135)
1600~ (136)
1600~ (137)
1600~ (138)
1600~ (139)
1600~ (140)
1600~ (141)
1600~ (142)
1600~ (143)
1600~ (144)
1600~ (145)
1600~ (146)
1600~ (147)
1600~ (148)
1600~ (149)
1600~ (150)
1600~ (151)
1600~ (152)
1600~ (153)
1600~ (154)
1600~ (155)
1600~ (156)
1600~ (157)
1600~ (158)
1600~ (159)
1600~ (160)
1600~ (161)
1600~ (162)
1600~ (163)
1600~ (164)
1600~ (165)
1600~ (166)
1600~ (167)
1600~ (168)
1600~ (169)
1600~ (170)
1600~ (171)
1600~ (172)
1600~ (173)
1600~ (174)
1600~ (175)
1600~ (176)
1600~ (178)
1600~ (179)
1600~ (180)
1600~ (181)
1600~ (182)
1600~ (183)
1600~ (184)
1600~ (185)
1600~ (186)
1600~ (187)
1600~ (188)
1600~ (189)
1600~ (190)
1600~ (191)
1600~ (192)
1600~ (193)
1600~ (194)
1600~ (195)
1600~ (196)
1600~ (197)
1600~ (198)
1600~ (199)
1600~ (200)
1600~ (201)
1600~ (202)_471
1600~ (203)
1600~ (204)
1600~ (205)
1600~ (206)
1600~ (207)
1600~ (208)
1600~ (209)
1600~ (210)
1600~ (211)
1600~ (212)
1600~ (213)
1600~ (214)
1600~ (215)
1600~ (216)
1600~ (217)
1600~ (218)
1600~ (219)
1600~ (220)
1600~ (221)
1600~ (222)
1600~ (223)
1600~ (224)
1600~ (225)
1600~ (226)
1600~ (227)
1600~ (229)
1600~ (230)
1600~ (231)
1600~ (232)_501
1600~ (233)
Primary production
2.4 Heterotrophic metabolism
Secondary production

Citation preview

Marine Ecology: Processes, Systems, and Impacts

This page intentionally left blank

• aline

co 0

Processes, Systems, and Impacts SECOND EDITION

Michel J. Kaiser • Martin J.Attrill • Simon Jennings David N.Thomas • David K.A. Barnes • Andrew S. Brierley • Jan Geert Hiddink Hermanni Kaartokallio • Nicholas V. C. Polunin • David G. Raffaelli With contributions from

Peter J. Ie B.Williams • Gareth Johnson • Kerry Howell Coleen Suckling • Anne Berit Skiftesvik

OXFORD UNIVERS ITY PRESS

OXFORD VNIVEltS ITY {' !lESS

Great Clarendon Street, Oxford OX2 5DP Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York Auckland Cape Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto With offices in Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries Published in the United States by Oxford University Press Inc., New York

© Oxford University Press 2011 The moral rights of the authors have been asserted Database right Oxford University Press (maker) First edition published 2005 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you must impose the same condition on any acquirer British Library Cataloguing in Publication Data Data available Library of Congress Cataloging-in-Publication Data Data available Typeset by TechType Printed in Italy on acid-free paper by L.E.G.o. S.p.A. - Lavis TN ISBN 978-0-19-922702-0

I 3 5 7 9 10 8 5 4 2

'It is likely that much present day published science depends on "fa ct"which has not been sufficiently checked. James Elroy Flecker, in his play Hassan, wrote: "Men who think themselves wise believe nothing until the proof. Men who are wise believe anything until the disproof." Perhaps in this com-

plicated world, one should steer a careful path between Flecker's two extremes.' G. E. (Tony) Fogg (1919-2005)

This page intentionally left blank

Preface Marine ecology: an introduction

The evolution of marine ecology

Approximately 2.2 billion people live within 100 Ian of a coastline. This figure is set to double by 2025. While the average population density along coastlines is currently 80 people krrr-, this increases to up to 1000 krrr- in countries such as Egypt and Bangladesh. Many of these coastal inhabitants depend directly upon marine resources for their subsistence or income. The world's oceans provide a wealth of goods and services. and are used as repositories for our waste products, yield renewable (wind and tidal energy) and non-renewable (oil and gas) forms of energy, provide important bulk transportation routes, provide a source of food, yield mined commodities (diamonds, heavy metals), and provide recreational benefits that support important tourism industries. Technological advances have enabled us to use areas of the oceans that previously were inaccessible to humans, and many marine resources are either fully or over-exploited. However. with technical advances. the increase in knowledge and material riches is often accompanied by increased consequences of technical failures, as seen in the Gulf of Mexico Deep Horizon blowout in 2010. Despite our growing use of the oceans and major efforts to catalogue the diversity and distribution. such as the Census of Marine Life. much of the marine realm has never been viewed by the human eye. Indeed, it is sobering to think that we probably know more about the surface of the moon than we do about the marine environment ofour own planet. Understanding marine ecological processes and systems are urgent research priorities if we are to comprehend the ecological effects of human activities that impact upon them and more widely on global systems. This understanding is essential to help society find ways of achieving sustainable use of marine resources. Thus marine ecology remains an exciting and pivotal subject that has matured into an integrated science that encapsulates biological. chemical, and physical processes from the microscopic to the global scale.

The development of marine ecology can be charted through three major eras. Early naturalists worked in an age when seafarers' stories of sea monsters abounded and authors such as Jules Verne romanticized exploration of the deep and the battle with the leviathan. The observations of early naturalists, such as Darwin, were mostly restricted to the shoreline, while scientific sampling of the abyss was performed by lowering crude sampling devices to the distant seabed. This must have been (and remains) an incredibly exciting time. as every sample probably contained an organism viewed for the first time by human eyes. Exploration of the oceans continues to be an ongoing task, with the discovery ofa new phylum in the last few decades (Chapter 1) . Then in the early to mid-twentieth century, ecologists such as Petersen and Thorson began to consider ecological rules that determined the distribution and abundance of marine species and communities (Chapters 3, 7,8, and 13). This coincided with the early beginnings offisheries science and concerted efforts to understand the processes affecting population variability in fish populations.

Nearly 40Ofo of the world's population live close to the coastline. The world's oceans are heavily exploited for mineral and biological resources even though much of the ocean remains unexplored.

The history of marine ecology can be divided into three main eras: (1) exploration and description; (2) experimental manipulation; (3) integration and application.

The second era of marine ecology began in the late 1960s and early 1970s, when ecologists such as Connell and Paine undertook their seminal research on the effects of disturbance and competition in ecology. using marine systems as models fortheir studies (Chapter 6) . Their work had a pivotal role in the development of general ecological theory, which then springboarded into the more easily studied terrestrial systems. This theme has developed to the present day, and spawned many manipulative studies of the role of predators and grazers in marine systems and long-term studies of food-web dynamics. Technological advances have enabled us to understand better the processes of primary and microbial production; the advent of stable isotope analysis has provided a common means to assess the trophic status (i.e. top predator. forage species, detritivore, secondary producer) of species in marine communities from around the world (Chapters 7, 8, and 10) and the development of remote sensing methods to describe the distribution and dynamics of primaryproduetion on global scales provided unprecedented insights into the ecology

Preface

of the global oceans. Novel molecular tools have offered new insights into the diversity of species complexes that previously were the source of debate amongst taxonomists (Chapter 1). While we still have a lot to learn about marine ecosystem processes, we have entered a new phase (the third era) in which research has become more urgently focused on the ecological ramifications of an ever-increas ing list of human impacts (Chapters 13, 14, and 15). This new focus still firmly relies upon ecological theory (Chapters 1, 3, 4, 7, 13, and 15) to understand how communities respond to exploitation and disturbance. These impacts occur against a background of climate change that is occurring at a rate faster than previously recorded in our time. Changes in water temperature, storm activity, and precipitation are now compounded by the potential of ocean acidification altering biochemical processes in the ocean. Activities such as comme rcial fishing have occurred for hundreds of years, but have sometimes reached such intensive levels that they

Ecosystem goods and services

have driven fundamental changes in ecosystem status . An increasingly complex range of contaminants is pouring into many coastal waters, and their pernicious sub-lethal effects may cause reduced survival of larval stages and alteration ofsexual characteristics in adult organisms . The incidences ofdeoxygenation in coastal waters have increased in recent years with catastrophic implications for the associated fisheries and aquaculture activities, not to mention degradation of ecosystem fun ctioning, goods, and services (see box below). The latter provide a clue to the direction of marine ecology of the future. While there are still many gaps to be filled, the latest exciting advances are being made by studies that are multidisciplinary, combining oceanography, biogeochemistry, and sedime ntology together with marine ecology, a trend that is set to continue into the future. Human impacts on the marine environment are set against a background of an increasing rate of global climate change.

from marine ecosystems. Cultural values are ofte n deeply embedded within human society, as typified by the bless-

The concept of ecosystem goods is fairly easy to grasp

ing of the fleet by the local Roman Catholic Bishop in

in tangible economic terms; for example, the value (US$)

Provincetown Harbour, New England (inset), where

of fish or other commodi ties extracted or farmed in the

a large proportion of the fishing commu nity can trace

ocean. Perhaps less obvious are the values attributed to

their roots to Portugal or the Azores. (Photographs: M. J.

the regulat ing functions, such as flood control and coastal

Kaiser.)

defence, and the cultural non-material benefits derived

,

. ,.

-

•,

Preface •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Provisioning

Regulating

Cultural

Products obtained from :

Benefi ts obtained from:

Non-material benefits obtained from :

ecosystems

regulati on of ecosystem processes

ecosystems

food

climate regulation

spirit ual

freshwater

disease co ntro l

recreational

fuel

flood con trol

aesthetic

biochemicals

detoxification

inspirational

genetic reso urces

po llinat ion

ed ucat ional

communal symbolic • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

Supporting Services necessary for th e pro duct ion of all oth er ecosystem serv ices Soil form ation Nutrient cycli ng Eco log ical processes/fu nctioni ng

These are exciting times, but even the multidisciplinary approach is constrained within the boundaries of' marine science'. This has been the typical approach of scientists , to offe r up our findings to the wider public and governmental bodies, at which point we have fulfilled our duty. This approach is rapidly being replaced by the realization that marine ecosyste ms have tangible value to society, not only in terms of the goods (fis h, aggregate, oil) that are yielded, but also in terms of the services that they provide (carbo n sequestration, coastal defence, waste repositories). Degradation of biodiversity is thought to reduce the capacity of the ecosyste ms to deliver goods and services, thus biodiversity loss has real economic, societal, and cultural costs for human society. For example, living m arine syste ms, such as coral reefs and mangrove forests, provide an important buffer between the ocean and the land. This role was brought sharply into focus w ith the 2004 tsunami that struck the Indian Ocean leaving over SOOO dead in Thailand alone, with the exte nt of damage often correlating with the exte nt of coastal defence.

good example would be the loss of the cultural services that occurs when a pristine flora and fauna is degraded (e.g. loss of w hales from Arctic waters deprives Inuit peoples of the cultural aspect of hunting whales, regardless of the practical need to acquire food) (see box above) . Different biodivers ity change scenarios (e.g. habitat fragmentation, contamination, over-exploitation) are likely to affect processes to a varying exte nt, because different kinds of taxa (large or small, primary producers or top predators) are lost under the different scenarios. A good example of the latter is the over-harves ting of bottom-dwelling fish and incidental removal of other seabed animals (b ent h os) on the Scotian Shelf off Canada. This has led to a decoupling of the ecosystem link between water column and seabed processes (b en th o p ela gic coupling) and ultimately resulted in a syste m dominated by mid-water (pela gic) fishes. In addition, specific goods and services may be supported by several different processes , further convoluting their relationship w ith biodivers ity. While ecosystem goods are reasonably simple concepts

Marine ecology is beginning to break out of traditional

to grasp, e.g. the acquisition of food or minerals, the

scientific boundaries and is beginning to interface with

cultural value of biodiversity is a more abstract concept.

economics and the social sciences to understand the wider societal importance of marine biodiversity.

Most experimental m anipulations of biodiversity indicate some relationship between biodivers ity and ecosystem processes; however, few have drawn out the links between biodiversity change and the output of goods and services. A

Using this book to study marine ecology Marine Eco logy: Processes, Systems, and Imp acts h as been written to address the current need to understand the appli-

Preface cation of marine ecology in a marine environment strongly influenced by human activities. The structure of the book reflects the integrated approach to marine ecology that is necessary to answer many of today's key marine environmental and conservation problems. which form the focus of the last section of the book. The bookis divided into 16 chapters arranged in four distinct sections. The opening chapter deals with the processes that affect patterns at a variety of spatial and temporal scales, diversity. community organization, and structuring processes. and provides a palaeoecological perspective on present-day marine systems. As a marine ecologist, it is important to have a grasp of the relevant time-scales that impact upon the systems in which we work. While much of the ecology we encounter deals with either instantaneous or relatively short-term (1-3 years in duration) processes. evolutionary ecologists think in terms of thousands to millions of years. Some environments. such as the deep sea, have remained relatively stable on an evolutionary time-scale. whereas coastal and shelf habitats have experienced far more frequent changes. This dynamic flux in the near coastal habitat is brought into focus by presentday findings, at sites currently 40 m beneath the sea to the west of Florida in the Gulf of Mexico, of human artefacts and animal bones from the early Holocene with evidence of butcher cuts and other implement shaping. Processes contains three chapters that address the fundamental global processes of primary and microbial production that fuel marine systems and the ecology of the organisms responsible. Chapter two describes primary processes. while Chapter three has been revised extensively to better convey its biological context. These two chapters lead into a new chapter that deals with secondary production. Systems then addresses in more detail estuaries. rocky and sandy shores, the pelagic environment. continental shelf seabed. the deep sea, mangroves. and seagrass meadows, coral reefs. and polar seas. Impacts tackles some ofthe most pressing environmental issues relevant to the marine environment that span the systems described beforehand, with chapters on fisheries. aquaculture. disturbance, pollution, and climate change. and finally marine conservation. The penultimate chapter also includes a consideration of the experimental approach needed to determine the effects of human impacts and deals with common pitfalls made by students undertaking field and laboratory projects. This second edition has been revised extensively throughout and the feedback from users of the first edition has helped us identify new areas for inclusion. As requested, we have supplemented the online supporting materials with worked examples (e .g. how to calculate secondary production) and advice on improving exam performance. Other textbooks have traditionally dealt with key physical and chemical environmental processes as a discrete unit, usually towards the beginning of the book. This section can be overlooked or its importance not appreciated at the time

of reading or forgotten by the time it becomes relevant in the text. In Marine Ecology: Processes. Systems, and Impacts, we have integrated the environmental processes at key points that are cross-referenced throughout the text. so that their relevance is immediate and the learning process enhanced. Some of these key processes are reiterated from a slightly different perspective or even repeated in a number of chapters so that learning is reinforced. Key words and concepts are highlighted in bold throughout the text to aid learning and revision. In addition to the definitions and explanations given in the text. an excellent online glossary of important marine biological terms can be found at the website of the Marine Life Information Network for Britain and Ireland (MARLIN; see www.marlin.ac.uk for more information) . Boxes are used to expand specific points, and offer interesting examples and case studies that illuminate the concepts being introduced. In this second edition we have highlighted in each chapter key techniques that are important to the contemporary marine ecologist and current focus boxes that we feel are likely to be of major interest in coming years. Finally, we have provided a short list offurther reading, trying wherever possible to recommend widely accessible literature and have provided a list of websites that will enable you to learn more about specific subjects or disciplines. Full citations for all references given in the chapters can be found at the end of the book. Marine ecology is a highly relevant and challenging subject that is fascinating to amateur. student. and professional alike. We hope that students using this textbook will gain a real feeling for the excitement of marine ecology as a subject of interest, a hobby, and a potential career. Michel Kaiser

Online Resource Centre Marine Ecology: Processes, Systems, and Impacts is supported by an Online Resource Centre, which holds various supplementary materials for students and registered adopters, including figures from the book available to download, videos, and a web link library including all the URLs cited in the book. Visit: www.oxfordtextbooks.co.uk/orc/kaiser2e/.

New to this Edition This 2nd edition has been revised by 30%, including an entirely new chapter on secondary production. Two new authors have been added to the team, and all chapters have been updated to include key works, issues, and topics published since 2005 . Coverage of socioeconomic issues and climate change has been enhanced in this edition and two new box types-Current Focus and Techniques-have been introduced to highlight important issues facing ecologists today and showcase contemporary research methods. respectively.

Acknowledgements As with any large project, this book could only be brought to fruition with the help and goodwill of many others. The authors thank the following for their collaboration

and help with the reproduction of illustrative materials: Alice Alldredge, Ann-Margret Amui-Vedel, Kirsty Anderson, Emmanuel Arand, Peter Auster, Phillip Assay, Tim Atack, Riitta Autio, Nick Baker, Ole Johan Brett, Gen Broad, Tracey Bryant, Andrew Butko, Blaise Bullimore, S. C. Cary, Patrice Ceisel, Chelsea Instruments, Kris Chmielewski, David Clausen, Joey Comiso, Finlo Cottier, John O. Dabiri, Paul Dando, Bruno Danis, Meg Daly, Gerhard Dieckmann, Beatriz Diez, Emily Downes, Nick Dulvy, Kurt Fedra, Kevin Fitzsimmons, Sarah Foster, Peter Fretwell, Jo Gasgoigne, David Gillikin, Brett Glencross, Ronnie Glud, Charles

Greenlaw, Sonnke Grossmann, Julian Gutt, Jason HallSpencer, Christian Hamm, Heinz Walz GmbH, IFREMER, Joachim Henjes, Hilmar Hinz, Keith Hiscock, Rohan Holt, James Hrynyshyn, Atsushi Ishirnatsu, Emma Jackson, Greg Jenkins, David Samuel Johnson, Matt Johnson, Mandy Joye, Johanna Junback, Paul Kay, Gunter Kirst, Christopher Krembs, Christoph Kuhne, HaITi Kuosa, Ruben Lara, Chris Leakey, Eva Leu, Lewis LeVay, Alan Longhurst, Ian Lucas, Ian Macintyre, Michal Mafias, Sophie McCully, lain McGaw, Jan Michels, Peter Miller, Craig Mills, Daniel Mos-

quin, NASA, Simon Neill, NOM, Ylva Olsen, Stathys Papadimitriou, James Perrins, Lasse Pettersson, Jarone Pinhassi, Lubas Polerecky, Joao Quaresma, Ivor Rees, Marcus Reckermann, David Roberts, Riccardo Rodolfo-Metalpa, Craig Rose, Royal Society for the Protection of Birds, George Russell, SAHFOS, Bill Sanderson, Ricardo Serrao Santos, Sedgewick Geology Museum Cambridge University, Sigrid Schiel, Shedd Aquarium, Sir Alistair Hardy Foundation for Ocean Science, Mariano Sironi, Smithsonian Institute, Wayne P. Sousa, South Australian Research and Development Institute, Michael Stachowitsch, Kare Telnes, The Hawaii Ocean Time Series Programme, Toru Takita, Jim Treasurer, Andreas Trepte, Paul Tucker, Tuna Boat Owners of South Australia!Australia and Fishing Management Authority, U.S. Fish and Wildlife Service, Katrien van Landeghem, Dolors Vaque, AnoukVerheyden, Amanda Vincent (Project Seahorse), Janet Voight, Stephen C Votier, Tom Webb, WHO! Graphics, Alan D. Wilson, Keith Wilson, Rory Wilson, Matthew Witt, Richard Woodcock, Boris Worm, Jeremy Young, Kakani Katija Young. The opening quote is from an article by Professor G.E. Fogg who died in 2005. The authors are grateful to the family of Professor Fogg for permission to reproduce his thoughts that remain as relevant as ever.

This page intentionally left blank

Outline Contents 1 Patterns in the Marine Environment

1

Part 1 PROCESSES

2 Primary Production Processes 3 Microbial Ecology: Production and the Decomposition of Organic Material 4 Secondary Production

33

89 126

Part 2 SYSTEMS

5 6 7 8 9 10

Estuaries Rocky and Sandy Shores Pelagic Ecosystems Continental Shelf Seabed The Deep Sea Mangrove Forests and Seagrass Meadows 11 Coral Reefs 12 Polar Regions

143 172

194 217 251 277 305 325

Part 3 IMPACTS

13 Fisheries 14 Aquaculture 15 Disturbance, Pollution, and Climate Change 16 Conservation

References Weblinks Index

357 377 401 429 450 485 489

This page intentionally left blank

Detailed Contents 1 Patterns in the Marine Environment

1.1 1.2 1.3 1.4

Introduction Biogeography Biodiversity Abundance and size Further reading

I I

9

15 23 29

Part 1 PROCESSES 2 Primary Production Processes

2.1 2.2 2.3 2.4 2.5 2.6 2.7 2.8 2.9 2.10 2.11 2.12 2.13

Introduction Photosynthesis Respiration Heterotrophic metabolism Light in water Light and photosynthesis Supply of inorganic nutrients The main limiting nutrients for growth Algal growth Seasonal trends in primary production Global trend in primary production Primary production in seaweeds Measurement of primary production Further reading

3 Microbial Ecology: Production and the Decomposition of Organic Material

3.1 3.2 3.3 3.4 3.5 3.6 3.7 3.8

Introduction The microbial powerhouse The ecological context in which the marine microbes are embedded The decomposition process Key organism groups in the oceanic microbial food webs The dynamics of bacterial growth and its measurement The seasonal cycle of production and consumption Oceanic microbes in global carbon and nutrient cycles Further reading

4 Secondary Production

4.1 4.2 4.3 4.4

Introduction Measuring secondary production Drivers of secondary production Size structuring in marine food-webs

33 33 36 42 43 44 46 49 53 64 69 69 76 78 87 89 89 89 91 93 97 115 118 123 125 126 126

129 134

136

Detailed Contents

4.5 Human impacts on secondary production Further reading

136 140

Part 2 SYSTEMS 5 5.1 5.2 5.3 5.4 5.5

Estuaries

6 6.1 6.2 6.3 6.4 6.5 6.6 6.7

Rocky and Sandy Shores

Introduction Estuarine organisms Productivity and food webs Diversity patterns in estuaries Other 'brackish-water' systems Further reading Introduction What is the shore? Environmental gradients and the shore Causes of zonation The organization of shore communities The shore network The future of rocky and sandy shores Further reading

7 Pelagic Ecosystems

7.1 7.2 7.3 7.4 7.5 7.6 7.7 7.8

Introduction Definitions and environmental features Pelagic inhabitants: consequences of size Temporal and spatial variability in pelagic ecosystems Sampling the open ocean Pelagic fisheries Regime shifts in pelagic marine ecosystems The future for pelagic marine ecosystems Further reading

8 8.1 8.2 8.3 8.4 8.5 8.6 8.7

Continental Shelf Seabed

Introduction Definitions and environmental features The seabed habitat and biota Functional roles of the biota Food webs in shelf systems Characterization of seabed communities Specific habitats Further reading

9 The Deep Sea 9.1 Introduction 9.2 Definitions and environmental features

143 143 151 159 165 168 171 172 172 173 174 179 181 190 192 193 194 194 195 198 200 208 212 213 214 216 217 217 218 224 231 235 239 241 250 251 251 252

Detailed Contents •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

9.3 Food supply to the deep sea 9.4 The organisms of the deep sea 9.5 Hydrothermal vents - islands in the deep sea Further reading

260 263 271 275

10 Mangrove Forests and Seagrass Meadows

277 277 278 290 304

10.1 Introduction 10.2 Mangrove forests 10.3 Seagrass meadows Further reading 11 Coral Reefs

11.1 11.2 11.3 11.4 11.5 11.6 11.7 11.8 11.9

Introduction Reef development and distribution Corals and coral communities Coral reef productivity and food chains Reef fauna Threats to coral reefs Reef growth and bioerosion Dynamics of reef animals Reefs and human society Further reading

12 Polar Regions

12.1 12.2 12.3 12.4 12.5 12.6 12.7 12.8 12.9 12.10

Introduction What is pack ice? Arctic vs Antarctic pack ice Life in a block of ice Sea-ice edges Polar benthos Polar bentho-pelagic coupling Endemism in polar benthos Gigantism in polar waters Birds and mammals Further reading

305 305 305 309 311 313 314 318 320 322 323 325 325 329 331 332 337 341 343 343 344 345 352

Part 3 IMPACTS 13 Fisheries

13.1 13.2 13.3 13.4 13.5 13.6 13.7 13.8 13.9

Introduction Global fisheries Fish production Fished species and their fisheries Fish population biology Fishing methods Fish stock assessment The management process Environmental impacts of fishing

357 357 357 361 361 362 363 366 368 370

Detailed Contents 13.10 Ecosystem-based fishery management

375

13.11 The future of fisheries

Further reading

376 376

Aquaculture

377

Introduction Aquaculture past and present How do we produce food from the sea? What is cultivated and where? Food requirements and constraints The role of biotechnology Negative effects of biotechnology Cultivation systems Cultivation of fish in cages Cage cultivation: a lousy system? Breaking away from the coastal margin Shrimp cultivation: the gold rush Shrimp farming and mangroves Cultivation of molluscs Ranching at sea A conservation role for aquaculture? Further reading

377

Disturbance, Pollution, and Climate Change

401 401

14 14.1 14.2 14.3 14.4 14.5 14.6 14.7 14.8 14.9 14.10 14.11 14.12 14.13 14.14 14.15 14.16

15 15.1 15.2 15.3 15.4 15.5 15.6

16 16.1 16.2 16.3 16.4 16.5 16.6 16.7 16.8 16.9

Introduction Ecological role of disturbance Measuring the effects of human activities Agents of change Climate change Interaction of multiple factors Further reading Conservation

Introduction Why conserve? What to conserve Economics of conservation Conservation policy and legislation Conservation in action Evidence-based conservation Life-cycle analysis The future Further reading

References Weblinks Index

378 381 383 385 386 386 387 387 389 391 393 394 395 397 398 400

402 406 413 421 426 428 429 429 431 432 435 439 442 447 448 448 449 450 485 489

Patterns in the Marine Environment

Chapter Summary

and from millions of years ago to th e present day. Pat-

Most space for li fe on Earth is in the vast oceans and seas.

terns occur in species' richness, abundance, ancientness, or

Li fe began in the oceans and remained confined to thi s

size, all of w hich are indicators of powerful changes o n th e

environment for hund reds of mi llions of years. Most maj or

planet surfac e in t ime and space. Oceans have wid ened or

gro ups (ph yla) of animals never left it. The wid e expanse

been co mpressed, risen and fallen , heated and cool ed, and

of th e oceanscape changes dramati cally, from und ersea

remain dyna mic places; most will have changed drastically

mountain ranges to sedi ment plains and coral reefs, to for-

in j ust the lifes pan of the reader of this book. Examining

ests of kelp. Pattern s of organisms, so obvious at th e shore,

som e of the maj or pattern s in organisms and their bio logy

are also evide nt from the po les to the trop ics, from coasts to ocean cent res, from th e shallows to the deep abyss,

gives a strong insight into the processes that determine

1.1 Introduction Humans are a land-living species and consequently most familiar w it h the terrestrial environme nt, yet the Earth is a blue planet and the oceans cover > 70% of its surface . Close to the continents this aquatic ecosystem takes the form of shallow seas just a few hundred metres deep known as the continental shelf. However, around Antarctica the mass of the huge (3-km thick) icecap has depressed the shelf to be as deep as 1000 m in places. Most of the oceanic habitat (and 51% of the earth's surface) is nearly 4000 m deep. This three-dimensional environme nt is populated throughout its depth by many organisms. The steep rises up to the continental shelf contrast with the large sedime nt-covered basins that span tens of thousands of square kilome tres, broken only by the undersea mountain ranges of midocean ridges. At these locations oceanic crust is formed and gradually moves outwards, pushing continents apart, and eventually disappears down beneath continental crust, forming deep oceanic trenches. Considering its volume ,

success and evol uti on of li fe on Earth.

the vast majority (c.99%) of the Earth's habitat is marine, where most major types of animal (phyla) have evolved and continue to live exclusively. Most of the vast water column and seabed (ben thic) habitat remain unobserved by human eyes. The first biological samples were only collected from the continental shelf of the Amundsen Sea (whic h spans 40 longitude- equivalent to the Med iterranean) in 2008. New species are still routinely found in deep-sea samples and even some of the larger animals on Eart h which live there, megamouth sharks and giant squid, have only recently been seen alive in their natural habitat. 0

Our impoverished knowledge of the ocean 's inhabitants is emphasized by the fact that it is not just new species that are described , but that even some of those that are high-profile and common , such as the crown-of-thorns starfish, now appear to be several species (like giraffes on land). Furthermore, entirely new classes or phyla (the highest taxonomic levels of animal types) have been discovered in just the last couple of decades.

Chapter 1 Patterns in the Marine Environment across a wide range of scales in time and space, and form the subject of this first chapter and are themes that reoccur throughout this book.

Box 1.1: A new phylum In 1995 an entire new phylum of tiny animals, the Cycliopho ra, was repo rted from a discovery two years earlier. As it is only 350 u rn in size and superficially resembles individuals of several other phyla

of small animals (Gastrotricha, Rotifera, and Entoprocta) , it could be considered unsurprisi ng that such animals are still being discovered. Surprisingly, though, the single species (Symbion pandora) lives on the mouthparts of Nephrops norvegicus-a very common, well studied, and widely consu med species,

ofte n referred to as scampi. S. pandora, or the 'Pandora', attaches to its host using a sucker and suspension feeds on particles in the water, a small parasitic male (whose sole purpose seems to be for breedi ng) is also shown attached in the picture below.

Feeding tentodes - - - -

'------ Anached male

'------ Stalk

-/--7"----- Sucker

Standing at the edge of a forest looking out over a prairie, lake, or into the tree canopy, it is easy to see how fragmented the land can be. Furthermore, even a simple climb up a mountain can reveal altitudinal changes and, though few have experienced it, most people understand that polar regions are deserts compared to the generally species-rich tropics. In contrast, the water column and wide ocean basins might be envisaged as fairly monotonous, uniform ecosystems. However, there are many features that punctuate them abruptly or gradually into many different environme nts . Changes in time, topography, chemis try, and oceanography allow for the development of patterns

1.1.1 Zonation Patterns in the marine environme nt are often beyond our immediate perception; we cannot always see them. Often, patterns are only revealed through sampling and subsequent interpretation. The number and size of samples collected and the type of equipme nt used will have a profound effect on what is found. Strong differences in opinion exist about even the most basic marine biotic patterns, each defined by evidence from a discrete set of samples (see also sampling in Chapter 8) . In many respects, patterns in the sea resemble those on land; for example, at a large scale along grad ients of solar radiation (latitudinal gradients), altitudinal (which in the marine environment is depth, thus bathymetry), from the coast to ocean/continent centres, and from young to old areas (e.g. from the mid-Atlantic ridge (new) to the far eastern or western Atlantic sea-floor (oldest)) . In the shallowest parts of the sea there are plenty of places where the type or nature of the organisms changes over tens of centimetres or metres, which we term zonation (Chapter 6). In warm tropical waters, the type and dominance of corals changes quickly with depth (Chapter 11). In polar seas the abundance and richness of marine life alters equally sharply in response to decreasing physical disturbance by floating icebergs that scour the seabed (Chapter 12). In certain types of environment, such as estuaries (Chapter 5) , rapid changes in biological constituents occur along the length of the estuary in response to a suite of changing environme ntal vari ables; patterns that are repeated at virtually all latitudes. Zonation is most apparent where the land meets the sea and it is here that it has been studied in most detail (Fig. 1.la). Zonation is not just driven by tolerance to physical conditions (though this is most important at the high shore level) . Connell's (1961a, 1961b) wo rk on barnacles demonstrated that interspecific competition and differential predation pressures strongly influence the location where species survive. In temperate regions across the globe different species and colours of algae and lichens indicate the grad ient of immersion on the lower and upper regions of the shore. Shore zonation is equally apparent in some muddy shores in changing saltmarsh vegetation or, at tropical latitudes, in mangrove trees and their associated fauna. Only towards the polar regions does shore zonation become increasingly constrained and ultimately disappear altogether at very high latitudes (Fig. 1.1b). At high polar latitudes (Fig. 1.1c), very few organisms can survive the constant abrasion by floating ice during the summe r, coupled with encaseme nt in winter ice

1.1 Introduction •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

as the sea surface freezes . Conversely this phenomenon causes zonation in the sublittoral zone as the frequency of ice scour (Chapter 12) decreases with depth and distance from the shore. In many ways, patterns in the sea resemble those on land with large-scale gradients in solar radiation , altitude

(depth), and geological age.

Zonation is driven at the land/sea interface by a combination of physiolog ical tolerance and competition for space and predation pressure. See Chapter 6 for a dia-

grammatic explanation of different zones in the intertidal and near-shore zone.

The littoral zone has gradients of immersion, exposure, shade, roughness (rugosity), topography, and many others.

With such a variety of micro-environmental variation it is easy to understand why the littoral zone is species' rich. Species specialize in response to different tolerances. exposure, food, and feeding methods (as well as to other factors), so there is potential for many species to co-occur when many environmental factors interact. Examples of this on a rocky shore include those species specialized to living on exposed rock face, in crevices, on the undersides or tops of boulders. overhangs, and in pools. But what about the variability of conditions away from the seabed, i.e, in the water column? In this seemingly uniform environment. many species also occur in close proximity. Hutchinson (1961) referred to this as the 'paradox of the plankton' (see Current Focus box in

40

50

60

70

Latitude "S

(el

Figure 1.1 Shore zonation. (a) Bands of barnacles, algae, and mussels in Tierra del Fuego (54°5), southern Argentina.

(b) Intensity of zonation in relation to latitude and the position of t he Polar Frontal Zone (PFZ). Diagram is a schematic suggesting manner of change of intensity of zonation based on strength of littoral macrobiota patterns at sites at

latitudes ind icated by (1) Tristan da Cunha, (2) Gough Island, (3) Prince Edward Archipelago, (4) Falkland Islands, (S) South Georgia, (6) Signy Island, (7) South Sandwich archipelago, (8) Haswell Island, (9) Adelaide Island, (10) Vestfold Hills, (1 1) McMurdo Sound. (Sa) Is Tierra del Fuego, which is actually north of the PFZ. Adapted from Barnes & Brockington (2003). (c) A denuded polar shore (Adelaide Island).

Chapter 1 Patterns in the Marine Environment 1.1.2 Oceanography

Box 1.2: Determinants of zonation patterns Sessile, arm o ured, ci rri ped crustaceans (com monly known as barnacles) are very abun dant and are even the dom inant organisms on hard surfaces on temper-

ate rocky shores. Connell (19 61 a) studied the distribut ion of one speci es (Chtham alu5 stellatus (see fig ure, below left), w hich occu rs in a dist inct vertical zone. Relative to most other marine organisms in the littoral, this zone is high up, so C. stellatus ind ividuals have to wit hstand high ly variable temperat ures,

dessicati on, and longe r periods wi t hou t foo d. This zone is not , however, of th eir choosing. C. stellatus larv ae settle cons iderably be low (and even above) this level on t he shore. Other factors, principally com petition w ith oth er organisms, such as the barnacle

Semibalanus balanoides (below right) , red uce the surv ival of recruits on t he lower shore to near zero. The more heavily armoured plates of S. balanoides crush C. stellatus individ uals w hen space becomes limit ing. The compet itors (and many of the predators) of C. stellatus fi nd the harsh con ditions hig her up on t he shore too d ifficult to endure so only at this level can C. stellatus prosper.

Chapter 7). The plankton contains many permanent representatives, but also many transient constituents, such as the larvae of seabed animals (b ent h os) . Larvae of individual species may diffe r in their time of release. residence time in the plankton, whet her they are feeding (p la nktotroph ic) , or have their own yolk sacs (lecithotrophic), and behaviour. The water column, like the land and seabed, has many sh arply changing physical features that effectively form environmental barriers that constrain the organisms that live there (Chapters 2, 3, and 7) . Benthic organisms are those that live in , on , or are anchored to the seabed , whereas those that move freely in the water column are known as pelagic organisms.

On a larger scale the water column has a strong pattern of zonation that occurs across its full depth range. similar to that found in the littoral zone. Most importantly, in the top few to 200 metres of the water column there is enough light (during the day) fo r primary producers to photosynthesize, termed the euphotic zone (Chapters 2 and 7) . As a result, the top 100- 200 m of open ocean water and 1-50 m of coastal water is a very different environment to that found below. Of course, even w ithin the euphotic zone there is a strong gradient of light intensity and wavelength with depth. Beyond a depth of 1000 m (most ofthe world's ocean volume) the ocean is effectively lightless, wit h a few smallscale exceptions, such as the bioluminescence produced by bacteria found in the light organs of deep-sea biota. Light striking the surface of the marine environment also imparts heat. thus the surface layers are the warmest and hence have lower density than the cold water beneath. Globally the temperature of deep water is relatively uniform at just a few degrees Celsius, in contrast with shallower water temperatures that fluctuate w ith latitude and season. In the polar regions, surface water is near freezing point at - 1.8So C in the winter, and just positive in summer. However, the water in polar regions is well mixed, as dense cold water sinks and wave height and wind speed are greatest at a latitude of 50- 60" (Fig. 1.2). Moving away from the polar regions, wit h a few exceptions, such as regions of upwelling, the global ocean is stratified into a warm upper layer, a rapidly cooling zone. and a lower cold zone. The n ature of thermoclines ch anges from place to place but in general the thermoclines in the tropics are more than 10°C warmer than those in temperate regions, and they are permanent rather than seasonal. Such stratification is important as organisms require nutrients and minerals, as well as light and respiratory gases. Thus away from permanently mixed areas, such as polar seas or upwelling zones, the surface layers of the sea also have strong changes in molecules used or produced by organ isms, such as nitrates. Locally other gradients, e.g. haloclines (salin ity) or pycnoclines (density), may also stratify water layers. The salinity of seawater is typically about 35 psu . Generally, changes in salinity that occur with eit her latitude or longitude across oceans are small, but are a little greater in the tropics (due to increased evapora tion of surface water) and lower close to continents and in the Arctic due to the influence of greater fresh water run-off (Chapter 5).

1.1 Introduction •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Thermoclines are a vertical zone of rapid temperature change in t he water column . Haloclines occur where two

Table 1.1 Example of changes in the marine

water masses of different salinity interact, e.g. in an estu-

environment wit h time-scale.

ary or towards the head of a fjord , where freshwater meets seawater. Both changes in salinity and temperature will affect water density.

Time-scale

Feature

Hours

High to low tides

Days

Spring to neap tides

Months

Seasonal temperature/ salinity/ currents

Years

EI Nino Southern Oscillation

Decades

Climate warming, ice sheet retreat

Centuries to millennia

Ice ages, Milankovitch cycles, sea-level fluctuations, sea floo r

psu-practical salinity units (see 5.1.4.).

There are many features that partition the ocean environment, and the positions of continents, islands, and subsurface marine mountain chains form obvious physical barriers. In the open ocean, differences in water density, currents, and fronts provide the conditions that lead to distinct water m asses. See Chapter 9 to understand more about the physical

spreading

and biological processes around sea mounts and Chapter 7 to understand how fronts form in the ocean .

Although current d irection and velocity of water m asses and patterns of wind across the globe are complex, there are general large-scale patterns th at occur, m ost obviously in water flow. Most deep (seabed) water is derived from the Southern Ocean . Cooled dense w ater (termed Antarctic Bottom Water, AABW) sinks in the Southern Ocean and flows away from Ant arctica, well into t he northern hemisphere abyssal regions. There m ay be seve ral curren ts that occur at diffe rent depths betwee n the deep AABW a nd surface water. For example , cool north ern water flows sout hwards in the mid-region of the water colum n in the Atlantic. At the sea surface, the world's oceans are dom inated by a series of gyres rotating clockwise in the northern hemisphere and ant iclockw ise in the southern hemisphere. Where these meet in the equ atorial region, strong curren ts flowin g westwa rds occur (as well as smaller countercurrents flowing eas twards). The current system of t he Southern Ocea n is dom inated by the circum polar curre nt, wh ich flows around the continent in a clockw ise direction. This is bot h the fastest m ajor curre nt in the world (flowing at 10 em s') and the only one that spans the entire water column from surface to the abyssal seabed (5 km down) . Surface currents are particularly important in mixing the water layers, which is a powerful agent t hat counters stratification, at least in the sh allower layers of the water column . As well as these large- and small-scale spat ial variations, the m arine environm ent changes over a variety of time-scales (Ta ble 1.1 ).

II

(.) Atlantic

10

0

1•

Podfic

lrdlun

-- , '. .~ c

•

Mean global

~

,S

••~ c 0 0

•c 0

c

e

•

~

5 700 N

5~N

,.,

lOoN

300 N

70°$

W5

Latitude(degre&s)

5r.:-:-(b)

-

-

-

-

-

-

-

-

-

-

-

-

-

-----,

t i

-a

• • o

•

J!

Latitude(degre&s)

Figure 1.2 The di stribution of mean wind speed and wave action in the marine environment with ocean basin and latitude. Plotted from data from Bentamy et al. 1996.

Chapter 1 Patterns in the Marine Environment Surface currents are particularly important in mixing

20 , --

-

-

-

-

-

-

-

-

-

-

-

-

-

---,

the water layers due to the frictional stress that occurs between two moving bodies of water (also see Chapter 8 to understand laminar flow and boundary layer effects

of flow at the seabed and how this affects biology).

1.1.3 Climate There is now much concern about accelerating climate change and the extent to which human activities are linked to this phenomenon (Chapter 14). The climate ofthe Earth, however, has been in a state of constant change; only the magnitude of the rate of change has varied with time (Fig. 1.3) . The most familiar environmental variable associated with climate is temperature. While air or land temperatures fluctuate more dramatically, sea surface temperature (SSn changes are more subtle due to the huge volume and high latent heat of water, which give it a strong buffering effect. It is important to understand what a change in t he rate of

change means. The following is illust rat ive only: if global ocean temperatures were increasing at a rate of 0.1 °C every 10 years then th is is a constant rate of change; however, if global ocean temperature changed O.1 °C from

year 1-10 and then 0.2°C from year 11-20, this is an increasing mag nitude of rate of change. In other words

the world ocean would be heating up faste r and faster. When global temperatures are high, sea-levels rise through thermal expansion and the melting of ice. There is great connectivity between many environmental variables, such that when SSTs rise. other environmental parameters change concomitantly. For example. warmer water is able to hold less gas and hence the oxygen needed for respiration (Chapter 14) . At present. icecaps occur over the two polar regions. which is a relatively unusual condition in palaeontological time-scales. Ice area expansions occur every winter (the geographical extent, but not the volume, of Antarctic sea ice doubles from summer to winter) . On a very much larger scale, each ice age spreads the icecap to lower latitudes from the poles, then retreats in interglacial periods. The rise and fall of sea-level has clear and important implications forthe marine habitat (Fig. 1.4) : the shallow sloping continental shelf is one of the most important habitats formost organisms with 90%ofthe World's marine primary production (Jennings & Kaiser 1998) . The extent of the continental shelf changes considerably with just a 50 m change in mean global sea-level (Chapters 5 and 8) . Changes in ice extent, which occur simultaneously with those in sea-level, are also important. literally scraping away entire habitats and thereby open up new space for colonists.

-40

--,\0

- 20

0

Millions of yeors ogo Figure 1.3 Sea temperature change with time in the

Southern Ocean (Adapted from Clarke et al. 1992).

The effects of sea-level rise inevitably mean that nearshore communit ies and continental-shelf comm unities are the most recently establ ished when measured in geological time-scales.

Strong signals of climate change have been found in the last century, particularly from 1916 to 1945 and from 1976 to the present. Earth's mean surface air temperature has increased by 0.6°C in a century. but some regions. such as the Arctic and west Antarctic air and soil temperatures. have warmed more than this in a decade (Walther et al. 2002) . Most recently, significant climate-related sea temperature increases have been measured in the Scotia and Bellingshausen seas of West Antarctica (Chapter 12) . There have. however, been drastic and rapid changes in the Earth's surface temperature before. even in the sea. These changes occurred in response to massive methane clathrate releases from below the seabed, major volcanic events. and after meteorite collisions (such as that near the Yucatan at the end of the Cretaceous period) (see Box 1.3) . Other prominent aspects of recent climate change have included increasing CO2 levels and changes in stratospheric ozone thickness. The first of these is strongly related to temperature changes through heat trapping and is referred to as 'the greenhouse effect'. Seasonal thinning of the upper atmosphere ozone (ozone holes) permits increased penetration of the ultraviolet wavelengths of light with their potential damaging effects to organisms. UV penetration of water is limited to just a few metres of the sea surface. so although potentially a serious issue in terrestrial, littoral, and very shallow aquatic habitats. it does not affect the majority of the volume of the global ocean environment. Aside from a strong signal of seasonality in the oceans and climate change. there are various other longer term but cyclical events such as Milankovitch cycles (which concern solar activity. such as solar flares) and the El Niiio Southern Oscillation (ENSO) . ENSO has been the subject of considerable scientific discussion after

1.1 Introduction •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

(0) 250 200 150 m 100 50

~~ 50-m long giant kelps that grow up to 0 .5 m a day. Production is measured using

of the total 'carbon captured' on Earth through the process of photosynthesis and production of biomass takes place in

bottled incubati ons or, increasingl y, from space using satel-

marine systems, and over 90% of the earth's CO2 is cycled

lite-borne ocean colour sensors that detect photosynthetic

and stored through marine systems. This chapter introduces

pigments in surface waters. The conversion of inorgan ic carbon into biomass, its subseq uent sinking to th e seabed,

the maj or factors that control primary production , and how to measure it.

2.1 Introduction The photosynthetic organisms of the ocean, as on land, are for the most part the fundamental food source on which marine ecosys tems are based (Field et al. 1998; Falkowski et al. 2000; Nellemann et al. 2009). In coastal waters , the large stands of seaweeds exposed at low tide, submerged kelp beds, or gently wafting meadows of seagrasses that fill coastal lagoons, are the obvious plants. These primary producers grow in much the same way as their terrestrial counterparts: assimilating carbon through photosynt hes is, and growing by taking up nitrogen, phosphorus, and a host of necessary ot her minerals and trace substances to generate new biomass. When considering photosynthesis and the production of new biomass we need to consider both production and loss processes, and both are important for this chapter (Fig. 2.2) . In the most simplistic terms, light energy is trapped and used to produce organic matter through photosynthesis, and this organic matter is broken down through respiration to release energy and heat.

Figure 2 .1 Sun light is the energy source for the primary producti on in the wo rld 's oceans, and is therefore the fundamental limiting factor co nt roll ing ocean productivity

(photograph David Thomas).

Chapter 2 Primary Production Processes The global scale of this cycle is m assive and the annual cycle of production and consumption has been calculated to have the same energy production of about 1.5 x 10 14 watts per year, equivalent to the annu al output of around 150 000 nuclear power stations . It is also a relatively efficient process, with 40% of the solar rad iation absorbed converted into organic material, which is slightly better than the best modern power station . See Kolber (2007) for an excelle nt description of the microbial ene rgy cycle of the oceans, in a way that forms a brief synops is of much that is covered in this chapter.

There is a large body of information on primary produc-

tion processes in aquatic systems, and for this chapter, rather than an extensive list of citations and reference list (as used by other chapters), readers are rather encouraged to use the extended reading list at the end of the chapter. These have been selected for the overviews they give and the synthesis of the primary scientific literature.

Citations are used for more specialized points, possibly not so widely covered in the more generalized texts.

Phorosynthesit

Liqht

(visible radiation)

I :I

Respiration

Primary production is the formation of organic matter

Organic meienel & oxygen

through the trapping of light energy and assimilation of

~

,, ,

inorganic elements.

.:: " o

~ - - . _ - - - - - - - ~ - - - - - - - _ . .- - - - -

, ,,

Heat (infrared radialio n)

rto;l

~

o

•E

!

2.1.1 Marine plants and algae

J

Mangroves, salt m arsh systems, and seagrass beds (see Chapter 10 for detailed cover of these systems) cover less than 0.5% of the global marine system , although it has been estimated that they account for between 50 and 71 % of all carbon storage in m arine sed iments. Although they are only about 0.05% of the plant biomass on land, they still represent a considerable carbon store when looked upon on global terms (Table 2.1; Laffoley & Grirnsditch 20 09; Nellemann et a1. 2009) .

~

IFlowofenergy I - - -

IFlowof material

I

Figure 2.2 The massive biological cycle. The energy of light, inorganic nutrients, CO 2 , water, and salts are co nvert ed to a complex mix of organic compounds and oxygen by photosynthetic organisms. Respiration releases CO 2 and energy, at the expense of oxygen and recycles nutrients to the inorganic state (image: Peter J. Ie B.

Williams).

Table 2.1. Comparison of global carbon storage by mangroves, seagrass meadows, kelp forests, and comparative terrestrial systems (extracted from Laffoley & Grimsditch 2009).

Ecosystem Type

Standing stock carbon (gC m-Z ) Plants

Mangroves

Soil

7990

Global carbon stocks (PgC)* Plants

Soil

1.2

18 4

7000

0.06

2. 1

120 -720

na

0.0 1-0.02

na

18 8

8000

3

128

Boreal forest

6423

34380

88

4 71

Temperate forest

5673

96 15

59

100

Tro pical forest

1204 5

12 2 73

2 12

2 16

Seag rass beds

Ke lp forests Croplands

.. P = peta and 1 Pg is equivalent to 10 15 g.

2.1 Introduction •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Figure 2.3 (a) Mangroves, li ke these in the Philippines, are hotspots of primary production in many coastal regions

(photograph: David Thomas). (b) Seagrasses are the only true marine plants and form extensive beds of high productivity in temperate and tropical coastal waters (photograph: Ylva Olsen).

Looks can be deceptive-while the seagrasses and mangroves, and many of the species inhabiting salt marshes. are true flowering plants (Fig. 2.3), the seaweeds are not. Seaweeds are algae and, although they are photosynthetic organisms, in contrast to the terrestrial plants, they are non-

(a)

flowering and do not have roots. leafy shoots, or sophisticated tissues for transporting water, sugars. and nutrients. Their major evolutionary lineages remain controversial, although recent molecular advances clearly indicate that,

apart from a few of the green algal species, the algae are only remotely linked to land plants. Seaweeds, seagrasses, and microscopic algae and bacteria are the primary producers in the oceans.

Seaweeds, or rather macroalgae, are a diverse group. ranging from mere encrustations on rock surfaces. to giant

(b)

brown algae such as Macroeystis prolifera and Neroeystis leutkaena, which reach lengths over 50 m long (Fig. 2.4) . The latter species is an annual. and grows taller than a mature oak tree in a single year. Macroalgae are easily seen by the human observer, but we need the assistance of a microscope to observe the microalgae that generate most of the primary production

in the oceans (Fig. 2.4) . We may not be able to see these individual phytoplankton cells, but we can certainly see their effects : clear waters can be turned brown almost overnight. when light, temperature. and nutrient conditions in the water are favourable. such that phytoplankton are induced to grow at such a rapid rate that they form an

Figure 2.4 The primary producers of marine systems

algal bloom.

range from large seaweeds (macroalgae) that grow attached to t he sea floor (a), down to microscopic

Phytoplankton can bloom rap idly given enoug h light and a sufficient supply of inorganic nut rients.

phytoplankton (b). Note the x1 0000 difference in scale between t he two images (photographs: Ian Lucas/Gerhard Dieckmann).

Chapter 2 Primary Production Processes

2.1.2 The phytoplankton The microalgae vary considerably in size ranging from about 2 urn in diameter to over 200 urn. They are very varied in form, some of the most elaborate being the silicate (glass) encased diatoms that have beguiled naturalists since the first microscope lenses became available (Armbrust 2009; Box 2 .1) . However, these microphytoplankton are not the only photosynthetic organisms to be found in the phytoplankton. Since the 1980s, a host of much smaller prokaryotic photosynthetic organisms have been shown to be an important component of the phytoplankton. These include cyano-baeteria such as those from the genus Synechococcus, cells about 1 urn in diameter, which are found in all waters except the polar oceans. Pelagic prochlorophytes in the genus ProchlorococclLS (cells of O.7 I'm diameter) were discovered in the late-1980s. These very small picoplankton are thought to be found in most waters around the globe, and contribute a high percentage of the total primaryproducrion ofopen waters (Figs 2.5 and 2 .6) . However, we are only just beginning to understand their role in global primary production, and in many oceanographic studies these tiny organisms remain overlooked (Binder et al. 1996; Fuhrman & Capone 2001; Karl 2002; Scanlan & West 2002) . Femtoplankton: 0 .02 to 0 .2 I'm. Picoplankton: 0 .2 to 2.0 I'm. Nanoplankton: 2.0 to 20 prn, Microplankton: 20 to 200 prn, Mesoplankton: 0.2 to 200 prn,

Picoplankton, 0 .2 to 2 IJm in d iameter, are important contributors to plankton primary production.

This chapter describes production processes in marine systems with a focus on photosynthetic organisms and the constraints acting on this process. while in Chapter 3

we explore the role of non-photosynthetic organisms. The growth ofall photosynthetic organisms is restricted primarily by the supply of light, carbon dioxide, oxygen, and the main

macro-nutrients (phosphate. silicate. and nitrate) . However, even when all these factors are adequate, the lack of trace elements can be enough to restrict growth (see Box 2.6).

There are many other mechanisms for utilizing energy sources other than light, as well as different sources of carbon for the generation ofnew biomass. Itis only proper that at least some mention is given to the diversity of metabolism. especially since this variety is fundamental for the microbial ecology (Chapter 3) and biogeochemical pro-

cesses found within marine systems.

2.2 Photosynthesis Algae (micro- and macroalgae) and cyanobacteria, such as Synechocccus and Prochlorococcus, are photoautotrophs, as they use light for their energy source and carbon dioxide (or one of its various forms in the water; see 2.2.1) to produce new organic matter. The photosynthetic reaction can be divided into a light

reaction and a dark reaction. The light reaction converts light into metabolic energy and reducing power. The dark reaction utilizes these to convert (fix) carbon dioxide and

form organic material. The overall reactions are :

+ light => 4[H+] + metabolic energy + 0 2

Light reaction 2H20

+ metabolic energy + CO2 => [CH,D] + H 20,

Dark reaction-HH" l

where [CH 20 ] is used as a general symbol for organic

material. Photoautotrophs use light as an energy source and carbon dioxide to produce new organic matter.

Figure 2.5 The advent of satellite-borne ocean colour sensors enables scientists to look

at the global distributions of phytoplankton in surface waters.

This image shows the SeaWiFS average chlorophyll concentration

collected from January 1997 to July 2005 (image: SeaWiFS Project, NASA/Goddard Space Flight Center and ORBIMAGE).

2.2 Photosynthesis •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 2.6 A co ncent rated w ater samp le f rom th e Arabian Sea, Indian Ocean, stai ned by t he fluorescent DNA stai n

DAPI , and viewed by ep ifluo rescence microscopy. Left: under exc itat ion by UV light, individual bacteria and flagell ates are v isible by th eir DAPI-induced blue flu orescence. Ri ght: the same preparati on under blu e light excit at ion. Yellow (Synechococcus sp.) and even smaller red flu orescing pi coplan kton cells (Prochlorococcus sp.) are v isible. Unlike in th e upper pi cture, only th e auto-flu orescence of the natural p hotosynt hetic pigments can be seen. Th e large, very bright cell is a dinoflagellate (Gymnodinium sp., about

zopm in

d iameter) (p hotog rap hs: Marcus Reckermann).

Photosynthetic organisms contain specialized light-sensitive pigments, such as chlorophylls, to absorb light energy, which is subsequently transferred to reduce CO2 to organic compounds. CO, is fixed w ithin the Calvin cycle, and the first step of the reduction of CO, in t his cycle is catalysed by the enzyme ribulose bisphosphate carboxylase/oxygen-

Box 2.1: THE DIATOM FRUSTULE

ase (RUBISCO). It is important that there is a high supply of CO, at the active site of RUBI SCO. Many species ofcyanobacteria and algae have active carbon-concentrating mechanisms (CCMs) that m aintain t he required high levels of CO, within the cells (Box 2.3).

The strength of the diatom frustule seems to be a most remarkable feature of these algae. Although diatoms are

Diatoms, a group of microalgae, are major contributors

grazed, they are clearly not an easy food sou rce to break

to the phytoplankton of marine and fresh water. There

into. The unique architectures and design of the frustules

are also many diatom species that live within and on top

give them immense mechanical strength, and the dia-

of sedi ments, as well as species that grow as epiphytes

tom silica has material properties co mparable to cortical

on the surfaces of animals, plants, and macroalgae (for

bone wi th greater elasticity tha n glass. In fact, the grazers

comprehensive review see: Arm brust 2009). The charac-

must exert t remendous force, and therefore expend extra

terist ic of all diatoms is that they produce cell walls made

energy, to break the frustules open and get to t he cell

of silicate, which are not only very beautiful to look at, but

also apparently very strong (Brownlee and Taylor 2002).

10)

Diatoms can form dense blooms in coastal wate rs, and are an important food source for protozoan and zooplan kton grazers. However, once formed, the diato m cases, or frustules, dissolve only slowly, and in some regions of the world's oceans, the sediments are characterized by diatomataceous or siliceous oozes: massive accumulations of diatom frustules that have sunk from the surface waters over eons of t ime. Many diatom species have h igh ly ornate f rustules, with spines, spi kes, hooks, and other protrusions. Many of these adaptations are thought to resist sinking and aid colony/chain formation, but also deter grazers from

Sophi sticated mod el s of diatom frustules, such as

attempting to eat them. The spines of diatoms have even

th is co mp uter-generated p ennate diatom, are helping

been known to clog fish gills and pierce delicate mem-

researchers understand how th e st ructures of the silica

branes in gill t issues.

cell w alls are related t o th eir ecol o gy and evo lut ion (image: Christian Hamm , Alfred Wegener Institute).

Chapter 2 Primary Production Processes

Ib) contents. Recent studies using microscopi c crash tests , as well as computer-based simulations, suggest that the diatom frustu les have arisen from an evolutionary arms race in w hich the capability of graz ing organisms to break

open its prey has been pitched against the evolution of very strong elastic diatom fr ustules (Hamm et al. 2003) . Both copepods and eup hausiids, major consumers of diatoms, have sil ica-edged mandibles an d gizzards lined with sharp crushing structures that function like teeth . It is likely that these structures have co-evolved w ith the devel-

Scanning electron micrographs of the mandibular

opment of the diatom frustu le, j ust as the anti-grazing

gnathobases of the copepod Calanoides acutus. The

sil ica spicules in grasses have co-evolved with the evolut ion of teet h in animals that g raze on land.

gnathobases of this species have strong tooth-like structures that consist of a different material from the rest of the gnathobases. These structures are very suitable for cracking hard diatom frustules (photograph: Jan Michels, Alfred Wegener Institute).

The strength of diatom frustules is possibly linked to an anti-grazing strategy.

that is primarily governed by the acidity (pH) , salinity, and temperature of the water: HCO; + H+

Carbon-concentrating mechanisms maintain high carbon

¢'>

H 2 CO,

¢'>

H 20 + cal.

dioxide levels at the RUBISCO enzyme. pH, temperature , and salinity govern the form of inorganic carbon in marine systems.

2.2.1 Carbon dioxide and photosynthesis in the sea Dissolved inorganic carbon occurs as several forms in seawater: carbon dioxide (CO,) gas, carbonic acid (H,C0 ,l , bicarbonate ions (HCO; ), and carbonate ions (CO:-). The proportions of these forms in seawater are in an equilibrium

In seawater with a salinity of 35 and a 'typ ical' pH of 8.1 to 8.3 (Box 2.4; Fig. 2.5) approximately 90% of the inorganic carbon occurs as HCO; . wit h 2 mmol L-l of HCO; and only about 10 umol L-1 in the form of CO, (Fig. 2.7) . RUBISCO requires CO, as a substrate . CO, is taken up directly by marine algae, but this is dependent on diffu -

Range of seawater

.. ..

o

.~ ~

e

10-1

§ = o o o o

.J!" 10-

2

Figure 2 .7 Relationship between pH and the relative proportions of dissolved inorganic carbon species in

10-' L-_---'--_~"---_--'--_ ____'_---'---'--_---': - _..J 4 5 6 7 8 9 10 II pH

seawater. Note the relative concentrations are plotted on a logarithmic scale (from Raven et al. 2005).

2.2 Photosynthesis •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

sion from low external concentrations compared with the high amount of carbon present in the Ilea; pool (Box 2.2). Surprisingly, there is still debate as to which inorgan ic carbon form is the predominant form used by marine algae (Burkhardt et al. 2001 ). He O; is t aken up by some algal species and this is converted wit hin the cell to CO 2 by the enzyme carbon ic anhydrase (Raven 199 5; Elzenga et al. 2000) . In m any algae, carbonic anhydrase act ivity has also been measured on the outer cell surfaces converting HCO; to CO 2 , which is then taken up into the cells. Note that in chemistry we talk about a substrate, whereas later in this book we discuss seabed habitats: the substratum.

Box 2.2: RUBISCO

The enzyme carbonic anhydrase converts

HCO~

to CO 2

within and on the outside of some cells.

Generally photosynthesis (both light and dark reactio ns) is represented by the following equation: 6e0 2 + 6H,o

+ 48 photons of light es 602 + C6H 1,o6.

This highly simplified equ atio n masks the great complexity of the photosynthetic process. However, it does show that for these organisms water is used as an electron donor to produce the reducing power in the overall metabolism, with oxygen produced as an end product. Because oxygen is produced, these organisms are referred to as being oxygenic photoautotrophs.

RUBISCO is an enzyme of very high molecu lar weight

of the cell. It is the most abundant protein on the planet (estimates of 40 million tonnes) . Given this estim ate, an d

and in planktonic algae amounts to 50% of the protei n

taking global produ ctivity at 100 x 10 9 tonnes per year,

light ,...-- HoNF ' --' CO, + H,O

Anoxic metabolism- alternative proton acceptors to oxygen

[CH,Oj [CH,Oj [CH,Oj

+ 2 HN0 3 + HNO, + 1 2 H,S04

-> CO, + H,O -> CO, -> CO, + H,O -> CO, + H,O

+ 2 HNO, + NH 3 1 + 2 H,5

Denitrify ing bacteria Denitrify in g bacteria Su lphate-reducing bacteria

2 H,5

• •• ••• •• •• •• ••• • • • • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• • •• •• •• • •• •• •• • •• •• •• •• • • • • • •• •• •• •• •• •• •• •• •• •• • •• • • •• • • • •• • • •• • • •• • • •• • • •• • • •• • • •• • • •• • • • •• • • •• • • ••

Chemoautotrophic metabolism-additional proton donors to organic material HN0 2 02 ~ HN0 3 Nitrite-oxidizing nitrifying bacteria

+;

NH 3 HzS

+ 0z + 202

~ ~

H20

+ HNOz H2S04

Ammonia-oxidizing nit ri fying bacteria Su lphur bacteria

2.4 Heterotrophic metabolism •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Sulphur-reducing bacteria use sulphate, thiosulphate, and elemental sulphur as electron acceptors in respiration. The metabolism produces sulphide or hydrogen sulphide, the rotten egg smell. characteristic of many anoxic waters and sediments. Methanogenic bacteria use CO2 as an electron acceptor, producing methane (CH4 ) as an end product. Anaerobic respi ration can resu lt in the production of potentially toxic products, such as hydrogen sulphide and methane.

Many of the products of anaerobic respiration are toxic (e.g, H2S, which is even more toxic than hydrogen cyanide) . This toxicity has very great ecological significance in water management, since plankton. zooplankton, and higher organisms (e.g. fish) are particularly susceptible to this toxicity and are at risk in environments that are prone to produce these compounds. Oxygen is always the preferred electron acceptor, and, providing there is oxygen in the water, these toxic compounds will not be produced.

Heterot rophic organisms obtain their carbon from the oxidat ion of organic matter, whereas autotrophic organisms obtain carbon from CO 2 ,

There are other groups of prokaryotes that use inorganic chemicals as their energy source (ch emo lit h o trop hs) . Most of these organisms obtain their carbon from CO 2, and so are autotrophs. There are many sources ofinorganic electron donor used by these prokaryotes, which include both bacteria and archaea. These include hydrogen sulphide, sulphur. ammonium, nitrite. and ferrous iron. Again some ofthese organisms can only survive in anaerobic conditions whereas others are tolerant of oxygen.

There are alternative proton acceptors to oxygen.

2.4 Heterotrophic metabolism Organisms that use chemical compounds as an energy source, rather than light, are called chemotrophs. The chemo-organotrophs include those bacteria and fungi that live via the oxidation oforganic compounds and in oxygenated habitats; they catabolize organic matter via aerobic respiration. Because these organisms do not get their carbon from CO2 , but rather from the oxidation oforganic matter, they are called heterotrophs. Those species that live in aerobic conditions use oxygen (oxygenic heterotrophs) as the external electron acceptor, whereas other species in anaerobic conditions (anoxygenic heterotrophs) can use other oxidized substrates. such as nitrate and sulphate. instead of oxygen as the terminal electron acceptor. The anaerobic heterotrophs are particularly important in anoxic sediments and the biogeochemical transformations that take place within these. These bacteria and fungi assimilate low molecular weight organic compounds, such as sugars, amino acids. pyruvate. ethanol, and acetate, which are transported directly into the cells. These organisms release hydrolytic enzymes to break down larger organic compounds into low molecular weight substrates that can then be transported into the cell and then respired and built up into new biomass. Heterotrophic organisms assimilate carbon derived from the oxidat ion of organic matter.

~----'--'---------)

( Anoxic means wit hout oxygen.

Figure 2.9 Beggiataa form filaments that twine together to form the white mats shown here. Beggiatoa is found

in habitats that have high levels of hydrogen sulphide, including deep hydrothermal vents, su lphur springs, sewage-contaminated water, and mud layers (photo: Samantha Joye, University of Georgia (www.marsci.uga.

ed u/Facu ItyPages/Joye/index.htmI). Examples of chemolithrophic bacteria include the sulphur-oxidizing bacteria, which grow in the tissues of hydrothermal vent organisms where sulphides are introduced into well-oxygenated seawater. Mats of Beggiatoa also grow on the reduced sulphur from the vents (Fig. 2.9) . Purple sulphur bacteria are another example oforganisms that oxidize H 2S and elemental sulphur: H,S + 20 , => SO ~- + 2W S + H,D + 3 / 20, => SO ~- + 2W

Nitrifying bacteria are vital for nitrogen cycling and the regeneration of nitrogen forms that can be utilized for growth in other organisms (Chapter 3) . Two groups of chemolithotrophic nitrifying bacteria exist: one group (including Nitrosomonas) oxidizing ammonium to nitrite and another group (including Nitrobacter) oxidizing nitrite

Chapter 2 Primary Production Processes to nitrate. The reactions in this vitally important process of nitrification are:

Nitrifying bacteria are important for nitrate regeneration in marine systems.

NH: + 0 , => NO; + 4W + 2eNO; + H20 => NO; + 2W + 2e-

Mixotrophs use both phototrophic and heterotrophic means for assimilating energy.

Box 2.4: Switching metabolism There are groups of organisms that can also swi tch

metabolism. Good examples are the anoxygenic phototrophic bacteria. These bacteria are capable of uti-

lizing organic carbon when it is available, but capable of photosynthe tic light utilization and CO 2 metabolism when organic carbon sources are low. These organisms are abundant in the upper oceans and are estima ted to

Bloom of the autotrophic ciliate Mesodinium rubrum

make up to 11% of the microbial community. There are also organisms, mixotrophs, which combi ne

in surface waters of the North Sea. This is an obligate phototrophic ciliate that contains endosymbiotic crypto-

the use of phototrophic and heterotrophic nutrition (e.g.

phyte chloroplasts. (b) The relationship between corals

Stoecker 199 9). Many phytoplankton species, phago-

and zooxanthellae is one of the best-known symbiotic

trophs, have been shown to be able to ingest particulate organic material to meet part of their nutritional require-

relationships in marine systems (photographs: David

Thomas).

ments. These range from small nanoflagellates that ingest bacteria and cyanobacterial sized particles th rough to photosynthetic dinoflagellates that can consume phytoplankton and small ciliates more than 10 urn in diameter.

gellates (zooxanthellae) and benthic corals. However, symbiotic relat ionships are also widespread in marine pelagic com munities. A variety of algal species from

Many phagotrophic algae increase their rates of particle

several classes have been observed to fo rm symbiotic

inges tion in response to nutrient limited conditions in

associations wi th protozoans, medusae, turbellarians, and siphonopho res. In most cases these relationships

order to obtain growth limiting compounds and elements. Some marine organisms, including some molluscs,

are highly species specific, most hosts only having one

forami niferans, helizoa, ciliates, and dinoflagellates retain

species as a symbiont. Certain species of heterotrophic

chlo roplasts that they have ingested when grazing on

dinoflagellates have cyanobacteria attached to their surfaces that sometimes reside within specialized pockets

photosynthetic organisms. The chloroplasts, although not fully integrated into the metabolism, can be a useful

of the host's cell wall. Planktonic radiolarians and foram-

source of energy. In general the chloroplasts do not func-

inifers can contain up to tens of thousands of symbiotic

tion for long periods of time in the new 'host', and their

algae per individual. It is clearly not an easy task to unravel the complexi-

function gradually declines and they are lost. However, in some species, such as the ciliate fv1esodinium rubrum,

ties of the metabolic pathways that are vital for the prod-

which is a major species in some 'red tides', are truly

uctivity in the oceans. With ever-i ncreasing analytical

photosynthetic organisms (Dolan & Perez 2000).

tools the current trend for the discovery of new microbial co mponents of the marine microbial wo rld is likely

One of the best-known symbiotic relationships in the marine world is that between photosynthetic dinofla-

Symbiotic relationships are vital for coral species, but also for planktonic radiolarians, foraminifers, turbellarians, molluscs, and siphonophores.

to continue.

2.5 Light in water Although many factors interact to determine the net primary production of photoautotrophs in the oceans, naturally it is light that is the dominant factor that determines the rate and extent of photosynthetic activity (Kirk 1994). It is both the quality of the light and the quantity of the light that reaches the chloroplasts w it hin the cells that control

2.5 Light in water •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

these reactions. As anybody who has dived or snorkelled in open waters can testify, the penetration of light can vary greatly (Fig . 2 .10a) . In clear waters, light can penetrate many hundreds of metres; but in waters heavily laden with sediment or particulate matter, it can be difficult to see a few metres. No matter how clear the water, below 1000 m water depth, essentially no light penetrates and hence most of the world's oceans with an average depth of 4000 mare permanently in total darkness (t h e aphotic zone, Chapter 9) . In general the photic zone (e u ph otic zone) seldom extends down to 200 m water depth, and in coastal waters light penetrates to depths of between 1 and 50 m. Without light, photosynthesis cannot take place.

In the clearest of waters light seldom penetrates below

200 m.

Much of the light incident on the water is reflected at the surface, and the transmission of light is then dependent on the quantity ofparticulate matter and also dissolved organic matter (DOM) in the water. There is an exponential loss of light as it passes through the water (called attenuation) due to absorbance of the light by the water itself, photosynthetic organisms. particles in the water, and humic material and various other DOM compounds that colour the water (Fig.2.10c) . Coloured water has very different optical properties than non-coloured waters.

Particles in the water, such as bacteria. plankton. and sediment, all contribute to the scattering of light in the water. which causes the attenuation of light. Therefore the distribution of such particles is intimately linked to the transmission of light through the water. Even bubbles,

Figure 2.10 (a) Light decreases exponentially with water depth, and as light passes through a body of water, it is not just the amount of light, but also the spectral quality of light that changes. (b) Light quality structures zones of submerged algae, such as these in a Baltic Sea rock pool (photograph: David Thomas.). (c) River waters often contain high amounts of dissolved organic matter (DOM). In humic-rich rivers, the DOM turns the waters brown. Where they mix w ith seawater, the coloured waters can greatly infl uence the optical properties of coastal waters (photograph: David

Thomas).

Chapter 2 Primary Production Processes 30,----------------,

ripples ofwater on the surface, and waves will have dramatic effects on the underwater light regime. These features may result in short-term fluctuations in irradiance, with focusing and defocusing of the light. This will produce a light regime more akin to a flashing light, which has been shown to enhance the photosynthesis of some phytoplankton

species. Bubbles, particles, and surface ripples all great ly alter the lig ht field underwater. It is notjust the transmission of light itself that is affected by the scattering and absorption oflight, but also the spectral quality of the light (Fig. 2.10a) . Water absorbs strongly in the red and infrared part of the spectrum, and so at deeper water depths the light is reduced in this part of the spectrum and effectively enriched in the blue and blue-green wavelengths. Water looks blue because of this differential absorption of the blue and red parts of the spectrum. Coastal waters have a large input of DOM. These reflect in the yellow-red part of the spectrum, hence the characteristic yellow/brown colour of some river and coastal waters (Fig. 2.lOc) . This matter is referred to in the literature as coloured (or chromophoric) dissolved organic matter or eDOM. As the DOM pool in natural waters consists ofa complex mixture ofcompounds, its absorption spectrum represents the sum of the different overlapping absorption peaks. eDOM absorbs light strongly in the UV and blue region of the light spectrum ( < 450 nanometres) and its absorption decreases in intensity with increasing wavelength . When present in high concentrations. eDOM therefore gives water a yellow-brown colour. The eDOM in oceanic waters is a mixture of matter derived from both autochthonous (marine) and allocthonous (terrestrial) sources (Fig. 2 .11), and the fluorescent and absorbtion characteristics of the colour in a water sample enable researchers to use eDOM as a tracer to work out the origin of a specific water mass within the water column.

25

-t

.§. 20

s ~

Marine derived CDOM Mountain river Streom draining ogrirulruralland Estuarine eDOM Peatland drainage (,10')

-"c 15

s'" ~

10

5

500

600

Wavelength (nm)

Figure 2.11 The absorption of light by different water types influenced by the chromophoric dissolved organic

matter (CDOM) within it. (Redrawn from Sendergaard and Thomas 2004).

specific. and within a single species can vary with season and even on shorter time-scales. As irradiance increases. the trend becomes gradually non-linear and a point is reached where further increases in irradiance do not result in increases in the photosynthetic rate. In other words, the rate of photosynthesis is light saturated (Pm~) ' The slope of the linear part oftheP/E curve is denoted by the symbol a. The saturation irradiance, Ek, is calculated from the intercept between a and Pmax. In some organisms, there can be a decrease in photosynthetic rates at high irradiances. This decrease is a result of photoinhibition. This results from damage to components of the photosystems, such as cellular membranes or electron-transport proteins. At hi gh li ght levels maximum rates of photosynt hesis can be inhibited, this is called photoinhibition.

Humic-rich coloured d issolved organic matter (CDOM) can significantly colour coastal waters.

2.6 Light and photosynthesis The relationship between photosynthesis and irradiance is described by the characteristic P/E curve (Fig. 2.12) . At low irradiance the photosynthetic rate is linearly proportional to increases in irradiance. At a particular irradiance the photosynthetic rate is equal to the respiration rate, the compensation irradiance, E c . This irradiance is species-

Just as in the terminology used for primary production. gross photosynthesis is equivalent to the total photosynthesis, and net photosynthesis is equal to gross photosynthesis minus respiration (Fig. 2.13) . The characteristics Pmax' Ee, Ek, and a are all speciesdependent, and also vary within a particular species. depending on environmental conditions of light, nutrient status. and temperature . Generally. Pmax increases with increasing temperature (up to physiological limits) and is higher in organisms that grow at high rates in nutrientreplete conditions. compared with growth-limited cells in poor nutrient conditions.

2.6 Light and photosynthesis •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

(0) P

a-

(b)

,,

, , --------- If---- ,,",

Pmox

-r

~

c ~

~

,,

--

2.0

-r

=

1.0

='-

~

'0;

~

c

p.

~

.sa

Po

•-

0 0.4

'0

~

~

0

= 0

-e 0

0

Compensationpoint

,

~

---= ... 0.2

-

~

I

E,

•

§: = 0

Phofoinhibilion

~

~

=

Ek

~

Irrodiance (£)

o

50

100

150

Irradiance umcl m·2 sec- 1

Figure 2.12 (a) The response to photosynthesis (I') in response to changes in irradiance (E}-a PIE curve. With increasing light, photosynthesis increases linearly and the slope of the increase is a. At the compensation irradiance Ec the photosynthetic rate is equal to the respiration rate (R). With increasing irradiance the linear trend ceases, and at the saturation irradiance (Ek) the rate of photosynthesis is saturated (Pmax). In some organisms, there can be a decrease in photosynthetic rates at high irradiances (photoinhibition). Respiration typically does not change with increasing

irradiance, and gross photosynthesis is indicated by P, and net photosynthesis by P, (after Lalli & Parsons 2004). (b) PIE curves for phytoplankton cells grown in high (0) and low light (0). In the top set the rate of photosynthetic carbon assimilation are expressed as a function of chlorophyll concentration of the phytoplankton. In the bottom set, the same data are expressed on a per cell basis. The low-light algae have acclimated to the low light by increasing cellular concentrations of chlorophyll , and on a per cell basis reach the same

Pmax as the high-light acclimated algae,

although their value of a is greater (i.e. more efficiently utilizing the lower irradiances).

Time course of oxygen concentrotion

." .- -• -• . '" ' il

~

~ 0

~ ~

~

~

0

~ ~

0

'"

Respiration

nme---

mation, and in low light conditions the Chlorophyll:Carbon (Chla:C) ratio can be considerably greater than that for the same organism acclimated at higher light levels (i.e. in the low light cells there is more chlorophyll per cell than in the cells at high light) . Under nitrogen, phosphorus, and trace metal (e.g, iron) limitation the Chla:C ratio of a particular photosynthetic organism tends to decrease. Likewise in lower temperature acclimated cells, the Chla:C ratio is lower than in cells acclimated at higher temperatures. The changing pigment concentrations of cells obviously have significant effects on the P/ E characteristics of a particular algal species (Fig. 2.12b) .

Figure 2.1 3 The relationship between gross

By chang ing pigment content algae can photoacclimate

photosynthesis (gross primary production), net

to changing light regimes.

photosynthesis (net primary production), and respiration.

2.6.1 Light acclimation Within certain limits, most photosynthetic organisms are able to acclimate to a given light regime (Macintyre et at. 2002; Raven & Geider 2003), mostly by altering the concentration of chlorophyll and/or accessory pigments per cell or per unit cell area. This process is called photoaccli-

A Chla:C ratio of 0.02 :1 is often cited in the literature and used in models describing phytoplankton dynamics. However, because chlorophyll concentrations within phytoplankton cells can be altered due to external stimuli (temperature, irradiance, and the growth status of the algae) within time periods of hours, the utility of this ratio is rather dubious. Furthermore, ratios in the order of0.0 1:1 to 0.005 :1 are not uncommon in field populations (Lefevre et at. 2003) .

Chapter 2 Primary Production Processes Another feature, exhibited by some algal cells w hen exposed to changing light conditions, is an obvious movement of the chlorophyll-containing chloroplasts wit hin the cells. The chloroplasts move along cytoplasmic strands in a process known as karyostrophy. Generally chloroplasts are distributed within the cell so that efficie nt light abso rption can t ake place. However, in high light, clumping of chloroplasts, often around the nucleus, is frequently observed, and is thought to be associated with mechanisms to protect cell organelles from damaging light effects. Although not universal within aquatic photosynthetic organisms, such

Box 2.5: Compensation and critical depths

mechanisms are known from terrestrial higher plants. It is likely that chloroplast-moveme nt processes are important for coping with rapidly changing light environme nts in turbulent surface waters or diurnal changes in light. Karyostrophy is a process by which chloroplasts move in reaction to changes in light conditions.

Compensation depth is the depth in a water column at which net photosynthesis is O.

It is worth noti ng that there is often a reducti on in the photosynthesis rates measured at t he surface of the w ater. This represents an often observed lowering of the

The euphoti c zone is the upper part of the water column

photosynthetic rate due to photoi nhibition in the very top-

that supports photosynthes is. The bottom of th is zone is

most metres of the water column.

generall y defined as the depth at wh ich 1% of the surface

Of co urse phytoplankton cells are not at a stat ic depth

irradiance is measured. However, a better representation

as they and/ or the water may move. In fact they are mixed

of the bottom of the euphotic zone is the compensation

either through out the wh ole water column or, w here w ater

depth. This is the depth at which the gross photosyn-

strat ificat ion takes place, wi thin surface mixed w ater lay-

thetic carbon assimilati on by phytoplankton equals th e

e rs (Chapter 7). Becau se of this, phytoplankton cells wi ll

respiratory carbon losses, or when the net photosynthesis

be mixed above and below the compensat ion depth, to

is O.

depths as deep as the mixed layer depth. When cons ideri ng net phytoplankton growth it is therefore more pert iA

B

E

nent to relate the daily integrated photosynt het ic gains to the integrated respiration losses over the w ater column

(day and nig ht) to the mixed layer depth. The critical depth is the water d epth w here the intePhotosynthesis(PJ

- -- -- -o(«mpensctlcndepth E( compensationlight intensity

grated daily photosynthetic carbon assimilati on is bal-

At the compensat ion depth (0,) the phytoplankton photosynthesi s is equal to the respirati on, i.e. the compensat ion light intensity Ec• Phytoplankton is mixed in the water column, above and below the compen sation depth, down t o the depth of mixing (D m) . The criti cal depth is the water depth w here the integrated water-column phot o synthesis is equal to the integrated wat er-column respiration . In this diagram the area bounded by the points A , B, C, &. D represents respiration, and the area A , C, &. E represents the photosynthesis. At the crit ical depth these two areas are equal. When the depth of mixing is deeper than the crit ical depth, no net growth takes place. When , however, the depth of mixing is shallow er than the crit i-

- - - - - - - - - - - - Omdepthof mixing

ca l depth net phytoplankton growth occurs. (After Lalli and Parsons 2004.)

2.7 Supply of inorganic nutrients •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

\0,000

• •

40,000

~ Critical depth

Phytoplankton Zooplankton

I

30,000

Data from the Norwegian Sea in 1949 showing the relationship between mixed layer depth, crit-

ical depth , and phytoplankton

Thickness mixed layer

and zooplankton abundance. Growth occurs only when the

20,000 10,000

•

N --

100

Q

200

t

-...-

•

1953,)

"

~'

0-rlI' ~

I

s

10

1\

20

21

30

above the critical depth. (Illus-

I

tration adapted from Sverdrup

~

E

depth of mixing is consistently

4

9

March

14

19

24

29

April

4

9

/'

~ :"

14 May

19

I'.

-i-

24

29

anced by the integrated daily respiratory carbon losses.

to grazin g organisms and the respiration of bacteria and

As long as suffic ient nutrients are present, net phyto-

other heterotrophic organisms. Interestin gly it led to a

plankton growth occurs when the mixed layer depth is shallower than the critical depth . When the mixed layer

major advance in the design of freshwater reservoirs, w here preventin g algal blooms is an impor tant part of

extends be low the critical depth algal growth is limited by

their management.

lig ht, and there is no net phytop lankton growth (Sverdrup 1953 ; Smetacek & Passow 1990),

dent light playa key role in th e seasonal dynamics of

The critical depth theory was first proposed by Sver-

phytoplankton (see be low) , These are discussed be low in

dru p in 19 53. In this theory the respiratio n losses are

conj unction w ith the inorganic nutrient demands of grow-

not j ust the algal respiration losses, but also losses due

ing phytop lankton po pul ations,

The critical depth is the water depth where the integrated daily carbon assimilation is balanced by daily respiratory carbon loss.

2.7 Supply of inorganic nutrients In addition to carbon , oxygen, an d hydrogen, the plant must incorporate other eleme nts into organic material, This arises as a consequence of the eleme ntal composition of the various macromolecules, notably proteins and nucleic acids. The principal add itional requirements are nitrogen and phosphorus, and in aqu atic ecology, these eleme nts are commonly referred to as nutrients or inorganic nutrients.

2.7.1 Nutrient status of water Waters that have low concentrations of essential nutrients for algal growth are called oligotrophic and are regions of low primar y productivity. In contrast, eutrophic waters

The seasonal changes of mixed layer depth an d inci-

have high concentrations of nutrients, and generally support high levels of primary production. Waters between the two states are referred to as mesotrophic waters, and these sustain intermediate levels of primary production. Most marine systems are classified on the basis of the annual primar y production, whic h is anot her way of express ing the supply or production of organic matter in the wate r body: Organic Carbon Supply Oligotrophic: < 100 g carbon m-2 year - 1 Mesotrophic: 100 to 300 g carbon m- 2 yea r-' Eutrophic: 300 to sao g carbon m- 2 year- 1 Hypertrophic: > sao g carbon m-2 year - 1

The process ofeutrophication can be defined as an increase in the rate of supply of organic matter to an ecosystem. This occurs when there is a change in the concentration of a factor (can be more than one) that limits algal growth , This is often an increase in inorganic nutrients, such as nitrogen or phosphorus, often associated with the run-off of artificial fertilizers from agricultural land (Chapter IS), The res ulting

Chapter 2 Primary Production Processes ecosystems especially vulnerable to eutrophication (Chapters 8 and 15) .

2.7.2 Supply of nutrients Photoautotrophs require a diverse range of elements for balanced growth. These include nitrogen, phosphorus, silicon, sulphur, potassium, and sodium (all known as macronutrients) . Many trace elements (micro-nutrients) are also required, including iron. zinc, copper. and manganese. as well as vitamins such as B12 (cyanocobalamin), biotin, and thiamine. Figure 2.14 Increased inorganic nutrient supply can result in excessive algal growth as shown by the mass of U1va spp. supported by nutrient-rich run-off from agricultural land in Ireland (photograph: David Thomas).

increase in algal growth (both phytoplankton and!or macroalgae), if excessive (Fig. 2.14), can have deleterious effects for the whole ecosystem (Skei et al. 2000) . It is important to stress that eutrophication is a process of change and is not a trophic state. For example, an estuary

may have been mesotrophic and is now classified as eutrophic, but it is not necessarily undergoing further eutrophi-

cation. Although eutrophication is generally perceived as a detrimental process. it is also important to stress that it can be a reversible process. There are also instances when low levels of eutrophication can even be considered as being a positive state for increasing the productivity of a specific water body.

A wide range of macro- and micro-nutrients are needed

for algal g rowth. Although each nutrient has the potential to limit the growth of photoautotrophs, in most marine environments it is either nitrogen or phosphorus that is generally the limiting element (cf. Box 2.6 and Boyd et al. 2010) . It is actually the supply of the nutrient to the organism that is critical. A nutrient can be present in low concentrations. but if the uptake rate by the organism is low, only a low supply rate is required. Naturally growth can be limited by the supply of more than one nutrient at anyone time: nutrients can be either biomass-limiting or rate-limiting. In the case ofthe former. the nutrients are exhausted so that no more biomass can be produced. In contrast. rate-limiting nutrients simply limit the rate of new biomass production by their rate of supply. Resupply of nutrients primarily takes place by molecular diffusion.

Eutrophicat ion can be defined as an increase in t he rate of supply of organic matter to an ecosystem .

Eutrophication is a revers ible process and not always detrimental.

Strictly speaking eutrophication is a process by which the productivity of an aquatic system is increased. and can therefore be caused by factors other than nutrient input. These factors include reducing the suspended material in a water body and therefore increasing the light levels available for photosynthesis, or changing the residence time of water within a particular system. Therefore, eutrophication is also a natural phenomenon, and is not always associated with anthropogenic activities. Coastal regions can receive high dosages of nutrients both directly via marine outfalls and by discharges from estuaries. This, coupled with their relatively long residence time. makes coastal

When a nutrient is taken up by an organism, there is immediately a reduction in that nutrient in the micro-environment surrounding the cell or organism. The resupply of nutrients takes place primarily by molecular diffusion from the bulk medium of water (Wolf-Gladrow & Riebesell 1997) . Surrounding each cell or surface in water is a diffusive boundary layer (DBL) in which water movement and molecular diffusion is restricted. The thickness of the DBL surrounding the organism is therefore critical to determining the rate at which nutrients are transported to cell surfaces. The smaller the organism, the smaller the DBL due to the surface area:volume relationship (Chapter 3) . This gives smaller organisms a physiological advantage at low nutrient concentrations and is presumed to be why small species of phytoplankton prevail in oligotrophic waters. Small phytoplankton species have a greater surface area:volume ratio than larger species.

2.7 Supply of inorganic nutrients •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 2.6: Iron and high-nutrient, lowchlorophyll regions

In the late-1980s, John Martin developed the idea that a lack of iron is the cause and laboratory experiments confirmed how vital iron is for phytoplankton growth. A series

In some areas of the world's oceans the supply and

of experiments in the Equatorial Pacific Ocean, where large

assimilation of ni trogen, phosphorus, and carbon appear

areas of the ocean (hundreds of square kilometres) were

not to be linked. In these waters the phytoplankton stand-

seeded with iron, led to substantial increases in phyto-

ing stocks are never large enough to assimilate the N and

plan kton growth. In particular, diatoms grew and it appears

P in the surface waters fast enoug h to deplete them at

that not all phytoplankton species are equally iron-limited

any tim e throughout the year. These are the 'high-nut rient ,

(Martin et al. 2002). Several oceanographic expeditions

low-chlorophyll' (HNLC) waters of the subarctic Pacific,

showed that , during spring in the Southern Ocean, phyto-

the Sou thern Ocean, and the equatorial Pacific.

plankton bloom in iron-rich waters but do not in waters with

Several hypotheses have been proposed to explain

limited iron reserves (de Baar et al.1995). It was pertinent

HNLC regions, including suggestions that in these regions

to therefore extend the Pacific iron-fertilization experime nts

light (either low or damaging high light intensity) limits

to the Southern Ocean. Several studies have now 'fertil-

production to a degree that inorganic nutrients are not uti-

ized' Antarctic water bodies and in all of these diatoms

lized or that grazi ng pressure limits the standing stocks of

did bloom in response to the added iron. This growth was

phytoplankton. Whereas these factors clearly do playa ro le

in turn responsible for the absorption of significant quanti-

to varyi ng degrees, the most compelli ng explanation is that

ties of carbon dioxide from the water during the experi-

the rate of supply of iron, an essential trace element for

ment (Boyd et al. 2000; Buesseler et al. 2004; Coale et

phytoplankton growth, is limited.

al. 2004). Much of this work is synthesized by Boyd et

Dissolved iron concentrations in offshore areas are

al. (2007). An extension of this work has been to investi-

extremely low, since the primary source of iron to the

gate regions w here natural upwelling water into iron-poor

surface waters of the oceans is from the land, either via

surface waters is responsible fo r enhanced phytoplan kton

atmospheric dust deposition in offshore areas or di rect

activity, such as on the Kerguelen Plateau in the Southern

depositions from land masses. Atmospheric dust depo-

Ocean (Blain et al. 2007; Pollard et al 2009).

sition in the two major HNLC areas- the Antarctic and

It is this link between the phytoplankton growth and draw-

equatorial Pacific Oceans-are the lowest in the world.

down of atmospheric carbon dioxide that fuels a vigorous

Conversely, in the equatorial North Atlantic, which receives

debate about these experiments. There is a concern that

large amounts of dust from the Sahara, iron concentra-

these results may be viewed as providing a simple answer

tions are sufficient for the complete assimilation of available

for mopping up excess carbon dioxide, thereby curbi ng

nitrates and phosphates.

the effects of increasing greenhouse gases. It is thought

. -... ....... ~e:S N.E~ ....... /

,

1

•

~

-- . .

....... -

,

'..-. I

.... A satellite image of an iron-fertilized patch during the Eisenex expedition to the Southern Ocean in 2000. The sparse phytoplank-

ton outside of the patch is striking compared with the abundant growth of phytoplankton within the patch following fertilization. The satellite image shows the increase in chlorophyll (orange/ red) compared to the waters surrounding the patch (blue). (Image:

AWl

Philipp Assmy & Joachim Henjes, Alfred Wegener Institute.)

Chapter 2 Primary Production Processes

by some that by spreading iron over huge swathes of the ocean, enhanced phytoplankton growth would effectively

al. 2004). Much of this de bate is add ressed in a special

trap carbon dioxide. Such ideas about large-scale ecological

ary 2008).

issue of the journal Oceanus (volume 46 published in Janu-

engineering have little to do with the work of the scientists

The real interest of th is work co mes fro m the implica-

conducting the experiments. Iron fertilization is in fact a poor

ti ons for the understandi ng of the atmospheric carbon

way to tackle greenhouse gas problems. Calculations show

dioxide levels in past cli mate history. This new evidence

that iron fertilization of the Southern Ocean would not in

supports the theory that low amou nts of atmospheric

fact be an effective mechanism fo r carbon dioxide removal.

carbon dioxide (measu red in ice cores taken in the Arctic

Levels of carbon dioxide are increasing at such a rate that ,

and Antarctic) during past ice ages may be linked to high

even by maximizing biological uptake in these oceans by

amounts of iron in Antarctic waters that suppo rted large

addi ng iron, there would still be a net increase in atmos-

standi ng crops of phytoplankton.

pheric carbon dioxide (Chishol m et al. 200 1; Buesseler et

( HNLC = high-nutrient, low-chlorophyll.

)

Lack of iron may limit the growth of phytoplankton in HNLC regions.

Iron-fertilization experiments have resulted in increased

phytoplankton growth within the fertilized patches.

Fertilization of the oceans with iron is not in any wayan

easy fix for combating rising atmospheric carbon dioxide

concentrations.

It has been estimated that for cells less than 1 urn in diameter, molecular diffu sion is adequate for the resupply of nutrients, but for larger organisms it is a major limiting factor. Therefo re mechanisms for reducing the DBL around the organism are key to the nutrient metabolism of aquatic organisms. Movement through the water, eit her by sinking or swimming, means that the nutrient-depleted bound ary layer is dragged with the organism, causing fluid from the layer to be she ared away. This can then be replaced by nutrient-replete water. Clearly the velocity and magnitude of distance travelled will affect the degree of replacement. However, it is estimated that swimming significantly reduces d iffusion-limitation only in organisms greater

131

(I)

151

Figure 2.15 An y property of an organism that alters the organism 's size and/or shape w ill alter the properties of the diffu se boundary layer (DBL). Therefore the variety of shapes and form s of phytoplankton shown here will have very different sinking rates as well as different characterist ics of the DBL surrounding the cells, co lo nies, o r chains. Starting from t op-left and moving clockwise the images are: (1) Dity/um brightwellii, (2) Ceratium tripos & Rhizoso/enia sp.,

(3) Eucampia zodiacus, (4) Guinardia flaccida , (5) Chaetoceros s ocia/is, (6) Coscinodiscus sp. (photographs: Ian Lucas).

2.8 The main limiting nutrients for growth •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

-- -

than 100 urn diame ter. In many of the organisms between 1 and 100 urn diame ter, movement is a means of relocating into regions of higher nutrient concentration, rather than address ing diffusion-limitation by altering DBL properties. Any property of an organism that alters the organ ism's size and/or shape will alter the properties of the DBL. The refore, organisms that form colonies or chains, such as the diatoms, change their shape and therefore sinking rate, and also the characteristics of the DBL surround ing the colony or chain (Fig. 2. 15) . The diffusive boundary layer is key to determining nutrient supply to a cell, or surface of a macroalga.

Figure 2.16 Structures o n the surfaces of macroalgae , such as the ripples on thi s Macrocystis pyrifera, can cau se

In the case of macroalgae and seagrasses, relief or structures on the thallus or frond surface will cause eddy formation and turbulent motion of water passing over the surface (see also Chapter 8). This will have the effect of reducing DBLs and therefore enhancing nutrient exchange. As macro algae and seagrasses cannot move in the water column by swimming or sinking, they rely on modification of the water movement across their surfaces to enhance nutrient exchange (Fig. 2. 16) . Seagrasses are also able to t ake up nutrients from the sed ime nts throu gh their root and rhizome systems. Ridges and structures on the surface of a macroalga can increase the rate of exchange of nutrients and dissolved gasses.

Naturally on exposed and turbulent wave-infl uenced waters, water exchange is never going to be a problem. In sheltered waters with little water movement, diffusion-limitation of nutrients becomes more of an issue. For example, the giant Pacific brown seaweed (Nereocystis luetkeana) has smooth blades in rapidly moving water, but in more sheltered waters its fronds are ruffled . The ruffled blades serve to increase the turbulence as water passes over them, thereby increasing nutrient supply and gas exchange to the fronds. In faster moving waters the ruffled blades would increase the risk of tearing because of their increased drag; instead the seaweed's smooth blades tend to form streamlined bundles that are not so easily damaged.

turbulent water movements over the surface of the frond s. This will increase the exchange of gases and inorgan ic nutrients compared with when undisturbed lamina flow passes over the surface (photograph: David Thomas).

2.8 The main limiting nutrients for growth The main products of photosynthesis are sugars, reductant (t he product of reducing enzymes), ATP, and oxygen, which are themselves substrates in further biosynthetic pathways (Table 2.2). The other m ajor inorganic nutrients needed for the myriad of molecules that make up a living organism occur in seawater as different chemical species : Nitrogen: N0 3, NO l , NH: , NH3 , Nz' and urea. Phosphorus : HPO'.;", PO';, and, H,PO•. Sulphur: 50'.;", H, 5.

Particular nutrients are critical for certain organisms, alt ho ugh not limiting for photoautotrophs in general. An example is silicate, for diatoms and silica-scaled prymnesiophytes (and some cysts of some dinoflagellate species) , which is present in several forms as well: H4 Si0 4 , H3 SiO. , and H3 SiO•. Nitrogen and phosphorus are the main growth-limiting nutrients in marine systems.

Table 2.3 Typical percentage biochemical and elemental composition of algal cell s.

"!o of an algal cell 40

"!oC 44

"!oH 6

"!o0 49

"!oN

Protein

40

53

7

23

16

Li pids

15

69

10

18

1

2

5

36

4

33

17

10

Biochemical

Carbohydrate

Nucleic acid & nucleotides

"!oP

"!oS 1

Chapter 2 Primary Production Processes The balance of these forms of anyone element is highly dependent on many complex biogeochemical processes. Many of the trace nutrients are actually only mostly found in complexed forms wit h organic compounds in seawater (Table 2.3). The nutrient demands of individual species are n aturally a reflection of its biochemical demands and composition. Clea rly the proportion of the relative macromolecules, e.g. lipid (cf, nucleic acid) , will determine the elemental composition of the cell and the relative demands for C, N, and P for growth. Although there is great variation in the composition of the cell, the functioning of the cell (i.e, the requirements for metabolism (enzymes-proteins) and reproduction (nucleic acid), sets constraints on the relative proportions of the various macromolecules, and con sequently the relative requ ire ments for carbon, nitrogen, and phosphorus during photosynt hesis.

2.8.1 Elemental composition of algae There are obvious nutrient demands that are virtually universal, and these will be discussed here. However, it must be stressed that in many instances it is not the major ino rganic nutrients (Table 2.4) that may limit growth, but rather the rate of supply of trace elements that restrict the growth rates (Box 2.6) . A typical algal cell is 400;0 protein , 400;0 carbohydrate ,

•• ••

'.

o

•• • -'If • •

. ~

•, •

•

• ,

o r

,• • ·.'••

• •

'.

•.

•

o

! '

.

0

••

• • I . ••• • I , •• • .0•. '.. , 1 • •• • , ' 0 • •

•

•

•I

'

•

-

. -, , '.. . .. -, ... ' .. . ..., • • • . • • • ., . • . . · • " . '. • ·.. . . . " •

0

'J

,

I

• "-

.

':,

'

o•

•

•

" ,•• •

o .

• • :.'•

~

•

•

•

'

•

•

to ... "~ •

•

o

-: ' '!. •

•

•

0

• "• f,. " • • , •

•

.... ,." • 0

0

•

~

..

•

--•

•

'. ,: • . ' • • #~ • • , , • It ~ . ... ..

•

:-

•

•• :

Figure 2.17 Epifluorescent photom icrographs of Nile-red st ained diatoms that sh ow the lipid droplets within the cells v ery clearl y (from Pri scu et at. 1990).

ited. In some cases there can be so much lipid production that the lipids can be seen as oil droplets with in the cells, and is one of the reasons algae have been the recent focus as possible biofuel sources (Fig 2.17 and also see Current Focus: Us ing algae for carbon sequestration and algal biofuel production) . It is straightforward to categorize the average composition of the organic materials within the phytoplankto n. If we rewrite the simplified photosynthesis equation to take into account the need for nitrogen (mostly supplied as nitrate) and phosphorus (sup plied as phosphate) we get:

15% lipid , and 5% nucleic acids.

Typically, marine phytoplankton are comprised of more than 40% protein, 5% nucleic acids and nucleotides, 40% carbohydrates, and 15% lipids. These proportions can vary greatly depending on the inorganic nutrient supply, age of the organ ism, temperature, and irradi ance cond itions. In particular the lipid fraction can vary cons idera bly during the lifetime of a phytoplankton cell, being < 10% in exponentially growing cells and increasing to > 25 % in cells in the station ary phase of growt h, where nutrients are lim-

..... • ... ' . • ,'. - -. • '.

,

106CO, + 16NO, + HPO~- + 122H,o + 18W => CI06H 2630 n oN16P + 13 8 0 2 Typically from the equ ation a bove , the ratio of carbon:nitrogen:phosphorus in healthy, actively growing algal cells is 106:16:1 . This ratio is referred to as t he Redfield ratio, after the oceanographer A. C. Redfield. Therefore the typical C:N ratio is 6.6 :1. This is a commo nly used parameter to measure the physiological status of algae, since when nitrogen is limited, or the algal cells are senescent or dying, the ratio increases considerably (Burkhardt &

Table 2.4 The major function s o f so m e select ed inorganic nutrients.

Nutrient

Examples of functions

Nitrogen

Major metabolic impor tance, structural ami no acid, p rotei n metabolism

Phosphorus

Structural in pa r ticular membranes and energy metabolism

Potassium

Osmotic re gulat io n, protein stability

Calcium

Ion transport, enzyme activation, stru ctural function

Magnesium

Ion transp ort, enzyme activation, pigments such as ch lorop hy ll

Sulphur

Stru ctu ral function, active in enzyme activity

Iron

Active in enzyme activity

Sodiu m

Ion transp ort , osmoregulation , enzyme activation

Manganese

Electron t ransport and membrane structu re

2.8 The main limiting nutrients for growth •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Riebesell1997; Lenton & Watson 2000; Geider & la Roche 2002). The Redfield rat io, carbon:nitrogen:phosphorus

IS

switch from carbohydrate production to the accumulation of lipid reserves. When there is a lack of nitrogen in the surrounding water, protein synthesis is suppressed and the relative proportion of lipid and carbohydrates increases.

106:16:1. The quotient of CO 2 to 0 2 from the above equation is 1.3. This is known as the photosynthetic quotient (PQ) (Williams 1998) . This quotient is highly dependent on the state of oxidation/reduction of the nitrogen source. When nitrate is taken up by an algal cell it has to be reduced within the cell to ammonium before it can be utilized in cellular metabolism (Fig. 2.22) . Algae can also take up ammonium (NHt) directly as a nitrogen source. avoiding the energy in the reduction stage when nitrate is assimilated (see below) . Therefore growth on ammonium is about 19% more efficient on comparing the PQ values. The resulting PQ is lower at around 1.09.

Ocean ode allile and death CO, -Althe balance poinl-

I

CO2 + nutrients

• Organic maUer

2.8.2 Carbon The supply ofinorganic carbon for photosynthesis and algal growth is seldom (if ever) limiting in marine systems. However, the role of oceans in the global carbon cycle has been the focus of intense study in the past decades, especially in relation to increasing carbon dioxide in the atmosphere as a result of anthropogenic activity (Box 2.3) . The biggest pool ofcarbon in the oceans is that locked up in the sediments, which is, globally, about 10 million Gigatonnes (Giga is x 10 9 ) . In comparison there are about 39 000 Gigatonnes ofdissolved inorganic carbon in the various forms discussed above. The next largest pool is that contained within the dissolved organic carbon (DOC) pool at about 700 Gigatonnes. It is striking to compare these numberswith the 30 Gigatonnes ofcarbon contained within the particulate organic carbon (POC) pool, which contains all of the organisms from bacteria to blue whales within the world's oceans (Fig. 2.19) .

Primary productian

106 CO, + 122 H,O + 16 HNO,+ H,PO, - [((H,OIi" +INH,I" +H,PO,] + 138 0,

30 Gigatonnes of carbon is contained in all of the partic-

ulate phase biology compared to 700 Gigatonnes in the dissolved organic carbon pool and 39 000 Gigatonnes in the inorganic carbon pool.

CO2 + nutrients

Organic metter

C

Atmasphere 750

Organic ( Bauam

~

Oissolved orgonic carbon (Ooq

- 700

Carbon expressed as Gigatonnes

Inorganic carbon

-39000 Figure 2.18 Primary production and decomposition (respiration) are driving the biogeochemical pathways w ithin marine systems in an almost closed 'grand cycle'

Partiwlate organic "rhan (Poq - 30 (living -3)

(from Cullen et al. 2007). PQ = the moles of

0 2

evolved per moles of CO 2 assimi-

Biogenic (arbon in surface marine sediments - 3000

lated.

It must be stressed that this discussion of elemental ratios and typical cell composition is oversimplified. The cell composition (and therefore elemental ratios) will vary greatly at different life-history stages, and with changes in the prevailing temperature, light, and nutrient status. For example, in older phytoplankton cells there is a marked

Figure 2.1 g Schematic to show the major pool of carbon within the oceans. Particu late organic carbon

(poq includes all organisms from

bacteria-sized particles

to whales. Dissolved organic carbon (DOC) is generally considered to be all carbon that can pass through a 0 .2

urn fi lter. (Image: Ruben Lara)

Chapter 2 Primary Production Processes There are many algae that deposit calcium carbonate (CaCO,) in their cell walls, sometimes together with

Calcification is related to photosynthetic activity and, in particular, the effects of pH on the dynamics ofcalcium and

smaller amounts of magnesium and strontium carbonates. In the phytoplankton, the most conspicuous group of algae to exhibit calcification are the coccolithophorids that produce external 'shells' composed ofcalcium carbonate plates called coccoliths (Brownlee & Taylor 2002) . These small phytoplankton species are common in all seas, although not as abundant in polar oceans. They can form extensive blooms where the ocean surface turns a milky white. One of the better-known species ofcoccolithophorid is Emiliana huxleyi, which can form blooms in the North Atlantic cov-

carbonate and bicarbonate in seawater. Certain polysaccharides in algal cell walls can actually block crystal growth and stop calcification taking place. The ability to produce these polysaccharides in the cell walls is the likely reason

why calcification is not ubiquitous in marine algae and that relatively so few species are calcified.

ering an area of the ocean equivalent to the size of Great Britain (Fig. 2.20) . The coccoliths sink and are incorporated into sediments. where they can accumulate in huge amounts locking up CaCO, (Young & Ziveri 2000) . Some microalgal and macroalgal species have calcified

cell walls. Normally when phytoplankton bloom there is a drawdown of CO 2 due to the assimilation through photosynthesis. However, the production of calcium carbonate structures by coccolithophorids can actually result in CO 2

being released to the atmosphere due to the formation of the calcium carbonate: Ca2+

+ 2HCO, => CaCO, + CO2 + H,o.

There are also many examples of calcareous brown, red, and green macroalgae, i.e. species that have deposited calcium carbonate in the form of calcite or aragonite crystals within their tissue. This can be so extensive that these species can be important in the formation oftropical atolls and help to cement coral reefs together (Chapter 11) . Calcite

and aragonite never occur together in the same alga. and there is still some debate as to the metabolic processes that acrually lead to the deposition. In some calcifying species the crystals are laid down outside the cells, such as in the green Halimeda, which causes aragonite crystals to precipitate in the spaces between the cells. In the fan-shaped

Figure 2.20 (a) Planktonic coccolithophorids ('roundstone-bearers'), such as this Coccolithus pelagicus, synthesize exquisitely sculptured calcium carbonate cell

walls known as coccoliths (photograph: Jeremy Young, Natural History Museum, London). (b) This MODIS satellite true-colour image shows the blues and greens of phytoplankton blooms occurring around Denmark, in the North Sea on the left, and within the Baltic Sea on

the right. The bright blue colour of the North Sea bloom is thought to be a coccolithophore-bloom reflecting blue/ white due to t he reflection of li ght by the coccoliths (image: Jacques Descloitres, MODIS Land Rapid Response Team. NASA/Goddard Space Flig ht Center, Visible Earth). (c) Several species of macroalgae have calcified cell walls, such as those comprising this maerl bed. Several species of coralline algae form maerl beds, which are often found

brownPadina. aragonite is precipitated in concentric bands on the outer surface of the thallus. The corallines such as Lithothamnion and Lithophyllum, on the other hand,

at depths of 0-35 m, although in some parts of the world

deposit calcite within their cell walls to the extent that the

commonly seen calcified macroalgae are the encrusting

cells become encased, except for the cellular connections

red species (with lichen-like growth forms) and articulated

(Fig. 2.20) .

Corollina offlcinalis combining here to form a vivid pink

In some coral reef systems over 70Ofo of the reef can be made from calcified macroalgae.

free-living calcified macroalgae have been found at depths

down to 200 m (photograph: Bill Sanderson). (d) More

fringe surrounding an intertidal rockpool (photograph: David Roberts).

2.8 The main limiting nutrients for growth •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

CURRENT FOCUS: Oceans as carbon sinks and ocean acidification

2 . As more CO2 is absorbed by the oceans, there w ill be reduction in the pH of the seawater and a corresponding decrease in the carbonate ion concentrat ion (see

Seawater is undersaturated with CO2 compared with the

figure be low) , which results in the process commonly

atmosphere and so there is a continual process by which CO2 diffuses acro ss the air-ocean surface and dissolves to

referred to as ocean acidification.

for the dissolved inorganic carb on (DIC) pool. The solubil-

Since the Industrial Revolution in the 1700s it is esti-

ity of CO 2 in seaw ater increases as temperat ure decreases

mated that the oceans have dropped in pH by about 0 ,1

and so a greater amount of CO2 dissolves in the Arctic and

pH unit and it is pred icted that by 21 00 the w orld 's oceans

Southern Oceans than in temperate and tropical waters (Takahash i et al. 2009), Coupled to this 'solubility pump ', the oceans also 'take up ' CO 2 due to photosynthetic assimilation. Ultimately this assimilated carbon is transported to the deep oceans as par ticulate matter sinks to the depths, although of course a con siderable amount of the organic matter produced is respired through microbial activity (see Chapter 3 ) . The uptake of CO2 by the biology of the oceans and removal to deep waters is referred to as the 'b iological pump '. In par t the oceans are mitigating against the well-recorded increasing atmospheric CO2 concentrat ions, primarily driven by anthropogenic greenhouse gas release, by absorbing CO2 through both th e solubi lity and biolog ical pum ps. However, there are two obvious problems ident ified in future global climate change scenarios (IPCC 200 7a, b, c) :

may have undergone a further decrease of about 0 .4 p H

1. As oceans warm , they will absorb less CO2 from the atmosphere since the so lubility of CO2 is less in warmer

units (Zeebe et al. 2009), 5urfo(e «eon

A!nmpllere

pro, (ppm)

pH

700

8.3

600

8,' ~b~iness OS" u~uol~

500

8,1

15920scenario (IP(( 1995)

400

[C01(oq)I COt l (p mol l-' )

ss

pH

30

25 10 15 10

[COt ]

8,0

300

7,9

'00

7,8

[(O!" II

300 250 '00 150 100

5

\0

0

0

1850 1900 19511 2000 1050 2100 18511 1900 19511 2000 2050 2100 y~, Year

Predicted changes in atmospheric CO2 to the year 2100 and associated changes in ocean pH and carbon chemistry, Adapted from Wolf-Glad row et al. 1999, At th e moment, th e surface of th e oceans is saturated in the vari ous mineral fo rm s of calcium carbonate (e.g.

water. 10' '" 60' 80' 100' 110' 140' 160' 180'1 60' 140' 110' 100' SO' 60' '" 10' 0' 10'

60'

60'

'/'..

\0'

",;e~

\0'

~'0

]0' ./-'-""'-"

40' , ]0'

?/'.:;,

10' 10'

10' 10'

0'

0'

10'

10'

-T..h'-4;#'f 10'

10' ]0 '

]0 '

,,'

\0'

,,' \0'

60' ~ /

10' '" 60' SO' 100' 110'140' 160' 180' 160' 140' 110' 100' SO' 60' '" 10' 0' 10'

@ill 2008 Apr I 13:42:53 1 - 108 - 96 - 84 - 72 - 60 -48 - 36 - 24 - 12 0

12

24

36

48

60

72

84

96 108

Net Flux {arums(m- 2 vear- 1)

Climatological mean annual sea-air CO 2 flux (g carbon m-2 year'] for the reference year 2000 (non-EI Nino conditions). The map is based on 3.0 million surface water pC0 2 measurements obtained since 1970. Thi s yields a net global air to sea flux of 1.42 Pg carbon year: ". Adapted from Takahashi et al. 2009.

Chapter 2 Primary Production Processes

calcite and aragonite) and these minerals do not dissolve;

showed that in the more acidic conditions, the coccoliths

whereas in deeper waters, where the waters are under-

(calcium carbonate plates) were more deformed than in

saturated in calcium carbonate minerals, they do dissolve.

those formed in normal pH conditions.

Because of the lowering of pH of ocean waters and the

This culture work was followed up by Iglesias-Rodriguez

parallel reduction of carbonate ions, the surface waters are becoming less satu rated in calcium carbonate and it

et al. (2008) who showed that calcification and primary production of E. huxfeyi were increased in cultures grown

is predicted that in the next 150 years the carbonate-

in more acidic waters and they interpreted their results

saturated surface waters in some regions, especially cold

as showing that already populations of E. huxfeyi were

polar waters, may disappear altogether (Feely et al. 2004;

already respondi ng to decreased pH surface waters. They

Raven et al. 2005).

also backed this up with addi tional field evidence to show

Such changes will bri ng about considerable change to all organisms that utilize calcium carbonate as part of their

how the average coccolith mass has increased over the past 220 years.

body skeleton or external structures. This clearly includes

The apparent discrepancy between the Riebesell et al.

the corals and molluscs, but also planktonic forami nfers and

and Iglesias-Rodriguez et al. results is an excellent example

calcareous phytoplankton such as the coccolithophores

of the difficulties in trying to answer a pote ntial simple

(section 2.8.2). The poten tial effects of such changes are

question such as: what do increased CO2 conditions do to

well reviewed by Orr et al. (2005), Fabry (2008), Fabry

calcification in a species of coccolithophore? As described

et al. (2008), and Browman et al. (2008).

by Fabry (2008), there are several explanations for the

A very good example of the debate about what the

discrepancies, including methodological issues on how to

effects of ocean acidification may have on marine organ-

realist ically change CO2 conditions in laboratory cultures

isms is exemplified by work carried out using coccolitho-

(also see Riebesell et al. 20 10). Maybe the most compel-

phores. Riebesell et al. (2000a) produced some highly

ling explanation is that both groups were actually experi-

convincing results that showed that there was very reduced

menting on different species of algae, or at least different

calcification in Emifiana huxfeyi grown in response to

populations of a single species with very different physi-

increased CO 2 loadi ng in laboratory cultures. They also

ological properties.

(a), (b) , (d), and (e) Emiliania huxleyi; (c) and (I) Gephyracapsa oceanica collected fram cultures incubated at [CO,I 12 pmol 1-1 (a-c) and at [CO,] 30-33 pmol 1-1 (d-I) , corresponding to Pcoa levels of about 300 p.p.m .v. and 780 to 850 p.p.m.v., respectively. Scale bars represent 1 I-Im. Note the difference in the coccolith structure (including distinct malformations) and in the degree of calcification of cells grown at normal and elevated CO 2 levels. (From Riebesell et al. 2000a.)

2.8 The main limiting nutrients for growth •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

2.8.3 Nitrogen Nitrogen is present in seawater as dissolved molecular N" ammonium (NH.i), nitrite (NO,), nitrate (NO,), and as organic forms such as urea, amino acids, and a diverse range of complex dissolved organic nitrogen (DON) compounds (Fig. 2.21) . In seawater, ammonia (NH,J exists as a mixture of the ammonium ion (NHt ) and NH 3 " At seawater pHs (approx. 8) over 95% is in the form ofNHr, With increasing pH, the relative contribution of NH3 increases (e.g. at pH 9, NH: is about 75%) . , -_ _ Regenerated NH. +

Fishand _ ethers

=-c-t---,-,-

I,.,"'h.m'""I Phytoplankton

II Rjv~

..•-

c o

-"

.~

••

Newnltrogen

z

Biota • ~-~-~--L~~~J

"

Oenltrificllfion

I

NOl"

===ni1rificolion NO£ -

Nitrogen is the element that most frequently limits primary production in the oceans. Only some cyanobacteria, such as Trichodesmium species can reduce (fix) nitrogen gas, and these species thrive in waters where other forms of nitrogen are limited and thus re strict the growth of other phytoplankton (Berman-Frank et al. 2001) . However, they still need sources of other nutrients, such as phosphate. Nitrate is the primary form of nitrogen assimilated by marine primary producers.

Blooms of nitrogen-fixing cyanobacteria are a feature of oligotrophic waters (particularly oceanic tropical coastlines), where nitrogen is present in the water in very low concentrations, thereby restricting the algal growth. Other nitrogen fixers are also found growing on and in sediments in coastal regions, saltmarshes, and estuaries, as well as in the roots of seagrasses and other saltmarsh grasses (e.g. Spartino spp.), where the nitrogen fixed by the cyanobacteria also supports the growth of the plants. In general, Nqis the primary source of nitrogen utilized by algae, although NO, and NH: can also be taken up (Fig. 2.17) . Whatever the original source of nitrogen, NHt is the form utilized in cell metabolism and NO, and NO, have to be reduced by the enzymes nitrate reductase and nitrite reductase within the cell: N0 3 ---t nitrate reductase ~ N02 nitrate reductase

N~

-

~ NHt

NH. +

Figure 2.21 Schematic of nitrogen in the ocean including input, transformation, and loss terms.

Only some species of cyanobacteria can fix nitrogen gas

directly.

More recently reported for marine systems is the Anammox process (Anaerobic ammonium oxidation) which is thought to account for large amounts of the Nz production in sediments and other suboxic systems (Fig 2.23 and Ward et al. 2007) . In this process, NH: and NO, are converted by the anammox bacteria into Nz. This is an important pathway in the marine nitrogen cycle, since it may account for why most of the NH1, which should theoretically be

NO , 3

,

Nitrate redudnse

NO -

Urea

Urea

-

Cell wall -

Nitrite reductase

llrecse

Figure 2 .22 Highly simplified schematic of major routes of nitrogen uptake and cellular transformation of inorganic nitrogen into amino acids by algae.

-CO, _ _ _ _ NH/ /

,

NH +

Ie)

Aminoacids ~ Aminoacids

-.. Amino acids

Chapter 2 Primary Production Processes 0.1 (Chapter 9) . In contrast, in coastal regions or sites of coastal upwelling, where input of nitrate can be high, t he f-ratio can be up to 0.8 (Chapters 7 and 8) . The inverse of the f-ratio gives th e number of times the element recycles per year, i.e, an f-ratio of 0.3 implies that an average nitrogen atom cycles around 3 times per year.

,

NO ~

_I \ ;,-,. ,

NO ~ 4

The f-ratio is the ratio of new production to total (new and recycled) production.

N,O 3

N,

2.8.4 Phosphorus

1

NH' .

.....1 - ~

Assimilation

Primary - ....- Heteronepbs producers

•

52 KH constant

--cs, -

(bl

In (b) , both species 1 and 2 have the same value of

J1 max ' However, spec ies 1 has a lower value of KN t han species 2 . In th is case, species 1 reaches its maximum growth rate at lower nutrient concent rat ions than spec ies 2. Therefo re, in low nut rient concentrat ions, species 1 w ill dominate, altho ugh at higher nut rient conditions both spec ies will grow equally.

--• -=~

0

~

In the third example (c), spec ies 1 has a higher J1 ma x

0

=

·0

II .... constant

~

=

~

K,51 < 52

('I

52 dominates -

:-

, ,,,

51 dominates

51

than speci es 2, but the latter has a lower KN t han species 1. At lower nutrient concen trations species 2 grows faster and dominates because it reache s its maximum growth rate at lower nut rient concentrat ions. However, at higher nutrient concentrations, species 1 dominates because of its greater maxi mu m growth rate.

.....-- 7"' - - - - - 52 Examples of possible variations p .... 51 > 52

In

nutrient growth

curves of competing pairs of phytoplankton with different specific growth rates (,Li) , maximum growth rates

Nutrient

•

(,Limax) and half saturation constants (~) for nutrient

uptake (from Lalli & Parsons 2004).

2.9 Algal growth •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 2.10: Definition of productivity terms

whether the community is g rowi ng o r contract ing. It is important not to confuse these terms and the use of net production, w hich is co mmonly fo und in the literatu re and

There is a set of definitions used in ecology that derive basically from th ree physiological processes, namely:

3

Photosynth esis

Whole community respiration

Fo r a number of reasons the two processes of photosynthesis (P) and respiratio n (R) are out of phase, so

= P. 2 Algal respiration = Ra • 1

could refer to either, is to be avo ided.

there will be places and times when and where P > R

= Rc '

The pri mary photosynthetic event is termed Gross

Production = P.

and R > R The difference between these two processes (P) - (R) is te rmed net community production (NCP) (see Box 2.5 regarding the critical depth). Unlike photosynthesis and respi ration, net community production is

The difference between productio n and respiration in

not a process in its own right: there is not a dedicated

the algal community is te rmed Net Primary Production (also Net Photosynthesis) = P - Ra '

set of enzymes or a single metabolic pathway tha t gives rise to NCP; rat her it is an arithmetic difference. Never-

The difference between production and respiration

theless it is arguably the most valuable plan ktoni c rate

within the whole community is termed Net Community

measurement we can make, and is the best descrip tor of

Production (also Net Ecosystem Production) = P-R c ' Net Primary Production tells us how much energy

the waxing and waning of the population. Net

and organic materi al is available to the heterotrophi c com-

net primary production (NPP; also referred to as net

munity, whe reas Net Community Production tells us

photosynthesis: see 2.8), which is photosynthesis minus

about the balance wi thi n the community as a whole, i.e.

autotrophic respi ration. Ari thmetically NPP > NCR

community

production should be distinguished from the similar te rm

CURRENT FOCUS: Using algae for carbon sequestration and algal biofuel production Under ideal conditions of light and replete nutrients, microalgae can grow at high rates and achieve high biomass. For several decades there have been numerous industrial driven research initiatives desig ned to intensively cult ivate microalgal cultures on a large scale. This has successfully been done in b ioreactors and shallow ponds/ raceways for the cultivation of algae for the nutraceut ical industry and fo r biomass pri marily for aquaculture feeds (http: / /www. algae.wu r.nl / UK/Welcome/). In the past ten years there has been renewed vigor in research into the large-scale growth of algae as a potential source of lipids that can be converted into biof uels and/or as a way of sequestering CO 2 from industrial processes. The case fo r the latter is a co mpelling one, since from a basic knowledge of Redfield ratio and the equations for photosynthesis and respirat ion it can be calcul ated that for 0.8 tonnes of algal b io mass produced, 1.8 tonne of CO2 will be assimilated. For this amou nt of algal b io-

trace nutrients. This addi tional requi rement for nutrients

Large-scale cultures of algae can be grown in bioreactors s uch as these, which ca n be expanded to fill large areas of land or in greenhouses. The key is to keep the tubing narrow enough to maximize the light penetra-

besides CO2 is one of the key factors to be considered in

tion (photograph: David Thomas).

mass to be produced there would need to be about 45 kg of nitrogen and 4 kg of phosphorus added to the system, as well as lower amounts of othe r maj or and

Chapter 2 Primary Production Processes

any economic analysis as to the viability of growing algae

processi ng the remaining biomass, it appears difficult to

in a sustainable way. Using industrial fertilizers clearly

see how biofuel production from algae can be competitive

adds a considerable cost to the product (algal biomass)

compared to the intensive cultivation of oil-rich terrestrial

and generates no greater benefit than growing normal

plants. See debate between Reijnders (2008) and Christi

efficient terrestrial crop species. However, if the algae can be grown utilizing nutrient-rich waters from industrial,

(2008) and further insight by Weyer et al. (2009).

municipal waste outlets, then of course the whole process

scale, it is important that light does not become limiting

becomes more tenable.

to growth. This nat urally dictates where on th e planet

In terms of carbon sequestration, of course, just producing biomass is not enough, but something has to

such systems are viable wi thout th e additional cost for ar tificial lighting. The cell cul tures will become dense and

be done with the biomass. As pointed out earlier in the

th erefore 'shelf shadi ng ' will prevent even illumination of

chapter, algae do produce lipids and in several species

all cells in a suspension. This effect can be minimized in

at various stages of growth and/or under specific environmen tal conditions, lipid content can increase over 20%

one of two ways:

of the biomass. The attraction of easily growing lipid-rich, high-biomass 'crops' of algae for biofuel production has achieved much attention. However, it should be stressed

In any design for a facility for growing on the industrial-

1. Growing t he cell suspensions In shallow ponds in which the algae are well mixed to ensure that they do not settle.

that in exponentially growing cultures of the vast majority

2. Growing the cell suspensions flowing through trans-

of algal species, the lipid content is relatively low « 10% of

parent t ub ing narrow enough to ensure th at light can

the total biomass). As compelling as the concept is, w hen

penetrate to the middle of the tube, even when the

all the costs of production, includi ng cost of nutrient addi-

cell suspension is very dense, but not so narrow that

tions, energy to remove the water from the cell suspension,

the shear stress acting on the cells actually causes the

energy to extract lipids from the biomass, and the costs of

cells to be damaged (Richmond 2004).

The potential use of large-scale cultivation of algae is hardly a new idea. Over 50 years ago this image was a rather fanciful idea about how massive algal farms could be set up in space to satisfy a future demand for human nutrition (Image from the journal Mechanix Illustrated, May 1954).

2.11 Global trend in primary production •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

2.10 Seasonal trends in primary production In nature it is impossible simply to consider the limitation of algal growth in terms of a single factor, as in the examples given above (Jickells 1998). Although only one nutrient may limit the growth of an alga at anyone time, whether or not an alga will grow will depend also on other growth-limiting factors of which the most important is light. No matter what the nutrient concentration, if there is not enough light to reach maximum photosynthetic rates. growth rates will be compromised. By contrast, if there is plenty of light to saturate photosynthetic systems. but there are no nutrients. growth will not take place. This is most vividly shown in the seasonal phytoplankton growth dynamics in temperate (mid to h igh latitude) waters in which seasonal thermal stratification of the water column takes place that is presented in Chapter 3 .

2.10.1 Succession of phytoplankton •

species When we measure phytoplankton dynamics in terms of increases in chlorophyll or particulate organic carbon concentrations in the water, there is the great danger in forgetting that these changes are the result of the growth through cell division of a number of phytoplankton species. Different phytoplankton species dominate at different times of the year. and this succession of dominant phytoplankton species is thought to be controlled by a complex mosaic of factors. such as temperature, irradiance, growth rates, and nutrient supply (Box 2.9; Fig. 2.29) . Added to this is the influence of grazing by protozoan a nd zooplankton species, which can have a major role. It is important to note that this succession is not the same as that Sea 5Urf,re

--• - N. c

'E

~ ~

Ihermedlne Nutrient flux

c

~

:: 140

160 180 200

M90919293~95%9 798990001~~M~M0 7~

0.05

0.1

0.15

0.2

0.25

0.3

Lon g-term trend s in cho ro p hyll a in th e HOT d ata set . Larg e inter- annual variatio n is dearly seen wit h peak values in 19 8 9 , 19 9 9 , and si nce 200 5 bein g greater th an th e ot he r years. NB Thi s is an o ligotrop hic site and th e maximum Chl-a values are ve ry mu ch less than peak values measured in more nutrient-ri ch systems. Al so note that th e maximum st anding stoc k of algae is between 60 and 140 m water depth and not at the surface (see Fig. 2.28) (image w it h perm ission of HOT pro gramme, http:/ /hahana.so est.haw aii.edu).

Chapter 2 Primary Production Processes

Of course the long-term t rends at anyone site may be

standing stock are recurrent and synchronous over large

unique to that site and a synthesis of results from several

geographic regions. As a conclusion of their work th ey

sites is a key to understanding controlling factors th at force

posed two fundamental ecological questions: ' ( 1) how do

results. This was attempted by Cloern and Jassby (2008)

estuari ne and coastal consumers adapt to an irregular and

who searched 11 4 databases from around the world for

unpredictable food supply, and (2) how can we extract

seasonal trends in phytoplankton biomass in te rms of

signals of cli mate change from phytoplankton observa-

chlorophyll concentration. Their analyses showed that there was much greater variability between and within the

tions in coastal ecosystems where local-scale processes can mask responses to changing climate?'. These are key

systems they looked at (estuaries, lagoons, shallow inland

ecological questions facing marine bio logists/b io logical

seas, coastal waters) compared to the terrestrial and true

oceanog raphers working with planktonic systems in the

oceanic sites for which seasonal variation in phytoplankton

co ming decades.

Figure 2.44 In this st riking pi cture, th e import ance of primary produ cti on p rocesses for th e marin e ecosystem can b e su mmed up: from th e microbes t o th e w hales th e energy harvested throu gh ph oto synth esis is th e basis of it all. This is a sout hern ri ght w hale mother wit h her calf swimming along the shores of Peninsula Valdes in Argentina. As they move their t ail s, a g reen t id e of phytop lankto n swirls b ehind th em . Algal blooms are becomin g more frequent in th e bays of Peninsula Va ldes, w here so ut hern right w hales gat her each year t o g ive b irth and nurse the ir calves (photog raph by Mariano Sironi, Instituto d e Conservac i6 n d e Ball enas, Bu enos Aires, Argentina. http:/ / www.icb.org.ar).

Further Reading •

••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Chapter Summary •

Abou t half of the global primary production takes place in marine systems. Most of the primary prod uction in the world's oceans is d ue to microscopic phytoplankton, si nce macroalgae are restricted to a rather

narrow band on coastlines.

•

Photosynthetic algae can vary in size from just a few

urn

to giant macroalgae > 50 m long. Growth of

primary producers is the difference between the gains from photosynt hesis and losses to respirati o n, excretion , and the construct ion of skeletal material and storage products.

•

Rates of primary production are mainly controlled by light and inorganic nutrient supply. The amount of light available for photosynthesis depends upon water depth, and the amount of lig ht-scattering particles that occur in the water:

•

The main limiting inorganic nutrients are nitrogen and phosphorus, while in certain marine systems trace elements such as iron are limiting.

•

Seasonal dynam ics of algal growth are controlled by a complicated suite of interactions between irradiance and nutrient supply, ultimately driven by the physical dynamics of the system.

•

Eutrophication of a water body is a reversible process and can be caused by factors other than solely increased inorganic nutrient loading of a system.

•

Frontal systems, gyres, river plumes, and coastal upwelling all influence the rate of primary production, as they influence the transport of nutrient-rich waters to the sea surface.

•

Primary production in polar oceans is restricted to a short summer season, in contrast to temperate waters where two peaks in production are often observed. Primary production of tropical waters is generally consistently low.

•

The measurement of small-scale primary production can be made using oxygen and carbon dioxide tracers, or electrodes and various fluo rometric techniques. On a global scale primary production is measured using satellite-borne colour sensors that are used to estimate the concentrations of plankton in the water:

Further Reading A classic introduction to phytoplankton dynamics and constraints on growth is presented by Fogg (199 1) as well as short essays by Smetacek (1999, 200 1, 2002), The evolutio n of modern phytoplankton is discussed by Falkowski et al. (2004), Both Falkowski and Raven (2007) and Williams et al. (2002) give comprehensive overviews of primary pro-

duction in aquatic systems, whereas del Giorgio and Wi lliams (2005) deal specifically with respiration. However, these primarily deal with phytoplankton, while Lobban and Harrison ( 1997), Lee (2008) , and Graham and Wilcox (2008) give good overviews of factors influencing primary production of macroalgae. Microbial processes and the underlying biochemistry of photosynthesis, respiration, and associated metabolism is given by Mad igan et al. (2008) , who also give a good overview of microbial physio logy and ecology, Bacterial metabolism and ecology is comprehensively covered by Dyer (2003) , as is general marine microbial dynamics by Kirchmann (2008), The influence of physical processes on primary production is dealt with by Mann and Lazier (2005), Bigg (2003) summarizes many of the large-scale ocean processes that infl uence primary prod uction. It is important to set the topics covered by this chapter into a wider context of biological oceanography, and Lalli and Parsons (2004), Libes (2009) , Mann and Lazier (2005) , Stumm and Morgan, 199 5, Millar (2004) , Cockell et al. (2007) , and Millero (2005) comprehensively link aspects of physics, chemistry, and biology. There are three excellent books published by The Open University (1995, 2000, & 2005) , that together make a superb companion text to discussions about issues re lated to marine primary production. For a more global consideration of primary prod uction and its role in global biogech emical cycles, comprehensive overviews are given by Andrews et al. (2003) , Black and Shimm ield (2003), Emersen & Hedges (2008) , Longhurst (2006) , Sar miento & Gruber (2006), and Schulz and label (2000), Broecker (2009) gives a comprehensive overvi ew of the oceans in terms of climate change. Arrigo (200 5) gives a comprehensive overview of the ro le of microorganisms, nutrient cycles, and biogeochemical cycling in marine systems.

Chapter 2 Primary Production Processes One of the best resources for informed short essays on many of the issues raised in this chapter can be found in Oceanus, a popular forum pub lished by the Woods Hole Oceanograph ic Inst itute. (http:/ /www. whoi.edu/oceanus/i ndex.do) . •

Andrews, J, E" Brimblecom be, P., Jickell s, T. D., Liss, P. S., & Reid, B. J. 2003 . An Introduction to Environ-

mental Chemistry. Wiley-Blackwell. •

Arrigo, K. R. 200S. Marine microorganisms and global nutrient cycles. Nature, 437 : 3 49-355.

•

Bigg, G, 2003. The Oceans and Climate. Cambridge Univers ity Press,

•

Black, K. D. & Shimm ield, G, B. 2003. Biogeochemistry of Marine Systems. Wiley-Blackwell .

•

Broecker, W. 2009. Wally 's quest to understand the oceans CaC0 3 cycle. Annual Review of Marine Science, 1: 1- 18.

•

Broecker, W. 2010. The Great Ocean Conveyor: Discovering the Trigger for Abrupt Climate Change,

Princeton University Press, •

Cockell, C; Corfield, R. , Edwards, N., & Harris, N. 2007 . An Introduction to the Earth-Life System. Cambridge University Press,

•

Del Giorg io, P. & Williams, P. J. Ie B. 2005. Respirotion in Aquatic Systems, Oxford University Press.

•

Dyer, B. D, 2003. A Field Guide to Bacteria. Comstock/Cornell paperbacks, Cornell University Press.

•

Emerson , S, R. & Hedges, J. I. 2008, Chemical Oceanogrophy and the Marine Carbon Cycle. Cambridge

University Press. •

Falkowski, P. G, & Raven, J. A. 2007 . Aquatic Photosynthesis 2nd edn. Princeton University Press,

•

Falkowski, P. G., Katz, M. E., Knoll, A. H., Quigg, A. , & Raven, J. A. 2004 . The evol ution of modern eukaryotic phytoplankton, Science 305: 354-360.

•

Fogg, G, E. 1991, Tansley Review No. 30, The phytoplankton ways of life. New Phytologist 1 18 : 19 1- 2 3 2 .

•

Graham, L. E. & Wi lcox, L W, 2008, Algae. Benjemin Cumm ings,

•

Kirchman, D. L, 2008. Microbial Ecology of the Oceans 2nd edn . Wiley Blackwell.

•

Lal li, C. M. & Parsons, T. R. 2004, Biological Oceanogrophy. An Introduction 2nd edn . Butterworth -

Heinemann. •

Lee, R. E. 2008. Phycology 4 t h edn. Cambridge University Press, Cambridge,

•

Libes, S, M. 2009. An Introduction to Marine Biogeochemistry 2nd edn. Academ ic Press.

•

Lobban, C. S, & Harrison, P. J. 1997. Seaweed Ecology and Physiology. Cambridge University Press,

•

Longhurst, A. 2006. Ecological Geography of the Sea 2nd ed n. Academ ic Press,

•

Mad igan , M. T., Martinko, J. M., & Parker, J. 2008, Brock Biology of Microorganisms 12th edn. Pearson

Education. •

Mann, K. H. & Lazier, J. R. N. 2005. Dynamics of Marine Ecasystems: Biological-physicallnteroctions in

the Oceans 3 rd edn. Wiley Blackwell. •

Miller, C. B, 2004, Biological Oceanography. Wiley Blackwell.

•

Millero, FJ. 2005. Chemical Oceanography 3 rd edn. CRC Press, Florida, USA.

•

Open Un iversity. 1995. Seawater, its Composition, Properties and Behaviour. Butterworth -Heinemann.

•

Open Un iversity. 2000. Waves, Tides and Shaffow-Water Processes. Butterworth -Heinemann.

•

Open Un iversity. 2005. Marine Biogeochemical Cycles. Butterworth-Heinemann.

•

Sarmiento, J. L. & Gruber, N. 2006. Ocean Biogeochemical Dynamics. Princeton University Press.

•

Schulz, H. D. & Zabel, M. 2000. Marine Geochemistry. Springer Verlag,

•

Smetacek, V. 2002 . The ocean's veil. Nature 419: 565.

•

Srnetacek, V. 2001 . A watery arms race. Nature 41 1: 745.

•

Srnetacek, V. 19 9 9 . Revo lution in the ocean. Nature 40 1: 647 .

•

Stumm, W. & Morgan , JJ, 19 9 5. Aquatic Chemistry-Chemical Equilibria and Rates in Natural Waters 3rd edn. Wiley Blackwell, Oxford, UK,

•

Williams, P. J, Ie B" Thomas, D. N., & Reynolds, C. S. 2002. Phytoplankton Productivity: Carbon Assimila-

tion in Marine and Freshwater Ecosystems. Wiley Blackwell.

Microbial Ecology: Production and the Decomposition of Organic Material

Chapter Summary Micro-organisms have the most important role in the recycl ing, decompositi on, and remineralization of organic material. This chapter will reveal how they play such a do minant role and introduce the most important organ ism groups in oceanic microb ial food webs. The ecological context into which these micro-organisms are embedded is developed and leads to a view that the microbial food web may be seen

as having two origins: photosynthes is and detrital organic matter. Th e production and composit ion of dissolved and

3.1 Introduction All sustainable systems are cyclic. In Chapters 1 and 2 the production of organic material by marine algae was considered. The production process utilizes energy in the form of light. water. and inorganic nutrients, suc h as nitrates, phosphates, and carbon dioxide. For the cycle of nature to be completed. t his energy must be rele ased as heat and the ele men ts ass im ilated into organic m aterial du ring photosynthesis, and then recycled back to their inorganic state. Th is process. the complement to photosynthes is. is respiration. In its n arrowest meaning. respiration is simply the biological oxidation of organic material, typically by oxygen. and the formation of water and carbon dioxide; the reformation of the inorganic nutrients is an intimately associated process. known by a number of synonyms: mineralization and remineralization (Chapte r 2) . As the process also results in the breakdown of organic m aterial it also carries the name decomposition. All living organisms respire; however. in the oceans this process is dom inated by the prokaryotic m icro-organisms (shortly m icrobes). notably the bacteria and archaea.

particulate organi c matter is explored, as is the basic process of decomposition. The organi sms that comprise the mi crobial communi ty are introduced together with the ir re lative abu ndances and interactions. The complex chall enge of how we measure microbial diversity and activ ity, and count micro-organisms in the oceans, leads to a consideration of the dynami cs of bacterial growth. Fi nally, the chapter concl udes by discussing the seasonal cycle of production and consumpti on a nd the role of marine mi crobes in the global carbon cycle and cli mate system.

Prokaryotic organisms are micro-organisms (bacteria and archaea) that do not, unlike eukaryotes (e.g. plants, animals), have separate organelles like a nucleus (Greek karyon), in their cells.

3.2 The microbial powerhouse We can readily perceive larger organisms as whales, fish, and large invertebrates in the seas since they occupy the same spatial scales (centimetres to tens of metres) as humans. In contrast, microbes can be seen and studied only w ith the help of sophisticated technology, but the same also holds true for most of the life in the dark abyssal layers of ocean. Temporal, spatial, and bod y-size scale issues, and t he necessary observational techniques and devices to study m icrobes, distinguish them from othe r organisms. Understanding the properties of the miniature scales inhabited by m icrobes is required if we are to really understand t he m and how they fun ction (see Box 3.2) . Although the oceans are mainly (99.99999%) water; the biota occupy only approxi-

Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material mately O.0 000 1 % of the total volume. From the organism's point of view the environment is very dilute and empty. To examine marine microbes, the first step is always to concentrate them from water samples. most often by collecting them on fine filters . The consequences for organisms ofliving in a dilute environment and the adaptations needed to cope with it will be discussed later in the chapter. It is difficult to convince even expert marine scientists that the biomass of micro-organisms is comparable to that of whales or fish, and that their activity, as we shall see, exceeds that of the combined metabolism of vertebrates many times. But whyis this 50, and why are marine microbes 50 important in the turnover oforganic material in the sea? Besides their qualitative importance in organic material cycling. prokaryotic microbes are very important in other aspects. Their genetic and metabolic diversity far exceeds the diversity of other groups of organisms. The estimated total number of all eukaryotic marine species. including all phyla of plants, algae, animals, and micro-organisms, in the seas and oceans is 230 000, ofwhich approximately 140 000 are known (world register of marine species at http:/ / www.marinespecies.org/) . Eukaryotic organisms have complex membrane-bound structures, like a nucleus, mitochondria, and chloroplasts in their cells. Eukaryotic organisms include plants, animals, fungi , and protists.

In contrast. the number ofbaeterial species is estimated to be from 1 000000 to 1 000000000 (Curtis et a1. 2002; Pedros-Alio 2006), of which only a tiny fraction is currently known. Metabolic versatility allows bacteria to carry out multiple fundamental biogeochemical processes vital for ecosystem functioning in the ocean. such as the decomposition and utilization of dissolved organic matter. nitrogen fixation, denitrification, and nitrification.

Body size has a major consequence for metabolism (Fenchel 2005) . All free-living organisms take in the metabolites necessary for their growth and dispose of their waste products through the body wall. This transfer is the principal limitation to maximum growth. thus surface area. rather than biomass, is ultimately the main determinant of metabolic rate : If an organism, such as a whale, were to achieve a metabolic rate comparable to a bacteria cell, the metabolic heat it produced would be so difficult to dissipate that its body temperature would rise to 1500°C-it would be white hot. We can explore the consequences of this simply by considering the organism as a simple sphere: S 4.,., 3 V r r3

rx

where r is the radius. S is the surface area (which will reflect metabolism), and V is volume (which is directly related to biomass) . Thus. in the case of our simplistic organism, the specific metabolic rate (metabolism/biomass = S/V) is proportional to l /r, i.e . inversely proportional to the organism's linear dimensions. If we take our end members of the marine community (the marine bacterial cell and the whale) to have linear dimensions of 0 .5 I'm (0.5 x 10-6 m) and 10 m, then if this simple rule is applied, the metabolic rate of a given mass of bacteria would be 2 x 10-', i.e. about 10 million times greater than the same biomass of a whale. The results of this simple calculation are shown in Fig. 3.1 . Now clearly the calculation is simplistic, as organisms, particularly larger ones. are not spheres; further they overcome the S/V limitation in part by increasing the surface areas available for exchange, by convoluted structures such as gills and lungs. Nonetheless there is a limit to this and so we end up with a broad compliance to the S/V rule. but it is not as simple or exact as the formula above. 125

3.2.1 Small organisms are important Why are small organisms so important? There are broadly two answers to this question. First. the primary production of organic material in the seas is associated with microscopic organisms (see Chapter 2 and section 3.8) and the usually large number ofsteps between the primary producers and the marine vertebrates results in the loss of almost all the organic material produced by photosynthesis such tharthere is very little forlarge organisms to live on (3.3.2). Second. and related to this. is the consequence of size. The marine pelagic community spans a range of size from marine bacteria (c.0.1 pg = 0.1 X 10- 12 g), arguably the smallest free-living organisms, to the whales (c.100 tonnes = 108 g), the largest ofanimals. This means that biological biomass spans 21 orders of magnitude.

-3-

11 -e--""-

-

I 000000000

Surfo(e area/volume Volume Areo

10

~

~

E

E

~

~

1000000

75

0

0

~

S

0

~

~

-""0

"0

--

11

~

1000

~

25

~ ~

10.1

~

1

10

100

1000

0 10000

Diameter (J.lm)

Figure 3.1 The relationship between diameter, volume, and surface area for a sphere.

3.3 The ecological context in which the marine microbes are embedded •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

3.2.2 How is metabolic activity distributed and which are the important organisms? Metabolic activity is constrained by metabolic capability and abundance . A surprising observation made by Sheldon et al. (1972) is that if estimates of biomass are assembled in logarithmic categories, there is comparatively little change with body size. Food-web theory suggests that a small decrease in biomass occurs with an increase in the size fraction, which is broadly upheld by field observations. Models that give the distribution of biomass through logarithmic increments of size (as length) suggest a small decrease with body size, which complies with the following relationship: biomass = k x (Size)-O·22 A plot of the above relationship is given in Fig. 3.2, along with the planktonic groupings that are mainly associated with the various size categories (see also Chapters 4 and 7) . 1.0

•

!

!•

' .9

,

a E

.2

~

•

••-.>; ~

~

' .8

•

-

•• ~ • ~ •

• •• ••

,•

•

0.6;;

.s•• ~ •

-•

!

j

~

, .7

:~

!

l

,

•

. - . • ~

~

~

~

~

0

••

•

~

•

~

~

~

•

••

a

-- .-

§

-

-- .§

§

§ §

§ §

--

-

Size (length in 11m)

Figure 3.2 The red line shows the theoretical distribution of biomass with size. The approximate size bands occupied by various planktonic groups are shown. 100

125

•a • • '0

~

a

1;;

~

l'

Distribution of metabolism with size Inueose intumuletlve metobcllsm with size

N

a

ca= 75 'j

."--• E

-

'"

-a

>;

6' "it' E

5.'

4' -a

~

.e

25

'd

\ -

2'

~

•>

~

-" ~

=

= = -

= = = -

= = = = -

Size (in I'mJ

= = = = -=

= = = = 8

-

Specific metabolic rate (metabolism/biomass) is inversely proportional to an organism's linear dimensions.

3.3 The ecological context in which the marine microbes are embedded Before we can explore the role and functioning ofthe microbial community. we need to understand the theoretical ecological context into which it is embedded. As microbes play a central role in the metabolism of organic material in the oceans. as in most other ecosystems, it is logical to outline the rationalizations surrounding the flow of organic material through an ecosystem. The flow oforganic material can be treated in the context of feeding interactions between organisms sharing the same habitat and forming food chains and food webs. Trophic levels indicate the position of an organism in a food chain or food web, hence primary producers make up the lowest trophic level, with the largest predators at the top.

Aquatic food webs are typically size-structured (e.g. Loeuille & Loreau 2005), meaning that body size is an important trait (although not the only one) explaining feeding interactions between organisms (see also Chapter 7) .

0

.~

a a

8'

E

a

~

E

E

-a

~

~

--

In Fig. 3.3 the distributions of activity and biomass given in Figs 3.1 and 3.2 are combined. Because the change of metabolism with size (Fig. 3.2) is much less than biomass (Fig. 3 .1), the resultant line is very similar to the surfaceto-volume relationship given in Fig. 3.1. Thus we have a basis for understanding the major part played by microorganisms in the plankton.

=' = = 8= =

E

8

-

Figure 3.3 The size distribution of metabolism and its progressive integral, with size. The rates are determined as the product of the size distribution of specific metabolic activity (Figure 3.1) and biomass (Figure 3.2) with size. The figure shows that most of the metabolism is associated with organisms less than 100 urn,

3.3.1 The concept and consequence of growth yield An organism cannot grow (convert food into body tissue) with 100o/n efficiency. The laws of thermodynamics show

that work must be done to create new tissue and that this requires energy. This energy derives from respiration. which occurs at the expense of some of the energy derived from assimilated food or photosynthetic assimilation (see Chapter 2 and Fig. 3.4). In addition some of the food is lost via excretion. Respiration and excretion both represent metabolic losses that result from converting food into new organism tissue, i.e. growth. Excretion encompasses both particulate (like zooplankton faecal pellets) and dissolved waste products. This introduces the notion ofthe efficiency

Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material ofgrowth, usually expressed as a growth yield or, since it is often expressed as a percentage, growth efficiency. . Growth yield

growth = Y" = food intake

G G = G + R + E or G + M

where G = growth, R = respiration. E = excretion. and M = metabolism. There is no fixed value for the term Yg, it varies with organism type (unicellular, multicellular), level ofcomplexity, behaviour (motile or non-motile), and stage of development (larva, juvenile, adult) . Typically values lie in the range of 10 to 30% (Chapters 12 and 13).

In this way we may link together the type of flow diagram shown in Fig. 3.4 into a string of trophic yields (see Fig. 3.5) . Given this as a concept we may calculate the overall yield of our simple food chain as:

overall efficiency = Yt = 2 X Yt = 3 X Yt = 4 X

•••

where Yt = 2' Yt = 3' etc.• are the yields at the various trophic levels. If we make the further simplifying assumption that in a given food web the values of Y can be treated as the same. then the above equation simplifies to: overall efficiency = (1';)"

Growth

G Food intake

Y"

growth yield = G/(G+M)

~~ M

Metabolism

Figure 3.4 Schematic of the apportionment of overall metabolism of a heterotroph into metabolism (M) and

growth (G).

3.3.2 Trophic yield and food chain

efficiency One organism's growth is another organism's meal. If we consider a simple linear food chain, comprised of physiologically similar organisms within each trophic grouping, we can extend the growth yield concept to a trophic yield. In this case the production (growth) at one level is taken as the food intake for the subsequent one (Chapters 4 and 7) .

production at trophic level. + 1 fu~k~W=Y= . . ' t production at trophic level.

where Yt is a simple representative trophic yield and n is the number of steps (note. one less than the number of trophic levels) in the food chain. This simple concept was the basis of the early work to predict the fishery potential of the oceans (Ryther 1969) . This concept allows us to explore the significance of growth (trophic) yield and the number of steps in the food chain. This sort of analysis can be extended to more realistic branched and interlinked complex food webs, with differentyields at various trophic levels. but the broad outcome is much the same, and at this level the additional complexity is not justified. The point made by these calculations (Table 3.1) is that both properties have a profound effect upon the overall efficiency of the food web, and most natural food chains (and in particular food webs) are, and need to be, energetically inefficient. This inefficiencyis a consequence of the very large fraction respired and recycled back (remineralized) to form the inorganic carbon and, more importantly. inorganic nitrogen and phosphorus, originally used during phytoplankton production. Without this efficient recycling of nutrients. the food webs in the oceans, as in any other ecosystem. would rapidly stagnate. We may now build recycling of nutrients into our developing conceptual model ofthe food chain.

Growlh

Food intake

Growlh G Y. = growthyield = GI(G+M)

•

Ett.....

Food intoke Metabolitm

Metabolitm

Trophic level 3

Metabolism

Trophic level 2 Trophi( level I

Figure 3.5 The simple scheme shown in Figure 3.4 embedded in a linear heterotrophic food chain. Photosynthetic

primary production (the green ellipse) is taken to be the starting point.

3.4 The decomposition process •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Table 3 .1 Ca lculat ion of the effect of trophic yie ld and the number of trophic levels o n overall losses and yields in a simplifi ed food chain.

Trophic yield (%j

Number of trophic levels in the food chain

5

2

Yield offood chain (as %) I 9

10 30

0.001 0.24

• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

Loss through the trophi c levels (%) 99 99.999 99.76 91

10 30

10 30

Yield from I tonne of phytoplankton production 10kg 10 9 90 kg 2.4 kg

3.4 The decomposition process So far we have explored a simple linear food chain, supported by photosynthetic production. The losses due to respiration have been built into this sequence in Fig. 3.6. We now need to consider the organic losses-the formation and decomposition of organic detritus. This leads to a realization that there is a second base to the food we b: a food chain leading from detrital organic material. Although decomposition is seen to be the prerogative of the microbes (the group referred to by ecologists as the decomposers), it is a process to which all heterotrophic organisms contribute , from bacteria to whales, although for the reasons discussed in 3.2.1, bacteria and the protists play the dominant role. Decomposition of organic material back into energy and inorganic material is a process to which all heterotrophic organisms contribute, although the microbes play a dominant role.

Decomposition, the breakdown of organ ic material by heterotrophic metabolism as a consequence of respiration, results in the production of ino rgan ic carbon (as CO2 ) , nitrogen (as ammonium) , and phosphorus (as phosphate) ; the process is collectively referred to as remineralization (or sometimes simply as mineralization) .

3.4.1 Marine detritus Although, as we will see later, there is direct release of soluble organic material from marine organisms during feeding

and growt h, it is conven ient to consider the decomposition process as starting from particulate material. Biological particulate material mostly consists of organic macromolecules as cellulose, proteins, ch itin, and fats. Protein- and carbohydrate-like components are most biodegrad able, w ith turnover times from months to years in the surface ocean, whereas other biological macromolecules, such as the components of bacterial cell walls themselves, as well as other molecules of bacterial origin, are mo re resistant to enzymatic attack and can persist in the environment even thousands of years (Loh et aI. 2004; Nagata 2008) . The initial stage of the whole degrad ation process is the conversion of the insoluble, non-diffusible material to low molecular weight (LMW) dissolved material by extracellular hydrolytic enzymes (digestive enzymes) . In principle, the first stage must occur outside the cell, in the gu t, in vesicles, or in the external environment. Bacteria are obligate osmotrophs, i.e. capable of taking only dissolved substrates into the cell. They must eit her secre te extracellular enzymes or use enzymes attached to their cell surface structures. The low molecular weight products (amino acids, sugars, fatty acids) may now diffuse or be actively transported into the cell, through the cell membrane in single-celled organisms (bacteria, protists) or the gut wall in the case of most metazoans. The subsequent stages of metabolism, and in particular the very final stages (respiration) , are complex biochemical processes that require a high level of organization that can only occur w it hin the cell (Chapter 2) . As the biochemical basis of respiration is rather universal in all heterotrophic organisms, we can now se parate the first stage in Fig. 3.4 into these two steps (see Fig. 3. 7). No food chain is entirely closed, there is always some

Chapter 3 Microbial Ecology: Production and the Decomposition of Organic Material Ircphk level3 Trophic level 2 Growth

Irephk level I Growlh

Ett.....

Food intoke Metabolitm

Food intake Metabolitm

PhatOiynthesii

Reminerolizotion of C, N, and P

Figure 3.6 The flow of respired nutrients has been added to Figure 3.5.

Growth Particulate & high MW material

Food intake Metabolism

Figure 3.7 An extended version of Figure 3.4, showing

the two stages in decomposition.

wastage of food along the way. Wastage may occur through faeces. from incomplete digestion, release of soluble organic material from the algae or heterotrophic organisms (exud ates), or damage of, or incomplete feeding upon, the prey (so called 'sloppy feeding') . All of these sources of wastage are included in the loss term 'excretion' in the food web model developed in this chapter. Dead organisms are also part of decaying particulate organic matter. In addition organic matter is transported from terrestrial ecosystems via rivers to estuaries. coastal waters, and continental shelf regions. This (both soluble and particulate material) is collectively known as marine detritus (see Fig. 3.8), the nature and origins of which are dealt with in the following section.

3.4.2 The nature and production of marine detritus Marine organic detritus is partly composed of the scraps left over from the various 'meals' of the marine heterotrophs. As such it has no particular composition and thus will vary with the type offood organism and the feeding mechanism. Although organic detritus may be of poor nutritional value to the organism giving rise to its production. the microorganisms have the metabolic and nutritional versatility to make a meal out ofit. In addition to the uneaten remains and dead organisms. there are two additional sources of marine detritus. Various marine organisms. including

the microbes. secrete mucilage or various classes of polysaccharide material (exopolymeric substances abbreviated to EPS; we revisit this in Chapter 8) during their growth and development; for example, coral are a rich source of mucilaginous material. Appendicularians (a class of chordates also known as larvaceans) surround themselves with a mucilaginous 'house'. which contains filtering apparatus with which food is garnered. When the filters become blocked they discard the 'house' and construct a new one; this process takes a few minutes and can be repeated up to a dozen times per day. A quite different source of organic detritus comes from the algae themselves. The mechanism and causes of release ofthis dissolved organic material are far from clear. It occurs in active as well as moribund cells, so it may be regarded as a 'normal' part of the metabolism of the algae. The release of dissolved organic material would appear to be high when the cells are under high irradiances and in such situations a metabolic pathway (photo-respiration), closely associated with the primary CO2 fixation, is known to produce compounds such as glycolic acid (glycolate) , and amino acids (serine and glycine) as by-products. However, this is probably only one of a series of processes giving rise to the release of these compounds. The extent of release in actively growing, unstressed cells, is probably in the range of 5 to 15% of photosynthetic production (Chapter 2), but may rise to 50 to 80% if the algae are stressed by high light or low nutrient conditions. Because of its multiplicity of sources and formation mechanisms, marine detritus is a heterogeneous mix of compounds and not readily amenable to detailed chemical analysis. The organic matter in the ocean forms a size continuum from millimetre to nanometre scales. For practical reasons the organic matter is typically divided into two categories based primarily on size. using fine filters, into so-called dissolved and particulate organic material (DOM and POM) . The point of separation is not exact but

3.4 The decomposition process •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Organicdetritus

~

-, ~

Growth

.Y' Y =g rowth yield= G/(G+Ml

,,'

Food inlll ke

/'

At .........

....

-:

, Growth

-,

Poololynthl.'lil

Reminerclizution of C, N,a nd P

Growth MelDbol i~m

34). To achieve such concentrated saline conditions. the water body has to have an evaporation rate greater than the inflow of fresh water, so

Ultraha line

r

/

0

o 5 15

25

Estuary

35 45 55 65 75 85 95

135 145

+300

Salinity

Figure 5.20 Hypothetical diversity trend over the fu ll salinity range including hypersaline waters.

Chapter 5 Estuaries •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

developed for estuaries and hyposaline seas (Fig. 5.20) . Generally, there is a decrease in diversity with an increase in salinity from 34 until the ultrahaline conditions are reached, which are inhabited by just a couple of species. The Remane diagram can be extended (Hedgpeth 1967; Fig. 5.20) to demonstrate how the diversity trend over the full salinity range may be expressed (Fig. 5.20) .

5.5.3 Lagoons Lagoons are comparatively small areas of sea that have been semi-isolated by the development of a barrier. Superficially, they appear similar to systems such as the Sivash, but generally lagoons are much smaller and in particular they are very shallow, generally only a few metres deep. Consequently, they rarely become stratified in the summer due mainly to wind action, but can vary in size considerably. The whole SE of the USA could be viewed as a series oflagoons and bar-built estuaries extending 4500 Ian along the coast. Most are much smaller, the largest in the UK being the 14 Ian Fleet lagoon in Dorset, England. Lagoons can form through the development of two main types of barrier. The deposition of sand can commence offshore, which eventually builds into a bar with no connection to the land (similar to bar-built estuaries), thus enclosing a shallow body of water. An example is the Laguna Madre in Texas, USA (Fig. 5.19b) . Alternatively, barrier formation can extend out from the land (longshore barrier), eventually isolating the lagoon (e.g. the Vistula lagoon, Poland; Fig.5.19a) . Lagoons demonstrate a wide range of salinity regimes,

from hyposaline (e.g. Vistula, 0-6) to hypersaline (e.g. Laguna Madre, 39-62). In rare cases a variable salinity gradient is apparent over very small scales within lagoons. an example being the Swanpool, Cornwall, UK. This is a small, generally hyposaline lagoon with depths < 3 m. A low sill at the seaward end of the lagoon enables full-strength seawater to overflow at high tides. Due to its density. this seawater slides to the bottom of the lagoon creating a halocline with low-salinity water floating on seawater and a fast transition in terms ofsalinityfrom 4 to 34 (see also ROFIs in Chapter 8) . In tropical areas, lagoons are often fringed by mangroves (see Chapter 10); reed beds, e.g. Phragmites are the dominant fringing plant in temperate areas. However. due to their size. shallow nature. and comparative stability, lagoons often differ markedly from estuaries and other larger brackish-water systems by possessing a diverse submerged plant community, with macrophytes able to root on the lagoon floor. The plants present reflect the salinity of the lagoon, with pond species, such as water lilies (e.g. Nymphea), present in the more freshwater systems, while halophytes dominate saline lagoons, in particular seagrasses such as Halodule spp. (Chapter 10). The fauna of lagoons tends to reflect the pool ofspecies in the neighbouring main body of water. but lagoon specialists can occur. Examples analogous to estuarine species are the lagoon cockle (Cera.stodermaglaucum) and the snail Hydrobia ventrosa . Halophytes are angiosperm plants that can tolerate increased salt levels in the sediment. These include seagrasses and saltmarsh plants.

Chapter Summary •

Estuaries represent the transition system between freshwater and marine biomes, but most estuar-

ies were only formed following the end of the last ice age 6-10 000 years ago. •

Conditions within tidal estuaries are exceptionally variable, particularly salinity, sediment type, oxygen, and temperature. This variability results in harsh conditions that are amongst the most challenging for life in the marine environment.

•

Estuarine systems include a mix of freshwater and marine organisms, few of which can tolerate the physico-chemical conditions present in the mid-estuary. Most successful organisms are excellent osmoregulators, which are capable of adjusting the balance between their internal body fluid salt concentrations and those of the external water. These species can be very abundant in estuarine mud .

•

The distribution of organisms within an estuary is not just controlled by salinity. Many organisms require the presence of mud, or depend on cues from other environmental variables, such as temperature or freshwater flow, to determine where they are found .

•

The amount of fresh water entering estuaries from the river has a major influence on the ecology of the system, affecting production, diversity, and distribution of organisms.

Further Reading •

Estuaries are exceptionally important nursery grounds for many marine fish species, young fish exploit ing the high food source and more favourable conditions for survival and growth. In temperate regions, saltmarshes associated with estuaries can also be important foraging areas for juvenile fish.

•

Estuarine food webs are powered by detritus from a range of marine, freshwater, terrestrial, and estuarine sources, although it would appear that terrestrial carbon is relatively unimportant, despite vast amounts entering temperate estuaries in autumn and win ter.

•

Estuaries are exceptionally important habitats for birds, particularly those on migration . Four and a half million shorebirds migrate to just the British Isles every yea r; where they exploit the high biomass of invertebrates in mudflats.

•

Many inl and seas, such as the Baltic and Black Sea, have conditions similar to estuaries, but generally do not have tides. In these systems the salinity gradient is much less variable and marine organisms tend t o be found at lower sali nities in these seas than in tid al estuaries.

Further Reading Books •

Adam, P. 1990 . Saltmarsh Ecology. Cambridge Un iversity Press, Cambridge.

•

McLusky. D.5. & M. Ell iott. 2004 . The Estuarine Ecosystem: Ecology. Threats, and Management. Oxford University Press, Oxford.

•

Sutherland. W. J. 199 6 . From Individual Behaviour to Population Ecology. Oxford University Press, Oxford.

Key Papers and Reviews •

Attrill, M. J. & S. D. Ru ndle 2002 . Ecotone or ecocl ine: ecological bo undaries in estuaries.

Estuar. Coast.

Shelf Sci 55: 929-36. •

Emmerson M. C. et al. 200 1. Consistent patterns and the idiosyncrati c effects of biodiversity in marine

ecosystems. Nature 4 11 (6833) : 73-77 . •

Lotze. H. K.• Lenihan. H. S.• Bourque. B. J., Bradbury. R. H.• Cooke, R G.• Kay. M. C. et al. 2006. Depletion, degradation, and recovery pote ntial of estuaries and coastal seas. Science 3 12: 1806-1809.

•

Rowntree, RA. & K.W. Able. 2007. Spatial and temporal habitat use patterns for salt marsh nekton: implications for ecolog ical fu nctions. Aquatic Ecology 4 1: 25-45.

•

Williams S. L. and Grosholz, E. D. 2008. The invasive species challenge in estuarine and coastal environments: marrying management and science. Estuaries &

Coasts 3 1: 3-20

Rocky and Sandy Shores

Chapter Summary

such as coastal d efence, recreat ion , and fisheries p rod-

The biodiver sity of the shore is exceptionally high com-

ucts. Shorelines around the world are experiencing maj or

pared to lan d, wi t h all major taxonomic groups represented .

impacts caused by human po pulat ion pressure and there is

Ecological research on shores has underpinned much of

a necessity to defend our economic and soc ial investment

present-day marine ecology and has strongly influenced mainstream ecology. In addition, shores are of increasi ng

in coastal development from the effects of accelerated sea-

concern to governmental policy-makers becau se of their

is therefore important not simply for intellectual reasons, but

recognized provision of goods and serv ices for humans,

for practical purposes if their full value is to be maintained .

6.1 Introduction The habitat created at the point where the land meets the sea is the most accessible part of the m arine environment for humans. To explore deeper and further out to sea requires rafts, canoes, or larger vessels and involves increased risks, wh ile the shore itself, including adjacent shallow waters, offe rs rich resources that can be collected wit hout great effort. It is therefore no surprise that early human settlements abound on coastlines, a pattern of habitation that persists to the present day. Shores are studied because they are accessible, taxonomically relatively simple, and provide ecological goods and services to society (see the Preface and Chapter 16 for a definition of goods and services).

Early m arine biologists found the shore attract ive for their science for similar reasons of access ibility and the diversity of habitats and their associated fauna. The biodivers ity of the shore is exception ally high compare d to land, with all major taxonomic groups represented (even insects, if you look hard enough) , and the fauna and flora are easily collected for study or m anipulated experimentally. As a

level rise. Understanding how shores function ecologically

result, it is not surprising that ecological research on shores has underpinned much of m arine ecology and has been the laboratory of prefere nce for m any m ainstream ecologists. In addition , shores are of increasing concern to govern mental policymakers because of their recognized provision of goods and services for humans, such as coastal defence, recreation, and fisheries products (Duarte 2000), and the curre nt threats to these services (Brown & McLachlan 2002 ; Kenn ish 2002; Thompson et al. 2002). Shore lines around the world are experiencing m ajor impacts caused by human population pressure and there is a necessity to defend our economic and social investment in coastal development from the effects of accelerated sea-level rise by spe nd ing many millions of dollars on coastal defence projects. Understand ing how shores function ecologically is therefore important not simply for intellectual reasons, but for practical purposes if their economic value, as well as their aesthetic and cultural values are to be m aintained. Shorelines around the world are experiencing increasing pressure from human developments that threaten their physical and ecological integrity despite our increasing dependence on the services provided to human society.

6.2 What is the shore? •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

6.2 What is the shore? Defining the shore is not as straightforward as it might seem. The early domination of shore ecology by northwest European and North American scientists who worked in macro-tidal areas has resulted in a very restricted perspective of a shore : the area between high- and low-water marks. As a result, shore ecology became synonymous with intertidal ecology. This was unfortunate for several reasons. First, many shores around the world do not experience significant tides and in such areas changes in air pressure will cover and uncover the shore to a far greater extent than tidal action (Fig . 6.1) . Second, the distribution and abundance of shore biota were inevitably understood in the context of tidal rise and fall, yet tides per se cannot be responsible for these patterns (Figs 6.1 and 6.2) . Third, the emphasis on tides as a controlling factor promoted the view that physical variables limited the distribution and abundance of shore organisms and thereby distracted attention away from the importance of biological processes. Fourth, the functional influence and extent of the shore may extend far into the terrestrial hinterland and down beyond the surf zone hundreds of metres offshore (Brown & McLachlan Environmental gradient

(0)

I

A

Not all shores experience significant tides, yet they support a typical 'intert idal' fauna and flora. The functional extent of the shore extends well above and well below normally recognized limits.

In this chapter, the focus is very much on rocky and sandy shores. Other kinds of shore habitats (estuary, mangrove, tropical reef) are dealt with elsewhere in this book, but given the broader network in which rocky and sandy shores operate, reference to these other systems draws attention to the important ecological linkages that exist between them. (I)

(bJ A

-~

Rolk

1990). The influence ofthe shore extends even further if a larger scale perspective is taken to include the supply oflarval stages from offshore water masses. the origins and end points of migratory taxa such as turtles and shorebirds, and the material linkages between shorelines ofdifferent types. Thus, as for other marine systems, defining 'the shore' is quite an arbitrary exercise and understanding patterns and processes within an area like the intertidal zone requires acknowledgement of a much larger scale system within which that limited area of habitat is set.

A

-~

\

~

Rock

-~

Rolk

Sea

Mean high tide

Sea

Sea ~

"-

~

\. Mean law tide

Figure 6.1 The wet-dry gradient (a) t hat characterizes the shore is set up by the interface between water and air. Waves

will extend this gradient up and down the shore (b), and tides (where present) further amplify the grad ient (e). The effect of the tide is th us to greatly expand an existing gradient, tides do not create the gradient per se.

Figure 6.2 Zonat ion patterns on contrasting shores. (a) Lichens and brown algae form distinct bands on an artificial rock wa ll at Pwllheli, North Wales, an area that experiences sign ificant tidal rise and fall of a few metres. (b) A typical shoreline in an essentially atidal area at Tjarno, Swedish west coast. (c) The angiosperms Spartina and Sa/icomia form characteristic zones at the edge of a salt marsh, Sylt, Germany.

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

6.3 Environmental gradients and the shore The shore is characterized by several environmental gradients (termed ecoelines elsewhere; e.g. Whittaker 1974) . These gradients interact and intersect in quite complex ways to generate specific environmental conditions for shore organisms. All other things being equal, specific and predictable biological assemblages will be found at the intersections of these gradients according to their physical, competitive, and physiological abilities to occupy particular sections of the gradients. a phenomenon known as zonation (Figs 6.2 and 6.3) . Different species have different physiological and ecological tolerances and hence occupy different sections of environmental gradients.

Four main gradients can be recognized on shores: wetness/dryness; exposure to wave action; substratum particle size; salinity.

6.3.1 Wetness/dryness The wetness/dryness gradient is set up at the tension between water and air. The environment becomes progressively drier with distance from the water surface and this gradient is amplified (not created) by waves and tides (Fig. 6.1) . Almost all of the plants and invertebrates encountered on rocky and sandy shores are marine aquatic in phyloSpecies A

-

Inueasingly stressful

Enviran.mental gradient

Increasingly benign-

genetic origin (Fig. 6.3), and the majority require access to the marine environment to complete their life history. Generally, species have different requirements (tolerances) and are able to live further or nearer to the water surface according to these tolerances. It does not follow that highshore organisms cannot withstand immersion in seawater: many appear to be restricted to high-shore levels because ofbiological pressures (e.g. predation or competition) from species living at lower shore levels (6.4.1 and Chapter 1). Most shore species are marine in origin and need regu lar access to the sea

6.3.2 Exposure to wave action A feature of all coastlines is that they experience wave action to varying degrees (Box 6.1) . Waves are generated by the frictional drag of wind on the sea surface: the longer the distance over which the wind blows (termed fetch), the higher the waves. Waves may also arrive on the shore in the form of swells; these are the ghosts oflarge, wind-generated waves produced by storms far offshore. The forces expended when waves arrive at the shore will depend on how much energy is extracted through friction as a result of direct contact with the immediate offshore substratum and any associated biological structures, such as kelp forests, reefs, or sandbanks. Thus, shallow sloping offshore areas will tend to dissipate the energy in the waves arriving at the shore, while steeper cliffs with deep water at their base will experience a much greater physical impact of wave action. Because waves are wind-generated, physically sheltered localities, such as fjords, narrow estuaries, and shores facing away from prevailing wind directions, will have less wave action on average. Wave action, of course, will vary daily and seasonally. Many of the anatomical and behavioural attributes of shore organisms reflect adaptations to minimize the risk of dislodgement by wave action and this allows different species to occupy different sections of the exposure gradient. Wave action is a major determinant of commun ity structure and composition , as well as individual shape, form , and behaviour.

Figure 6.3 Zonation of two species along a generalized environmental gradient running from stressful to benign conditions (with respect to the organisms). The two species A and B occupy different sections of the gradient according to their ability to tolerate physiological stress (left-hand tail of the distribution) or biotic interactions

(right-hand tail of the distribution; see also 6.4). Note that for terrestrial taxa, such as saltmarsh plants, the sea is a stressful environment, while for marine taxa, it is the land that is unfavourable.

Shore ecologists use the terms 'wave action' and 'exposure' synonymously, and the latter should not be confused with exposure to air when shores are exposed by receding tides, more properly termed 'emersion'. In addition, the concept ofexposure to wave action is difficult to apply sensibly to sandy beaches and mudflats, because of the complex interactions between particle size, beach slope, and wave energy. Sediment shore ecologists thus prefer to describe a beach as having a particular morphodynarnic state that

6.3 Environmental gradients and the shore

Box 6. 1: Wave formation Waves are generated by friction from wi nds at the air!

right seabed conditions, these coasts produce some of the best waves sought by surfers. Althoug h the surface

water interface. The length of fetch (the distance over

features of waves are clear to see, internal waves occur

which ai r moves unimpeded by a land mass) , wind speed,

beneat h the surface, which decay towards the seabed.

directio n, and duration, and the depth of water all affect the period and height of waves. Waves can conti nue

These internal waves rarely persist beyond a depth of

to be propagated even wi thout the influence of wi nd,

internal waves will create physical disturbance on the sea-

this is known as swell , which decays gradually over time

bed, which will increase with decreasi ng water depth. This

in the absence of wind. Coasts that are exposed to the ocean typically have swell with a long period. Given the

produces a gradient of wave distu rbance on the sea floor

..- .

, , -a .~

E

~

Uprush

~

Surf or breoker zone

! ....

Reformed wovei break

!

•

WOVe!; reform indeeper water

Outer lineof breckers

50 m. However, as waves pass into shallower areas, the

that decreases with distance offshore and with depth.

Wove«est

Wove«est

I

Bockwoih

\..Wove trough sutter

Ofkhore bar

occupies a point along a reflective-dissipative spectrum, rather than a wave exposure grad ient (see 6.3.5) . 'Morphodynamic state' is preferred to the term 'w ave exposure 'to describe sandy beaches and mudflats.

!stillwater level

Oceanbonom"

often too unstable to permit surface attachme nt and the fauna lives within the beach (the infauna and meiofauna; Box 6.2) , unless wave action is sufficiently low. Shores of intermediate particle size are very inhospitable for marine life because they are too unstable for surface dwellers and are comprised of particles that are too large for an infaun allifestyle (Fig. 6.4). Thus, different species are capable

6.3.3 Particle size Shores can be ordered along a particle-size gradient ranging from extremely large particles, such as a cliff or boulder beach, to those made up of very fine particles only a few microns in diameter (Fig. 6.4). Large particles provide a stable surface for attachme nt, and epifauna and flora dominate such shores. In contrast, finer particle sands are

of living in d ifferent sections of the particle size grad ient and many of them are specialized to cope w it h the unique conditions presented. The sizes of the particles that make up the shore have a huge effect in determining the kinds of organisms that can survive there.

Box 6.2: Macrofauna and meiofauna

per unit mass. This means that their energetic importance

In addition to the commonly encou ntered larger infauna

can be as high, and in many cases higher, than that of

of beaches and mudflats, such as clams, shrimps, and

the macrofauna in the beach. Meiofaunal taxa also occu r

polych aete worms, a rich variety of tiny organisms live

on rocky s hores (Hicks 198 5; Gibbons & Griffiths 1986)

on, and between, t he individual par ticles, including

in association with the microhabitats provided by large r

nematodes, harpacticoid copepods, gastrotrichs, archaic

species, but they have been less well studied than those

groups of polychaetes, kinorhynchs, and flatworms. These

in sediments. Notwi thstanding thei r small size and thei r

are grouped together as the meiofauna. Because of thei r

taxonomic and identification challenges, meiofauna are an

small size (typically less than a milli metre) these taxa are

extremely rewarding group to work with, since so little is

not familiar to most marine b iologists, let alone the non-

certai n about thei r ecology and functional importance in

expert. They occur in very large numbers, hundreds per

marine intertidal systems. For an excellent website dedi-

10 0 em" of beach, and because of thei r small individual

cated to meiofauna see: www.meiofau na.org

body size (only a few fl9) , they have high res piration rates

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

The physical refuge provided for infaunal taxa by fine particle shores brings additional challenges. Coarse (sandy) and fine (muddy) particle beaches will present very different physical and microbiological environments, mainly due to their differences in surface area available for microbial activity and their capacity to retain water at low tide (Fig. 6.5) .

6.3.4 Salinity This gradient has been largely dealt with in Chapter 5 and only a summary is provided here for completeness. The salinity gradient is generated by the meeting of fresh water

I'I _~""

and seawater and the habitat where this occurs most obviously is the estuary. Here. river water with a very low concentration of ionic salts meets marine water with very high levels of such ions. The degree of physical mixing between seawater and fresh water can range from very little. with the less dense fresh water flowing over the top of the marine water. to complete mixing, where turbulence by large waves can result in similar salinities at the water surface and the seabed. The exact nature of the mixing and hence structure of the vertical and longitudinal salinity gradient will be variable for anyone estuary. depending on the relative volumes of fresh and sea water, wind-driven physical turbulence that results in mixing of fresh and sea water and

Ihl

lei

-.

Idl

IgI ~~

lei

Ihl Epifcunc/flcrc

Epifo un9 cnd mccrophytes;

.. --

Infounc

Nc mccrobictc

;11

£fEo

Ai"

{Iilh

Laflle boulden

Small bou lden

Cobble! Shingles (ool'llllOnd

(Tens of melT1is)

(Me/res)

(Centimetres)

(Millime/res)

Fi nelll nd

", (Microns)

Figure 6.4 The environmental gradient of particle size, ranging from large rocks and cliffs to mud composed of grains

only a few microns in diameter: (a) exposed cliff (Otago Peninsula, New Zealand); (b) sheltered cliff (Little Loch Broom, Scotland); (c) boulder shore (Isle of Wight, England); (d) shingle beach (Norfolk, England); (e) sandy beach (Clacton , England); (I) mangrove (Manakau , New Zealand); (g) seagrass bed (Moray Firth, Scotland). (h) Shore organisms can only live on the sides of the larger particles (epifauna and flora), and between the particles (infauna) on sandy beaches and mudflats (except in extremely sheltered habitats where some epifauna and flora reappear). Intermediate-sized particles that make up shingle and cobble beaches present a hostile environment for both types of organism, because they are too large to retain water and too mobile for surface attachment.

6.3 Environmental gradients and the shore spring-neap tid al patterns. The distribution of t he fauna and flora along this gradient will thus represent a response to the average cond itions present. The majority of species found in estuaries are marine in origin, wit h few freshwater taxa penetrating far downstream.

6.3.5 Interactions between gradients and zonation patterns

• • •

Mud

.. o

-----

-§ -

Fine sand

All t he above grad ients interact to generate particular cond itions for life on shores. For instance, increasing wave action will amplify the wetn ess-dryness grad ient, and t hereby uplift biological zones w it h increasing wave exposure. Wave action and water movement will sort particles according to their mobility and in the process drive the overall beach environment towards a more reflective or a more d issipative morphodynamic state (Table 6 .1) . The interactions between salin ity and particle size are complex and dealt wit h in Chapter 5. The types of fauna and flora recorded at any location on a shore can be understood as the biological responses to the product of these interacting gradients, allow ing for biogeography (Chapter 1). The overall patterns of d istribution and abundance are revealed as zonation patterns, which are most obvious on exposed macro-tidal rocky shores, and least obvious in sheltered sandy fl ats. Not surprisingly, we understand much better the processes maintaining rocky shore zonation t han is the case for other shore habitats. One of the most important features of roc ky shore zon ation patterns is the similarity that occurs worldwide. These were described most elegantly by Stephe nson and Stephenson (1949, 1972 ), in a period when marine ecology was developmental and more descriptive. Similar, but not identical, types of fauna and flora occupy similar positions

Coarse sand

• -- -- -

l-

20

o Reducing

0

Oxidizing

Figure 6.5 The ave rage parti cle size t hat ma kes up sandy beac hes and mudflats has a profound effect o n

the physico-chem ical co ndit ions experienced by the infauna. Mud s have a mu ch g reater surface area available

for micro bial activity by virt ue of th eir small individual

particle s ize. They a lso reta in water better than sands and a re usual ly waterlogged. Th e mi crobial activity reduce s co mpounds, suc h as iron and sulp hate, in th e sed iment

creati ng ano xic co ndit ions the extent of which is refl ected in th e depth at which the sedi ment changes co lour from o ra ngey-brow n (oxi dize d iron particles) to dark brown o r black (reduced iron sulphi de) (see also Cha pte r 8).

Table 6 .1 So me of the features of beaches at th e ext reme ends of th e morpho dynamic spect ru m. Intermediate morphodynami c stat es have intermediate f eatures. After Raffaelli and Haw kin s (1996).

Dissipative beaches

Reflective beaches

Sediments

Fine

Coarse

Waves

Slope

Small Shallow

Large Steep

Swash conditions

Benign

Harsh

Fauna

Rich

Impoverished

(,j

Ib}r--

-

-

-

-

-

-

-

"'I

Di ssipative (a) and refl ective (b) beach es o n the Co ro mandal coast , New Zealand .

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

on shore gradients, independent of biogeographical region

structuring processes that operate on all rocky shores: only

(Fig. 6.6) . The significance of these universal features of zonation is that they imply similar and strong underlying

a limited range of body forms and phylogenies can cope with life on shores. Also, these consistencies in the major

Figure 6.6 The universal zonation

scheme proposed by Step henson and Stephenson (1972). The main zones are where biota occur worldwide, with slight modifications according to biogeography. This zonation is

well-illustrated by this rocky shore on the Otago Peninsula, New Zealand (left), or the Nort h American example (above). In the North American exam ple, Pisaster starfish can be seen

lying j ust beneath the band of black/

Supra linoral fringe

,:~....~

~IQ(k lichen and litterlnld snoil.1

blue mussels on a shore in Vancouver Island, Canada. These voracious predators limit th e lower distribution

Mid-Iinoral zone

of the mussels and actively contri bute

(barnacles, mussels)

to th e creation of d ist inct zonation patterns as d iscussed later in this

chapter. Photograph: lain McGaw.

,

...-...-...-...-:;:~~~fra-littOrOI fringe (large kelps] oo.l';

~\..""'-- -

--

--

__ -

""

~

Infro-linoral zone

6.4 Causes of zonation •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

zoning species worldwide have permitted the invention of a spatial referencing framework for the unambiguous location (within a shore) of where particular studies were undertaken (Fig. 6.6) . Thus, the term midlittoral (or eulittoral) would conjure the same mental image of a shore habitat for all rocky shore ecologists.

Dahl's scheme

Remarkably similar general patterns of zonation recur throughout the world which offers interest ing possibili-

ties to undertake comparative studies .

Similar schemes have been proposed for sandy shores (Fig. 6.7), and there is some evidence of universal zonation patterns for crustaceans (Dahl 1952). However, most general environment of the beach, rather than its biology (Salvat 1964). Figure 6.7 'Universal' zonation schemes for sandy

6.4 Causes of zonation

beaches provided by Dahl (1952) based on the occurrence of crustacean groups, and Salvat (1964) based largely on the degree to which water is retained by

Given the striking zonation patterns seen on rocky shores. and to a lesser extent on sandy shores and mudflats, it is not surprising that a major preoccupation of shore ecologists has been discovering the determinants ofzonation. Earlier workers naturally assumed that the tides must be in some way responsible. given the intimate association between the so-called intertidal area and the twice-daily rise and fall of the tides. Various schemes and theories were advanced. exemplified by the critical tidal level arguments put forward by Colman (1933), and later developed byDoty (1946) and others. It was argued that as one moved down the shore, there were certain regions where only small differences in shore level were characterized by large changes in the period of immersion. when averaged over a year. In other words. the immersion-emersion gradient was particularly steep at these points and thus critical for any species that decided to settle in these regions. Upper and lower distributional limits of several species seemed to coincide precisely with these critical levels. While plausible, indeed compelling, Underwood's (1978) re-examination of this theory revealed the basic science as thoroughly flawed. species' distributional limits occurred haphazardly along the shore rather than in groups, and re-plotting of the tidal data did not support the idea of critical levels. Nevertheless, the concept lingers on in several marine ecology textbooks. perhaps because of a reluctance to take the tides out ofintertidal ecology. Zonation patterns on shores cannot be explained by ti dal rise and fall. The concept of a critical tidal level that dictates e ntirely the patterns observed on shores still persists in some marine ecology textbooks. This is an out-dated concept and should be t reated accordingly.

the sediment.

Given that the majority of species encountered on rocky and sandy shores are marine and aquatic in origin. we should not be surprised that the upper zonal limits of a large number of species have been shown to be associated with physiological tolerance to factors such as desiccation and thermal stress. In general, experiments have shown that species found higher on the shore are more able to tolerate dryness and thermal stress than lower shore species. Many of the experiments have been focused on adult individuals, but it is often the environmental conditions experienced by the recruit (larval) stages that more importantly determine the adult distributions, especially for sessile taxa. such as barnacles and mussels. The juveniles of many mobile taxa. such as marine snails, recruit onto lower shore levels, and later migrate to higher levels as they become larger and their physiology alters such that they can cope with harsher environmental conditions. Juvenile stages of most species (terrestrial oraquatic) tend to be the mostvulnerable to stress. Upper dist ributional li mits of species are generally (but not always) set by t heir to le ra nce to physical factors.

The determinants of lower zonal limits are not easy to attribute to physical faerors. Why should aquatic organisms require a certain period of drying? Several pioneering studies (e.g. Baker 1909) demonstrated that high intertidal species actually grew better under a lower shore tidal regime, while Stephenson and Stephenson (1949) suggested that competition and/or predation might be responsible for some zonation patterns. However. it was Joseph Connell's

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

now classic experiments on the determinants of zonation patterns in the barnacles Chthamalus montagui and Semibalanus balanoides that provided the most rigorous argument for biological factors setting lower distributional limits ofshore species (Connell 1961a, 1961b) . The persua-

siveness ofthese experiments lies in the controlled manipulation (removal in this case) of one species (Semibalanus balanoides) occupying the zone immediately below another potentially competitive species (Chthamalu.s montagui). Connell was able to show that in the absence of competition for space, a limiting resource on his rocky shore, the higher shore species could survive at lower shore levels than those at which it was normally found . This manipu-

lative approach to understanding the determinants of zonation patterns has been emulated repeatedly by many workers. As a result, it is now something of a paradigm in rocky shore ecology that lower distributional limits of species occur as a result of biological factors, while physical factors set upperlimits to distributions. However, there are exceptions, especially amongst the macroalgae (Hawkins & Hartnoll1983). Thus, grazers may prevent the upshore extension of foliose seaweeds on some Australian shores (Underwood & Jernakoff 1981), red and brown seaweeds grow further upshore in the absence of limpets on the Isle of Man (Hawkins & Hartnoll 1985), and the green seaweed Codium may be partly limited by grazing from above (Ojeda & Santilices 1984). Notwithstanding these exceptions, an intriguing question posed by this paradigm is whether it is applicable to the zonation patterns that occur along other kinds of gradients, particularly the wetness-dryness gradient on sandy shores, but also to salinity, exposure, and particle size gradients in other habitats. Competition and predation have been shown to be important determinants of lower distributional limits of species on many rocky shores.

There has been very little exploration of this question for the last three environmental gradients, but some work has been done on zonation patterns on sandy shores. One of the issues for sandy shore (and mudflat) ecologists is that the description of zonation patterns in these habi-

tats requires the destruction of the medium in which the organisms live: quantitative sampling involves digging out volumes of sediment and separating the fauna, usually by sieving or elutriation. Nevertheless, this approach reveals zonation patterns that are usually not visible at the sediment surface (Fig. 6.8) . Zonation patterns, as well as their underlying causes, are much harder to detect on sandy beaches and mudflats.

Marine ecologists have sought to understand the role of individual species within sediment communities by systematicallyremoving particular species and studying the consequences. Carrying out such species removal experiments in sandy beaches or mudflats is fraught with interpretational problems if the habitat has to be disrupted to such a severe extent. Just think how difficult it would be to remove 10 individuals of one species from a patch of sandy beach that contains 100 individuals comprising 20 species. A second problem arises in that, unlike the sessile fauna of rocky shores, the infauna is mobile and can easily move back into areas cleared in manipulative experiments. In other words, it is difficult to maintain the integrity of the experimental design ofspecies removal experiments (but see Techniques box) . Third, the beach fauna lives in a three-dimensional environment and displays zonation verticallyas well as horizontally, and some species redistribute themselves at each high tide. Experiments aimed at removing potential competitors therefore have an additional layer of complexity. Fourth, it is not clear whether space is a limiting resource for which competition occurs in sandy beaches and mudflats, in the same way that it does on rocky shores. Certainly, the intensive interference competition, where individuals overgrowor crush one another, that is seen between spaceoccupying species on rocky shores is virtually absent in sediment assemblages, probably because individuals tend to be mobile (as opposed to the many attached biota found on rocky shores) and can simplymove awayfrom one another. Space is not such a severe constraint on sandy shores as the fauna are mobile and can relocate to avoid competition.

EHWI ~-~------;'::~: Figure 6.8 Zonation on a sandy beach , Newburgh,

Scotland. Only the most abundant species are

----""

ElWI

represented for the sake of clarity. Data from Raffaelli et al. (1991).

6.5 The organization of shore communities Despite these issues, several investigations have demonstrated the importance of physical factors in setting upper distributional limits, such as Petersen and Black's (1987, 1988) transplant experiments of the bivalves (Circe and Placamen ) to higher shore levels, where they grew more slowly and suffe red higher mo rtality due to physical facto rs. The importance of biological factors in setting distributionallimits is illustrated by Posey's (1986) study of a Californian beach. Here, the burrowing activities of the ghost shrimp Ca llianassa excluded a tube-dwelling worm Phoronopsis from higher shore levels, while the lower distributionallimits of the shrimp were probably set by predation by a fish, the sculpin Leptocottus. Such manipulative studies are few and far between and, as in the case of Posey's study, both upper zonal limits may be set by biological interactions. Clearly, the factors responsible for zonation in a three-dimensional habitat, such as a sandy beach, are not as clear as for two-dimensional rocky shores.

6.5 The organization of shore communities In common w ith all other biological assemblages, shore communities are organized by a combination of top-down (consumer-driven) and bottom-up (resource-driven) processes. Many of the classic studies on top-down processes in food webs were first performed on rocky shores . Consequently, there has been a tendency to generalize these results across all shores and even across all types of ecosystem. Notwithstanding the fact that some of these earlier studies would be unlikely to pass the present-day peer-review process (Box 6.3), they have made a major contribution to mainstream ecological theory. Before we discuss the relative importance of different processes in the dynamics of shore assemblages, it is worth rehearsing the features of shores that make them so amenable to studying these kinds of questions.

6.5.1 The role of field experiments Of all the arguments that can be used to convince scientists that a particular viewpoint is correct, the experimental falsification of hypotheses has proven the most persuasive (i.e. the rejection of the null hypothesis). Field experiments h ave to be properly designed and analysed so that there is no ambiguity in their outcome (Underwood 1981 , 1997; Hurlbert 1984, Huston 1997) . An important aspect of their design is that the experimental plots (areas wit hin which the manipulation occurs) need to be replicated many times and dispersed appropriately over the study area (see Chapter 15 ). This is often very difficult to achieve for many types of taxa and ecosystem (Raffaelli & Moller 2000) , but not for shores . The small body size, high dens ities, and smallscale nature of spatial patterns of shore species means that

Box 6.3: Manipulative field experiments The most convincing manipulative field experime nts are those in which the treatme nt and control plots are highly replicated to provide the necessary statistical power to detect an effect of a particular manipulation. Such powerful designs will convince the most critical reviewer or edi tor (see Chapter 15) . It is therefore somewhat ironic that the two rocky shore experiments that ecologists are completely persuaded by are fatally

flawed in this respect. The first is Lodge's (1948) removal of the limpet Patella from a wide strip running down a shore on the Isle of Man, UK, and the subsequent bloom of algae in the manipulated area. The second is Paine's (1974) set of experime nts on

Pisaster on the Washington coast, where removal of the starfish saw a massive increase in mussels and a collapse in community structure (Fig. 6.9). Neither study used a properly replicated experimental design, and there were essen tially no controls (Raffaelli & Moller 2000). Yet the scientific commu nity is persuaded by these experime nts that Patella and Pisaster are keystone species. Why? Because (a) the effects were so dramatic, and (b) the resultan t changes in abundance and distribu tion of algae and mussels were completely outside the 'norm ' for similar rocky shore commu nities. However, Lodge and Paine were lucky to get away wi th it: the effects of predator removals are often much more subtle and a proper experimental design is advised to all would-be manipulators! For fu rther discussion, see Raffaell i and Moller

(2000).

many relative ly small plots can be located w ithin a small spati al exte nt. The three-dimensional variation w it hin shore sed iments is usually compressed into a layer no more than 20 em deep. In addition, processes of interest tend to operate over relatively short ecological time-scales (weeks to years), allowing them to be investigated wit hin the traditional 3- to 5-year research grant period. Finally, of course, shores are highly accessible and en able sampling to occur with high precision; you can be sure that you collected your samples from w ithin the experimental plot you intended to sample. These features mean that it is much easier to investigate certain types of processes on shores compared to other habitats, such as forests or the deep sea. The outcome of experimental manipulations of shore communities are only persuasive if executed correctly and unambiguously.

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

However, while sh ores are highly amenable to the experimental manipulative approach, not all questions can be satisfactorily addressed in this way, especially those questions concerned with processes that operate over large spatial and long temporal scales (Raffaelli & Moller 2000) . Seductive as they are, field experiments are not the answer to every problem, although they are a powerful investigative tool. Despite the experimental design issues that surround some of the earlier field experiments (Box 6.3), there is no doubt that top-down processes are of prime importance on some kinds of shore. Experiments involving the removal of suspected key consumers. such as predatory starfish. or whelks. and herbivorous sea urchins or limpets, have often revealed strong competitive interactions between species whose populations are regulated by the available spatial re source (e .g, the availability of rock surface forthe settlement of barnacles) . Often a competitive dominant emerges in the absence of the consumer, with a resulting loss of inferior competitors and a lower overall community biodiversity (Fig . 6 .9) . While such experiments are dramatically effective in demonstrating the importance of top-down control by what have become termed keystone predators, their outcomes need to be placed in context (Pace et at. 1999) .

6.5.2 Keystone predator or prey? The keystone status of starfish, such as PiseLSter (Fig. 6.9), or limpets, such as Patella, is not due to any inherent attributes of these species. Their status depends entirely on the response of their prey resource to reduced consumption, and in that sense the actual identity of the consumer is irrelevant. In other words, the factors that drive the competitive dynamics of the prey should be the focus of investigation. For instance, while Pisaster has been shown to be a keystone predator on exposed coastlines along the northwestern USA, on other shores this is not the case. Similarly, the whelk Morula has an organizing role on some shores in New South Wales, Australia, but not on all shores (Fairweather & Underwood 1991) . A keystone species may simply be another 'brick in the wall' in different circumstances. In other words, the iden-

tity of keystone species can be highly context specific. One factor that determines whether a 'keystone effect' will be seen in the relatively simple communities of temperate systems (see below) is the recruitment dynamics of the dominant prey. This realization has led to the development of an extremely important, but at the same time incredibly

Keystone predator

Superior prey

Spedes-rlth assemblage

Slkhcster, New Zealand

Plscster, USA

, - - - - - - --, : Keystone : : predator :

20

15

~------- ~

,, , , , '- , ,

, ,, ,, , ,

10

L __ I

Superior

Spedes-pcor

prey

assemblage 5'-

Starfish present

-'

Starfish removed

0'-

Starfish present

-'

Starfish removed

Figure 6.9 The role of keystone predators in maintaining species' richness. Left top: a strong controlling interaction between a competitively superior prey and its predator permits the coexistence of an associated module of other species. Left bottom: breaking the link releases the superior prey, which monopolizes the resources on which the modu le species depend (after Paine 1980). On the right are examples of how species' richness is reduced in the absence of

keystone starfish in the US and New Zealand (after Raffaelli and Hawkins 1996).

6.5 The organization of shore communities •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

challenging, area of shore ecology known as supply-side ecology (Gaines & Roughgarden 1985; Gaines et al. 1985; Lewin 1986) . The significance of this area is best demonstrated by considering the dynamics of species with off-

shore early life-history stages, such as barnacles. mussels, and algae. Recruitment of these taxa usually occurs every year, but it is the strength of a particular year's cohort of recruits that will determine the outcome ofcompetition and hence community organization on the shore. Heavy recruitment by the dominant competitor will. in the absence of

a consumer. lead to the exclusion of inferior competitors. However. if recruitment of the dominant competitor is poor. other species will not decline in the absence of the so-called keystone predator. These processes are also critical determinants of the likelihood of the successful colonization of species that have been introduced into new ecosystems through human activities. Population recruitment processes operating far out at sea may profoundly affect the outcome of interactions on the shore, especially for those species that have offshore dispersed larvae.

The central question for understanding the dynamics of these communities is therefore 'what determines recruitment strength?'. The answer rests in the ocean climate determinants of the offshore currents that carry the larvae or spores to the shore. If there are plenty of larvae in the currents and if these sweep the shore at the right time. then recruitment will be strong. In this respect it is unfortunate that there has been an emphasis on the keystone nature of the consumer, because the dynamics of these shores may in fact be driven by events hundreds of kilometres offshore. If this larger-scale perspective is taken, it could be argued that bottom-up, not top-down processes organize the shore. Finally. in shore communities with a more complex set of predators. such as those found on many tropical shores (Menge & Lubchenco 1981 ; Menge et al. 1985) and in temperate estuaries and mudflats (Reise 1985; Raffaelli & Hall 1992), the removal of anyone predator does not usually lead to the kinds of cascading effects documented for some temperate rocky shores. since the remaining species simply mop up any released prey resource. This effect is known as diffuse predation (Hixon 1991) . Keystone predators are not therefore a characteristic of such shores.

6.5.3 Primary and secondary space Top-down effects on shores are most obvious between consumers and those prey species that are primary spacelimited. That is, they compete aggressively for the rock surface. Such taxa include truly sessile groups, such as algae. barnacles. oysters, and sponges, as well as semisessile taxa. such as mussels. Interactions between these

taxa are typically of the interference type. including overgrowth, crushing, smothering, and chemical warfare (algal and sponge allelochemicals) . Taxa that are not sessile can move away from such interference competition, which explains why competitive exclusion, and hence keystone effects. are harder to demonstrate in the mobile species found in sandy shores and mudflats, as well as for rocky shore gastropods and amphipods. Thus, by keeping mussel densities low. Pisaster is partly responsible for maintaining a high diversity of primary-space occupiers. but reduces biodiversity overall by reducing the habitat available for those secondary-space occupiers living in the highly complex mussel matrix. a system ofextremely high biodiversity on rocky shores (Suchanek 1992) . The structure created by beds of primary-space occupiers, such as mussels and oysters, permits a high local biodiversity of associated fauna to develop due to increased habitat complexity and organic enrichment from the production of faeces and pseudofaeces.

6.5.4 Bottom-up processes Despite a great deal of effort, much of it involving manipulative field experiments. it has been hard to demonstrate consistently an important role for top-down processes for sandy beach and mudflat communities (Raffaelli & Hawkins 1996) . These systems often support a much larger range ofconsumers. including shorebirds. crustaceans. and fish, which occur in large numbers and have high energy demands (Table 6.2; Chapter 5) . One might therefore expect top-down control in such systems, but this has been difficult to demonstrate experimentally. There are a number of faerors that might be involved: low natural predator densities, poor experimental design. prey movement in and out of cages, inappropriately sized cages, insufficient time duration for the experiment, and, finally. a real absence of top-down control (see Techniques box) . There is no doubt that many experiments that have attempted to discern the importance of predation in these systems suffer from experimental design problems (Raffaelli & Moller 2000) . Experiments in these habitats are typically short-term (weeks to months) and may be too short to reveal anything but the initial, transient dynamics. which mayor may not be the same as the longer term behaviour of the system. This is important given that the effects ofcompetitive interactions, e .g. for food resources, among prey species are likely to be subtle and long-term. The outcome of competitive interactions between mobile species may be much less dramatic than for sessile taxa because mobile taxa can move to avoid competition.

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Table 6 .2 Exampl es of high co nsumpt ion rates by shoreb irds feedin g on (a) macro phyte stand ing cro p, and

(b) invertebrate produ cti on . Data from Thayer et al. (1984) and 8aird et al. (1985), respectively.

"!o

Prey

Consumed)

Prey

(a) Macrophytes

"!o

Consumed)

(b) Invertebrates

Zostera

30-75 20 13

Ruppia

Potamogeton

Ythan estuary

36

Tees estuary

44

Langebaan lagoon

20

(a) Seagrass bed Moray Firth, Scotland; (b) wading birds that are typical invetebrate feeders.

(, j

-

•

.. ..

'-

Ib)

•

TECHNIQUES: Experimental approaches to understand species interactions in soft shores

The essence of any experimental approach towards understanding the ecological significance of species' interactions is that if two species perform equally well when they are together and when they are not together, then

The techniques and approaches for sampling and map-

there can be no significant interaction between them. Con-

ping the distribution and abundance of shore species and

versely, if thei r performance is different in the two situ-

relevant environmental variables are well-documented, but

ations, then they must interact in some way. Setting up

there are few guides to help those who wish to explore

experiments w here particular species are either present or

dynamic interactions between species, especially for soft

absent requires creative methodologies, especially in the

shores. Here, we describe a case study focused on explor-

case of field experiments where the intervention technique

ing the interactions between species ranging from shore-

may itself produce so-called 'hidden treatment effects'

birds to small invertebrates, on tidal flats in north-east

(Huston 1997). Below are some ways in which experi-

Scotland, and which comprise the Ythan food web.

ments were carried out on Ythan species, in the field and

The Ythan food web is relat ively simple, comprising only

the laboratory, in order to identify important interactions.

c.100 macro-species, but an unknown number of meio-

Carryi ng out experimental manipulations like the ones

faunal and microbial taxa. The trophic interactions between

described above is not for the faint-hearted. A major

these species are well-documented (e.g. Hall and Raffa-

advantage of the Ythan is its sheltered nature (we never

elli 199 1; Gorman and Raffaelli 2003), but the dynamic

lost any experiments due to scouring or to cages being

importance of those interactions, and their consequences

washed away by storms, unlike our experience in other

for system structure and function, had not been explored

more exposed locations). This is important because such

using experimental manipulations of the ki nd pioneered

experiments often have to run for a co nsiderable time

by rocky shore ecologists. Partly, this was because such

(many months). The naturally muddy nature of the site

experiments were thought to be too difficult, and indeed

meant th at increased siltation inside fine meshed cages

they can be. However, the Ythan team persevered and their

was rarely sig nificant. Also, the site is a nature reserve,

approaches and the lessons learned may be useful for oth-

minimizing chances of vandalism, and the team were based

ers embarking on such experiments, including questions of

on-si te at Culterty Field Station, only a few hundred metres

how biodiversity is related to ecosystem functioning (see

from the experimental sites. Of course, experiments alone

Current Focus box).

are not sufficient to fully elucidate all the interactions: we

6.5 The organization of shore communities

spent a great deal of time doing more empirical natural histo ry in order to help us interpret the results and to check

face, including the fish, so we could be sure that predators

the integrity of the treatments (many of these species

you decide to embark on such experiments, you will need

leave recognizable tracks and signs on the sediment sur-

nerves of steel, but the final product is well worth it!

Taxa manipulated

Response

we re really present or absent in the different treatments) . If

Technique

Issues

Reference

taxa

and roofed with thin, horizontal

No sedimentation effects (cage Raffaelli & Milne 'mesh' is coarse and does not 1987

strings, that let fish and

slow water flow ) . Strings may

epibenthic predators in, but

get fouled by drifting algae

excluded birds.

and need to be kept clean

Shorebirds

Benthic infauna Large (me-scale] plots fenced

(Redshank

(amphipads,

(Tringa polychaetes. totanus) , Dunlin oligochaetes, (Calidru5 snails) alpina) , Shelduck

regularly.

(Tadorna

.. ~c:~~~~~)

.

Eider ducks

Mussels

Eiders feed by diving onto

Because there are no sides

Raffaelli et al

(Somateria

and their associated

intertidal beds of mussels when they are covered by the

to the cages, water flows are natural, but there may be

1990

invertebrate

tide. They can be excluded

significant shading effects on

community

by a simple coarse-mesh roof

microbial communities within

suspended on stakes within

plots (needs to be explored)

mollissima )

large (m--scele) plots. Other species, some birds and all fish and epibenthic predators have access to mussels. Ad ult flatfish

Benthic infauna Large (me-scale) plots fenced

Fouling of cages by drift algae

Raffaelli & Milne

(PJatichthys

(amphipads,

and roofed with coarse mesh

can reduce flow s and lead to

1987

ffesus)

polychaetes,

(several em) exclude flounders.

build up of sediment inside

oligochaetes,

cages, so they need to be

snails)

checked and cleaned reg ularly. Exclosures like this exclude all other large predators and have to be used in conjunction with the designs described above to interpret results.

• • • • • • • • • • • • • • • • • • • • • • • ••••••••••••••••••• ••• ••••• •••••• ••• ••• ••• •••••••••••••• ••• •••• ••• •••• ••• •••• ••• •••• ••• •••• ••••••••••••• •• •• ••••••••••• Jaquet and The relatively small mesh is Small fis h Benthic infauna Large (c. 1 m 2 ) enclosures with

(gabies

(amphipads,

an intermediate mesh ( 1-2

likely to red uce flows and lead

Pomatoschistus

polychaetes,

cm) to enclose predators. If the

to higher levels of suspended

spp) and j uvenile flatfish

oligochaetes, snails)

substratum is prone to drying out at low tide, then a short

material (sediment and perhaps invertebrates) inside

(PJatichthys

2 -3-cm wall may be needed

the enclosure. However,

ffesus)

around the inside of the cages

because comparisons of

to retain sufficient water.

response fauna are made

Also, solid barriers should

betwee n cages with fish

be inserted inside the cages

at natural densities and

and pushed in flush with the sediment surface to ensure that

cages without fis h, then any difference between the

enclosed fish (and invertebrate

treatments cannot be d ue to a 'hidden treatment'.

prey) cannot bury out of the

Raffaelli 1989

caged area. • • • • • • • • • • • • • • • • • • • • • • • ••••••••••••••••••• ••••••••••••••••• ••• ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •••••••••••••

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Taxa

Response

manipulated

taxa

Epibenthic crustaceans

(brown shrimp

Crangon crangon and the shore crab Carcinus maenas)

•

Technique

Benthic infauna Relatively small (0.25 m 2 ) (amphipods, enclosures with a small mesh polychaetes, (a few mm, depend ing on the size of the predators) oligochaetes, snails) to enclose predators. If the substratum is prone to drying out at low ti de, then a short 2-3-cm w all may be needed around the inside of the cages to retain sufficient wate r, although crabs and shrimps are usually good at 'digging in' as the ti de recedes. Solid barriers should be inse rted inside the cages and pushed in flush with the sediment surface to ensu re that enclosed shrim ps and crabs (and invertebrate prey) cannot bu rrow out of the caged area.

Issues

The small mesh can be expected to reduce flow s

Reference

Raffaelli et al. 19 8 9

and lead to higher levels of suspended mate rial inside the enclosure. However, because comparisons of response fauna are made between cages with shrimps/crabs at natural densities and cages without shrimp/crabs, then any difference between the treatments cannot be due to a 'hidden treatment'.

• • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

Invertebrate s (ragworm Hediste

Solid walled. box cages c.20 and meiofauna. x 20cm, roofed with fine mesh (500!J m or less) . Cage

Small infauna

diversicolor,

pushed in almost flush with

amphipod

sediment. Solid sides prevent

Corophium

movement in and out of cages

volutator)

of manipulated species and of

As above.

Raffaelli and

Hall 19 9 5; Lim ia and Raffaelli 19 9 7

response species. • • • • • • • • • • • • • • • • • • • • • • • •• • • • • ••• • • • •• •• •• • • • •• •• • •• • •• • •• • •• • • • ••• • •• • • • • • • • • • •• • • • • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • •• • •• • • ••• • • • •• •• •• •• • • • • • •• •

Mussels (Mytilus edulis)

Epifauna, infauna, and meiofauna

Sheets (0.25 m 2 ) of mussels removed from within mussel beds, rinsed to remove any associated sediment and inverteb rates and re-Iaid on bare ti dal flats. Sheets secured by pegs until firmly attached to sediment surface.

Tube worms

Infauna and

(Lanice

meiofauna

conchilega)

Ar tificial tu be fields (0.25 m 2 plots) created with drinking straws of a similar diameter and shape to Lanice tubes.

Sheets should be kept as intact as possible (not alw ays easy) . Since the effects of mussels are likely to be via increased deposition of fine sediment thro ugh red uced flows and mussel pseudofaeces, this 'hidden treatment' is not a problem for interpretation.

Ragnarsson and

Raffaelli 19 9 9

Ragnarsson and The density and protru d ing height of tubes is expected to Raffaell i 2000 have an impact on sediment deposition / erosion rate s. Tops of tubes act as attachment sites for filamentous algae, w hich may be an effect of interest or an unwanted 'hidden treatment'. Assembling large numbers of tubes (typically several thousand for an experiment) is not the most exciting job.

6.5 The organization of shore communities

Taxa

Response

manipulated

taxa

Lugworms

Infauna and

(Arenicola

meiofauna

marina)

Technique

Lugworms added to plots (c. < 1 m 2 ) of defaunted sediment, other plots left as controls. All sediment caged below surface with fine mesh.

Issues

All treatments start with defaunated sediment, w hich is difficult to establish and

Reference

Ragnarsson and

Raffaelli 2000

manouver in large quantities. Because all plots are similarly defau nated , any difference between treatments must

be due to the presence of lugworms. • •••••• ••••• ••••• ••••• ••••••••••••••••••••••••••••••••••• ••• •••••••••••••••••••••• • •••• ••••••• ••••••• ••••••• ••••••• ••••• • • • • • • • • • • • • • •• •• • • • • •

Weed

Infauna and

Sheets of algae secured to

With large plot sizes of several

mats (Ulva

meiofauna

mud flat to produce plot sizes of

m 2 , coverage becomes uneven

0.25 to 5 m"

and patchy.

intestinalis)

Hull 198 7; Raffaelli et al. 19 98

Manipulative field experiments on the Ythan estuary, Aberdeenshire. Top left: flounder-exclusion cages. Top right: cages with different densities of gobiid fish . Centre: a cage for maintaining different densities of small crustacean predators (note barriers that prevent escape from the caged area once the cage is sunk into the mudflat). Bottom: tracks left by flounders (left) and shorebirds (right) provide evidence that the cages work (or don 't) at excluding the right predator and that control (uncaged) plots are visited by predators.

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Notwithstanding the above criticisms of manipulative field

experiments in sediment systems, it would seem that bottom-up processes dominate, with predators limited by their prey. rather than vice versa. Many prey individuals remain inaccessible to predators, living out of reach for much of the time within the sediment and only a proportion of the prey standing stock (as opposed to production) may be predated. The dominance of bottom-up processes is perhaps not surprising given that sandy shores and mudflats tend to be net importers of organic matter from elsewhere; for example, upstream and along the coast in the case of estuaries, and from kelp beds in the case of many exposed sandy beaches. Most prey ind ivid uals in mudflats and beaches are unavailable (Le. buried to deep in the mud) to predators like shorebirds and fish , and their numbers are driven by the supply of organic matter and ot her food resources.

6.5.5 Disturbance and bioturbation A feature of sediment systems. whether intertidal. sublittoral or deep sea. is physical disturbance to the structure of the sediment and alteration of the physico-chemical environment by the organisms themselves or external events such as storms and ice-scour. Species living within the sediment move through it. ingest and egest particles. and draw oxygen-rich water down from the surface to depth (Rhoads 1974) . This local-scale biological disturbance (bio turb a tion) can change the environment for other species. for

instance by loosening and destabilizing the sediment fabric and making it more vulnerable to erosion by water movement. Alternatively. species that pump oxygenated water through burrows create a more favourable environment for other species (Fig. 6.10; Box 6.4; Chapter 8) . In addition to changing the local environment for associated species, bioturbation will also alter the flux of nutrients between the sediment and the overlying water and in this respect the biodiversity of intertidal flats may have an overall impact on ecosystem functioning. an emerging hot topic in ecology (Curent Focus) . Many epibenthic predators, including flatfish, crabs, and shorebirds, disturb the sediment surface intensely during their feeding activities (Hall et al. 1993) . While the resultant pits and surface features created tend to fill in with fine material and perhaps detritus. on most beaches the local effects are quickly erased by bedload transport (Fig. 6.10) . Of course, not all interactions can be classified as top-down or bottom-up: many are mutualistic or facilitatory, as in other kinds of ecosystem and these are reviewed in Box 6.4. In summary, the picture that emerges from evaluations of top-down and bottom-up processes on shores is that a mixture of both is always present to differing degrees and this mixture will vary with the relative strength of consumer and resource recruitment. as well as the influence of wider-scale processes, such as ocean currents and catchment run-off. The latter is a particularly important concept in the emerging field of coastal zone management in which the interactions between land and the adjacent marine areas are of fundamental importance.

Figure 6.10 (a) Effect of bioturbation by burrowing ghost shrimp Callianassa, (Manakau, New Zealand), which piles up a large growing mound (seen here in section) by ejecting processed sediment through the top of its burrow entrance (Tamaki & Flach 2000 ). Note the oxygenated burrow walls caused by the animal pumping water from the surface

(shown as light brown sediment lining burrow). (b) A depression or pit made by an eagle ray feeding at the sediment surface on small bivalves (Manakau , New Zealand). Such pits form significant structures on intertidal flats (Thrush et al.

1991).

6.5 The organization of shore communities

Box.6.4: Facilitation in marine communities

does not have a negat ive effect on any of the other species involved (i.e. commensalism and mutual ism) (Bron-

stein 19 9 4 ) . Facilitation includes all forms of positive Organisms that live w ithin an assemb lage are intercon-

interacti on, from 'tightly coevolved, mutua lly obligate rela-

nected through a co mplex series of interacti ons (Grimm

t ionships to loosely facultative relationships' (Stachowicz

199 5) that can be either neutral, positive, or negat ive,

20 01). Facilitation can affect marine systems at all levels

depending on the organisms involved. Organi sms exhibit

of organizat ion, from ind ividual organisms (e.g. specif ic

a range of interact ions wi t h different co mpo nents of their

Symbiodiniu m spp. end osymbiont dinoflagellates in cor-

commun ity such that a predator of one species may be

als; Lajeunesse et at. 20 03) to the formation of large biogen ic structures by foundation species that facilitate

the prey of another (e.g. Travis et al. 2006). A recently emerging area of interest is that of the 'facil-

wh ole biotopes (e.g. horse mussel reefs or maerl beds;

itator', a phrase more often associated w ith corporate

see Chapter 8). Further examples of facilitation at differ-

business events! Interspecific facil itation is any interaction

ent levels of organization within communit ies are given in

that has a positive effect on one of the species, but that

the table below.

Table Modes of facilitation in the marine benthos. These broad mechanisms of facilitation are common to all biomes.

Mechanism

Notes

Habitat creation Habitats may be created by a singl e foundation species or a guild of speci es

•

Examples Reef-buil ding corals 1

Increases general habitat heterogeneity

Oysters and mussels-

Provides a suriace for attachment

Seagrass beds"

Provision of a

Transform ing a two-dimensional structure into a th ree-dimensional structure

Reef-buil ding corals 1

refuge

provides an environment wh ere prey is able to shelter from potential predators

Oysters and mussels-

Relic structures remain ing once species are dead can facilitate long after

Seagrass beds"

organisms are gone (Aronson and Precht 2001; Munksby et at. 2002)

Polychaete worms"

••• •••• ••••••• ••••••••••• ••• •••• ••••••• ••• ••••••• •••• ••• ••••••• ••••••• ••••••• ••••••• ••••••• ••• •••• ••• •••• • •• ••• ••• ••• ••• ••• ••• ••• ••• ••• ••• •••

Hydrodynamic

Decreases flow velocity and increases sedimentation (Luckenbach 198 6)

Reef-buil ding corals 1

modification

Facilitates by increasing sed iment stability (Bruno and Kennedy 2000) ,

Oysters and mussels-

improving food delivery (Worcester 199 5; Shashar et al. 1996) , and by

Seagrass beds"

increasing pro pagul e retention (Eckman 198 3; Bruno 2000)

Polychaete worms"

Amelioration

Intertidal organisms retain mo isture at low tide, shade substrate and provide

Fucoid alqae''

of desiccation

moisture for associated species (Thompson et al. 199 6; Bertness et al.

stress

19 99b ) Allows species to exte nd their realized niche (Bertn ess et at. 19 99 b)

•

• •• •••• ••• • • •• •••• ••• •• •• ••• •••• •• • •••• ••• • ••• • • • •••• • •• ••• • ••• ••• • • •• •• • • ••• •• • •••• •• • • ••• •• • •••• • •• ••• • • •• ••• • •• • •• • •• ••• • •• •• • ••• ••• • •• • • •

Amelioration of

Through bioturbation and bioirrigat ion, organisms cause th e oxic-anox ic

Luqworrns''

anoxic stress

chernocllne to move dow nwards in sediment th us facilitating by reducing

Ghost shrimps?

anoxic stress

Stingray"

Commonly caused by bioturbating and bioirrigat ing infauna (Pearson 2001 ; Rosenberg 2001 ; Meysman et at. 2006)

· Enhanced

Increases the supply or retent ion of agents of reproduction

. Reef-buil ding corals 1

pro pagule

Oysters and mussels-

retention

Seagrass beds" Polychaete worms"

Kelp" ' Luckhurst and Luckhurst 19 78 ; Jones and Syms 19 9 8; Syms and Jones 2000. 2004; 2Tolley and Volety 2005; "Dean et at. 2000; Lee and Berejikian 2009; "Schwindt and Iribarne 2000; Dame et at. 2001; Schwindt et at. z ooa a, 2004b; sKappner et al. 2000; 6Reise 19 8 1a, 198 1b; Reise and Volkenborn 2004; Vo lkenborn and Reise 2007; Volkenborn et al. 2007, 2009; "Ber kenbusch et al. 2000. 2007; "v alentine et al. 1994; " Estes and Palm isan 1974, Carr 1989.

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

6.6 The shore network The previous section has stressed both the openness and connectivity of shores. Ecologists are usually required to delimit spatially (and temporally) their study areas in order to m ake sense of the complexity present, but the linear continuity of the coastline and its openness to the ocean necessitates a broader perspective if one is to truly understand how shores work. While conceptualizing a particular shore as a part of a larger network is relati vely straightforward, quantifying those linkages will be a d aunting t ask and one that is best suited to modelling as opposed to empirical approaches . However, there are a number of general features that can be described empirically. Shores are highly open systems, receiving and exchang-

Coastal water movements have an incredibly significant impact upon the change and pattern in shore organ isms, and are responsible for the transport of inorganic nutrients, organic m aterial, sediment and its associated infauna, larvae, and spores within the water column, as well as smalle r fish and crustacean consumers . Often, m ajor shifts in com munity structure and composition on the shore can only be satis factorily explained by cons idering near-coast hydrodynamics. The irony is that m any shore ecologists are not trained in this a rea and that mainstream ecologists seeking to use the shore as a convenient laboratory for testing theory m ay not be aware of the importance of water movement. Our understanding of suc h physical processes is further hampered by the paucity of data routinely collected. Clearly, this is an aspect of shore ecology in need of urgent support and development.

ing resources and propagules with each other and with offshore systems.

CURRENT FOCUS: Biodiversity and ecosystem functioning-how many species does a shore need?

primary producti on, but mari ne intertidal systems have

The past 10-1 5 years have seen an explosion in research

increasingly played a part in unravelling these relati on-

focused on the relat ionship between biodiversity and eco-

ships and the mechan isms behind them (Bulling et al.

system functioning in an attempt to describe the relation-

20 0 6 ). This is partly because shores provide ideal experi -

ships between the number of different kinds of organ ism

mental systems (t his chapter) for exploring and test ing

in an ecosystem and the rates of ecosystem processes

mainstream ecological theory, but also because they are

(figure a) that underpin the serv ices that provid e benefi ts

rep resentat ive of a system that covers c.80% of the

to society (Balvanera et al. 2006 ) . The qu estion is an

planet surface: the sea bed , characterized by small inver-

important one given the signif icant species losses from

tebrates that go about their business w ithin and on the

ecosystems as a result of anthropoge nic act ivities: are

sediment and in doing so may govern the biogeochemi cal

there crit ical numbers and kind s of species needed to

fluxes at the sediment-water interface.

sustain particular processes?

Much of the earlier research in this area was dominated by terre strial ecologists working on plant biodiversity and

Much of the work to date in th is area has involved maintaining different co mb inations of species, levels of species' richness and biomasses in high ly controll ed micro- or meso-cosm facilities, rather than in situ on the tidal flat or beach. This is be cause for sediment habitats it is d ifficult to manipu late infaunal species' richness in the fie ld w ithout disrupting the sediment habitat and inc urri ng 'hidden treatment effects' (Huston 19 97) , although some have in

fact achieved this (e.g. Bolam et al. 2002). Meso-cosms oft en emp loy defaunated sedi ment to w hich species are then carefully added in order to ensure the treatments are correct. This allow s a high degree of experimental cont rol Biodiversity

so that the effects of biodiversity on, for instance ammonium fluxes, can be unequivocally interpreted (Bulling et

Fig a. Possible relati onships between biodiversity and

al 2006). Whilst this approach is good for experimental

ecosystem processes (function s). The three different

design considerat ions, it lacks the realism of the fie ld sit u-

models, cu rvilinear, linear, and random , describe the

ation and is be st suited for understanding and expl oring

different impacts of species loss on ecosystem process

mechan isms and relationships, rath er than provi d ing true

rates (after Raffaelli 2010).

estimates of fluxes under d ifferent diversity scenari os. In

6.6 The shore network

40

our own experiments in this area, it is clear that the

Nereisdiversicofor

biot urbatory behaviou rs of different species can have a large effect on nutrients leaving the sediment-water

Corophium va/uta/or

interface. Large, mobile burrowers such as the polychaete Hediste diversicofor have a much greater impact

Hydrobia ufvae

than the surficial ploughing snail Hydrobia ufvae (figure b). It is clear that the number of species is less important than species ' identity. This is confirmed by studies

4

on functionally similar and dissimilar species on South

biomass (g wet weight)

B

Australian sandflats: nutrient release rates are higher when several different functional types are represented

40 Boston Bay, South Australia

-~ 30

than when all the species are of the same functional type (figure b).

-

' Raffaelli (2010).

o without flow o withflow +

+

+

+ Fig c Effect of flow (shaded bars) vs. static (clear bars) mesocosm conditions on the release of ammonium

o

100

200

ammonia ±I s.e. (1-1 mol /litre)

300

400

from sediments by three species of interdrial inverte-

brates. Modified from Biles et al. (2003).

Chapter 6 Rocky and Sandy Shores •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Often , major shifts in community st ructure and composition on the shore can only be satisfactorily exp lained

by

considering near coast hydrodynamic processes.

In addition to the physical transport ofliving and non-living material on- and offshore, and between different shore types. larger organisms can make purposeful migrations. These include larger fish, reptiles, birds, and mammals, which undertake such journeys for breeding, feeding, otto find a refuge from bad weather or predators. Their use of the shore can be considerable. especially for warm-bloodied taxa with high energy demands, such as shorebirds and marine mammals (Table 6.2), although, as argued in 6.5.5, cascading effects on the community are rarely detectable.

greatly on beach dynamics. For sandy shores, ASLR may increase erosion, create a steeper beach profile and increase turbidity (Goss-Custard et aI. 1990). With less organic matter retained in the beach, there will be a lower biomass of infauna. These problems will be exacerbated ifbeaches are protected by hard engineering, as the available beach area will be progressively sandwiched between a rising sea-level and an immovable structure. the so-called coastal squeeze. The net result of sea-level rise for many soft shores will therefore be a smaller, less productive beach (Fuji & Raffaelli 2008), although other scenarios are possible, depending on sedimentation patterns and the relative rise of the sea and land (Beukema 2002; Goss-Custard et aI. 1990). Sea-level rise not only reduces intertidal area, but pro-

6.7 The future of rocky and sandy shores The future of rocky and sandy shores depends on the temparal perspective taken. A series of key analyses looking at impacts and threats to 2025 (Brown & McLachlan 2002; Kennish 2002; Thompson et aI. 2002, Kennish et aI. 2009) have identified a continued increase in many of the anthropogenic impacts that shores experience today. mainly because of projected increases in coastal populations worldwide. Looking further ahead to 2080, accelerated sea-level rise (ASLR) will undoubtedly impinge upon lowlying sedimentary shores and estuaries. but also on rocky shores because of changes in currents and hence transport patterns, as well as changes in wave climate (Chapter 15) . Accelerated Sea-level Rise, d ue to cl imate change, will have large-scale impacts on sandy beaches and mudflats over the next 50-1 00 years.

Beaches are dynamic physical entities. maintained by processes operating above and below the beach as com-

monly defined (Brown & McLachlan 1990), so that changes in sediment supply and wave climate are likely to impact

found ly alters sediment distribut ions.

It is likely that rocky shores, at least those below high cliffs, will not be subject to coastal squeeze. since the biology can migrate upwards over time without impediment. However. both rocky and sandy shores in some regions could experience a more severe wave climate, due to an increase in storminess with climate change (IPCC 2001) . Of most concern, perhaps. is the suspected relationship between sea-level and the return time of storm surges, catastrophic flooding events that can remove entire beaches and mudflats. For instance, one estimate suggests that an increase in sea-level of 0.5 m, well within the range predicted by 2080, can alter the return time of a 1.5 m storm surge from 1 in every 100 years to 1 in 10 years or less (IPCC 2001) . How shore communities, both soft and hard, would respond to catastrophic disturbances at a frequency that approximates the lifespan of much of the shore biota is hard to predict. However. longer lived species would have difficulty adapting to such conditions due to their lower fecundity and infrequent recruitment. The frequency of catastrophic wave action is likely to increase dramat ically with rises in sea-level.

Chapter Summary •

Rocky and sandy shores are the most accessible parts of the marine environment and contain representatives of almost all the major classes of animals and plants.

•

Rocky and sandy shores occur at either end of an environmental gradient of habitat particle size

that ranges from very large (cliffs and boulders) to very small (individual sand grains). Species occupy sections of this gradient and the wetness/dryness (shore level) and wave-action gradients, and reveal zonation patterns that are most obvious across the shore level gradient.

Chapter Summary

•

The distribution and abundance of these species are determined

by their tolerances to physical

factors, such as water movement and desiccat ion, and to biological factors , such as competition , biotu rbation , and predat ion. •

Rocky and sandy shores provide excellent laboratories for exp loring mainstream ecolog ical concepts. Much of t he pioneering research using controlled experimental manipulations has been carried out on the seashore.

•

Different kinds of shore are net exporters or importers of energy, especially detrital material. Understanding ecological funct ioning requires shores to be viewed as connected networks.

•

Sandy and muddy shores are particularly vulnerable to climate change induced sea-level rise,

because they are often prevented from transgressing inland.

Further Reading Little and Kitching (200 1) is an excellent concise book that deals with rocky shores, w hile Raffaelli and Hawkins (1996) consider in depth the deve lopment of interti dal ecology. Raffaell i and Moller (2000)

critically evaluate the use and misuse of experimental approaches in ecology. Reise (1985) is a detailed consideration of the ecology of tidal flats. •

Bertness, M. D. 2007 . Atlantic Shorelines, Natural History and Ecology. Princeton University Press, Woodstock, UK.

•

Little, C. & Kitching, J. A. 200 1. Biology of Rocky Shores. Oxford Un iversity Press, Oxford.

•

Raffaelli, D. & Haw kins, S. J. 1996. Intertidal Ecology. Chapman and Hall.

•

Raffaelli, D. G. & Moller, H. 2000. Manipulative experiments in animal ecology-do they prom ise more than they can deliver? Advances in Ecolagicol Research 30: 299-330.

•

Reise, K. 19 8 5. Tidal Flat Ecology. An Experimental Approach to Species Interadions. Springer-Verlag, Berlin.

Pelagic Ecosystems

Chapter Summary

ants, but great whales and jellyfish alike are s ubject to the

Away from coastal boundaries and above the seabed, the

conseq uences of pelagi c ecosystem variabil ity. Physical

pelagic environment encompasses the entire water column

process es in the pelagic exert major cont rol on biologi cal

of the seas and oceans. The pelagic envi ronment extends

activity, and lead to substant ial geograp hic vari ability in pro-

from the sea surface to th e abyssal depths, from the tropics to the polar regions, an d is a highly heterogeneous and

duction. Know ledge of biophysical interactions is essent ial for und erstandin g ecolog ical patterns and processes in the

dynamic three-d imensional habitat. It is th e most volumi-

pelagic environment, for management of fisheries ecosys-

nous habitat on Earth. The pelagic environment is home

tems, and will be key for predictin g changes in th e pelagic

to some of the most revered and reviled marine inhabit-

induced, for examp le, by cl imate change.

7.1 Introduction The term pelagic means 'o f the open sea', and the pelagic realm is a largely open, unbounded environme nt in which the inhabitants have freedom, within physiological limits, to move in three dimensions. The pelagic environment is the largest habitat on Earth. Contrary to the common perception that the sea is an unchanging, relentless expanse, the open ocean is an environment where variability is very much the norm. Patchiness in physical properties (e.g. temperature, salinity, turbidity), biological production, and biomass exists at a range of scales in space (centimetres to hundreds of kilometres) and time (minutes to decades and beyond). One of the key challenges to understanding open-ocean function lies in understanding the mechanisms that cause, and consequences of, this patchiness (Mackas & Tsuda 1999; Mitchell et aJ. 2008). The open ocean is a highly dynamic and variable environment, even though it may appear superficially uniform to the human eye when viewed from the shore.

Despite the fact that much of the open ocean is remote from land, beyond the horizon for land-based observers, it has not

escaped human impacts. For example, 90% of stocks of large pelagic fish, such as tuna (Scombridae) and jacks (Caran gidae), may have been removed by fishing (Myers & Worm 2003), and whole zooplankto n com mun ities h ave shifted their spatial distribution (Beaugrand et aJ. 2002) , possibly in response to ocean warming, itself most likely caused by ant hropogen ically-released greenhouse gasses OPCC 2007) . Microscopic plastic fra gments are also widespre ad in the oceans, and have accumulated in the pelagic zone (Thompson et a1. 2004) wit h damaging consequences for a variety of orgamsms . Despite its apparent remoteness, the open ocean has been influenced strongly by human activities such as fishing , pollution , litter, and anthropogenic climate warming.

The pioneering studies of open-ocean ecology made from vessels wit h evocative n ames such as Discovery , Cha llenger, and Atlantis have been enhanced in recent years with observations from technologically advanced research platforms that include Earth-orbiting satellites (Bricaud et aJ. 1999) and unmanned autonomous underwater vehicles (AUVs; see Box 7.5) (Griffi ths 2003) . The aim of this chapter is to provide a synt hesis of open -ocean ecosys tem fun ction and the

7.2 Definitions and environmental features •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

factors that control it, insight into difficulties associated with sampling the heterogeneous pelagic realm, and some examples of ecological step-changes (regim e shifts) in the global pelagic environment.

7.2 Definitions and environmental features The pelagic realm spans the entirety of the water column, beginning at the sea surface and ending just above the seabed (the benthic realm; Chapters 8 and 9) . This midwater marine ecosystem is the largest on Earth and comprises over 99.5% of the planet's habitable space (Robison 2004) . The pelagic realm can be subdivided by total water depth and distance from shore. The neritic zone lies adjacent to shore, over continental shelves, and covers about 8% of the Earth's total sea area. Out beyond the continental shelf break, which is delimited typically by the 200-m depth contour (isobath), lies the vast, open oceanic zone (92%of the total sea area, covering 65%of the Earth's sur-

face) . There are numerous differences between the neritic and oceanic zones, differences that arise not least because of differences in proximity to land and consequent differences in nutrient and sediment loading in the water column (much of the sediment load in the seas and oceans is terrigenous and is delivered by rivers and estuaries; Chapter 5) . Sailing out from a coastal port towards the open sea it is common to notice a transition from turbid to clear, blue waters. This transition is obvious not just from the deck of a ship but is visible from space. Indeed, interpretations of satellite remote-sensed observations of ocean properties have to distinguish 'Case l' waters, where the ocean colour is determined predominantly by algal pigments, from 'Case 2' waters, where reflections from particulate matter dominate (Fig. 7.1) (Babin et al. 2003) . Differences in particulate loading lead to differences in underwater light climate that, along with different nutrient availabilities, have led to differing photosynthetic architectures in neritic and oceanic phytoplankton. Offshore species of diatoms have evolved lower photosystem 1 and cytochrome b(6)f complex concentrations, enabling them to decrease their

Figure 7.1 An enhanced truecolour view of ocean colour

from the SeaWiFS satellite (18 May 1998 13:08 GMT) showing Case 1 and 2 waters around and to the south-west of the British

Isles, North-West Europe. Satellite images were received by the NERC Dundee Satellite Receiving Station

and processed by Peter Miller and Gavin Tilstone at the Plymouth Marine Laboratory (PML) Remote Sensing Group (http://www. neodaas.ac.ukl). SeaWiFS data courtesy of the NASA SeaWiFS project and Orbital Sciences Corporation.

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

iron requirements without compromising photosynthetic capacity (Strzepek & Harrison 2004) . However, oceanic diatoms have probably sacrificed their ability to acclimate to the rapid fluctuations in light intensity that characterize dynamic and turbid coastal waters. Another adaptive biological consequence of the difference in sediment and particulate loading between the oceanic and neritic zones can perhaps be seen in squid anatomy. Myopsin squid inhabit the neritic zone (for example Loligo forbesi, which is common in north-west European coastal waters. or L. opalescens from the west coast of the USA) and have a membrane across the eye that may serve to protect the eye from particulate irritants suspended in the water: in the open ocean myopsin squid are replaced largely by members of the suborder Oegopsina (for example, the European flying squid, Todarodes sagittatus) in which the membrane is absent, pos-

primary production (Chapter 2) and because it enables visual predation (predators that hunt using the sense of sight) . In deeper, darker waters tactile predation (predation by touch) dominates (Eiane et al. 1999), but in clear oceanic waters the threat from visual predators is increased because these predators can detect preyovergreater ranges (Aksnes & Giske 1993). Shark attacks on humans often occur in turbid waters (Cliff 1991), possibly because under these conditions prey recognition is difficult and humans are mistaken for typical prey such as seals. The upper part of the water column into which light penetrates is called the photic zone. In clear tropical oceanic waters this zone may extend as deep as 200 m (much less in more turbid, temperate locations), although at this depth light intensity will usually be too low to drive photosynthesis (Chapter 2) .

sibly because it is unnecessary. The neritic and oceanic zones are very different, due in part to their differing distances from the coastline and associated differences in particulate and nutrient loading.

Open ocean and coastal diatoms have different photosynthetic architectures that enable them to cope with different nutrient availabilities and light climates.

The presence of a protective eye membrane in neritic squid may be an adaptation to heavy particu late loading in near-shore seas.

The pelagic component ofthe open ocean can be divided further by depth. The upper surface of the ocean is known as the neustic zone and, in the tropics especially, is a habitat made harsh by exposure to high levels of ultraviolet radiation. Floating organismsinhabiting this zone typically have a blue colouration (Fig. 7.2) due to the presence of protective pigments that are able to reflect this damaging part of the light spectrum. The development of the ozone hole in the Earth's atmosphere has resulted in increased levels of UV radiation reaching the Earth's surface (the ozone layer acts as a UV shield), particularly in the southern hemisphere. In the Southern Ocean, Antarctic krill (Euphausia superba) may be particularly vulnerable to UV-induced DNA mutation because krill DNA is rich in thymine, which is the base that is most susceptible to UV radiation damage (Jarman et a1. 1999). Since krill migrate away from the sea surface during daylight hours, however, their behaviour will probably serve to limit DNA damage, but UV damage to other species remains a distinct possibility, and photosynthesis by Antarctic phytoplankton shows inhibition by elevated UV (Smith et al. 1992). Light also plays an important role in pelagic ecosystem function away from the neustic zone, both because it drives

Figure 7.2 The Portuguese Man o'War (Physalia physalis, a colonial Cnidarian) floats at the sea surface and has a blue colouration (photograph: joaoquaresma.com). Organisms that live in the neustic zone are particularly vulnerable to increases in UV radiation.

The upper 200 m of the water column is also known as epipelagic (Fig. 7.3) . Light at the red end of the spectrum is absorbed rapidly by seawater and does not penetrate far into the epipelagic zone (Chapter 2) . Red colours are effectively invisible at depth, therefore, and many pelagic crustaceans adopt this colour as a means of camouflage against visual predators (Fig. 7.4) . Below the epipelagic zone are, sequentially, the mesopelagic (200 to 2000 m), the bathypelagic (2000 to 4000 m), and the abyssopelagic (4000 to 6000 m) zones. As depth increases, organisms in the pelagic environment are faced with increasing physiological challenges: pressure increases by 1 atmosphere for

7.2 Definitions and environmental features •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

every 10 mincrease in depth (Box 7.1 ; 1 atmosphere = 1 kg cm- 2, equivalent approximately to the mass ofa bag ofsugar balanced on your finger tip) and in some locations oxygenminima layers (Rogers 2000) arise at depth because oxygen is depleted by bacteria breaking down material sinking from the sea surface. Low oxygen concentrations render J

compartments of the world ocean inhospitable to multicel-

lular life. and ongoing warming together with rising atmospheric CO 2 will see an expansion of oxygen minima zones,

perhaps by more than 50% by volume, by the end of the twenty-first century (Stramma et al. 2008) . In general terms the total mass of biota per unit volume of seawater decreases with depth (Yamaguchi et al. 2002) . This is because, with the exception of energy input by chema-autotrophic processes at hydrothermal vents (Chapter 9), biological processes in the deep sea are fuelled entirely by photosynthetically-generated organic

Figure 7.4 A mesopelagic zoop lankton/nekton sample

matter from the illuminated surface region. This material

showing the predominance of red-coloured crustaceans

either sinks passively, sometimes in strong pulses of'marine snow' (Billett et al. 1983), or is transported downwards by

(photograph: Andrew Brierley).

vertically-migrating organisms that excrete, or are eaten, at

depths deeper than which they feed. Animals migrating vertically through a series ofoverlapping yet ever-deeper depth zones form togethera 'ladder' ofmigration from the surface to the deep down which carbon is passed as if in a chain of ever-smaller buckets. As material descends further from the

bon does, however, reach the deep ocean interior, where it can be consumed by organisms on the sea bed or incorporated into sediments (Billett et al. 2006) . Trapping, or sequestration, of carbon in the deep sea is the end-point of the so-called 'biological pump' that transfers atmospheric CO 2 to the ocean (Lutz et al. 2007).

surface it becomes distributed through an ever-increasing volume afwater. This dilution effect means that as distance

The total mass of biota per unit volume of seawater

from the surface increases, food availability decreases, with

decreases with depth.

the consequence that less animal biomass can be sustained

at depth. In the deep pelagic zones, energy efficiency is particularly important and animals adopt stealthy, sedentary lifestyles and use cunning mechanisms to ambush prey in

Energy efficiency is important in the deep pelagic due to

the dispersed nature of potential food.

darkness (Seibel et al. 2000) . Photosynthetically-fixed car-

High water

Pelagic

, j

Neritic

. Low water llfterul •

(antinental shelf

Oceanic

Epipelagic

-~

200m

~. ~ ~

[ Phatic

~

Mesapelagic

- - -- ----- -------- --- --- --- --- ----------

%~~ !!> "

1000 m

-

.~

0

Bathypelagic

~- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - -

...

~ 4000m

Benthic _ ---Abyssal ~--\-a~a~p"I~9~C___

6000m

Hadal

• Figure 7.3 Depth zones in the pelagic realm.

I

1 ‫סס‬oo

m

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

The word plankton is derived from the Greek word pla-

Box 7.1: Seawater as a dense and viscous (sticky) medium Seawater is denser and more viscous than air. The increased density offers advantages to some mari ne organisms, for example, providing physical support

that reduces the need fo r skeletal strength (beached whales suffer because their skeletons are inadequate

to support their bulk in air), but also presents challenges such as rapidly increasing pressure with depth. Seawater density varies as a function of the concentration of dissolved salts (salinit y; salinity is reported without units since it is defined in terms of the ratio of the electrical conductivity of seawater

nao, which means 't o wander'.

Plankton can, however, move vertically, adjusting their depth, and do so pronouncedly during diel vertical migrations (DVM) at dawn and dusk (Fig. 7.5). Diel vertical migrations are a ubiquitous feature of pelagic ecosystems (Hays 2003) and are thought to be driven primarily by the trade-off required to enable plankton to feed in the foodrich upper water-column and yet to avoid the illuminated upper layer in daylight because of the increased risk of visual predation incurred there at that time (Tarling 2003). This is probably not the whole story, however, as vertical migration some times continues in the constant darkness of polar winter (Berge et al. 2009) .

to the electrical conductivity of a po tassium chloride standard; see also Chapter 5) and tempera-

Daily and seasonal changes in incident light intensity

tu re (warm water is less dense than cold water).

have profound effects on biological processes in the

The strength of cohesion, or stickiness, of a fluid is

pelagic environment, driving vertical migrations and

quantified by its dynamic viscosity. The dynamic

seasonal plankton blooms.

viscosity of olive oil, for example, is 40 t imes tha t of seawater. The motion of a particle of a given size and velocity is more impeded thro ugh a medium of greater dynamic viscosity (thin k of a marble sinki ng through a bottle of water and a bottle of olive oil). For a fluid of a given dynamic viscosity (e.g. seawater) the conti nuity of motion of a particle is controlled by its velocity and size, and can be quantified by the Reynolds' number (Re). For a given fluid, Re is simply: (particle velocity x particle size)/ dynamic viscosity. Re is dimensionless because the units used in its calculation cancel out. Broadly speaking for small organisms moving at slow speeds Re is less than 10 0 0 and seawater is 'sticky': ciliates, for example, stop the moment they cease swimmi ng. For larger

Some organisms, such as copepods and chae rognat hs, complete their entire lifecycle as plankton and are called holoplankton. Others, such as fish lar vae and barnacle larvae, spe nd only a part of their lifecycle as pl ankton, either growing or settling out to the seabed as they age, and are called meropl ankton. A planktic phase provides opportunities for dispersal and colo nization, but is also a stage that is particularly vulnerable to predation (Pechenik 1999 ). Planktotrophic larvae (larvae that have an exte nded pl anktic phase) may suffe r higher per capita mortality than lecithotrophic larvae that have a limited planktik phase, but planktotrophic organisms may achieve more wides pread genetic dispersal than lecithotrophes (Todd et al. 1998).

organisms travelling at higher speeds Re is greater than 1000: the inertia of a large pelagic fish, for

Animals whose larvae have a prolonged planktic phase

example, enables it to continue gliding through the

(i.e. that are planktotrophic) generally produce a higher

water even after it has ceased active swimming (see

number of eggs per unit body mass than do animals

also Chapter 3).

with lecithotrophic larvae. This may be because mortality rates in the plankton are high.

7.3 Pelagic inhabitants: consequences of size Pelagic organisms can be divided into two categories on the basis of their locomotory prowess. Plankton are unable to counteract the influence of horizontal currents and so drift passively in the horizontal plane (ocean currents often exceed 1 knot or e. 0.5 m s").

Organisms that are capable of swimming to the extent that they can overcome horizontal currents are known as nekton. Inhabitants of the open ocean span several orders of magnitude of size, ranging from viruses, bacteria, and protozoa to large predators such as sharks and whales, which may reach many metres in length and body masses of several tonnes. Generally speaking, large organisms are nektic and smaller organisms are planktic: micronekton have intermediate swimming abilities and are of the order of 4 em in length (for example, large euphausiids such as Antarctic krill). This size-relate d difference in mobility arises in part because of the interaction betwe en size and

7.3 Pelagic inhabitants: consequences of size •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

I

I

IIII

II

I

I

I

I

I

I

II I I

-50

100 200 300

-60

"" 400 ~ 500

-70

_

.§.

=

~

.~

= J!! =

0

~ ~

600

-80

700

-J8

-36

-J4

-J2

-JO

- 28

-26

-24

'----------.J -90

longitude degrees Figure 7.5 An echogram showing the rapid ascent of zooplankton and nekton (as detected using a 38 kHz scientific echo-sounder) from depth to the near surface at dusk. This migration from 400 m to 50 m takes less than 2 h. The

upper bar indicates periods of day (light blue) and night (dark blue). Temporal and spatial variability are tightly intertwined in this echogram.

viscosity (Box 7.1) : seawater is essentially a 'sticky' medium for small organisms (Van Duren & Videler 2003) and, for them, a constant expenditure ofenergy is required to maintain motion. There are exceptions to the size-mobility gen-

eralization. however, and the Arctic lion's mane jellyfish (Cyanea arctica) that may attain tentacle lengths of 40 m, remains a passive, planktic drifter. The very smallest planktic organisms include viruses and bacteria (Azam & Worden 2004) and protozoa (Struder-Kypke & Montagnes 2002). The small size of these organisms belies their importance to pelagic ecosystem function. Viruses are a major cause of mortaliry, a driver of biogeochemical cycles, affect the form of available nutrients and the termination of algal blooms (Suttle 2005) . Dissolved organic carbon is taken up by bacteria, which are consumed byheterotrophic nanoflagellates and in turn by ciliates in the so-called microbial loop at the base of the food chain (Chapter 3) . This loop recycles organic matter that is too small to be consumed by metazoan plankton, and the metazoans are able to prey upon ciliates. The microbial loop therefore fuels the pelagic food chain, and is especially important in oligotrophic waters (Lenz 2000) . Very few pelagic organisms dismantle their prey before eating, a behaviour more common in benthic biota such as crabs.

As well as impacting mobility, organism size is also a

major architect of pelagic food-web structure. Pelagic organisms will typically consume food items whole, and the size of item thatan animal can consume is constrained by its mouth size, such that predators are usuallysubstantially larger than their prey (Cohen et al. 1993; Jennings & WaIT 2003) . This concept is well captured by Brueghel's picture Big Fish Eat Little Fish, in which small fish are tumbling out of the mouths

of successively bigger fish (Fig. 7.6) . A more taxonomically extensive example from the North Sea has unicellular algae, such as diatoms (c. 100 11m diameter), grazed by copepods (e.g. Calanus finmarchicus, c. 3 mm length), which are in turn predated by herring (dupea harengus, c. 20 em length), which might be consumed by gannets (Sula ba.ssana, c. 180 cm wing span), or minke whales (Balaenoptera acutorostrata, c. 7 m length). This strongly size-structured progression is in marked contrast to many terrestrial food chains where small predators (for example, hyenas, body mass c. 40 kg) may cooperate in social groups to take herbivores that are considerably larger (e.g, wildebeest, c. 250 kg). In terrestrial systems, animals that forage in social groups can deal with prey items much larger than themselves.

Pelagic food webs are often far more complex than the simple four-linked-chain diatom-copepod-fish-bird example from the North Sea. An analysis of a 29-species' food web for the Benguela ecosystem. for example. undertaken to determine ifculling Cape fur seals (Arctocephalus pusillus pusillus) would increase biomass of commercially important hake (Merluccius spp.) (Yodzis 2000) noted that there were over 28 million pathways including hake and seals! This complexity of food webs, and the fact that most levels can be controlled either from above (top-down control, e.g, by predation) or below (bottom-up control, e.g. by food limitation; Verity & Smetacek 1996) renders it very difficult to make predictions of the consequences of bioregulation. In general. smaller mean predator:prey body size ratios are characteristic ofmore stable environments, and food chains are longer when mean predator:prey body size ratios are small (Jennings & Warr 2003) . Systems that have shorter food chains are generally much more susceptible to trophic cascade effects (Brierley 2007; Chapter 8) .

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

The complexity of food webs means it is difficult (if not impossible) to predict the outcome of selective culling of higher predators on lower tropic levels. Nevertheless, there is increasing evidence that populations of top predators, such as seals, may, at current levels, have a disproportionate predation effect on fish populations.

Oscillation that exhibits decadal-scale variability (Chavez et al. 2003; see also Chapters 1, 8, 13, and IS). Fish, which are generally longer lived than zoop lankton, are impacted by environmental variabil ity over longer t ime-scales.

7.4.1 Physical processes contributing to temporal and spatial variability

Figure 7.6 'Big Fish Eat Little Fish:' by Pieter Brueghel the Elder (1557) showing smaller fish tumbling from the mouths of bigger fish. The Metropolitan Museum of Art, Harris Brisbane Dick Fund, 1917 (17.3.859).

7.4 Temporal and spatial variability in pelagic ecosystems The open ocean is not homogenous. Interactions between physical and biological processes result in variability over a range of temporal and spatial scales, and patchiness is a key feature of pelagic ecosystems. The Stommel diagram (Fig. 7.7) illustrates the scales of variability that are inherent characteristics of pelagic ecosystems, from centimetres to thousands of kilometres horizontally and from seconds to millennia. and shows how variations in time and space are interlinked. It is important to appreciate the interplay of temporal and spatial scales, and it is a theme that recurs throughout this book. Phytoplankton are short-lived and are influenced by small-scale mixing processes (Martin 2003) . The diel vertical migration (DVM) of zooplankton at dawn and dusk is restricted to certain times of day but occurs everywhere (Pearre 2003), indeed DVM is the largest coordinated movement of biomass on the planet. Fish, which are generally longer lived than zooplankton, are impacted by environmental variability over longer timescales: the Peruvian anchoveta (Engraulis ringens), for example, is influenced strongly by the E1 Nino Southern

The physical properties of the open ocean are heterogeneous by depth, position (latitude, longitude), and over time. In addition to the depth-related changes in light intensity and oxygen concentration already mentioned. vertical gradients in water temperature. density, current velocity, and nutrient concentration may also exist. Solar heating warms the upper ocean leading to the development of a thermal gradient by depth. In some regions, combinations of tidal and winddriven processes cause turbulence and mixing of heated surface water. with cooler water below. However, in regions or seasons where winds are light and wave action slight. or in water that is too deep to be mixed completely by tidal flow (Chapter 8). pronounced vertical stratification can become established: warm surface waters then become effectively isolated from cooler. deeper waters by a thermocline. Vertical stratification is also promoted in situations where fresh water is introduced. Rain, river run-off. and ice-melt all introduce fresh water to the surface of the ocean. Low salinitywaters are less dense than high salinity waters (Box 7.1) and stabilize the upper water column because more energy is required to mix low salinitywaters downwards. The strong density gradient between the mixed, buoyant, low-salinity surface waters and underlying high-salinity waters is known as the pycnocline. The depth of the mixed layer, as bounded by the pycnocline or thermocline, will vary depending upon prevailing conditions (Chapters 2 and 8) . Where winds are light and wave action slight, or in water

t hat is too deep to be mixed completely by tidal flow, vertical stratification can develop.

As well as causing downward mixing. wind can lead

to the upward transport of water from depth. Such winddriven upwelling occurs over a range ofscales. At the small scale. Langmuir circulation is generated as wind blows steadily across calm water, causing near-surface vortices several metres in diameter to develop parallel to the wind flow (Box 7.2) . At the interfaces between neighbouring vortex cells, alternating lines of upward divergence and downward convergence develop. Flotsam accumulates on the surface above the downward zones, leading to the development of prominent, parallel wind lanes on the surface. Zooplankton may also accumulate in downward

7.4 Temporal and spatial variability in pelagic ecosystems

__ IOOOOKm

Ice age variations JI __ 1000 Km

Annual cycles

§;~~ I __ IOOKm J ,'/ "'-_G.-,---~

.,-lOKm

9

A. 'Micro' pmrhs R. Swarms C. Upwelling D. Eddies andrings E. Island effects F. 'EI Nino' type events G. Small ocean basins H. Biogeogrcphitol provinm I. Currents and Oleanic fronts - length J. Currents K. Oleani! fronts - width

o D o

Ship, Moorings Satellites

log l (em) .-- 1 em

Biomass variability

Time

o

log P(sec)

Figure 7.7 The Stammel diagram , overlain to show the scales that can be sampled with various platforms, and features

such as fronts. Modified from ICES Zooplankton Methodology Manual, Harris et al. (eds), (2000), page 36. Copyright 2000, with permission from Elsevier.

zones because they are able to swim upwards against the flow (Pershing et al. 2001). Langmuir circulation can lead to the accumulation of

zooplankton and flotsam , which forms visible wind lanes, at the sea surface.

At the large scale, wind plays a role inducing flow in most surface curre nts. Curre nts do not flow parallel to the direction of the w ind but, due to interactions w it h the Coriolis force, when averaged over the whole of the water column, curre nts move at 90° to the wind. Movement is to the right

of the wind in the northern hemisphere and to the left in the southern hemisphere. This movement is called Ekman transport (Box 7.2). It contributes sign ificantly to gene ral ocean circulation and can result in pronounced upwelling. In the case of the Benguela Curre nt, for example, and other southern hemisphere eastern boundary currents, the prevailing sout h-easterly winds blow alongshore and drive near-shore Ekman flow away from the coas t. This in turn draws cold, nutrient-rich waters from depth to the surface at the coast (Carr & Kearns 2003) . Changes in global wind patterns have the potential to affect upwelling and the ecosystems that are dependent upon them (Grantham et a1.

Box 7.2: Wind-driven circulation processes

on the sea surface running parallel to the direction of the

As wind blows over the surface of the sea it generates

ents up from deep water beneath the pycnocline.

waves and induces vertical and horizontal mot ion in the water. Langmuir cells are small-scale, parallel, helical

Large-scale ocean currents are also induced by wi nd, but occur at angles to the direction of the wind rather than

vortices tha t are often apparent as a series of wind lanes

parallel to it. This is because of the interaction between

wind. Vortices are usually not large enough to bring nutri-

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

friction and the Coriolis force . The Coriolis fo rce is the force experienced by a mov ing bo dy of w ater due to th e

ceases. Cumulative impacts of Coriolis force result in an

fact that the planet is rotating. The water colu mn can be

depth. Curren t vectors in all layers form a spi ral pattern

thought of as a series of horizontal layers. The upper layer

known as an Ekman spiral. The averaged effect of the

at the sea surface is subject to wi nd friction (w ind stress)

spi ral is that the mean motion of the wi nd-driven (Ekman)

at the top and water fr iction (edd y viscosity) at the bot-

layer is at right angles to th e wind direction. Reprinted

tom. Subsequent layers are impacted by friction with lay-

from Ocean Circulation (2nd edn), the Open University

ers above and beneath. Slippage between layers results in

Course Team (2001) , pp. 42 and 68. Copyright 200 1,

an exponential decrease in current speed with depth until,

with permission from Elsevier.

increasing angle of deviation away from th e wi nd wi th

below the depth of frictional influence, wi nd influence

Downwelling [ronverqentes where seoweed, debris, foom, ond plankton a«umulate)

Helical vortices -----:-;

Wind stress

'-

---J

Average mation of the Ekman layer

Average monon of the Ekman layer

Ioriolis force Ioriolis farce

-- --

__ - - ___

~

_~ ~ -

~~-

-~

Depth,! frictional infl uence

Upwelling (divergen,e)

7.4 Temporal and spatial variability in pelagic ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Horizontal boundaries between water masses with different physical properties are known as fronts (Box 7.3) . Fronts occur at a range of scales, from tidal mixing fronts that separate mixed and stratified waters in coastal seas (Hill et al. 1993) to major oceanographic boundaries such as the North Wall of the GulfStream and the Antarctic Polar Front (Taylor & Gangopadhyay2001) . High-velocitycurrent jets associated with fronts can be important long-distance transport routes for many marine organisms: Antarctic krill (Euphausia superba) are transported widely throughout the Scotia Sea from breeding centres off the Antarctic Peninsula on frontal currents (Thorpe et al. 2004), and large oceanic squid, such as Illex illecebrosus, take advantage of currents for distribution and feeding (O'Dor 1992) . Meanders in fronts can lead to columns of water (core rings) being shed from one side of the front to the other; the retroflection of the Agulhus current around the southern tip of Africa, for

example. sheds warm core rings regularly into the south Atlantic (Garzoli et al. 1999) and this so-called Agulhas leakage is an important mechanism for transoceanic mixing. Vertical variations in current flow lead to shear stress that has major ramifications for horizontal structuring in the ocean (see Current Focus box) . Whilst it is recognized commonly that organisms are influenced by physical processes in the ocean. it is less widely accepted that organisms can influence ocean dynamics. However, recent work has suggested that animals can influence biogeochemical cycling (Wilson et al. 2009) and, more controversially. ocean mixing (Kunze et at. 2006; Katija and Dabiri 2009; Fig. 7.8): rather than just being passive occupants that are impacted by physical change. life forms in the pelagic can make active and climate-influencing contributions to planetary function (Brierley & Kingsford 2009). Most fronts are highly mobile, dynamic features that cannot be represented accurately by single, static lines on charts.

7.4.2. Consequences of temporal and spatial physical variability for pelagic primary productivity and biogeography

Figure 7.8 Drift of dye behind a swimming Mastigias spp. jellyfish showing the mixing that animal motion can induce (image from Katija & Dabiri 2009: http:// www.nature.com/natu re/journal/v460/n 72 55/fig_tab/ nature08207J2.htm l).

The depth to which water-column mixing occurs, the mixed-layer depth, has major implications for primary production in the open ocean because photosynthesis only takes place in illuminated surface waters. If the mixed layer is deep it is possible that phytoplankton will sink or be carried down below the compensation depth (Chapter 2). reducing net production. In temperate waters. primary production is minimal during winter when light levels and temperatures are low and the upper water column is thoroughly mixed by storm action and convection (Backhaus et at. 2003) . Phytoplankton blooms do not commence until calmer, warmer weather in the spring leads to upper watercolumn stratification. From this point on, phytoplankton cells are retained in the upper mixed layer, benefit from the increased illumination from the sun as it reaches higher angles in the sky, and grow and reproduce rapidly. Phytoplankton require nutrients such as phosphate. silicate, and nitrate to grow. As phytoplankton blooms develop, concentrations of these nutrients become depleted and the effective isolation of the mixed layer from the larger nutrient pool beneath means that nutrients are not replenished. In temperate waters, nutrient limitation may inhibit phytoplankton growth throughout the summer months. A second bloom may though occur at the onset ofautumn when winddriven mixing brings nutrient-rich waters from beneath

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

the pycnocline up in to the illuminated surface layer (Diehl 2002) . In the North Sea the classic two-peaked (spring and autumn) phytoplankton bloom pattern has been disrupted by eutrophication: riverine input of nutrients from agricultural and industrial run-off have overridden natural nutrient limitation and led to more-or-less continuous summer phytoplankton production (Heath and Beare 2008) . Although the development of stratification is a neces-

sary precursor to phytoplankton bloom formation in temperate waters, the persistence of an upper layer that is

effectively cut off by density and temperature gradients from the waters beneath can eventually inhibit phyto-

plankton growth. A phytoplankton maximum can develop at the pycnocline in high summer as this is the interface between nutrientrich deep water and illuminated but nutrient-depleted surface stratified waters.

In regions of the world where upwelling is persistent throughout the year (Box 7.2) nutrients tend not to be limited and annual primary production levels are high. However, in the Pacific off South America changes in prevailing weather conditions associated with the El Nino Southern Oscillation reduce the usually strong upwelling, and ensuing nutrient limitation has dramatic negative consequences for primary production and fisheries in coastal waters. Tropical ocean basins tend to be permanently stratified and primary production levels are low. As a consequence, surface waters in these tropical regions lack particulate matter and are very clear: such waters are termed oligotrophic. Open ocean waters distant from land can be enriched with nutrients in dust blown from land. Wind-blown (aeolian) Saharan sand fertilizes the open Atlantic with iron. increasing production (Jickells et al. 2005), but winds can also bring pollutants and Red Sea plankton may be poisoned by copper in desert dust (Paytan et al. 2009) . Other areas of the world ocean have low phytoplankton biomass despite the presence of high nutrient concentrations. These HNLC (high nutrient, low chlorophyll) regions include the Southern Ocean and Equatorial Pacific, and hypotheses proposed to explain their existence include grazing pressure and absence of trace elements, particularly iron (Chapter 2) . The oceans generate about half of Earth's annual global primary production (48.5 Petagrams of 104.9 Pg C; Field et al. 1998) but since 1999, global ocean primary production has fallen by 0 .19 Pg C per year (Behrenfeld et al. 2006) . The majority of this reduction has occurred in the permanently-stratified low latitude oceans (roughly 4S"N to 45"S) because warming and strengthening stratification have caused nutrient limitation. In polar regions, increased wind strength (leading to increased mixing and nutrient

replenishment) and reducing ice extent (that reduces water-column shading) could lead to increased open ocean primary production, but these increases (e.g. 0.03 Pg C per year since 2003 in the Arctic; Arrigo et al. 2008) will probably not counteract the mid-latitude reductions. Recently, Smetacek (2008) has proposed that the depletion ofbaleen whales in the southern oceans may be responsible for the decline in primary productivity. With the removal of the great whales from the ocean. the anticipated ecosystem response was predation release for prey species such as krill. However, krill have declined and have been replaced to some extent by biota such as salps. Smetacek's (2008) theory is that whales were keystone species in this ecosystem. Krill consume phytoplankton and thereby capture elements such as iron. If krill die and sink to the ocean floor, the iron is lost from the pelagic system. However, if the ktill are consumed by whales, the iron is then defaecated back into the pelagic zone and becomes available to primary producers. Smetacek (2008) described this as 'manuring the oceans' (see also Nicol et al. 2010) . In the same way that fronts on weather maps mark boundaries between different air masses. fronts in the sea are boundaries between dissimilar bodies of water. Fronts occur off estuaries at boundaries between fresh and salt water, in shelf seas between tidally-mixed and stratified waters, at continental shelf breaks adjacent to upwelling regions and. at the global scale. between major current systems. Fronts tend to be sites with higher biological activity than the surrounding water masses, often because nutrients are transported upwards into the stratified euphotic zone at fronts. Tidal-mixing fronts (also known as shelf sea fronts) occur between tidally mixed and stratified waters. They occur when the intensity of turbulent mixing caused by tidally induced flow over the seabed is sufficient to overcome the barrier to mixing caused by thermal stratification. In simple terms, this is a function of the strength of the tidal flow and water depth; a strong tidal flow will generate sufficient turbulence to completely mix shallow water. On the stratified side of the front, nutrient concentrations in the warm surface waters are depleted and the strong thermal gradient prevents nutrients from beneath being mixed upwards. Phytoplankton growth is therefore nutrient-limited and low. On the well-mixed side of the front, although nutrients are not limited, phytoplankton are continually mixed down out of the illuminated surface layer and growth is light-limited. Atthe front itself, stratification weakens sufficiently to enable some vertical nutrient flux but remains strong enough to hold phytoplankton in the photic zone long enough for them to take advantage of the nutrients. A study in the North Sea found new production at tidal fronts to be low (Heath and Beare 2008) and it was concluded that, in order to accord with the traditional view that these areas are highly productive zones. they must be loci of high recycled production. Increased phytoplankton

7.4 Temporal and spatial variability in pelagic ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

production at fronts leads to higher zooplankton standing stocks and increased densities of predators and underlying benthos (see also Chapters 2 and 8). Plankton grazers, including Basking sharks and Manta rays, may forage in these food-rich zones (Priede and Miller 2009) .

-., 7

25

s,

E

;;

20

1;;

• = s 'is

- 15 = 10 = -5 + u: -S

Iron is thoug ht t o be one of the key limiting t race elements in HNLC regions, and experimental iron ferti lizati o n in t hese locat io ns has stimulated phytoplankton

prod uction (Boyd et al. 2007).

Global variation in the pattern of annual primary production is strikingly clear in images of averaged chlorophyll concentration obtained through satellite imagery (see Fig. 2.5, Chapter 2) . Regional coherence in the pattern of annual phytoplankton production has been used as one diagnostic feature in the hierarchical separation of the global ocean into distinct biogeographic biomes and provinces (Longhurst 2006) . A biome is the largest coherent community unit that it is convenient to recognize, and Longhurst (2006) distinguishes four in the global ocean, which are characterized by the principal mechanisms driving their mixed layer depth: in the Westerlies biome local winds and irradiance force the mixed layer depth; in the Trades biome the mixed layer depth is influenced by largescale ocean-circulation processes; in the Polar biome the presence of buoyant. fresh water from ice melt in spring constrains the mixed layer depth; and in the Coastal biome diverse processes including upwelling force the mixed layer depth. Within these biomes. 51 provinces are recognized (Chapter 1). Separation of the global ocean into provinces is very useful because it allows regional differences in physical oceanography to be used to gain understanding, and make predictions. of regional differences in ocean ecology.

~

/"

~

~

~

0

1

2 50

3 100 150 200 250 Total phytoplankton production (g (m"2 yr 1)

300

Figure 7.9 The relationship between primary production and nekton production. Fish and squid production =

(0.095 phytoplankton production) - 3.73, r' = 0 .96. 1

= Atlantic Ocean gyre centre, 2 = Atlantic Ocean gyre boundaries, 3 = Hawaiian waters, 4 = Bothnian Sea, 5

= Gulf of Riga, 6 = Gulf of Finland, 7 = Baltic Sea, 8 = Nova Scotian shelf, 9 = Gulf of Maine, 10= Mid-Atlantic bight. Redrawn from Iverson 1990. Copyright 2000 by the American Society of Limnology and Oceanography, Inc.

shelf seas and regions with strong upwelling account for the vast majority of the world's commercial catch (Watson & Pauly 2001), whereas oligotrophic central open-ocean basins contribute little. Commercially important pelagic fish species do not consume phytoplankton directly but usually predate zooplankton and micronekton that are primary consumers. Understanding zooplankton ecology is therefore key to understanding fisheries production. GLOBEC (global ocean ecosystem dynamics; http://www. globec.org) was a global research effort to unde rstand interactions between primary consumers, higher trophic

Knowledge that a particular area of ocean lies in a par-

levels, and fishe ries.

ticular province enables predictions to be made regarding ecosystem function there, even if field data for the specific area are lacking.

7.4.3 Consequences for higher trophic levels of variability in primary production Regions of the world's ocean with high primary productivity support richer pelagic communities. with higher total biomass. than do regions with low primary production. In fact there is a direct linear relationship between the magnitude of annual primary production and nekton (fish and squid) production (Sommer et at. 2002; Jennings et at. 2008) (Fig. 7.9) . This relationship is apparent in the distribution of global fish catches (Chapter 13) : nutrient-rich

Many zooplankton populations are bottom-up controlled (that is they are limited by food availability) (Richardson & Schoeman 2004) . Zooplankton blooms are only able to develop once phytoplankton biomass and production has become sufficient to sustain zooplankton grazing rates. In temperate waters, therefore. peaks in zooplankton biomass occur in spring and autumn slightly after the phytoplankton blooms. In high latitudes, where seasonality is extreme and the phytoplankton bloom is limited to a single spring/summer peak. some zooplankton species survive the dark. food-impoverished winter months in deep water in a dormant state called diapause. Copepods including Calanus finmarchicus in the sub-Arctic North Atlantic and Calanoides acutus in the Southern Ocean build up large stores of lipids during summer feeding, a small proportion of which fuels their survival overwinter. At the end ofsummer, growth and development are arrested and individu-

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

als sink. over wintering in a sta te of hibernation at depths between 500 m and 2000 m (Box 7.3) . In late w inter or early spring, copepods emerge from diapause and migrate to the surface to spawn. Because of the short production season. the timing of reproduction is critical at high latitudes. By using lipid reserves accumulated in the previous year to fuel reproduction. these copepods can spawn early, independent of the present year's phytoplankton bloom, and ensure that their young are in place to fully exploit the short lived phytoplankton bloom. Co/anus finmarchicus survives food-depleted winter months in the north Atlantic by drawing on lipid reserves.

This also enables it to produce young in advance of the phytoplankton bloom in the following year.

The timing of the phytoplankton bloom not only influences zooplankton secondary production but also places a significant control upon organisms that predate up on zoo-

Box 7.3: Diapause depth, water density, and lipid composition

plankton. Developing fish larvae 'surf on the wave of zooplankton production' and the match-mismatch hypothesis (Cus hing 1990) proposes that larval fish survival w ill be gre atest in years when the period of plankton production overlaps most closely with the period oflarval food demand. Satellite data that revealed between-year variations in the timing of the spring phytoplankton bloom support this hypothesis wit h regard to haddock (Melanogrammus aeglefinus ) on the shelf east of Nova Scotia (Platt et al. 2003 ; Fig. 7.10) . An index of larval haddock survival (size of age 1 year class divided by spawning stock biomass) showed that two exceptionally strong yea r classes occurred when the peak of the spring phytoplankton bloom was between 2 and 3 weeks earlier than the long-term average. An early bloom may reduce larval mortality by starvation. Survival of larval fish is greatest when the overlap between the period of planktic food availability and food demand by fish is greatest.

It is not yet clear what the main evolutionary drivers of variation in copepod lipid co mposi tion are. In order to survive the winter individuals need to descend below

The overwintering depth of the copepod Co/anus finmar-

the depth of wi nter mixing, and will also have increased

chicus varies throughout its distribution range in the north

chances of survival overwi nter if they descend below

Atlantic. In the eastern Norwegian Sea, for example, Cafo-

depths where predators can operate. In Norwegian fjords,

nus overwi nters at about 800 m, whereas in the Iceland

overwi nteri ng is shallower in fjords where visual predators

Basin overwi ntering is at around 150 0 m (Heath et al.

are absen t (Bagoien et al. 200 1), but the winter distri-

2004), despite the fact tha t both locations have similar

but ion of predators in the open ocean is not yet known.

total water depths (c. 2000 m) . The water-colu mn vertical

Ironically, therefore, individuals tha t feed too successfully

temperature profile varies markedly throughout the north

over summer and lay down excessive lipid reserves may

Atlantic: in the eastern Norwegian Sea the temperat ure at

be unable to sink to depths below predators; th is would

the overwintering depth is approximately O°C, whereas in

p rovide a strong selective pressu re agai nst over-con-

the Iceland Basi n it is much warmer (4°C) . This physical

sumption and may be one reason w hy some copepods

variation provides much insight into the variation of the

enter diapause early in the year w hen the phytoplankton

overwi ntering depth. At the onset of diapause Co/anus

b loom is still in full swing. Since current flow is different

becomes physically inactive and sinks passively until it

at different depths, the overwintering depth will also have

reaches the depth where it is neutrally buoyant. This is the

a profound influence on the location at w hich individual

depth at which the density of the copepod is the same as the density of the surroundi ng seawater, which itself is a

Co/anus surface afte r diapause. In order to complete its lifecycle successfully, Cafonus has to surface at a location

function of ambient temperature and salinity. One of the

where offspring can be spawned and hatch and eat, and

major contributors to variation in density between cope-

descend to overwinter to complete the lifecycle. It is likely

pods is lipid composition, such that density decreases as

that few depths will enable this to be achieved, providi ng

the proportions of lipid increases. Using knowledge of

another sou rce of selection. It is clear that the lifecycle

the temperature and salinity at the overwi nteri ng depth in

of Cafonus is t ied very closely to its environment; under-

several locations, and hence the density there, it has been

standi ng the environmental space-ti me dynamics will be

possi ble to predict the propo rtion of lipid that should be

vital to gaining full understanding of regional variability in

expected in individuals overwintering at particular loca-

Co/anus abundance and consequences to higher t rophic

tions. A very good linear relat ionship has been found

levels such as fis heries (Heath et al. 2008).

between predicted and actual values (Heath et al. 2004).

7.4 Temporal and spatial variability in pelagic ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Spatial, as well as temporal. coherence is required between production and consumption if high-biomass pelagic communities are to develop. At the large scale, it has been suggested that iron fertilization in regions of low primary productivity could enhance production up the food chain to zooplankton and fisheries, and that the increased photosynthesis could also lead to an increased drawdown of atmospheric carbon dioxide (an enhanced biological pump) that may mitigate against climate change (Lovelock & Rapley 2007) . Complex trophic interactions, however. make implementation of this far from straightforward (Cullen & Boyd 2008). Indeed, recent observations

of phytoplankton blooms in the Southern Ocean, stimulated by natural iron enrichment of waters flowing past the Crozet Islands, suggest blooms stimulated artificially are weak, perhaps because oflarge losses of the artificially

10 _

8

~-

1981

•

•• 6 -g 1998

c

•

-~

.;: 4

2

1980 2001 •

• 2

2000 • •1979,1997 1

0

-I

-2

Anomalies in the timing of spring blooms (weeks)

to mitigate the effects ofclimate change through purposeful addition of iron to the ocean (Pollard et al. 2009) . At the

Figure 7.10 Larval haddock survival (size of the year class at age 1 (R) divided by spawning stock biomass (SSB» against deviation from the mean time of the annual peak in phytoplankton production. Timing of the peak of the spring phytoplankton bloom explains 89% of the

smaller scale, patchiness is essential for maintaining eco-

variance in larval survival , providing strong support for

system function. If phytoplankton and grazers were mixed homogenously, then resource depletion would soon occur,

the match-mismatch hypothesis. Redrawn from Platt et al.

added iron. This has significant implications for proposals

(2003) with permission from the author.

whereas patchiness and spatial segregation enable higher

overall biomass to be maintained (Brentnall et al. 2003; Mitchell et al. 2008) . Furthermore, if zooplankton did not aggregate in high densities, then pelagic filter-feeders, such as basking sharks (Cetorhinus maximus) and baleenwhales,

prey in the wide expanse of the open ocean remain largely unknown and different cues are likely to be important at

would not be able to survive on a diet of these organisms.

different spatial scales (Fauchald et al. 2000) . A growing

Whales incur high energetic costs while foraging (Acevedo-Gutierrez et al. 2002) and it has been estimated, for example, that Right whales (Eubalaena glacialis) require

body of evidence suggests that many marine predator species do not forage at random across the pelagic expanse.

copepod prey concentrations to exceed a minimum thresh-

predators make occasional long-distance relocations to 'new' search areas and undertake numerous short forays in

old of 4500 individuals m~3 of seawater just to balance the energy expended during feeding (Beardsley et al. 1996).

ing fish, squid, marine mammals, and birds (Durazo et al. 1998) . The exact mechanisms by which predators locate

but follow search patterns with Levy-like distributions:

each area (Sims et al. 2008) . This type of foraging may be

Furthermore, whilst some euphausiid species aggregate to form swarms. perhaps to gain protection from predators,

an evolutionary response to distributions of prey including

paradoxically it is swarm formation that makes krill viable prey for whales: it has been suggested that if krill off Nova

ecosystems prey are located regularly in production 'hot

spots' (Davoren et al. 2003), attracting larger predators

Scotia were dispersed uniformly at average densities, then

in a predictable manner. Conservation measures aimed

fin whales feeding there would need to swim at 900 km h' to eat their fill in an 8-h period (Brodie et al. 1978) .

at reducing conflict between wildlife and fishers need to

If phytoplan kton and grazers were mixed homogenously, th en resource deplet ion would soon occur, whereas spati al segregation enables higher overall biomass to be

zooplankton that also exhibit Levy distributions. In some

account for geographic variability such as this in ecosystem management plans. Fisheries for Antarctic krill. for example. may in future be required to operate outside the

foraging areas ofland-based central-place foragers during their breeding season (Constable & Nicol 2002) .

maintained . Conservation measures aimed at reduci ng conflict

Frontal regions tend to be characterized by increased

between wild life and fishers need to take in to account

primary production and to support particularly rich pelagic

th e fact th at predators sometimes forage at production

communities (Box 7.3). Fronts are therefore sites of intense

hotspots that occur at oceanographic features such as

feeding activityand are targeted by mobile predators includ-

fro nts.

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

7.5 Sampling the open ocean The some times extreme horizontal, vertical, and temporal patchiness that is characteristic of pelagic ecosystems, and the huge size-range of organisms inhabiting the open ocean, present considerable difficulties for quantitative sampling. Early studies of the open ocean depended almost completely on fishing nets to sample living organisms. Netting remains an important component of biological oceanographic research, but the systems in use tod ay are considerably more complex than those used in the pioneering d ays (Wiebe & Benfield 2003) . These days, nets are often equipped with depth, temperature, salinity, and other sensors. Data from these sensors can be relayed to the ship in real time, either along conducting cables or via acoustic links, and enable nets to be placed accurately in the sec-

CURRENT FOCUS: Microlayers and the 'paradox of the plankton'

tion of the water column of particular interest (Brierley et al. 1998). Optical particle counters (OPCs) can be used instead of nets to obtain estimates of zooplankton numerical density (He ath 1995), and photograph ic and video devices en able high -qu ality im ages of ocean inhabitants to be obt ained (Benfield et al. 1996). Light is attenuated rapidly by seawater though, and visu al sampling is often constra ined by water clarity (Chapter 2) . Sound, on the other hand, propagates very efficiently through seawater, as is testified by the long-range vocal commun ications of some whales. Scientific echo-sounders can be used to detect and quantify abundance of zooplankton and fish (Holliday & Pieper 1995), and ever-increasing sampling resolution (see Techniques box) is detect ing biologically important features such as micro-layers (McManus et al, 2003), which are likely to be of very m ajor importance to pelagic ecosystem function (see Curre nt Focus box).

several days. Thin layers produce micro-environments of physical, chemical, and biological parameters. They contain densities of organisms several orders of magnit ude

In 19 61 Hutchinson expounded the 'Paradox of the

highe r than adjacent depth zones (Benoi t-Bi rd 2009),

Pl ankton', questioning how it could be possi ble for such a

and may be important fo ragi ng sites for fish and other

large number of plan kton species to coexist in the appar-

pred ators. Layers at different depths in the same area

ently homogenous pelagic environment. The t radi tional

may contain distinct plankton assemblages. The species

ecological view is that a variety of niches are needed if

or populations that comprise each distinct thin layer prob-

species are to coexist, otherwise competitive exclusion

ably aggreg ate in response to different sets of biological

enables a single species to dominate. Recent experi men-

and/or physical processes.

tal and theoretical work supports this view (Levine and

Microlayers someti mes occu r at the pycnocline as zoo-

Hill e Ris Lambers 2009). Traditional pelagic-sampling

plankton forage on material that is suspended there, but

techniques, such as vertical netting, reversing thermo m-

may be deeper or shallower. Layers can occu r in strati-

eters, and early echo-sou nders, provided only quite low

fied water where current sheer is low, but sheer has also

vertical sampli ng resolution, and contributed to the per-

been proposed as one of the forming mechanisms. Some

ception th at, other than the thermocline, there was little

phytoplankton cells are motile and swi m upwards against

vertical structuring in the water colum n (see Tech niques

gravity. When they swim upwards into shear zones, zones

figure, upper panel). A w ater colum n with little ver tical

where the direction of ho rizo ntal flow changes rapidly

heterogeneity woul d provide little opportunity for niche

over a sho rt vertical range, they are made to t umble

differentiation, and a low number of niches should sup-

because of an interaction of gravitational and viscous

port only low diversity. Advances in the resolu tion of opti-

torques. When the shear exceeds a critical threshold, tum-

cal and acoustic sampling tech nology (see Techniques

bling prevents the phytoplankton from swim ming further

box) have, however, led to the discovery of widesp read

upwards and they become trapped- the process is called

'thin layers' of high biological activity in the ocean (McM a-

gyrotactic trappi ng (Du rham et al. 2009; see the figu re

nus et al. 2003). Th e existence and persistence of plan k-

below ) . This mechanism is a good example of how b io-

tic thin layers generates great biological heterogeneity

logical patchiness arises as a consequence of physical

in the water colum n, and may go some way to expl ai n

heterogeneity in the ocean. Understa nding exactly how

the 'Paradox of the Plankton'. Thin layers, which range in

physical and biological processes interact could lead to

thickness from a few centimetres to a few metres, may be

more powerful ecosystem models of, for example, the

many kilometres in horizo ntal extent and may persist for

fo rmation of harmful algal blooms (Grunbaum 2009) .

7.5 Sampling the open ocean

lu}

Ib}

~UI ZI

- - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - --

x...I----:-+-~ T,

----------------- ----------------------

F====:: S" ulzl

I Hul az I Gyrotacti c trapping. (a) A gyrotacti c phytoplankton 's

centre of mass (red) is displaced from its ce nt re of buoyancy (x = z = 0). As a result, the swimming direction in a shear flow, u(z), is set by the balance of gravitational (Tg ) and vi scous (T) t orques. V is swimm ing

While modern imaging and acoustic technology have improved our ability to sample the ocean realm , we continue to be reliant upon often-rudimentary nets to obtain

biological samples.

At the larger scale, organisms that must come to the sea surface to breath (e.g. seals, whales) , or that forage over the sea surface (e.g. seabirds) , can be counted at sea by observers on research vessels. Alt hough much biological oceanograph ic data are still collected from sh ips, logistic cons tra ints place restrictions on the amo unt of time that ships can spend at sea. In order to make longer term obser-

~

~ ~( )

speed and m is mass. (b) Schematic of gyrotactic trapping. Cells can migrate vertically at low shear but tumble and become trapped where lSI > SCR' accumulating in a thin layer. (From Durham et al. 2009.)

vations, or observations over large extents of ocean, other sampling platforms or techniques are required. Moored instruments can be used to collect long time-series of data from spot locations (Schofield et al. 2002). Auto no mous underwater veh icles (Box 7.S), gliders , and verticallyprofiling floats, such as those in the Argo network (www. argo .ucsd.edu) , have the potential to be able to operate in weather conditions that curtail sampling from ships, and in add ition can work in environments that are impenetrable to sh ips. These autonomous and Lagrangian platforms and sensors ('ALPS', Dickey et al. 2008) are providing a wealth of valuable in situ data.

TECHNIQUES: Active acoustic sampling

whales, and other toothed whales use sound at higher

Li ght is attenuated rapidly by seawater and travels only

frequencies (40 Hz- 30 0 kH z) to locate prey in turbid and deep-hence dark- locations. Sound is a very effect-

relatively short distances, but sound propagates very

ive medium for scientific sampli ng in the ocean, and a

efficient ly. Thus, whereas cuttlefish can use changes in

variety of devices are in common use for pelagic and seabed exploration. The process of actively transmitting

skin colouration to communicate visually over ranges of several metres, baleen whale s use low-frequ ency sound (between about 10 and 30 Hertz) to communicate

over ranges of kil ometres and beyond. Dolphins, sperm

sound in to the water and detecting the returned echoes is called active acoustic sampling (as opposed to passive

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

sampling w hich involves j ust listening, for example for animal vocalizations).

ated continuously produce a 2D dataset, where the x-axis on the echogram is time rather than distance.

In the most basic form of active acoustic sampling,

The strength, or intensity, of an echo from a water-

downward-facing echo-sounders transmit regular pulses

colum n target is a function of many factors including tar-

of single-frequency sound ('pings') that are reflected or backscattered by the seabed and targets in the water col-

get size, shape, density, and acoustic frequency. In very

umn. A typical ping might be 1 millisecond long, and ping

the sou nd waves have a similar wavelength to the target

rates of 1 ping per second can be achieved to sample the

size. Wavelength (A, m), frequency (f, Hz ) , and sound

entire water column in the c. 200 m depths of on-shelf locations. The frequency of choice for biological sampling

velocity (c, m S·1) are linked according to the equation:

is usually in the range of tens to hundreds of kHz. Bio-

from which it can be seen that for a fixed sound velocity

logical targets can include single fish, fish schools, plank-

(a nominal value for the speed of sou nd in sea water

ton, and aggregations of organisms that in some cases

is 1,500 m s' ") waveleng th decreases as frequency

form continuous layers. Layers in mesopelagic depths

increases. Sound at 38 kHz has a wavelength of approxi-

are called deep scattering layers. These are a promi nent

mately 3.9 cm, and 12 cm anchoveta (Engraulis ringens)

and ubiquitous feature of the world ocean, comprising

tha t have swim bladders about 4 cm long (air-filled swim

commu nities of crustaceans, myctophid fish and other

bladders are very strong acoustic targets) will yield an

organisms, and have been known since the early days

echo almost twice as intense at 38 kHz than at 120

of acoustic sampli ng in the 1960s. Echo-sounders oper-

kHz, where the wavelength is 1.2 ern. Euphausiids j ust

ated continually along a research vessel's survey track

15 mm long, by contrast, including Antarctic krill Euphau-

yield data tha t provide a two-dimensional slice through

sia superba, return echoes that are about 35 t imes more

the watercolumn (2D; x

= distance, y = depth).

A visual

general terms, targets scatter sound most efficiently w hen

c =f 'A,

intense at 120 kHz than at 38 kHz.

representatio n of these data is known as an echogram

The fac t that different organisms produce different

(Fig. 7.5). Echo-sounders can also be mounted on fixed

re lat ive echo intensities at different frequencies, or dif-

moorings, facing upwards or downwards, and when oper-

ferent echo spectra, can be used to discriminate different

Acoustic Frequency: 1100 kHz

_ 15 ~:------:==:::i==~===;;;;;;;;;;;j;;;;;;;;;;;;;==1

-"".'" E

10

~

5

oI":-::-~-----------60 min, 2m

•

•

"

•

o 1min, 0.125m 15:00

12:00

-80

-75

-70

18:00 Time of Doy

-65

-60 -55 -50 Volume Smtterlna Strencth fdBl

21 :00

-45

00:00

-40

-35

-30

The bottom panel shows an acoustic record co ll ected in 1998 by an upward-looking 1100 kHz echo-sounder. The colour scale shows echo intensity, which is greatest in regions of the water column where organism packing density or biomass is highest. The record has a sampling resolution of 1 minute x 0 .125 m, and reveals a persistent thin layer between 5 and 10m from the echo-sounder. The upper panel shows the same data averaged on to a 60 minute x 2 m vertical grid , which was the state-of-the-art as recently as 1994: no fine layer is evident in that record. From Holliday et al. 2003.

7.5 Sampling the open ocean

species and/or sizes of targets. This in turn enables the development of automated processes to identify and sum

presence of persistent thin layers. The Current Focus box provides additional details on these hith erto unknown

echoes from particul ar species, and for abundance esti-

fine-scale features, features that could explain the main-

mates for species to be generated from acoustic survey

tenance of biological diversity in pelagic ecosystems. Multi beam echosounders sample a fan of beams that

data in a robust and repeatable manner. Annual biomass est imates of numerous pelagic species includi ng krill, her-

might make up an almost- 180° swath beneath a vessel.

ring, and anchovy are determ ined fro m acoustic surveys,

When operated continually along a survey track, these

and these estima tes feed in to processes that set annual

instruments deliver a th ree-dimensional (3D; depth x along-track positio n x across-track position) view of the

catch quotas. The resolut ion of acoustic sampling has increased

water colu mn (Gerlotto et al. 199 9) . Multibeam sonars

greatly in recent years, and will likely continue to do so

enable entire fish schools and krill swarms to be imaged,

given ongoing engineering and electronics advances. The

providi ng new insig hts into agg regative behaviour and the way in which predators interact with prey (Cox et al.

figu re on the previous page shows how high-resolution sampling by a moored echo-sounder has revealed the

There are essentially two strategies that can be followed when sampling the dynamic pelagic environment: Lagrangian or Eulerian. Lagrangian or current-following sampling obtains time-series of data from the same parcel of water, whereas Eulerian sampling obtains data from the stream of water that passes by a fixed geographic location. These contrasting views of space and time can give markedly different perspectives on biological and physical processes.

Earth-orbiting satellites are able to provide coverage of the entire surface of the global ocean on a weekly basis and deliver near-synoptic information on, for example, sea surface temperature, chlorophyll concentration, and frontal position (Miller 2004) . Satellites can also be used to track the movements of larger an imals as they forage at sea over extended periods of time (Thompson et al. 2003) and can relay d ata from instruments attached to the an imals. Leatherback turtles (Dermochelys coriacea ), for example, have been tracked in the north Atlantic (Hays et al. 2004) and time-depth recorders attached to their carapaces h ave revealed that they undertake asto nishingly deep di ves (to more than 1000 m; Houghton et al. 2008) . Leatherbacks are critically endangered, and a major source of mortality for them is capture by pelagic fisheries. Knowledge of leatherback distribution and dive characteristics obtained via satellite telemetry could lead to the implementation of conservation measures designed to reduce the interaction of turtles with fisheries, and thus reduce by-catch (Hays et al. 2004) .

2009).

In addition to providing fascinating data on the behaviour of an imals, sensors attached to animals can, by 'exploiting' their behaviour, provide a completely new view of ocean processes. Elephant seals, for example, undertake long journeys in the Southern Ocean in winter, travelling to oceanographically important locations at times of year when conventional research vessels seldom venture. CTD profiles from instruments attached to these animals have cast new light on sea ice formation and dyn amic frontal processes in the Southern Ocean (Charrassin et a1. 2008) . By measuring the high-latitude ocean during winter, elephant seals fill a 'blind spot' in our sampling coverage, and these 'an imal oceano graphers' have the potential to greatly improve our understanding of ocean fun ction. Satellites can relay information from tags attached to airbreathing animals, such as whales and turtles, collecting data about their behaviour and patterns of movement in near real time.

The capacity of scientists to be able to collect d ata from the pelagic realm seems ever to be increasing. Plans are afoot to establish a series of permanent, automated ocean observatories that will be able to deliver multidisciplinary data continuously in real time, yea r on year. Although these systems will contribute enormously to our understanding of ocean ecosystem fun ction, they will present new ch allenges in terms of extracting meaningful summaries from potentially overwhelming quantities of d ata.

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 7.4: Autonomous underwater vehicles Autonomous Underwate r Vehicles (AUVs) are unmanned

submersibles that can be programmed to navigate in th ree dimensions underwater. They can carry a variety

of scientific instruments and are able to make measurements in parts of the ocean th at are inaccessible, either physically or op erationally, to conventional research platforms such as ships. The Autosub AU\/, for example, has been equipped wi th a scientific echo-sounder and

deployed on missions beneath Antarctic sea ice. There, it has made obse rvations on the distribution of krill under ice, and of ice thickness, that were impossible to make using ice-breaking research vessels (Brie rley et al.

2002). Autosub is among the largest of AUVs presently ava ilable to the scientific community, with an instrument

payload capacity of 10 0 kg (we ight in water). Autosub is 7 m long x 1 m in diameter, weig hs 2 400 kg, is powered by manganese alkali batteries, propeller-drive n, has a range of about 800 km, and a maximum depth capabil-

ity of 1600 m. Web lin k: http:/ /www.noc.soton.ac.uk/ index.nf/usl_php?page=as (photog raph: Andrew Brierley). Autosub has con tinued to pioneer the exploration of hostile, under-ice envi ronments. This exploration is not wi thout risk though and in 2005 the origi nal vehicle

combines a high depth capability (6000 m) with long

became stuck in Antarctica under the Ronne Ice Shelf.

range (500 km) . These characte ristics, that are usually

Since then, however, developments have con tinued, and

mutually exclusive, were achieved by developing pressure

Autosub has ach ieved missio ns of over 50 km beneath the Pine Island Glacier. A new generation Autosub 6000 with deep ocean capability has been built. Autosub 6000

balanced lithium polymer batte ry tech nology, eli minat-

7.6 Pelagic fisheries

ing the need for expensive and bulky pressu re resistant housings.

Fisheries for pelagic species have the potential to be among the most sustainable and least damaging to the

Fisheries for pelagic species have the potential to be among the m ost sustainable and least d amaging to the enviro nment. Shoaling species like the Atlantic mackerel (Scom ber scom brus) and North Sea herring (Clupea harengus) form single-species agg regations, and by-catch of non-target species is minor compared to the demersal sector (Chapter 13). Stocks of mackerel, in particular, seem to be bucking the global trend of decline and faring well under good m anage ment and regulation. Myctophids, or lantern fish, are small mesopelagic fish that form a major component of oceanic deep-scattering layers. They have been fished historically in the sout h-west Indian Ocean and in the South Atl antic, but fishing ceased in 1992 because of unfavourable econom ics and m arket-resistance, and myctophids are not presently under threat.

environment.

Planktivorous fora ge fish, such as sardine and anchovy, h ave vital ecosystem functions, particularly in upwelling zones, where they form an important mid-trophic-level link in so-called wasp-waist ecosystems (Cury et al. 2000). In these systems one, or just a few species, of small planktivorous fish dominate their trophic level. Abundance of these species can fluctuate wildly under variable enviro nment al regimes and high fishing pressure and may result in m ajor ecosystem changes. Fishing for large tropical pelagic fish, including tuna and jacks, has also had substantial impact. Analyses of long-lining d ata suggest that 90% of biomass of large pelagic fish m ay have been removed (Myers & Worm 2003) . Open-ocean fisheries have tended to develop

7.7 Regime shifts in pelagic marine ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

ahead of management procedures (maybe by as much as 15 years) and, in the case of pelagic long-line fisheries, it is possible that the estimated pre-exploitation biomass to which management processes are anchored are unrealistically low because they represent already-depleted stock levels. This 'missing baseline' presents particular difficulty for the long-term restoration ofstocks because the size of the stock pre-exploitation remains unknown, and thus it is very difficult to say when, or if, restoration has been achieved. Not only has long-lining hit pelagic fish hard, but it has been, and is still, responsible for substantial declines in albatross populations. Albatrosses take baited long-line hooks as they are thrown from fishing vessels, drowning as the long-line sinks. Some populations are showing marked and continuing decline (ruck et al. 2001) but elsewhere, notably off South Africa, efforts to educate fishermen as to practices that can limit conflict are having major success: for every 100 albatrosses being killed in fisheries in South African waters in 2006, 85 are now (as of 2009) being saved. Seine netting for tuna also suffers from by-catch. particularly of dolphins, although, following international outcry, practices are in place to reduce the impact to levels that are now ecologically sustainable (Hall 1998). It is possible that the estimated pre-exploitation pelag ic fish biomass t o w hich management processes are anchored are unrealist ically low because they represent already-depleted stock levels, the so called 'rn issinqbaseline' effect.

The whole issue of 'dolphin-safe' tuna remains the subject of debate and there were moves in the United States to ease legislation relating to the defi nition of the prod-

uct. See also 'Eco labelling' in Chapter 16.

Squid are fished on the open seas, mostly using hooked, coloured lures (jigs) at night to catch animals attracted to bright lights. The high-intensity lights used to attract squid to jigs are so bright that they can be seen from satellites, and this has opened a new mechanism for potentially monitoring and managing open-ocean squid fisheries (Rodhouse et al. 2001) . Robust management is particularly important for squid because they are short-lived. often semelparous (spawn once and die), species and therefore vulnerable to over-fishing. since there are few cohorts to provide a buffer from failure of any single generation. Squid also respond rapidly to changing oceanographic conditions and it is becoming increasingly clear that it is essential to understand interactions between squid and their ocean environment in order to predict interannual variations in recruitment. Recruitment of the squid Illex argentinus to the Falkland Islands' fishery, for example, increases in years when water temperatures over the squid egg-hatching

grounds are favourable (16 to 18'C) .ln years when movement of the highly dynamic front between the Brazil and Falkland currents displaces waters of favourable temperature from over the hatching area, recruitment is reduced (Waluda et al. 2001) . Semelparous animals, such as squid , are particularly vulnerable to over-fishing as their populations are not composed of multiple cohorts that provide a safety net against over-exploitation.

7.7 Regime shifts in pelagic marine ecosystems Ecologists have long recognized that ecosystems may exist in 'multiple stable states'. In the oceans, conspicuous and rapid jumps from one state to another have become known as regime sh ifts (Scheffer et al. 2001) . Shifts typically take less than one year to occur and regimes may persist for decades (Hare & Mantua 2000) . Regime shifts may be driven by climatic changes, fishing pressure, or both, and may be evident in physical and biological ecosystem parameters. In the north Pacific. for example, statistically significant regime shifts in 1977 and 1989 are apparent in a composite index of 100 biological and physical time-series, including the Pacific Decadal Oscillation (PDO), zooplankton biomass estimates, and salmon catches (Fig. 7.11). Regime shifts present major challenges for scientists attempting to manage fisheries. In the North Sea a regime shift in 1988 was evident from plankton time-series data from the Continuous Plankton Recorder (CPR) surveys (Reid et al. 2001) . It has been suggested that this shift was caused by increasing flow of Atlantic waters into the North Sea, an increase that was correlated with a change in the North Atlantic Oscillation Index (NAOl) (Heath & Beare 2008) . Recruitment ofcod (Gadu.s morhua) in the North Sea has declined since the mid-1980s: it is possible that changes in the plankton following the regime shift have had a negative impact on the supply of food to young cod (bottom-up control) and have brought the end of the 'gadaid outburst' that previously brought good catches of cod (Beaugrand et al. 2003) . In the face ofsuch possible environmental impacts on fisheries, it is clear that future attempts to manage fisheries will need to take environmental factors into account, as well as data on fish population dynamics and catch levels. This realization has led to calls for the development of an holistic, ecosystem approach to fisheries management (Pitkitch et al. 2004; Chapters 13 and 16). The 19 88 regime shift in the Nort h Sea may have been caused by an infl ux of nut rient-rich Atlantic water.

Chapter 7 Pelagic Ecosystems •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Although not necessarily a symptom of regime shift per se.jellyfish appear to have increased in prominence in many pelagic marine ecosystemsworldwide in recent years (Richardson et at. 2009). Jellyfish blooms have occurred in the Bering Sea. the northern Benguela current. and elsewhere, possibly in response to climate and fishing effects. Indeed, it has been suggested that jellyfish-dominated communities are the inevitable end-point in pelagic ecosystems perturbed by fishing (Pauly & MacLean 2003) . In the North Sea, correlations between the abundance ofjellyfish and an Index describing the periodically fluctuating North Atlantic Oscillation (NAOI) have been detected (Lynam et at. 2004) . Furthermore it seems as though the recruitment of herring (Clupea harengu.s) in the North Sea is adversely affected by high jellyfish abundance. The jellyfish-herring link is probably mediated by a number of associations. Jellyfish prey upon herring eggs and larvae. and also compete with her1977 regimeshih ~

Ia

'"

II~

05

~

ll i

II

III I

·1.0 1965

~ ,

ing time-series of data are enabling more changes to be detected. A note of caution is perhaps necessary regarding this apparent increasing prevalence, however: simulation 1990 studies looking at random, independent time-series with the same frequency content as the Pacific Decadal Oscillation have shown that techniques used to identify 'regime

-r

I IIq 1975

1965

,

,

1980

1985

1989 regimeshih

shifts' may find them in noise. Detection of step-changes does not therefore necessarily provide evidence of processes leading to any meaningful regime shift (Rudnick & Davis 2003), since the step changes may be artifacts of the data.

1.0 J!!

£: E

~

Jl

consequence of overexploitation of pelagic fish stocks.

incidence of regime shifts is increasing, or that accumulat-

0 ·05

Jellyfish-dominated pelagic communities may be one

There has been an almost exponential rise in the incidence of the term 'regime shift' in the scientific literature since the early 1990s. It is possible that this is because the

1.0

T L iTT

ring for zooplankton food . Juvenile haddock gain shelter amongst the tentacles ofsome jellyfish, so haddock recruitment benefits from the presence ofjellyfish: adult haddock are predatory upon herring and jellyfish therefore mediate increased predation by haddock (Lynam & Brierley, 2007) . Complex interactions between climate and jellyfish may therefore impact fish stocks. even in the absence of fishing. and could have major implications for the recovery of fish stocks. even after any cessation of fishing. Understanding these linkages will be important for 'ecosystem-based' management: indeed, it has already been shown that implementation of the jellyfish-haddock-herring interaction in an ecosystem model of the North Sea improves predictions of gadoid recruitment (Mackinson & Daskalov 2007) .

05

IlL liI I

.. T ~ 1"

0

I

I

·05

, 1 .1 • .1 .1

·1.0 1975

1980

1985

1990

1995

2000

Figure 7.11 Mean and standard error of a composite

index of 31 physical and 69 biological parameters from the north Pacific between 1965 and 1997, showing significant step changes or 'regime shifts' in 1977 and 1989. The physical time-series represent atmospheric and oceanic processes, while the biological time-series all relate to oceanic species ranging from zooplankton to salmon and groundfish. Each of the time-series

was

normalized before plotting and statistical analysis by subtracting the mean across both regimes and then

dividing the data for each regime by the standard deviation for that regime. Standard errors for each year were computed as

In,where S is the standard deviation

across all variables within a year and

n is the number

of time series used in the calculation «100). Redrawn

from Scheffer et al. 2001 with Nature Publishing Group's copyright permission and permission from the author.

7.8 The future for pelagic marine ecosystems With an ever-increasing human population. and an evergrowing demand for food protein, it seems likely that pressure on the open ocean is likely to continue to grow. There is a history of fisheries advancing further from shore. into deeper and more distant waters, as conventional coastal resources are depleted, and this looks set to continue. Fishing effort has already had major impacts on the global ocean. As traditional fish species are removed, fishing effort turns from these higher trophic-level predators to smaller species. This phenomenon has become known as fishing down the food web (Paulyet at. 1998) and is ecologically unsustainable. Humans are not just altering the open-ocean ecosystems by removing biomass but are also degrading it by addition. The incidence ofwaste in the ocean is increasing, with floating rubbish potentially distributing species far

7.8 The future for pelagic marine ecosystems • ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

beyond their usual ranges, leading to alien colonizations of distant shores (Barnes 2002) . Introductions ofalien species

A recent forecast of the likely state of aquatic ecosystems in 2025 identified climate warming as the most sig-

in ballast water from cargo ships has also had devastating effects on pelagic ecosystems. such as the introduction of the ctenophore Mnemiopsis leydii to the Black Sea (Kideys 2002). This ctenophore, a native of the eastern USA, was predatory upon fish eggs and led to the collapse of the Black

nificant single threat (Chapter 15), and climate changes

Sea anchovy fishery. Dumping CO2 at sea in an attempt to reduce further increases in atmospheric concentrations is

being investigated (Hunter 1999) . As well as the addition ofobjects and organisms, human activityhas also increased noise levels in the ocean. Low-frequency noise from shipping, oil-exploration. and military activities may adversely impact cetacean communication and foraging (Croll et

al. 2001) by masking the sounds these animals generate. Killer whales (Orcinus orca) in the waters of Washington State, USA, increase the lengths of their calls significantly (by about 15%) in the presence of whale-watcher boat traffic, and probably do so in an attempt to overcome the noise

generated by these boats that may mask their usual calls (Foote et al. 2004) . Propagation of underwater sound in the range of frequencies used for cetacean communications will increase as the ocean become more acidic (Chapter 15) . Expected changes in ocean acidity could enable sounds to travel up to 70 per cent farther underwater, increasing the

levels of background noise in the oceans and potentially

have already had measurable impacts on sea-ice extent

and zooplankton distributions (Polunin 2005) . Temperature change is the most pervasive threat to marine eco-

systems globally (Halpern et al. 2008) and, if it continues unchecked, it could result in multiple extinctions before

the end of this century (Jackson 2008; Brierley and Kingsford 2009) . Perhaps the biggest climate-related threat to north Atlantic pelagic marine ecosystems arises from the possibility that increased warming and consequent freshen-

ing of the Arctic may switch off the North Atlantic current (NAC) and hence perturb global ocean circulation (Rahmstorf 2002) . Because of interactions between circulation, vertical mixing, nutrient supply, and production, reduction

of the NAC could reduce north Atlantic plankton biomass by more than half, and reduce global export production by more than 20% (Schmittner 2005) . It is probable that changes like this have happened multiple times during the Earth's history, and occurred over very short periods. If, as some models predict, this were to happen again in the near future, the consequences for the Earth's ecosystem and climate would be so severe that concern for the state of the

pelagic realm would probably not be at the top of humanity's agenda.

affecting the behaviour of marine mammals (Hester et a1.

2008) . The incidence of waste in th e ocean is increasing, wit h floating rubbish potentially distributing species far beyond their usual ranges leading to alien colon izat ions of distant shores.

Chapter Summary •

The pelagic realm is highly heterogeneous, and production is patchy in both space and time. Production is generally higher closer to land, because of increased nutrient input (rivers, upwelling), and close to the surface because of light availability. There is a direct link between primary production and fisheries' production.

•

Organism size has a major bearing on mobility in the pelagic environment. Plankton are generally small «10 mm long) and are unable to swim against currents, but drift passively on them. Larger organisms (nekton) can move actively against currents. Plankton can however move vertically and undertake pronounced diel migrations that contribute significantly to the 'biological pump'.

•

Pelagic food-webs are size-structured: small organisms are consumed by a succession of larger grazers or predators. Most biomass occurs at the lowest trophic levels (grazers) and gradually decreases at increasingly higher trophic levels.

•

Environmental heterogeneity and the large range of pelagic organism-size (from plankton to whales) presents a severe challenge for sampling the pelagic environment. Technological advances

Chapter 7 Pelagic Ecosystems provide the means to collect ever-increasing quantities of data, but net sampling remains important for collection of biological material. •

Pelagic fish that form large single-species' shoals should be amongst the most straightforward to manage and can be exploited with little risk of bycatch. Nevertheless, even pelagic species that inhabit remote locations far from land have been impacted severely by fishing.

•

Pelagic ecosystems can suffer step-changes, shifting rapid ly from one state to another. Such 'regime shifts' may be due to impacts of climatic change, and have major implications for ecosystem management.

Further Reading Longhurst (2006) provides an excellent description of the causes and consequences of geographic variab ility throughout the world 's ocean, Mann and Lazier (2006) give a broad coverage of b iological responses to physical processes in the ocean, and Miller (2004) provides a broad coverage of 'biological oceanog raphy' , A useful plankton atlas of the North Atlantic was published in Volume 27 8 of Marine Ecology Progress Series (20 0 4 ) , This provides a summary of Continuous Plankton Recorder (CPR) methods, and describes how this invaluable long-term record has become an important implement in our understand ing of how pelagic ecosystems respond to global change, Steele (2004) provides a brief review of regime shifts and their defi nition. His article is the first article in a special issue dedicated to regime shifts. The book Fisheries Acoustics by Simmonds and Maclennan (2005) provides excellent coverage of the use of sound for sampling aquatic environments, as well as some information on sound production by marine animals. •

Anonymo us, 20 0 4, Continuous plankton records: plankton atlas of the Nort h Atlantic Ocean (195819 99 ) , Marine Ecology Progress Series 278. Supplement available on line at: http:/ / www.int-res.com/ abstracts/meps/CPRatlas/contenls,htm l

•

longhurst, A. R. 2006, Ecological Geography of the Sea (2 nd edn) . Academ ic Press, San Diego,

•

Mann, K, H, & l.azler.L R. N, 2006, Dynamics of Marine Ecosystems: Biological-Physical Interactions in the Oceans (2nd edn) . Blackwell, Oxford,

•

Miller, C. 20 0 4, Biological Oceanography, Wiley-Blackwell.

•

SlrnrnondsJ. & Maclennan, D, 2005, Fisheries Acoustics, Theory and Practice (2nd edn) . Blackwell, Oxford ,

•

Steele, J. H. 20 04. Reg ime shifts in the ocean: reconciling observations and theory. Progress in Oceanography 60: 13 5-4 1.

Continental Shelf Seabed

• •

Chapter Summary

eycom bed w ith burrowing crustaceans and worms through

Continental shelves are the most heavily explo ited and uti-

species-impoverished mob ile sands to bedrock encrusted

lized areas of the wo rl d 's oceans and support the greatest

w ith luxuriant growths of particulate feed ers and algae. The

level of biological production. The ecology of the shallow

benthos is a critical link in the transfer of organic material

shelf areas is st rongly influenced by phy sical processes such as w aves, t ides, currents, erosion, and inputs of mate-

and nutrients from the w ater col umn above to t he seabed.

rial from the adjacent land mass. These processes generate

amo ng regi ons, w ith greater web complexi ty at mid to high

a great diversity of ecosystems and habitats at regional

latitudes. Systems w it h strong linkages amo ng individ ual

and local scales. The composi tion of the seabed and its associated biota are a direct reflect ion of the physical pro-

species are prone to troph ic cascades and are mo re sensi-

cesses that act upon it and vary from mud sedi ments hon-

regime shifts.

8.1 Introduction The world's continental shelves contribute only 8% of the global sea-surface. Nevertheless, their shallow nature means that most of the waters of the continental shelf fall wit hin the euphotic zone (Chapters 2 and 7) , which coupled wit h organic and mineral inputs via riverine discharges and strong physical mixing of the water colu mn and seabed. make them among the most productive and economically important regions of the world's oceans (Costanza et aJ. 1997) . In regions where the shelf is narrow, nutrients are add itionally supplied through upwelling of water from the deep sea. The high productivity found on continental shelves fuels high levels of secondary production (see Chapter 4) , which in turn underpins major global fisheries (Chapters 2, 7, and 13) .

The flo w of energy th ro ugh food webs varies considerably

t ive to the removal of key species lead ing to ecosystem

The abundant plankto n and fish fauna found in these waters are a key food resource for populations of top predators, such as seabirds and marine mammals. In add ition to their status as hotspots of biological activity, the proximity to the coastline and shallow n ature of shelf seas means that they have become the focus of intensive human activities and, in addition, receive agricultural and industrial contaminants from terrestrial run-off (Curre nt Focus). Sh ipping, fishing, exploration for, and extraction of, hydrocarbons, mining of sed iments and minerals, underwater cable laying, wind farm and tid al barrage development, offs hore aquaculture and recreation are just some of the major activities that occur and impact upon the continental shelf-sea environment. The ecology of the continental shelf is under ever-increasing levels of human usage, which has resulted in major changes in ecosystem structure in some localities.

Primary production in shelf seas fuels 900;0 of the world 's fisheries landings, consequently future environmental

The intensive use of the coastal shelf inevitably increases

changes that impact upon primary production are likely to have major consequences for shelf sea ecosystems and the goods and services that they provide (Pauly & Christensen 1995).

the risk of environmental damage from activities such as over-fishing, eutrophication, mineral extraction, dumping of waste, and oil spill accidents. The effects of these human activities may be exacerbated by the additional stress imposed by the current rapidly changing environmental conditions, particularly if they act synergistically.

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

CURRENT FOCUS: Catchment to coast-joined up research

from one form to another, and determi nes the bioavai lability of the materials for phytoplankton, microbes, and macrofauna.

It is rare in ecology for marine an d terrestrial scientists

Land-management pract ices are equally importa nt

to work together, their boundaries of research are clearly

determi nants of the content of run-off w it hin a catch-

defined as either essentially dry or wet and salty ! Su ch

ment. Plant ing of hed ges, trees, the stocking density of

compart mental ization has no do ubt arisen due to t he dif-

livestock, and the app lication of ferti lizers and pesticid es,

ferent sampling techniques that are used for these envi-

all have an impact on the q uality of w ater discharged into

ronments, an d the chemistry of the marine environment often means that you cannot si mply apply a t errestrial

estuaries and coastal systems.

technique in an aquatic context (the chemical composi-

ness in coastal w aters w ill increase co astal erosion and

ti on of seawater plays havoc w ith some scientific instru-

wave stress that is an important source of mortality for

mentation) . How ever, changi ng g lobal envi ronmental

coastal benth ic pop ulati ons. Indeed , it is li kely that the

con dit ions mean that t he impacts of physical processes,

biomass supported in som e coastal areas w ill decrease

such as rainfall and stor mi ness, are likely to have the

significantly w ith consequences for ecosystem processes

greatest impact in the coastal zone, such that marine sci-

and benthic feed ing predators.

In add it ion to these lan dward effects, increasing sto rmi-

enti sts need to begin to consi der ho w terrestrial catchment processes are likely to affect coastal ecology and shelf systems in the fut ure. We kno w from cli mate forecasts that precip itatio n events are likely to become less or more intens e in d ifferent parts of the world. Rainfall erodes terrestri al sediments and flushes nutrients and organic material from w ithin a catchment and ultimate ly transports those components into rivers and estuaries. This, coupled wi t h increasing temp eratures altering th e ability of upland bog to retain its dissolved organ ic carbon, mean that the composition of run-off is li kely to change the quality of w ater d ischarged into rivers. The nutrients and organic materials that pass

Ultimately, the quality of material that emerges from the

into rivers are altered by biogeochem ical and microb ial

mouth of this estuary into the adjacent coast is deter-

processes as they pass dow n the system towards the

mined by the land-management practices that affect

open sea. The intensity of rainfall w ill affect the rate of

the surrounding catchment and the regime of rainfall

flushing through the system and hence the residence t ime

and erosion pattern s that impact upon it (photograph:

during w hich nutrients and organic matter can be altered

Manfred Heyde).

8.2 Definitions and environmental features The contine ntal shelf extends from the extreme low-water m ark on the shoreline down to a depth of approximately 200 m and is termed neritic (Chapter 7). Th is region extends beyond the land from between nearly zero up to 1500 km offs hore out to the shelf break. Beyond this point the continental shelf slopes down to the abyssal plain (Chapter 9) . The shelfbreak is an area where biological a nd geological m aterial from the continental shelf is supplied to the shelf slope , through a variety of processes suc h as the death of organ isms or more dramatically via submarine mudslides. Only on extreme low-water spring tides, or

in the strandline wreckage in the upper shore that occurs after an onshore storm, are we able to observe unaided some of the organisms that live at the shallowest edge of the contine ntal shelf. Generally the continental slope h as a shallow gradient of ap proximately 1 0 except in regions where glacial activity has sculpted a more dramatic seabed. The shallow depth of the continental shelf and its position adjacent to the physical barrier of the land m ass mean that it is strongly influenced by physical forcing processes, suc h as glaciation events, currents, waves, the formation of fronts and water turbidity (Fig. 8.1). The interaction of these processes is influenced by shelf width and geographic disposition and is strongly re lated to consistent patterns in regional ecosystem structure .

8.2 Definitions and environmental features •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Physical processes perform a key role in the continental shelf environment due to its proximity to land, inputs of fresh water, seabed topography, and shallow

depth.

to the west of Florida in the GulfofMexico at a present-day depth of 4D m below sea-level. Glacial deposits characterize much of the continental shelf bed in the higher latitudes and are typified by fields of boulders and gravel beds. The continental shelf is relatively young in geological terms and has undergone dramatic expansion and

8.2.1 Influence of glaciation events The physical and biological characteristics of the continental shelf habitat are strongly influenced by the geological composition of the seabed, much of which has resulted from past glacial events that have had a profound influence on coastal margins and shallow near-shore seabed structure (Fig. 8.2) . The melting and formation of ice sheets causes the sea-level to rise and fall respectively, while the Earth's

crust is lowered underthe weight ofice, butrebounds (rises) in its absence (Box 8.1) . Thus areas hundreds of kilometres offshore may have been dry land at some point in recent geological history. This is reflected in the surface topography of the seabed where it still possible to see drowned river deltas (e.g, off the River Congo in Africa) , while evidence of hominid butchery of large mammal bones has been found

contraction as a result of glaciation events. Evidence for these events can be seen vividly on the seabed as drowned river plumes, boulder fields, and glacial scour-

ing. See Fig. 8.2 and Box 8.1.

8.2.2 Importance of waves and flow The physical effects ofwave5 have important consequences for the ecology of the shallower areas of the shelf (Emerson 1989), and their effects reach down to a depth of 80

m on open Atlantic coasts during gale-force conditions (Chapter 6) . Clearly, the depth to which waves influence benthic ecology will depend on the extent to which the coastline is sheltered from prevailing winds and the extent of fetch (Hiscock 1983). In areas where the physical force

I

Gases

4

Heat

~~ ,~0,, / ,

, , ,

II

,

Sediment/land Estuarine sediments

Sea bed 1. River (aaslal zane 2. Estuary [ 3. (aastal baundary layer 4.Shelf praper S. Shelf break

Slape sedimenls

Figure 8.1 Key processes that influence the continental shelf environment (adapted from Alongi 1998). POM = Particulate organic matter, DIN:;; Dissolved inorganic nitrogen, DOM ::;: Dissolved organic matter.

S

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

•

+

o

05

I

~i1 om"tr'"

Figure 8 .2 This multibeam-derived image of the seabed to the north of Anglesey, Irish Sea, shows the dramatic impact of past glacial events o n the sea bed . Submarine drumlins are clearly visible in this image, shown as a series of rounded mounds and pits. Such a clear image is unusual as the pits are normally filled in with deposits of fine sediment; however, the strong tidal cur rent s in this area have prevented sediment infilling (image courtesy of Katrien Van Landeghem).

of waves causes sediment movement, wave action can be a m ajor cause of m ortality among be nth ic animals and has been shown to affect secondary production by limiting the body size of organisms that can survive in a highly energetic environment (Emerson 1989). Water movement generates curre nts and these affect both the shallow and deeper parts of the shelf. The phenomenon of flow is extremely important for the ecology of the contine ntal shelf. as it affects the passive and active transport of organ isms. their gametes. and larvae (Techn iques box), and the rate of supply of food from the pelagic system to the seabed , and places upper

physical constraints on the type of organ isms that live in particular h abitats. Thus close to the shoreline. the seabed is affected most strongly by bot h waves and currents. as we move further offs hore the effects of waves reduce and the effects of curre nts begin to dominate the physical and biological processes on the seabed . This grad ient is clearly reflected in the biomass of sessile filter and deposit feeding biota. which increase wit h distance away from shallow into deeper water where the physical stress associated with waves and curre nts decreases and the seabed is therefore less frequently subjected to physical disturbance.

TECHNIQUES:Where do all the larvae

from, or tow ards, the surface (the speed of flow is high-

go?

est at the surface and lowest close to the seabe d-an d negligible at the boundary layer). In t he fig ure, we show

Tidally driven currents are essential for the dispersal of

the output of a particle-tracking mod el t hat w as used to

the larvae of many organisms. Rel at ive to the speed of

understand the likely dispersal pattern of scallop larv ae

surface currents, most larv ae are capable of only small

spawned within an area closed to scallop-fishing activities.

movements (a few body lengths per second compared

Understanding the orig in and end point of scallop larval

with flow speeds typically of >0.5 rn s'"). Larval behav-

dispersal helps us to understand how we might design

iour in response to envi ronmental cues, such as light and

a netwo rk of protected areas th at would increase the

salinity, can induce vertical mig rat ion in the water column,

sustainabil ity of the scallop popul at ion (see also Online

hence dispersal speed is altered as the larv ae move away

Resou rce Centre for a video simulation) .

8.2 Definitions and environmental features

The output of a larval-dispersal model for scallop released from Douglas Bay

(D), Isle of Man . The darker red the

areas, the higher the probability of larvae arriving in that area of the sea after

3 weeks of drifting in the plankton (the typical period required for development prior to settlement to the seabed). Image courtesy of Simon Neill.

Box 8.1: Rise and fall of the continental shelf edge

tially 14 000- 10000 years ago during the last glaciation event. After thi s pe ri o d, global sea-level changes have had a major influence on the coastal landscape. About

The coastal margins of the State of Maine (USA) have

14 000 years ago global (eu st at ic) sea-level w as about

left clear evi dence of the rise and fall of coastal margins

11 0m below its present level. However, the wei ght of local ice-sheets that were over 1 km thick depressed the

in respon se to glacial events. Land -level alte red substan-

lal

0

•>

Maine shoreli ne

.e 40 c

--• --• -•• c

~

Offshore Holotene shoreline \

50

Helerene with lome glooomorine

0

~

60

c

-a

--• ~

E

70

~

~

Q

80

Ibl Ice sheet

Retreating ftesheet melt wafe r

,..,.

Terrestriol deposits Sea level

-

Glociomarine deposits Sea level

rIS ing

Seo level

(a) Reflect ion of sound waves from the seabed strata at a depth of cAD m offshore of Maine USA shows the successive deposition of glaciomarine material during various glaciation events. (b) A schematic image to show the various stages of vertical movement of the continental shelf in relation to glacial retreat and changes in sea-level.

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

level of the Earth's crust, which meant that relative sealevel was 70 m above that of the present day. Eustatic sea-level was relatively low, but rising as the ice sheets began to melt. Ultimately, the re lease of the weight of the ice allowed rebound of the land to outpac e the rate of the rising global ocean. Thus, local relative sea-level fell (as the land rose), until it reached 55 m below the pres-

coastline to move well offshore of the present coast. Thus withi n the space of 4000 years the coastal margi n varied by as much as 12 5 m, with a coastline that expanded or contracted by te ns to hundreds of kilometres depending on the slope of the local continental shelf and coastal margin (the shallower the slope the greater the incu rsion or excurs ion by the sea).

ent sea-level about 11 000 years ago. This caused the

Fetch is the uninterrupted distance over which winds

exert friction at the sea surface.

The ecological importance of wave action diminishes with reducing fetch and distance from the shore as water depth increases. Animals that are either attached to a substratum or that move relatively little or infrequently are termed sessile. The rising and falling water mass has important implica tions for organ isms that live on the shore (Chapter 6) . An equally important result of this oscillation is the flow or current that is generated as the water floods into, or ebbs from,

restricted areas of coastl ine. Current is incre ased w hen a wate r m ass m oves through, or around , land-bounded restrictions or across ir regularities in the seabed topography. Typically, stra its and the narrow mouths of estuaries have some of the strongest tidal flows, reaching speeds of up to several metres per second . Headlands and bedro ck protrusions from the seabed also present restrictions to the flow of wate r and lead to stro ng cur rents around their apex (Fig. 8.3; see also Online Resource Centre video simulation associated with the Techniques box) . As water m oves over the seabed, the uneven se abed induces friction, which slows the immediate wate r column above, so seabed currents are rarely as fast as sea-s urface currents (except in areas of the deep sea ). Currents and the associated bottom shear stress, influence food availabilWest

East

o

Figure 8 .3 Current velocity generated through the tidal rise and fait of water in a sea basin is exacerbated dose to the coast, where coastal morpholog y and restrictions increase the speed of flow. This can be seen dearly for the example of the northwestern European shelf above, with strong mean surface velocities in the English Channel , the southern North Sea, and the George's Channel. Current velocities are also increased around headlands, such as off the North of Scotland and around the coast of Brittany and Normandy on the coast of France. The darker the blue lines, the higher the current velocity. Adapted from Metcalfe et al. 2002 .

2

4

6

8

1"o 54 z

Velocity keyemf

l

- - - Over75 - - 25· 75 Under 25

8.2 Definitions and environmental features •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

ity for benthic communities (Jenness & Duineveld 1985) and benthic secondary production (Warwick & Uncles 1980; Wildish & Peer 1983). High levels of shear stress cause scouring of the seabed and its biota, while high current velocities inhibit effective feeding activity. Biota that live in such environments tend to have characteristics or behaviours that enable them to cope with the extremes of physical stress. Typically, attached biota are highly flexible or encrusting, while mobile fauna will often seek shelter from currents within the sediment or in crevice habitats. At the other extreme. areas with reduced water movement at the seabed will not replenish the supply of food to the seabed, which then becomes a limiting factor for the growth of benthos. At a certain current velocity threshold, food particles transported from other areas will begin to sink to the seabed, where they become available as food to the benthos (Creutzberg 1984; Widdows et al. 2010) . The exact figure for the current velocity threshold will depend upon particle size and buoyancy. The latest research highlights how flow is strongly related to the rate of passive exchange of nutrients and oxygen between the top few millimetres of the sediment surface and the overlying water. A reduction in flow reduces the diversity ofthe surface sediment microbial assemblage, which in tum alters the physical properties of the sediment. Different microbes produce different types of extracellular products that coat sediment grains and hence affect properties such as shear (Biles et al. 2003) . Flow velocity influences the rate of supply and resuspension of particulate matter to and from the seabed, is linked to the rate of nutrient exchange at the sed i-

dient between the two bodies ofwater means that a flux of nutrients occurs from the mixed water mass to the nutrientdepleted upper stratified waters of the adjacentwater mass. This fuels primary production to a level higher than in the surrounding waters (Chapter 7) . As full salinity seawater approaches the coastline. it interacts with lower salinity water discharged as an estuarine plume. The difference in density between the two bodies of water sets up a frontal system due to the density gradient between the two bodies of water (the less dense estuarine water is more buoyant than full salinity seawater) and may deflect the estuarine water along the coastline in one direction due to the Coriolis force (Chapter 7) . Agood example of such a plume is the discharge from the River Rhine in the North Sea, which flows northwards along the Dutch coastline . These areas have become termed regions of freshwater influence or ROFIs . Elevated production of phytoplankton at fronts attracts both fish and their predators, such as seabirds and marine mammals, and results in a greater supply of organic matter to the benthic fauna.

The elevated primary production at fronts fuels production in the benthos and in pelagic and demersal fisheries. As a result. fronts are often the foci of fisheries' activities but also attract piscivorous and planktivorous seabirds and sea mammals, and there is evidence to suggest that fronts may be associated with above-average by-catches of marine mammals. such as the harbour porpoise (Phocoena phocoenu) (McGlade & Metuzals 2000; Trites et al. 2007) .

ment-water interface, and places upper constraints on the body size of biota that can live in a particular habitat.

8.2 .3 Fronts and production The development of fronts has important ecological implications in areas where water becomes stratified (Chapter 7) . During winter periods. the water column of the continental shelf is held in a well-mixed state by high winds and wave action. This means that dissolved oxygen, carbon dioxide, and nutrients are relatively evenly distributed from the sea surface to the seabed. The water column remains well ntixed throughout the year in areas where the seabed currents are strong and cause turbulent mixing. typically close to the coast in shallow water. In offshore waters and areas not strongly influenced by tidal mixing. periods of prolonged warm temperatures and calm conditions lead to stratification. This results in thermal depletion ofoxygen at the seabed and nutrients in the surface layers of the water column. Frontal systems occur at a point where a stratified and mixed body of water meet. The resulting density gra-

8.2.4 Light and turbidity Water depth and turbidity are important determinants of the distribution of benthic algae in the shallow waters close to the coast. Areas of the seabed affected by estuarine plumes are generally severely light-limited due to the associated high load of suspended sediment and phytodetritus, which attenuates light in the first few metres of the water column (Chapter 2) . Thus these areas of the seabed tend to be dominated by animals, and any algae are restricted to the very shallowest water adjacent to the shore. In contrast. coastal areas that are typically open to the ocean. and have limited riverine discharge. have much clearer waters and here a full range of algae can be found with clear zonation from the shallow to the deeper water ofgreen (shallow), brown, and then red (deep) algal dominance. In these situations algae can be dominant in terms of their biomass. The width of the algal-dominated zone will depend on water clarity and slope of the seabed (the clearer the water and lower the slope the greater the area of seabed that will be suitable for algal growth) .

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Algae are restricted to a narrow zone of near-shore shallow waters in regions where major riverine discharge and near-bed tidal resuspension of sediments increase the

turbidity of the water column.

8.2.5 Regional ecosystem types Basin-scale oceanographic processes va ry with shelf seabed and coastal morphology (Warwick & Uncles 1980). These characteristics vary on a regional basis and are the primary determinants of regional shelf ecosystems. In the absence of the effects of fisheries, pollution, or the flux of ant hropogenic materials, a relatively small number of physical factors regulate vegetation types or phytoplankton biomes th at are modified by basin -scale circulat ion patterns and coastal morphology (above). The close coupling between physical processes and the biology of shelf seas enables them to be partitioned into broad regional ecosystem types, which Longhurst (1995) attributed to seven model systems. These systems are presented in Table 8.1 and show the link between regional physical processes, primary production , and then the linkages to other compartments in continental shelf ecosystems (Chapters 1 and 7) . While each of t he ecosystems with in each model displays diffe rences in species composition, there is a high degree of similarity among the ecosystems at higher levels of organization (e.g. primary producers, secondary production processes, top predators) .

In the absence of human intervention through fishing , pollution, or other forms of ecological disturbance, continental shelf ecosystems can be categorized under seven models according to the dominant physical processes and shared ecological features at higher levels of organization. Human intervention can lead to entire regime shifts within these systems in which the species' composition is maintained but the relative dominance of each species changes.

8.3 The seabed habitat and biota While it may be tempting to consider the continental shelf seabed habitat as rather two-dimens ional compared to the pelagic habitat above (Chapter 7) , it is very much a t hreedime ns ional habitat, even though the third d imension, depth, is much more compressed than in pelagic systems. While in pelagic systems the depth dimens ion can exceed several thousands of metres in which biota can be found from the water's surface to just above the seabed of the deep sea. The seabed hab itat is bounded by the depth to which biota can burrow and continue to live (usually no more than 2 m within the sed iment) and the extent to which they penetrate into the waters above (30 to SO m for some of the largest kelp genera such as Macrocystis) (Fig. 8.4) . In some cases the biota are the key constituent of the habitat, as in kelp forests, mussel and oyster reefs, m aerl beds, corals, and sponges. We will deal with specific examples of these habitats later in the chapter (8.7) .

Table 8 .1 Seven models of co nt inental s helf ecosystems giving th eir geographic locality, the principal primary and seco ndary production processes and ot he r key co mpo ne nts and cha racte rist ics at higher trophic levels (adapted from Longhurst 1995).

Model

Geographic location

Primary and secondary production

Higher trophic levels

Model 1

Eastern Siberian and Laptev Sea coasts of Siberia.

Productivity is light-limited, with seasonal cycle symmetrical about local irradiance max imum . Latter corresponds with solar max imum or min imal snow cover.

Benthic invertebrates are abun dant and diverse providing food fo r abun dant but low-d iversity populations of fish and squid. Large euphausiids (krill) , characteristic of open-water regions, are replaced by small Euphausia crystallophorias and provide food for pelagic fish (Pleurogramma spp.) and crab-eater seals.

Polar

irradiancemediated production peak in regions permanently ice -covered

Northeastern and Northern coasts of Greenland . Northern coasts of Canadian archipelago to west Beaufort Sea. Almost entire coast of Antarctica .

Below ice, phytoplankton productivity and zooplankton b iomass are low, but abundant flora in the infiltration zone at th e ice-seawater matrix . Underside of ice < 2 m thick may support de nse growth of d iatoms associated w ith abun dant po lychaetes, copepods, and amphipods.

8.3 The seabed habitat and biota

Model

Geographic location

Primary and secondary production

Higher trophic levels

Model 2

Coasts of Greenland .

Polar irradiance-

North America from Newfoundland to th e Aleutians.

Shallow po lar halocline induces water column stability very early in open-water.

Production exceeds consum ption in the water column and supports rich and d iver se macrobenthos, esp ecially in boreal regions, where shelf areas uncovered by ice are much more exte nsive than around Antarctica. Low-diversity fish fauna, especially in th e Antarctic, where small Nototh enids dominate . The w ider Arctic shelves support a greater diversity of Gad idae, Sebastldae, Anamlcbos sp p. Grey whale, wal rus, and bearded seal are boreal be nthic feed ers, having no austral equivalents.

mediated production

peak in regions where Ice-cover

dis perses partially or

completely in summer, or only wh ere

Northern Asia from Finland

to the Sea of Okhotsk. Short sectors of Antarctic coast in midsummer in

eastern Ross Sea, to east of Ronne ice shelf and in Dumont d 'Urvilie Sea.

broken pac kice develops.

Productivity is light limited , its seasonal cycle being symmetrical about th e local irradiance maximum. Where pack-ice remains, con ditions may resemble Mod el l . After ice -melt, in open water, phytoplankton accumulates during th e period wh en p roductivity inc reases, and then tracks its initial de cline. Phytoplankton is dominated by d iatoms, a subsurface chlorophyll maximum is often observed; in shoal water, significant b iomass of benthic macroalgae develop. Planktonic herbivores are represented by abundant large co pepods, euphausiid s and salps, of which some species form swarms that suppo rt major stocks of baleen whales and seals.

•• • •••• •••• • ••• ••• • •••••• •••••• •••••• •••••• •••••• ••••• • ••• • •• ••• ••••••• ••• ••• ••••••• ••• • •• ••• ••• ••••••• ••• •• • •• • • • •• • • • • • • • • • •• • • • • • • • • • • • •• • • • •• • • •

Mod el 3 Canonical spring-autumn blo oms of

mid-latitude continental shelves

On mid-latitude continental shelves, under th e influence of the global westerly w inds. From Finland to Iberia and off the Mediterranean. From Newfoundland to Florida. Off Tasmania and south ern Australia.

After w inter mixing, a p ulse of productivity and chlorophyll is induced by estab lishme nt of water column stability. Thereafter summer stratification is associated with relatively low productivity. Prog ressive mixing in autumn may induce renewed productivity fuell ed by nutri ents accumulated below the summer pycnocline . This sequence is modifi ed by intermittent windinduced coastal convergence and d ive rge nce, and persiste nt water column mixing in regions wh ere tidal velociti es excee d critical valu e. Effects of est uarine tu rbi dity p lume s may mask th e canonical sequence, which weakens towards th e equator. The balance between pico-autotrophs and larger algal cells is more equitab le than in very high latitud es. In shoal water, esp ecially at high er latitud es (Norway, Iceland, Newfoundlan d, Tasmania) th ere is significant autotrophic p roduction in kelp beds. Small co pepods d ominate the inshore herbivorous plan kton, larger species nearer th e shelf ed ge, often over-wintering in deep water. Their seasonal cycle of abundance follows that of phytoplankton.

Most autotrophic production passes directly or indirectly th rough th e macrobenthos, which is abundant, diver se, and characteristic of each sediment type. Diversity of fi sh fauna exceeds that in polar ecosystems (typically 200 species of >50 families). In boreal regions, major stocks of shoaling Clupeldae and Scom bridae together with mainly de mersal Gad idae, Percidae, and Pleuron ecti dae.

In much more restricted austral shelf regions, dupelds occur as in th e north, together with a more-difficult-to-specify demersal fauna. Energy flow from pelagic invertebrates is mainly to dupeids and scombrids, from be nthos mainly to demersal fis h fauna.

• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • •

Mod el 4

Topoqraphyfo rced summer production

Falklands shelf, the southern North Sea, th e shelf of th e Gulf of Alaska wh ere tidal mixing consistently d ominates the stability of th e water mass, temperate North Pacific where the oceanic permanent halocline passes inshore across the shelf, so constrain ing w inter mixing to water above th e pycnocline. New Zealand and sim ilar locations wh ere, topographicallyforced upwell ing sites in shallow water dominate th e productivity sequence.

The seasonal productivity sch ed ule, otherwise appropriate to Model 3, is instead forced by oth er factors (see adjacent column), d iffering regionally. Consequently, p hytoplankton productivity tends to peak in mid-summer rather than in spring. In many respects the autotrophic biota, and ene rgy flows, are broadly similar to those ap propriate to Model 3 ecosystems.

In many respects th e heterotroph ic b iota, and energy flows, are broadly similar to those appropriate to Mo del 3 eco systems.

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Model

Geographic location

Primary and secondary production

Higher trophic levels

Model 5

The Atlant ic from Iberia

Intermittent production

to Senegal and Gabon to

at coastal

The Pacific from Oregon to Mexico and Peru to southern Chile. The Indian Ocean from Oman to Kenya.

These are th e 'classical ' coastal upwelling regions of easte rn boundary current and oth er coasts, som e of which occur at relatively low latitudes. The shelf is characteristically narrow, and th e influence of river effluents minor.

Bent hic consumers are abundant, but not d iverse, and there is much physical exp or t of organic material into deep basins on th e shelf or across th e shelf ed ge into deep water. Along th e shelf edge, deep -water rockfish (Sebastes) are abundant, characteristic, and diverse.

d ive rgences.

Benguela.

The equator-wa rd com ponent of the Trade winds induces strong and persistent offshore Ekman drift, inducing upwelling of nutrient-rich deep water. This p rocess is usually strongest during summ er. Similarly, in th e Ind ian Ocean th e South-west Monsoon forces offshore drift, principally off Somalia. Upwelling results in a rap id increase in primary production of phytoplankton, principally d iatoms, and chlorophyll accumulation coincides with th e durat ion of upwell ing periods. The biota have low divers ity and high coll ective biomass. Special ized invertebrate herbivores are large calanoi d copepods (typically Ca/anus or Calanoides) , euphausiids and filter-feeding anomuran crabs, each having life history tactics that take th em into deep water, or th e shallow sea-floor, during non-upwelling periods. Kelp forests reach th eir maximum development and generate significant autotroph ic product ion and accumulation of biomass. There is heavy, intermittent settlement of large p hytoplankton cells and faecal material to th e sediments, frequently resulting in an oxygen deficit at certain depths on the narrow shelves.

Anchovies (Engraulis, Cetengraulis) are ubiquitous vertebrate herbivores, w ith in addition, sardines (Sardinella longiceps) in th e Indian Ocean. Populations of predators, mostly pe lagic c1upeids (Sardina , Sardinops) , mackerel (Scomber) , hake (f'v1erluccius, f'v1icromesistius) , sealions, and piscivorous seabirds are characteristic of th ese regions.

............. .................... ...... ...... ... ... ...................... ............. ................ ............. ........ ........ .................. Model 6 Small amplitude response to trade wind seasonality in regions with sign ificant coastal river d ischarge s which d ominate over oceanic processes that would otherwise dete rmine seasonal changes.

Amazon, Niger, Congo, Indus, Ganges, Ir rawaddy, Mekong, and oth ers. These are wet tropical coasts, d ominated by th e effluent of a few major rivers or many smaller river systems. In th e Atlantic, th e Gulf of Guinea, the Guianas, and north ern Brazil. In th e easte rn Pacific, from Columbia to southern Mexico. In the Indo-Pacific, from the South China Sea to south-western India, including much of th e Indonesian Archipelago and th e northern coast of Aust ralia.

Trad e wind regimes force only weak seasonality in mix ed layer depth, observed minor changes represent the geostrophic resp onse of the pycnocline to seasonality in trade wind stress rath er than mi xing. The basin-wide slope of the th ermocline has important consequ ences in th e Pacific and Atlantic Oceans; to th e west it lies deeper than th e shelfedge, but in th e east it is at mid-shelf level. In the east , therefo re, the benthic regime has typical tropical character shorewards of this line, but more temperate characteristics in cool water seawards. On easte rn Atlant ic and Pacific coasts, th e nutrient cline is perennially shallower than th e phot ic depth, except during excep tional events, and vertically-inteqrated production rate is not normally liq ht-Hrnited . Everywh ere, river d ischarges into th e low-salinity surface layer have strong seasonality, reflecting regim es of wet and dry seasons, so that th e seasonal sch edule of p rimary product ion rate is govern ed by nutrient input from th e land and possibly reduced irradiance due to p rolonged heavy cloud cover during wet seasons. Autotrop hic organisms are ty pically small cells, excep t in coastal b looms fu elled by river-borne nitrate, which are dominated by Coscinodiscus and oth er diatoms. The b iomass of coastal subtidal macroalgae is not significant due to water turbidity. Consumers are numerically d ominated by small copepods, but diatom blooms support large stocks of herbivorous c1upeids (Atlantic-Ethma/osa, Brevoortia; Ind oPacific- Sardinella /ongiceps). A large p roportion of d iatom material sinks to the seab ed.

Bent hic community ty pes conform to sediment types, and wh ere th ese resemble those of cool er seas, members of the global suite of benthic infaunal communities occur (e.g. clams such as Venus) . Inshore, orqanic-rich sediments may be exte nsive and support stocks of crustacea dominated by pe naeid shrim ps. These sediments are prone to resuspension by wave action In monsoon seasons. Fish fauna is diverse at all taxonomic levels and includ es a higher p ropor ti on of pelagic sp ecies than in Mod els 3 and 4 at highe r latitudes.

8.3 The seabed habitat and biota

Model

Geographic location

Primary and secondary production

Higher trophic levels

Model 7

In th e Atlantic, only th e Caribbean. In th e Indo-Pacific

Ecosystem of shallow seas off th e coasts of the dry tropics, wh ere river efflue nts are minimal. Many isolated islands and archipelagos in tropical seas are surround ed by reduced Mod el 7 ecosy ste ms, of which th e dominant characteristic is th e d evelopment of coral reefs where topography pe rmits, elsew here unconsolidated sediments are dom inated by carbonate sand.

The macrobenthos asso ciated with coral ree f fo rmations is exceptionally diverse at all taxonomic levels.

Small amplitude

res ponse to trade w ind

seasonality in regions off

dry coasts with relatively . . rnmor river

discharges.

parts of the Arabian Sea, the Red Sea, north-east Australia , and of the Indonesian archi pelago.

There is w eak seasonality in mixed layer dept h, and nutrient clin e is usually shallower than th e photic depth, except during excep t ional events. Most p rimary production occurs in the benthos. Macroalgae (Sargassum) , encrust ing coralline green (Halimedia) and red algae, cyanophyte mats and sea-grass meadows dominate community p roduct ion, in addition to th e activity of symbiotic dinoflagellate s within th e tissues of many invertebrates: scleractlnian corals, giant clams (Tridacna), co elenterates (alcyon ians, anthozoans, and scyphozoans), large ascidians and encr ust ing sponges. Nutrient sources and fluxes are various: advection, upwelling, vertical flux in fractured basement rocks, some terrestrial runoff. Nitrogen-fi xing bacteria occur in the tissu es of some corals, and cyanobacteria fix nitrogen w ithin algal mats. Internal exchange s of nutrients within and between organisms is highly compl ex. Export from th e benthic ecosyste m, exc ept in th e form of carbonate ero ded to sand and gravel factions, is a small but complex flux.

On open sandy sediments, unencumbered with reefs, very high densities of filterfeeding crabs (Pinnixa, Xenophthalmus ) are typical, together with oth er organ isms, especially filterfeeding clams. Fish fauna is also diverse, both taxonomically and functionally. Parrot-fish (Scaridae) are among th e most important herbivores, directly consum ing coralline and oth er algal mats, and these may fo rm a large-fraction of total fish b iomass. An intense and complex network of trophic links betwee n fish and benthic invertebrates is characteristic of this ecosyste m. This trophic complex supports a w ide variety of large predators.

Water clarity is high, and p hytoplankton is d ominated by th e plco- and nano-fractions, as in oligotrophic ocean ecosyste ms. These are consumed by protists and small zooplankters th emselves th e p rey of many filter- and tentacular-feedinq polyps of corals and oth er co elenterates.

Body size affects bot h production processes and the degree to which biota are associated with particular h abitats (see also Chapter 4). The body size of animals living in the seabed is affected by burrowing ability and constraints on respiration due to oxygen exchange. The body size of attached biota that inhabit the surface of the seabed are constrained by physical processes, suc h as shear due to curre nt velocity. The degree of mobility of the biota (i.e. their life mode) varies from those organisms that are firml y cemented to a substratum, to anemones that are able to reposition themselves by a few mm per day, to highly mobile crabs and fishes that migrate tens or hundreds of kilometres every year. The mobility of the biota affects their ability to respond to environmental change and places a constraint on the extent and range of habitat that can be utilized.

8.3.1 Body size and position The m ajor groupings of an imals based on body size are macrofauna, meiofauna, and the microbiota. The meiofauna are usually de fined as those organisms that would pass through a sieve with a mesh diameter of 0.5 mm but that would be retained on a mesh of 0 .063 mm. The meiofauna are the least well-stud ied, yet probably the m ost diverse, group of m arine organ isms that can be observed directly using light microscopy (Lambshead et al. 200 1). Anything larger than this is termed the m acrofauna. The small body size of meiofauna means that their rates of production (how much biomass is gene rated wit hin a given time ) is much higher than for the larger m acrofauna. Accordingly, meiofaunal population responses to environmental and human disturbances can occur within days and weeks , which make them excellent indicators of environmental stress (e .g. pollution, physical disturbance). Most

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

(bJ

(II

•

Figure 8.4 The three-dimensional extent of the seabed habitat will vary considerably depending on the hardness and stability of the seabed. Rocky substrata provide a firm and stable anchorage for many animals and plants such as kelp, soft corals, and sponges. The stability of this substratum means that often these animals are able to attain much larger body sizes than similar or the same species found in less stable habitats (a). Very few organisms can penetrate bedrock. Substrata that are composed of particles can vary considerably in stability from bedrock to fine muds and clays. Even the largest and heaviest particles can become mobile in certain sea conditions. Boulders provide interstitial spaces that act as refugia and provide a firm anchorage for epibiota. As particle size decreases, so the ability of animals to penetrate into the sediment increases until in the softest sediments it is limited only by the depth to which oxygenated water can be circulated into burrow systems. On mixed sediments (gravely shelly sands) the upper size of epibiota is constrained by near-bed currents (animals that grow too big will be sheared off the seabed) leading to adaptations such as a flattened body form (b). However, softer sediments like mud tend to have a less diverse array of emergent epibiota and are usually limited to soft bodied animals like anemones and sea pens (c).

research has been devoted to the study of macrofauna due to their amenability to experimental and observational studies. Nevertheless, the contribution of the microbiota (dinoflagellates, diatoms, bacteria) to biomass and production in coastal seas is often under-represented, and in the tropics can considerably exceed that of meiofauna and macrofauna combined (Fig. 8.5; see also Chapter 3) . Body size and longevity is also an important determinant of the rate of recovery after a disturbance has occurred. Small animals recolonize areas of disturbance via larval recruitment on a scale of days or weeks, whereas increasingly larger or slow-growing biota can take many months or years to recolonize and attain their former biomass. The most extreme example of the latter would be slow-growing deep-water corals found on the continental slope edge or on seamounts (Chapter 9) or maerl (calcareous algae) beds (Hall-Spencer & Moore 2000) .

the substratum. In some cases calcareous algae form their own unique biogenic habitat, these maerl beds harbour a high diversity of biota due to their complex structure. Infaunal organisms live buried within the substratum, either entirely (such as free-burrowing polychaete worms and heart urchins) or partially. Examples of partially buried infauna include burrowing shrimps, which build gal-

-• -=~

c

e

•• =

-=~ • -= = -

7 6 5 4 3 2 1 0

Bacteria

Meiafou na

Macrainfauna

Epifouna

Bacteria

Meiafou na

Macrainfauna

Epifouna

50

40

.... 30 c

'6 20

Despite th eir cont ribution t o benthic production and diversity, meiofauna and the microbiota are the least well-stud ied size-classes of marine biota.

The biota can be categorized according to their relative position within or on the seabed. Epibiota are those emergent organisms that are anchored in or upon the substratum (e .g, corals, anemones, hydroids) or those free-living organisms that move about on the surface of the substratum (e .g, gastropods, starfish, crabs, fishes) . Macroalgae are almost exclusively epibenthic and grow attached to

~

c

~

10 0

Figure 8.5 Estimates of mean biomass and production of different size classes of benthic biota in the Gulf of Papua, northern Coral Sea (Alongi, D. M. & Robertson, A. I. 1995. Factors regulating benthic food chains in tropical river deltas and adjacent shelf areas. Geo-Marine Letters

15:

14~ 152.

Copyright Elsevier 1995.)

8.3 The seabed habitat and biota leries within the substratum but emerge periodically to forage for food or mates, or burrowing sea cucumbers that live within the sediment and extend feeding tentacles onto the sediment surface . In very shallow subtidal areas with good illumination at the seabed, unicellular diatoms and dinoflagellates contribute to the microbial community, and along with cyanobacte ria and bacteria, inhabit the

interstitial spaces between sedime nt particles (Paterson & Black 199 9 ) (Box 8.2). The microbiota have an important influence on the cohesive properties of the sediment through the production of extracellular organic secretions that modify flow and other important ecosystem functions such as nutrient exchange.

Box 8.2: Current flow over the seabed Smooth turbulent flow

Rough turbulent flo w Freestream No laminar sub-layer

logarithmic layer

lam inar sub-layer Microbial infillin g

Cohesive

Non-cohesive

Mussels lmreese turbulent flowbuyincreasingsurface topographicrelief

Hydrodynamicallyrough

The fi gure shows the impact that microb ial organisms can

present it significantly affects the flow of part icles and

have on flow over the seabed by inf illing the gaps between

nutrients to and from the bed. The bi ological significance

sedim ent part icles to create a 'smoother' surface. A rough

of the physics becomes clearer w hen we consi der the

bed w ill experience greater stress for the same overall

cons equ ence of animal growth on the seabe d. Mussels

flow than a smoot h bed. This has important consequ ences

settlin g onto a smooth substratum will increase t he sur-

for plants and animals living at the sed iment surface. Under

face complexity of the bed making it 'rou gher'. This in tu rn

rough , t urbulent conditions, turbulent eddies are formed

will increase turbulent flow over the seabed. The t urbulent

th at impact the bed and increase the likelihood of erosion

flow breaks down the boundary layer and encourages a

of the sed iment and resid ent bi ota. Under such condi-

downward transport of phytoplankton from the layers of

t ions it is not possible for t he viscous laminar sub-layer

water above, encou raging further growth and an increase

to form. This is someti mes termed the boundary layer,

in the rough ness of the bed. Paterso n, D. A. & Black, K.

wh ich acts as a hydrodynamic and molecu lar buffer zone

19 99 . Advances in Ecologicol Research, 29: 15 5-1 9 3 .

between the bed and the flow above. When th is layer is

Copyright

© Elsevier 19 9 9 . 2

--

E

3 l= =L

6

~ ~ ~

--•

0 0

0

~

4

~

>

--0

~

~

~

• 0

0

0

The image represents the chloro-

3

0

5

Phytoplankton depleted bymusselfiltration withtime

'15

-

6

~

~ ~

-0 0 0

~ ~

0 0

~ ~

Q

0 11.00

7 12.30 Time (hi

phyll a (food for mussels and other filter-feeders) profile in a body of water followed across a mussel bed over a 1.5-h period . Within 1.5 h nearly a third of the plankton was removed from the entire water column. Water height rises from 11.00 to 12.30 with the incoming tide. (Image: J. Gascoigne.)

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

8.3.2 Life mode and mobility of biota The sessile components of the benthos are more closely associated with the composition and physical characteristics of the seabed and show seasonal growth followed by periods of winter dormancy at higher latitudes. This is true both of macroalgae and particularly of colonial animals, such as hydroids. In contrast, much of the epibenthos exhibits varying degrees of mobility from crawling gastropod molluscs and starfishes to highly mobile fish. Despite their apparently slow speed, starfish are known to occur in dense feeding aggregations. which move slowly and systematically across the seabed. consuming animals in their path. Where these 'swarms' coincide with commercial shellfish beds they can cause severe economic losses for cultivators. Many crabs (e.g. Cancer pagurus and Maja squinado) move inshore in the spring and summer where mating occurs. often in dense aggregations, followed by a movement into deeper offshore water during the winter months to avoid wave action and severe decreases in nearshore water temperature. Sessile biota show seasonal patterns of growth and dormancy at hig h latitudes, while mobile epifauna exhibit varying degrees of inshore/offshore movement in response to water temperature. Inshore migrations of many decapods (crabs and lobsters) coincide with mating aggregations.

The distribution of bottom-dwelling fish can be linked strongly to certain habitat types within regional seas, particularly when associated with specific habitats such as

reefs or kelp beds. However, in regions where sediments predominate at mid to high latitudes, fish species are often associated with a range of sedimentary habitats that may vary from fine sand to gravel as in plaice (Pleuronectes platessa) (Kaiser et al. 1999a; Shucksmith et al. 2006) (Fig. 8.6) . Such variation in habitat use can be attributed to different behavioural characteristics at different life-history stages. Juvenile plaice are strongly selective of specific sediment grain sizes, as this determines their ability to burrow into the substratum to evade predation; however, adult plaice are released to some extent from predation pressure (apart from fishing) and utilize a wider range of habitats (Gibson & Robb 1992; Shucksmith et al. 2006). Some species make extensive spawning migrations (Box 8.3) . For example, plaice in the eastern English Channel migrate hundreds of kilometres to reach spawning grounds in the North Sea and show activity patterns that utilize the prevailing tidal currents to reduce the energy expended during the migration (Metcalfe & Arnold 1997). Other fish, such as bass (Dicentrachus labrax), undertake seasonal migrations that track the rise and fall of seawater temperature as they require a minimum seawater temperature of 9°C for ovary maturation to occur. Typically, stocks move north from the coast of France and up through the English Channel and Irish Sea in late spring, returning south in the late autumn with falling water temperature. However, over the past decade there is a stronger tendency for bass to over-winter in waters where previously they were only transient. This change in behaviour is directly linked to increasing seawater temperatures and has also extended the range of this species further north.

Figure 8.6 Fish show high habitat affinities when the habitat is structured, as in reefs or kelp beds. However, fish associated with sedimentary habitats tend to be less closely associated with a specific habitat and may occur across a wide range of sediment types at different stages of their life history. Here an adult plaice is photographed on a uniform

sandy habitat (a), while fish such as this red gurnard (b) are more closely associated with highly structured habitats. The inset maps show the position at which each of these photographs were taken and highlight great spatial variation at

scales of 1-Skm.

8.4 Functional roles of the biota

Box 8.3: Migration in continental shelf seas or;-.,-------;:------: Sea surface

20

-

..

E

(urrent direction

.- --. 5 N

Plaice are normally bottom-dwelling fish that spend much

day. When the tidal stream flowed in a northerly direction

of their time buried in the sediment and, althoug h they

towards the spawning grounds, the fish was seen to swim

are widespread, they show temporally stable patterns in

up into the water colu mn where it swam with the current

distribution, which is stro ngly associated wi th the environ-

When the t ide t urns in the opposite di rection, the fish

mental characteristics of the seabed habitat (Hinz et al.

descends to the seabed where it waits for the next turn

2003). However, plaice also unde rtake extensive move-

of the tide. By adapting its behaviour to take advantage

ments to thei r spawning grounds. The data above were

of the prevailing current, plaice are able to move several

obtained during a study in which a plaice was tagged wi th

hundred km in less than a week (redrawn from Metcalfe

data loggers that recorded the fish's depth throughout the

et al. 2002).

8.4 Functional roles of the biota As in all biological systems, the continental shelf seabed community has representatives that can be categorized accord ing to what they consume (predators, scavenge rs, herbivores, filter feeders, suspens ion feeders) or what they do to the physical structure and processes within the habitat (bioturbators, eco-engineers).

8.4.1 Predators and scavengers Most animals in continental-shelf systems are highly flexible in terms of their feeding strategy. Nearly all predators will also scavenge carrion; for example, fish (d ab, Limanda limanda ), starfis h (Asterias ru bens), decapods (Cancer irrorat us), and gastro pod snails (e.g. whelks, Bue-

cinu rn undaru rn). Even herbivorous sea urchins (e.g. Echi-

nus esculentus ) and suspens ion feeders such as brittlestars (e .g. Ophiura ophiura, Ophothrixfragilis ) are known to feed on carrion from time to time. These animals are known as facultative scavengers. There is some controversy as to the possible existence of obligate scavengers, i.e, animals that consume only carrion, but it appears possible considering the physiological energetic constraints . The most likely candidates would seem to be sm all (< 6 mm long) lysianassid amphipods of the genus Orehomene, wh ich appear to specialize in the consumption of crustacean carrion. This group of amphipods show m any specialist adaptat ions to a scavenging lifestyle, such as the ability to survive extended periods without food and to gorge on carrion such that their body size increases by up to 500%. However, a convincing experimental demonstration of an obligate scavenging lifestyle remains elusive (Ruxton & Houston 2004) .

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Many consumers at high latitudes exhibit multiple feeding modes and often resort to scavenging when carrion is available-t hese are facultative scavengers. Carrion is

more likely to occur at high latitu des where physical processes are a significant source of natural mortality.

The existence of a purely scavenging (obligate) lifestyle remains speculative in cont inental-shelf systems. If they

occur, obligate scavengers are most likely to be fo und

among t he small-body-sized scavenging amp hipod fauna.

8.4.2 Grazers Grazing animals include herbivorous fishes, such as some blennies (Blenniidae), sea breams (Sparidae), gastropod molluscs, and sea urchins, all ofwhich playa key role in the maintenance of diversity within algal-dominated communities. Herbivory in fishes is much more prevalent towards lower latitudes, while at higher latitudes herbivores are primarily invertebrates. In systems in which a particular species or guild is the predominant grazer. they can have a keystone or eco-engineering role on the habitat through their consumption ofcertain types of algae. Grazers are not the only eco-engineers, as we will see a little later (8.5.1). Grazers also include carnivores such as nudibranch molluscs (sea slugs) that consume encrusting bryozoa, soft corals. and sponges by scraping at the colonies with their radula. Some of these associations may be very specific; for example, the sea slug Tritonia hombergii graze dead men's fingers (Alcyonium digitatum) and may be one of the few predators of this soft coral. Many of the external morphological features of bryozoa (spines) and the extracellular products of sponges and soft corals act as defence mechanisms against the predatory activities of sea slugs, which has developed into an 'evo lutio nary arms race' between predator and prey. The development of comp lex ornamentat ion in gastropod shells is a stro ng evol utionary driver of cheliped morphology (claw design) in snail-eating crabs and is a classic example of the 'evolutionary arms race'.

8.4.3 Particle feeders Filter feeders such as oysters. mussels, and clams extract phytoplankton from the water column and suspended matter from just above the seabed (su spe nsion feeding) . An individual animal of 1 g ash-free dry weight is estimated to filter 57litres of water per day (Heip et al. 1995). Con-

sequently, filter feeders have an important role in bentho-pelagic coupling as they process phytoplankton and suspended organic matter into faeces and pseudofaeces, which are deposited on the seabed. This material is rich in organic matter. which is processed by the microbial community and in turn feeds suspension feeders such as clams (e.g, Mya truncata), and bulk sediment processors such as irregular sea urchins (Echinocardium cordatum), sipunculans, and polychaetes. Bryozoa, hydrozoans, sponges, and anemones are particle feeders; although there is some evidence that the latter two animal types can also absorb dissolved organic matter through their body wall as a supplementary food source. These groups are more prevalent in deeper water than filter feeders that rely upon a supply of phytoplankton. Indeed, there is a strong negative relationship between depth and filter-feeder biomass, declining down to 50 m from 3 to 0.2 g carbon m-2 for the North Sea (Bryant et al. 1995). Biomass is somet imes calculated as the dry weight of living tissues (including shell material) minus the ash remaining after combustion , i.e. ash-free dry weight.

Pseudofaeces are the means by w hich filter-feeding biota rid themselves of indigestible or rejected particles. These particles are bound in mucus secreted by gill tissues. M ucus production requires energy expenditure and is one reason why filter feeding ceases when suspended sediment loads become excessive.

8.4.4 Bioturbators Animals can have both a stabilizing and a destabilizing role within sediments. Palaeoecologists have studied in great detail the manner in which live animals perturb sediment structures. This has given them insights regarding the likely agents of trace fossils that have recorded the passage of animals through or across sediment habitats. A seminal publication by Schafer (1972) describes in detail the different modes ofsediment disruption that occur as a result of animal activities. These vary from the surface bulldozers. such as irregular sea urchins and gastropods, to the feeding pits of starfish and elasmobranch fishes such as rays, to the burrow labyrinths and chambers created by burrowing crustacea (Box 8.4 and Current Focus) . The cumulative effects of these animal related sediment disturbances are known as bioturbation.

Bioturbators have left their mark in fossilized sedimentary rocks. These are termed trace fossils.

8.4 Functional roles of the biota Bioturbators perform a key role in seabed systems as they enhance the passage of oxygenated water deeper into the sedime nt than it would ot herwise penetrate by passive diffusion between sed ime nt particles. Increases in surface sediment porosity have been found in association w it h the deposit-feeding bivalve Yoldia limatula and at a depth of 9-12 cm as a result of the deposit-feeding activities of the polychaete Heteromastus fi liform is (Mulsow et al. 2002) . The physical movements of these animals as they feed and reposition disrupts sedime nt structure and thereby

Box 8.4: Influence of fauna on sediment structure

increases sediment porosity. The depth and complexity of the burrow structures vary considerably among different species and can vary in depth from a few centimetres to metres (Jones & Jago 1993). These burrows can extend well into the deeper layers of the sedime nt that are characteristically coloured black due to the bacterial production of hydrogen sulphide (H,S) in the absence of oxygen. The burrows themselves increase the surface area available for oxygen and nutrient exchange that enco urages enhanced microbial activity on and in the burrow walls. For example,

(0)

(a) Callianasid shrimps live in soft muddy/sand sediments and create intricate sub-sediment passageways. Apart from the burrow entrance there are other connections to the sediment surface that emerge within sediment mounds that act as chimneys on the seabed. These chimneys cause water to accelerate as it passes over the mound , which draws water within the chimney out. This causes the water within the burrow system to move through the passageways and thereby encourages new oxygenated water to be drawn into the burrow system. The shrimp store food and 'garden' microbial activity inside chambers. (b) Echiuran worms use their highly extendable proboscis to gather surface sediment matter at great distances (150 cm) from the entrance of their burrow. Once the sediment has passed through their gut it is expelled in a faecal mound. Echiuran burrows are often inhabited by lodgers such as blennies and scale worms.

(c) Feeding pits are excavated by starfish while trying to consume a burrowing sea urchin (photograph: James Perrins).

(b)

Chapter 8 Continental Shelf Seabed •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

the brittlestar (Amphiurafiliform is) occurs in densities as h igh as 70 0 m? in Galway Bay, Ireland. The burrow s con structed by such a high d ensity of a nimals can expose 1.4 m 2 of burrow w all m- 2 of the seabed (Solan & Kennedy 20 03 ) .

Sediment conveyors, suc h as callianassids and ech iu ran worms , transfer surface sed ime nts to deeper layers wit h in the sed imen t, w hich results in a pe ak in ch lorophyll

a concentration that is greater than that at the sed ime nt surface . Branch an d Pringle (1987) found that ch lorophyll

a concentration was greatest at a depth of 15-25 em in the presence of Callianassa kraussi. At this depth the sub-surface sediments are reworked by burrowing animals such as urchins (Echinocardium corda t um ) an d polychaetes such as Scoloplos armiger, w hich ingest sed imen t from w hich they digest organic m atter an d bacteria . These processes recycle minerals and nutrients w hen the y a re transferred to the surface o f the seabed as sed imen t m ound s and faecal pellets. Bioturbators increase the complexity of the surface of the substratum through the creation of pits and mounds and enhance the exchange of oxygen and nutrients across burrow walls that occur to a depth of up to 2 m in the sediment.

Sed imen t conveyors m ake a sign ifican t con tr ibu tion to the resuspension of sed imen t in the overlying water colu m n and influence seabed topogra phy. Rowden et al. (1998) und ertook both laboratory a nd field trials u sing the mud sh r imp (Callianassa subterranea) and found that sed imen t reworking va ried with temp erature and h ence season. They estimated a n a n nual sed imen t turnover budget o f 11 000

CURRENT FOCUS: Estimation of ecosystem functioning in sediments

g (d r y weigh t) m? yr ' . Field observations a t a site in the Nort h Sea demonstrated that the sediment expelled by the mud sh rim p formed unconsolidated volcano-like m ounds, w h ich sign ifican tly m odify seabed su rface topography. Ca llianassa subterranea's m aximum con tr ibu tion to sediment resuspension results in a lateral sed imen t transport r ate of 7 kg m' month:". Thus, mud sh rim ps n ot on ly re work sedim ent d ee p w it h in the substratu m bu t are also important d eterminants of the rate of sed imen t exchange between adjacen t sed imentar y h abitats. Ech iu ran wor ms are a bu ndant bioturbators of mud sedim ents. However they are extremely d ifficu lt to stu dy in laborator y stu d ies due to their fragility, an d the y a ppear to be relatively immobile once established. Hughes et al. (1 99 9 ) studied the rate of sedimen t ejection by the ech iu ran worm Maxmuelleria lankesteri in the field. They found that burrows and sed imen ts persisted throughout the I -year stud y period a nd that worms ejected sediments year round . The m ean ejection rate was 2748 g burrow-' y ' . The su perficial sed imen t, on w hich M. lankesteri feeds, was ve r y r ich in organ ic matter, w ith m onthly valu es of a pproximately 12-17% sediment dry weigh t . Ejection rate remained con stan t at labile fractions of organic matter below - 50% , bu t increa sed sh ar ply a bove this threshold, so sedimen t ejection rate increased w ith increa sing food qu ality. Bu r rows a ppeared to be static an d individual ejecta m ounds cou ld persist for longer than a yea r. Th is is qu ite different to d eepsea ech iu ra for w h ich changes in burrow m orphology are more frequent and prob ably relate to the higher quantity of labile organ ic m atter on the con ti nen tal shelf.

BPj is the community bioturbation potent ial at sampling pointj, estim ated as the sum of the products of the sedi-

Mixing of marine sediments by the resid ent fauna is an

ment reworking mod e for each species i (R) and its ash-

important ecosystem function (Naaem et al. 2002) that

free dry mass (AFDM ij ) . Sj is the observed number of

increases the penetrat ion of oxygenated wa ter d eeper into the sediment than w ou ld occur w ithout these fauna.

species (speci es richness) at sampling point j. Sed iment reworking mod es (R) are defined in a number of reviews

Thus sediments w ith a high biomass of fauna that mix sediments w ill enhance biological production of micro-

(e.g. Solan et al. 2004 ; Michaud et al. 2006) . R, values ranged from - 1 (for sediment stabilizers) to 4 (for sedi-

bia l, mei ofaunal , and macrofaunal biota. Different species wi thin an assemblage w ill affect the sediment to a

ment regenerators). We can relate the bioturbation potential of an assem-

greater or lesser extent depending on their feedi ng mode

blage of organisms by quantifying the sediment mixing

or lifesty le (e.g. active burrower versus sedentary deposit feeder). It is possible to est imate the b iot urbation poten-

depth using a sediment p rofile imag ing camera (SPI)

tial for the speci es sam pled at an individual sampling point

mounted above a prism contain ing distilled water with a

according to the followi ng equation (Solan et al. 2004) :

side-mounted tran sparent Perspex plate. As the prism is p ushed into the sediment it is possible to obtain a pho-

s,

BFj =

L ;=1

(Rhoads & Cand e 197 1). The SPI consists of a ca me ra

R, ' AFDMij

tographic image of a vert ical transect of the sediment. The resulting image can be analysed wi th image-analysis

8.5 Food webs in shell systems

reduced sediment fracti ons, using a standardized pixel intensity th reshold.

software. The image is partitioned into layers of binary images, from which it is possi ble to separate oxic and (b)

1·1

18 16 _14 E -"-1 2 g-lO

18 16

E 14

-

•

.:.0 8

••

:!-: , 0

2

•

I

•

.• j •

•

- ~-! 12 fi

•

•

""-

ca 6 4 2 0

( SO m, but it has also been pointed out that such scars may increase in size as the whale grows. However. there appears to be an even bigger species, the 'colossal' squid Mesonychoteuthis hamiltoni, a specimen of which was caught in 2003 from 2000 m off New Zealand (http:/ /www.tonmo. com/science/publicigiantsquidfacts.php) . Why do giant taxa exist in the deep sea? Several theories have been produced, including links to the metabolic effects of great hydrostatic pressure and cold. the differences in dissolved oxygen levels (see 12.9), delayed onset of sexual maturity. and indeterminate growth-organisms live a very long time and continue growing. Other ideas relate to the method of food capture. and perhaps have a clearer evolutiona ry route. For example, giant scavenging amphipods could be an adaptation to a foraging strategy where high motility is needed to locate sparsely dispersed food. However, we are still not clear how, or why, animals often living in extremely oligotrophic areas become so large.

9.5 Hydrothermal vents-> islands in the deep sea Thirty years ago, practically all deep-sea ecology was focused on the comparatively featureless deep-sea bed and our impressions ofdeep-sea life were therefore determined by this image. However, discoveries over the last couple of decades, through the use of submersibles and more intensive acoustic mapping, have demonstrated that the ocean basin is not a continuous. featureless floor but within these plains are a series of other features that have exciting, unique, and often diverse communities: islands in a sea of mud. Most are based on unusual outcrops of hard substrate that have been formed by different means, and include sea mounts (De Forges et al. 2000) and deep-sea coral reefs (Hall-Spencer et al. 2002; Fig.9.2c) . However, the most dramatic and unusual island communities are associated with hydrothermal vents.

9.5.1 What and where are hydrothermal vents? Hydrothermal vents are associated with parts of the ocean floor that exhibit high levels of tectonic activity, such as the spreading axes of plate formation (mid-ocean ridges), and vent clusters have been given evocative names such as 'Rose Garden' and 'Snake Pit'. The first vent was observed in 1977 on the Galapagos Rift (Pacific) from the submersible Alvin (Fig. 9 .3a) by a team including Bob Ballard-the man

Figure 9 .18 (a) A black smoker. (b) A dense aggregation of ventimentiferan tubeworms (Riftia) near a hydrothermal vent. (Copyright: NOAA.)

Chapter 9 The Deep Sea •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

behind the rediscovery of the Titanic. The system was found by 'chance' when investigating temperature anomalies in surface waters. Within such regions, hot magma chambers occurnear the seabed and heat up water that has permeated into the ocean floor; water temperatures above lOQOC are possible due to the high hydrostatic pressure that prevents waterboiling. This superheated water erupts back out ofthe seabed carrying with it a rich cloud ofminerals, such as sulphides, methane, manganese, and many other trace metals. The vent therefore often appears as smoke emerging from a chimney formed by mineral deposits (Fig. 9 .1Sa) . The hottest, and most dramatic, type of vent is therefore termed

'black smoker' due to the colour of the plume, and water temperatures within the plume can be up to 350°C. 'White smokers' also exist, which tend to be a little cooler. and in some areas hot water escapes through cracks and crevices in the seabed to form diffuse vents with water temperatures much lower than the smokers. Hot emissions from smokers are rapidly mixed in the cold deep-sea. so most vent animals generally live in water temperatures close to the ambient of 2°C (the plume water also contains no oxygen), though there are astonishing exceptions, such as the polychaete worm Alvinella pompejana (or Pompeii worm; Fig. 9 .19), which forms burrows on the vent chimneys (Cary et a1. 1998) . Water temperatures within the worm burrows measured by Alvin were found to average 6SoC, with frequent spikes up to 81 °C. Pompeii worms emerge from burrows to feed on filamentous bacteria and have been known to survive short exposure to 105°C! Alvinella is the most thermotolerant eukaryotic organism known.

9.5.2 Production at hydrothermal vents Hydrothermal vents are exceptional among deep-sea islands, and vastly different from the rest of the deep sea, in having a huge biomass of associated organisms (Fig. 9.1Sb) . Clearly, alternative methods offood supply are sustaining these communities. and this production is autochthonous and related to the supply of reduced compounds (particularly sulphur compounds) emerging from the vent. Vent assemblages are sustained by primary production generated by bacteria through chemosynthesis (Box 9.2) and considered of little importance until recently, when vents were investigated. Chemo-autotrophic bacteria are present in hydrothermal fluid and tend to be members of the most ancient Archaea. These can tolerate exceptionally high temperatures and are therefore either known as hyperthermophiles (SQ-115°C) orthe most extreme superthermophiles (> 115°C) . Bacteria are also free-living in the vent environment, such as the filamentous bacteria fed upon by Alvinella, and thus provide a continually replaced food supply for vent animals. However, the comparatively large biomass associated with

Figure 9.19 The Pompeii worm (Atv/nella popejana}-the most thermotolerant multicellular organism on Earth?

(Copyright: Nature.)

vents is not primarily explained by production offree-living bacteria, but through chemosynthetic, symbiotic bacteria that live within the vent invertebrates. A group of animals unique to vent environments has therefore evolved that relies upon a symbiotic relationship with bacteria.

9.5.3 Classic vent animals Probably the most striking examples of this dependence on symbiotic organisms are the large vestimentiferan tubeworms characteristic of vent communities in the Pacific (Fig. 9. I Sb). Previously these worms were classified within another unusual worm group, the Pogonophora, then given a phylum of their own (Vestimentifera), but through molecular analysis are now known to be highly developed members of the Polychaeta. The 1 to 2 m long worms, such as Riftia pachyptila, live in white tubes attached to the vent surrounds (15 to 20°C) with a red tentacular plume extending from the tube, which can be retracted quickly when disturbed. While superficially the worms look like normal, if large, tube-dwelling polychaetes feeding on particulate material, they have two strange anatomical features: they completely lack a mouth and digestive system and they have a specialized organ (tro ph o som e) that houses che-

9.5 Hydrothermal vents

islands in the deep sea

•••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

mosynthetic bacteria deep within the animal's body; bacteria compose up to 50% of the weight of the worm. Riftia relies on bacteria for its organic carbon supply, the plume of tentacles is used to uptake other nutrients from the surrounding environment. Other key components of the vent fauna are large, white bivalve molluscs, which form extensive clusters in cracks and crevices around smokers and other vents. These are typified byrwo genera: the giant clam (Calyptogena; Fig.9.20), which can grow up to 26 ern, and the vent mussel (Bathy modiolus). These molluscs also house symbiotic bacteria (in cell vacuoles rather than a specific organ), which supply the majority of the bivalve's organic carbon needs. Calyptogena takes in ambient CO2-rich water over the gills through siphons, while its foot extends into the crevice where it lives in order to exploit warm sulphide-rich vent fluids. The other major group present on vents are decapod crustaceans. which scavenge off other vent animals rather than having endosymbiotic bacteria. Squat lobsters are common. but Pacific vents also have associated crab species (e.g, Bythograea thermydron ; Fig.9.20) that are key members of the vent food-web but comparatively uncommon anywhere else in the deep sea due, perhaps. to the planktonic larval strategy generally adopted by the group. How this species has colonized and adapted to life on vents is therefore an interesting question, but it would appear that larval stages of the crab remain in the vicinity of the vent. Like shallow-water crabs, large numbers of eggs are produced, but first-stage zoea of Bythograea have been captured in plankton tows of bottom water over vents rather than at the surface thousands of metres above. However, the most remarkable feature is the megalopa (settling larval stage), which is enormous compared with shallow-water crabs (5-10 cm carapace length) and common in both water overlying vents and within clumps of Riftia where they appear to take refuge.

Vestimentiferans are classic features ofPacific vents. but in the mid-Atlantic (whose vent systems have a very different fauna to the Pacific), the dominant animal is often a species of shrimp (e.g, Rimicaris exoculata; Fig.9 .20), which can form huge swarms around hydrothermal vents. These shrimps are characterized by large, paired dorsal eyes that can extend halfway down the midline of the shrimp; the shrimps do not possess normal eyes and eyestalks. It has been proposed that Rimicaris can detect thermal radiation emitted from hot vent fluids, thus enabling the shrimp to navigate around the vent without being cooked. While the tubeworms, bivalves, and decapod crustaceans are the most prominent groups associated with vents. most other taxa are also represented, particularly sessile and sedentary animals. such as sponges and anemones. Few fish species are found only in vent habitats. an exception being the well-named Thermarces, which has aspects of its biochemistry adapted for high temperatures as well as high pressure. The fish appears to feed on the abundant swarms of amphipod crustaceans (Halice) that can reach densities of > 1000 1-1above lower temperature vents! The exact composition of vent assemblages and the relative position of species at a vent seem closely related to the chemical speciation within the vent water (Luther et a1. 2001) . Significant differences in oxygen, iron, and sulphur speciation are correlated with the distribution of taxa in different microhabitats.

9.5.4 other types of vent and seep Not all chemosynthesis-based communities in the deep sea rely on hot-water vents and distinct assemblages have been discovered associated with other conditions, where a suitable concentrated source of nutrients is available. Most of these are termed cold seeps; for example. where oil leaks onto the sea floor from underground reservoirs.

Figure 9 .20 Examples of organisms associated with hydrothermal vents. (a) The giant vent clam Calyptogena (Photo taken by Richard A. Lutz). (b) Swarms of shrimps (Rimicaris) around vents in the North Atlantic (© Missao Seahma, 2002 (FCT, Portugal PDCTM 1999MAR15281) w/IFREMER).

Chapter 9 The Deep Sea •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

These communities are often dominated by the bivalves that have symbiotic relationships with chemosynthetic bacteria. The deepest chemosynthesis-based community so far discovered is at 7326 m in the Japan trench (Pacific) and is dominated by the bivalve Maorithyas hadalis (Fujikura et al. 1999) . At this site, as in other trenches, the assemblage is sustained by chemosynthesis using the high sulphide content of the sediment associated with the geologic fault . A large deep-sea oil 'lake' exists on the sea floor in the northern Gulf of Mexico. The lake is ringed by deep-sea bivalves, which can cluster so closely that individuals get pushed into the lake-with fatal consequences.

2.5

-" ~

~

0

-.'" ~

(oj

Riffio pochypnlo

0

2.0 0

1.5

0

:E

8 o o

1.0 0.5 0 2.0

-~

1

3

2

Bothymodiolus thermophilus

(bJ

"

1.5

'2>

0 0

.'"~

9.5.5 Dispersal and gene flow in vent •

orgamsms

0

1.0

. ____ 0 - -

__ A - - - - - - - -

:E

~

",03.

0.5

Most vent organisms are uniquely associated with vents or seeps, and a feature of vent fauna is the number of endemics, many with ancient lineages. The persistence of ancient taxa has led to suggestions that vents have been compara-

tively immune to major planetary extinction events. as they are only indirectly dependent on the sun. However. hydrothermal vents are comparatively temporary in nature as the Earth's crust will move over the magma chamber and the vent will 'die'. Observation of the Rose Garden vents near the Galapagos Islands since discovery in 1979 has suggested some degree of succession as the vent matures and its chemical nature changes (Hessler et al. 1988; Van Dover 2000) . Rifria seems associated with comparatively new vents, but declines in relation to decreases in sulphide concentration . The bivalves, however. persist and even expand their populations as vestimentiferans disappear. suggesting possible competitionbetween mussels and tubeworms. New vents will clearly emerge through the same geological process, but one of the most interesting aspects of vent ecology is how organisms disperse between vents and how new vents become colonized . The majority ofvent organisms appear to have larvae with abbreviated development (lecit hotroph ic), so will be colonizing nearby vents. Surveys in the Pacific have suggested vents are generally < 10 km apart but there is up to 100 km between vent fields, presenting dispersal problems between these strings of islands for short-lived larvae of endemic vent species (Van Dover 2000) . If dispersal, and thus gene flow, is limited then there would be extensive genetic differentiation between vent fields. Two different models of gene flow are apparent in vent taxa (Vrijenhoek et al. 1998; Van Dover 2000) . Rifria fits a 'stepping-stone' model with most gene exchange occurring between neighbouring populations and gene flow declining with distance (Fig. 9.21a), whereas patterns of gene flow are different for Bathymodiolus (Fig. 9.21b) where migration rate appears unrelated to distance. This is termed the 'island' model suggesting long-distance dispersal and mixing of larvae within a 'migrant pool'. The

0

0

~

o

4

1

2

3

4

log (distonce) Figure 9.21 Gene flow models in vent organisms. (a) Rlitia, the isolation-by-distance model, with migration rate decreasing with distance. (b) Bathymodiolus, the island model, where migration rate is constant, regardless of distance.

vent mussel appears to be unusual in this respect. though its apparent wide dispersion may be also influenced by its ability to colonize a range of seep and vent types. Despite the general lack of dispersal ability, vent organisms appear to successfully colonize the majority of vents. The puzzle of how poorly dispersing larvae can travel large distances has focused on the supply of potential steppingstones between vents that provide the suitable nutrient supply for chemosynthesis to occur. Whale skeletons provide such a resource (HzS is produced by bacterial decomposition of lipids). so larvae could disperse over several generations (Smith & Baco 2003) . Conversely, it has also been suggested that some groups of organisms may have originally invaded vents from biological material, such as whale bone and wood; analysis of such material from the deep sea revealing small mussel species (e.g . Idas washingtonia) in the same subfamily as Bathymodiolus, which appear to have preceded vent specialization within this lineage (Distel et al. 2000) . These small bivalves possess chemosynthetic endosymbionts, utilizing sulphide produced by wood decomposition, so it is feasible that wood (and bone) were vectors that originally transported mussels to vents. While vent taxa appear to disperse effectively, through a variety of strategies. it would appear that some deep-sea islands remain uncolonized . Recently. a new vent field was discovered in the mid-Atlantic (named 'Lost City'), which had steep-sided black smokers and dense microbial communities, yet none of the large invertebrates associated

Further Reading • ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

with other Atlantic vent systems (Kelley et al. 2001) . This new field lies 15 km off the main axis of the mid-Atlantic

currents have not, as yet, brought settling larvae of vent organisms.

ridge and clearly is in a position where the main dispersive

Chapter Summary •

The deep ocean floor (below 200 m) represents the largest habitat on the planet, but the least known. The abyssal plain extends across the bottom of much of the ocean at depths of 40005000 m.

•

Sampling the deep-sea floor is except ionally difficult and is an expensive undertaking. As a result, much of our knowledge of larger organisms comes from photography and comparatively few samples. More recent ly, submersibles have revolutionized how we can sample and observe this distant environment.

•

Conditions on the abyssal plain are remarkably constant, generally being dark and cold (2°C), w ith the seabed made up of fine , deep mud. Hydrostatic pressure is over 500 times that at the surface.

•

Food supply is the main limiting factor for deep-sea animals, as the food web relies on the fall of organic material from the surface layers, mainly as 'marine snow'. This fall is seasonal in temperate regions, giving regu lar annual cues to benthic organisms.

•

Only 1-3"0 of surface production reaches the ocean floor, so animals on the abyssal plain are in low abundance and total biomass. However; individual animals can grow very large, with giant members of groups such as sea spiders, amphipods, and xenophyophores (giant single-celled protozoans) a feature of the deep sea.

•

There is much controversy over how many species live in the deep-sea, with estimates as excessive as 100 million! We will never know the actual number, but it is possible that the majority of species on earth live in the deep sea.

•

Many deep-sea organisms produce light, known as bioluminescence. This can be for a range of functions, such as attracting prey, deterring predators, spotting prey in the dark, and advert ising for mates.

•

In the late 19705 and early 1980s the use of submersibles assisted the discovery of an entirely new ecosystem in the deep-sea-hydrot hermal vents. The sulphur in these vent systems is used by bacteria to generate production throug h chemosynthesis-primary production without t he need for sunlight. Many vent animals, such as giant tube worms known as vestimentiferans, have vast numbers of these bacteria living symbiotically in t heir bodies and providing them with a food supply.

•

How vent animals disperse continues to puzzle marine ecologists. Some species may use steppingstones on t he ocean floor to reach new vents. Whale carcasses could be very impo rtant for vent animal dispersal as their bones contain sulphur.

Further Reading Books •

Gage, J. D. & Tyle r, P. A. 199 1. Deep-Sea Biology: a Natural History of Organisms at the Deep-Sea Floor. Cambrid ge University Press, Cambridge.

•

Herring, P. 2002 . The Biology of the Deep Ocean. Oxfo rd Un ive rsity Press, Oxford.

•

Van Dover, C. L. 2000. The Ecology of Deep-Sea Hydrathermal Vents. Pri nceton Un ivers ity Press, Princeton , NJ.

Chapter 9 The Deep Sea Key papers and reviews •

Levin, LA., Etter, RJ. , Rex, M.A., Gooday, AJ., Smith, CR, Pineda et al. 200 1. Environmental infl uences

on reg ional deep-sea species diversity. Annual Review of Ecology and Systematics 32, 51 -93 . •

Martin , W" Baross, J., Kelley, D" & Russell, MJ, 2008, Hydrothermal vents and the origin of life, Nature

Reviews Microbiology 6, 805-814. •

Rex, M.A. et al. 2006, Global bathymetric patterns of stand ing stock and body size in the deep-sea benthos. Marine Ecology Progress Series 317: 1-8.

•

Roberts J.M ., Wheeler AJ., & Freiwald A. 2006. Reefs of the deep: the biology and geology of cold-

water coral ecosystems. Science, 213 : 543-547.

Mangrove Forests and Seagrass Meadows

Chapter Summary

the product ivity of mangrove fore sts. Spec ies such as mud-

Mangrove forests and seagrass meadows represent two of

skippers demonstrate incred ible levels of adaptation to life

the most valuable marine habitats in the world, rivalled only

in this intertidal habitat. Seag rass beds provide a st ructural

by co ral reefs for their importance in providing a high level

hab itat on generally feat ureless soft-sediment bottoms, and

of productivity and physical structure that supports a considerable biodiversity of associ ated animals. However, both

so are uti lized by a w ide and diverse range of fish and inver-

systems are remarkable in that they are based on higher

from predation. Seag rass meadow s are also vital grazing

pl ants more generally associated w ith terrestrial systems,

areas for large vertebrates, such as turtles and sea cows.

so mangrove trees and seag rasses demonstrate fascinating

Both mang roves and seag rasses provide a range of fu nctions

physical, biological, and life-cycle adaptati ons that enable

that influence the w ider coastal ecosystem and have value for

survival in the marine realm. Mangrove forests host a unique

humans, so their fragmentation and loss has conseq uences

mix of marine and terrestria l animals, including insects, birds,

far beyond the orga nisms that live associated wi th these

fish, and particularly crabs, w hose activities heavily influence

plants.

10.1 Introduction A fund amental, and obvious, difference between the ecology of terrestrial and marine systems is the taxonomy of the main primary producers that power the respective food webs. Production within the ocean environment (Chapter 2) is mostly generated by small, often microscopic algae, suppleme nted in coastal waters by larger brow n, red, and green macroalgae attached to the seabed and intertidal zone. Generally, standing biomass is low (on a global scale) , although production itself can be very high. With comparatively few exceptions (as we will see), marine animals do not generally rely on plants for shelter, giving the impression that the sea is an animaldominated, rather than plant-dominated, system (thin k of coral reefs, for example). The terrestrial environme nt, in contrast, is dominated by large primary producers such as trees, grasses, and herbaceous flowering plants (a ngio sp er m s), which are comparatively recent in evolution ary terms; terrestrial angiosperms , for example, only appe aring extens ively in the fossil record approximately 100 million years ago. Wher-

tebrates, providing a physical ho me, food supply, and shelter

ever conditions allow, the land is covered by plants and so the m ajority ofland an imals utilize plants as a structural habitat. In a sim ilar manner to insects, which dominate the terrestrial animal fauna, few terrestrial vascular plants have been able to exploit marine cond itions . In fact, only one group is able to live full y beneath the sea: the seagrasses. These angiosperms can grow, flower, and reproduce all within the subtidal e nviron ment, and in parts of the world form vast mea dows in coastal habitats. This results in a very unusual habitat, much more similar to those on land than those generally found in the sea, and therefore providing an important prod uction source and home for m any associa ted marine organisms . Two other important coastal systems are created by higher plants: mangrove forests and saltm arshes. For more details on saltmarsh ecology see Adam (1993).

Wh ile these assemblages of plants cannot tolerate continual immersion in seawater, they are highly adapted to

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

dealing with the problems faced by plants on the fringes of the marine environment. Consequently they too can cover

huge areas of the land/sea interface and provide a key role both in terms of the functioning of coastal ecosystems and the provision of a structural habitat for a diverse range of species. Saltmarshes tend to be associated with estuarine or

lagoonal systems at higher latitudes; their ecology is therefore outlined in Chapter 5. Mangroves, on the other hand, are closely connected with both marine and estuarine conditions, and have a diverse and important associated

fauna. Together with coral reefs and seagrass meadows. mangroves are recognized by UNEP as the most important marine habitats. This chapter will therefore discuss how two contrasting plant groups (seagrasses and mangroves) are able to survive in the marine environment. and, in particular, investigate their relationship with a diverse and often unusual range of animals, which associate them-

selves with these plant-based habitats.

10.2 Mangrove forests 10.2.1 What is a mangrove? Mangroves are woody trees or shrubs that flourish at the sea/land interface in sheltered tropical coastal and estuarine regions where fine sediment collects. They can be subdivided into two categories : true mangroves, which only occur here. and mangrove associates. which can also be found elsewhere. e.g. rainforest. An individual tree is termed a mangrove. while the whole forest habitat is a mangal (or simply 'mangrove forest') . There are three basic forms of mangrove. depending on shore morphology and sediment. salinity regime of the surrounding water.

and the relative tidal and freshwater influence (Fig. 10.1) . Riverine mangroves form where there is a low tidal range and a dominance of freshwater flow, such as the deltas of major rivers. Most of the large areas of mangrove forest in Asia are riverine mangroves. Tide-dominated mangroves

are fully intertidal, often in full-strength seawater and are subject to high-wave action. These are also termed 'fringing' mangroves and are often the pioneer species that first colonize the intertidal mudflats. Basin mangroves occur to the landward-side of fringing mangroves, where there are lower tidal currents and wave action, but where salinity can

be highly variable due to evaporation and rainfall. For an excellent, more detai led text on mangrove ecol-

ogy, see Hogarth (1999).

Figure 10.1 Examples of types of mangroves: (a) riverine mangrove, (b) tide-dominated (or fringing) mangrove, (c) fring ing mangrove roots w ith associated community of animals. Copyright: (a) US Fish & Wildlife Service, (b) NOAA, (c) Martin Attri ll.

Mangroves are taxonomically diverse (Tomlinson

1986), with representatives in mangals of 16 very different plant families . This suggests that the mangrove habi-

families dominate the world's mangrove flora, however,

tat has evolved separately at least 16 times . Two main

is the Avicenniaceae, represented by eight species of

in terms of both diversity and ecological role. The first

10.2 Mangrove forests •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

the genus Avicennia (the black mangrove); the second, the Rhizophoraceae, which includes the red mangrove (Rhizophora, 8 species) together with three other genera (Bruguiera, Ceriops, and Kandelia) . Other important families include the Combretaceae (which includes the white mangrove. Laguncularia). the Sonneratiaceae (important in Australia and Southeast Asia; 5 species), and also one species of palm (Palmae), Nypa, demonstrating the width of mangrove taxonomic range. Nypa pollen and fruits have fossilized well, due to the conditions in mangrove forests, providing information on the evolution of palms and climate change. Nypa fruits from the Eocene (60 mya) have been found in the UK!

mangrove associates, generally forest plants that are able to tolerate the conditions found in the high swamp, but cannot deal with the excessively harsh environment inhabited by the true mangroves. So why do mangroves show such a distribution pattern in relation to distance from the sea and why is it so difficult for terrestrial trees to inhabit the coastal fringe? Two main factors limit plant distribution: increased salt levels and waterlogged sediment, although other more minor factors (such as soil nutrient levels) can also have an influence.

10.2.2 Where are mangroves found?

When considering how terrestrial organisms penetrate the intertidal zone. we have to invert our usual perception about the stresses affecting marine organisms living in this habitat. On a soft-sediment shore, high salinity levels and water being maintained within the sediment are crucial to the survival of a marine organism. but both cause extreme problems for terrestrial plants used to living in dry soil with minimum salt content.

Mangroves are strictly tropical, and their distribution across the globe coincides very closely with that of coral reefs, but they are also found in tropical regions where local conditions do not favour reef development, such as the Amazon region of South America. Distribution is generally confined to the 20°C isotherm either side of the equator. modified by either warm currents extending their distribution (e .g. east Australia). or cold currents extending into the tropics (e .g. west South America) . Diversity is highest in the Indo-West Pacific (IWP) and declines dramatically away from this region to a minimum in the Caribbean/West Atlantic (Ellison et al. 1999). This is thought to be due to increased local diversification following continental drift (vica r ia n ce hypothesis), ratherthan the IWP being the centre of origin of mangrove taxa and from where they subsequently dispersed to other parts of the world. Mangroves develop wherever shallow-sloping, generally muddy shores are available within this region, especially lagoons, estuaries. and river deltas. Diversity is then due to separate evolution of species. rather than dispersal from a centre of origin. A vicariance event is t he formation of a barrier to genetic exchange that causes separation of related taxa (e.g. continental drift, glaciation).

Within a mangrove forest. there is a clear pattern of distribution of species with distance away from the sea. The fringing mangrove species are found at the sea edge, and across most of the world these pioneer trees tend to be species of Rhizophora. Other true mangrove families inhabit conditions behind these fringing species; in Florida, for example. Avicennia and Laguncularia are located in the mid-swamp, Laguncularia preferring natural topographic highpoints where sediment is less waterlogged. Behind these true mangroves are distributed a range of

10.2.3 How mangroves deal with living in a marine environment

Waterlogged sediment The thick, waterlogged mud present in mangrove forests presents a key problem for trees, the sediment is exceptionally low in oxygen and tree roots need oxygen to respire and function. Mangroves have developed three main morphological adaptations to enable their roots to obtain oxygen despite growing in anoxic conditions (Box 10.1) . All involve root structures that exit the sediment enabling air to be taken in though special pores (called lenticles) and keep the section of root within the sediment supplied with oxygen.

Dealing with increased salt levels The presence of salt results in two main problems for trees living in marine conditions. First. the uptake of salt disrupts cellular mechanisms and is fatal for most plants. This can be dealt with through either exclusion of salt by roots, tolerance ofsalt in tissue (this is much higher in mangroves than other plants), or secretion of excess salt through the bark or by shedding leaves (they often taste salty iflicked). Second. and perhaps most importantly, salt water in sediment reduces the osmotic difference between the root and the sediment making it difficult to take up water (Hogarth 1999) . Rhizophora only takes water from the top 50 em of soil (fresh water is less dense than seawater and hence occurs in the upper layers of soil in these systems) and it is thought that Avicennia excludes 90-95% salt at root surface (salt can be excreted, though we are not sure exactly how it is excluded) . Due to this osmotic difference, mangroves take up water much less easily than other plants

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 10. 1: Mangrove root structures Different mangrove families have varyi ng st rategies enab ling them to get oxygen to roots w ithin anoxic sed iment. Rhizophora produces aerial roots (a), w hich

leave the tree up to 2 m from the ground and then penetrate the so il, giving the tree support. The aerial section is rich in lenticles to take in air. Rhizophora can al so produce aerial branches to aid oxygen uptake. Bru-

guiera roots periodically break the soil surface during

growth, producing 'knees' above the sediment surface (b) through wh ich air is taken up. Avicennia roots have a feature symbolic of mangrove forests, w ith vertical tubes (pneumatophores) emerg ing every 15- 30 em from horizontal roots (c) . The tip of each tube has abundant lenticles for air uptake. A 2 to 3 m high Avicennia can have up to 10 0 0 0 pneumatophores.

(0)

and so n eed a much greater proportional root biomass to ach ieve this (the add itional growth needed for roots therefore restricting energy being put into vertical growth and reproduction) . Wit h in a mangrove forest. trees inhabiting higher salinity soils have a larger below:above ground biomass ratio than those in more freshwater conditions , highlighting the efforts required to survive in marine sedi ments (Saintilan 199 7; Fig. 10.2a). Mangroves also have much greater root biomass than ot her trees. In Australia, mangrove root biomass was estimated as 125 tonnes per hectare (r ha-' ), compared with 9 0 t har! for large eucalyptus and 32 t ha-! for Acacia (Snowden et aJ. 2000). The difficulty in taking up water has additional important consequences. Plants tend to regulate temperature by transpiration. allowing water to be evaporated from leaves to cool the plant. Mangroves cannot afford to cool leaves primarily by this route as water is a limiting resource. but to achieve maximum photosynthesis leaves also need to be held perpendicular to the sun-which consequently maximizes temperature increase ! Rhizophora holds leaves at angles to the sun depending on how exposed the leaf is. Those at the edge of the tree, in full sun, are held at 75' , thus preventing overheating, while shaded leaves furt her back into the tree are fully exposed to the sun d irection (0°) .

o

E

(01 10

o Avicennia

1

•

• Aegiceras

~

o o

e=

i5

~

••

o

s ~

(b)

=

o•

500

--= E E

~

0

20

10

(bl

•o

30 Salinity

40

50

S./anceo/ato

400

o S. alba 300

~

'"

200

\

100

(e)

0

"-

,

,

20

40

""0

,

,

60

80

100

Salinity (% seawater)

Figure 10.2 Dealing with salt levels. (a) The cost

of living in high salinity s e d ime nt s- ma ng roves require proportionally larger root biomass to enable water uptake when salinity is high . (b) Comparative distribution along a s a linity gradient of two closely related Sonneratia s pe cies, their natural distribution relating to a combination of salt tolerance and competitive ability.

10.2 Mangrove forests •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Salt tolerance also varies between species within the same genus, which relates to their natural distribution within a mangrove forest. For example. in Australia, Sonneratia alba has a higher salinity tolerance than S. lanceolata and is therefore found closer to the sea. However. S. lanceolata outcompetes S. alba at lower salinities as it can grow taller (Ball & Pidsley 1995; Fig. 10.2b) .

10.2.4 How do mangroves reproduce? Mangroves all produce flowers. which require pollinating. A large range of flower size and method of pollination exists, reflecting mangrove taxonomic diversity. from the small wind-pollinated flowers of Rhizophora to the large, beautiful blooms of Sonneratia and Bruguieru. which are pollinated by bats, moths, birds, and butterflies. The key problem facing mangroves living in marine sediments is dispersal of resulting seeds, which would need to tolerate inundation and high salt-levels, or be dispersed by the sea. Most mangroves demonstrate a degree ofvivipary; following pollination the growing embryo remains on the parent plant (up to several months) . The young plant therefore does not leave the adult as a seed or fruit, but as a fully developed seedling known as a propagule. The most advanced vivipary is shown by Rhizophora (Fig. 10.3)seedlings in South-East Asia have been recorded up to 1 m long. Mangroves put a huge amount of energy into propagule production; Avicennia in Costa Rica can produce more than 2 000 000 propagules ha- 1 representing 10 to 40% of net primary production (Smith 1992) .

yr"

Vivipary is the process of giving birt h to live young and is generally associated wit h animals. In plants, it refers to the seeds germinating on the plant instead of falling.

Rhizophora seedlings drop from the parent plant directly into the water. Initially they float horizontally, turning vertically after about a month when roots develop (by 40 days) . The roots drag on the bottom and the seedling can get stranded horizontally, or sink, where they erect themselves vertically after rooting. If not rooted after 30 days, propagules retain buoyancy and are viable for > 1 year. although survivorship is species-specific and dependent on propagule weight. So, why are mangroves only found in the tropics? The combination of three key components has a high energy cost: being a tree, tolerating salt. and coping with waterlogged soil. The environmental conditions (light limitation) in temperate regions would not allow photosynthesis all year round and so the tree would not gain enough energy to survive. Mangroves provide an incredibly complex structural habitat, both above the water line and below it through

Figure 10.3 The propagules of Rhizophora. Photograph: Martin Attril!.

the root system. The assemblage of organisms associated with mangroves is therefore a unique mixture of animals that colonize the mangrove forest from both the land and the sea, resulting in a dynamic and diverse associated community.

10.2.5 Terrestrial organisms associated with mangroves Non-woody plants are not common in the marine section of mangrove forests, due to the same pressures of salinity and waterlogged soil that affect the mangroves themselves. Epiphytic species that can avoid the sediment are the most successful, particularly those belonging to two groups-the bromeliads and the mistletoes. Insects. however. are successful, as anyone who has visited a mangrove swamp will know to their cost! Ants. termites, and mosquitoes are particularlyabundant (Hogarth 1999), with some mosquitoes moving on to unusual hosts; Aedes pembaensis, for example. has been recorded feeding off mudskippers at low tide. This species also has an unusual life cycle, laying eggs on the

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

pincers ofcrabs, after which the larvae develop in the crabs' burrows. The major ecological impact ofinsects. however. is their grazing activity on the leaves of the mangroves. damaging the leaf and thus reducing the potential of the tree for photosynthesis. growth. and reproduction. The seasonal emergence of caterpillars (e.g, the moth Nophopterix) can have particularly dramatic impacts. Grazing can also have

A range of terrestrial vertebrates has also become specialized for life in mangroves, including species of reptile and amphibian that have developed exceptionally high

tolerance to high salinity water. One example is the crabeating frog (Fejervarya cancrivora, Fig. lOAc) . Amphibia are not generally associated with marine systems, but F. cancrivora can survive as both tadpole and adult due to exceptional osmoregulatory abilities. The most diverse and obvious group ofvertebrates in mangroves, however, is the birds. which use the mangrove forest for nesting, feeding, and as a roost at high tide. Many mangrove systems around the world are protected specifically due to the high numbers of these high-profile organisms they support. The bird fauna is a mix between waterfowl and terrestrial species that feed off insects, etc.• within the mangrove canopy.

a controlling effect on the successful settlement and growth of new propagules. Sousa et al. (2003) noted that settling Rhizophora propagules were only successful in clear gaps within the existing forest (e.g. those caused by lightning strike) . While offering better growth conditions, refuge from predation by the beetle Coccotrypes rhizophorae (Fig. 10Aa, b) was just as important, with seedling mortality increasing with distance from the gap into the forest.

•

,

.

•

• • •

•

• •

•

1

•

•

., • ,.' •

~

•

•

.-

•

. , . .,

-.' '. • ••

•

-

•

•

-•

•

• •

••

•

••

•

Figure 10.4 (a). The beetle Coccotrypes rhizophoroe, a key predator of new settling mangrove progagules (b) (with kind permission from Springer Science & Business Media from Sousa et al. 2003). (c) The crab-eating frog Fejervarya cancrivora, one of the few amphibians able to survive in marine conditions (copyright Nick Baker, www.ecologyasia com). (d) The gastropod Terebrolia pa/ustris, adults of which are able to graze mangrove leaves (photograph: Christoph Kuhne).

10.2 Mangrove forests •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Crocodiles are frequenctly associated with mangroves.

Croeady/us acutus, for example, has special salt glands that remove salt from its body which is acquired during

feeding activities.

The complex nature of the mangrove ecosystem allows extensive niche differentiation within the canopy bird fauna. Noske (1995) studied the feeding guilds of these birds in Malaysia, recording 17 species from four contrasting feeding guilds (neetarivores, aerial hawkers, bark foragers, foliage insectivores) . Within these guilds, species avoided direct competition through small-scale spatial variation in their distributions. For example, two species of woodpecker were each restricted to a different tree species (Avicennia and Sonneratia). and thus separated within the forest due to differential distribution of the mangroves. Within the same tree, two species of foliage insectivores (flyeater, Gerygone sulphurea, and ashy tailorbird, Orthotomus ruficeps) were spatially separated by height, the flyeater only foraging below 4 m in the canopy and the tailorbird at the canopy top. Hutchinson (1957) defined a niche as an In-d imensional hypervolume' representing a space of all environmental factors that affect the welfare of a species. Niche overlap can therefore potentially result in competition, niche d ifferentiation allowing species to coexist.

Mangrove birds can be key species for the conservation of mangrove habitats, but full details of their ecology is necessary in order to plan suitable management strategies. A good case study is that of the scarlet ibis (Eudocimw; ruber, Fig. 10.5) within the Caroni Swamp in Trinidad. The ibis forages within the channels of the swamp and returns to roost in the tops of trees at dusk-a spectacular sight when thousands ofbirds return at once. Caroni Swamp comprises

over 5600 ha of mainly state-owned habitat, principally mangrove. and is fed by four rivers. The ibis population peaks in autumn/winter (up to 10000 birds); most birds then migrate to South America leaving behind a small breeding population (Bildstein 1990). Despite protection of their mangrove habitat. this is a reversal of the situation in the 1950s and 1960s, when the majority of birds stayed to breed. so the decline in breeding numbers was somewhat of a worrying puzzle. Non-breeding birds feed off marine prey, such as fiddler crabs (Uca) and polychaetes (Nereis), but it was noted that nestlings raised on such salty prey did not develop properly, breeding adults switching to foraging in freshwater areas inland. Despite official protection of the mangrove forest. much of the freshwater wetland in Trinidad had been drained for rice production. removing the ibis's feeding grounds. As a result the birds began to migrate to the Orinoco delta to breed, where freshwater habitat was still available. A further twist to the story was uncovered when high levels of mutation (chlorophyll deficiency) were recorded in Rhizophora in parts of Caroni Swamp (Klekowski et al. 1999), traced to high levels of mercury within the sediment under the trees. particularly those where scarlet ibis were nesting. Samples of feathers from ibises and other birds in the roost revealed that the ibis had exceptionally high levels of mercury in their feathers (41 ppm compared with 6 ppm for other species) . The high level of mercury in feathers was traced to the ibis's new foraging grounds in the Orinoco. which are key gold-mining areas . The mining operations release high levels of toxic metals into the watershed . Mercury is accumulated in feathers (Chapter 14), so when the ibis returned to Trinidad for winter to moult, the feathers contaminated the soil and impacted the mangroves. Many birds demonstrate a remarkable tolerance to metal contamination, being able to 'dump' metals in feathers and then shed them, removing the toxin.

Figure 10.5 The scarlet ibis,

Eudocimus tuber, an inhabitant of mangroves in the Caroni swamp,

Trinidad (photograph: Mike Lane, rspb-images.com).

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

TECHNIQUES: Animal-attached remote sensing Many large vertebrates associated wi th marine and coastal environments, like the scarlet ibis discussed in this chapte r, move consid erabl e dist ances during migration to breeding grounds or whilst foraging. Traditionally, such movements have been stu died and

inferred by visual observations (e.g. the ibis flying to Orinoco), or by tagging organisms (e.g. bi rd rings, fish tags) and recording when these marked individuals are seen, or caught, elsewhere. Such methodology is limited, wi th respect to its power of inference, particularly if the organisms of interest are not easy to observe, move long distances across oceans, or (as is the case wi th most marine organisms) th ey are primarily under

Ireland

•

Wales

England

" ..-Jaw'tsJt. . ...

(a) A gentoo penguin , PygosceJis papua, with a multi-channel data recorder on its back (from Ropert-Coudert &. Wilson 2005). (b) Recorded flight paths of Gannets (Morus bassanus) foraging from Skomer Island , superimposed on water depth, fishing intensity, and chlo rop hyll a production (courtesy Stephen Votier and Matthew Witt).

10.2 Mangrove forests

wate r. Conseq uent ly, met hods have been developed using

increasi ngly sophisticated miniturized technologies that allow us to attach devices to organisms (see figu re a) and follow them more closely. Such devices can record exactly where organisms have been and, most recently, simultaneously record more complex information on their environment, physiology, and behaviour. This branch of

science is known as telemetry (Greek: tele ros-

far, met-

measurement ) and the technology is termed ani-

mal-attached remote sensing or bio-Iogging fo r s hort (Ropert-Coude rt & Wilson 2005). Bio-Ioggers can be

attached to organisms, record their movements, and then be retrieved later (e.g. fro m seabi rds at breeding colonies; e.q. Wilson 2003), can auto mat ically release from the organism and be recovered (e.g. 'pop-up ' tags on large fis h; Gore et al. 2008), or provide streamed data via satellite o r mob ile receiver (Block et al, 2005) . Bio-Ioggi ng has revo lut ion ized our knowledge about the movements and foraging patterns of seabi rds- previously very little was known beyo nd at-sea observa tions abo ut what b irds do away from th eir colony and w here

(c) Basking shark Cetorhinus maximus (photo: NOAA).

they go. Figure (b) provides an illust ration of t he movement t races obtained by suc h devices, which include GPS

either side of the Atlantic. Additionally, basking sharks are

capability to record location, in this case forag ing t rips

not protected outside of Europe, so east Atlantic sharks

of the gannet Morus bass anus from Skom er Island off

could be exposed to hunting in w aters ou tside European

Wales. Birds flyaway from the co lony in co mparat ively

protection meaning th is endangered species may be more

straight lines and change their movem ent pattern as they

vulnerable than we thought

circle to forage at a range of locations. Geo- referenced

Bio-Iogging can also provide information on the physi-

data can then be co mpared wi th other data sets, such as

ology and behaviou r of a marine organism whilst it is div-

primary produ ction hotspots or key fishing areas, to pro-

ing and foraging. For example, beak ang le senso rs have

vi de insights on the cues used by gannets to find suitable

been attach ed to penguins (Spheniscus magellanicus)

feeding grounds (see also plaice vertical movements in

carrying bio-Ioggi ng devices, which record every t ime

Chapter 8).

the beak is open w hilst the animal is at sea, in addition

Bio-Iogg ers have also provided information on the

to the range of environmental parameters (Wilson et al.

movement of large fish, such as t una (Block et al. 2005)

2003). These devices are retrieved after one fora ging

and basking sharks (Gore et al. 2008). The basking shark

run, and reveal when penguins take breat hs at the surface

Cetorhinus maximus (figure c) is the world's seco nd larg-

and can also determine w hen they cap ture prey under-

est shark (grow ing up to 10m) , feeding on coastal plan k-

water (Wilson et al. 2002). Penguins seem to be able to

ton during the summer around productive coasts, such as

predict and prepare for deep dives, as they take an extra

the w est coast of the British Isles. A series of satelli te tags

breath at the surface for every 2.5 m increase in maximum

that monitor position and depth w ere attached to sharks

depth (Wilson 2003, Ropert-Coudert & Wilson 2005) ;

off the Isle of Man (in the Irish Sea; Gore et al. 2008)

the descen t rate is also quicker for deep dives. Penguins

to fin d ou t where the British sharks w ent in wi nter w hen

have to assess the best strategy for air intake and divi ng in

they are rarely seen ; it was assum ed they headed sou th

relat ion to opti mally exploit ing available prey; for example,

down the coast of Europe. However, one fem ale shark

taking in more breaths allows deeper divi ng, but requires

travelled over 9500 km across the Atla ntic to t he coast

more time spent at the surface. The beak sensors indicate

of Newfo und land and on route dived to a depth of 1264

that b irds inhale an ext ra breath for every fo ur fis h caug ht

m , using th e deep m id-ocean! This finding has major

in t he dive beforehand, providi ng enough oxygen for prey

impli cations for ou r understanding of the species and its

pursuit, but minimizing the time spent at the surface away

conservation, as it is clear fish around the globe can prob-

from the prey (Ro pert-Co udert & Wilso n 2005).

ably intermingl e rather than being in discrete populations

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

10.2.6 Marine organisms associated with mangroves Examples from the vast majority of marine taxa can be found associated with mangroves or in the surrounding sediment; the sessile fauna attached to submerged roots is particularly diverse. the roots providing a hard substratum for attachment that otherwise is restricted in a soft-sediment environment (Farnsworth & Ellison 1996; Figure 10.lc) . Despite domination by long-lived groups. such as sponges and ascidians, the mangrove root community in Florida was found to be incredibly variable, and the assemblage composition on individual roots changed dramatically over short time periods (l to 2 months; Bingham & Young 1995). This was thought to be related to the intensity of stochastic perturbations. such as physical disturbance from strong tidal flow and predation causing large fluctuations in the abundance of certain species. This disturbance prevented competitive processes from producing a stable. equilibrium community. There is some evidence that this 'fouling' community on mangroves can impact the fitness of mangrove trees due to their smothering effect, perhaps impeding gaseous exchange. In Hong Kong, Aegiceras corniculatum fouled with large numbers of barnacles were found to produce fewer flowers, the energy needed to cope with respiratory stress perhaps affecting resources available for reproduction (Li & Chan 2008) .

the adults graze directly on mangrove leaves once their radula has metamorphosed to be able to penetrate the leaf surface. Ontogenetic means relating to t he development of an organism. Thus ontogenetic changes are those that occur

over the developmental life cycle (e.g. a larva will have different characteristics to an adult, such as an ontoge-

netic change in feeding). The classic marine organisms generally associated with mangroves tend to inhabit burrows within the surrounding mud and. unlike those in temperate mudflats, for example, are much more active at low tide. Two key

Sessile organisms are those that are fixed in place so they cannot move, such as barnacles and sea squ irts. Stochastic means involving a random or chance variable. For example, a severe storm is a stochastic perturbation.

Fewer marine species are associated with mangrove trees above the water line; except for gastropod molluscs. the majority are detritivores or graze off epiphytic algae. The most abundant mangrove snails are members of the genus Littoraria and, in a similar process to mangrove birds. different species show distinct niche separation within the mangrove. For example, in Papua New Guinea, L. pallescens lives on the mangrove leaves (where it grazes on algae rather than the leaf itself), L. intermedia inhabits tree bark in freshwater creeks. while L. scabra is also associated with bark. but on seaward trees (Hogarth 1999). This species undertakes a daily vertical migration up and down the tree in order to avoid becoming totally submerged (Alfaro 2008), varying its diet as it encounters different sub-habitats during its migrationit is even able to ingest and assimilate zooplankton. Few marine snails are actually able to feed on the mangrove leaves themselves, an exception being Terebralia palustris (Fig. lOAd) . This species demonstrates an ontogenetic change in diet, the young feeding off detritus, whereas

Figure 10.6 Mudskippers: mangrove fish remarkably adapted to life out of water. Here Periopthalmadon is gu lping air to take it down into its burrow

(photographs: Toru Takita and Atsushi Ishimatsu).

10.2 Mangrove forests •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

groups will be considered further here: mudskippers and crabs. Mudskippers (Fig. 10.6) are unusual fish related to gobies, represented by several long-named genera (e.g. Periophthalmus, Boleophthalmus, Scartelaas) and are exceptional among fishes in their amphibious behaviour. They live in water-filled burrows, emerging as the tide drops, often following the tide in and out (Ikebe & Oishi 1996) to forage, 'walking' across the mud surface using modified pelvic and pectoral fins. Most are omnivores. but some species specialize (e.g. Periophthalmodon feeds on crabs) . Mudskippers are highly physiologically adapted to this amphibious lifecycle, but do have to return periodically to their burrows

(Box 10.2) . However, they are remarkably tolerant to desiccation; Periophthalmus cantonensis, for example, can survive 2 .5 days out of water, while P. sobrinus spends 90% of time out of water and can lose 20% of its

body mass yet survive (Gordon et al. 1978) . Crabs are perhaps the most important group of mangrove fauna. They are particularly abundant and diverse in this habitat, have a major impact on sediment dynam-

ics through their burrowing activity, and are the main processors of mangrove detritus. The action of crabs has a major influence on the whole functioning of the mangrove system (as we shall see) and so they are an example of an ecosystem engineer. Two main families of crab are dominant in mangroves : the Grapsidae (e .g. Sesarma,

Fig. 10.7b) and the Ocypodidae (e .g. fiddler crabs such as Uca, Fig. 10.7a) . The grapsids have the most important role in terms of the functioning of the mangrove ecosystem, so we will look further at how they influence forest

productivity. An ecosystem engineer is an organism that directly or ind irectly modulates the availability of resources to other species. It is able to modify, maintain, and create

hab itats (see Lawton & Jones 1995; and Chapter 8).

Mangrove leaves are exceptionally unpalatable for invertebrates due to high proportions of carbon exacer-

bated by high tannin levels. Generally it is assumed that a C:N ratio of < 17 is required to be profitable to invertebrates (i.e. there is enough nitrogen in the substance to be worth the effort), but ratios in mangrove litter can

be 70 to 100 for Rhizophora (Lee 1998). Consequently, the majority of carbon produced by the mangrove forest is liable to be exported away from the syste m as leaves, or the nutrients become locked up due to slow microbial decomposition. Grapsid crabs, however, have the rare ability to utilize mangrove leaf litter as a prime food

source, despite its apparent unpalatability, but the digestive mechanisms for this important feeding habit have yet to be elucidated. A few species, such as S. messa, are

able to feed directly off fre sh leaf material; S. leptosoma has even been observed making daily vertical migrations up mangrove trees to graze on live leaves (Van-

nini et al. 1995). Grapsid crabs also store leaves within burrows (Fig. 1O.7b), so fulfil an important function in retaining carbon material within the mangrove syste m .

Robertson (1986) concluded that S. messa populations could remove or store up to 28% of all Rhizophora litFigure10.7 The two main families of crabs dominant in

mangrove forests. (a) Ocypodidae: Uca lactea annulipes feeding on a dead crab. (b) Grapsidae: Perisesarma samawati dragging a leaf down into its burrow (photos: Verheyden & Gillikin www.mangrovecrabs.com).

ter, with major implications for the reduction oforganic matter export from mangrove forests and thus the flow

of energy into coastal systems (Lee 1998) . Grapsid crabs also have a major ecological impact

through their burrowing activity (bio turba tion; see also Chapter 8), which can influence the chemical make-up of

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 10.2: How mudskippers aerate their burrows Mudski ppers' burrows are constructed in highly anoxic

sediment and measurements wi thin burrows have shown that the wa ter in deeper chambers contains practically no oxygen at all. It has therefore been some-

wh at of a puzzle as to how mudskippers cope with these inhospitable conditions, part icularly as eggs are laid and reared in ap parently hyp oxic w ate r. Ishimatsu

et al. (1998) noted that wal king near Periophthalmodon burrows caused bubbles of gas to be released

up the main shaft. Further observations revealed how mudskippers oxygenate d their living quarter s- before ente ring the burrow the fi sh fi lls t heir mouth cav-

ity with ai r (Fig. 10 .6 ) and trans ports this down t he burrow, often making ret urn trips. Air released in the breeding chamber becomes trapped, providing an oxygen reservoir for the fish and develop ing embryos that are often laid on the roof of chambers, w here air w ill accumulate.

0, 80% surtece ---' l --

disturbance of the experi ment had an effect, termed procedural control) ; and control areas (e ) , which were left alone . Levels of so il chemicals were measured and forest production assessed by the fall of stipules (for growt h, stipules are outgrowths of the leaf base, whic h are shed as the leaf grows) and the number of m ature propagules on trees (for reproductive outpu t) . Bu rrowing was found to have significant effects on the sed iment chemistry, w ith increases in sulphide and ammo nia in exclusion plots due to lack of aeration by burrowing, which would normally allow oxidatio n to nutrients more useful to plants. There were also significant impacts o n forest productivity, w ith higher growt h (stipule fall ) and propagule production in areas that included crabs, particularly during the m ain su mmer growing season (e. g. Fig. 10 .8) . The conclusions from work u nd ertaken in Australia and SE Asia are unequivocal: crab ac tivity is key to the healthy functioning of mangrove forests through recycling of organic m aterial and bioturbation. However, Mcivor and Sm ith (1 995) assessed the ecological roles of crabs in Florida mangrove forests, where the family Xanthid ae is more common than grapsid crabs . Xanthid crabs do not have leaf-processing abilities, so it was concluded that in the Americas, crabs do not have a significant role in leaf breakdown, the latter is presumably achieved primarily by microbial action .

5

Breeding chamber eggs on roof

= ---

4

~ ~

c ~ c ~ ~

3

Crob removal

~

c

E c

02 < 3% surfoce

~

~

2

E

30cm

~

z

I

the sedimen t and subsequent forest productivity. This is exemplified by a study in Queensland, Australia (Smith et al. 1991 ), which investigated the impact ofremoving crabs from mangrove areas. The st ud y includ ed three treatments: a removal area (R) , where all crabs were trapped and removed; a disturbance area (D), where activity was undertaken but crabs not removed (to see if the physical

0'--( DR

Nov

( 0R ( 0R ( 0R ( 0R ( 0R ( 0R Apr Mav Dec Jon Feb Mar

Figure 10.8 The results of crab-removal experiments on mangrove forest productivity. The production of new propagules was greater in areas that included crabs due to their bioturbating activities (Smith et al. 1991).

10.2 Mangrove forests •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

10.2.7 The wider role of mangrove ecosystems Mangrove forests as a whole provide a range of valuable functions that influence surrounding coastal systems, and impact on human activities such as fisheries (Chapter 12). Two of the most important are their potential role in nutrient input and energy flux between mangrove and marine systems, and the provision of a nursery for fish species that recruit to local fisheries and coral reefs. Despite the efforts of crabs, much detrital material from mangroves is exported out of the swamp to surrounding systems, particularly from fringing mangroves (Robertson et al. 1992), providing a large potential source of food. Jennerjahn & lttekkot (2002) estimated that 46 x 10 12 g C/yr (i.e. 46 000 000 tonnes!) of mangrove carbon reaches the ocean each year, representing 11 % of all terrestrial carbon entering the marine environment. The relative value of this material to marine organisms within adjacent systems is inconsistent. due to the general unpalatibility of the tree leaves to marine animals. The use of stable isotopes (Chapter 4 .3 .2) has proved valuable in assessing how important mangrove detritus is compared with other carbon sources. Schwamborn et al. (2002) investigated the uptake of different carbon sources by crustacean larvae in a tropical estuary to which a large amount of mangrove detritus was exported. They found the contribution of mangrove carbon to larval nutrition to be negligible, with only the zoeae of porcelain crabs having a significant proportion of mangrove carbon in their tissues. A similar. though perhaps even more unexpected. result was found in the tropical Embley River estuary in Australia (Loneragan et al. 1997). Stable isotope analysis was utilized to investigate whether seagrass- or mangrove-derived carbon were important carbon sources for commercial prawn species in the outer estuary. Organic matter in the sediment was found to correspond to the main local source. but this pattern was not reflected in the tissues of the prawns. While prawns that inhabited seagrass beds did seem to rely completely on seagrassderived material, mangrove-dwelling prawns did not depend on carbon from mangroves, but utilized either algae or seagrass material. Mangrove leaf litter does not even seem to be valuable in nutrient-poor habitats, and Lee (1999) demonstrated that additions of mangrove detritus to sandy substrata did not enhance the marine benthic community. perhaps due to the high associated tannin levels. It therefore appears that carbon from mangroves is rarely directly utilized by marine organisms, the carbon probably entering the food web following bacterial decomposition and recycling.

However, mangroves do have a clear physical role influencing the flux of material to coastal systems by providing a buffer for land run-off, e.g. from storms. During the terrible Indian Ocean tsunami of December 2004, areas in SE India where mangroves had been cleared suffered more damage than adjacent coasts where mangroves remained (Danielsen et al. 2005) . This was a tragic illustration of the important role of mangroves that act as 'green' barriers to coastal erosion processes. In particular. mangroves reduce the amount of sediment washed into the coastal region, which would otherwise negatively impact adjacent reef systems through increased turbidity that reduces light penetration (Hogarth 1999); where mangroves have been removed (e .g. for shrimp farming) there are potential consequences for the health and survival of local reef systems. Tannins, among many other chemicals, have been produced by plants in an 'arms race' with insect grazers. Such chemicals are unpalatable, so help protect the plant. Tannins are responsible for the astringent taste of unripe fru it and red wine.

Mangroves have a clear positive role in the provision of recruits to local fisheries and, in particular, coral reef systems. This conclusion had been somewhat anecdotal (Baran & Hambrey 1998) due to the presence ofjuvenile coral reef fish in mangrove systems, but Mumby et a1. (2004) have now unequivocally demonstrated the value of mangroves to coral reef fish populations. Working in Belize, they assessed the assemblage of fish present on replicate reefs with or without a rich mangrove stand nearby (Fig.10.9a) . There were marked differences in the reef-fish communities between the two sets of sites (Fig. 10.9b), and mangrove extent was the dominant factor that affected the fish assemblages. In particular, the biomass of fish species known to use lagoons or mangroves as juveniles was enhanced in reefs near to mangrove-rich areas. Mumby et al. (2004) concluded that the main reason for these results was that, once fry are large enough to leave seagrass habitats, mangroves provide a refuge for juveniles from predators and a plentiful food supply that increases juvenile survivorship and recruitment to coral reefs. They noted that the largest herbivorous fish in the Atlantic. the parrotfish Scarus guacamaia. whose life history critically depends on mangroves, has become locally extinct since mangrove removal. It is clear that conservation policies targeted at protecting coral reef habitats also need to consider nearby mangrove systems.

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

N -------. I

(a) Mangrove ,xlenl (rirh" seart') Reef ,ysl,m 101_102 km lit, 10°_10 1 km Transect 10-2_10 -1 km

8

TU

L

T

G

(

33

36-11

79-84

25

46-57

25

••• - .

.. -----

-

• •• ----

Mangrove-rich profil'

••• -.-

Mangrove-scorce profile

(h) Stress: 0.19

a GE L

a GW

aa GW aL

Figure 10.9 Experiment by Mumby et al. (2004) in Belize to assess how impo r tant mangroves are as a nursery ground for coral reef fish. Coral sites, w ith and without associated mangroves, were studied (a) and it was clear that coral reefs with nearby mangroves had a d ifferent fish community w ith a higher b iomass. (b). Mu ltidimensional scaling ord ination showing the similarities between fish communities at each site--the closer the sites on th is 'map', the more similar their fish assemblages. Blue squares are all the mangrove-rich sites.

10.3 Seagrass meadows 10.3.1 What are seagrasses? Seagrasses are the only truly marine angiosperms. generally growing in soft sediments in shallow coastal waters. Below ground there is a network of rhizomes and roots (Fig. 10.10), the rhizomes spread horizontally joining individual plants, while the roots extend vertically into the sediment. The root-rhizome network of the Mediterranean Posidonia oceanica can build up over hundreds of years. forming a peat-like 'm a tte' several metres thick (Borg et a1. 2006), which has even been used as a tool for

dating ancient wrecks due to its known growth rate. Above ground the seagrass is made up of discrete shoots that emerge from the rhizome and comprise several strap-like, lam ina te leaves that grow from the base of the shoot (the leaf sheath), although the genus Halophila has rounded leaves Fig. 1O.l1b. The number and height of leaves varies considerably between species. the longest leaves (over 6 m) belonging to the Japanese species Zostera caulescens (Aioi et a1. 1998; Fig. 10.11c, d) . In suitable conditions (see 10.3.2), seagrasses can form extensive meadows covering la rge areas of seabed (e.g. the seagrass bed within the Spencer gulf near Adelaide. Australia. covers

10.3 Seagrass meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 10.10 Schematic d iagram representing the main structural features of a seagrass.

- - leaves

- - leaf sheath - - leafsear (= node) - - Internode(vertical rhizome) Apical meristem (horizontal rhizome) Internode

. __ (horizonlol rhizome) root

over 4000 km-; Keuskamp 2004) with densities of shoots > 1200 m-2 (e.g, Posidonia oceanica; Borg et al. 2006),

with sheaves adapted to high-energy environments; (b) hydrophilous, and thus submarine, pollination; and (c)

creating one of the most important and extensive subtidal marine habitats in the world. The taxonomy and origin ofseagrasses has been subject

extensive lacunar systems that enable transport of oxygen to the below-ground structures in anoxic sediments.

to much debate, but seagrasses are clearly polyphyletic and generally assigned to two families, Potamogetonaceae and Hydrocharitaceae, neither of which is related to the grasses familiar on land. Fossil evidence suggests

Polyphyletic-a useful grouping of organisms that has

that seagrasses first appeared in the marine environment

around 100 million years ago. the oldest Cretaceous fossils include the genus Posidonia. but their ancestors are

more than one evolutionary root form. For example, 'winged vertebrates ' would include birds and bats, but each has very different origins. Hydrophyte

a true

plant that has fully adapted to live in water. Hence also hydrophilous.

uncertain. Two candidates have been put forward : coastal

The diversity of seagrasses is surprisingly low. with

plants (e.g. saltmarshes, mangroves) and freshwater hydrophytes. Some seagrasses have lignified stems and

only c.50 species represented worldwide (Hemminga & Duarte 2000), although this figure has generated much

two genera are viviparous. linking them to mangroves, required to survive in the marine environment, such as basal meristems and lacunar gas transport systems

discussion. The majority of the species are contained within three of the oldest genera: Zostera, Posidonia, and Halophila . There is little evidence that seagrasses have ever been more diverse. a major reason perhaps being

(Hemminga & Duarte 2000) . Certainly it seems likely

due to the very low rate of sexual reproduction (10.3.3)

that the seagrass habitat has evolved several times over

they have evolved, seagrasses possess three key attributes that enable them, uniquely. to colonize the marine

and dispersal restricting gene flow. However, seagrasses are exceptionally plastic in nature, and also show much genetic diversity even within meadows (Reusch et a1. 1999a), which means it remains unclear how many species of seagrass exist (Box 10.3) . Most seagrass meadows are monospecific, particularly in temperate regions. but tropical meadows have been reported with up to 12 sea-

environment (Hemminga & Duarte 2000) : (a) leaves

grass species present (Duarte 2001).

while freshwater plants show many of the adaptations

the last 100 million years (perhaps from both ancestral routes), with the genera Phyllospadix (Fig. 1O.lla) and Enhalus appearing significantly later than other seagrass groups (Larkum & den Hartog 1989). However

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

10.3.2 Where are seagrasses found? Unlike mangroves and saltmarshes, seagrasses are found in all the world's coastal seas except for Antarctica (probably d ue to ice scour) and cove r approximately 0. 1 to 0.2% of the global ocean (Duarte 2002) . Some species have extensive d istributions , such as Zostera marina (eelgrass) , which occurs in Europe from the White Sea to the Mediterranean, on both coasts of Nort h America and the Nort hwest Pacific (Gree n & Short 2003). Ot her species are more restricted . Posidonia ocean ica is the dominant seagrass across the Mediterranean, bu t is not found elsewhere, whereas some seagrasses have a very narrow range indeed ; P kirkmanii occurs only in a sm all area off SW Australi a. The peak of d iversity occurs in Malaysia, and seagrass species richness declines with distance along m ajor cur rents from this point (Muka i 199 3) , resulting in su ggestions that this may be the centre of origin for seagrasses (Hemminga & Du arte 2000) . With in their biogeographical range, much of the coast is devoid of se agrass due to unsuitable habitat cond itions; so individual se agrass beds can potentially be separated by large d istances of inhospitable coast. The vast m ajority of se agrasses re quire a soft substratum that will en able

Box 10.3: Diversity of seagrass: how many species are there? Seag rasses are morp ho log ically plastic, a te rm that describes speci es that ap pear very different depending on the envi ronment to w hich they are exposed.

As classification is generally based on morphological features (e.g. shape of leaf margins), there is around a 20% uncerta inty w ithin the seag rass world as to how many species of seag rass actually exist, wit h most arguments focused within the three main genera (Hafop hila, Zostera, Posidonia ). Molecul ar tax-

onomy (e.g. the use of DNA markers) has he lped the confusion to some degree and ten ded to reduce the number of existing speci es defined using morpho logical featu res. For example, intertidal Zostera marina looks d ifferent from subtidal plants and in the

UK has been considered a separate species (Z angustifolia) , although genetic evi dence from mainland Europe

suggests it is just a plastic form of Z. marina. Outside the UK the speci es is not recognized . However, the use of genetics has raised further problems, and has drawn into do ubt the identity of some genera. For example, the genetic distance between Heterozostera and Zostera is similar to that between species of Zos-

Figure 10.11 Examples of different seagrass forms. (a) Pbyttospadts iwatensis, part of a genus that can grow on rocky s ho res and are known as s urf grasses (photograph: Daniel Mosquin). (b) The broad-leaved Halaphilia ovalis (photograph: Keith D. P. Wilson). (c) The world 's largest s ea g rass, Zostera caulescens from Japan. The person in (d) is 1 .83 m tall (photos: Akihiro Dazai, Shizugawa Nature Center).

tera, suggesting th at one genus shoul d include both

these taxa (Hemminga & Duarte 2(00) . Whatever the final total of species, it is clear that seagrasses are a very low-diversity group.

1

10.3 Seagrass meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

the clear waters off the island of Malta has been recorded as far down as 40 m (Borg et al. 2005) . High-turbidity

the penetration of roots; although some species can grow on rocks (e.g. Phyllospadix, Posidonia) this is unusual and most only develop on sand or mud. However, some features of soft sediments make plant

water can therefore be a limiting factor for seagrass colonization and growth.

growth impossible, particularly highly mobile or exposed sediments that can result in burial of colonizing sea-

While the lower level of a seagrass bed is set by light levels (unless limited by habitat availability, e.g. the pres-

grasses, or those with very high inputs of organic matter resulting in reduced, anoxic sediment conditions. Paradoxically, the presence of a seagrass meadow on soft sediment can increase the sediment organic content, from both the seagrass production itself and the capture of other detrital material. Seagrass beds can also change the particle size distribution of the sediment. the baffling effect of seagrass blades slowing water currents and enhancing the deposition of fine sediment particles. Seagrasses therefore have a very complex relationship with the sediment, which we are only starting to untangle.

ence of coral reefs in the tropics). factors controlling the

Seagrass is also limited by the light levels, which must be above the threshold where photosynthesis is still possible.

upper limits are less well studied (Hemminga & Duarte 2000) . Several seagrass species, such as Zostera marina and noltii, Phyllospadix, and Halophila spp., can form extensive intertidal meadows (Fig . 10.12) . Desiccation can be minimized by the structure of the bed. dense continuous seagrass trapping water beneath the flat-lying leaves. Ultraviolet damage is also thought to be a major factor preventing intertidal survival, particularly of subtidal species, while in some regions upward extension may be prevented by physical factors such as wave exposure. ice scour, or the lack of suitable substratum.

As a result, the maximum depth where seagrass meadows are found is related to their compensation point.

The depletion of the ozone layer primarily through our

This depth is controlled by the clarity of the water, so in

ation , in particular the damaging UVb. There is much

comparatively turbid. temperate regions. seagrass beds are found at depths shallower than in clear. tropical or Mediterranean water. Zostera marina in Europe is generally found above 6 m depth, whereas Posidonia oceanica in

speculation abou t its effects on plants, but concerns

use of CFCs has allowed increased fluxes of UV radi-

include inhibition of photosynthesis and the cost of tissue repair and production of blocking compounds (see

also Chapter 12).

Figure 10.12 (a) An intertidal seagrass meadow of Zostera marina at Salcombe, SW England. (b) Close up of Z.

Marina plants. (Photos: Martin Attril!.)

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Many seagrasses show a tolerance to a wide salinity range (for example, Z. marin a occurs in full -strength seawate r and also down to a salinity of 5 in the Baltic), and seagrasses often are a major feature of estuaries and hypersaline lagoons (Chapter 5), although the majority of species perform optimally und er fully marine conditions. However, success in estuaries and similar coastal systems m ay be limited by high levels of plant nutrients in the water, whic h is becoming an increas ing p roblem through agr icultural run-off (Chapter 14). Such high levels of, for example, nitrate and ammonium, can d irectly affect the growth of seagrass (Short et al. 1995), but it also influences the competitive balance between the seagrass prod uctivity and that of algae associated with the seagrass meadow. represented by an epiphytic assemblage growing on the leaves or by macroalgae that grow alongside, or amongst, the seagrass meadow.

ing the exte nsive natural Posidonia ocean ica bed s with consequen t loss of large areas of seagrass coverage (see Cu rrent Focus box). While not so dramatic, the Japanese seaweed Sargassum m uticum poses a threat to native Zostera beds in Nort h-west Europe. While direct competition under natural cond itions does not appear to occur, physical damage to seagrass bed s (e.g. from boat anchors) can allow the colonizatio n of Sargassum, and once established it appears that seagrass cannot reclaim the space. Large beds of Zostera in NW France have been lost to Sargassum by this mechanism (Givernaud et al. 1991 ) and it wo uld also appear that seagrass beds may, unfortunately. aid the settleme nt of Sargass um, the seagrass cano py can trap floating fragments of the seaweed that can then become attached and grow wit hin the root-sedimen t matrix (1\veedley et al. 2008) .

20 0 r - - - - - - - - - - - - - - , BO

Epiphytes are organisms growing on the surface of plants, but not deriving nutrition from them. Generally the term is used for other plants (including algae), but sessile animals such as bryozoans can also be termed

150

epiphytes.

Williams and Ruckelshaus (1993) d emonstrated that Zoste ra marina showed a saturation-type response to increasing nitrogen levels; above sedimen t ammo nium conce ntrations of 100 umol l-' the seagrass was unable to increase growt h rates. Once ove r such a threshold. algal growth may con tinue. resulting in a shift in dominance w it hin the seagrass bed (Short et al. 199 5). This can have detrimental results for the seagrass, in particular due to light limitation imposed by the algae reducing seagrass productivity and. ultimately. survival. Hauxwell et al. (200 1,2003) demonstrate d that eelgrass (2. marin a ) was now absen t or d isappeari ng in all Waquo it Bay estuaries (Massachusetts) d ue to excessive algal growt h (Fig. 10.1 3), exceptthose that received the lowest land -derived nitrogen loads. Introduced algae are also posing a severe threat to seagrass coverage in Europe. The alga Caulerpa taxifolia has been acciden tally introduced to the Med iterranean from sout hern France and is spread ing rapidly. smot her-

MmroQ Igee

60

0 E

o0-

--~

--

--= ~

-

~

~

100

40

~

0

~

o

0

E

E

o

=

~

E

. ~

0

20

Eelgrass

o o

100

200

300

""

o 400

Nilrogen loading role (kg N·h,l.y" ) Figure 10.13 The relationship between the growth of seagrass and macroalgae at increasing levels of nitrogen loading, indicating algal biomass increases relative to seagrass under increasing nutrient co nd it io ns.

CURRENT FOCUS: Invasive species

ships. A vast range of species have therefore been introduced into terrestrial, freshwa ter, and marine

Ever since humans have been moving round the world

regions across the globe where they are not native, with

we have been transporti ng species with us, either

over 500 such species established in the coastal waters

intentionally for cultivation and recreational hunting, or as stowaways in, for example, the ballast water of

of the USA, for example. Where conditions are similar to native areas, the species can be incorporated into the

10.3 Seagrass meadows

flora an d fauna of the new region: a significant number of familiar terrestrial species in northern and southern latitu des have been introduced (e.g. rabbits and green shore crabs). A large proportio n of introduced species do not cause significant problems, but this is not the case wh en an introduced (or 'alien') species becomes invasive. These organisms can outcompete, or outgrow, native fauna and flora causing large changes in native biodiversity and often fo rm very large populatio ns indeed. Consequ ently our introduction of invasive species is now seen as one of the main global th reats to biodiversity, even leading to the ter m 'invasional meltdown' (Grosholz 2004). In response to this increasing threat to biodiversity, governm ent agencies have been set up to deal with this crisis, such as the US Departm ent of Agricul tu re National Invasive Species Informat ion Center (http://www.i nvasivespeciesinfo. gov). This body has clearly defined invasive species as: (1) non-native (or alien) to the ecosystem under consideration and (2) whose introduction causes or is likely to cause economic or environmental harm or harm to human healt h. What makes an introduced species become invasive? Certai n traits seem key to invasion success (Kolar &

Lodge 2001), including: the ability to reproduce rapidly and both asexually and sexually; fast growth; high dispersal abili ty; the ability to deal with a wide range of environmental conditions and food types, and release from nat ural predators and parasites that con trolled populations in nat ive areas. In particul ar, an important factor in the persistence of invasive species is termed propagule pressure: the rate at which a species is introduced to the ecosystem. Successful establishment has been correlated with th e number of introduction events and number of organisms introduced (or inoculum size; Drake et al. 2005). Therefo re, it is more likely a species beco mes invasive if humans are continually introduci ng it to new areas. The Invasive Species Speci alist Group (http:/ /www.

Three of the world 's top 100 worst invasive species:

issg.org) has produced a Top 100 of the world 's worst

(a) Caulerpa taxifolia (photo: NOAA), (b) The South

invasive species, which includes a range of organisms

African native ribbed mussel ; Au/acomya ater (centre),

causing major problems in marine habitats, such as the

surrounded by the invasive blue mussel Myti/us galfo·

seaweed Cau/erpa taxifofia (a), the mussel fv1yti/us galfo-

provincia/is (photo: Martin Attrill), (c) Carcinus maenas

provincia/is (b) and the crab Carcinus maenas (c) .

(photo: Ar Rouz).

Cauferpa taxifofia is a popular decorative alga used in

fish tanks and seems to have been introduced acciden-

exceptionally fast and is able to cover 100% of the sea-

tally into the Medi terranean in 1984 from the Oceano-

bed, smo thering all native sessile invertebrates, algae,

grap hic Museum in Monaco. By 2000 it had colonized

and, in particular, the seagrass Posidonia oceanica. Inva-

13 1 km' of seabed at 103 locations along 191 km of

sion of seagrass beds seems particularly successful when

coast (Occhipi nti-Ambrogi & Savini 2003). The aquarium

seagrass has already experienced some decline due to

strain of th e alga (cap tive bred to be resistent) grows

other human pressures; dense meadows seem to rest rict

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

C. taxifofia to the bed margins, but impacted beds seemed too fragile to resist the progagule pressure (Occhipint iAmbrogi & Savi ni 2003) and competitive ability (Pergent et al. 2008) of the invader. C. taxifolia has been rep lacing Posidonia across the Mediterranean where it can invade damaged beds, vastly reducing native speci es' diversity and fish hab itat; the seawee d also prod uces toxic substances (caulerp enynes) aiding its invasion. More recent ly, the same Caulerpa strain has been documented in Californi a (Jousson et al. 2000), where $US6 mill ion w as spent up to 2004 trying to eradicate it, and in 2002 it appeared in Sydney Harbour. A second Caulerp a species (C racemosa) has more recently been introduced to the Mediterranean from Australia, the first record being off Lybia in 19 9 0 (Klein & Verlaque 2008) and in the following 17 years it has spread quickly to 12 countries and all maj or islands in the Mediterraean. This invasion event could be one of the most serious in the Mediterranean (Klein & Verlaque 2008), but has not received as much attention as C taxifolia. f\1ytilus galfoprovinicialis is native to the Mediterranean and surrounding areas, but in 19 7 4 was introduced to the west coast of South Africa, most li kely through ballast w ater. It spread dramatically (about 11 5 krn -year" ") and now occupi es available rocky shore along the whole of the west coast of South Africa and at least the southern half of Namib ia (Branch & Steffani 2004). Its rapid spread w as due to a series of key features of the invader itself and also the nat ive communi ty, such as t he high productivity and strong wave action of the South African West Coast, a lack of predators and parasites, and the mussel's fast growth and high rep roductive output. Indigenous mussels have been competi tively displaced in the interti dal, particularly the endemic species Aulacomya ater, and the new mussel matrix has also affected the grazing ability, and thus population, of som e native limpet speci es such as Scuteflastra argenvilfei (Branch &

Changes to the global cover of seagrass have raised much recent concern, Green and Short (2003) stating that 15% of seagrass worldwide had been lost over the 10-year period up to 2003, due mainly to a combination of human activities. However, seagrass within the northern hemisphere, particularly Z. marina, was devastated du ring the 1930s by a mysterious wasting d isease that killed massive areas of seagrass and resulted in the loss of many beds in Europe and Nor th America. The culprit was identified as a slime mould Laby rinthula zosterae, causing brown spots to appear on the leaves, whic h spread to the shoot wit hin weeks. Many of the surviving beds were located wit hin

Steffani 2004). However, this invasive species has had some unexpected positive effects. The African black oystercatcher, Haematopus moquini, is one of Afric a's rarest wadi ng b irds, wi th a population that was as low as 3000 pai rs (Coleman & Hockey 2008). The rapid colonization of rocky sho res by large f\1. galfoprovincialis has provided a new, more accessible, and widesp read food source for t he oystercatcher, result ing in an increase in t he popul at ion size and a much more successful breeding rate: in 19 7 8 only 10 % of pai rs raised two chicks, which had increased to 30% by 1988. Carcinus maenas is the most common intertidal and

estuarine crab in northern Europe, yet its introduction to other parts of the world through ballast and aquaculture has caused large problems, particularly in estuaries along t he east coast of the USA where it w as first recorded in 181 7 . This crab is now found on the west coast of the USA , whe re it grows larger than in other areas; it also occu rs in Aust ralia. In general, Carcinus is a maj or pest of the shellfish industry. In the USA, Carcinus potentially interacts wi th th e native estu arine blue crab Calfinectes sapidus, th e two crabs' abundance being neg atively cor-

related, although Calfinectes may in this case show resistence to the Carcinus invasion as the European crab is not found in Ch esape ake Bay w here Caflinectes is com mon (DeRivera et al. 2005). However, in California, Carcinus predation has affected the spread of another introduced species. The clam Gemma gemma has been present in Bodega Harbor for nearly 50 years wi thout showi ng signs of be ing invasive, but t he situa tion changed upon t he arrival of Carcinus in 1989 (Grosholz 2004) as the crab beg an preferentially predati ng th e nat ive Nutricola clams freeing up space on the shore for Gemma to spread. It is clear that invasive species can also have indi rect effects and positive interactions wi th other alien species that may be difficult to predict.

estuaries, from where d ispersal and recolonization could occur. It has been suggested that the salinity tolerance of the seagrass was greater than th at of the slime mould, allowing some beds to survive in reduced salinity refug ia (Durako et a1. 2003) .

10.3.3 Reproduction and growth of seagrasses Seagrasses can reproduce both sexu ally and, rarely, asexually (e.g. through f r agments of drifting r h izom e) ,

the prominence of sexual reproduction within beds vary-

10.3 Seagrass meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

ing widely across species and geographical location. The majority of seagrass genera are dioecious, which is relatively rare in terrestrial angiosperms and has been suggested as a way of avoiding self-fertilization (Hemminga & Duarte 2000) .

coatings of Zostera) . However. evidence suggests they do not disperse far from source. 80% of Zostera seeds from a

Chesapeake Bay population remaining within 5 m of their bed of origin (Orth et al. 1994). The seedlings themselves may also be a dispersive stage, while in the two viviparous genera (Amphibolis and ThalcLssodendron), the seed-

lings develop attached to the mother plant. However, it would appear that the survival of both seeds and seedlings is very low indeed, the probability that any given

Dioecious-having separate male and female plants.

Flowers tend to be produced seasonally, even in tropical species where it often coincides with very high spring

shoot will successfully establish a new seagrass genet is 1000 years old

extension of the below-ground rhizomes into uninhabited surrounding soft sediment (as long as the conditions of that sediment favour seagrass growth), eventually producing a new shoot unit, or ramet. Growth rates vary

(Reusch et al. 1999b) and represents the largest known marine plant, covering a total area of 6400 m 2 and weighing approximately 7000 kg! In contrast. flowering occurs relatively commonly within intertidal Zostera beds, such as those in Northern Ireland. It appears that disturbance and stress enhance seagrass flowering, and thus sexual

considerably between species but tend to be related to the size of the seagrass, with a negative relationship between rhizome diameter and horizontal extension rate (Duarte

1991; Fig. 10.l4a) . AI; a result, the smallest species, such as Halophila ovalis (Fig. 10.lIb), can spread up to 5 m y '

reproduction, compared with more stable subtidal beds, which favour vegetative growth.

and are often regarded as pioneer species in multi-species meadows. Rhizomes can also branch. allowing a twodimensional colonization of new sediment.

Practically all seagrass species have hydrophilous pollination, a development within seagrasses that allows survival in marine systems, pollen being released into the water column to fertilize female flowers (Hemminga &

The time between the development of two seagrass

Duarte 2000) . The resulting seeds vary in their disper-

units is known as the plastochrone interval and is a use-

sal ability; some species have negatively buoyant seeds (e .g. Halodule spp.) that will not travel far, while others possess structures that enhance buoyancy (e.g. the seed

ful measure to compare growth rates between species

(oj

--... ----

1000

9 0 0

0

100

-r

I

0

00

~

~

0 0

~

g

=

0

~

0

0

t

0

~

-

E

0

0

:;;

-a

-.., -."= -

0

E

g

0

10

~

0

g

0 0

N

.~

0 0

g

I 05

7

6

~

5

T\

pi'

4

II 3

0

~

8

~

g

=

10

(bl

g g

g g

and under different environmental conditions.

,

,

,

,

1.0

2.0

4.0

8.0

I

16.0

~ .t

2

o

"-

[Y

,

,

,

,

,

,

,

,

611/90 911/90 12/1/90 313191 611/91 911/91 12/1/91 3/2/92 6/1/92 9/1/92

Rhizome die meIer (em)

Dete

Figure 10.14 (a) The growth of seag rass rhizomes of different sized seagrass species rhizomes grow faster. (b) Seasonality in seagrass prod uctivity-Zostera

smaller species w ith thi nner

marina off Washington State, USA.

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Leaf growth can be highly seasonal in temperate species, relating to temperature and especially light levels. A study on Zostera marina on the west coast of the USA exemplifies such seasonal patterns of production (Nelson & Waaland 1996; Fig. 10.14b), peak summer values being 6.5 times those in winter. Unlike the beds themselves, leaves do not live particularly long, with a lifespan generally shorter than land plants (Hemminga et al. 1999) . Leaf age also varies considerably between species (up to a year for Posidonia oceanica), but most will shed leaves throughout the growing season (e.g, Zostera mean leaf lifespan is < 100 days), resulting in large amounts of plant organic matter entering the coastal ecosystem; in dense seagrass areas (e.g. parts of the Mediterranean) much of this litter can wash up on beaches, where in some locations it has been harvested by local people for use as an agricultural fertilizer.

10.3.4 Factors structuring the assemblages associated with seagrass Seagrass meadows make available a high level of physical structure within what is usually a comparatively homogenous, featureless subtidal habitat. Additionally they are highly productive systems (from both the seagrass and the associated algae) and so provide potential food and shelter for a wide range of organisms. Many studies have demonstrated that seagrass beds have a richer associated community than surrounding soft sediments. including invertebrates living in the sediment and on seagrass blades (Connolly 1997; Lee et al. 2001), larger mobile invertebrates (e.g. crabs, cephalopods), and certain fish that shelter within the meadow (Jackson et al. 2001) . This is perhaps not surprising as seagrass clearly provides a complex structure within which animals can hide from predators, and also provides completely new habitats (e.g. the leaves) that will host species not found in soft sediment. Lee et al. (2001) highlighted this, by demonstrating that all invertebrates recorded living in soft sediments off Hong Kong were also present in adjacent seagrass beds, but 48 additional species were only found associated with seagrass. However. the structural complexity of the habitat may not be the only factor influencing this boost in species diversity. Edgar (1999) undertook some elegant experiments with artificial seagrass and found that a much richer community developed in treatments that also included seagrass detritus than those with simply artificial leaves. He concluded that small invertebrates required the provision of food and showed little dependence on solely the seagrass structural characteristics.

Some fish are only found in a certain habitat, such as seag rass beds. These are termed obligate inhabitants,

and wo uld disappear with loss of habitat. Other fish use the bed o ut of 'cho ice ' at certain times of the day. These are known as facultative inhabitants.

Seagrass beds have an important role as a nursery ground for the juveniles of commercially important fish

species (Jackson et al. 2001) . For some species, the physical habitat is key as a shelter from predation, but other fish are attracted to seagrass beds due to their supply of food in the form of invertebrates; Jenkins and Hamer (2001) demonstrated that King George whiting (Sillaginodes punctata, Fig.1O.15b) juveniles tended to be associated with density of their prey (small crustaceans) as much as seagrass habitat. Clearly, seagrass beds are important due to a combination of shelter and food supply. Similarly, seagrass beds may attract larger predators too, preying on the small fish and larger invertebrates sheltering in the bed. Predation pressure has been suggested to be a major force structuring the assemblages found within seagrass beds. For example, denser parts of seagrass beds (i.e. those with more shoots per metre) have been shown to provide more shelter for prey items (Edgar & Robertson 1992). Predators maybe expected to forage less efficiently in dense. thick seagrass, thus providing a refuge for smaller animals . A further factor that may influence the success of predators is distance from the edge of a bed, the presumption being that the further in the bed a prey organism is. the harder it is for predators to reach it. This has been demonstrated in a range of experiments where survival of prey in the field has been measured; Bologna and Heck (1999), for example, reporting that bay scallops (Argopecten irradians, Fig. 1O.15a) living along edges of beds, suffered a higher predation than those within the meadows. However. these scallops on the edge also seemed to grow quicker. so there may be a trade-off between survival and growth. A method used to assess relative predation levels in seagrass beds is tethering. Prey items (e.g. prawns) are attached to lines and placed within different parts of the seagrass bed. Comparative losses to predation can then be recorded (e.g. Hovel & Lipcius, 2001) . Gorman et al. (2009) tethered juvenile cod (Gadu.s spp.) over a range of seagrass patch sizes and found highest predation levels occurred on the edges of intermediate size patches (25 m 2 ) , suggesting predators may be attracted to larger patch areas because of increased prey numbers. but patches of this size do not provide enough safety for prey. Seagrass beds also host their own predator species, which utilize cryptic camouflage to hide within the canopy and feed

10.3 Seagrass meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

off small invertebrates and, occasionally, fish. The bestknown group are the Sygnathidae-the pipefish and seahorses (e.g. Hippocampusjayakari, Fig. 10. 15c) which can

Figure10.15 Organisms using seagrass beds as cover.

(a) The bay scallop Argopecten irradians within a seagrass bed (photo: Dave Clausen). (b) King George whiting Sillaginodes punctata (photo: Peter Macreadie). (c) The cryptic predatory fish Hippocampus jayakari (photo: Ole Johan Brett).

be found associated with seagrass beds across most of the world. Seahorses, in particular, have a very high conservation status. resulting in protection ofseagrass beds in some regions (see also Chapter 14). Additional to theories on predation refuge, there is a direct relationship between the structural complexity of a meadow and the associated organisms. which also can explain their distribution within a bed. A5 a habitat becomes more architecturally complex. it is expected that more niches will become available. allowing higher numbers of species to be supported. Such a relationship has been observed with coral reef fish and cactus-dwelling insects, for example. Similarly. there have been clear examples within seagrass beds of measures of complexity being related to diversity. Webster et al. (1998) demonstrated a positive relationship between shoot density and associated invertebrates. while several classic studies have positively related seagrass biomass to the number of species recorded (e.g. Heck & Orth 1980). Increasing seagrass biomass has been seen as an analogue for seagrass complexity, but Attrill et al. (2000) raised an alternative explanation that high seagrass biomass simply provides a greater leaf area (due to the two-dimensional nature of the leaves) and so the relationship is a species-area effect; more species are recorded because a greater area has been sampled. Attrill et al. (2000) highlighted this by demonstrating a close relationship between diversity and seagrass biomass. but not with alternative measures of structural complexity (Fig. 10.16) . Whatever the reason, thicker, healthier beds do seem to provide a more favourable habitat for increased diversity. At a larger spatial scale, the structure of a seagrass meadow itself can also affect the assemblage oforganisms associated with it. A key concern in seagrass (and terrestrial) ecology is the fragmentation of beds (habitat) into smaller patches. Patchy beds can be naturally generated by specific environmental conditions, but much fragmentation of continuous beds is due to human activities, such as damage caused by boat anchors. propellers. or moorings (Fig. 10.17) . Habitat fragmentation has a range of consequences that impact organisms living within that habitat. The overall area of the seagrass can be reduced, which may impact big species requiring a comparatively large territory. so the relative importance of fragmentation for conservation is a major issue : is one large area better than several small areas? This has become known as the SLOSS debate: Single Large Or Several Small reserves. A further consequence offragmentation is that discrete patches of seagrass can form islands that are separated from the next patch by bare sediment, potentially isolating organisms from the main population. Crossing this sediment therefore presents a risk, and corridors of vegetation are very important for the movement of species

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

30

•

2l l-

20 -- 15f--

30

••

~

g

l-

Ci. g

~

• •

•

g

'0 g

~

g

10 l-

g

••

• • • • • •• •••

••

•

~

•

g

•

g

•

~

•

-g

~

•

5f-

g

d

z

100

•

2l

~

z

0

-- 20 .::- 15

•

200 Complexily index

300

400

10

•

5 0

100

•• 200

•

..•

•• • • • • • •• ••

300

•

•

• •

•

400 500 600 Seog ro~ biomass (g. OWl)

700

800

900

Figure 10.16 The relationship between invertebrate d iversity and seagrass arch itecture. Attrill et al. (2000) demonstrated that structural complexity was not related to associated diversity, but there was a relationship with seagrass biomass. They suggested this was due to increasing biomass providing a larger area to sample, and so

more species were encountered .

such as crabs (Micheli & Peterson 1999). Fragmentation also increases the edge effect within seagrass habitat. a patchy bed having a much larger edge:area ratio than continuous beds. Previously we saw how predators are potentially much more successful at the edges of beds, so increasing the amount of edge can increase overall predation pressure. Fragmentation can also change water flow and sediment deposition, and ultimately physical conditions within a bed. While the detrimental impact of fragmentation on land is comparatively well-accepted, evidence from seagrass beds is more equivocal. Bowden et al. (2001) demonstrated higher diversity of sedimentdwelling invertebrates in large Zostera marina patches than small ones, but McNeill and Fairweather (1993) found that several small patches had a higher overall diversity than continuous patches of the same area. Studies into the impact of patch size on predation pres-

sure have also produced contrasting results. Irlandi et al. (1999), for example, worked on the role of fragmentation on the survival ofthe same scallop species as Bologna and Heck (1999), but found no consistent patch size effect. The sea is a relatively open system , as there are rarely any barriers at a localized scale to organ ism dispersal through the water between habitat 'islands" unlike between two forest areas, for example. Factors such as

the longevity of the larval dispersal phase and mesoscale oceanic physical barriers determine connectivity between different areas of the sea.

The consequences of fragmentation within the marine environment (beyond the detrimental loss of overall area) require further investigation, but processes involved may be quite different in this open system to those on land.

Figure 10.17 Zostera marina

bed in Jersey, English Channel. The clear patches are gaps in the seagrass meadow caused

by the physical impact of mooring chains used by the

yachts. (Photograph: Emma Jackso n/ Paul Tucker.)

10.3 Seagrass meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

However. there is one further scale of organism size reliant on seagrass where seagrass loss may have more notable consequences.

10.3.5 Seagrass as a food supply for large grazers The majority of small grazers, such as gastropod molluscs and amphipods, which inhabit seagrass beds generally feed on the epiphytic algae, rather than directly grazing the seagrass leaves. Such grazers therefore potentially have a role in limiting the growth of such algae within seagrass beds, and thus could influence the productivity of the seagrass itself by preventing algal overgrowth and shading (Williams & Ruckelshaus 1993). Additionally, invertebrate grazers may be key in reducing the impact of increasing nutrients within coastal systems, which may favour growth by algae over seagrass (10.3.2), although experiments are so far inconclusive (e .g. Keuskamp 2004) . The only invertebrates that demonstrate a major grazing impact on the seagrasses themselves are sea urchins, with examples of overgrazing apparent across the globe in tropical and temperate waters (Eklofa et al 2008) . An example is Lytechinu.s variegatu.s, which can occur in huge numbers (up to 360 m-2 ) within seagrass beds off the east coast of North America. The urchin has been demonstrated to seriously overgraze beds in Florida, removing (for example) nearly 0.8 km- of meadow in 8 months (Rose et al. 1999). The major direct grazers of seagrass are. however, marine vertebrates, in particular two groups: the turtles and the sea cows (Sirenia) . Both groups have representative species that feed primarily on seagrass and can have major impacts on the growth. productivity. and structure of seagrass meadows. The green turtle (Chelonia mydas, Fig. 10.18b) grazes primarily on Tholassia testudinum (hence its common name, turtle grass, Fig. 10.18a), particularly in the Caribbean and adjacent tropical regions. The green turtle is actually brown , so its name may appear somewhat inappropriate. However, it was named

after the colour of its fatty flesh. The turtles were hunted primarily to make turtle soup.

Young turtles are pelagic omnivores, but once they reach 20 to 35 em in size they begin benthic foraging, preferably on seagrass, though they will graze on algae where seagrass is not available (BjomdaI1980) . Adults demonstrate a die! feeding pattern, resting during the night (e.g. on coral reefs) and foraging during the daytime. Their specific foraging strategy depends on the seagrass density. In high-density areas turtles are selective, avoiding older leaves or those covered in epiphytes. and consuming the

Figure 10.18 (a) Tha/assio testudinum is known as turtle grass (photo: NOAA). (b) The green turtle, Chelonia mydos, which grazes primarily on seagrass, giving the seagrass its

name (photo: www.adakris.com). young leaves or leaf tips, which are more nutritious and have lower lignin content. Turtles are seen to return to the same feeding area in order to graze newly grown vegetation. This continued grazing stresses the plant, resulting in reduced leaf production, so eventually these feeding areas are abandoned. In beds oflow density, turtles are less selective and forage more widely. Four extant species of Sirenia exist: three species of manatee (Fig. 10.19), and the dugong (Dugong dugan) . Manatees are not seagrass specialists; while they feed off seagrass when in salt water, manatees spend much time in freshwater where they forage on submerged vegetation. For example, water hyacinths are a staple food for the West Indian manatee (Trichechus manatus) in many Florida rivers. The dugong occurs in the Indo-West Pacific region and is more strictly marine, with seagrass forming the main diet. Unlike manatees. dugongs can feed in large herds of 100 to 200 individuals, particularly in the extensive seagrass beds off northern Australia. Unlike turtles, dugongs often take the whole seagrass plant, roots and all, leaving distinctive feeding trails through the seagrass bed (Preen 1995) . In dugong foraging areas off Australia. the seagrass beds are composed of two main species :

Chapter 10 Mangrove Forests and Seagrass Meadows •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Fig 10.19 Manatees, and particularly dugongs, feed on seagrass and generate d isturbance to the seabed. Manatee use of habitat close to the shore in shallow water, e.g. Florida, makes them vulnerable

to injury by boat propellers. (Photograph: Oxford Scientific/photolibrary.)

Zostera capricorni is the dominant large species interspersed with patches of the fast-growing pioneer Halophila spp.. Dugongs prefer to feed on Halophila as it has a high nitrogen content and low proportion of fibre. and as a pioneer species Halophila is the first to recolonize the disturbed areas left by dugong feeding. In this way, grazing by herds of dugongs alters the species composition of the seagrass meadow, stimulating the growth of Halophita, and herds have been observed grazing the same location for up to a month as they crop the new growth of Halophila within their grazing trails. This activity has been termed cultivation grazing, as the dugongs' feeding results in a greater proportion of their favoured food supply.

m-2 y-l) and borealforests (800 gm-2 y-'; Whittaker 1975). Seagrass beds therefore provide large amounts of carbon for input into coastal systems. supporting food webs and commercially important species such as prawns (see Loneragan et al. (1997) in 10.2.7, for example) . The high leaf biomass produced by seagrass beds is also harvested by humans for a range of uses, such as packing material. fibre for use in mat weaving, and even seagrass furniture and storage boxes (Green & Short 2003). It is useful to compare seagrass productivity with that of other systems: savannah> 900 9 m- 2 boreal forests = 800 g m- 2 y-' , lakes and streams = 250 g m- 2 Rainforests, however, produce 2200 9 m~2 y-' (Whittaker

v:'.

r' .

19 75). As well as four existing species of sea cow, a further species (the 10-m long Stellers sea cow, Hydrodamalis gigas) was hunted to extinction by 1768-within 30 years of its discovery in the Arctic waters of the Bering

Strait.

10.3.6 The wider role of seagrass meadows As well as providing a habitat maintaining high levels of biodiversity. a nursery ground for fishery species, and providing food for large endangered grazers, seagrass beds perform other critical functions that make them valuable to both coastal ecosystems and humans (Green & Short 2003) . For a marine ecosystem, seagrass beds have exceptionally high biomass and productivity: Duarte and Chiscano (1999) estimated an average production of 1012 g dry weight m-2 y-l. This is higher than other marine primary producers, such as macroalgae (365 g dry weight m-2 y-l) and phytoplankton (128 g dry weight m-2 y-l), and comparable to key terrestrial systems such as savannah (900 g

Seagrass beds also provide key ecological services. The root-rhizome system enhances sediment stabilization and thus prevents erosion, while the foliage slows water currents through their baffling effect. encouraging sediment to settle and preventing resuspension. Extensive seagrass beds therefore are stabilizing features within the coastal landscape, and provide a natural form of coastal protection. In the low-lying Wadden Sea (Netherlands), seagrass debris was traditionally used to make dykes. and restoration of Zostera marina beds through transplantation is being investigated as a natural barrier to protect the coast (van Katwijk 2003) . Perhaps the greatest value of seagrass beds is. however, indirect roles in water purification and nutrient cycling (Green & Short 2003) . Through sedimentation processes and the active uptake of nutrients into the seagrass meadow ecosystem. large seagrass beds can be effective in removing nutrients from the water column and trapping them for a comparatively long time in leaflitter; most algal-dominated or planktonic systems have a much quicker turnover of nutrients. Seagrasses can therefore help mitigate problems

10.3 Seagrass meadows • ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

of eutrophication (10.3.2) and even bind organic pollutants. Similarly. seagrasses can help drawdown and remove carbon dioxide and play some role in the amelioration of climate change, particularly species such as Posidonia oceanica whose root-rhizome matte can persist for hundreds of years. While their overall impact compared with phytoplankton in the world's oceans will be low, their high productivity gives them a disproportionate influence in coastal systems (Green & Short 2003).

Seagrass beds therefore provide a range of goods and services of benefit to coastal ecosystems and humans (see Chapter 16). Costanza et al. (1997) attempted to put an economic value on the world's ecosystems relating to these services, suggesting seagrass/algae beds are worth $19 004 ha- 1y-1, mainly due to their nutrient cycling role. Green and Short (2003) therefore estimated the global value of seagrasses to be $3.8 trillion (i.e. $3.8 x 1012 ) , but pointed out that this does not represent the total worth of the ecosystem and is not a purchase value!

The matte of Posidonia can be roug hly aged due to known growth rates. It has therefore been used to date

old wrecks in the Mediterranean!

Chapter Summary •

Mangroves and seagrasses are both 'true plants' and their aggregations represent two of t he most valuable marine hab it ats in the world, being highly productive and with a very high associated biodiversity.

•

Mangroves are found mainly in the tropics and are woody trees that can flourish at the land/sea interface. Through morphological and physiological adaptations, mangroves can deal with their roots being in waterlogged, anoxic sediment, and can tolerate the high levels of salt, surviving in conditions that would be fatal for most plants.

•

A dynamic mix of terrestrial and marine organisms share mangrove forests. They are important sites for many bird species, including species of hi gh conservation status such as scarlet ibis.

•

Crabs are t he most important marine group of organisms associated w ith mangroves, their burrowing activity and consumption of leaf litter being important for carbon cycling and in turn ing over the sed iment (which affects the production of mangroves).

•

Mangroves have an important wider role, exporting carbon to surrounding areas, protecting the coast from erosion and providing a nursery area for many fish species, including those from coral reefs.

•

Seagrasses are the only angiosperms that can survive fully submerged in the marine environment. They are found across the world's coastal seas and can form huge meadows covering 1000s of km 2 •

•

Meadows mainly form in shallow subtidal soft sediments in clear water, but can extend int o the intertidal zone or even grow on rocks. In the clear waters of the Mediterranean, Posidonia beds can grow down to 40 m.

•

Seagrass leaves form a substratum for the settlement of a d iverse epiphyte community. The relationship between seagrass and algae is complex, and can be altered by increased nutrient levels that favour the algae, outcompeting the seagrass.

•

The physically complex nature of seagrass beds, compared to surrounding bare sand, results in meadows having a high associated biodiversity of marine animals (invertebrates and fish). The diversity and abundance of animals is associated directly with the amount and complexity of seagrass that is present, from the density of shoots to the overall areal cover of seagrass.

• The global cover of seagrasses has been reduced dramatically (15% from 1993 to 2003) as they are sensitive to changes in light levels, nutrients, and human mechanical disturbance.

Chapter 10 Mangrove Forests and Seagrass Meadows

Further Reading Books •

Green, E, P. & Short, F. 1. 2003, World Atlos of Seaqrasses. University of Cal iforn ia Press,

•

Hemminga, M, A. & Duarte, C M, 2000, Seogross Ecology Cambridge University Press,

•

Hogarth, P. J. 19 9 9, The Biology of Mongroves, Oxford University Press, Oxford ,

Key papers and reviews •

Alongi, D,M, 2002 , Present state and future of the world's mangrove forests, Environmental Conservation 29: 331 -349,

•

Duarte, C. M. 2002. The future of seagrass meadows. Environmental Conservation 29: 192-206.

•

Jackson, E" Rowden, A.A., Attrill, MJ" Bossey, SJ" & Jones, M,B, 200 1, The importance of seag rass beds as a habitat for fis hery species, Oceonogrophy ond Morine Biology: on Annuol Review 39, 269-303 ,

•

Molnar, J.L" Gamboa, R.L" Revenga, C , & Spaldi ng, MD, 2008, Assessi ng the g lobal threat of invasive

species to marine biodiversity. Frontiers in Ecology and the Environment 6: 4 8 5-4 9 2. •

Ropert-Coudert, Y. & Wilson, R.P. 2005. Trends and perspectives in animal-attached remote sensing. Frontiers in Ecology and the Environment 3 , 4 3 7-444.

Coral Reefs

Chapter Summary

silently above them observing the inhabitants. Indeed, reef

The first sight of a coral reef has inspired many to seek a

research has burgeoned with the advent of widely available

career in marine b io logy. The bands of bright colou r fringi ng

scuba-diving gear in the 1950s. However, for millions of

the coasts of tropical islands and highlighting small coral

people in the tropics, reefs are not only a source of fascina-

atolls in an otherwise deep-blue ocean are a marvel to most

tio n, but thei r mai n source of food, buildi ng materials, and

of us and attract a globally significant tou rism business.

income. The activities of bu rgeoning human populations

These reefs can be hund reds of metres thick, and yet they

are th reateni ng co ral reefs around th e world, and although

have been built by a thin veneer of living coral tissue. Spe-

reefs can be highly productive, growth of the reef itself can

cies' diversity on reefs can equal that in rainforests, but reefs are probably more accessi ble because you can float

be a transient process, easily upset by changes in climate,

11. 1 Introduction Coral reefs support some of the most diverse and productive communities in the marine environment. Living corals create limestone formations that may be thousands of kilo metres long and hundreds of metres deep. While the sm all polyps that form living coral are best viewed under a microscope, limestone coral reefs are clearly visible from space. Coral reefs const itute a shallow, productive, and brightly illuminated ecosystem, supporting an am azing diversity of plant and animal species . In many areas, by providing protection from wave ene rgy, they also help foster ecological oases such as of mangroves and seagrass beds (Chapter 10) , in otherwise deep and oligotrophic oceans. Coral reefs are an iconic ecosystem; they figure prominently in advertising, attract major tourism and exemplify the complexities of the marine environment. This chapter describes the global distribution and typology of coral reefs, the biology of reef building corals, and the factors that influence their growth and reproduction. We will look at the productivity of re efs, and the biology and diversity of animals supported by this production and

sedimentation, fis hing, and pollution.

habitat. Despite their vas t size, reefs are among the most sensitive of marine habitats to human disturbance; they are in fact the marine ecosystem most threatened with anthropogenic degradation. We consider the roles of climate change, fishing, and pollution in driving this degradation.

11.2 Reef development and distribution From the seafarer's perspective, reefs are rocks close to the sea surface that can damage a ship's hull. However, coral reefs are distinct because they are biogenic, or deposited by living organisms (Veron 2000). Growing corals and calcare ous algae deposit carbonate and this can form vas t limestone structures that raise the living reef high above the surround ing seabed. Thus, the Great Barrier Reef in Australia extends for 2000 km and has an are a of 48 000 km-, and Enewet ak Atoll in the tropical Pacific is over 1300 m thick. While the reef at Enewetak Atoll is probably 50 million years old, most of the limestone that forms the structure of the Great Barrier Reef was deposited in the last 500

Chapter 11 Coral Reefs •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

000 years and most modern reef grow th d ates only from the last 10 000 years, during the present interglacial period (Holocene) (Chapter 1). Most reefs are found within a band 30° north or south of the equator (Fig. 11.1 ) . The extent of shallow-water coral reefs worldwide is 284 300 km- (Table 11.1 ) ; this is only around 3% of the total tropical continental shelf area but is inordinately rich in terms of biodiversity. Coral reefs cover q....

'J~~

q.~ q.~ ~oS'

Daily mean soil temperatures

~

/0

:.

~

~

of the most hostile places on Earth for life to survive, but surprisingly they support considerable life. Contrary to the

~"\

5

deep into pack ice, throughout the year. They become floating laboratories and are key to the rapid progress

·50 · ·5 > · 5. < 0

o

no chongefinaeose

13.9 Environmental impacts of fishing •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

gests that the current biomass oflarge fishes weighing 4-16 kg and 16-66 kg, respectively, is now 97'4% and 99·2% lower than in the absence of fisheries exploitation, while the community biomass (fishes 64g to 66kg) is 38% lower than predicted in the absence of exploitation. Community biomass is less affected because small and intermediatesized fishes can still be productive at high rates of fishing (Jennings & Blanchard 2004) . Throughout the world's seas, there are examples oflarge, slow-growing species becoming locally and regionally extinct. These include groupers and large parrotfishes on tropical reefs and sharks and skates in the Atlantic (Dulvyet al. 2003).

13.9.2 Birds and marine mammals

mortality rates do not threaten the long-term viability of the population (Allen 1985; Hall 1996) . However, while many

consumers were concerned about dolphins. far fewer were concerned about sharks, and it has become clearthat shark by-catches in tuna long-line fisheries have led to worldwide collapses in some shark populations (Baum et al. 2003). Seabirds are caught by accident in long-line and gill

net fisheries . There is particular concern for the viability of wandering albatross (Diomedea exulans) populations because these albatrosses are frequently caught on longlines used to catch southern bluefin tuna (Thunnus maccoyii) and Patagonian toothfish (Dissostichus eleginoides) in the Southern Ocean (Fig. 13.14) . The bluefin runa fleet deploys 107 million baited hooks annually and killed 44 000 albatrosses prior to 1989. Despite the introduction of

some conservation measures, this albatross could decline to extinction ifhook numbers are not dramatically reduced. Seabird catches on long-lines are an inconvenience for

Fishing is often most vehemently criticized when birds, marine mammals, and turtles are taken as by-catch. These impacts have consistently attracted more public attention than the impacts offisheries on fish, and have forced fishery closures and significant changes in fishing methods. Mass dolphin mortality in the eastern tropical Pacific tuna purseseine fishery during the 1960s and early 1970s attracted

birds. However. some bird populations have already been so

considerable public attention and provoked widespread criticism ofthe environmental impacts offishing. Hundreds

depleted by fishing that any further by-catches are likely to threaten their viability (Weimerskirch et al. 1997).

the fishers as well. They lose bait and have to reset the lines.

Conservation measures introduced include bird scarers and devices that set the lines below the diving depth of the

of thousands ofdolphins were killed annually because purse

seiners set their nets around pods of dolphin to catch the tuna that swam with them. When the nets were hauled. the

13.9.3 Trawling impacts on the seabed

dolphins were trapped and usually died. By 1980, the population ofeastern spinner dolphins (Stenella longirostris) was reduced to one-fifth ofits original abundance. Intense pub-

When trawls are dragged over the seabed, they are bound to kill animals and damage habitats. The significance of trawling impacts depends on the habitats where they are fished and levels of narural disrurbance on the fishing grounds. On sandy seabeds in shallow, tide-swept, and wave-impacted

lic pressure and consumer boycotts of tuna products led to new fishing practices to release trapped dolphins alive and

the use of observers to monitor dolphin mortalities on all • purse seiners.

areas, most of the animals living on and in the seabed are

and line caught 'dolphin friendly' tuna. Levels of marine

very well adapted to high rates of mortality and disrurbance, and the effects of trawling are relatively minor (Chapters 8 and 15) . Conversely, in deep areas where wave and tidal action are low and the seabed habitat is dominated by habi-

mammal by-catch in most fisheries are now set so that the

tat-forming (biogenic) species. trawling can have major and

Today, annual dolphin mortality is less than 5% of that

in the 1970s. and consumers increasingly purchase pole

(0)

~

:AI;

(b)

Figure 1 3.14 (a) A drowned black-browed albatross caught up in the meshes of a trawler fishing in the Southern Seas.

(b) These shags became entangled in a ghost-fishing bottom-set gill net while trying to extract the gadoid fish (middle). (Photographs: (a) Richard Woodcock (b) Blaise Bullimore.)

Chapter 13 Fisheries long-term impacts that reduce both biomass and diversity (Jennings & Kaiser 1998; Kaiser & De Groot 2000). Typical examples of vulnerable habitats are maerl beds, coral reefs, and the biogenic habitats on sea mounts. The impacts

of trawling on sea mounts are perhaps the most dramatic described to date (Box 13.3 ). Simple empirical and modelling stud ies have shown that many seabed species w ill be extirpated if trawling frequencies exceed 2 to 3 times per year. However, large-scale stud ies of the distribution of fauna on many major fishing grounds

show that many vulnerable species persist. The reason for this is that trawling d isturbance is actually very patchy (Fig. 13.15). While m any shelf seas are swept, on average, at least twice each year, fishers tend to return to favoured fish-

ing grounds and trawl tows that they know to be free from obstructions. As a result, some areas may be trawled 10 to 15 times each year, while adjacent areas are vir tually unfished. Provided that spatial patterns of effort are consistent from year to year, animals can recolonize fished areas from those that remain unfished. Management measures that increase the long-term homogeneity of effort, such as rotating closed areas, m ay increase the cum ulative effects of trawling. In add ition to the changes to ecosystem processes caused by bottom fishing d isturbance, alteration of the seabed may also change its functional importance for associated target species. In other words, not only does fishing deplete fish stoc ks, but it may also adversely affect their habitat. This

Box 13.3: Trawling impacts on sea mounts

re alization has sparked a flurr y of activity to identify wh at has become termed 'essential fish h abitat'. Amendments to the US Magnuso n-Stevens Act require fisheries m anagers to co ns ider the wider ecological impacts of fishing ge ars upon fish h abitat in addition to issues such as fishing effort control and total allow able catches (Auster & Langton 1999 ). Essential fish habitat (EFH) is a description open to interpretation, but it is clearly defined w ithin legislation to mean 't hose waters and substratum necessary to fish for spawning, breeding, feeding or growth to maturity'. This legislation is an important step towards an ecosystem based fisheries management (13 .10) as it recognizes the potential negative effects of the direct and indirect effects of fishing on fish populations. The introduction of this legislation caused a hiatus among m anagers, w ho we re faced w ith the t ask of identifying EFH for a multitude of species. This revealed large voids in our knowledge about the basic biology of many of the species currently under management. Some elements of EFH, such as spawning and nursery areas, are relatively well-known for the majority of com mercially explo ited species, and in many cases these are already afforded some protection by permanent or seasonal area closures. Nevertheless, for some particularly vulnerable species, such as rays, we know w here breeding aggregations occur, but the habitat into which the eggs are laid remains open to speculation . However, of equal relevance are the habitat quality issues that affect the acquisition of food and the

as fishing vessels can now 'mine ' them for stocks of longlived and slow-growi ng species, such as orange roughy

Technological development of fishi ng gears and fish-

(Hofpfostethus atfanticus). Electronic positioning systems

ing boats is making more and more habitat accessible

on the vessels and nets can be used to posi tion the net

to trawling. Sea mou nts, once difficult to locate and too

precisely and to traw l on the relat ively ti ny sea mounts

rocky to trawl, have been heavily fished in recent decades,

tha t rise from depths of several kilometres to within 500

A multi beam image of Ely Sea mount. A caldera is visible at the top. (Image: Jason Chaytor/NOAA).

13.9 Environmental impacts of fishing •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

to 2000 m of the surface.

Sea mounts are unique deep-sea environments, and,

sea mounts and has immedi ate knock-on consequences for fish and invertebrates th at use coral habitat.

because they rise from great depths, their topog raphy

When t rawled and untrawled sea mounts are compared,

enhances local wate r cur rents. These currents carry

it is obvious th at the untrawled mounts have a diverse

nutrients and prey over the sea mounts, and rich complex com munities of suspension feeders, such as corals,

inverteb rate fauna of high b io mass, dominated by suspension feeders including hard and soft corals, hydroids,

develop, in contrast to the low biomass communities of

sponges, and brittlestars. Of the inverteb rate species

deposit feeders on the surroun ding seafloor. Many ben-

studied on untrawled sea mounts south of Tasmania,

thic species living in association with sea mounts are new

2 4-43% were new to science and 16--33% we re prob-

to science, long-lived, and vulnerable to traw ling.

ably rest ricted to the sea mo unt environ ment. The benthic

When sea mounts are fished for the first time the nets

biomass on untrawled sea mo unts w as 10 6 % g reater,

can take by-catches of several tonnes of coral! In fact,

and the number of species per sample 46% g reater, tha n

as the first orange ro ughy fisheries developed off New

on traw led sea mounts. The unwanted effects of traw ling

Zealand, there was interest in starting a precio us coral

on these habitats provided justification for establishing a

industry based on black coral by-catch! The damage to

'Mari ne Protected Area' around twelve sea mounts.

coral is the first and most dramatic effect of traw ling on

avoidance of predators. The identification of those habitats that may have an important or 'essential' functional role for individual species is likely to be complex for those species that utilize different habitats at partic ular stages of their life history. For example, many fish species start life close inshore , moving further offshore as they increase in bod y size (Rijnsdorp & van Leeuwen 1996) . It might be relatively straightfor ward to identify EFH for fish strongly associated w ith seabed str uctures, such as reefs or bioge nic habitats (seagrasses, m angroves, oyster beds), however many fish in temperate systems exhibit highly flexible lifestyles and utilize a wide range of different habitat types. Never theless, for such species, it is possible to identify areas that consistently attract the greatest proportion of the population, and presumably these areas fulfil some functional role. Previous studies of the relationship between fish assem blages and their environment have focused on the relationship between fish distribut ion and enviro nmental variables such as salin ity, depth , and substratum type (e .g. Smale et al. 1993). In some cases these variables are good co rrelates of some fish assemblages. They do not necessarily defi ne the essential fe atures of a specific h abitat; rather they constitute a co mponent of that habitat that m ay act as a sur rogate for some other more important habitat feature . Habitat complexity and str ucture appear to be important physical features for some fish species (Auster et aI. 199 7). Many stud ies have demonstrated the relationship between flatfish species and the sediment particle composition of the seabed (Gibson & Robb 1992). For example , small plaice are better able to bury themselves in sediments that have a particular grain-size composition and choose particular sedimentary habitats accordingly. Hence, a specific particle size-compos ition m ay be an essential habitat requirement for flatfish, w hereas the presence oflarge sess ile epifauna or

Source: Koslow et al. (2001) .

•

-.. ....

~

Figure 13.15 The patchy spat ial distribution of bottom trawling activity around the UK in 2007. Each point is the record of a vessel location from a sat ellit e vessel monitoring syst em. (Lee et al. 2010.)

rocky substrata might be considered non-essential. In contrast, str uctural complexity g reatly increa ses the survival ofjuvenile roundfishes as it provides refuge from predation (Tupper & Boutillier 1995) (Box 13.4). Just because we find fish associated with a particular habitat does not necessarily ind icate that the habitat h as an essential functional role. For example , there is great interest in the relatively recent discovery of deep-water co ral reefs on the continenta l shelf edge of the Nort h Atlant ic and elsewhere. These reefs provide prominent habitat features in a relatively uniform seabed landscape and act as foci for fish such as redfish (Sebastes spp.) for w hich there is a commercial fishery. Conser vation gro ups a rgued for the

Chapter 13 Fisheries

Box 13.4: Essential fish habitat organisms, such as sea scallops, o r the t roug hs of sand Biogenic (living) and physical features of seabed habi-

waves provide cove r for silver hake (Merluccius biliniaris)

tats can have a critical function for certain commercially

from where they ambush prey (b). Attached fau na, such

important species. Mud habitats appear to have few large-

as sponges, provide complex th ree-dimensional structure

scale topographic features, but large cerianthid anemone s

in which fish, such as sculpin (Myoxocephalus sp.), can

provide shelter for animals such as spider crab (Lithodes

shelter from predators and ambush their prey (c).

(Photographs: © Peter Auster.)

sp.) (a). Depressions in the seabed formed by other

(01

protection of the reefs on the basis that they provided EFH for the redfish (Malakoff 2004) . However, redfish are found in a wide variety of h abitats across a large geog raph ic area, and despite a concerted research effort evidence of a critical link between redfish ecology and deep-water corals remains uncertain (Fossa et al. 2002; Kaiser 2004) .

13.9.4 Effects of fishing on coral reefs In Chapter 11, we saw that coral reefs are among the most delicate and highly structured m arine habitats. The topogra phic comple xity of reefs provides refuge and feeding opportunities for m any fish and invertebrate species. Areas of act ively growing reefs that h ave not been damaged by human activities can sustain fishery yields of up to 5 tonnes km- year! (Fig. 13.1 6). These fisheries are usually prosecuted by line and spear fishers, who cause minimal d amage to coral and catch a range of species from many trophic levels. However, growing human populations have driven the

(bl

development and expansion of fisheries on tro pical coasts, and fishers are inc reasingly turning to habitat destructive fishing methods to maintain yields. For m any fishers, who have few, if any, alternative so urces of food and income, there is no choice but to do this. Muro-ami drive netting, bottom set gill nets, and heavy traps have all caused habitat destruction on reefs. Muro-ami fishing is widely practised in South-East As ia and involves fishers driving fish towards a net w it h weighted scare-lines that are dro pped repeatedly on to the coral. However, fishing with explosives has even greater effects on reefs. Explosive, blast, or dynam ite fishing is pract ised in m any regions, and although it is often illegal, this is unlikely to deter fishers desperate for food and income. Repeated blast fishing, whe re explosive charges are detonated over and on the reef, soon reduces large areas of actively growing reef to rubble. Needless to say, fisheries of this type are not sustain able, killing manyjuvenile and non -target species and destroying their habitat.

13.10 Ecosystem-based fishery management •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Figure 13.16 Selling fish caught in a coral reef fishery in Fiji.

Photograph: S. Jennings.

Fisheries also have indirect effects on coral reefs. Sea urchins and fishes, such as the colourful parrot and surgeonfishes, are the dominant herbivores on reefs. The persistence of herbivorous fish on reefs depends on the presence offish that eat sea urchins. These urchin predators maintain sea urchin populations at a size where their low gross production makes them poor competitors with herbivorous fish. If populations of urchin-eating fish are reduced by fishing, then urchin populations expand and the urchins graze reef algae to such low levels that herbivorous fish can no longer compete. The dominance of urchin grazers on heavily fished reefs has knock-on consequences for corals. Thus, herbivorous fish clear space for coral settlement, and enhance the growth and survival of young coral colonies, while urchins erode the substrate as they graze and prevent coral recruitment and growth. On heavily fished reefs where urchins dominate the grazer community. bioerosion leads to loss of structural complexity, reduced fish biomass and disruption of the ecological processes responsible for fish production (McClanahan 1992) (see also Chapter 8) .

13.9.5 Effects of fishing on kelp forests As in our last example of the indirect effects of fishing, we look at another situation where urchins playa keystone role. Kelp forests are found in many cool. shallow. and nutrientrich coastal waters (Chapter 8), and support diverse fish and invertebrate fisheries. Sea urchins graze on kelp, and when sea urchins become abundant, either as a result of high levels of recruitment or the indirect effects of fishing, they can graze kelp until the kelp forest ecosystem shifts to an alternative state, known as 'u rch in barren ground'! The extent ofMacrocystis kelp forests offsouthern California has shrunk dramatically since the mid-twentieth century. This is partly the result of changing oceanographic conditions and pollution. but is also due to the depletion of urchin

predators. Both the spiny lobster (Panulirus interruptus) and the sheepshead (Semicossyphus pulcher) were once sufficiently abundant to help limit urchin populations, but this is no longer the case. Ironically, a large fishery that targets the red sea urchin (Strongylocentrotusfranciscanus) has now developed, depleting urchin populations and allowing the reestablishment ofkelp in some areas (Tegner & Dayton 2000) . Compare this example of a fishing effect wit h that of hunti ng of sea otters in Chapter 8.

13.10 Ecosystem-based fishery management Fisheries can provide society with huge benefits in terms of income. food, and employment, but instead. fisheries are often unsustainable and an environmental threat. The ecosystem approach to fisheries management (EAFM) is widely adopted by the current management agencies. The EAFM is part of the ecosystem approach and is consistent with the concept of sustainable development, which requires that the needs offuture generations are not compromised by the actions of people today. The broad purpose of the EAFM is to plan, develop, and manage fisheries to meet the multiple needs and desires ofsocieties. butwithoutjeopardizing the options for future generations to benefit from the full range of goods and services (including, of course, non-fisheries benefits) provided by marine ecosystems (FAD 2003) . The approach is usually geographically specific, adaptive. considers multiple drivers. takes account ofuncertainty, seeks to balance multiple objectives, and involves stakeholders (FAD 2003; Browman & Stergiou 2005; Murwaski 2007) . The success of the EAFM depends on whether high-level governmental commitments to an EAFM can be turned into

Chapter 13 Fisheries specific. tractable, and effective management actions that will lead to better fish-stock management and remedy the unwanted impacts of fishing on non-target species. habitats,

and ecological interactions. With some notable exceptions, such progress with implementation has been slow to date (Pitcher et al. 2009) . Moreover, implementation of EAFM will not remove the high, short-term costs of moving towards sustainability (principally the costs ofcapacity reduction and providing alternative employment) and ways ofmeeting and mitigating these costs still need to be explored.

habitat and non-target species will be used to set targets for ecosystem-based fishery management and to assess the success of management action. The choice of indicators is likely to reflect the growing priorities of species' and habitat conservation as justifiable goals of management, and it is likely that increasingly large areas of the sea will be closed to fishing in order to meet conservation objectives (Chapter 16) .

13.11 The future of fisheries

Many of the existing moves towards the implementation of the EAFM have often been characterized by management

action to mitigate the environmental impacts of fishing on a case-by-case basis. Thus turtle excluder devices (lEDs) have been fitted to trawls to stop turtles being killed as by-catches, or fisheries for small pelagic 'forage' fishes have been closed in the vicinity of seabird breeding colonies. These management actions are likely to be the first steps in a long process

of integrating environmental concerns into fisheries' management, and many commentators now see the EAFM as an evolutionaryratherthanrevolutionaryprocess. In the longer term it is likely that indicators of the impacts of fishing on

Many fisheries are currently fished beyond sustainable limits and expected reductions in fishing effort will provide longterm benefits, by creating more productive and more profitable fisheries and reducing environmental impacts. Capacity for improved fisheries' management will be greater in the developed world where there will be some commitment to meeting the short-term costs of effort reduction. The prospects for sustainability in poorer nations are not so good. unless the international community makes the financial commitment to provide alternative livelihoods for fishers.

Chapter Summary •

Fisheries are a vital source of food , income, and employment, especially in the developing world . Around 80 million tonnes of fish are landed each year and 20 species of fish account for over 40Cfo

of these landings. •

Fishing gears can be described as active or passive. Active gears are towed towards the fish , while passive gears are not. Fishing gears catch a range of species, including bycatches, that will be discarded

by the fishers if they are not worth eating or selling. •

Stocks fluctuate in abundance as a result of natural and fishing effects. Variations in egg and larval survival have a major impact on the size of year classes recruiting to the fishery.

•

Fish stocks are usually assessed to predict the size of catches that can be taken without compromising future catches. Fishery management actions consist of catch controls, effort controls, and technical measures.

•

Fisheries have environmental costs that can threaten rare species and the sustainability of the fished resource. There have been increasing attempts to mitigate these costs by adopting the precautionary approach and ecosystem-based fishery management.

•

Large reductions in global fishing capacity are needed to get the greatest social and economic benefits from fisheries and to ensure that biodiversity conservation and sustainability goals are met.

Further Reading A wide-ranging introduct ion to marine fisheries ecology is provided by Jennings, Kaiser, and Reyno lds (2 0 01 ). Th is book describes f isheries exploitation, conservation, and management in tropical, temperate, and polar environments, and focuses on issues of contemporary concern such as marine reserves, the effects of fish ing on coral reefs, and the incorporation of the precautionary princ iple into management advice.

• Jenn ings S., Kaiser M. J. & Reyno lds J. D. 2 0 01. Marine Fisheries Ecology . Blackwell Science, Oxford.

Aquaculture

Chapter Summary Aqu acu lture in marine systems can be traced back to well

ates its own environmental prob lems and has led to disease

before Roman t imes. Even then it was clear that the culture

outbreaks, over-harvest ing of forage fi shes to generate fish-

of marine speci es w as feasib le only at great expense. While

meal, genet ic dilution of w ild stoc ks from farm escapees,

freshw ater products conti nue to contribute most in terms of lan dings and val ue, marine produ cts are becoming increas-

and has caused eco log ical problems in areas where local carry ing cap acity has been exceeded. A better understand-

ingly important, and technological advances make it more

ing of these issues w ill help to ensure that aquacultu re is

viable to produce fi sh and other biota at reasonable cost

undertaken in an environmentally sustai nable manner.

and w ith a reduced environmenta l impact. Aquaculture ere-

14.1 Introduction Marine aquaculture continues to be a rapidly expand ing global industry and is probably one of the best examples of our ability to take biological knowledge and apply it to improve the biological and economic yield from the marine environme nt. Given current rates of global human population growt h, it will be necessary to produce an additional 40% of protein from the sea by 2030. As current yields from capture fisheries taken around the world have either reached a plateau or are diminishing, there is a growing need to consider aquaculture as an alternative source of obtaining protein from the sea. As many wild capture fisheries have collapsed and local economies have suffered the consequences of the ensuing economic hardship, many have pointed to aquaculture as the solution to the impending shortfall in food production from the sea. Some even speculate that aquaculture could remove the need to fish wild stoc ks altogether. As our understanding of the life-history requireme nts of an increasing range of species increases, so previously 'd ifficult' species have become more feasible subjects for cultivation. In addition to these advances, increasing automation, improved feed

technology, and high technology waste -treatme nt systems have contributed to a decline in the costs of production of many species. As a result, fish-farmed cod (Gadus morhua) landed on the shelves of major retail outlets for the first time in 200 1 (although this remains financially unviable at present given the subsequent demise of the comme rcial companies involved ). Although aquaculture can be traced back several millennia, it is still an industry very much in its infancy in some parts of the world and consequently is associated with its own social and environme ntal problems that vary according to geographic context. Indeed some sectors, such as shrimp cultivation, have witnessed their own 'gold rush' as a result of high market values of shrimp . As with any new industry, the primary concern of participants has been to invest in technology and research des igned to overcome the problems of production and stock control, such that the enterprise becomes economically viable. In contrast, less attention has been given to the environmental conse quences of cultivation practices. Yet it is ironic that in many parts of the world the environme ntal impact of aquaculture practices has become one of the impediments to the further expansion of the industry. Thus it appears that short-

Chapter 14 Aquaculture • • •

•

• • • •

•

• • •

••

• •

••

• •

••

• • •

••

• • • • • •

•

• • •

•

• • • •

•

•

•••

• • •

term economic return continues to dominate the business of aquaculture in developing countries . This chapter aims to introduce the historical developme nt of aquaculture, the variety of techniques used to rear a range of different organisms, the technology employed to increase productivity, and the environmental and biological consequences of aquaculture in m arine ecosystems. As aquaculture involves the rearing of organisms in an artificial environment, there are potential welfare issues that are of concern to wider society, hence the chapter also considers this issue. The environmental impacts of aquaculture have become one of the impediments to its further expansion.

14.2 Aquaculture past and present Fishes, molluscs, crustaceans, and plants have been cultivated by humans for several thousand years. Archaeological evidence is strongly suggestive of the culture of carp (Cyprinidae) by early civilizations as widely distributed as China, Japan, and Italy. Indeed, carp are recurrent motifs in art from these regions. Car p were no doubt cultivated for their food value but also for their aesthetic appeal. whic h gave rise to varieties such as koi carp, much valued by aquarists in present-day cultures. Carp are an ideal species for cultivation due to their tolerance of high-stocking densities and low dissolved oxygen levels, their omnivorous diet and high growth rates. However, marine species present a much greater technological challe nge because of their requirement for high water quality and, in many cases, their carnivorous diets, a fact recognized long ago by the Romans (Box 14.1). Fish have been cultured for many thousands of years. However, the culture of marine species is far more

•

• • • • • • • • • • •

••

• • •

••

• •

•

• • • • •

•

• • • • • • •

•

• • •

•

• •

•

• • •

••

• •

•

•

•

• • • • • • •

•

• •

In past and present times aquaculture of omnivores or shellfish has provided an easily harvested and reliable source of food .

In the past, aquaculture has provided a reliable and easily harvested source of protein that is independent of natural fluctuations in capture fisheries. However, the present-day production of fish-oil, which is key for the cultivation of carnivorous fish species, has declined over the last two decades; this means that the further expansion of this sector of aquaculture may be impeded (Current Focus : The catch-22 of aquaculture) . The term 'a qu a cu ltu re' has only been in use for about 40 years, which coincides with its incre asing industrialization, most notably in the salmonid sector of the industry. The term 'culture' implies human intervention that enhances production of the cultivated species. This m ay be very simplistic at one level (e.g. the introduction of nutrients and organic material from animal wastes, as in Chinese polyculture systems), ranging through to highly sophisticated computer-controlled culture in intensive water-recirculation systems. In the early 1970s the production offreshwater and marine fish and shellfish was the equivalent of only 12% of the annual world fish landings for human consumption (c. 6 million tonnes). At that time, this source of protein provided 4% of the world's supply of animal protein, excluding the contribution of milk. In As ian countries, aquaculture makes a far greater contribution to the overall supply of animal protein due to the prevalence of freshwater aquaculture in this area, and almost 75% of fish cultivation arises from Asia (Allsopp 1997; Subasinghe et aJ. 2009). Since the early 1970s, the production of finfish has increased ten-fold while the contribution of capture fisheries to world protein supply has only doubled (Fig. 14.1). As a result, in 2007, aquaculture contributed c. 45% to the global production of fisheries, worth US$94.s billion at first sale value, of which marine systems contributed US$37.S billion (FAO 2007).

demanding than that of freshwater species. While production of protein from wild-capture fisheries reached a plateau in the early 1990s and latterly has begun to decline, aquaculture now provides nearly 45%

Box 14.1: Aquaculture in Roman times 'There are two kinds of fish-ponds, the fresh and the salt. The one is open to common folk, and not unprofitable, where the Nym phs furnish the w ater for our domestic fish; th e ponds of the nobility, however, fi lled w it h sea-water, for whi ch only Neptune can furni sh the fish as w ell as the water, appeal to t he eye more than the purse, and exhaust the po uch of the owner rather than fill it.' From Rerum Rusticarum by Marcus Terentius Varro (12 7- 126 BC), translated by Hooper & Ash (1934).

(65.1 million tonnes) of all aquatic products (both freshwater and marine).

While m arine-capture fisheries are governed by enviro nmental factors that affect recruitment and hence are unpre dictable and vulnerable to over-exploitation, aquaculture is largely dependent upon inputs of feed and upon good m anagement of the cultivation system to avoid disease and enviro nmental degradation. These criteria for successful aquaculture in some way appear to be more att ain able than a more rational use of wild fisheries. Despite this, m any aquacu ltu re practices are themselves d ependent upon wild-capture fisheries to provide protein from lower down the food chain (e .g. smaller fishes, such as sandeels,

14.2 Aquaculture past and present •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Ammodytes spp., or anchoveta) to make fishmeal. However,

culture from its dependence upon wild fisheries, which

this irony h as been brought sh ar ply into focus by some that

provide an unpredictable product of var iable quality. With

have made a case that aqu aculture is partly the cause for the demise of certain world-capture fisheries (Naylor et a1.

the increasing move towards genetically engineered crops, it should be possible to manufacture feeds that contain the particular protein and lipid requirements of marine piscivorous species (Current Focus).

2000). For this and other reasons, plant-based fish-feeds

are seen as the most attractive solution to disengage aqua-

CURRENT FOCUS: The catch-22 of aquaculture

n- 3 fatty acids (Sathivel 2002), and it is now com mon practice to integrate fish offal products from the process-

At present, the cultivation of predatory finfish species is

ing industry into the feed admi nistered to Pongosius cat-

highly dependent upon the availability of fish oils th at

fish. However, in certain parts of the developed world,

are included in the formulated diets that are fed to these

such as Europe, there is an illogical squeamishness about

species. As a result, aquacultu re is a net 'consumer' of

feeding recycled body tissues to the same species, w hich

wild captu re fisheries, in particular, of oil rich species

no doubt stems from the feed-related disease outbreaks

such as anchoveta and othe r small pelagic species. While

tha t occu rred in terrestrial livestock. Unlike terrestrial live-

it is possible to replace the protein in fish feed wi th plant-

stock, many carnivorous fish species are nat urally can-

derived alternatives, the rep lacement of fish oil with plant-

nibalistic.

based oils is not so simple. Fish oil has a particularly high

In addition to fish, other marine biota may produce suf-

content of n- 3 highly unsatu rated fatty acids (HUFAs)

ficient n-3 HUFA to provide a viable alternative to fish oil.

that are essential for the optim al growth and healt h of

Recent studies have examined the potential of unicellular

farmed fish (Tu rchini et al. 2009). Thus, the availability

algae, copepods, and benth ic invertebrates. In particular,

and efficacy of the use of fish oil presents a challenging

the cultu re of Co/anus finmorchicus generated sufficient

bottleneck to the further development of the aquacultu re

n- 3 HUFA to adequately replace fish oil in the diet of cul-

industry focused on carnivorous fish, especially given the

tu red Atlantic salmon (Olsen et al. 2004). However, the

continued decline in the annual production of fish oil from

cultivation of copepods in sufficient quantities to replace

1985 (1481 t) to 2006 (988 t) . The same issues do

fish oil remains uneconomically feasible at present, but

not apply to the cultivation of herbivorous or om nivorous

could be a promisi ng possibility at some poi nt in the

freshwater species, such as carp and tilapia.

future. The use of unicellular o rganisms also offers the possi bility of using gene manipulation to produce strains

What are the alternatives?

tha t will generate commercially viable quantities of n-3

Current research indicates th at fish can cata bolize oils

HUFA. The use of unicellular algae would be energetically

produced by plant species such as soya, linseed, palm,

more efficient that cultivating copepods because there is

canola, and sunflower. This means that some of the fish oil

one less energy transfer step in the process (sunlig ht-

currently used in fish meal is simply used to maintain the

algae vs sunlight-algae-copepods).

metabolism of the fish by providing a sou rce of energy

Even once the above issues have been reso lved, there

and hence this can be replaced by a plant substitute. A

are other considerations that may affect the future desi r-

vegetable oil that would provid e a good substitute for fish

ability of farmed fish fed alternative diets wi th lower lev-

oil would have a high satu rated fatty acid and monoun-

els of fish oil. One of the strongest marketing messages

saturated fatty acid content (Tu rchini et al. 2009). Many

attached to fish-related products are the health advan-

forms of vegetable oil are rich in n-6 and n-9 fatty acids

tages conferred by eati ng fish, many of w hich are related

and they can be blended to produce an optim al feed that

to its high n-3 HUFA content. A reduction of the latter

achieves good growth rates, although this will still lack

in the final product could detract from its marketability.

sufficient HUFA to produce the same results as a feed

Conversely, a red uct ion in the use of fish oils would likely

blended wi th fish oil.

decrease the likelihood of bioaccumulation of polychlori-

One method to reduce the reliance on industrial fish-

nated biphenyls and related co mpounds in the tissues of

eries to generate fish feed is to improve the manner in

farmed fish. It is clear that the issue of findi ng an accept-

w hich we utilize waste from the fish-processing industry.

able replacement for fish oil in the diet of cultivated fish

Fish viscera contain livers, w hich are storage organs that

is a key issue if we are to make the necessary prog ress

contain high levels of fish oil. Viscera retained from pro-

to max imize the future potential of marine fish cultivation

cessed catfish contained up to 2 1 mg

s'

dry weight of

as a signi fican t sou rce of dietary protei n.

Chapter 14 Aquaculture Aquaculture is often dependent upon feeds produced from fish at low trophic levels, such as sandeels and anchovies, which have high fish-oi l content. These 'fisheries to feed fish' are themselves a major environmental concern.

In terrestrial systems, the domestication and farming of animals has centred on cattle, pigs, sheep, goats, chickens, turkeys, geese, and duck. The restricted range of farmed species means that technology is easily transferable between species in terrestrial systems. This restricted range ofspecies contrasts sharply with the hundreds offish, mollusc, crustacean, and, latterly, echinoderm species that have become the subject of widespread cultivation. The diversity of farmed marine species makes their cultivation an exciting though onerous area of research, as the individual requirements of such a wide range of taxa require specific research effort. A much greater range of animal species is cultivated in marine systems compared with land-based systems. The diversity of cultivated species in marine systems greatly increases the research burden necessary to bring these species to commercial levels of production.

Algae and bivalve molluscs are among the most attractive candidates for cultivation, as these are the most efficient in converting energy into biomass that is available for consumption, and they are ranked second and third behind finfish in terms of tonnes of production (Fig. 14.2) . Algae produce sugar and starch through the process of photosynthesis. hence, provided water clarity is sufficient and there are adequate nutrient supplies in the water column, little input is required by the cultivator (Chapter 2) . Bivalve 120

~

•00

.e0 60 0 0

.,

30

~ 0

s

Carrying capacity is the amount of biomass that can be supported in terms of oxygen and food requirements by a particular volume of water. Once the carrying capacity of a system is exceeded, the effects of competition will increase density-dependent mortality and possibly

water quality. To date approximately 300 species are cultivated across all aquatic systems. Of these. 20% are carnivorous. but these yield only 10% by weight of all production. However. carnivorous species tend to be those most prized by gourmets and consequently they command high prices per unit weight and contribute 40% ofall aquaculture revenue. Although herbivorous and omnivorous fishes (e.g. tilapias and carps) continue to account for the majority of global fish production, they still command a relatively low price per unit weight. Nevertheless, they are the best subjects to fulfil basic world food-requirements as they do not require sophisticated cultivation systems and are inexpensive to rear. They also tend to be species that are highly tolerant of high stocking densities and low dissolved oxygen levels. Thus. in a world with an ever increasing human population, these are the fish that are likely to meet the future demands as a basic source of high quality dietary protein. While herbivorous and omnivorous freshwater fish continue to dominate world fish aquaculture production in terms of biomass, carnivorous fishes continue to command the highest per unit we ight financial value.

90

•• -••

molluscs are filter feeders and feed on naturally occurring phytoplankton in the water column and convert this to body tissue. Again. little or no input is required to provide sufficient food for the cultivated species, although care is needed to ensure that bivalves are not overstocked to the extent that the carrying capacity of the local environment is exceeded. In contrast, most fish and crustaceans feed on animals higher up the food chain; hence overall energy conversion efficiency is reduced (Box 14.2) .

0

~

iE-30 -60 1950

1960

1970

Year

19BO

1990

2000

2007

r-... Food fishsupplies fromoquowlture Food fishsupplies fromrupturefisheries Non-food uses

Figure 14.1 Ut ilization of fish supplied from wi ld capture and aquaculture sources in terms of fish used for human consumption or fish used for no n-food uses, e.g. fert ilizer,

fuel. Source: FAD (2007).

To this day, freshwater fish form the largest component of world aquaculture production. both in terms of tonnage and financial value (Fig. 14.2) . For fish production, it is apparent that freshwater and diadromous (e.g. salmonids) fish products remain the dominant sector of the market. while in the marine and brackish water sectors, molluscs. algae. and crustaceans dominate (Fig. 14.2) . However. freshwater fish products are. in general, relatively low value per unit of production compared with marine fish products, which are worth at least three times as much as freshwater equivalents (Fig. 14.2) . However. marine products are more risk prone and hence costly to produce. as the marine sector of aquaculture remains an emergent industry (FAO 2002) .

14.3 How do we produce food from the sea? •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

1·1 30000

Box 14.2: Conversion efficiency

. 2\ 000

Conversion efficiency refers to the passage of energy through food-chains and webs and is discussed in Chapters 4 and 7. As one organism consumes another, energy is used to create body

• 20000

-e ,

~ 15000 ~

10000

tissue, for metabol ism and reproduction, wh ich

\000

results in net energy loss. Some organ isms are more

0 MiS(eliollE!oUl aQuatic animals

efficient at converting one form of organic material into another, but the net result always results in energy loss. As more and more links are added

Ibl 30000

•

~ 20000

while the food chain that links microalgae to large

1\ 000

carnivorous fishes , such as sharks, is one of the most ineffici ent. In contrast, the produ ction of edible

10000

protein from bivalves is highly efficient as there are

0

gae--bivalves) .

DiodromoUl (rUlta(e20%) for Northern Asia and the Sahara (lPCC 2000) . Even if these predictions are accurate. it is difficult

to ascertain their consequences given the changing use of water abstraction with industrial growth in many of the countries affected . Changes in the quantity of freshwater discharged from estuaries into coastal waters will affect the intensity of stratification that occurs along the density gra-

dient formed in the Region of Freshwater Influence (ROFl, Chapter 8) . Thus the changes reported in Table 15.3 are likely to lead to an increase or decrease in the strength of alongshore density driven currents which may have important ecological consequences for the dispersal oflarvae and propagules and other organisms associated with fronts. 30

-~ ~

~

2l

• Tidal • Fluvial and 'incombination'

20

0

~

0

15

~

~

~

E

~

z

10

5

regions in the world occur in regions of intense upwelling, the potential for climate change to affect fisheries seems highly likely (Bakun 1990) . Recent anomalous changes in the upwelling of cool, nutrient-rich water off the coast of the western United States led to an extensive anoxic event resulting from unusually high productivity. Extensive areas of the seabed from the continental shelf edge to within 700 m of the surf zone were severely oxygen depleted. resulting

in mass kills of commercially important fish and shellfish species (Grantham et at. 2004) . Changes in wind patterns may alter wind-induced currents that are important for larval transport, which means that larvae may no longer

be conveyed to habitats suitable for further development (Heath 1992) .

15.5.4 Ocean acidification Levels of atmospheric carbon dioxide (CO,) are rising and are reducing oceanic pll, causing shifts in seawater carbonate chemistry (Doney et at. 2009) . This process, termed ocean acidification (OA), has seen our oceans absorb up to a third of atmospheric CO 2 since the onset of the Industrial Revolution (Sabine et at. 2004) . Increasing the concentration of CO2 disrupts the natural buffering capacity of seawater towards higher concentrations of carbonic acid,

dissociating into hydrogen (H+), bicarbonate (HCO,), and carbonate ions (CO~~; eqn 15 .1) . Increased H+ production already has caused the pH of seawater to decrease from a pre-industrial pH of 8 .16 to present levels of pH 8.05 (Guinotte & Fabry 2008) and is forecast to decrease further by 0.3-0.5 pH units at the end of this century, equivalent to a 100-150 % H+ increase (Houghten et at. 2001; Caldeira & Wickett 2005) . Such large-scale changes in ocean pH are the greatest experienced over the last 300 million years (Caldeira & Wickett 2003) but continue to rise at an accelerating rate outstripping even the most pessimistic of projections.

CO 2 (arm) iii CO 2 (aq)

+ H,D iii H2C03 1i1 H+

+ HCO,IiI 2W + CO;Figure 15.10 The increasing frequency of closures of the River Thames barrier in recent years is one indication of the increasing effect of elevated rainfall and greater incidence of tidal surges and sea level change (King

2004).

(15.1)

The organisms most at risk are marine calcifying organisms (i.e. molluscs, echinoderms. crustaceans) that biomineralize carbonate (CO~~) and calcium (Ca 2 +) ions to form

calcium carbonate (CaCO,) skeletal or shell structures (eqn 15.2) (Current Focus) . As more CO 2 enters oceanic surface waters. the seawater's natural buffering capac-

ity steals away these vital carbonate building blocks that

15.5.3 Water circulation

are required for calcification by converting the reactive H+ and CO;- ions towards more stable HCO, (eqn 15 .1) .

Intensification of alongshore wind stress on the ocean surface may already have increased coastal upwelling intensity (Bakun 1990) . As many of the most productive marine

Thus the availability of these carbonate ions (referred to as the saturation state) will determine whether organisms

can successfully deposit their vital CaC0 3 scaffold. Seawa-

15.5 Climate change •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Table 15.3 Mod elled river discharge und er present day and future rainfall scenarios, showing th e difference in discharge for wate rsheds w ith or w it hout dams.

I

Discharge 1960s (km ' yr-') Africa Dam unirnpacted

Dam impacted

Kouilou Cross Chari Seneg al Congo (Z aire) Volta

28.4 59.9 29.1 5.7 1349.0 32.8

Discharge 2050s Relative change (km' yr-') ("!o) 20.0 61.8 34.3 2.5 1267.5 4 8 .1

- 2 9 .6 3. 1 17 .9 - 5 6 .0 - 6 .0 46.7

•• •••••••••••••••••••••••••••••••• •••••••••••••• ••••••••••• ••••••• ••••••• ••••••• ••••••• ••••••• •••• ••• •••• ••• •••• ••••••• ••••••• ••••••• •••• ••• •••••••

Asia Dam unirnpacted

cs Chu Salween (Thanlwin) Nad ym

Dam impacte d

Ku ra Ganges-Brahmaputra Indus

22.3 98.5 16 .0 22.0 1 186.9 121. 2

20.8 13 5 .2 26.5 13.7 13 8 8.4 174 .6

- 6 .7 37.2 65.9 - 3 7.8 17.0 4 4 .1

1.5 13 5.4 10 0 .7 1 1.1 32.7

0.9 147 .5 13 3 .6 9.5 4 0 .1

- 4 0 .6 9.0 32.7 - 14 .3 22.8

6.5 142.0 26.5 13 .0 23 4.0 101.2

6.2 174. 1 32.8 9.7 2 46.3 12 3 .4

- 4 .9 22.6 23.8 - 2 5 .1 5.2 2 1.9

12 .3 187.2 0.2 30. 1 530.6 1.3

3.4 246.0 0.8 7.7 540.0 2.4

- 7 2 .0 3 1.4 212.2 - 74 .3 1.8 8 1.6

Australasia

Dam unirnpacted

Merauke Fly Sepik

Dam impacted

Murray Ramu

Europe

Dam unimpacted

Dam impacted

Adour Pechora Mezen Kuban Volga

Severn, Dvina North and Central America

Dam unimpacted

Dam impacted

Patuca Yu kon Kobu k Grande de Matagalpa

Mississippi Colorado

•• ••••••• ••••••• •••• ••••••• •••••••••••••• ••••••••••••••••••••••••• ••••••• ••••••• ••••••• ••••••• ••••••• •••• ••• •••• ••••••• ••••••• ••••••• •••• ••• •••••••

South America

Dam unimpacted

Dam impacted

Coppename Essequibo Santa Cruz Parnai ba Am azonas-Orinoco Doce

10 .7 155. 1 0.9 26.6 6802 .4 2 4 .4

0.7 78.8 1.0 5.0 5536.5 33.4

- 9 3 .4 - 4 9 .2 17 .3 - 8 1.2 - 18 .6 37. 1

The authors used a HadCM 3 cli mate-change mode l under the A2 scenario to generate their outputs. What is clear is that the changes in rainfall and hence d ischarge vary considerably from one region to another. In some cases, rivers with dams show much greater changes relative to more 'natura l' free-flow ing river systems. The conclusion is that habitat restoration and naturalization of river systems may be important to develop resilience to climate driven changes in precipitation (Palmer et al. 2008).

Chapter 15 Disturbance, Pollution, and Climate Change

CURRENT FOCUS: Ocean acidification Labo rato ry-based expe riments have confi rmed that high CO 2 conditions impact marine calcifyi ng organisms

through changes in calcification rates (increased and decreased) , and via distu rbance to physiological and metabolic processes (Ries et al. 2009). Such expe riments

are extremely important in aiding our understanding of how organisms might react to GA. However, most of these

tri als are short-term relat ive to the organism's average lifespan and do not rep licate the chronic effects of OA that will span decades. Chronic exposure to increased CO2 may

have complex effects on the growth and reproduct ive success of calcareous marine organisms (Doney et al. 2009) and could induce physiological acclimat ion or flexibili ties that are not observed in short-term experiments. Longte rm experiments currently in prog ress will be essential to det erm ine whether calcifying org anisms can demonstrate acclim ation to this rapid ly changing envi ronment. Marine volcanic vent sites (Chapter 9) reduce seawate r pH and provi de insights into the poten tial implications of OA. Com mun ities abund ant with calcareous organisms loc ate d beyond the vents shift towards com munities that lack corals and have significant reductions in sea urchi ns

and coralline algae (Hall -Spencer et al. 2008). Fu rthe rmore gastropod shells dissolve increasi ng their risk of predation due to the reduced carbonate satu ration state. Further work on these natural underwater OA laboratories is required to better understand the implications of OA and how communities coul d be affecte d as preli minary observations do not bode well fo r the futu re of calcifying organisms. Comparat ive stu dies using natural systems can be complicated by the effects of confounding variables that make it diffi cult to arrive at unambiguous conclusions. HallSpencer et al. (2 0 0 8 ) chose thei r sites carefully such that

coralline algae) at a mean of pH 8.2 but few epiphytic

all vents were at ambient temperatu re and there were no

calcifiers (only bryozoan s such as Electra po sidoniae)

differences that relate d to chemicals such as arsenic and

occurred on seag rass fronds at mean pH 7 .6. (d , e).

sulphu r that are often associated with other vent systems.

Photos: Riccardo Rodolfo-Metalpa.

Observational evidence of the effects of acidification Figure (a) shows a Posidonia oceanica seagrass meadow located at a shallow CO2 vent at a depth of 2 m off the Italian coast (Ischia). This location provided an opportunity to undertake a comparative study of calcifying organisms that occurred in close proximity to a source of elevated CO 2 (Hall-Spencer et at. 2008). Photo: Riccardo Rodolfo-Metalpa. Martin et al . (2008) examined calcifying epiphytes on the fronds of the Posidonia oceanica that occurred in

They also examined rocky shore communities at the

seawater with different pH values (b, c). Fronds of sea-

CO 2 vents. In locations where the seawater had a mean

grass were heavily fouled by epiphytic calcifiers (mainly

pH 8.13 , they found abundant calcify ing species, such

15.5 Climate change •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

as coralline algae, Paracentrotus Iividus, Mytilus 90110-

most likely susceptible to OA. Furthermore, some larval

provincia/is, and barnacles (f), but where seawater had a

species, such as echinoderms, form skeletal structures in

mean pH 7.79, coralline algae were absent and limpets

a yet more readily soluble form of CaC0 3 : magnesium cal-

such as the Patella caerulea (9) showed signs of severe

cite. Labo ratory studies of larval responses to OA are lim-

shell dissolution . Photos: Riccardo Rodolfo-Metalpa.

ited and have so far demonstrated inhibitory effects that increase the risk of recruit ment failure under conditions of OA Notable effects include reduced sperm swimming speed, red uced egg size and fertilization success, as well as increased occurrences of abnormalities and mortality. However, these larvae have been derived from adults not previously exposed to high COz conditions. Although these trials do indicate the underlying stress responses of larvae, they do not offer enough information on an organism 's ability to acclimate and adapt towards OA. Experiments currently in progress have observed abnormal development of larvae obtained from adults previously

Colonies of the symbiotic coral Cladocora caespitosa (h) were transferred into the vent area and showed live polyps but skeletal dissolution after 3 months at pH 7.43 (i). Photos: Riccardo Rodolfo-Metalpa.

exposed to high COz' as well as reduced survival 0). OA is a recent phenomenon wi th key research emerging only wi thin recent years. It is evidently clear that many organisms can display detrimental reactions towards OA, while others appear to be able to compensate for it, but at what cost? We still have much to learn about OA's impacts on our oceanic flora and fauna from the individual level to food-web impacts.

•• •

- ...- .... .~

Experimental evidence of the effects of ocean acidification

Psammechinus miliaris sea urchin larvae derived from

In order to survive, marine calcifiers must be able to con-

adults exposed to normal concentrations of CO2 (right)

tinue to populate through reproduction to display possible

and high concentrations of CO2 (left). The larva on the

adaptations tow ards OA Early life-stages are the most

right shows abnormal development. The scale bars

sensitive part of an organism's life cycle, and therefore

100

~m

(photographs Coleen Suckling).

=

Chapter 15 Disturbance, Pollution, and Climate Change

15.6 Interaction of multiple factors

ter saturated with CO~- allows organisms to biomineralize their CaC0 3 structures, but in undersaturated conditions they cannot. Marine CaC03 is typically secreted in two main forms: calcite and aragonite (aragonite is 50% more soluble

We have provided a sample of the influence of human

than calcite) . The stability of each form is governed by the

activities on the marine environment. We have dealt with

amount of available CO~-, temperature, salinity, pressure,

each of these factors separately for simplicity, but multiple

and a stoichiometric solubility product for each form (Feely et al. 2004) . These factors determine the depth at which

able to dissolution. The elevated partial pressure of CO,

factors may operate at the same time or in sequence. While one factor on its own may not have serious consequences for an organism or community, the synergistic action of several factors may prove catastrophic. For example, organisms under one form of environmental stress (e.g. rising mean sea temperatures) may be less able to cope

has increased its depth of influence in the ocean and has

with the physiological demands of adapting to increas-

contributed towards the upward shoaling of the carbonate saturation horizon by 50-200 m over the last 200 years (Sabine et al. 2004) . This has narrowed the depth range over which organisms can calcify normally. Models forecast

ing frequencies of freshwater discharge that might occur with changing rainfall patterns, and their resilience may be further weakened by exposure to industrial contaminants. The effects of multiple and sequential human interference are well illustrated by a testimony given to the United States Congress to encourage it to consider the consequences of introducing a non-native oyster into Chesapeake Bay. Declines in native oyster stocks in Chesapeake

calcite and aragonite become undersaturated, known as the saturation horizon. Below this depth boundary, organisms that utilize CaC0 3 for biogenic structures will be vulner-

further upward shoaling of this saturation horizon, causing surface waters to become undersaturated with respect to aragonite in many parts of the oceans by the end of this

century, although parts of the Southern Ocean already are undersaturated (Orr et al. 2005) .

Bay are well documented and have been linked to reduced

of OA's effects on marine calcifying organisms. Colder waters naturally retain more CO 2 and are more acidic than warmer waters (Guinotte & Fabry 2008) . As a result, saturation states are highest in shallow, warm tropical waters

water quality and overfishing, but attempts to reinvigorate the oyster stocks have repeatedly failed. One solution appears to be to introduce a non-native species that may be more tolerant of present day environmental conditions and parasitic fauna that were accidentally introduced into Chesapeake Bay as a result of past aquaculture introductions or discharge of ship's ballast water. The testimony

and lowest in cold, high latitude regions (Feelyetal. 2004) .

given in Box 15.6 highlights the complex considerations

There is particular concern over the future of polar marine organisms that are uniquely adapted towards their cold surroundings. In an environment where larval and adult development is ten times slower than in warmer regions of the

that face managers of natural resources that have to weigh the ecological risks and potential benefits of such introductions.

CO'3-

+ Ca' + ~ CaCO3

(15.2)

Geographic location will playa key role to the extent

world, the ability for organisms to adapt to these changing conditions is highly questionable. Changes in wind stress may intensify coastal upwelling and have been linked already to anomalously high production and mass kills of commercially important fisheries.

15.6 Interaction of multiple factors •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Box 15.6: Non-native oysters in the Chesapeake Bay

Fisheries Conservation, Wildlife and Oceans, Commi ttee on resources, United States House of Representative in

2003 by Professors J. L. Anderson and R. Whitlatch, both This text is paraphrased from a testimony given to the

experts in oyster ecology and the ecology of Chesapeake

108th US Congress (Fi rst Session), Subcommittee on

Bay.

Good morning Mr Chairman and members of the Subcommittee. Thank you for this opportunity to speak to you about the proposed introduction of the non-native oyster Crassostrea ariakensis . The [native] oyster stock in the Chesapeake Bay has declined dramatically. Harvest is now about one per cent of what it was at the end of the nineteenth century. Fishing pressure and habitat degradation resulting from agricultural, industrial, and residential pollution, deforestation, and oyster reefdestruction have contributed to the decline. In recent decades, however, the diseases MSX and Dermo have been identified as the core reasons for further decline. It should be noted that MSX is caused by a parasite that was introduced to the East Coast from Asia. Fisheries' management efforts and various restoration programs have not been successful in restoring the oyster stock to date. The loss of the oyster has been devastating to the oyster industry and its dependent communities. Those that remain in the Chesapeake oyster processing sector now rely on oysters that are brought in from the Gulf of Mexico region and other areas for their economic survival. Furthermore, the loss of oysters has contributed to declines in water quality and clarity. The introduction of the non-native Suminoe oyster, or Crassos trea ariakensis, from Asia has been proposed as a solution to these difficult problems. Indications are that it may grow well in the Chesapeake Bay and it is known to be resistant to MSX and Dermo. Despite the positive results of introductions of some oyster species, some extre mely negative consequences have been observed as well. A major risk of introducing a non-native oyster comes from pathogens, such as MSX, or the introduction of other animals or plants that may be attached to oysters. While in Australia and New Zealand, introduced non-native oysters have displaced native oysters. Aquaculture of ste rile non-native oysters, represents an appropriate interim step that possesses least risk (in terms of the available options) to the Chesapeake Bay and its dependent communities. However, limits and controls on aquaculture practices must be implemented to minimize the risk of introducing pathogens or reproductive non-native oysters during this transitional phase. This approach may provide limited benefit to parts of the oyster industry and it provides decision-makers with the added information required to make future decisions. Moreover, this option allows more time for innovative, science-based efforts to restore native oyster populations. On the other hand, the option of not allowing any introduction fail s to address fishing industry concerns and will not result in improved understanding of the ramifications of non-native introductions. It may also increase the risk of rogue or uncontrolled introductions. The option of the direct introduction of reproductive non-native oysters, is not advised given the limited knowledge base on C. ariakensis and the potential for irreversible consequences of introducing a reproductive non-native oyster into the Chesapeake Bay. It is unlikely that there exists any 'quick fix' to the Chesapeake oyster situation .

Chapter 15 Disturbance, Pollution, and Climate Change

Chapter Summary •

Natural agents of disturbance to marine commu nities and systems occur across a full range of spatial and tem poral scales.

•

The response of commu nity metrics (diversity) to d ist urbance can be predicted from ecological

paradigms, such as the intermediate disturbance hypothesis. •

The relative impact of human activit ies on marine ecosystems needs t o be assessed against a background of natural environmental fluctuations that occur at a variety of tem poral scales. Our ability to detect the effects of human intervention critically depends on an appropriate analytical or experimental ap proach.

•

Coastal shelf environments are subjected t o the most intensive human activities that include fishing, aq uacu lture, mi neral and hydrocarbon extraction, shipping activit ies, tourism , and discharges

of effluents and pollutants. •

Eutrophicat ion, which has result ed from elevated inputs of organic matter and nutrients from agricultural run-off, has caused widespread blooms of toxic microalgae and anoxic events that have resulted in mass mortalities of marine biota.

•

Persistent contaminants, such as PCBs, have subtle effects at t he population level by affecting survivorship of larvae and juveniles. The full impact of these contam inants is a subject of specu lat ion.

•

The congested inhabitation of coastal margins means that much of the world's population is vu lnerable to changes in sea level linked to global climat e warmi ng.

•

Increases in global rainfall will elevate freshwater and sediment d ischarge into coastal waters thereby affecting density-d riven currents in ROFls and w ill change the dist ribut ion of biological commu nities.

Further Reading Clarke et al. (1994) provi de a readable and sympathetic (to the non-mathematical) guide to the detection of ecological changes in marine (and other) communities. Evans et al. (200 0) provide a synthesis of the debate surrou nding replacement of tributyl tin w ith suitable, less environmentally damag ing alternatives. Hall (2002) provides a review of agents of change in coastal systems in the present and also examines possible future impacts. For an up to date review of ocean acid ification see Fabry et al (2008) . •

Clarke. K. & Warwick, R. 199 4 . Change in Marine Communities: an Approach to Statistical Analysis and Interpretation. Natural Environmental Research Council , Plymouth Marine Laboratory, Plymouth.

•

Evans, S, M., Birchenough, A. e., & Brancato, M. S. 2000, The TBT ban: out of the frying pan into the fire? Marine Pollution Bulletin 40: 204-2 1 1.

•

Fabry, VJ" Seibel, BA, Feely, RA & Orr, J,e. 2008, Impacts of ocean acidification on marine fauna and ecosystem processes. ICES Journal of Marine Sciences 65: 4 14-432.

•

Hall, S. J. 2002. The continental shelf benthic ecosystem : current status, agents for change and future prospects. Environmental Conservation 29: 350-374.

Conservation

Chapter Summary

As a reader of this book you probab ly do, but many others

In 1768 , only 27 years after they had bee n discovered, the

in the world w ill be more concerned wit h the source of their

giant Steller sea cows (Hydrodamafis gig as), w hich grazed

next meal. In dealing w ith issues of conservation and sus-

on algae around Bering Island , were driven to exti nction by

tainable developm ent , the marine ecologist enters a wid e

hunters. North Atlantic right whales (Eubalaena glacia/is) were reduced to near extinction by commercial whaling

arena, w here practice and po li cy are also sw ayed by moral, cultu ral, polit ical, soci al, and econo mic values. However, this

in the eighteenth and nineteenth centuries, and only 300

is also a challenging and rewardi ng arena, w here science

remain today. Large fishes of all spec ies are increasingly

plays a key role in assessing the sustainability of human

rare following decades of over-exploitation, and marine habitats are lost as a result of land reclamation, polluti on,

impacts, prioritizi ng conserv at ion projects, and underp inning the development of effective conservation pol icy.

and commercial development. Shou ld w e, and do we, care?

16.1 Introduction In preceding chapters, we have seen how pollution, fisheries, and aquaculture, together with clim ate change, have impacted, and are continuing to impact, the m arine environment. Given that humans are the most sign ificant consumer of natural resources on the planet, these are just a subset of the possible activities (Table 16.1) that impact the m arine environment. In many cases, human impacts are unsustainable, threate ning species, habitats, and ecosystems, and the environmental goods and services they provide. One recent analysis attempted to estimate the distribution of combined human impacts on the world's oceans. The distribution of impacts was very patchy, and the highest impacts occurred in some coastal regions close to human population centres (Fig 16.1 ). However, the analysis also suggested that no areas remain unaffected by human influence and that 41 % of the area cons idere d was affected by multiple drivers. In the broadest sense, the coastal areas with high impacts are often those that are stud ied most intensively by scientists, while areas where impact is expected to be lower are often

less well-known . For example, an analysis of records in the Ocean Biogeographic Information System, which is cons idere d to be the most compre hensive datab ase with records of the distribution and identity of marine taxa, showed that the gre at majority of m arine diversity was described for shallow coastal waters, wh ile the records of diversity for deep, pelagic are as were relatively scarce (Fig 16.2) . On the one hand this is a good sign, that we are focusing research efforts in areas most likely to be impacted by human activities, but, on the ot he r, it is a concern that we know so little about areas that are starting to be impacted by direct and indirect human impacts. Applied m arine ecology is the source of scientific evidence to identify when and where conservation actio n is needed, both by assessing the sustainabihty of impacts and developing methods to mitigate unsustainable impacts. Good scientific knowledge of a system can be needed to support effective conservation, but it is not necessarily sufficient to achieve it; since progress towards conservation objectives will be strongly influenced by social and economic factors.

Chapter 16 Conservation (01

• •

•

•

•

Very 10. impact «1.4)

o law impact (1.4-4.95)

o Medi um impact (4.96-11.47) o Medium High impact (8.47- 121

•

High impact (12-15521

•

Very High impact [> 1552)

(bJ r;::::::;-:--=- -, •

Figure 16.1 Global map (a) of cumulative human impact

Relative volume

0

on marine ecosystems as predicted by Halpern et al.

(2008). Inset boxes show highly impacted regions in the Eastern Caribbean (b), the North Sea (c), and the Japanese

1000

waters (d), and one of the least impacted regions, in

2000

northern Australia and the Torres Strait (e). From Halpern

et al. 2008.

3000

-.... E

~

m C

Figure 16.2 Global d ist ribution of marine taxa recorded

4000

taxonomic records for each combination of sample and bottom dept h is standardized to the volume of water. The inset shows in greater detail the continental shelf

6000 7000 8000 9000 10000

and slope, where the majority of records are found . From

Webb et al. 20 10.

-

5000

in the BOIS database. Area is scaled on the graph to be proportio nal to volume of ocean. The number of

-

c.35 xlO6km3

Number of rercrds

Continental shelfand slope 0

Ill"

200

10'

400

10'

600

10'

800

10' Ig;

1000 II 000

16.2 Why conserve? • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • ••

a whole range of actions. It m ay include outright protection of populations or areas from human disturbance; but it may also involve zoning and other types of regulation that help to keep human use within sustainable limits.

Table 16.1 Principal human impacts on the marine environment.

Aggregate extraction and mining Aquaculture

Sustainable management requires human intervention to

Dredgi ng

maintain or create an environment that does not compro-

Engineering and co nst ruction

mise the wellbeing of future generations.

Fisheries Land-based impacts Military activities

Oil and gas Reclamation

i

Recreation Renewable energy

Shipping

Applied marine ecology underpins conservation advice

and action through the provision of a robust evidencebase of science.

At least in political terms, conservation contr ibu tes to sustainable development. Sustainable development requires that the needs of future generations are not compromised by the actions of people today. Sustainable development h as m any facets, and includes social objecti ves, suc h as human equ ity. Conse rvationists highlight that recognition of the natural limits on hum an population and economic growt h must go hand in hand w it h attempts to meet social objectives. Increasingly, n ational and international a greements express a move towards sustainable development, and these underpin much of the conservation and environmental pro tection legislation we see tod ay. The contemporary tre atment of conservation contrasts with the preservationist approach, which focuses on the protection of species and habitats wit hout reference to n atural change and human requirements (Agardy et a1. 2003). It is important to m aintain a sense of pers pective in conservation and remember that, even wit hout human intervention, some species would become extinc t through n atural processes. In this chapter, marine conservat ion is considered as a contribution to sustainable management of the seas. Consistent with sustainable development, sustainable management requires human intervention to m aintain or create an environment that does not compromise the wellbeing of future generations. The extent to which individuals, towns, regions, nations, and the international commun ity regard long-term human wellbeing as dependent on the presence of a clean, produc tive, and biodiverse marine enviro nment, will determine the strength of ethical and economic support for m arine conservation. Conservation potent ially involves

In this chapter, we cons ider the ethical a nd economic foundations of marine conservation, together with how conservation issues can be identified and prioritized. We discuss the role of poverty in driving the use of the m arine enviro nment and highlight how marine conservation has to find a way to accommodate the short-term needs, aspirations, and expectations of humans. We therefore look in some detail at the economics of m arine conservation , the strengths and weaknesses of the policies that promote it and the legislation introduced to back it up. We also describe how conservation policy is implemented and give some examples of the successes and failures of conservation initiatives.

16.2 Why conserve? Ecology is at the scientific heart of conservation, since population growth is limited by the ava ilability of resources, and species interact wit h each other and their abiotic environment. Thus the n atural enviro nment limits the scope for development and exploitation, and sets an ever-changing baseline (e .g. the effects of climate change) . Apart from the fa ct that some conservation objectives, suc h as protection of particular species and maintenance of water quality, are now incorporated into law, conservation is justifiable on ethical and econom ic grounds. However, perceptions of conservati on differ and justification is never a strictly quant itative exercise; one person's sustainable harvesting of renewable fish populat ions will be another's devastation of a fragile marine environment. Conservation of biological diversity has been a m ajor focus of recent conservat ion efforts. As mentioned in Chapter 1, biodiversity has been define d as 't he variability among living organisms from all so urces including, inter alia, terrestrial, m arine, and ot her aquatic ecosystems and the ecological complexes of which they are part; this includes diversity within species, among species and of ecosystems' (Convention on Biod ivers ity; Box 16.1 ). Some of the key justifica tions for biod ivers ity conservation are: ( 1) that humans have moral a nd ethical responsibilities to care for life on Eart h, (2) that living organisms enrich our lives, (3 ) that 'e cosyste m services' are provided by many species, and (4) that living organisms allow ecosystems to adapt to change and are a source of materials that benefit humans (Kunin & Lawton 1996) . At the personal level, belief in the

Chapter 16 Conservation relevance of various justifications will depend on social circumstances. Thus moral and ethical responsibilities to care for life on Earth may not hold much sway if you are starving. A common justification for the sustainable use of the m arine environment is that m arine species provide import ant benefi ts for humans (Norse 1993). Thus, fisheries and aquaculture are a vital source of food, income, and employment, particularly in the world's poorer countries (Chapters 13 and 14); and marine species are the source of m any useful compounds, such as the algal polysaccharides, carrageenans, and agars that are used in food m anufacture. The sea is also an important so urce of non-biological resources, suc h as hydrocarbons for fuel and sand and gravel used in bu ilding. Such direct economic benefits from the sea are probably the easiest to quantify, as they have real economic value (i.e. they are tradable commod ities on the wo rld's stock m arkets), but are not necessarily the most important benefits derived from marine systems. Benefit may also derive from goods and services that have no 'tru e ' market value, suc h as the storm protection affo rded by coral reefs, control of carbon dioxide in the atmosphere, and waste and nutrient removal or recycling (Table 16.2). In some attempts to value the marine environment, these services are the most valuable properties of the seas and oceans . However, their value is rarely accounted for when assess ing the sustainability of human impacts. We look at issues associated with cost ing suc h services later in this chapter in sect ion 16.4. The m arine enviro nment is widely used for recreation, and coral reef-related tourism can be one of the most valuable industries in ot herwise poor countries with little other means of wealth generation (Chapter 11 ). People using the sea for recre ation generally choose a clean, healthy, and productive environment in preference to one that is polluted and animal poor.

Box 16. 1: International agreements that support marine conservation At the World Summit on Sustai nable Development

(WSSD) in Johannes burg (2002), the follow-on meeting to the United Nations Conference on Environment

and Development (UNCED) held in Rio de Janeiro, Brazil in 1992, signatories agreed on a plan of implementation for sustainable development. The plan gives high priority to integ ration of the th ree components of sustainable development, namely: economic development, social development, and environmental protection. It also recognizes the particular circumstances of the major regions of the world, including the plight of small island states, for which coastal zone management and sea level rise are important issues. Recognizing that marine ecosystems are critical for global food security and sustaini ng economic prosper-

ity (fisheries and shipping), the WSSD plan of implementation included strong commitments to improved conservation of the marine environment, including

application of an Ecosystem Approach by 2010 (Box 16.3), implementation of the FAO code of conduct for responsible fisheries (fisheries that do not overexploit fish populations or harm marine wildlife and habitats), maintenance of the productivity and biodiversity of important and vul nerable marine and coastal areas, establishment of marine protected areas, development of nat ional and international programmes for halting the loss of marine biodiversity, and control of pollution and the spread of alien species. These can be seen as a wish list rather than a series of actions that will be universally implemented on the timescale suggested. However, raising these issues at international summits highlights thei r importance and underpins improve-

16.3 What to conserve

men ts in environmental protection at inte rnational, national, regional, and local levels. There can be rapid uptake of high-level commit-

At a societal level, the general greening of governme nt policy is intended to encourage nations, companies, and individuals to conduct their activities in a sustainable way. Many of these actions, and the ways in which society addresses and fails to address issues of sustainability, are covered in 16.5. However, when human impacts are not m anaged in a sustainable way at source, conservation efforts often focus on h alting unsustainable rates of habitat or species loss. Unfortunately, the magnitude of existing human impacts on the m arine environment is such that a great deal of effo rt is focused on fighting rearguard actions rather than planning for sustainabiHty before the impact occurs (cure the cause n ot the sympto ms) . It is hoped that the greening of government policy will help to encourage proactive, rather than re active, conservat ion . Proactive conservation, for example, might require that measures to mitigate unsustain-

ments in other fora. For example, following WSSD, the 2002 Ministerial Declaration of the Fifth International Conference on the Protection of the North Sea recognized the need to manage all human activities using an Ecosystem Approach that co nserves biological diversity and ensures sustainable development. Subsequently, at the national level, the United Kingdom Government published 'Safeguarding our Seas', a strategy for the conservation and sustainable development of the marine environment. This included specific commitments to marine conservation, such as the adoption of an ecosystem approach, that were consistent with the requirements of WSSD. Source: http://www.johannesburgsummit.org/

16.3 What to conserve •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Table 16.2 Examples of ecosystem services from natural marine ecosystem s (Costanza et at. 1997).

Ecosystem service

Examples

Gas regulation

Oceans balancing CO 2 content of atmosphere, thus regulating atmospheric temperature

Water regulation

Oceans as ultimate source of water as a basis for agriculture, industry, and

Nutrient cycl ing

transport Gaseous fixation and organic matter decom position as sources of nitrogen for

Waste treatment

primary production in all ecosystems Breakdown of sewage by micro-organisms in conti nental shelf waters

Provision of nat ural refugia Food production

Habitats such as seagrass and saltmarsh as nursery grounds for fisheries Coastal waters as generators of fishery products

Provision of raw materials Sourcing of genetic materials

Marine sediments and rocks as sources of aggregate for build ing Provide natural compounds useful in medicine

Provision of recreat ion Provision of cultural assets

Offer sport fishing habitat, opport uniti es for ecotourism Offer resources for aesthetic, educational, and scientif ic purposes

able impacts are incorporated into plans for development or exploitation before those plans are sanctioned (16.6.1) . Conservation actions must be prioritized to ensure appropriate use of limited funds, but decisions can be difficult and emotive.

Prioritization is needed to identify the conse rvation actions that make the biggest contribution to sustainability. At the global level, prioritization involves international decisions about the investment in combating threats such as climate change. At regional and local scales, prioritization is needed to decide how scarce resources should be allocated to proactive and reactive conservation, and the specific issues to address. Prioritization involves many difficult and emotive decis ions . Thus the last few surviving individu als of a species usu ally attract great public and media interest, and provide impetus for conservation action, but may stre tch, disp roportionately, resources that could be used for large-scale habitat conservation or maintaining the abundance of common species that play important roles in the ecosys tem and provide direct benefits to humans. In public perception, marine conservation is often epitomized by conce rn for marine mammals, seabirds , and sea turtles, even though less conspicuous species and marine h abitats are threatened by human activities . The tendency to 'value' some species more than others is a consistent trait in humans when surveyed for their willingness to contribute financially (willingness to pay) to the conservation of biodiversity. Large charismatic taxa (marine mammals) attract higher bids than organisms at lower trophic levels such as invertebrates and algae [Ressurreicac et al. 2010).

Conservation will never be an entirely logical process when so many value judgements are involved , and since attempts to conserve whales a nd dolphins often gain strong public support, efforts to conserve them may be more successful. Protecting such charismatic species may also have positive and negative implications for h abitats and other ecosystem components on which they depend. An example of the former might be the removal of fishing from a particular locality to avoid cetacean by-catch, which may have concomitant beneficial effects for associated species (e.g. seabirds or fish). Negative effects can result when the protected species becomes a 'pest', as exemplified by the conflict between sport fishermen and fish-eating cormorants or seals. Methods for conservation prioritization of individual species are often relatively quantitative. Thus the World Conservation Union OUCN) produces a 'Red List' of threatened species, which is intended to be an easily and widely understood system for classifying species at high risk of extinction (Box 16.2) . This system is used to class ify all the world's animal species for which d ata are available, and many fishes and marine mammals h ave been listed . Species are prioritized for conservation by the IUCN:

httpv/wwwlucnredlfst.crq.

Habitat conservation is now playing a greater role in the marine environment, with widespread calls for greater use of marine reserves. Thus far it has not been poss ible to create very large marine reserves, so animals such as whales are still managed on a population-by-population basis. Habitats and regions can be ranked for conservation priority according to factors including their biological diversity within particular biogeographical regions (Chapters 1, 7,

Chapter 16 Conservation and 8) and roles in sustaining particular species or groups of species. The process of selecting sites for conservation will typically involve the measurement or description of attributes of a site or series of sites, an evaluation of these measures against a set of criteria and a method of combining the results to enable ranking of sites (Bibby 1998) . Measures typically include species' diversity and rarity, size of area, representativeness, naturalness (naturally a very h ard thing to define ), cultura l criteria, and vulnerability. Combining all scores is a problem, as some are strictly quantitative (area, diversity), while others are qualitative (naturalness). One approach is to rank sites based on quantitative criteria and then to deal with practical considerations at the final stage. Prioritization of habitats and regions for conservation can be a quantitative and qualitative process that can complicate the integration of these data into a single reference point.

Networks of marine protected areas may be proposed to help conserve species and habitats. The idea here is that a set of reserves is selecte d to meet specific conservation objectives, such as the representation of each of the community types known in a region at least once, or the conservation of a fixed proportion (e.g. 30%) of biodiversity fe atures. Algorithms can search a species or attribute by site database to find a minimum set of areas that meet a given objective. If sites are selecte d sequentially to define a minimum set to meet a stated objective, then the select ion of any new site depends on the properties of those already selected. Thus the new set complements the series. A w idespread tool used to develop such networks is the MarXan software developed by Hugh Possingham and colleagues at the Univers ity of Queensland. The tool has adv anced considerably since its early inception, when it was possible only to integrate biological and habitat data for consideration . More recently the tool has been expanded to integrate social and economic data , such that it is possible to set a fixed conservation objective that is achieved by minimizing economic and social costs

Box 16.2: The nrcx Red List

included in the list. Some fish-stock managers argue that

The IUCN Red List recog nizes seven categories of spe-

the reference poi nts used for management are conserva-

cies extinction, threat, and endangerment where there are

tive, and if population biomass were kept at, or above,

sufficient data (see figu re). The categorization is based

those targets then there would be little risk of extinction.

on factors such as reduction in population size over a

Others argue that the observed rates of decline in many

specified time period, geograp hic range size, and abso-

exploited fish populations meet listing criteria and that the

lute population size. A species may be listed as critically

population biology of fish makes them no less prone to

endangered, for example, because it has decreased in

extinction than many bird and mammal species (Hutch-

abundance by >90% over the last 10 years or 3 gen-

ings 2001). Regardless of the pros and cons of these

erations. Marine mammals and turtles have been listed

arguments, the Red List has a role in highlighting species

for some time, and other marine species are increasingly

that are severely depleted or threatened wi th extinction,

appearing on the list. Certain sharks, rays, and chimaeras

and should help to promote the conservation action that

are likely to be added. There has been some debate about

is sought by fishery managers and conservationists alike.

whether managed commercial fish stocks should be

Source: http: / /www.iucnredlist.org

Extinct (EXJ Extinct in thewild (EW) Critically endangered (CR) (Adequate dataJ

(Threatened)

Endangered (EN) Vulnerable (VUJ

(EvaluatedJ

Near threatened (NT) least concern(lCJ Data deficient (DO) Not evaluated (NE)

16.4 Economics of conservation •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

(a) Using only bialagi,,1 dete

(el Fine resolution economic dala Fishing

Figure 16.3 MarXan software generated different marine reserve designs according to the type of data used. The outcome of using only conservation data (a), conservation

revenue

per PU

and economic data (b). Panel (c) shows the distribution of economic activity expressed as gross revenue per

-

annum per planning unit (PU) area and clearly shows the spatial heterogeneity in the commercial value of different areas around the coastline, with darker areas having

Idl Ircnemlr impact

Ibl Using biologicol and economic dolo

the highest value. Panel (d) shows the economic impact on stakeholders of the scenarios shown in panel (a =

I.l

minimising) and panel (b = fine resolution). Integrating

. ,

o , e -o . ie ,§ .-

economic considerations reduced considerably the

'~

economic costs in the short-term. Note however, this

_E

figure does not account for any economic benefits that might be accrued from the implementation of marine

.~

'g g O.S

-~ ,g-

reserves.

o

ArelHTlinimizing

Fine resolution

to marine stakeholders (see Richardson et al. 2006) . The value ofsuch tools is their ability to investigate the outcome of different management scenarios. In a case study in Wales (UK), Richardson et a1. (2006) were able to demonstrate that the inclusion of the spatial data on the distribution of economic activities related to fisheries significantly reduced the financial impact on the key stakeholders (fishers) while maintaining the conservation objectives (Fig. 16.3). MarXan freeware is now widely used in the planning of networks of marine conservation zones or marine protected areas and was used to inform the design of the Great Barrier Reef conservation areas (http://www. uq .edu.au/marxan).

Rigorous quantitative procedures for prioritization are often seen to be essential, and yet the approaches to prioritization we have described can be seen as an intellectual rather than a real-world exercise. Indeed, many sites are protected simply because they were in areas where enforcement was possible, where they brought immediate economic benefits to a local community, or where there was regional or national support for protection, or perhaps more importantly minimal opposition to their creation. It is also important to recognize what site-based conservation can and cannot achieve. The openness of marine systems means that pollution impacts. for example, have to be tackled by reducing polluting inputs, not by setting up reserves. A terrestrial analogy was the acid rain that fell on Sweden in the 1970s and 1980s. Conservation actions (e.g. liming lakes) in Sweden had minimal effect until the UK Government was persuaded to take action to reduce sulphur emissions from its coal-fired power stations. which were the cause of the acid rain. Similar arguments can be proposed for stopping fishing and habitat damage too,

because reserves displace activities while outright control of the activities is needed to stop them. It would be inexcusable to lose sight of the activiry and thus fail to address the problem at source. This is why conservation of the marine environment involves other actions, such as regulation of fisheries and pollution (see Chapters 13 and 15) and integrating the management of multiple uses (16.5) . Such linkage between multiple issues, together with the fact that each issue may be addressed by different government departments and nations, has highlighted the need for more joined up conservation objectives and methods of planning. One framework for achieving this is dubbed the 'e co syste m approach' (Box 16.3).

16.4 Economics of conservation Economic development has environmental costs, which are rarely paid for by the businesses, governments. and individuals that profit from the development. The assimilation of sewage by ecosystems and side effects of species' declines wrought by fishing are cases in point; the polluter and fisher, respectively. are rarely asked to bear the costs of their actions. Failure to take account of the environmental cost of human activities has meant that development is driven by false economic incentives and disincentives, and is unlikely to be sustainable. Moreover. because many human activities in the marine environment, especially fisheries. are subsidized or unprofitable, there are very high short-term economic costs associated with moving towards sustainability. The high short-term costs of changing human behaviour are one of the greatest impediments to effective conservation. Fisheries provide an excellent example of the way in which short-term economic forces promote unsustain-

Chapter 16 Conservation

Box 16.3: The ecosystem approach The recognitio n that sectoral issues that affect the mari ne environment were often managed in different ways, by enti rely different bodies and without sufficient

regard for thei r cumulative or synergisti c impacts, has led to the recognit ion that a more 'joi ned-up' app roach was needed to ensure environmental protection. The ecosystem approach is intended to provide this. It has variously been defined as 'the integrated management of human activities, based on know ledge of ecosystem

dynamics, to achieve sustainable use of ecosystem goods and services, and maintenance of ecosystem integrity' or in less scientific terms, as an approach th at

'puts emphasis on a management regime that maintains the health of the ecosystem alongside app ropri ate human use of the marine environment, fo r the benefit of current and future generations'. As with the aspi rations of inte rn ational meet ings, th ese defini tions are 'high level ' and do not he lp to

ability, even when the long-term econom ic benefits of sust ainable fisheries are known to be high. For the fisher, the decision w hether to catch fishes now or leave them in the sea w ill depend on their future va lue. If the value of a fish stock 5 years in the future is perceived to be less than the money that could be made after 5 ye ars by catch ing the fish now, selling them, and investing the money in a bank, then there is an economic incentive to fish as hard as possible in the short-term . This is known as 'disco un tin g the future'. Discount rates are used to measure the rate at w hich the perceived value of a resource, such as a fished stock, falls over time. Discount rates reflect the cost of return on altern ative investments. Thus if you 'invest ' so me money in fish by leaving them in the sea, you require that its value should grow at least as fast as the value of money in the bank. If the value of fish in the sea grows more slowly, or if the future value of the fish might be jeopardized by activities of competing fishers, then it is a good economic strategy to catch the fish sooner rather than later. The present value (PV) of income V, t years into the future is:

v,

set operational management obj ectives. The science

PV(V,) =

sup port and adv isory process must th erefo re seek to guide the choice of objectives and met hods of achieving them. This work is cu rrently in the early stages, but is likely to revo lve arou nd the development of a suite of indi cators of human activity and ecosystem impacts that can be used to measure the success of management and th e respo nse of the ecosystem. With any such approach , the main challenges are separating the ecological impacts of the human activ ity fro m the impact of environmenta l and

(l

+ 8)'

where 0 is the discount rate. The decline in perceived value of a unit of income at different discount rates is shown in Fig. 16.4. High discount rates (typically 0.1 to 0.2) tend to be used by fishers because fishers are uncertain about reaping the benefits from fishes left in the sea, especially when their competitors might catch them, and processes such as stock recruitment are highly unpredictable. Fishers' rates are typically higher than bank interest rates and thus it generally pays to catch fish and invest the profits. This explains why

clim atic effects, and deve lo ping an approach that

1.0. - - - - - - - - - - - - - - - - - - ,

is sufficiently powe rful to detect imp acts on the ti mescales that matter to managers (the lifetime of Governments and often sho rter).

0.8

The Co mm ission set up by the 1982 Convent ion on the Conservat ion of Antarctic Marine Living Resources

(CCAMLR) has ta ken an ecosystem approach to tackli ng anthropogenic (mainly fishery-rel ated) mortality

m

of marine animals. The problems include loss of alba-

m

t rosses and petrels to fishery long-lines, entanglement

~

0.6

0

> >

.= 0

~

0.4

of marine mammals in marine debris, and impacts of fishing on the seabed. In the first case, the Commission acted by controlling the timing of fishing and manner of

0.2

fish offal disposal, as well as requiring scientific observers on all vess els fishing outside nat ion al w aters in CCAMLR areas. The management of the Great Barrier

o

10

Reef Marine Park (Box 16 .4 ) also provides an example

20

30

40

50

Time Iyearsl

of an ecosystem approach. For fu rther details see the CCAMLR (www.ccamlr.

org) and GBRMPA (www.gb rmpa.gov.au) websites.

Figure 16.4 The decline in the perceived value of a unit of income at different discount rates. Thus the economic benefits of intact and the modified ecosystem must be directly co mpared .

16.4 Economics of conservation •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

species such as whales, wit h very low growth rates, were 'mined' rather than fished sustainably. Market instruments that capture at a private level the social and global values of sustainable fishing through, for example, premium pricing for sustainably harvested fish, may be an important step towards sustainability (Kaiser & Edwards-Jones 2006). OUf arguments about the effects of discounting on fisheries also apply to other forward projections of value; for example, in the context of climate change. Thus if global warming has costs in 25 years, the willingness to invest in mitigating them now wo uld be very low, even if the discount rate were small (Hanley 1998 ). Where areas of the marine environme nt are being converted for human uses, such as aqu aculture, there are several key questions to ask about the costs of such conversion. For example, what is being lost and what gained, who are the beneficiaries and losers, and what is the economic rationale for conservation? In recent years, a growing range of approaches have been applied to value the services provided by marine ecosystems (Techn iques box) . Valu ing

TECHNIQUES: Valuing marine ecosystems

the functions of intact ecosystems alone is inadequate for supporting decision-making because human-converted ecosystems also have value to society. Thus the economic benefits of intact and the modified ecosystem must be directly compared. Two marine case studies are instructive in this regard. Full economic valuation of Philippine mangrove, as against the aquaculture to which it may be converted (assuming a 6% discount rate over 30 years), shows that conversion makes sense in terms of short-term private benefits . However, when external costs such as loss oflong-term timber and charcoal supply, offshore fisheries, and storm protection, are incorporated, the total economic value (TEV) of mangrove is around 70% greater than that of shrimp farms. Sim ilarly, on Philippine reefs (assuming 10% discount over 10 years), destructive fishing practices had high initial benefits to the users, but the benefi ts of sustainable reef fisheries and tourism were then lost. The TEV of intact reef was 75% higher than that of a destructively fished reef (Balmford et aJ. 2002).

about their (hypothetical) responses to changes in the availability of ecosystem services. For example, in the

There is growing pressure to emphasize the economic

contingent valuation approach, people may be asked how

costs and benefits of different conservation options, and a

much they are willing to pay (WTP) , or, alternatively, how

range of tools have been developed to value marine eco-

much they are willing to accept (WTA) in compensation,

system services. Broadly, economic valuation methods can

for a given change in an ecosystem service. While conti n-

be divided into revealed preference or stated preference

gent valuation methods focus on payments, choice mod-

methods that value use and non-use values, respectively.

elling is an alternate stated preference method in which

Revealed preference methods estimate the ' use value' of

people are asked to rank the acceptability of the status

ecosystems, while stated preference methods provide an

quo against other scenarios for ecosystem services. A

alternate approach when services are not marketed. This

criticism of WTP methods is that they can generate unre-

is a particularly useful approach for rather nebulous con-

alistic values that have yet to be tested by attempting to

cepts such as 'beq uest value' and 'cultural value'.

extract the stated value from human society.

Revealed preference methods can include market

All the methods for valuing ecosystem services are

analysis where, for example, coral reefs or fisheries are

subject to biases and concerns, and the development

valued in terms of their contribution to tourism or catches.

of these methods is an active area of research. Another

In other cases, avertive behaviour and replacement-cost

issue that has recently been raised is the need to avoid

methods may be used. These assume that the cost of

double counting when valuing services. For example,

aver ting environmental damage is a proxy for the benefits

when services are classified in groups such as 'support-

that a service provides or that the replacement cost of a

ing services ', 'provisioning services', 'regulating services',

service provided by marine ecosystems, such as nutrient

and 'cult ural services'. To avoid the risk of double coun t-

cycli ng, is a proxy for its value. Another example mig ht be

ing, Fisher and Turner (2008) recent ly proposed an

the loss of a mangrove forest that fulfils many functions

alternate classification of servi ces as 'intermed iate' (e.g.

including prevention of storm damage to the coastli ne. A

prima ry production, nutrient cycl ing) , 'fi nal services' (e.g.

'value' can be attributed to this service in terms of the

habitat provision, fisheries production), and 'benefits'

cost incurred to build a concrete breakwater to replace

(e.g. food and recreat ion) , all supported by abiotic inputs

this service if the mangrove were to be removed.

like sunlight and nutrients. In this approach, servi ces and

Stated preference methods include choice modelling and contingent valuation. Here, people are questioned

benefits are distinguished and double-counting is avoided because only the final benefits are valued.

Chapter 16 Conservation

Table Expressed willingness to pay (Euros) to prevent a given (10 %) decline in marine biodiversity of different taxa or marine biodiversity in its entirety showing the median and mean values stated by

residents and vi sitors to the Azores (Ressurreicao et al, 2010). Level of Loss

Sample Group

Median

Mean

Algae

10 %

Visitors

23 €

66 €

Birds

10 %

Visitors

25 €

71 €

Fish

10 %

Visitors

30 €

86 €

Invertebrates

10 %

Visitors

24 €

68 €

Mammals

10 %

Visito rs

30 €

85 €

All marine species

10 %

Visito rs

138 €

58 1 €

Valuation Scenario

• • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • • ••

Algae

10 %

Residents

16 €

45 €

Birds

10 %

Residents

17 €

48 €

Fish

10 %

Residents

20 €

58 €

Invertebrates

10 %

Residents

16 €

46 €

Mammals

10 %

Residents

20 €

58 €

All marine speci es

10 %

Residents

96 €

405 €

This image shows a researcher questioning tourists about their willingness to pay to prevent a given loss in species diversity in the Azores Archipelago. The study investigated preferences for marine mammals, seabird s, fi sh , marine invertebrates, and algae (see table). As in other studies, there were stronger preferences for the charismatic fauna (fish and mammals), but, more importantly, respondents were willing to pay much more to co nserve ' b io d iversity' in its entirety co mpared with the summed values they gave for each of the taxa independentl y. An extension of this study also revealed that WTP for biodiversity was relatively consistent over a 3-year period that straddled the global financial crisis between 2007 and 2009, which demonstrated an unexpected resilience to the background economic climate.

16.5 Conservation policy and legislation •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Other copitol inputs

Ecosystemsand the production of services

D Primary and intermediate processes

BioturbotiO"r---V

Nutrient '--'\ cycling

Biodiversity

Final ecosystem services

Goodsjhenelits

People

~ Volueo! goods....

~ ....01 which II value

Food production ,--,/

Mangrove '--'\

trees Primary production r-r-v

Biomass r--V

Ieaste! defence

A schemat ic to show the provision of primary and intermediate processes by biodiversity through t o final ecosystem services and how these underpin the provision of good s o r benefits to human society. Goods have direct

monetary va lue that ca n be traded as commodities, whereas ecosystem services (ES) have monetary value that is assessed through the techniques described in this box such as 'will ing ness to pay' (adapted from Fisher et al. 2008).

16.5 Conservation policy and legislation Human impacts on the marine environment are determined by the actions of individuals, villages, towns, cities , nations, and businesses steered by government regulations or ince ntives, social pressure, conscience, or market forces. These impacts can be mitigated, even eliminated , by a variety of means, but in this the actions of individuals are of paramount importance. Human behaviour can be infl uenced by many means includ ing education, persuasion, economic incentives, legal pressure , and militar y force. Broadly speaking, conservation faces a choice between top-down and bottom-up approaches, or more usu ally some mixture of the two, to achieve its goals. The greater the proportion of society that is influenced by its own desire to conserve, the more effective conservation is likely to be. In practical terms, this means that humans impacting the environment should see and share in the benefits of conservation and sustainable development. This requires effective education. Two countries that exemplify this are Australia and New Zealand. These countries h ave adopted extremely 'green' policies towards use of the marine environment.

Education and experience in the early years of life have a major influence on attitudes and actions . Childre n who regard conservation as an important issue are likely to retain this opinio n when they diverge into a ra nge of careers or lifestyles. Education, at least for most children and young adults, is based on a syllabus that is mandated by regional or national government. The content of this syllabus can influence how people subsequently respond to, and deal with, sustainable development issues. In many countries, the general 'greening' of government policy is now reflected in the school syllabus and this has encouraged childre n to think about the role of conservation and sus tainable development, and has also increased aware ness of issues such as climate change that may not be locally visible. However, childre n attend ing a small school on a Pacific island where 90% of animal protein comes from fish will have a very different perception of the marine environment from childre n at a landlocked inner city school where their exposure to marine species is through aquaria, supermarket counters, and restaurants. Education level also strongly influences the responses given in contingent valuation studies of ecosystem services. People educated to degree level or higher cons istently give more pos itive res ponses or are willing to pay higher values to conserve abstract concepts such as

Chapter 16 Conservation Figure 16.5 Monterey Bay Aquarium in California, USA, is one of many large aquariums that runs education programmes with a strong conservation message. Copyright

Monterey Bay Aquarium.

biodiversity. Care needs to be taken to tease out people's willingness to pay from their ability to pay-richer people are able to pay more than those with low incomes (Ressurreicao et al. 2010) .

sity and the Johannesburg World Summit on Sustainable Development (WSSD) (Box 16.1) . Several governments

Nature reserves and public aquaria also play an increas-

have expressed aspirations to move towards embedding

ing role in teaching parties of visiting schoolchildren and adults about the marine environment. For example, the Monterey Bay aquarium in California, USA opened in 1984 and is visited by 1.8 million people a year. This aquarium

the principles of sustainable development in all a spects of

runs education programmes to raise awareness of overfishing of ocean species, such as the bluefin tuna (Fig. 16.5) .

Thus by displaying related rona species in aquaria, visitors are able to see animals that would rarely be seen except in

cans and photographs. This must have a major effect on perceptions ofthese animals, which will increasinglybe seen as beautiful and endangered sea creatures, rather than overpriced food in short supply. For those parts of society that do not see the benefit of

sustainable development. or are unable to support it. economic incentives and legal measures are needed. Rigorous policing and heavy fines do change the behaviour of some groups of people but they are unlikely to be effective with-

out the support of wider society, and this support is most likely to be gained through persuasion and bottom-up processes, such as those fostered by education.

Policies on sustainable development are influenced by the electorate. non-governmental organizations (NGOs), the media, science, industry, and economic and military concerns. Governments are lobbied on many issues by people with many perspectives (st akeh old ers), and for every

argument in favour of conservation and sustainable development, there are likely to be opposing arguments from

those sectors of society that fear losses of food. income. or access rights. Nevertheless. there is a general 'greening' ofgovernment

policy, driven in part by international gatherings and dec-

larations such as the Rio Convention on Biological Diver-

policy, rather than having an environment ministry that has to compete with, rather than work with. other ministries. such as industry, transport, and fisheries, for funding and

influence. Indeed. the treaty of the European Community states 'that environmental protection requirements are to be integrated into the definition ofCommunity policies and activities. in particular with a view to promoting sustainable development'. Of course, it often takes a long time for such high-level aspirations to be converted into action. Many current systems for marine environmental management are confused by conflicting interests and shared responsibility. For example, in UK estuaries, human activities are regulated by at least 80 parliamentary acts and a series ofEU regulations. Even though several estuarine sites of important conservation status have been designated for protection as SSSls (Sites ofSpecial Scientific Interest), port and harbour authorities still regulate shipping activity in

these areas, and gravel or sand extraction can be licensed. Thus many perceive sites that have legislated conservation status to be 'paper parks' that have only weak enforcement to prevent degradation of conservation features. Even in cases where the need for rapid conservation action is recognized. many groups often have to liaise and reach agreementbefore action canbe taken. Thus the North Atlantic right whale (Eubalaena glacialis ) was brought near to extinction by commercial whaling, and by the 1900s the population numbered around 300 individuals. Despite

complete cessation ofcommercial whaling. the right whale was still at risk from entanglement in fishing gear and col-

16.5 Conservation policy and legislation •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

lision with ships. A population analysis in 1998 suggested that the rates of mortality affecting the whale population could drive the whale to extinction within 200 years (Caswell et al. 1999). The only way to save the whale was to reduce mortality, and this could best be achieved by reducing the probability of ship collisions, which accounted for 80% ofall deaths. Such collisions often occurred in the Bay of Fundy, where a shipping route crosses one of the main feeding areas used by the whales. In late 2002, after several years of pressure from the WWF and other bodies, the International Maritime Organization gave the Canadian Government permission to reroute shipping in the Bay of Fundy. The new shipping lanes came into effect on 1 July 2003 and are expected to reduce the risk of ship collisions by 80% and should help to prevent the extinction of the population (Fig. 16.6). Clearly in such cases, good scientific advice, and both national and international understanding and agreement, are needed. International agencies can playa key role in coordinating conservation actions across many areas ofjurisdiction. Thus whales, turtles, fishes, and water currents do not respect national boundaries, and local or national conservation will often be ineffective. The International Whaling Commission, for example, tries to regulate whaling on a global scale, though agreement is hard to reach in such an international agency when countries perceive conservation issues in different ways and some seek to continue exploitation while others strive to ban it.

The recognition that management of many human activities in the marine environment has become overly complex and heavily influenced by sectoral concerns has prompted the development of an ecosystem approach (Box 16.3) . This approach builds on other attempts to improve cooperation among sectors. through approaches such as 'int eg rated coastal zone management' (lCZM), which have already been widely used with various levels of success in some coastal regions. Integrated coastal zone management (lCZM) is a dynamic, multidisciplinary, and iterative process that promotes sustainable management of coastal waters and lands (coastal zone). ICZM brings together all those involved in the development. management. and use of the coast in a framework that facilitates integration of their interests and responsibilities. Over the long term. ICZM seeks to balance cultural, economic, environmental. recreational. and social objectives in order to achieve common goals. In Europe the environmental concerns that have led to the development of ICZM thinking include the impacts of fishing (Ch apter 13), aquaculture (Chapter 14), pollution (Chapter 15), rapid human population growth, and poor employment opportunities in coastal communities. Integrated coastal-zone management provides a framework for management of multiple human impacts and activities. The integrated approach of ICZM is consistent with the ecosystem approach to management in t he marine environment.

•

., Grond ' Monon

r

•~

%.-"

Island

Atlantic Ocean New .hipping lanes - - Old .hipping lanes - - _. Right whale feeding grounds

Figure 16.6 Shipping lanes in the north-west Atlantic were moved to reduce the probability that endangered

right whales wou ld be struck by ships.

A European Union (EU) ICZM Demonstration Programme consisting of 35 projects in a range of socio-economic. cultural. administrative, and physical conditions across Europe in 1996 to 1999 concluded that a sectoral approach (e.g, dealing with issues impact by impact) to management did not meet the needs of managing complex issues in coastal areas. Management should therefore be inherently inter- and multidisciplinary; promote integration of the terrestrial (e.g. human settlements. watershed considerations) and marine (e.g. fisheries) components; highlight the need for integration of all relevant policy areas, sectors, and levels of administration; and use informed participation and cooperation ofall interested and affected parties to assess the societal objectives. In short. ICZM implies a new style ofgovernance that involves partnership with all ofthe segments of civil society, and solicits the collaboration ofall coastal zone stakeholders in the conception and implementation of a development model that is in their mutual interest (European Commission 2000) . Eight principles have been drawn from successful coastal management initiatives and helped to form the basis for a call on ED member states to set up national strategies for ICZM by 2006 (European Commission 2002) . These principles include: (1) a broad overall perspective; (2) a long-

Chapter 16 Conservation term perspective taking into account the precautionary principle; (3) adaptive management; (4 ) local specificity and diversity; (5) working with natural processes and carrying capacity of ecosystems; (6) involving all parties in the management process; (7) support and involvement of relevant administration bodies at national, regional, and local levels; (8) a combination of instruments to facilitate coherence between sectoral policy objectives. Thus in Europe, the move towards ICZM recognized the important role of coastal lands and waters for nature and ICZM is an ambitious strategy, or at least a wish list, for addressing some of the overarching environmental concerns for the coastal zone. ICZM is considered a prerequisite for successful management of coastal and marine resources around the world, and many international bodies, such as the Food and Agriculture Organization of the United Nations. Intergovernmental Oceanographic Commission, United Nations Environment Programme, and the World Bank. support and promote ICZM. When it comes to environmental decision-making at a global level, the dichotomy in the sustainability, profitability, and capacity for species' and habitat conservation in the developing and developed world needs to be recognized. Developing countries still have some of the greatest assets in wilderness areas and biological diversity. but they have the greatest human population growth rates and fewer resources for conservation. It is also worth remembering that opportunities for conservation in developed Western nations are often subsidized bypoor people. The removal of capacity in developed countries can have harsh social and economic consequences in the short term but, in the longer term, these are often softened by government subsidies and job opportunities in other sectors of the economy. In the poorer countries of the world, fishing is often the occupation of last resort for families with no other opportunities for subsistence. The scale of poverty and reliance on fisheries in the developing world has been widely described elsewhere (Kent 1998) . It is possible that 1 billion people in 40 developing countries may lose access to their primary source of protein as a result of overfishing (UNDP 2003) . The international community will have to intervene to provide funding for conservation in the poorer countries. This would, for example, include providing the means to generate alternatives sources of livelihood to alleviate the poverty that lies at the root, for example, ofdestructive fishing practices and unsustainable coastal development that threaten biological diversity.

16.6 Conservation in action Action to meet the objectives of marine conservation is being taken on many fronts, and this has involved many levels of ecological (species, habitats, ecosystems) and

administrative (local and international, NGO and governmental) organization. To show how all of these levels are being incorporated is beyond the scope of this book; instead we give three examples that help to illustrate the range of actions involved. The first of these is the assessment of environmental risk in any project, in the process referred to as 'enviro nmen t al impact assessment' (EIA) . The second is ecolabelling, which provides consumers with a basis for environmental choice and seeks voluntary participation of an industry in practices that meet sustainable development objectives. The third is the use of marine reserves (marine protected areas), from which fishing and other forms of extractive use are excluded. As we consider these various forms of conservation action, it is worth considering the overall context in which conservation policy is implemented. Most conservation action is ultimately driven by high-level objectives. As we have seen, these objectives are often chosen internationally at fora such as the World Summit on Sustainable Development (Box 16.1). Then, sustainable development strategies have to be developed to help meet the objectives. Conservation actions consistent with the strategies are then taken to meet the objectives. Progress towards objectives is monitored, and strategies and actions (hopefully not objectives!) amended to ensure objectives are met.

16.6.1 Environmental impact assessment (EIA) The aim ofElA is to prevent. reduce, or offset any adverse impacts of each and every major development affecting the environment, including the sea (Barrow 1997) . EIA is a formal process to identify and predict the environmental impacts of a project, with a view to mitigating adverse impacts or addressing them in revised plans. Such assessments are required for activities such as oil-rig and wind-farm construction, and aggregate extraction. Interestingly, however. fisheries' development is usually exempt from EIA. The omission of fishing has led to some internal argument among the industries concerned in Europe, since fishing has been identified as the greatest threat to the marine environment by the Oslo and Paris Commission, which upholds the Convention for the Protection of the Marine Environment of the North-East Atlantic from dumping and land-derived and offshore sources of pollution. The purpose of EIA is to support the objectives of conservation and sustainable development by integrating environmental protection requirements into the planning process at the earliest possible stage. The EIA process serves to predict the environmental. social. economic. and cultural consequences of a proposed activity and to assess plans to mitigate any adverse impacts resulting from that activity. Although there is much variation in practice, particularly among countries, EIA often provides a focus

16.6 Conservation in action •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

for the involvement of society in reviewing the potential impact of the activity, through submissions from the public and government bodies. Environmental impact assessment aims to predict the impacts of development and to mitigate or avoid those impacts that are unsustainable.

Once it is decided that an EIA should go ahead, a sixstage process begins. This involves seoping, quantification, report production, decision on project, and, if the development is allowed to go ahead, development and monitoring. During seoping, all the potential impacts of the projects are listed, and during the quantification stage, the magnitude of each impact is assessed in relation to the existing habitats, species, and activities at the proposed development site . Based on scoping and quantification, an Environmental Statement is produced and this is reviewed by government and associated agencies to determine whether development should go ahead. A developing and more comprehensive form of impact assessment is Strategic Environmental Assessment (SEA) . SEA assesses the wider impacts of any development. taking account of interactions with other forms of development and the wider environment.

16.6.2 Ecolabelling Consumer choice can have a powerful influence on the use of the marine environment as demonstrated by the boom in sales of 'do lp h in friendly' or 'd olp h in safe' tuna when the public saw the first pictures of dolphin kills in tuna purse seine net fisheries . Today, increasingly detailed information is available on the provenance of wild caught fish. What we ultimately buy in the supermarket may influence the behaviour of fishers and other users of the marine environment.

In Great Britain, the Marine Conservation Society publishes a 'Good Fish Guide' to help consumers who like to eat seafood but are concerned about the impacts of fishing on fish stocks, marine wildlife, and habitats, to choose fish that come from sustainably managed fisheries that minimize damage to the marine environment and do not harm other wildlife. Organizations such as the Seafood Choices Alliance are important non-governmental bodies that attempt to generate consensus among users of seafood (retailers. processors, importers. and catching sector) about how to move towards sustainable and safe seafood (see website http :/ /www.seafoodchoices.com) . Internationally, the Marine Stewardship Council (MSC) runs a market-based certification programme and seafood

ecolabel to recognize and reward sustainable fisheries . The MSC was founded in 1996 as ajoint venture between WWF and Unilever, became an independent charitable organization in 1999. and is funded by grant income and royalty fees paid for use of the MSC ecolabel on products. Products bearing the MSC ecolabel have won the patronage of royalty and celebrity chefs alike, and retail giants put MSC ecolabelled products on their shelves, with an ever increasing range of different products currently on offer. Fisheries certified under the MSC scheme include the Western Australian rock lobster, New Zealand hoki, Bering SealAleutian Islands pollack, and Alaska salmon. The certification process is conducted by a panel of independent scientists who assess the fishery against criteria for the status of the stock, ecosystem impacts due to fishing, and the management systems in place (Philipps et al. 2003) . Several groups now certify or recommend fishery products from sustainable fisheries (see http://www.mcsuk.

org and www.msc.org).

With the commitment to improving fishing practices by the industry, qualification for the MSC ecolabel should be relatively straightforward for fisheries where the choices of how much fish to catch and how to catch it are under the control of a single group of fishers. It will be in their interest to invest in long-term sustainability and in ecolabelling that will attract premium prices and access to consistent markets. However. as we saw in Chapter 13. the majority of the world's fisheries are not like this, and most fishers have little control over the setting of fishing quotas. and they share the fish resource with other fishers and nations who may not choose to fish responsibly and are caught up in the race to fish . Fishers who participate in these fisheries may be impeded from realizing their ambition to move towards MSC certification due to the actions of others that are beyond their control. Thus the MSC scheme focuses very much on consumer choice as the driver for change in fisheries (Kaiser & Edwards-Jones 2006) . Interestingly, although consumer choice is held up as the main driver for change by the MSC, it is the major retailers that have had the most significant impact in terms of changing fishers' behaviour to date. Many of the world's largest retailers have stated a desire to source all fish-related products from MSC certified fisheries by 2012 . Thus retailers have set a new standard. irrespective of consumer choice. The reasoning behind this may seem to be a wholehearted acceptance of sustainable use of natural resources, but another explanation may be simply that unreliable sources of fish from collapsed or teetering fisheries is simply bad for business and over-complicates supply-chain logistics. Irrespective of the above, the MSC benchmark set by retailers has initiated significant changes in the attitude and behaviour

Chapter 16 Conservation of fishers' organizations in d eveloped countries (previously many were skeptical of the benefits of accreditation) and this is perhaps reflected in the tenfold increase in the number of certified fisheries in just the last 5 years. The MSC has its detractors and supporters, leading to contemporary debate on the role of the organization in promoting sustainable fishing (see Hilborn & Cowan 2010; Jacquet et al. 2010; Kaiser & Hill 2010).

16.6.3 Marine reserves Reserves, where human activity is spatially controlled or banned, have useful roles to play in marine conservation and there has been an upsurge of interest in them, often stimulated by growing appreciation of the effects of fishing on habitats and species. It is notable that < 1% of the marine environme nt has reserve status as opposed to 6% of land, and this alone suggests that marine reserves need to be more extensive than they are. No reserve can be fully effective at protecting m arine life if ships can spill oil and ot her toxic su bstances in the vicinity, if curre nts feed contaminan ts to the animals living there, if animals migrate from the reserve and can be affected by fishing or pollution elsewhere, and if climate change drives the protected species to ot her locations. The proper solution to these problems lies in the effe ctive regulation of the human activities involved. Thus far, the greates t progress in tackling large-scale issues in marine conservation has involved t ackling the impacts directly. For exa mple, by stopping whalers killing whales, preventing yachts using TBT on their hulls, and controlling d ischarges of heavy metals and radio activity into the marine environmen t (Chapter 15). Wit h some of these activities controlled, and moves towards greater limitation of fishing effo rt, now is a good time to start using reserves more widely to support marine conservation.

Box 16.4: The Great Barrier Reef Marine Park

Marine reserves protect a very small proportion of the marine environment. In the open marine environment, the use of reserves for conservation must go hand in hand with control of human activity outside the reserve.

One of the success stories in marine reserve conservation is that of the large Great Barrier Reef Marine Park in northeastern Australia (Box 16.4). However, many marine reserves are small and vulnerable to climatic events, landderived pollution and run-off, and poaching. Small reserves on and around coral reefs have provided most of the evidence for the potential conservation benefits of reserves. Most important has been the demonstration that when protection is effective, many site-attached reef fish species and invertebrates attain greater densities and sizes than in areas where they are fished. This may be important to fisheries because these species may produce larvae that w ill support recruitment to fished areas, may themselves migrate out into the fished areas, and, in the case of rot ational closure, ma y ultimately be caught directly. Alt hough there is some evidence for rapid buildup of abundance of fished species soon after protection, this is very soon dissipated when areas are reopened; thus rotational closure seems not to be a useful strategy, unless fishing effort is otherwise curbed. With respect to other potential benefits of marine reserves to fisheries, late juve niles and adults do mi grate to fished areas, but the movement is often over small distances, and unless fishing effort is otherwise reduced, this is unlikely to compensate for the loss of yield due to protection. The protection of adult fishes to ensu re larval recruitment to fished areas is perhaps the most useful potential benefit of marine rese rves to sustainable fisheries, but regrettably, it is the least well understood. Once establishe d, marine reserves can undoubtedly

Barrier Reef Marine Park Authority (GBRMPA), and the GBR was recognized as a World Heritage Site in 198 1.

The Great Barrier Reef (GBR) Marine Park is an example

The GBR Marine Park is divided into four sections for

of one of the first attempts to conserve and manage at

management purposes (figure a), and the challenge for

the ecosystem scale. The GBR Marine Park Act (1975)

managers is deciding who can do what and where in each

underpins the conservation of the GBR, providing for

of the sections. Zoni ng plans for each section (e.g. figure

conservation of the GBR and sustainable use of the sur-

b) provide for activities that are as-of-right, wi th permis-

rounding region. The main tool for protecting and preserv-

sion, or prohibited, and widely available maps ensure that

ing the GBR, as requi red by the Act, is zoning. Zoning

all potential users are aware of restrictions on their move-

separates conflicting human activities and protects the

ments and activities.

most vulnerable areas. The Park is managed by the Great

16.6 Conservation in action •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

The least rest rict ive zones are 'general use' in which

(b)

activi ties such as shippi ng and traw ling may be permitted, but mining, oil drill ing, commercial spear-fishing,

,•

and spear-fishi ng with breathing apparat us are not

••

e

Other zones provid e for habitat protection, estuarine conserva tion, or general conservation, w hile pe rmit-

•e 0

a

•

~

ting restricted commercial or recreat ional use. The most

uowlture Bait nellin Booti ,di¥i , hoto ro h (rabbin tro in Horm t filhing lor aQuarium fish, rl n eIIhwr Hormt fi lhing lor lell IU[umber,lrolhul, tro ilol rOlk lob~er Limited lolleltin Limited I ear filhin lnorkelonl Line filhin Nelli n other than boit neni Reseonh other than limited im II resecnh Shipping (other than in a delignated Ihipping oreo) Tourilm Pro rom Trocnionol use of marine reseures Trowli Trolling

restrict ive zones are 'marine national park zones', w hich

are no-take 'areas'; 'scientific research zones', which only all ow access fo r agreed scientific research; and 'preservat ion zones' w here all entry is prohi bited except in emergencies and to con duct scientific research that woul d be impossible elsewhere. In 2004, a new zoning plan w as introduced to incorporate 28 new coastal protected areas and a Representative Areas Prog ram, w hich ensu res that examples of th e ent ire range of habitats and biodiversity are represented wi thin highly Marine National Park zones. 14"\

(0)

A-N (oral See •• • •••

.. --.. ~---~

--...

-----

Permit

•s •

•• a

•~ --• , • •• -• i -. ,s .• • • • j s l' •s •

-~

~

.~

•• 0

• 0

~

~

e • ':§

~

0

•0

• ••• • 0

• •

~

••

0

•a

• 0

0

~

Permit Permit

Permit

Permit

rT----,----------,---,-------,----,

ws

For Northern section

;:::::== ~

Inirm senen (cru] Sec

-~-_.-_.-

renfrel

section

.--

.... Mockoy(nprirom senen

Iuims •

The four management areas of the Great Barrier Reef Marine Park.

Zoning of the Cairn s/Cooktown Management Area of the Great Barrier Reef Marine Park with a key t o permitted activities. For further details see the Great Barrier Reef Marine Park Authority website (http:/ /www.gbrrnpa.gov.au).

Chapter 16 Conservation

Box 16.5: Paying for marine conservation Polici ng Mari ne Protected Areas (MPAs) is an expensive busi ness and governments rarely provide adequate fundi ng. Given that the polici ng and management of a small MPA requi res several staff and around € 100 000 per year, income from recreational divers tha t use MPAs could make an important financial contribution to effective marine conservation.

Over 200 MPAs in the Caribbean and Central America contain coral reefs that are likely to attract recreat ional scuba-divers. Indeed, a survey of MPA use by dive operators showed that 46% conduct at least 80% of their diving in a MPA

At present, only 25% of MPAs wi th coral reefs charge divers an entry or user fee, and this is typically €2-3 per dive or diver. However, divers have already shown willi ngness to pay up to €25 per day to access some MPAs, and this is only a fraction of their total expendi ture on equipment, training, accommodation, and entertainment. The wider Caribbean and Central America is a prime location for diving and attracts 57% of all international scuba-diving tourists. Provided the recreational use of MPAs can remain consistent with the goals of conservation and sustainable development, higher charges for diving access to all MPAs would help secure much needed funding for MPA protection and management. Indeed, if user fees were raised to around €25 per diver this would raise approximately €93 million per year, sufficient to cover some 78% of the predicted shortfall in funds for MPA management in this region.

Source: Green & Donnelly (2003).

h ave an important educational role in d rawing public atten tion to areas of special ecological significance, providing opportun ities to see rel atively undisturbed marine h abitats, and encouraging people to observe the benefits of conservation. The Great Barrier Reef Marine Park, and some othe r reserves around the world, also show that marine reserves can be very successful econo mically (16.6) . Th is is important, as econo mic success is likely to foster comm un ity support and good enforceme nt, both of which are paramount to success ful management. On many coral reefs, diving tourism is a key source of income to support reserve man agement. However, not all areas benefit from tourist

ex pend iture and, as wit h other conservation tools, there are socio-economic cons traints to the effective man agement of marine reserves. Some of the best studied marine reserves a re at Su milon and Apo Islands in the ce ntral Philippines, and Russ and Alcala (1996) have described 20 years of hopes and fru strations on Sumilon Island. A marine reserve was established there in 1974, but there h ave been several major breakd owns of management. Remarkably, this was at a site where the aggregate fisheries' yield from the island was higher when the marine reserve was ope rating (Russ & Alcala 199 6). One of the key problems with management on the island seemed to be that fishers were not convinced of the real benefits of the marine reserve and were not full y involved in its management. There are other examples of re peated breakdown of reserves on tropical reefs. Together they indicate that management imposed from outside the commun ity, and wit hout the support of the commun ity, is unlikely to work. Given the small areas that are designated as reserves in the marine environment and the key role that they can play in protecting species an d h abitats of conse rvation concern, they should be used more wide ly to support conservation objectives. However, the designation and effective protection of marine reserves must go h and-in-hand with direct control of overall human impacts (Fig. 16.7). In this section on conservation in action, our examples h ave shown that, because of the multiple concerns, the complexity of the issues and interdisciplinary demands of decision-makers, conservation action is as much art as science. The uncertainty of environmental decision-making was well illustrated by the concerns for deep-sea pollution raised by the disposal of the Brent Spar oil platform (Gage & Gordon 1995 ; Angel & Rice 1996) . Shell aba ndoned plans to dispose of this redundant oil-sto rage platform by sin king it in water 2200 m deep in the northeastern Atlantic. Shell had been given scientific advice that deepsea disposal was the best environmental option, but environmental groups protested that toxic residues wou ld leak from the platform and contaminate the food-chain. Greenpeace boarded the platform in a bid to pre vent its sinking and eventually the Brent Spar was to wed to a fjord in Norway to be dismantled. It may well be that the environmental costs of disposing of the platform inshore have been greater than those of deep-sea disposal, and the arrival of the platform inshore also caused controversy in Norway. Scientists have continued to d ebate the pros and cons of the various disposal options, and yet the des ire of Greenpeace to make an issue of the disposal and the ens uing campaigns at fuel stations in Germany effectively forced the final disposal option.

16.7 Evidence-based conservation •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

h~m~m .~'~~-~~·~I~ ~ ~ nli ~ DESTRUCTIVE FISHING PROHIBITED

r

De c

JJ Electricity ~{ cJ The Fisheries Prot

i(!t

r.tl

I 1'1

*;1 a 20 I~ ][ &. !f.i ~t 6 fill I J 11 Ordinance (Ca p. 17 1) carries a ~fAX'lM UM FIN E ew $200.1100 A~ J) 6 ~ IONTI IS I 'tl)H:I SO~ 'l EST III fl'1 'i'i' ilB U< fl'1 til J7 1

1'1.\ ,Ifj

,_ /i;lr1:'';

JlI! W I

Agr lcultun... Ftshcrtes and Ce nserva tlnn Department

Figure 16.7 This sign at Tai 0 fishing village in Hong Kong informs people that they can still fish, but only if they do it in an environmentally sustainable manner. The use of indiscriminate and destructive fishing practices is illegal and fishers are subject to heavy fines and a prison sentence if they ignore the warn ings. (Photo copyright: Johanna Junback.)

16.7 Evidence-based conservation As scientists, we are primarily driven by the desire to understand better the natural systems that operate in the marine environment. Understanding causal relationships requires a deductive hypothesis driven approach that aims to eliminate external influences that might generate errors in our reasoning. However, conservation is an emotive area of science and is prone to 'belief-based science', where scientists decide upon a position and then look for evidence to support it (Hilborn 2006; see Chapter 13). Similar problems can occur in the field of medicine, where scientific errors can endanger human life . Thus it is not surprising then that some of the most robust scientific evaluation methodologies have arisen in the field of medicine, where systematic review methodology has been developed to provide a framework for the evaluation

of multiple independent studies. This approach has been advocated for conservation biology through the Centre for

Evidence-Based Management (http:/ /www.cebc.bangor. ac.uk) . Systematic review defines the protocols used to search the available published literature using specific criteria for selecting or rejecting the inclusion of the studies located. The evidence-based approach is important as it generates conclusions that avoid issues of publication bias

(the tendency ofjournals to publish only positive outcomes or certain types of study) or at very least to highlight the issue. An example of the application of the approach is the study of the response of fish and other taxa to the implementation of no-take marine reserves in temperate systems

(Stewart et at. 2010) . The study validated the conclusions of some previous studies, but highlighted potential publication bias in data that reported biomass metrics as the

response variable (for fish) . The study also highlighted the potential for habitat-confounding effects in the response metrics in the reported studies, which often did not provide adequate habitat data for a robust validation of their conclusions. Anybody undertaking a systematic review soon realizes how poorly scientists report data that are

Chapter 16 Conservation vital for understanding or interpreting the reported results (journals do not like long tables of results, although the internet should make access to original data easier) . The most important characteristic of systematic review is its rigour, which provides policy makers with a high level of confidence in the reported findings and recommendations.

•

Remaining energy sources

D 14 .-- - - - - - - - - - - - - ---1 1 1

Natural gas

Hydropower

12

Mineral oils

10

16.8 Life-cycle analysis In Chapters 13 and 14 we looked in detail at the ecological issues that are associated with food production in the marine environment. Both wild-capture fisheries and aquaculture contribute significantly to the world supply of protein, and this will need to increase into the future. Aquaculture is becoming increasingly important and is likely to overtake wild -capture fisheries as the main source ofaquatic protein production inthe next 5 years. In additionto the ecological problems associated with wild-capture fisheries and aquaculture, the post-harvest processes also have associated impacts on the environment that are generated from the transport and processing of the product. It is important to consider all stages of the production process to have a truly objective view of whether one form of production might be better than another. Such an approach is adopted by Life Cycle Analysis (LCA), which was developed primarily for land-based industries. Although still in its infancy for foodbased products, it provides a valuable basis for influencing the sourcing policy of retailers. An interesting example of the application of this technique was a comparison of the environmental impacts of wild-caught cod and farmed salmon compared to farmed chicken (Ellingsen & Aanondsen 2006) . What the LCA revealed was that the capture phase (fishing) for cod and the feeding phase for salmon and chicken dominated all the other environmental impacts considered in the study. The production of chicken was the most energy efficient. but cod and salmon production were similar in this respect. However, to produce a 200 g fillet of cod, the environmental impact (footprint) of fishing gear affected an area of seabed 100 times larger than the area of land needed to grow the food necessary to produce a standard 200 g fillet of chicken. The analysis also demonstrated that, if salmon aquaculture could become more dependent on plant-derived sources of protein. it would become much more environmentally friendly than current practices used to produce salmon (Fig. 16.8) . (See also http:/ /www.ecotrust.org/lca for information about LCA ofsalmon farming.)

16.9 The future

4

2

o

Formed solmon fillet Farmed vege-salmanfillet

Figure 16.8 Life-cycle analysis showing the energy score for the production of a farmed chicken fillet, a farmed salmon fillet, or a farmed 'vegetarian' salmon fillet , given the possibility of new advances in feed production.

The energy consumed (MJ) per fillet unit (FU) is lowered considerably if salmon farming could move further away from feeds dependent on wild-capture fisheries. From:

Ellingsen, H. & Aanondsen, SA (2006) Environmental impacts of wild caught cod and farmed salmon-a comparison with chicken. International Journal of Life

Cycle Analysis, 1: 60-65.

ments to successful conservation are the massive changes to marine habitats and species that have already occurred and the emphasis on reactive rather than proactive management. However, awareness of marine conservation issues is growing and many governments have made international commitments to sustainable development and the ecosystem approach. Few of these international commitments have yet to be translated into successful conservation action, but there are some encouraging examples that suggest combined controls on human impacts and large-scale marine zoning schemes, which include marine reserves. could lead to long-term improvements in sustainability. The wealthy developed world currently has more capacity to implement conservation measures, and yet many poorer nations are responsible for species-rich and productive marine environments. In many poorer nations, prospects for improved sustainabilityare not good, unless the international community commits to supporting and financing the ecosystem approach and subsidizing the very high shortterm social and economic costs associated with moving towards sustainability. Current conservation actions take place in a marine envi-

Every contemporary conservation action takes place in a marine environment that has already been dramatically altered by human activities. Some of the biggest impedi-

ronment that has a lready been dramatically altered by human activities.

Further Reading •

••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Chapter Summary •

Conservat ion is the sustainable management of the marine environment. Sustainable management requires human intervent ion to maintain or create an environment t hat ensures that the well-bei ng of future generat ions is not compromised.

•

National and internat ional agreements express an aspiration to move towards sustainable development, and these underpin much of the conservation and environmental protection legislation that

we see today. •

There are ethical, ecological, and economic reasons to conserve, but short-term economic forces often d rive unsustainable development, despite the long-term economic benefits of conservat ion.

•

Recent conservation policy reflects a high-level aspiration to achieve sustainable development. However, converting high-level aspirations into practical , funded, and effective conservation actions remains a challenge.

•

Sustainable development includes not only biological and ecological considerations, but also involves a considerat ion of the conseq uences of actions (e.g. conservation) for local economies, and social and cultural structures.

•

Conservat ion actions invo lve many levels of ecological (species, habitats, ecosystems) and administrative (local to inter national) organization. Their success depends on the w ealt h and cul t ural values of society.

Further Reading Kunin and Lawton ( 1996) provide a holistic analysis of the importance of b iod iversity and the necessity for conservat ion. Norse (1993) provides a conservat ionist's po int of view of t he int eg rat ion of conservat io n in decision making, wh ile Sutherland ( 199B) provides an objective v iew of the role of conservation wi th case stud ies. •

Kunin, W. E. & Lawton, J. H. 1996. Does biodiversity matter? Evaluat ing the case for conserving species. In K. J. Gaston (ed.) Biodiversity: a Biology of Numbers and Difference. Blackwell Science, Oxford,

pp. 2B3-30B. •

Norse, E. A. (ed.) 19 9 3. Global Marine Biological Diversity: a Strategy for Building Conservation into Decision Making. Center for Marine Conservation, Washington.

•

Sutherland, W. J. (ed.) 19 9 B. Conservation Science and Action. Blackwe ll Science, Oxford.

References Abram, N. J ., Gagan, M. K., McCuloch, M. T., Chappell, J., & Hantoro, W. S. 2003. Coral reef death during the 1997 Indian Ocean Dipole linked to Indonesian wildfires. Science 301: 952-955. Acevedo-Gutierrez, A., Croll, D. A., & Tershy, B. R. 2002. High feeding costs limit dive time in the largest whales. Journal ofExperimental Biology 205 : 1747-1753. Ackley, S., Wadhams, P., Comiso, J . c., & Worby, A. P. 2003. Decadal decrease of Antarctic sea ice extent inferred from whaling records revisited on the basis of historical and modern sea ice records. Polar Research 22, 19-25. Adam, P. 1990. Saltmarsh Ecology. Cambridge University Press, Cambridge. Aebischer, N. J ., Coolson, J . C., & Colebrook, J . M. 1990. Parallel long-term trends across four marine trophic levels and weather. Nature 347: 753-755. Agardy, T., Bridgewater, P., Crosby, M. P., Day, J ., Dayton, P. K., Kenchington, R. et al. 2003. Dangerous targets? Unresolved issues and ideological classes around marine protected areas. Aquatic Conservation: Marine andFreshwater Ecosystems 13: 353-367. Agnew, D J; Pearce, J., Pramod, G., Peatman, T., Watson, R., Beddington, J. R., & Pitcher, T. J. 2009. Estimating the worldwide extent of illegal fishing. PloS ONE 4 (2) : e4570. Aguilera, J., Bischof, K' Karsten, D., Hanelt, D., & Wieneke, C. 2002. Seasonal variation in ecophysiological patterns in macroalgae from an Arctic fjord : II. Pigment accumulation and biochemical defence systems. Marine Biology 140: 1087-1095. Ainley, D. G., Tynan, C. T., & Stirling, I. 2003. Sea ice; a critical habitat for polar marine mammals. In D. N. Thomas, & G. S. Dieckmann, (eds), Sea Ice-An Introduction to its Physics, Chemistry, Biology and Geology, Blackwell, Oxford. Aioi, K., Komatsu, T., & Morita, K. 1998. The world's longest seagrass, Zostera caulescens from northern Japan. Aquatic Botany 61 : 87-93. Aksnes, D. L., & Giske, J . 1993. A theoretical-model of aquatic visual feeding. Ecological Modelling 67: 233250. Alfaro, A. C. 2008. Diet of Littoraria scabra, while vertically migrating on mangrove trees: gut content, fatty acid, and stable isotope analyses. Estuarine Coastal and Shelf Science 79 : 718-726. Allen, R. L. 1985. Dolphins and the purse-seine fishery for yellowfin tuna. In J . R. Beddington, R. J . H. Beverton, & D. M. Lavigne (eds), Marine Mammals and Fisheries. George Allen, & Unwin, London, pp. 236-252. J

Aller, J . Y., & Stupakoff, I. 1996. The distribution and seasonal characteristics of benthic communities on the Amazon shelf as indicators of physical processes. ContinentalShelfResearch 16: 717-75l. Allsopp, W. H. L. 1997. World aquaculture review: performance and perspectives. In E. L. Pikitch, D. D. Huppert, & M. P. Sissenwine (eds), Global Trends: Fisheries Management, American Fisheries Society Symposium. Bethesda, Maryland, pp. 153-165. Alongi, D. M. 1998. Coastal Ecosystem Processes. CRC Press, Cambridge MA. Alverson, D. L., Freeberg, M. H., Pope, J . G., & Murawski, S. A. 1994. A global assessment of fisheries bycatch and discards. FAD Fisheries Technical Paper 339. Anderson, P., & Sorensen, H. M. 1986. Population dynamics and trophic coupling in pelagic microorganisms in eutrophic coastal waters . Marine Ecology Progress Series 33: 99-109. Angel, M., & Rice, A. 1996. The ecology of the deep ocean and its relevance to global waste management. Journal ofApplied Ecology 33 : 915-926. Arcos, J . M., Ruiz, X., Bearhop, S., & Furness, R. W. 2002. Mercury levels in seabirds and their fish prey at the Ebro Delta (NW Mediterranean) : the role of trawler discards as a source of contamination. Marine Ecology Progress Series 232: 281-290. Aristegui, J ., Agusti, S., Middelburg, J . J., & Duarte, C. M. 2005. Respiration in the Mesopelagic and Bathypelagic Zones of the Oceans. In P. A. del Giorgio, & P. J .le B. Williams (eds), Respiration in Aquatic Ecosystems. Oxford University Press, Oxford, pp. 181-205. Arlinghaus, R., Cooke, S. J, Schwab, A., & Cowx, 1. G. 2007. Fish welfare: a challenge to the feelings-based approach, with implications for recreational fishing. Fish, & Fisheries 8 : 57-7l. Armbrust, E. V. 2009. The life of diatoms in the world's oceans. Nature 459 : 185-192. Arntz, W. E., Brey, T., & Gallardo, V. A. 1994. Antarctic zoobenthos. Oceanography and Marine Biology, An Annual Review 32: 241-304. Arntz, W. E., Gutt, J ., & Klages, M. 1997. Antarctic marine biodiversity: an overview. In B. Battaglia (ed.) ,Antarctic communities: species, structure and survival, Cambridge University Press, Cambridge, pp. 3-14. Aronson, R. B., Macintyre, 1. G., Wapnick, C. M., & O'Neill, M. W. 2004. Phase shifts, alternative states, and the unprecedented convergence of tow reef systems. Ecology 85 : 1876-189l. Arrigo, K. 2005. Marine microorganisms and global nutrient cycles. Nature 437: 349-355.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Arrigo, K. R., van Dijken, G. L., &Pabi, S. 2008a. The impact of a shrinking Arctic ice cover on marine primary production. Geophysical Research Letters 35, L19603, doi: 10.1029/2008GL035028.

Auster, P. J ., Malatesta, R., & Donaldson, C. 1997. Distributional responses to small-scale habitat variability by earlyjuvenile silver hake, Merluccius bilinearis. Environmental Biology ofFishes 50: 195-200.

Arrigo, K. R., van Dijken, G. L., & Bushinsky, S. 2008b. Primary Production in the Southern Ocean, 1997-2006. Journal of Geophysical Research 113.C08004, doi: 10.1029/2007JC004551 . Atkinson, A., Seigel, V., Pakhomov, E., & Rothery, P. 2004. Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432: 10D-103. Attrill, M. J . 1998. A Rehabilitated Estuarine Ecosystem: the Environment and Ecology ofthe Thames Estuary. Kluwer Academic Press . Attrill, M. J . 2002 . A testable linear model for diversity trends in estuaries. Journal ofAnimal Ecology 71: 262269. Attrill, M. J ., & Power, M. 2000a. Modelling the effect of drought on estuarine water quality. Water Research 34: 1584-1594. Attrill, M. J., &Power, M. 2000b. Effect on invertebrate populations of drought induced changes in estuarine water quality. Marine Ecology Progress Series 203 : 133-143. Attrill, M. J., & Power, M. 2002. Climatic influence on a marine fish assemblage. Nature 417: 275-278. Attrill, M. J ., & Rundle, S. D. 2002. Ecotone or ecoeline: ecological boundaries in estuaries. Estuarine and Coastal Shelf Science 55: 929-936. Attrill M. J., Harmoll R. G., &ThurstonM. H. 1990.Adepthrelated distribution of the red crab, Geryon trispinosus (Herbst) [= G. tridens Kroyer]: indications of vertical migration. Progress in Oceanography 24: 197-206. Attrill, M. J ., Rundle, S. D., & Thomas, R. M. 1996. The influence of drought-induced low freshwater flow on an upper-estuarine macroinvertebrate community. Water Research 30: 261-268. Attrill, M. J., Power, M., & Thomas, R. M. 1999. Modelling estuarine Crustacea population fluctuations in response to physico-chemical trends . Marine Ecology Progress Series 178: 89-99. Attrill, M. J., Strong, J . A., & Rowden, A. A. 2000. Are macroinvertebrate communities influenced by seagrass structural complexity? Ecography 23: 114-121. Attrill, M. J ., Stafford, R., &Rowden, A. A. 2001. Latitudinal diversity patterns in estuarine tidal flats : indications of a global cline. Ecography 24: 318-324. Attrill, M. J. Rundle, S. D., Fraser, A., & Power, M. 2009. Oligochaetes as a possible entry route for terrigenous organic carbon into estuarine benthic food webs. Marine Ecology Progress Series 384: 147-157. Auster, P. J ., & Langton, R. W. 1999. The effects of fishing on fish habitat. In L. Benaka (ed.), Fish Habitat: Essential Fish Habitat and Restoration, American Fisheries Society, Bethesda, Maryland, pp. 15D-187.

Auster, P.J., Lindholm, J ., Schaub, S., Funnell, G., Kaufman, L. S., &Valentine, P. C. 2003. Use of sand wave habitats by silver hake. Journal ofFish Biology 62 : 143-152. Azam, F., & Long, R. A. 2001. Oceanography: Sea snow microcosms. Nature 414: 495-498. Azam, F., & Worden, A. Z. 2004. Microbes, molecules, and marine ecosystems. Science 303: 1622-1624. Azam, F. 1998. Microbial Control of Oceanic Carbon Flux: the Plot Thickens. Science 280: 694-696. Babin. M., Morel. A.• Fournier-Sicre, V., Fell. F., & Stramski, D. 2003. Light scattering properties of marine particles in coastal and open ocean waters as related to the particle mass concentration. Limnology and Oceanography 48: 843-859. Backhaus, J . 0., Hegseth, E. N., Wehde, H., Irigoien, X., Hatten, K., & Logemann, K. 2003. Convection and primary production in winter. Marine Ecology Progress Series 251 : 1-14. Baco, A. R., & Smith, C. R. 2003. High biodiversity levels on deep-sea whale skeletons. Marine Ecology Progress Series 260: 109-114. Bagley, P. M., Smith, A., Priede, I. G. 1994. Tracking movements of deep demersal fishes in the Porcupine Seabight, North-east Atlantic Ocean. Journal of the Marine Biological Association ofthe UK 74: 473-480. Bagoien, E., Kaartvedt, S., Aksnes, D. L., & Eiane, K. 2001. Vertical distribution and mortality of overwintering Calanus. Limnology and Oceanography 46: 1494-1510. Bailey, D. M., Bagley, P. M., Jamieson, A., Collins, M. A., & Priede. I. G. 2003. In situ investigation of burst swimming and muscle performance in the deep sea fish Antimora rostrata (Gunther, 1878). Journal ofExperimental Marine Biology and Ecology 285-286: 295-311 . Baird, D., Evans, P. R., Milne, H., &Pienkowksi, M. W. 1985. Utilisation by shorebirds of benthic invertebrate production in intertidal areas. Oceanography and Marine Biology: Annual Review 23: 575-597. Baker, S. M. 1909. On the causes of the zoning of brown seaweeds on the seashore, ll. New Phytologist 9 : 54-67. Bakun, A. 1990. Global climate change and intensification of coastal upwelling. Science 247: 198-201. Ball, M. c., &Pidsley, S. M. 1995. Growth responses to salinity in relation to distribution of two mangrove species. Sonneratia alba and S. lanceolata. in northern Australia. Functional Ecology 9 : 77-85. Balmford, A., Bruner. A.• Cooper, P., Costanza. R.• Farber. S., Green, R. E. et a1 2002. Economic reasons for conserving wild nature. Science 297: 95D-953. Balvanera, P., Pfisterer, A.• Buchmann, N.• He, J-S .• Nakashizuka,T., Raffaelli, D., & Schmid, B. 2006. Quan-

References tifying the evidence for biodiversity effects on ecosystem functioning and services. Ecology Letters, 9 : 1146-1156, doi: 10.1111/j.1461-Q248.2006.00963.x. Baran, E., & Hambrey, J . 1998. Mangrove conservation and coastal management in Southeast Asia: what impact on fishery resources? Marine Pollution Bulletin 37: 431-440. Barnes, R. S. K. 1989. What, if anything, is a brackish water fauna? Transactions of the Royal Society of Edinburgh, Earth Sciences 80: 235-240. Barnes, R. S. K. 1994. The Brackish-water Fauna of NW Europe. Cambridge University Press, Cambridge. Barnes, D. K. A. 2002a. Biodiversity: invasions by marine life on plastic debris. Nature 416: 808-809.

Barnes, D. K. A. 2002b. Polarisation ofcompetition increases with latitude. Proceedings ofthe Royal Society ofLondon B 1504: 2061-2069. Barnes, D. K. A. 2003. Competition asymmetry with taxon divergence. Proceedings of the Royal Society of London B 270: 557-562. Barnes, D. K. A., & Brockington, S. 2003. Zoobenthic biodiversity, biomass and abundance at Adelaide Island, Antarctica. Marine Ecology Progress Series 249 : 145-155. Barnes, D. K. A., & Dick, M. H. 2000. Overgrowth competition between clades:Implications for interpretation ofthe fossil record and overgrowth indices. Biological Bulletin 199: 85-94. Barnes, D. K. A., & Fraser, K. P. P. 2003. Rafting by five phyla on man-made flotsam in the Southern Ocean. Marine Ecology Progress Series 262 : 289-291. Barnes, R. S. K., & Hughes, R. N. 1999. An Introduction to Marine Ecology. Blackwells Publishing. Oxford. Barnes, D. K. A., & Peck, L. S. 2008. VulnerabilityofAntarctic shelf biodiversity to predicted regional warming. Climate Research 37: 149-163. Barnes, D. K. A., Kaiser, S., Griffiths, H. J., & Linse, K. 2009) Marine, intertidal, freshwater and terrestrial biodiversity of an isolated polar archipelago. Journal ofBiogeography 36: 756-769. Barrow, C. J. 1997. Environmental and SocialImpact Assessment: an Introduction . Edward Arnold, London. Bathmann, U., Scharek, R., Klass, C., Dubischer, C. D., & Smetacek, V. 1997. Spring development ofphytoplankton biomass and composition in major water masses of the Atlantic sector of the Southern Ocean. Deep-Sea Research 44: 51-67. Baum, J . K., Myers, R. A., Kehler, D. G., Worm, B., Harley, S. J ., & Doherty, P. A. 2003. Collapse and conservation of shark populations in the northwest Atlantic. Science 299: 389-392. Beardsley, R. c., Epstein, A. W., Chen, C. S., Wishner, K. F., Macaulay, M. c., & Kenney, R. D. 1996. Spatial variability in zooplankton abundance near feeding right whales in the Great South Channel. Deep-Sea ResearchPartII- Topi-

cal Studies in Oceanography43: 1601-1625.

Beaugrand, G., Reid, P. C., Ibanez, F., Lindley, J . A., & Edwards, M. 2002. Reorganization of North Atlantic marine copepod biodiversity and climate. Science 296: 1692-1694. Beaugrand, G., Brander, K. M., Lindley, J. A., Souissi, S., & Reid, P. C. 2003. Plankton effect on cod recruitment in the North Sea. Nature 426: 661-664. Becagli, S., E. Castellano, O. Cerri, M. Curran, M. Frezzotti, F. Marino, A. Morganti, M. Proposito, M. Severi, R. Traversi and R. Udisti. 2009. Methanesulphonic acid (MSA) stratigraphy from a Talos Dome ice core as a tool in depicting sea ice changes and southern atmospheric circulation over the previous 140 years. Atmospheric Environment, 43 : 1051-1058. Behrenfeld, M. J., O'Malley, R. T., Siegel, D. A., McClain, C. R., Sarmiento, J . L., Feldman, G. C., Milligan, A. J ., Falkowski, P. G., Letelier, R. M., & Boss, E. S. 2006) . Climate-driven trends in contemporary ocean productivity. Nature 444: 752-755. Beja, 0., Avavind, L., Koonin, E. V., Suzuki, M. T., Hadd, A., Nguyen, C. et al. 2000. Bacterial rhodopsin: Evidence for a new type of phototrophy in the sea. Science 289: 1902-1906. Beja, 0 ., Spudich, E. N., Spudich, J . L., Leclerc, M., & DeLong E. F. 2001 . Proteorhodopsin phototrophy in the ocean. Nature 411 : 786-789. Beja, 0., Suzuki, M. T., Heidelberg, J . F., Nelson, W. C., Preston, C. M., Hamada, T. et aL 2002. Unsuspected diversity among marine aerobic anoxygenic phototrophs. Nature 415: 630-633. Bellwood, D. R., & Hughes, T. P. 2001. Regional-scale assembly rules and biodiversity of coral reefs. Science 292 : 1532-1534. Bellwood, D. R., Hughes, T. P., Falke, c., & Nystrom, C. 2004. Confronting the coral reef crisis. Nature 429: 827-833. Belt, S. T., Masse, G., Rowland, S. J ., Poulin, M., Michel, C. and LeBlanc, B. 2007 A novel chemical fossil of palaeo sea ice : IP25. Organic Geochemistry 38: 16-27. Belt, S. T., Masse, G., Yare, L. L., Rowland, S. J., Poulin, M., Siere, M. A. et aL 2008) Distinctive 13C isotopic signature distinguishes a novel sea ice biomarker in Arctic sediments and sediment traps. Marine Chemistry 112 : 158-167. Benfield, M. c., Davis, C. S., Wiebe, P. H., Gallager, S. M., Lough, R. G., & Copley, N. J . 1996. Video Plankton Recorder estimates of copepod, pteropod and larvacean distributions from a stratified region of Georges Bank with comparative measurements from a MOCNESS sampler. Deep-Sea Research Part II - Topical Studies in Ocean-

ography43: 1925-1945. Benfield, M. c., Grosjean, P., Culverhouse, P. F., Irigoien, X., Sieracki, M. E., Lopez-Urrutia, A. et al. 2007. RAPID. Research on automated plankton identification. Oceanography 20: 172-187.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Benner, R. 2002. Chemical composition and reactivity. In D. A. Hansell, & C. A. Carlson (eds), Biogeochemistry of Marine Dissolved Organic Matter . Academic Press, Amsterdam, pp. 59-90. Benoit-Bird, K. J . 2009) . Dynamic three-dimensional structure of thin zooplankton layers is impacted by foraging fish . Marine Ecology-Progress Series 396: 61-76. Bentamy, A' Grima, N., Quilfen, Y., Harscoat, V., Maroni, C., & Pouliquen, S. 1996. An Atlas ofSurface Windfrom ERS-l Scatterometer Measurements, lFREMER publication, pp. 229, lFREMER, DRO/OS, BP 70, 29280 Plouzane, France. Berge, J., Cottier, F., Last, K. S., Varpe, 0., Leu, E., Soreide, J. et al. 2009) . Diel vertical migration ofArctic zooplankton during the polar night. Biology Letters 5: 69-72. Berghahn, R. 1996. Episodic mass invasions of juvenile gadoids into the Wadden Sea and their consequences for the population dynamics ofthe brown shrimp (Crangon J

crangon). Marine Ecology 17: 251-260. Berman-Frank, I., Lundgren, P., Chen, Y-B., Kupper, H., Kolber, Z., Bergman, B., & Falkowski, P. 2001 . Segregation of nitrogen fixation and oxygenic photosynthesis in the marine cyanobacterium Trichodesmium. Science 294 : 1534-1537. Beukema, J . J . 2002. Expected change in the benthic fauan of Wadden sea tidal flats as a result of sea-level rise or bottom subsidence. Netherlands Journal of Sea Research 47: 25-39. Beukema, J ., & Cadee, G., 1986. Zoobenthos responses to eutrophication of the Dutch Wadden Sea. Ophelia 26 : 55-64. Bibby, C. J . 1998. Selecting areas for conservation. In W. J. Sutherland (ed.), Conservation Science and Action. Blackwell, Oxford, pp. 176-201. Bildstein, K. L. 1990. Status, conservation and management of the scarlet ibis Eudocimus rubber in the Caroni Swamp, Trinidad, West Indies. Biological Conservation 54: 61-78. Biles, C. L.. Solan. M.• Isaksson, I.. Paterson, D. M., Ernes, C., & Raffaelli, D. G. 2003. Flow modifies the effect of biodiversity on ecosystem functioning : an in situ study of estuarine sediments. Journal of Experimental Marine Biology and Ecology 285-6: 165-178. Billett, D. S. M., Lampitt, R. S., Rice, A. 1.., & Mantoura, R. F. C. 1983. Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature 302: 520-522. Billett, D. S. M., Bett, B. J ., Jacobs, C. 1.., Rouse, I. P., and Wigham, B. D. 2006. Mass deposition of jellyfish in the deep Arabian Sea. Limnology and Oceanograph 51: 2077-2083. Binder, B. J., Chisholm, S. W., Olson, R. J ., Frankel, S. 1.., & Worden, A. Z. 1996. Dynamics of picophytoplankton, ultraphytoplankton and bacteria in the central equatorial Pacific. Deep Sea Research (part 2) 43: 907-931.

Bingham, B. 1.., & Young, C. M. 1995. Stochastic events and dynamics of a mangrove root epifaunal community. PSZNI: Marine Ecology 16: 145-163. Birkeland, C. 1997. Life and Death on Coral Reefs. Chapman & Hall, New York. Bjern, P. A., Finstad, B., Kristoffersen, R., McKinley, R. S., & Rikardsen, A. H. 2007. Differences in risks and consequences of salmon louse. Lepeophtheirus salmonis (Kroyer), infestation on sympatric populations of Atlantic salmon. brown trout, and Arctic charr within northern fjords lCES Journal ofMarine Science 64: 386-393. Bjorndal, K. 1980. Nutrition and grazing behavior of the green turtle Chelonia mydas. Marine Biology 56: 147154. Black, E. A., & Truscott, J . 1994. Strategies for regulation of aquaculture site selection in coastal areas . Journal of AppliedIchthyology 10: 294-306. Blackman, F. F. 1905. Optima and limiting factors. Annals ofBotany 19: 281-295. Blain, S., Queguiner, B., Armand, 1.., Belviso, S., Bombled, B., Bopp, I.. et al. 2007. Effect of natural iron fertilization on carbon sequestration in the Southern Ocean. Nature 446: 1070-1075. Block, B. A., Teo, S. 1.., Walli, A., Boustany, A., Stokesbury, M. J . W., Farwell, C. J . et al. 2005. Electronic tagging and population structure ofAtlantic bluefin tuna. Nature 434: 1121-1127. Blome, D.• & Riemann, F. 1999. Antarctic sea ice nematodes, with description of Geomonhysteraglaciei sp. nov. (Monhysteridae) . Mitteilung des Hamburgischen Zoologischen Museum lnstituts 96: 15-20. Boenigk J ., & Arndt, H. 2002. Bacterivory by heterotrophic flagellates : Community structure and feeding strategies. Antoine van Leeuwenhoek 81 : 465-480. Bolam, S. G., Fernandes, T. F., & Huxham, M. 2002 Diversity. biomass and ecosystem processes in the marine benthos. Ecological Monographs 72 : 599-615. Bologna, P. A. X., & Heck, K. I.. 1999. Differential predation and growth rates of bay scallops within a seagrass habitat. Journal ofExperimental Marine Biology and Ecology 239: 299-314. Borg, J . A., Rowden, A. A., Attrill, M. J ., Schembri, P. J ., & Jones, M. B. 2006. Wanted dead or alive: high diversity of macroinvertebrates associated with living and 'dead' Posidonia oceanica seagrass matte . Marine Biology 149 : 667-677. Borg, J . A., Attrill, M. J ., Rowden, A. A., Schembri, P. J ., & Jones. M. B. 2005. Architectural characteristics of two bed types of the seagrass Posidonia oceanica over different spatial scales. Estuarine Coastal and Shelf Science 62 : 667-678. Borja, A., & Dauer, D. M. 2008. Assessing the environmental quality status in estuarine and coastal systems: comparing methodologies and indices . Ecological Indicators 8: 331-337.

References Borja, A., Franco, J ., & Perez, V. 2000. A marine biotic index to establish the ecological quality ofsoft-bottom benthos within European estuarine and coastal environments. Marine Pollution Bulletin 40: 1100-1114. Born, E. W., Wiigc, 0 ., & Thomassen, J. 1997. Seasonal and annual movements of radio-collared polar bears (Ursus maritimus) in northeast Greenland. Journal of Marine

Systems 10: 67-77. Boschi, E. E. 2000. Species of decapod crustaceans and their distributions in the American marine zoogeographic provinces. Revista de Investigacion y Desarrollo Pesquero 13: 1-136. Bowden, D. A., Rowden, A. A., & Attrill, M. J . 2001. Effect of patch size and in-patch location on the infaunal macro-

invertebrate community of Zostera marina seagrass beds. Journal of Experimental Marine Biology and Ecology 259: 133-154. Bowler, c., Karl, D. M., & Colwell, R. R. 2009. Microbial oceanography in the sea of opportunity. Nature 459 : 180-184. Boyd, P. W., and 22 others. 2007. Mesoscale iron enrichment experiments 1993-2005: Synthesis and future directions. Science 315 : 612-617. Boyd, P. W., Jickells, T., Law, C. S., Blain, S., Boyle, E. A., Buesseler, K. O. et a1. 2007. Mesoscale iron enrichment experiments 1993-2005: Synthesis and future directions. Science 315: 612-617. Boyd, P. W., Strzepek, R., Feixue, F., & Hutchins, D. A. 2010. Environmental control 0 open-ocean phytoplankton groups: now and in the future. Limnology and oceanography 55: 1353-1376. Boyd, P. W., Watson, A. J ., Law, C. S., Abraham, E. R., Trull, T., Murdoch, R. et al. 2000. A mesoscale phytoplankton bloom in the polar Southern Ocean stimulated by iron

fertilization. Nature 407: 695-702. Branch, G. M., & Pringle, A. 1987. The impact of the sand prawn Callianassa kraussi Stebbing on sediment turnover and on bacteria, meiofauna and benthic microfauna. Journal of Experimental Marine Biology and Ecology 107: 219-235. Branch, G. M., & Steffani, C. N. 2004. Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck) .

Journal ofExperimentalMarine Biology and Ecology 300: 189-215. Brandt, A., De Broyer, C., Gooday, A. J ., Hilbig, B., & Thomson, M. R. A. 2004. Introduction to ANDEEP (ANtarctic benthic DEEP-sea biodiversity: colonization history

and recent community patterns) . A tribute to Howard L. Sanders. Deep-Sea Reserach Part II, 51 : 1457-1465 . Brandt, A., Gooday, A. J., Brandao, S. N., Brix, S., Brokeland, W., Cedhagen, T. et aL 2007 First insights into the biodiversity and biogeography of the Southern Ocean deep sea. Nature 447,307-311. Breitbart, M., Middleboe, M., & Rohwer F., 2008. Marine

viruses: community dynamics, diversity and impact on

microbial processes. In D. L. Kirchman (ed) Microbial Ecology of the Oceans, 2nd edn. John Wiley & sons Inc. New York, pp. 443-480. Brentnall, S. J., Richards, K. J ., Brindley, J ., & Murphy, E. 2003. Plankton patchiness and its effect on larger-scale productivity. Journal ofPlankton Research 25 : 121-40. Brey, T. 1998. Growth performance and mortality in aquatic macrobenthic invertebrates. Advances in Marine Biology

35: 153-243. Brey, T., 2008. Population dynamics in benthic invertebrates. A virtual handbook. Version 01.2. http:/ /www. thomas-brey.de/science/virtualhandbooklnavlog/ index.htm!. Alfred Wegener Institute for Polar and Marine Research. Germany. Brey, T., & Gerdes, D. 1997. Is Antarctic benthic biomass

really higher than elsewhere? Antarctic Science 9 : 266267. Bricaud, A., Morel, A., & Barale, V. 1999. MERlS potential for ocean colour studies in the open ocean. International Journal of Remote Sensing 20: 1757-1769. Brierley, A. S. 2007. Fisheries ecology: hunger for shark fin soup drives clam chowder off the menu. Current Biology 17: R555-R557. Brierley, A. S., & Thomas, D. N. 2002. Ecology of Southern Ocean pack ice. Advances in Marine Biology 43: 171-276. Brierley, A. S., & Kingsford, M. J . 2009. Impacts of climate change on marine organisms and ecosystems. Current Biology 19: R602-R614. Brierley, A. S., Ward, P., Watkins, J . L., & Goss, C. 1998. Acoustic discrimination of Southern Ocean zooplank-

ton. Deep-Sea Research Part II - Topical Studies in Ocean-

ography45: 1155-1173. Brierley, A. S., Fernandes, P. G., Brandon, M. A., Armstromg, F., Millard, N. W., McPhail, S. D. et aL 2002. Antarctic krill under sea ice: elevated abundance in a narrow band just south of ice edge. Science 295: 1890-1892. Briggs, J. C. 2003. Marine centres of origin as evolutionary engines. Journal ofBiogeography 30: 1-18. Brodie, P. F., Sameoto, D. D., and Sheldon, R. W. 1978. Population-densities of euphausiids off Nova-scotia as indicated by net samples, whale stomach contents. and sonar-comment. Limnology and Oceanograph 23 :

1264-1267. Broecker, W. S. 1997. Thermohaline circulation, the Achilles heel ofour climate system: Will man-made CO, upset the current balance? Science 278: 1582-1588. Broecker, W. S., Sutherland, S., & Peng, T. H. 1999. A possible 20th-century slowdown of Southern Ocean deepwater formation. Science 286: 1132-1135. Browman, H. L., & Stergiou, K. I. (eds) 2005 Politics and socia-economics of ecosystem-based management of marine resources. Marine Ecology Progress Series 300 :

1-73.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Browman, H. I., Vezina, A. F., & Hoegh-Guldberg, 0 . 2008. Effects of ocean acidification on marine ecosystems. Theme Section, Marine Ecology Progress Series 373 : 109-309. Brown, J . 1995. Macroecology. University of Chicago Press, Chicago. Brown, C., & Laland, K. N. 2001. Suboski and Templeton revisited: Social learning and life skills training for hatchery reared fish. Journal of Fish Biology 59 : 471493. Brown, A. C., & McLachlan, A. 1990. Ecology of Sandy Shores . Elsevier, Amsterdam. Brown, A. C., & McLachlan, A. 2002. Sandy shore ecosystems and the threats facing them: some predictions for the year 2025. Environmental Conservation 29: 62-77. Brown, M. V., Schwalbach M. S., Hewson, I., & Fuhrman, J . A. 2005. Coupling 16S-ITS rDNA clone libraries and ARISA to show marine microbial diversity:Development and application to a time series. Environmental Microbiology 7: 1466-1479. Brownlee, c., & Taylor, A. R. 2002. Algal calcification and silification. In Encyclopedia of Life Sciences. Macmillan Publishers Ltd, Nature Publishing Group. http:/ /www. els.net. Bryant, A' Heath, M., Broekhuizen, N., Ollason, J., Gurney, W., & Greenstreet, S. 1995. Modeling the predation, growth and population dynamics of fish within a spatially resolved shelf sea ecosystem model. Netherlands Journal ofSea Research 33 : 407-421 . Buesseler, K. 0 ., Andrews, J. E., Pike, S. M., & Charette, M. A. 2004. The effects of iron fertilization on carbon sequestration in the Southern Ocean. Science 304: 41441 7. Bulling, M. T., White, P. C. L. W., Raffaelli, D. G., & Pierce, G. J . 2006. Using model systems to address the biodiversity-ecosystem functioning process. Marine Ecology Progress Series 311 : 295-309. Burna, A. G. J ., de Boer, M. K., & Baeten, P. 2001. Depth distributions of DNA damage in Antarctic marine phytoand bacterioplankton exposed to summertime ultraviolet radiation. Journal ofPhyeology 37: 200-208. Burke, W. T. 1994. The New International Law of Fisheries: UNCLOS 1982 and Beyond. Clarendon Press, Oxford. Burkhardt, S., & Riebesell, U. 1997. CO, availability affects elemental composition (C: N : P) of the marine diatom Skeletonema costatum. Marine Ecology Progress Series 155: 67-76. Burkhardt, S., Riebesell, U., & Zondervan, I. 1999a. Stable carbon isotope fractionation by marine phytoplankton in response to daylength, growth rate, and CO, availability. Marine Ecology Progress Series 184: 31-41. Burkhardt, S., Riebesell, U., & Zondervan, I. 1999b. Effects of growth rate. CO 2 concentration, and cell size on the stable carbon isotope fractionation in marine phytoJ

plankton. Geochemica et Cosmochima Acta 63 : 37293741 . Burkhardt, S., Amoroso, G., Riebesell, U., & Sultemeyer, D. 2001. CO, and HC03 uptake in marine diatoms acclimated to different CO 2 concentrations. Limnology and

Oceanography46: 1378-1391. Caddy, J . 1998. A short review of precautionary reference points and some proposals for their use in data-poor situations. FAO Fisheries Technical Paper 379: 30 pp. Cadee, G. c., Gozalez, H., & Schnack-Schiel, S. B. 1992. Krill diet affects faecal string settling. Polar Biology 12: 75-80. Caldeira, K., & Wickett, M. E. 2003. Anthropogenic carbon and ocean pH . Nature 425: 365. Caldeira, K., & Wickett, M. E. 2005. Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. Journal of Geophysical Research (Oceans) 110: C09S04, doi : 10.1029/2004JC002671. Caley, M. J ., & Schluter, D. 1997. The relationship between local and regional diversity. Ecology 78 : 70-80. Carling P. A. et al. 2006. The morphodynamics and internal structure of intertidal fine-gravel dunes: Hills Flats, Severn Estuary, UK. Sedimentary Geology 183: 159-179. Carlon D. B. 1999. The evolution of mating systems in tropical corals. Trends in Ecology and Evolution 14: 491-495. Caron. D. A., Worden. A. Z., Counrway, P. D., Demir. E, & Heidelberg, K. B. 2009. Protists are microbes too: a perspective. ISMEJournaI3 :4-12. Carr, M. E., & Kearns, E. J . 2003. Production regimes in four Eastern Boundary Current systems. Deep-Sea Research Part II- Topical Studies in Oceanography 50: 3199-3221. Cary, S. c., Shank, T., & Stein, J . 1998. Worms bask in extreme temperatures. Nature 391 : 545-546. Caswell, H., Fujiwara, M., & Brault, S. 1999. Declining survival probability threatens North Atlantic right whale.

Proceedings of the National Academy of Sciences 96 : 3308-3313. Cavicchioloi, R. 2002 . Extremophiles and the search for extraterrestrial life. Astrobiology 2 : 281-292. Cavicchioli, R., Siddiqui, K. S., Andrews, D., & Sowers, K. R. 2002. Low-temperature extremophiles and their applications. Current Opinion in Biotechnology 13: 253-261 . Chamberlain, G. 1997. Sustainabilityofworld shrimp farming. In E. L. Pikitch, D. D. Huppert, & M. P. Sissenwine (eds), Global Trends: Fisheries Management, American Fisheries Society Symposium, Bethesda, Maryland, pp. 195-212. Chan, T. U., & Hamilton, D. P. 2001. The effect offreshwater flow on the succession and biomass of phytoplankton in a seasonal estuary. Marine and Freshwater Research 52 : 869-884. Chang, C. W., lizuka, Y., & Tzeng, W. N. 2004. Migratory environmental history of the grey mullet Mugil cepha-

References Ius as revealed by otolith Sr: Ca ratios. Marine EcologyProgress Series 269 : 277-288. Chapelle, G., & Peck, L. S. 1999. Polar gigantism dictated by oxygen availability. Nature 399 : 114-115. Chapelle, G., & Peck, L. S. 2004. Amphipod crustacean size spectra: new insights in the relationship between size and oxygen. Oikos 106: 167-175. Chapman, P. M., & Brinkhurst, R. O. 1981 . Seasonal changes in the interstitial salinities and seasonal movements of subtidal benthic invertebrates in the Fraser River estuary, B. C. Estuarine Coastal Shelf Science 12: 49-66. Charlier, R., & Charlier, C. 1992. Environmental, economic and social aspects of marine aggregates' exploitation. Environmental Conservation 19: 29-37. Charrassin, J. B., Hindell, M., Rintoul, S. R., Roquet, F., Sokolov, S., Biuw, M. et al. 2008. Southern Ocean frontal structure and sea-ice formation rates revealed by elephant seals. Proceedings of the National Academy of Sciences USA 105: 11634-11639. Chavez, F. P., Ryan, J ., Lluch-Cota, S. E., & Niquen, M. 2003. From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science 299 : 217-221. Chisholm S. W. 2001. Stirring times in the Southern Ocean. Nature 407: 685-687. Chisholm, S. W., Falkowski, P. G., & Cullen, J . J . 2001. Discrediting ocean fertilization . Science 294: 309-310. Choi, J . S., Frank, K. T., Leggett, W. C., & Drinkwater, K. 2004. Transition to an alternate state in a continental shelf ecosystem. Canadian Journal of Fisheries and Aquatic Science 61 : 505-510. Christi, Y. 2008. Response to Reijnders: Do bifuels from

microalgae beat biofuels from terrestrial plants? Trends in Biotechnology 26: 351-352. Church M. J . 2008. Resource control of bacterial dynamics in the sea. In D. L. Kirchman (ed) Microbial Ecology of the Oceans, 2nd edn. John Wiley & sons Inc. New York, pp.335-382. Chyba, F. F., & Phillips, C. B. 2002. Europa as an abode of life . Origins of Life and Evolution of the Biosphere 32 : 47-68. Clarke, A. 1992. Is there a latitudinal diversity cline in the sea? Trends in Ecology and Evolution 7: 286-287. Clarke, A., Crame, A. J, Stromberg, J . 0 ., & Barker, P. F. 1992. The Southern Ocean Benthic Fauna and Climate Change : A Historical Perspective [and Discussion] . Phil. Trans R Soc. Lond. B 338: 299-309. Clarke, A. C., & P. A. Tyler. 2008. Adult Antarctic krill feeding at abyssal depths. Current Biology 18: 282-285. Clarke, K., & Warwick, R. 1994. Change in Marine Com-

munities: An Approach to Statistical Analysis and Interpretation . Natural Environmental Research Council, Plymouth Marine Laboratory, Plymouth. Clark, P. U., Pisias, N. G., Stocker, T. F., & Weaver, A. J . 2002. The role of the thermohaline circulation in abrupt eli-

mate change. Nature 415 : 863-869. Clarke, A., Murphy, E. J ., Meredith, M. P., King, J . c., Peck, L. S., Barnes, D. K. A., & Smith, R. C. 2007. Climate

change and the marine ecosystem of the western Antarctic Peninsula. Philosophical Transactions of the Royal Society B 362 : 149-166. Clarke, A. c., Meredith, M. P., Wallace, M. I., Brandon, M., & Thomas, D. N. 2008. Seasonal and interannual vari-

ability in temperature, chlorophyll and macronutrients

in Ryder Bay. northern Marguerite Bay, Antarctica. Deep Sea Research PartII 55 : 1988-2006. Cliff, G. 1991. Shark Attacks on the South-African Coast between 1960 and 1990. South African Journal of Science 87: 513-518. Cloern, J . E., & Jassby, A. D. 2008. Complex seasonal pat-

terns of primary producers at the land-sea interface. Ecology Letters 11 : 1294-1303. Coale. K. H .• Johnson, K. S., Chavez. F. P.• Buesseler, K. 0., Barber, R. T., Brzezinski, M. A. et al. 2004. Southern

Ocean iron enrichment experiment: carbon cycling in high- and low-Si Waters. Science 304: 408-414. Cockell, c., Corfield, R., Edwards, N., & Harris, N. 2007.An Introduction to the Earth-Life System . Cambridge University Press. Cambridge. Coggan, R.• Populus. J.• J., W.• Sheehan, K., F.• F., & Pile, S. 2007. Review of standards and protocols for seabed habitat mapping. MESH www.searchrnesh.net/, 1-203. Cohen, J . E., Pimm, S. L., Yodzis, P., & Saldana, J . 1993.

Body sizes of animal predators and animal prey in food webs. Journal ofAnimal Ecology 62: 67-78. Coles, S. L., & Brown, B. E. 2003. Coral bleaching - capacity for acclimatization and adaptation. Advances in Marine Biology 46: 183-223. Collie, J . S., Hall, S. J ., Kaiser, M. J ., & Poiner, I. R. 2000.

A quantitative analysis of fishing impacts on shelf-sea benthos. Journal ofAnimal Ecology 69: 785-799. Colman, J . S. 1933. The nature of intertidal zonation of plants and animals. Journal ofthe Manne BiologicalAssociation ofthe United Kingdom 61 : 71-93. Comiso, J . C. 2002. A rapidly declining Arctic peren-

nial ice cover. Geophysical Research Letters 29, doi : 10.1029/2002GL015650. Comiso, J. C. 2003b. Large-scale characteristics and variability of the global sea ice cover. In D. N. Thomas, & G. S. Dieckmann (eds), Sea Ice-An Introduction to its Physics, Chemistry, Biology and Geology. Blackwells Publishing. Oxford. Comiso, J. C. 2010. Variability and trends in sea ice cover. In: Sea Ice, 2nd edn (eds DNThomas, & GS Dieckmann) . Wiley-Blackwell Publishing. Oxford, pp. 205-246. Connell, J . H. 1961a. The influence of inter-specific com-

petition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42: 710-723. Connell, J . H. 1961b. Effects of competition, predation by

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Thais lapillus and other factors on natural populations of the barnacle Balanus balanoides. Ecological Monographs 31 : 61-104. Connell, J . H. 1978. Diversity in tropical rain forests and coral reefs. Science 199: 1302-1310. Connolly, R. M. 1997. Differences in composition of small, motile invertebrate assemblages from seagrass and unvegetated habitats in a southern Australian estuary. Hydrobiologia 346: 137-148. Constable, A. J ., & Nicol, S. 2002. Defining smaller-scale management units to further develop the ecosystem approach in managing large-scale pelagic krill fisheries in Antarctica. CCAMLRScience 9 : 117-131. Convey, P., Barnes, D. K. A., & Morton, A. 2002. Debris accumulation on oceanic island shores ofthe Scotia Arc. Antarctica. Polar Biology 25: 612-617. Cook, A. J ., FoxA. J ., Vaughan, D. G., & Ferrigno, J . G. 2005. Retreating glacier fronts on the Antarctic Peninsula over the past half-century. Science 308: 541-544. Cooper, D. J ., Watson, A. J ., & Ling, R. D. 1998. Variation of PCO, along a North Atlantic shipping route (UK to Caribbean) : a year of automated observations. Marine Chemistry 60: 147-164. Costanza, R' d'Arge, R' de Groot. R., Farber. S., Grasso, M.• Hannon, B. et aL 1997. The value of the world's ecosystem services and natural capital. Nature 387: 253-260. Costello, M., Deady, S., Pike, A., & Fives, J., 1994. Parasites and diseases ofwrasse (Labridae) being used as cleanerfish on salmon farms in Ireland and Scotland.lnM. D. J . Sayer, J. W. Treasurer, & M. J . Costello (eds), WrasseBiology and Use in Aquaculture, Fishing News Books. Oxford, pp. 211-227. Cotte, C., & Guinet, C. 2007. Historical whaling records reveal major regional retreat of Antarctic sea ice. Deep Sea Research Part I, 54: 243-252. Cottier, F. R., Tarling, G. A., Wold, A., & Falk-Petersen, S. 2006. Unsynchronized and synchronized vertical migration of zooplankton in a high arctic fjord. Limnology and Oceanography 51 : 2586-2599. Cottrell M. T., & D. L. Kirchman 2000. Natural assemblages of marine Proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and highmolecular-weight dissolved organic matter. Appliedand Environmental Microbiology 66: 1692-1697. Coutant, C. C. 1990. Temperature-oxygen habitat for freshwater and coastal striped bass in a changing climate. Transactions oftheAmerican Fisheries Society 119 : 240-253. Cox, M. J., Derner. D. A.• Warren. J. D.• Cutter. G. R.. & Brierley, A. S. 2009. Multibeam echosounder observations reveal interactions between Antarctic krill and airbreathing predators. Marine Ecology Progress Series 378: 199-209. Crame, J. A. 1999. An evolutionary perspective on marine J

J

faunal connections between southernmost South America and Antarctica. SdentiaManna 63 : 1-14. Crame, J. A. 2000. Evolution of taxonomic gradients in the marine realm: evidence from the composition of recent bivalve faunas . Paleobiology 26: 188-214. Cranfield, H.J., Michael, H. J., & Doonan, I. J .1999. Changes in the distribution of epifaunal reefs and oysters during 130 years of dredging for oysters in Foveaux Strait, southern New Zealand. Aquatic Conservation: Marine and Freshwater Ecosystems 9: 461-483. Cranfield, H. J., Rowden, A. A., Smith, D. J., Gordon, D. P., & Michael, K. P. 2004. Macrofaunal assemblages of benthic habitat of different complexity and the proposition of a model of biogenic reef habitat regeneration in Foveaux Strait, New Zealand. Journal ofSea Research 52: 109-126. Creutzberg, F. 1984. A persistent chlorophyll a maximum coinciding with an enriched benthic zone. In P. E. Gibbs (ed.), Proceedings oftheNineteenth European Marine Biology Symposium, Cambridge University Press, Cambridge, pp.97-108. Croll, D. A., Clark, C. W., Calambokidis, J., Ellison, W. T., & Tershy, B. R. 2001. Effect ofanthropogenic low-frequency noise on the foraging ecology of Balaenoptera whales. Animal Conservation 4: 13-27. Cullen, J. J ., & Boyd, P. W. 2008. Predicting and verifying the intended and unintended consequences oflarge-scale ocean iron fertilization. Marine Ecology Progress Series 364: 295-301. Cullen, J . J ., Doolittle, W. F., Levin, S. A., & Li, W. K. W. 2007. In situ instrumentation. Oceanography 20: 34-46. (http:/ /www.tos .org/oceanography/ issu e s/issu e_ archive/issue_pdfs/20_2/20.2_cullen_et_al.pdf) . Curran, M. A. J ., van Ommen, T. D., Morgan, V. I., Phillips, K. L., & Palmer, A. S. 2003.lce core evidence for Antarctic sea ice decline since the 1950s. Science 302 : 1203-1206. Curtis, T. P., Sloan W. T., & Scannell J . W. 2002. Estimating prokaryotic diversity and its limits. Proceedings ofthe NationalAcademyofSciences USA 99: 10494-10499. Cury, P.• Bakun, A.• Crawford. R. J. M., Jarre, A., Quinones. R. A., Shannon, L. J ., & Verheye, H. M. 2000. Small pelagics in upwelling systems: patterns ofinteraction and structural changes in 'wasp-waist' ecosystems. ICES Journal of Marine Science 57: 603-618. Cushing, D. H., 1969. Upwelling and the production offish. Advances in Marine Biology 9: 255-334. Cushing, D. H. 1975. Marine Ecology and Fisheries. Cambridge University Press, Cambridge. Cushing, D. H. 1988. The Provident Sea . Cambridge University Press, Cambridge. Cushing, D. H. 1990. Plankton production and year-class strength in fish populations - an update of the match mismatch hypothesis. Advances in Marine Biology 26: 249-293.

References Cusson, M., & Bourget, E., 2005. Global patterns of macroinvertebrate production in marine benthic habitats. Marine Ecology Progress Series 295 : 1-14. Dahl, E. 1952. Some aspects ofthe ecology and zonation of the fauna on sandy beaches. Oikos 4 : 1-27. Dahle, L. A. 1995. Off-shore fish farming systems. INFOFISH-

Intemational2 : 24-30. Dalzell, P., Adams, T. J . H., & Polunin, N. V. C. 1996. Coastal fisheries in the Pacific Islands. Oceanography and Marine Biology: Annual Review 34: 395-531 . Danielsen. F., Serensen, M. K., Olwig, M. F.. Selvam, V., Parish, F., Neil, D. et al. 2005. The Asian tsunami: a protective role for coastal vegetation. Science 310: 643. Davidson, A. T., & van der Heijden, A. 2000. Exposure of

natural Antarctic marine microbial assemblages to ambient UV radiation: effects on bacterioplankton. Aquatic

Microbial Ecology 21 : 257-264. Davoren, G. K., Montevecchi, W. A., & Anderson, J . T. 2003.

del Giorgio, P. A., & Williams, P. J . Ie B. (eds) 2005 . Res-

piration in Aquatic Ecosystems . Oxford University Press. Oxford. del Giorgio, P. A., & Williams, P. J . le B. 2005. The global

significance of respiration in aquatic ecosystems: from single cells to the biosphere. In P. A. del Giorgio & P. J. Ie B. Williams (eds) Respiration in Aquatic Ecosystems. Oxford University Press, Oxford. pp. 267-300. DeLong, E. F. 2009. The microbial ocean from genomes to biomes. Nature 459: 200-206. Deming, J . W. 2002. Psychrophiles and polar regions. Current Opinion in Microbiology 5 : 301-309. Dernie, K. M., Kaiser, M. J ., & Warwick, R. M. 2003. Recov-

ery rates of benthic communities following physical disturbance. Journal ofAnimal Ecology 72: 1043-1056. Derocher, A. E., Lunn, N. J ., & Stirling, I. 2004. Polar bears in a warming climate. Integrative and Comparative Biol-

ogy44: 163-176.

Search strategies of a pursuit-diving marine bird and the

Diaz, R. J ., & Rosenberg, R., 2008. Spreading Dead Zones

persistence of prey patches. Ecological Monographs 73: 463-48l. Dayton, P. K. 1985. Ecology of kelp communities. Annual Review ofEcology and Systematics 16: 215-245. Dayton, P. K. 1994. Community landscape: scale and stability in hard bottom marine communities. In P. Giller, A. Hildrew, & D. Raffaelli (eds), AquaticEcology: Scale, Pattern and Process, Blackwell Scientific Publications. Oxford, pp. 289-332. de Baar, H. J. W., de Jong, J. T. M., Bakker, D. C. E., Loscher, B. M., Veth, c., Bathmann, U., & Smetacek, V. 1995. Importance of iron for plankton blooms and carbon dioxide drawdown in the Southern Ocean. Nature 373: 412-415. de Beer. D. 2000. Potentiometric microsensors for in situ measurements in aquatic environments. In J. Buffle, & G. Horvai (eds), In situ Monitoring ofAquatic Systems: Chemical Analysis and Speciation. Wiley, & Sons, London, pp.161-94. De Forges, B. R., Koslow, J . A., & Poore, G. C. B. 2000. Diver-

and Consequences for Marine Ecosystems. Science 321 : 926-929. Dickey, T. D., Itsweire, E. C., Moline, M. A., & Perry, M. J. 2008. Introduction to the Limnology and Oceanography

Special Issue on Autonomous and Lagrangian Platforms and Sensors (ALPS) . Limnology and Oceanography 53: 2057-206l. Diehl, S. 2002. Phytoplankton, light, and nutrients in a gradient of mixing depths: Theory. Ecology 83 : 386-398. Distel, D. L., & Roberts, S. J . 1997. Bacterial endosymbionts in the gills of the deep-sea wood-boring bivalves

Xylophaga atlantica andXylophaga washingtona. Biological Bulletin 192: 253-26l. Distel, D. L., Baco, A. R., Chuang, E., Morrill, W., Cavanaugh, C. M., & Smith, C. R. 2000. Do mussels take wooden steps to deep-sea vents? Nature 403 : 725-726. Dittmar, T., & Kattner, G. 2003. The biogeochemistry of the

river and shelf ecosystem of the Arctic Ocean: a review.

Marine Chemistry 83 : 103-120.

sity and endemism of the benthic seamount fauna in the

Dixon. D.• Mayewski, P. A., Kaspari, S.• Kreutz, K., Ham-

southwest Pacific. Nature 405: 944-947. de la Mare, W. K. 1997. Abrupt mid-twentieth-century

ilton, G., Maasch. K, et at. 2005. A 200 year sulfate

decline in Antarctic sea-ice extent from whaling records.

Nature 389 : 57-59.

record from 16 Antarctic ice cores and associations with Southern Ocean sea-ice extent. Annals of Glaciology 41 :

De Vias, J ., 1979. Annual food intake by Plaice and Flounder in a tidal flat area in the Dutch Wadden Sea, with special

155-166. Doherty, P. J . 2002. Variable replenishment and the dynamics of reef fish populations. In P. F. Sale (ed.), Coral Reef

reference to consumption of regenerating parts. Nether-

Fishes: Dynamics and Diversity in a Complex Ecosystem .

lands Joumal ofSea Research 13: 117-153. Deegan, L. A., & Garritt, R. H. 1997. Evidence for spatial variability in estuarine food webs. Marine Ecology Progress Series 147: 31-47. del Giorgio P. A., & Gasol J . M. 2008. Physiological structure and single-cell activity in marine bacterioplankton. In D. L. Kirchman (ed) Microbial ecology of the oceans, 2nd edn. John Wiley & sons Inc. New York pp. 243-298.

Academic Press, Amsterdam, pp. 327-355. Dolan, J . R., & Perez, M. T. 2000. Costs, benefits and charac-

teristics ofmixotrophy in marine oligotrichs. Freshwater

Biology 45: 227-38. Doney, S. C., Fabry, V. J., Feely, R. A., & Kleypas, J . A. 2009. Ocean acidification: the other C02 problem. Annual Review ofMarine Science 1 : 169-192. Dore, J . E., Lukas, R., Sadler, D., Church, M., & Karl, D.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

M. 2009. Physical and biogeochemical modulation of ocean acidification in the central North Pacific. PNAS 106: 12235-12240. Doty, M. S. 1946. Critical tidal factors that are correlated with the vertical distribution of marine algae and other organisms along the Pacific coast. Ecology 27: 315-328. Drake, J . M., Baggenstos, P., & Lodge, D. M. 2005. Propagule pressure and persistence in experimental populations. Biology Letters 1: 480-483. Dring, M. J., & Brown, F. A. 1982. Photosynthesis of intertidal brown algae during and after periods of emersion; a renewed search for physiological causes of zonation. Marine Ecology Progress Series 8: 301-308. Duarte, C. M. 1991. Allometric scaling of seagrass form and productivity. Marine Ecology Progress Series 77: 289-300. Duarte, C. M. 2000. Marine biodiversity and ecosystem services:an elusive link. Journal ofExperimental Marine Biology and Ecology 250: 117-132. Duarte, C. M. 2001. Seagrass Ecosystems. In S. L. Levin (ed.), Encyclopedia of Biodiversity, Vol. 5. Academic Press, pp. 255-268. Duarte, C. M. 2002. The future of seagrass meadows. Environmental Conservation 29: 192-206. Duarte, C. M., Chiscano, C. L. 1999. Seagrass biomass and production: a reassessment.AquaticBotany65: 159-174. Ducklow, H. 2000. Bacterial Production and Biomass in the Oceans. In D. L. Kirchman (ed.), Microbial Ecology ofthe Oceans. John Wiley & Sons, Inc. New York, pp. 85-120. Dulvy, N. K., & Reynolds, J . D. 1997. Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proceedings oftheRoyal Society ofLondon B 264: 1309-15. Dulvy, N. K., Sadovy, Y., & Reynolds, J . D. 2003. Extinction vulnerability in marine populations. Fish and Fisheries 4: 25-64. Durako, M., Zieman, J ., & Robblee, M. 2003. Seagrass ecology. In W. Nuttle, J. Hunt, & M. Robblee (eds), A Synthesis ofResearch on Florida Bay, Florida Bay Science Programme/US Geological Survey, pp. 7.1-7.36. Durazo, R., Harrison, N. M., & Hill, A. E. 1998. Seabird observations at a tidal mixing front in the Irish Sea. Estuarine Coastal and ShelfScience 47: 153-164. Durham, W. M., Kessler, J . 0 ., & Stocker, R. 2009. Disruption of Vertical Motility by Shear Triggers Formation of Thin Phytoplankton Layers. Science 323: 1067-1070. Dyer, K. R. 1997. Estuaries: a Physical Introduction . John Wiley, New York. Dyhrman, S. T., Chappell, P. D., Haley, S. T., Moffett, J . W., Orchard, E. D., Waterbury, J. B., & Webb, E. A. 2007. Phosphonate utilization by the globally important marine diazotroph Trichodesmium . Nature 439: 68-71. Eadie, B. J., McKee, B. A., Lansing, M. B., Robbins, J. A., Metz, S., & Trefry, J . H. 1994. Records of nutrient-

enhanced coastal ocean productivity in sediments from the Louisiana continental shelf. Estuaries 17: 754-765. Easttnan, J . T. 2000. Antarctic notothenioid fishes as subjects for research in evolutionary biology. Antarctic Science 12: 276-287. Edgar, G. J. 1999. Experimental analysis of structural versus trophic importance of seagrass beds. I. Effects on macrofaunal and meiofaunal invertebrates. Vie Melieu 49: 239-248. Edgar, G. J ., & Robertson, A.1. 1992. The influence of seagrass structure on the distribution and abundance of

mobile epifauna: pattern and process in a western AustralianAmphipholis bed. Journal ofExperimental Marine Biology and Ecology 160: 13-31. Edgar, G. J., Barrett, N. S., Graddon, D. J ., & Last, P. R. 2000. The conservation significance of estuaries: a classification of Tasmanian estuaries using ecological, physical and demographic attributes as a case study, Biological Conservation 92: 383-397. Edwards, M., Beaugrand, G., John, A. W. G., Johns, D. G., Licandro, P., McQuatters-Gollop, A., & Reid, P. C. 2009. Ecological Status Report: results from the CPR survey 2007/2008. SAHFOS Technical Report 6 : 1-12. Plymouth, U.K. Eiane, K., Aksnes, D. L., Bagoien, E., & Kaartvedt, S. 1999. Fish or jellies - a question of visibility? Limnology and

Oceanography44: 1352-1357. Eicken, H. 1992. The role of sea ice in structuring Antarctic ecosystems. Polar Biology 12: 3-13. Eilers, H., Pemthaler J ., & Amann, R. 2000. Succession of pelagic marine bacteria duringenrichment:Aclose look at cultivation-induced shifts. Appliedand Environmental Microbiology 66: 4634-4640. Eklofa, J . S., de la Torre-Castroa, M., Gullstr6mb, M., Ukuc, J., Muthigad, N., Lyimoe, T., & Bandeira, S. O. 2008. Sea urchin overgrazing of seagrasses: a review of current knowledge on causes, consequences, and management. Estuarine Coastal and ShelfScience 74: 569-580. Elahimanesh, P. 2001 . Sturgeon in Iran. Fisheries 26: 41-44. Ellingsen, H., & Aanondsen, S. A. 2006 Environmental impacts of wild caught cod and fanned salmon - a comparison with chicken. InternationalJournal ofLife cycle Analysis 1: 60-65. Ellison, A. M., Farnsworth, E. J ., & Merkt, R. E. 1999. Origins of mangrove ecosystems and the mangrove biodiversity anomaly. Global Ecology, & Biogeography 8: 95-115. Elzenga, J . T., Prins, H. B. A., & Stefels, J . 2000. The role of extracellular carbonic anhydrase activity in inorganic carbon utilization ofPhaeocystisglobosa (Prymnesiophyceae) : A comparison with other marine algae using the isotopic disequilibrium technique. Limnologyand Ocean-

ography45 : 372-80. Emerson, C. W. 1989. Wind Stress Limitation of Benthic

References Secondary Production in Shallow, Soft-Sediment Communities. Marine Ecology Progress Series 53: 65-77. Emmerson, M. C., Solan, M., Emes,

c., Paterson,

D. M., &

Raffaelli, D. G. 2001. Consistent patterns and the idiosyncratic effects of biodiversity in marine ecosystems. Nature 411 : 73-77. Estes, J. A., & Duggins, D. o. 1995. Sea otters and kelp forests in Alaska: generality and variation in a community

ecology paradigm. Ecological Monographs 65 : 75-100. Estes, J. A., Tinker, M. T., Williams, T. M., & Doak, D. F. 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282: 473-476. European Commission 2000. Communication from the Commission to the Council and the European Parliament on Integrated Coastal Zone Management: a strategy for

Europe. COM 2000 547 final. European Commission, Brussels. European Commission 2002. Recommendation ofthe Euro-

pean Parliament and of the Council2002/413/EC of30 May2002. concerning the implementation ofIntegrated Coastal Zone Management in Europe. Official Journal

(L148/24 of6 June 2002. Evans, J. C. 2009. The ethics offish welfare. Journal ofFish Biology 75 : 2872-2874. Evans, S. M., Birchenough, A. C., & Brancato, M. S. 2000. The TBTban: out of the frying pan into the fire? Marine Pollution Bulletin 40: 204-211. Fabry, V. J. 2008. Marine calcifyers in a high-C02 ocean. Science 320: 1020-1022. Fabry, V. J., Seibel, B. A., Feely, R. A., & Orr, J. C. 2008. Impacts of ocean acidification on marine fauna and eco-

system processes. ICES Journal of Marine Science 65 : 414-432. Fairbridge, R. W. 1980. The estuary: its definition and geodynamic cycle. In E. Olavsson, & I. Cato (eds), Chemistry and Geochemistry ofEstuaries . John Wiley & Sons, New York, pp. 1-35. Fairweather, P. G., & Underwood, A. J. 1991. Experimental removals of a rocky intertidal predator: variations

within two habitats in the effects on prey. Journal of Experimental Marine Biology and Ecology 154: 29-75. Falconer R. A., Xia J. Q., Lin B. J., Ahmadian R. 2009. The Severn barrage and other tidal energy options: Hydro-

dynamic and power output modelling. Sci China Ser E-Tech Sci, 52: 3413-3424. Falkowski, P., Scholes, R. J., Boyle, E., Canadell, J., Canfield, D., Elser, J. et al. 2000. The global carbon cycle: a test of our knowledge of earth as a system. Science 290: 291-296. Falkowski, P. G., Barber, R. T., & Smetacek, V. 1998. Biogeochemical controls and feedbacks on ocean primary

production. Science 281 : 200-206. FAO 1995. Code ofconductfor sustainablefisheries . Food and Agriculture Organization of the United Nations. Rome.

FAO 2002 . The state of world fisheries and aquaculture (SOFIA) . Food and Agriculture Organization of the United Nations, Rome. pp. 150. FAO 2003. Fisheries management. 2. The ecosystem approach to fisheries. Rome: FAO. FAO 2007. Food and Agriculture Organisation of the United Nations (FAO) Fisheries and Aquaculture Statistical Database. URI.: http:/ /www.fao.org/fishery/statistics/ global-aquaculture-productionlen.FAO, Rome. Farnsworth, E. J., & Ellison, A. M. 1996. Scale-dependent spatial and temporal variability in biogeography of mangrove root epibiont communities. Ecological Monographs 66: 45-66. Fauchald, P., Erikstad, K. E., & Skarsfjord, H. 2000. Scaledependent predator-prey interactions: The hierarchical

spatial distribution of seabirds and prey. Ecology 81 : 773-783. Feely. R. A.• Sabine. C. L.. Lee, K.. Berelson, W., Kleypas, J.• Fabry, V. J., & Millero, F. J. 2004. Impact of anthropogenic C02 on the CaC03 system in the oceans. Science 305: 362-366. Fegan, D. F. 1996. Sustainable shrimp farming in Asia : vision or pipedream. Asian Aquaculture 2: 22-24. Fenchel, T. 2005 . Respiration in aquatic protists. In P. A. del Giorgio, & P. J. Ie B. Williams (eds), Respiration in Aquatic Ecosystems. Oxford University Press, Oxford, pp. 47-56. Fenchel, T., & Glud, R. N. 2000. Benthic Primary production and 02-C02 dynamics in a shallow water sediment: Spatial and temporal heterogeneity. Ophelia 53: 159-171. Field, C. B., Behrenfeld, M. J., Randerson, J. T., & Falkowski, P. 1998. Primary production of the biosphere : Integrating terrestrial and oceanic components. Science 281 : 237-240. Fisher. B.• & Turner, R. K. 2008 Ecosystem services: classification for valuation. Biological Conservation, 141 : 1167-1169. Fisher. R. Turner, K., Zylstra, M., Brouwer, R., De Groot. R.• Farber. S. et aL 2008. Ecosystem services and economic theory: integration for policy-relevant research. Eco-

logical Applications 18: 2050-2067. [doi: 10.1890/071537.1] . Fogg, G. E. 1998. The Biology ofPolar Regions. Oxford University Press. Oxford. Foote, A. D., Osborne, R. W., & Hoelzel, A. R. 2004. Environment-whale-call response to masking boat noise.

Nature 428: 910. Fossa, J. H., Mortensen, P. B., & Furevik, D. M. 2002. The deepwater coral Lophelia pertusa in Norwegian waters: distribution and fisheries impacts. Hydrobiologia 471 : 1-12. Frank, K. T., Petrie, B., Choi, J. S., & Leggett, W. C. 2005. Trophic cascades in a formerly cod-dominated ecosys-

tem. Science 308: 1621-1623.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Frank, K. T., Petrie, B., & Shackell, N. L., 2007. The ups and downs of trophic control in continental shelf ecosystems. Trends in Ecology, & Evolution 22: 236-242. Fromentin, J., & Planque, B., 1996. Calanus and environment in the eastern North Atlantic. II. Influence of the North Atlantic Oscillation on C. finmarchicus and C. helgolandicus.MarineEcology Progress Series 134: 111-118. Fuhrman, J . A., & Azam, F. 1980. Bacterioplankton secondary production estimates for coastal waters of British Columbia, Antarctica, and California. Applied and EnvironmentalMicrobiology 39: 1085-1095. Fuhrman, J . A., & Azam, F. 1980. Thymidine incorporation as a measure of heterotrophic bacterioplankton production in marine surface waters: Evaluation and field

results. Marine Biology 66: 109-120. Fuhrman, J . A., & Capone, D. 2001. Nifty nanoplankton. Nature 412: 593-594. o Fuhrman, J. A., & Hagstrom A. 2008. Bacterial and archaeal community structure and its patterns. In D. L. Kirchman

(ed) Microbial Ecology of the Oceans, 2nd edn. John Wiley & sons Inc. New York, pp. 45-90. Fuhrman, J. A. 1999. Marine viruses and their biogeochemical and ecological effects. Nature 399 : 541-548. Fuhrman, J . A. 2000. Impact of viruses in bacterial processes. In D. L. Kirchman (ed) Microbial Ecology of the Oceans. John Wiley & sons Inc, New York pp. 327-350. Fuhrman, J. A. 2009. Microbial community structure and its functional implications. Nature 459: 193-199. Fuhrman, J . A., Hewson, I., Schwalbach, M. S., Steele, J . A., Brown, M. A., Green, J . L., & Brown, J . H. 2006. Annually reoccurring bacterial communities are predictable from ocean conditions. Proceedings ofthe nationalAcad-

emyofScience USA 103: 13104-13109. Fuhrman, J . A., Steele, J . A., Hewson, I., Schwalbach, M. S., Brown, M. V., Green, J . L, & Brown J . H. 2008. A latitudinal diversity gradient in planktonic marine bacteria.

Proceedings ofthe NationalAcademyofScience USA, 105: 7774-7778. Fujii, T., & Raffaelli, D. 2008. Sea-level rise, expected environmental changes and responses of intertidal benthic macrofauna in the Humber estuary, UK. Marine Ecology

Progress Series 371 : 23-35. Fujikura, K., Shigeaki, K., Tamaki, K., Maki, Y., Hunt, J . C., & Okutani, T. 1999. The deepest chemosynthesis-based community yet discovered from the hadal zone, 7326 m deep, in the Japan Trench. Marine Ecology Progress Series 190: 17-26. Gage, J . D., & Gordon, J . 1995. Sound bites, science and the Brent Spar: environmental considerations relevant to the deep-sea disposal option. Marine Pollution Bulletin 30: 772-779. Gage, J. D., & Tyler, P. A. 1991. Deep-Sea Biology: a Natural History of Organisms at the Deep-Sea Floor. Cambridge University Press, Cambridge.

Gage, J., 1992. Benthic secondary production in the deep sea. In: G. T. Rowe, V. Pariente, (eds.), Deep-Sea Food Chains and the Global Carbon cycle. Kluwer Academic Publishers, Dordrecht, pp. 183-198. Gaines, S. D., & Roughgraden, J. 1985. Larval settlement rate, a leading detreminat of structure in an ecological community of the intertidal zone. Proceedings of the

National Academy ofSciences USA 82: 3707-3711 . Gaines, S. D., Brown, S., & Roughgraden, J. 1985. Spatial variation in larval concentrations as a cause of spatial variation in settlement for the barnacle Balanus glandula. Oecologia 67: 267-272. Gao, K' Wu, Y., Li, G., Wu, H., Villafane, V. E., & Helbing, E. W. 2007. Solar UV radiation drives C02 fixation in marine phytoplankton: a double edged sword. Plant Physiology 144: 54-59. Garrick, R. c., Sands, C. J ., & Sunnucks, P. 2006. The use and application of phylogeography for invertebrate conservation research and planning. In: Insect Biodiversity and Dead Wood : Proceedings of a Symposium for the 22nd International Congress ofEntomology (eds Grove, S. J ., & Hanula, J. L.), pp. 15-22. General Technical Report SRS-93. US Department of Agriculture Forest Service, Southern Research Station, Asheville, North J

Carolina. Garrison. D. L. 1991 . Antarctic sea ice biota.AmericanZool-

ogist31 : 17-33. Garrison, D. L., Close, A. R., & Reimnitz, E. 1989. Algae concentrated by frazil ice: evidence from laboratory experiments and field measurements. Antarctic Science

1: 313-316. Garzoli, S. L.. Richardson. P. L.. Rae. C. M. D., Fratantoni, D. M., Goni, G. J ., & Roubicek, A. J . 1999. Three Agulhas rings observed during the Benguela Current experi-

ment. Journal of Geophysical Research - Oceans 104: 20971-20985. Gaston, K. J ., & Spicer, J .1. 2004. Biodiversity: an Introduction. 2nd edn. Blackwell Science, Oxford. Geider, R. J ., & la Roche, J . 2002. Redfield Revisited : variability ofC : N : P in marine microalgae and its biochemical basis. European Journal ofPhycology 37: 1-17. Geider, R. J., De Lucia. E. H.• Falkowski. P. G.• Finze, A., Grime, J . P., Grace, J . etal. 2001. Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats. Global Change Biology 7: 849-882. Gerdes, D., Hilbig, B., & Montiel, A. 2003. Impact oficeberg scouring on macrobenthic communities in the highAntarctic Weddell Sea. Polar Biology 26: 295-301. Gerlotto, F., Soria, M., and Freon, P.1999. From two dimensions to three: the use of multibeam sonar for a new approach in fisheries acoustics . Canadian Journal of

Fisheries and Aquatic Sciences 56: 6-12. Giangrande, A., & Licciano, M. 2004. Factors influencing

References latitudinal pattern of biodiversity: an example using Sabellidae (Annelida, Polychaeta) . Biodiversity Conservation 9 : 1633-1646. Gibbons, M. J ., & Griffiths, C. L. 1986. A comparison of macrofaunal and meiofaunal distribution and standing stock across a rocky shore with an estimate oftheir produetivities. Marine Biology 93 : 181-188. Gibson, R. N., & Robb, L. 1992. The relationship between body size, sediment grain size and the burying ability ofjuvenile plaice Pleuronectes platessa L. Journal ofFish Biology 40: 771-778. Gibson, D. R., & Sommerville, C. 1996. The potential for viral problems related to the use of wrasse (Labridae) in the farming of Atlantic salmon. In M. D. J . Sayer, J . W. Treasurer, & M. J . Costello (eds), Wrasse - Biology and Use inAquaculture. Fishing News Books. Oxford, pp. 240-246. Gill, J . A., Sutherland, W. J., & Norris, K. 2001. Depletion models can predict shorebird distribution at different spatial scales. Proceedings ofthe Royal Society ofLondon Series B, 268: 369-376. Giovannoni S. J ., & Stingl, U. 2005. Molecular diversity and ecology of microbial plankton. Nature 437: 343-348. Giovannoni. S. J'J Tripp. H. J., Givan, S.• Podar, M.• Vergin, K. L., Baptista, D. et al. 2005. Genome streamlining in a cosmopolitan oceanic bacterium. Science 309 : 1242-1245. Givernaud, T. J., Casson, J., & Givernaud-Mouradi, A. 1991. Etudes des populations de Sargassum muticum sur les cots de Basse. Norrnandies, France. In M. Elliott. & J . P. Ducrotoy (eds), Estuaries and Coasts: Spatial and TemporalIntercomparison . Olsen, & Olsen, pp. 129-132. Glasby, G. P. 2000. Lessons learned from deep-sea mining. Science 289 : 511-553. Glud, R. N., Santegoeds, C. M., DeBeer, D., Kohls, 0 ., & Ramsing, N. B. 1998. Oxygen dynamics at the base of a bioflm studied with planar optodes. Marine Ecology Progress Series 14, 223-233. Glud, R. N., Tengberg,A., Kiihl, M., Hall, P. O. J ., & Klimant, I. 2001 . An in situ instrument for planar 02 optode measurements at benthic surfaces. Limnology and Oceanography 46: 2073-2080. Glud, R. N., Rysgaard, S., & Kuhl, M. 2002. A laboratory study on 0 2 dynamics and photosynthesis in ice algal communities: quantification by rnicrosensors, 0 2 exchange rates, 14C incubations and a PAM fluorometer. Aquatic Microbial Ecology 27: 301-311. Glynn, P. W. 1997. Bioerosion and coral reef growth: a dynamic balance. In C. Birkeland (ed.), Life and Death on Coral Reefs. Academic Press, New York, pp. 68-95. Goldberg, D. S., Takahashi, T., & Slagle, A. L. 2008. Carbon dioxide sequestration in deep-sea basalt. Proceedings of the National Academy ofScience USA 105: 9920-9925. Gordon, M. S., Ng, W. W. S., & Yip, A. Y. W. 1978. Aspects

of the physiology of terrestrial life in amphibious fishes. III. The Chinese mudskipper Periophthalmus cantonensis. Journal ofExperimental Biology 72 : 57-75. Gore, M. A., Rowat, D., Hall, J., Gell, F. R., & Ormond, R. F.

2008. Transatlantic migration and deep mid-ocean diving by basking shark. Biology Letters 4: 395-398. Gorman, A. M., Gregory, R. S., & Schneider, D. C. 2009. Eelgrass patch size and proximity to the patch edge affect predation risk ofrecently settled age 0 cod (Gadus) .JournalofExperimental Marine Biology and Ecology 371 : 1-9. Goss-Custard, J. D., McGrorty, S., & Kirby, R. 1990. Inshore

birds of the soft coasts and sea-level rise. In J. J. Beukeema, W. J . Wolff, & J . J . W. N. Brouns (eds), Expected Effects of Climate Change on Marine Coastal Ecosystems. Kluwer, Dordecht, pp. 189-193. Gould, S. J. 1989. Wonderful Life. W. W. Norton, & Co, New York. Gould, S. J ., & Calloway, C. B. 1980. Clams and brachiopods-ships that pass in the night. Paleobiology 6: 383396. Gowen, R. J ., & Bradbury, N. B. 1987. The ecological impact

of salmonid farming in coastal waters: a review. Oceanographyand Marine Biology:An Annual Review 25: 563575. Gram, L., Grossart, H. -P., Schlingloff, A., & Kiorboe T. 2002. Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobaeter strains isolated from marine snow. Applied and Environmental Microbiology, 68: 4111-4116. Grantham, B. A., Chan, F., Nielsen, K J., Fox, D. S., Barth, J . A., Huyer, A et al. 2004. Upwelling-driven nearshore hypoxia signals ecosystem and oceanographic changes in the northeast Pacific. Nature 429: 749-753. Grassle, J. F., & Maciolek, N. J . 1992. Deep-sea species richness:regional and local diversity estimate from quantitative bottom samples. American Naturalist 139: 313-334. Grassle, J . F., & Saunders, H. L. 1973. Life histories and the role of disturbance. Deep Sea Research 20: 643-59. Grassle, J. F. 1989. Species diversity in deep-sea communities. Trends in Ecology and Evolution 4: 12-15. Gray, J . S. 2001. Marine diversity: the paradigms in patterns ofspecies richness examined. ScientiaMarina 65:41-56. Green, R. H. 1989. Power analysis and practical strategies for environmental monitoring. Environmental Research 50: 195-205. Green, E. P., & Donnelly, R. 2003. Recreational scuba diving in Caribbean marine protected areas: do the users pay? Ambio 32: 140-144. Green, E. P., & Short, F. T. 2003. World Atlas ofSeagrasses. University of California Press. Greenberg, R. S., Maldonado J . E., Droege S., Mcdonald M. v. 2006. Tidal marshes: a global perspective on the evolution and conservation of their terrestrial vertebrates. Bioscience 56: 675-685.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Gresty, K. A., & Quarmby, C. 1991. The trophic level of Mytilicola intestinalis Steuer (Copepoda: Poecilostomatoida) in Mytilus edulis L., as determined from stable isotope analysis . Proceedings of the Fourth International Conference on Copepoda; BuUetin ofthePlankton Society ofJapan, Special Volume, pp. 363-371. Griffiths, G. E. 2003. Technology and Applications ofAutonomous Underwater Vehicles . Taylor. & Francis. London. Grunbaum, D. 2009. Ecology Peter Principle Packs a Peck of Phytoplankton. Science 323: 1022-1023. Guinotte, J. M., Fabry, V. J . 2008. Ocean acidification and its potential effects on marine ecosystems. New York AcademyofSciences 1134: 320-342. Gutt, J. 2000. Some 'driving forces' structuring communities of the sublittoral Antarctic macrobenthos. Antarctic Science 12: 297-313. Gutt, J. 2001. On the direct impact of ice on marine benthic communities, a review. Polar Biology 24: 553-564. Gutt, J., & Piepenburg, D. 2003. Scale-dependent impacts of catastrophic disturbances by grounding icebergs on the diversity of Antarctic benthos. Marine Ecology Progress Series 253: 77-83. Haamer, J. 1996. Improving water quality in a eutrophied fjord system with mussel farming. Ambio 25: 356-362. Haas, C. 2004.Late-summerseaice thickness variabilityin the Arctic Transpolar Drift 1991-2001 derived from groundbased electromagnetic sounding. Geophysical Research Letters 31 : L09402, doi: 1O.1029/2003GL019394. Haas, c., Pfaffling, A.• Hendricks. 5 .• Rabenstein. L.. Etienne, J . L., & Rigor, I. 2008 Reduced ice thickness in Arctic Transpolar Drift favours rapid ice retreat. Geophysical Research Letters, 35: L17501, 10.1029/2008GL034457. Hackett, J . D., Anderson, D. M., Erdner, D. L., & Bhattacharya, D. 2004. Dinoflagellates: a remarkable evolutionary experiment. American Journal ofBotany 91 : 1523-1534. Haddock, S. H. D., McDougall, C. M., & Case, J . F. 2004. The Bioluminescence Web Page, http z/ z'lifesci.ucsb.edu/ biolum/. Haedrich, R. L., & Merrett, N. R., 1992. Production/biomass ratios. size frequencies, and biomass spectra in deep-sea demersal fishes . In: G. T. Rowe, V. Pariente, (eds.), Deepsea Food Chains and the Global Carbon cycle. Kluwere Academic Publishers, Dordrecht, pp. 157-182. Haines, J., & Maurer. D. 1980. Quantitative faunal associates of the serpulid polychaete Hydroides dianthus. Marine Biology 56: 43-47. Hall, S. J . 1994. Physical disturbance and marine benthic communities: life in unconsolidated sediments. OceanographyandMarineBiologyAnnual Review 32: 179-239. Hall, M. A. 1996. On bycatches. Reviews in Fish Biology and Fisheries 6 : 319-352. Hall, M. A. 1998. An ecological view of the tuna-dolphin problem: impacts and trade-offs. Reviews in Fish Biology and Fisheries 8: 1-34.

Hall, S. J . 2002. The continental shelf benthic ecosystem: current status, agents for change and future prospects. Environmental Conservation 29: 350-374. Hall, S. J., & Raffaelli, D. G. 1991. Static patterns in food webs: lessons from a large web. Journal ofAnimal Ecology 63: 823-842. Hall, S. J ., Robertson, M. R., Basford, D. J ., & Fryer, R. 1993. Pit-digging by the crab Cancer pagurus: a test for longterm, large-scale effects on infaunal community structure. Journal ofAnimal Ecology 62: 59-66. Hall-Spencer, J . M., & Moore, P. G. 2000. Impact of scallop dredging on maerl grounds. In M. J . Kaiser, & S. J. De Groot (eds), Effects of Fishing on Non-Target Species and

Habitats: Biological, Conservation and Socio-Economic Issues . Blackwell Science, Oxford, pp. 105-118. Hall-Spencer, J . M., & Moore, P. G. 2000. Limaria hians (Mollusca: Limacea) : a neglected reef-forming keystone species. Aquatic Conservation:Marine andFreshwaterEcosystems 10: 267-277. Hall-Spencer, J, Allain, V., & Fossa, J . H. 2002. Trawling damage to Northeast Atlantic ancient coral reefs. Proceedings oftheRoyal Society ofLondon B 269 : 507-511. Hall-Spencer, J. M., Rodolfo-Metalpa, R., Martin, S., Ransome, E.• Fine, M., Thrner et al. 2008. Volcanic carbon dioxide vents show ecosystem effects of ocean acidification. Nature 454: 96-99. Halpern, B. S., Walbridge,S., SeJkoe, K. A., Kappel, C. V., Micheli, F., D'Agrosa, C. et al. 2008. A global map of human impact on marine ecosystems. Science 319: 948952. Hamm, C. E. 2000. Architecture, ecology and biogeochemistry of Phaeocystis colonies. Journal ofSea Research 43 : 307-315. Hamm, C. E., Merkel. R.. Springer, 0 .. Jurkojc, P.• Maier, C., Prechtel, K., & Smetacek, V. 2003. Architecture and material properties ofdiatom shells provide effective mechanical protection. Nature 421 : 841-843. Hamner. W. M., Jones, M.S., Carleton. J. H., Hauri, I. R., & Williams, D. M. 1988. Zooplankton, planktivorous fish and water currents on a windward reefface. Great Barrier Reef, Australia. Bulletin ofMarine Science 42: 459-479. Handy, R. D., Owen, R., & Valsami-Jones, E. 2008. The ecotoxicology of nanoparticles and nanomaterials: current status, knowledge gaps, challenges and future needs. Ecotoxicology 17: 315-325. Hanley. N. 1998. Economics of nature conservation. In W. J. Sutherland (ed.), Conservation Science and Action. Blackwell, Oxford, pp. 220-236. Hannach, G., & Siglo, A. C. 1998. Photoinduction of UVabsorbing compounds in six species of marine phytoplankton. Marine Ecology Progress Series 174: 207-222. Hare, S. R., & Mantua, N. J . 2000. Empirical evidence for North Pacific regime shifts in 1977 and 1989. Progress in

Oceanography47: 103-45.

References Hargrave, B. T., Prouse, N. J., Phillips, G. A., & Cranford, P. J. 1994. Meal size and sustenance time in the deep-sea amphipod Eurythenes gryllus collected from the arcticocean. Deep-Sea Research Part I 41 : 1489-1508. Hartstein, N. D., & Rowden, A. A. 2004. Effect ofbiodeposits from mussel culture on macroinvertebrate assemblages at sites of different hydrodynamic regime . Marine Environmental Research 57: 339-357. Harvell, C. D., Kim, K., Burkholder, J . M., Colwell, R. R., Epstein, P. R., Grimes, D. J. etall999. Emerging marine diseases-climate links and anthropogenic factors. Science 285: 1505-1510. Harvell, C. D., Mitchell, C. E., Ward, J . R., Altizer, S., Dobson, A. P., Ostfeld, R. S., & Samuel, M. D. 2002. Climate warming and disease risks for terrestrial and marine biota. Science 296: 2158-2162. Hatcher, B. G. 1988. The primary productivity of coral reefs: a beggar's banquet. Trends in Ecology and Evolution 3: 106-11. Hatcher, B. G. 1997. Organic production and decomposition.ln C. Birkeland (ed.), Life and Death on Coral Reefs. Chapman & Hall, New York, pp. 140-174. Hauxwell, J., Cebrian, J., Furlong, C., & Valiela, I. 2001. Macroalgal canopies contribute to eelgrass (Zostera marina) decline in temperate estuarine ecosystems. Ecology 82 : 1007-1022. Hauxwell, J ., Cebrian, J., & Valiela, I. 2003. Eelgrass Zostera marina loss in temperate estuaries: relationship to land-derived nitrogen loads and effect of light limitation imposed by algae. Marine Ecology Progress Series 247: 59-73. Hawkins, S. J ., & Hartnoll, R. G. 1983. Grazing of intertidal algae by the marine invertebrates. Oceanography and Marine Biology:Annual Review 21 : 195-282. Hawkins, S. J ., & Hartnoll, R. G. 1985. Factors determining the upper limits of intertidal canopy-forming algae. Marine Ecology Progress Series 20: 265-271 . Hays, G. C. 2003. A review ofthe adaptive significance and ecosystem consequences of zooplankton diel vertical migrations. Hydrobiologia 503 : 163-170. Hays, G. c., Houghton, J . D. R., & Myers, A. E. 2004. Endangered species-Pan-Atlantic leatherback turtle movements. Nature 429: 522. Heath, M. R. 1992. Field Investigations of the early Life Stages of Marine Fish. In J . H. S. Blaxter, & A. J. Southward (eds), Advances in Marine Biology. Acadentic Press, London,pp.2-133. Heath, M. R. 1995. Size spectrum dynamics and the planktonic ecosystem of Loch Linnhe. ICES Journal ofMarine Science 52 : 627-642. Heath, M. R. 2005. Changes in the structure and function of the North Sea fish foodweb, 1973-2000, and the impacts of fishing and climate. ICES Journal of Marine Science 62: 847-868.

Heath, M. R., & Beare, D. J . 2008. New primary production in northwest European shelf seas, 1960-2003. Marine Ecology-Progress Series 363 : 183-203. Heath, M. R., Boyle, P. R., Gislason, A., Gurney, W. S. C., Hay, S. J., Head, E. J . H. etal. 2004. Comparative ecology of overwintering Calanus finmarchicus in the northern North Atlantic, and implications for life cycle patterns. ICES Journal ofMarine Science 61 : 698-708. Heath, M. R., Rasmussen, J.• Ahmed, Y.•Allen, J., Anderson. C. I. H., Brierley, A. S. et al 2008. Spatial demography of Calanus finmarchicus in the Irminger Sea. Progress in Oceanography 76: 39-88. Heck, K. L., & Orth, R. J . 1980. Seagrass habitats: the roles of habitat complexity, competition and predation in structuring associated fish and motile macroinvertebrate assemblages. In: V. S. Kennedy (ed.), Estuarine Perspectives. Academic Press, pp. 449-464. Hecker, B., Logan, D. T., Gandarillas, F. E., & Gibson, P. R. 1988. Canyon and slope processes study Vol 3 : Biological processes. Lamont-Doherty Geological Observatory, Columbia University, New York. Hedgpeth, J . W. 1967. Ecological aspects of the Laguna Madre, a hypersaline estuary. In G. H. Lauff (ed), Estuaries. Washington, DC. American Association for the Advancement of Science Publication 83, pp. 408-419. Heip, C. H. R., Goosen, N. K., Herman, P. M. J ., Kromkamp, J ., Middelburg, J . J ., & Soetaert, K. 1995. Production and consumption of biological particles in temperate tidal estuaries. Oceanography Marine Biology: AnAnnual Review 33: 1-149. Helbing, E.W., Villafane, V. E., Ferrario, M., & Holm-Hansen, O. 1992. Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species. Marine Ecology Progress Series 80: 89-100. Helbling, E. W., Burna, A. G. J ., de Boer, M. K., & Villafane, V. E. 2001. In situ impact of solar ultraviolet radiation on photosynthesis and DNA in temperate marine phytoplankton. Marine Ecology Progress Series 211 : 43-9. Hemminga, M. A., & Duarte, C. M. 2000. Seagrass Ecology. Cambridge University Press, Cambridge. Hemminga, M. A., Marba, N., & Stapel, J . 1999. Leafnutrient resorption, leaf life span and the retention of nutrients in seagrass systems. AquaticBotany 65 : 141-58. Herring, P. 2002. The Biology oftheDeep Ocean. Oxford University Press, Oxford. Hessler, R. R., Sntithey, W. M., Boudrias, M. A., Keller, C. H., Lutz, R. A., & Childress, J . J . 1988. Temporal change in megafauna at the Rose Garden hydrothermal vent (Galapagos Rift; eastern tropical Pacific) . Deep-Sea Research 35 : 1681-1709. Hester, K. C., Peltzer, E. T., Kirkwood, W. J., & Brewer, P. G. 2008. Unanticipated consequences ofocean acidification: A noisier ocean at lower pH. Geophysical Research Letters 35: L19601 .

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Hewson, I., Steele, J . A., Capone D. G., & Fuhrman J . A. 2006. Temporal and spatial scales of variation in baeterioplankton assemblages ofoligotrophic surface waters. Marine Ecology Progress Series 311 : 67-77. Hicks, G. R. F. 1985. Meiofaunaassociated with rocky shore algae. In The Ecology of Rocky Coasts (eds Moore P. G., Seed R.), Hodder and Stoughton, London, pp. 36-56. HiddinkJ. G., & Kaiser M. J . 2005. The importance ofabundance-limiting factors in the development of ecological indicators. Ecography 28: 264-271 . Hiddink, J. G., Jennings, S.• Kaiser, M. J., Queir6s, A. M.• Duplisea, D. E., & Piet, G. J ., 2006. Cumulative impacts ofseabed trawl disturbance on benthic biomass. production and species richness in different habitats. Canadian Journal ofFisheries and Aquatic Sciences 63 : 721-736. Hiddink, J . G., Rijnsdorp, A., & Piet, G., 2008. Can bottom trawling disturbance increase food production for a commercial fish species? Canadian Journal of Fisheries and Aquatic Science 65: 1393-1401. Hilborn R. 2006. Faith-based fisheries. Fisheries 31 : 554555. Hilborn, R. 1992. Hatcheries and the future of salmon in the Northwest. Fisheries 17: 5-8. Hilborn, R. 1996. Risk analysis in fisheries and natural resource management. Human Ecological Risk Assessment 12: 655-659. Hilborn, R. 1999. Confession of a reformed hatchery basher. Fisheries 24: 3D-I. Hilborn, R., & Cowan, J . H. 2010 Marine stewardship: high bar for seafood. Nature 467: 531. Hilborn, R., & Walters, C. J . 1992. Quantitative Fisheries Stock Assessment: Choice, Dynamics and Uncertainty. Chapman & Hall, New York. Hill, A. E., James, I. D., Linden, P. F., Matthews, J . P., Prandie, D., Simpson, J. H. et al. 1993. Dynamics of Tidal Mixing Fronts in the North Sea. Philosophical Transactions ofthe Royal Society ofLondon Series A: Mathematical Physical and Engineering Sciences 343 : 431-446. Hinz, H' Kaiser, M. J., Bergmann, M., Rogers, S. I., & Armstrong, M. 2003. Ecological relevance of temporalstability in regional fish catches. Journal of Fish Biology 63 : 1219-1234. Hinz, H' Bergmann, M., Shucksmith, R., Kaiser, M. J., & Rogers, S. I., 2006. Habitat association of three flatfish species (Pleuronectes platessa, Solea solea and Microstomus kitt) in the English Channel. ICES Journal ofMarine Science 63: 912-927. Hiscock, K. 1983. Water movement. In R. Earll, & D. G. Erwin (eds), Sublittoral Ecology. Oxford University Press, Oxford, pp. 58-96. Hixon, M. A. 1991 . Predation as a process structuring coral reef fish communities. In P. F. Sale (ed.) The Ecology of Fishes on Coral Reefs. Academic Press, San Diego, pp. 475-508. J

J

Hobbie J. E., DaleyR. J ., & Jasper S. 1977. Use ofnuclepore filters for counting bacteria by fluorescence microscopy. Appliedand Environmental Microbiology 33 : 1225-1228. Hogarth, P. J . 1999. The Biology ofMangroves. Oxford University Press, Oxford. Holliday, D. V., & Pieper, R. E. 1995. Bioacoustical Oceanography at High-Frequencies. ICES Journal of Marine Science 52: 279-296. Holliday, D. V., Donaghay, P. 1.., Greenlaw, C. F., McGehee, D. E., McManus, M. M., Sullivan, J . M., & Miksis, J . I.. 2003. Advances in defining fine- and micro-scale pattern in marine plankton. Aquatic Living Resources 16: 131-136. Hollingsworth, A., & Connolly, R. M. 2006. Feeding by fish visiting inundated subtropical saltmarsh. Journal of Experimental Marine Biology and Ecology 336: 88-98. Hooper, W. D., & Ash, H. B. 1934. Translation of On Agriculture by Marcus Terentius Yarra. Harvard University Press, Cambridge, MA. Houghton, J . T., Ding, Y., Griggs, D. J ., Noguer, N., Van der Linden, P. J., Xiaosu, D. et al. 2001. Climate change 2001 : The Scientific Basis. Cambridge University Press, Cambridge, UK, 881 pp. Houghton, J . D. R., Doyle, T. K., Davenport, J ., Wilson, R. P., & Hays, G. C. 2008. The role ofinfrequent and extraordinary deep dives in leatherback turtles (Dermochelys coriacea) .Journal ofExperimental Biology 211 : 2566-2575 . House, K. Z., Schrag, D. P., Harey, C. F., & Lackner, K. S. 2006. Permanent carbon dioxide storage in deep-sea sediments. Proceedings of the National Academy of Science USA 103: 12291-12295. Hovel, K. A., & Lipcius, R. N. 2001. Habitat fragmentation in a seagrass landscape : patch size and complexity control blue crab survival. Ecology 82 : 1814-1829. Hoyer, K., Karsten, U., & Wiencke, C. 2002. Induction of sunscreen compounds in Antarctic macroalgae by different radiation conditions. Marine Biology41 : 619-627. Hubbard, D. K. 1997. Reefs as dynamic systems. In C. Birkeland (ed.), Life and Death of Coral Reefs. Chapman & Hall, New York, pp. 43-67. Hughes, D. J., Atkinson, R. J . A., & Ansell, A. D. 1999. The annual cycle ofsediment turnover by the echiuran worm Maxmuelleria lankesteri (Herdman) in a Scottish sea loch. Journal of Experimental Marine Biology and Ecology 238: 209-309. Hull, S. C. 1987. The growth of macroalgal mats on the Ythan estuary with respect to their effects on invertebrate abundance. PhD thesis, University of Aberdeen. Hunter, K. A. 1999. Direct disposal of liquified fossil fuel carbon dioxide in the ocean. Marine and Freshwater Research 50: 755-60. Huntingford, F. A., & Kadri, S. 2009 Taking account of fish welfare : lessons from aquaculture? Journal ofFish Biology 75 : 2862-2867.

References Huntingford, F. A., Adams, C. E., Braithwaite, V. A., Kadri, S., Pottinger, T. G., Sandoe, P., & Turnbull, J . F. 2006. Current issues in fish welfare. Journal ofFish Biology 68: 332-372. Huntingford, F. A., Adams, C. E., Braithwaite, V. A., Kadri, S., Pottinger, T. G., Sandoe, P., & Turnbull, J . F. 2007 The implications of a feelings-based approach to fish welfare: a reply to Arlinghaus et at. Fish and Fisheries 8: 277-280. Hurlbert, S. H. 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs 54: 187-211. Huston, M. A. 1997 Hidden treatments in ecological experiments: Re-evaluating the ecosystem function of biodi-

versity. Oecologia 110: 449-460. Hutchings, J . A. 2001. Conservation biology of marine fishes : perceptions and caveats regarding assignment of extinction risk. Canadian Journal of Fisheries and

Aquatic Science 58: 108-121. Hutchings, J . A., & Myers, R. A. 1994. What can be learned from the collapse of a renewable resource- Atlantic Cod Gadus morhua, of Newfoundland and Canada. Canadian Journal of Fisheries and Aquatic Sciences 51 : 2126-46. Hutchinson, G. E. 1957. Concluding remarks. Cold Spring Harbor Symposium on QuantitativeBiology 22 : 415-427. Hutchinson, G. E. 1961. The paradox of the plankton.American Naturalist 95: 137-45. Iglesias-Rodriguez, M. D., Halloran, P. R., Rickaby, R. E. M., Hall, I. R., Colmenero-Hidalgo, E. Gittins, J . R. et at. 2008. Phytoplankton calcification in a high-C02 world. Science 320: 336-340. Ikebe, Y., & Oishi, T. 1996. Correlation between environmental parameters and behaviour during high tides in

Periophthalmus modestus. Journal of Fish Biology 49 : 139-147. Intergovernmental Panel on Climate Change CIpCC) 2000. Special Report on Emissions Scenarios. Cambridge University Press, Cambridge.

Intergovernmental Panel on Climate Change CIpCC) 2001 . Climate Change 2001 : Impacts, Adaptation and Vulnerability. Cambrdge University Press, Cambridge. Intergovernmental Panel on Climate Change CIpCC) 2007a. Climate Change 2007: Mitigation of Climate Change. Cambridge University Press. Intergovernmental Panel on Climate Change CIpCC) 2007b. Climate Change 2007: Impacts, Adaptation, and Vulnerability. Cambridge University Press. Intergovernmental Panel on Climate Change CIpCC) 2007c. Climate Change 2007: The Physical Science Basis. Cambridge University Press.

Intergovernmental Panel on Climate Change CIpCC) 2007d. Climate Change 2007: Synthesis Report. Contribution of Working Groups I, 11 and III to the Fourth Assess-

ment Report of the Intergovernmental Panel on Climate

Change [Core Writing Team, Pachauri, R. K. and Reisinger,A. (eds.)] Geneva: IPCC; 2007. Irlandi, E. A., Orlando, B. A., & Ambrose, W. G. 1999. The effect of habitat patch size on growth and survival of juvenile bay scallops (Argopeclen irradians) . Journal of Experimental Marine Biology and Ecology 235: 21-43. Ishimatsu, A., & Kurihara, H. 2008. Short- and long-term impacts of CO2 ocean sequestration on marine animals. 2008 Western Pacific Geophysical Meeting, Cairns Australia. invited presentation summary. http:/ /unit.

aist.go.jp/emtech-ri!news_topics/2008WPGM/PDF/ OS24B_01.pdf. Ishimatsu, A.• Hishida, Y.• Takita, T.• Kanda. T.• Oikawa, S., Takeda, T., & Huat, K. K. 1998. Mudskippers store air in their burrows. Nature 391 : 237-238. Iverson, R. L. 1990. Control of marine fish production. Limnology and Oceanography 35 : 1593-604. Iversen, M., Eliassen, R. A., & Finstad, B. 2009. Potential benefits of clove oil sedation on animal welfare during salmon smolt, Salmo salar L. transport and transfer to

sea. Aquaculture Research 40: 233-241. Jablonski, D. 1999. The future of the fossil record. Science 284: 2114-2116. Jackson, J . B. C. 1979. Overgrowth competition between encrusting cheilostome ectoprocts in a Jamaican cryptic

reef environment. Journal ofAnimal Ecology 48: 805823. Jackson, J . B. C. 2008. Ecological extinction and evolution in the brave new ocean. Proceedings ofthe NationalAcad-

emyofSciences USA 105: 11458-11465. Jackson, E. L., Rowden, A. A., Attrill, M. J., Bossey, S. F., & Jones, M. B. 2001. The importance ofseagrass as a habitat for fishery species. Oceanographyand Marine Biology: An Annual Review 39 : 269-303. Jacobson, D. M., & Anderson, D. M. 1986. Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms.Journal ofPhycology 22 : 249-258. Jaquet, N., & Raffaelli, D. G. 1989. The ecological importance of sand gobies in an estuarine system. Journal of

ExperimentalMarineBiologyandEcology 128: 147-156. Jacquet, J ., Pauly, D., Ainley, D., Holt, S., Dayton, P., & Jackson, J . B. C. 2010. Seafood stewardship in crisis. Nature 467: 28-29. Janssen, H. H., & Gradinger, R. 1999. Turbellaria (Archoophora: Acoela) from Antarctic sea ice endofauna examination of their micromorphology. Polar Biology

21 : 410-416. Jarman, S.• Elliott. N.• Nicol. S., Mclvlinn, A.• & Newman,

S. 1999. The base composition of the krill genome and its potential susceptibility to damage by UV-B. Antarctic Science 11: 23-26. Jenkins, G., & Hamer, P. 2001. Spatial variation in the use of seagrass and unvegetated habitats by post-settlement

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

King George whiting in relation to meiofaunal distribution and macrophyte structure. Marine Ecology Progress

Series 224: 219-229. Jennerjahn, T. C., & Ittekkot, V. 2002. Relevance of mangroves for the production and deposition of organic matter along tropical continental margins. Die Naturwissenschaften 89: 23-30. Jenness, M. I., & Duineveid, G. C. A. 1985. Effects of tidal currents on chlorophyll a content of sandy sediments in

the southern North Sea. Marine Ecology Progress Series 21 : 283-287. Jennings, S. 2007. Reporting and advising on the effects of fishing. Fish and Fisheries 8: 269-276. Jennings, S., & Blanchard, J . L. 2004. Fish abundance with no fishing : predictions based on macroecological theory.

Journal ofAnimal Ecology 73 : 632-642. Jennings, S., & Kaiser, M. J . 1998. The effects of fishing on marine ecosystems. Advances in Marine Biology 34: 201-352. Jennings, S., & Warr, K. J . 2003. Smaller predator-prey body size ratios in longer food chains. Proceedings ofthe Royal Society ofLondon Series B: Biological Sciences 270: 1413-1417. Jennings, S., Kaiser, M. J ., & Reynolds J . D. 2001a. Marine Fisheries Ecology. Blackwell Science, Oxford. Jennings, S., Melin, F., Blanchard, J. L., Forster, R. M., Dulvy, N. K., & Wilson, R. W. 2008. Global-scale predictions of community and ecosystem properties from

simple ecological theory. Proceedings oftheRoyal Society ofLondon B 275: 1375-1383. Jickells, T. D. 1998. Nutrient biogeochemistryofthe coastal zone. Science 281 : 217-222. Jickells, T. D., An, Z. S., Andersen, K. K., Baker, A. R., Bergametti, G., Brooks, N. et aL 2005. Global iron connections between desert dust, ocean biogeochemistry, and

climate. Science 308: 67-71 . Jones, N. S. 1950. Marine bottom communities. Biological Reviews 25 : 283-313. Jones, S. E., & Jago, C. F. 1993. In situ assessment of modification of sediment properties by burrowing inverte-

brates. Marine Biology 115: 133-42. Jones, E. G., Collins, M. A., Bagley, P. M., Addison, S., & Priede, I. G. 1998. The fate of cetacean carcasses in the deep sea: Observations on consumption rates and scavenging species succession in the abyssal NE Atlantic

Ocean. Proceedings ofthe Royal Society ofLondon B 265: 1119-1127. Jones, G. P., Milicich, M. J ., Emslie, M. J., & Lunow, C. 1999. Self-recruitment in a coral reef fish population. Nature 402: 802-804. Jones, G. P., McCormick, M. I., Srinivasan, M., & Eagle, J. V. 2004. Coral decline threatens fish biodiversity in marine reserves. Proceedings ofthe NationalAcademy ofSciences USA 101 : 8251-3.

Jousson, 0 ., Pawlowski, J., Zaninetti, L., Zechman, F. W., Dini, F., Di Guiseppe, G. et at. 2000. Invasive alga reaches California. Nature 408: 157-158. Jiirgens K., & Massana R. 2008. Protistan grazing on marine bacterioplankton. In D. L. Kirchman (ed) MicrobialEcology ofthe Ocecns, 2nd edn. John Wiley & sons Inc. New York, pp. 383-442. Justid D. 1991. Hypoxic conditions in the northemAdriatic Sea:historical development and ecological significance. InR. V.Tyson, & T. H. Pearson (eds) ,Modern and Ancient

Continetal ShelfAnoxia. Geological Society Special Publication, London, pp. 95-102. Justic, D., Rabalais, N. N., & Turner, R. E. 2005. Coupling between climate variability and coastal eutrophication:

evidence and outlook for the northern Gulf of Mexico. Journal ofSea Research 54: 25-35. Kaiser, M. J . 2003. Detecting the effects of fishing on seabed community diversity: importance of scale and sample

size. Cow;ervationBiology 17: 512-520. Kaiser, M. J. 2004. Fish in deep-water coral habitats. Science 304: 1595. Kaiser, M. J ., & de Groot, S. J . 2000. The Effects ofFishing on

Non-Target Species and Habitats: Biological, Cow;ervation and Socio-Economic Issues. Blackwell Science, Oxford. Kaiser, M. J., & Edwards-Jones, G. 2006. The role of ecolabelling in fisheries management and conservation.

Cow;ervation Biology 20: 392-398. Kaiser, M. J ., & Hill, L. 2010. Marine stewardship: a force for good. Nature 467: 531 . Kaiser, M. J ., Laing, I., Utting, S. D., & Burnell, G. M. 1998. Environmental impacts of bivalve mariculture. Journal ofShellfish Research 17: 59-66. Kaiser, M. J ., Rogers, S. I., & Ellis, J . R. 1999a. Importance of benthic habitat complexity for demersal fish assemblages. In L. Benaka (ed.), Fish Habitat: Essential Fish Habitat and Restoration . American Fisheries Society, Bethesda, Maryland, pp. 212-23. Kaiser, M. J ., Cheney, K. L., Spence, F. E., Edwards, D. B., & Radford, K. J. 1999b. Fishing effects in northeast Atlantic shelf seas: patterns in fishing effort, diversity and community structure. VII . The effects of trawling disturbance on the fauna associated with the tubeheads

of serpulid worms. Fisheries Research 40: 195-205. Kaiser, M. J., Collie, J. S., Hall, S. J., Jennings, S., & Poiner, I. R. 2002. Modification of marine habitats by trawling activities: prognosis and solutions. Fish and Fisheries 3 :

114-136. Kaiser M. J ., Bergmann M., Hinz H., Galanidi M., Suchksmith R., Rees E. I. S. et at. 2004. Demersal fish and epifauna associated with sandbank habitats. Estuarine, Coastal and ShelfScience 60: 445-456. Kaiser, M. J., Clarke, K. R., Hinz, H., Austen, M. C. V., Somerfield, P. J ., & Karakassis, I., 2006. Global analysis and prediction of the response of benthic biota to fish-

References ing. Marine Ecology Progress Series 311 : 1-14. Kaiser, S., Barnes, D. K. A., & Brandt, A. 2007 Slope and deep-sea abundance across scales: Southern Ocean isopods show how complex the deep sea can be. Deep-Sea Research II 54: 1776-1 789. Karentz, D., Cleaver, J . E., & Mitchell, D. 1. 1991. Cell survival characteristics and molecular responses ofAntarctic phytoplankton to Ultraviolet-B radiation. Journal of Phycology 27: 326-341. Karl, D. M. 2002. Hidden in a sea of microbes. Nature 415 : 590-591 . Karsten, U., Wulff, A., Roleda, M. Y., Muller, R., Steinhoff, F. S., Fredersdorf, J . and Wieneke, C. 2009. Physiological responses of polar benthic algae to ultraviolet radiation. BotanicaMarina, 52 : 639-654. Katija, K., & Dabiri, J . o. 2009. A viscosity-enhanced mechanism for biogenic ocean mixing. Nature 460: 624-U687. Keeling, C. D., & Whorf, T. P. 2000. The 1,800-yearoceanic tidal cycle: A possible cause of rapid climate change.

Proceedings of the National Academy of Sciences 97 : 3814-3819. Kelley, D. S., Karson, J . A., Blackman, D. K., Fruh-Green, G. 1., Butterfield, D. A., Lilley, M. D. et al. 2001. An off-axis hydrothermal vent field near the mid-Atlantic Ridge at 30 N. Nature 412: 145-149. Kennish, M. 2002. Environmental threats and environmental future of estuaries. Environmental Conservation 29 : 78-107. Kenny, A. J., & Rees, H. 1. 1996. The effects of marine gravel extraction on the macrobenthos: results 2 years postdredging. Marine Pollution BuUetin 32: 615-22. Kent, G. 1998. Fisheries, food security and the poor. Food Policy 22 : 393-404. Kent, M., Gill, W. J ., Weaver, R. E., & Armitage, R. 1997. Landscape and plant community boundaries in biogeography. Progress in Physical Geography 21 : 315-354. Keuskamp, D. 2004. Limited effects of grazer exclusion on the epiphytes of Posidonia sinuosa in South Australia. AquaticBotany 78: 3-14. Kideys, A. E. 2002. Fall and rise of the Black Sea ecosystem. Science 297: 1482-1484. . King, D. A. 2004. Climate change science : adapt, mitigate, or ignore? Science 303 : 176-177. King, G. M. 2005. Ecophysiologyofmicrobial respiration. In P. A. del Giorgio, & P. J . Ie B. Williams (eds), Respiration in Aquatic Ecosystems. Oxford University Press, Oxford, pp.18-35. Kiorboe, T., & Jackson, G. A. 2001 . Marine snow, organic solute plumes. and optimal chemosensory behavior of bacteria. Limnology and Oceanography 46: 1309-1318. Kirchman, D. 1. (ed.) 2000. Microbial Ecology ofthe Oceans. John Wiley & Sons Inc., New York. Kirchman, D., K'Nees, E., & Hodson, R. 1985. Leucine incorporation and its potential as a measure of protein syn-

thesis by bacteria in natural aquatic systems. Applied and Environmental Microbiology 49: 599-607. Kirk, J . T. o. 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Cambridge. Kirst, G. 0 ., & Wieneke, C. 1995. Ecophysiology of polar algae. Journal ofPhycology 31 : 181-199. Klages, M., Vopel, K., Bluhm, H., Brey, T., Soltwedel, T., & Arntz, W. E. 2001. Deep-sea food falls : first observation of a natural event in the Arctic Ocean. Polar Biology 24: 292-295. Klein, J ., & Verlaque, M. 2008. The Caulerpa racemosa invasion: a critical review. Marine Pollution Bulletin 56 : 205-225. Klekowski, E. J., Temple, S. A., Siung-Chang, A. M., Kumarsingh, K. 1999. An association of mangrove mutation, scarlet ibis and mercury contamination in Trinidad. West Indies. EnvironmentalPoUution 105: 185-189. Knowles. T. G., Brown, S. N, Wariss, P. D. Lines. J. Tinarwo, A., & Sendon, M. 2008. Effects of electrical stunning at slaughter on the quality of farmed turbot (Psetta maxmia) .Aquaculture Research 39 : 1731-1738. Knowlton, N. 2001. The future of coral reefs. Proceedings ofthe National Academy ofSciences ofthe USA 98: 54195425. Kolar, C. S., & Lodge, D. M. 2001. Progress in invasion biology: predicting invaders. Trends in Ecology and Evolu-

tion16: 199-204. Kolber, Z. 2007. Energy cycle in the ocean: Powering the microbial world. Oceanography 20: 79-88. Koslow, J . A. 1997. Seamounts and the ecology of deep-sea fisheries. American Scientist 85: 168-76. Koslow. J. A.• Gowlett-Holmes, K.• Lowry, J. K., O'Hara, T., Poore, G. C. B., & Williams, A. 2001 . Seamount benthic macrofauna off southern Tasmania: community structure and impacts of trawling. Marine Ecology Progress Series 213: 111-125. Krause, G. H., & Weis, E. 1991. Chlorophyll fluorescence and photosynthesis: the basics. Annual Review of Plant Physiology and Plant Molecular Biology 42 : 313-349. Krembs, C., Gradinger, R., & Spindler, M. 2000. Implications of brine channel geometry and surface area for the interaction of sympagic organisms in Arctic sea ice.

Journal ofExperimental Marine Biology and Ecology 243 : 55-80. Krembs, C., Eicken, H., Junge, K., & Deming, J . W. 2002. High concentrations of exopolymeric substances in Arctic winter sea ice : implications for the polar ocean carbon cycle and cryoprotection of diatoms. Deep Sea Research (Part 1) 49: 2163-2681. Kuhl, M. Rickelt, 1. F., & Thar, R. 2007. Combined imaging of bacteria and oxygen in biofilms. Applied and Environmental Microbiology, 73 : 6289-6295. Kunin, W. E., & Lawton, J . H. 1996. Does biodiversity matter? Evaluating the case for conserving species. In K. J.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Gaston (ed.), Biodiversity:A Biology ofNumbers and Difference . Blackwell Science, Oxford, pp. 283-308. Kunze. E.. Dower. J. F.• Beveridge. I.. Dewey. R., & Bartlett. K. P. 2006. Observations of biologically generated turbu-

lence in a coastal inlet. Science 313: 1768-1770. Kunzig, R. 2000. Mapping the Deep: the ExtraordinaryStory ofOcean Science. Sort Of Books, London. Kurlansky, M. 1997. Cod: A Biography of the Fish That Changed the World . Walker, & Company, New York. Laffoly, D., & Grimsditch, G. (eds.) 2009. The Management of Natural Coastal Carbon Sinks. mCN, Gland, Switzerland. 53pp. Lalli, C. M., & Parsons, T. R. 2004. Biologiool Oceanography. An Introduction, 2nd edn. Butterworth-Heinemann. Lambshead, P. J . D., & Boucher, G. 2003. Marine nematode deep-sea biodiversity-hyperdiverse or hype? Journal of Biogeography 30: 475-485 . Lambshead, P. J . D., Platt, H., & Shaw, K. 1983. The detection of differences among assemblages of marine ben-

thic species based on an assessment of dominance and diversity. Journal ofNatural History 17: 859-74. Lambshead, P. J. D., Tietjen, J ., Moncreiff, C. B., & Ferrero, T. J . 2001 . North Atlantic latitudinal diversity patterns in deep-sea marine nematode data. Marine Ecology Progress Series 210: 299-301. Lampitt, R. S. 1985. Evidence for the seasonal deposition of detritus to the deep-sea floor and its subsequent resuspension. Deep-Sea Research 23A: 885-897. Lampitt, R. S., & Burnham, M. P. 1983. A free fall time lapse camera and current meter system 'Bathysnap'with notes

on the foraging behaviour of a bathyal decapod shrimp. Deep-Sea Research I 30: 1009-1017. Larkum, A. W. D., & den Hartog, C. 1989. Evolution and biogeography of seagrasses, In A. W. D. Larkum, A. J . McComb, & S. A. Shepherd (eds), Biology ofSeagrasses, Elsevier, pp. 112-156. Lawrie, S. M., Speirs, D. c., Raffaelli, D. G., Gurney, W. S. C., Paterson, D. M., & Ford, R. 1999. The swimming behaviour and distribution of Neomysis integer in realation to tidal flow. Journal ofExperimental MarineBiology and Ecology 242 : 95-106. Lawton, J . H., & Jones, C. G. 1995. Linking species and ecosystems: organisms as ecosystem engineers. In J. H. Lawton, & C. G. Jones (eds), Linking Species and Ecosystems, Kluwer Academic Publishers, pp. 141-150. Leakey, C. D. B., Attrill, M. J ., & Fitzsimons, M. F. 2009. Multi-element otolith chentistry of juvenile sole (Solea solea), whiting (Merlangius merlangus) and European seabass (Dicentrarchus labrax) in the Thames Estuary and adjacent coastal regions. Journal of Sea Research 61 : 268-274. Lee, S. Y. 1998. Ecological role ofgrapsid crabs in mangrove ecosystems: a review. Marine and Freshwater Research 49 : 335-43.

Lee, S. Y. 1999. The effect of mangrove leaf litter enrichment on macrobenthic colonization of defaunated sandy substrates. Estuarine Coastal and ShelfScience 49 : 703-712. Lee, S. Y., Fong, C. W., & We, R. S. S. 2001. The effects of seagrass (Zostera japonica) canopy structure on associated fauna: a study using artificial seagrass units and sampling of natural beds. Journal of Experimental Marine Biology and Ecology 259: 23-50. Lee, J ., South, A. B., & Jennings, S. 2010. Developing reliable, repeatable, and accessible methods to provide high-resolution estimates of fishing-effort distributions

from vessel monitoring system (VMS) data. ICES Journal ofMarine Science 67: 1260-1271. Lefevre, N., Taylor, A. H., Gilbert, F. J ., & Geider, R. J . 2003. Modeling carbon-ta-nitrogen and carbon-to-chiarophyll-a ratios in the ocean at low latitudes: evaluation

of the role of physiological plasticity. Limnology and Oceanography 48: 1796-807. Legendre, L., Ackley, S. F., Dieckmann, G. S., Gullicksen, R., Horner, T., Hoshiai, T. et al. 1992. Ecology of sea ice biota. 2. Global significance. Polar Biology 12: 429-44. Lehody, P., Bertignac, M., Hampton, J., Lewis, A., & Picaut,

J. 1997. El Nino Southern Oscillation and tuna in the western Pacific. Nature 389: 715-717. Leininger, S., Urich, T., Schlater, M., Schwark, L., Qi, J.,

Nicol, G. W. et al. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442 : 806-809. Lenihan, H. S., & Peterson, C. H. 1998. How habitat degradation through fishery disturbance enhances impacts

of hypoxia on oyster reefs. Ecological Applications 8 : 128-140. Lenton, T. M., & Watson, A. J . 2000. Redfield revisited, 1, Regulation of nitrate, phosphate, and oxygen in the ocean. Global Biogeochemical qycles 14: 225-248. Lenz, J . 2000. Introduction. In R. P. Harris, P. H. Wiebe, J . Lenz, H. R. Skjoldal, & M. Huntley (eds), ICES Zooplankton Methods Manual. Academic Press, London. Leu, E., Sereide, J. E., Hessen, D.O., Falk-Petersen, S.• Berge, J. 2011 . Consequences of changing sea ice cover for primary and secondary producers in the European Arctic: timing, quantity and quality. Progress in Ocean-

ography doi: 10.101b/j.pocean.2011.02.004. Leventer, A. 1998. The fate of Antarctic 'Sea ice diatoms' and their use as paleoenvironmental indicators .Antarc-

tic Research Series 73 : 121-137. Levin, L. A. 1994. Paleoecology and ecology of xenophyophores. Palaios 9 : 32-41 . Levine, J . M., & Hille Ris Lambers, J . 2009. The importance of niches for the maintenance of species diversity. Nature 461 : 254-257. Lewin, R. 1986. Supply-side ecology. Science 234: 25-27. Li, S. W., & Chan, B. K. K. 2008. Adaptations to barnacle

References fouling in the mangroves Kandelia obovata andAegiceras

corniculatum. Marine Biology 155: 263-271 . Lillebe, A. I., Flindt, M. R., Pardal, M. A., & Marques, J . C. 1999. The effect of macrofauna, meiofauna and microfauna on the degradation of Spartina maritima detritus

from a salt marsh area. Acta Oecologica 20: 249-258. Lindholm, J., Auster, P. J ., & Valentine, P. 2004. Role of a large marine protected area for conserving landscape attributes ofsand habitats on George's Bank (NW Atlantic) . Marine Ecology Progress Series 269 : 61-68. Link, J . S. 2002. Does food web theory work for marine ecosystems? Marine Ecology Progress Series 230: 1-9. Little, C., & Kitching, J . A. 2001. Biology of Rocky Shores. Oxford University Press, Oxford. Lizotte, M . P. 2001. The contributions of sea ice algae to Antarctic marine primary production. American Zoolo-

gist 41 : 57-73. Lodge, S. M. 1948. Algal growth in the absence of Patella on an experimental strip of foreshore, Port St Mary, Isle

of Man. Proceedings and Transactions oftheLiverpool Biological Society 56: 78-83. Loeuille, N., & Loreau, M. 2005. Evolutionary emergence of size structured food webs. Proceedings ofthe National Academy ofScience USA 102: 5761-5766. Loh, A. N., Bauer, J . E., & Druffel E. R. M. 2004. Variable ageing and storage of dissolved organic components in the open ocean Nature 430: 877-881. Loneragan, N. R., Bunn, S. E., & Kellaway, D. M. 1997. Are mangroves and seagrasses sources oforganic carbon for penaeid prawns in a tropical Australian estuary? A mul-

tiple stable-isotope study. MarineBiology 130: 289-300. Long, R. A., & Azam, F. 2001. Antagonistic interactions

Lunn, N. J., Stirling, I, Andriashek, D., & Richardson, E. 2004. Selection. of maternity dens by female polar bears in western Hudson. Bay. Polar Biology 27: 350-356. Luther, G. W., Rozan, T. F., Taillefert, M., Nuzzio, D. B., Di Meo, C., Shank, T. M., Lutz, R. A., & Cary, S. C. 2001. Chemical speciation drives hydrothermal vent ecology.

Nature 410: 813-816. Lutz, M. J ., Caldeira, K., Dunbar, R. B., & Behrenfeld, M. J . 2007. Seasonal rhythms of net primary production and particulate organic carbon flux to depth describe the

efficiency of biological pump in the global ocean. Journal ofGeophysical Research, Oceans 112: 26. Lynam, C. P., & Brierley, A. S. 2007. Enhanced survival of O-group gadoid fish under jellyfish umbrellas. Marine Biology 150: 1397-1401. Lynam, C. P., Hay, S. J ., & Brierley, A. S. 2004. Interannual variability in abundance of North Sea jellyfish and links to the North Atlantic Oscillation. Limnology and Oceanography49 : 637-643 . MacArthur, R. H., & Wilson, E. O. 1967. The Theory ofIsland Biogeography. Princeton University Press, Princeton. Macintyre, I. G., & Glynn, P. W. 1976. Evolution of modern Caribbean fringing reef. Galeta Point. Panama. American Association of Petroleum Geologists Bulletin

72: 1054-1072. Macintyre, H. 1.., Kana, T. M., Anning, T., & Geider, R. J . 2002. Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in

microalgae and cyanobacteria. Journal ofPhycology 38: 17-38. Mackas, D. 1.., & Tsuda, A. 1999. Mesozooplankton in the

among marine pelagic bacteria. Applied and Environ-

eastern and western subarctic Pacific: community structure, seasonal life histories. and interannual variability.

mental Microbiology 67: 4975-4983.

Progress in Oceanography 43 : 335-363.

Longhurst, A. R. 1995. Seasonal cycles of production and consumption. Progress in Oceanography 36: 77-167. Longhurst, A. R. 2006. Ecological Geography ofthe Sea. 2nd

MacKenzie, R. A., & Dionne, M. 2008. Habitat heterogeneity: importance of salt marsh pools and high marsh

Edn . Academic Press. San Diego. Lorance, P., & Trenkel, V. M. 2006. Variability in natural behaviour. and observed reactions to an ROV. by mid-

marshes. Marine Ecology Progress Series 368: 217-230. Mackinson, S., & Daskalov, G. 2007. An ecosystem model

surfaces to fish production in two Gulf of Maine salt

of the North Sea to support an ecosystem approach to fisheries management: description and parameterisa-

slope fish species. Journal of Experimental Marine Biology and Ecology 332: 106-119. Lovelock, J . E., & Rapley, C. G. 2007. Ocean pipes could help the Earth to cure itself. Nature 449: 403-403. Ludsin S. A., Fryer B. J., Gagnon J. E. 2006. Comparison

tion. Scientific Series Technical Report, Cefas Lowestoft 142: 196pp. Marion. G. M., Fritsen, C. H., Eicken, H.• & Payne. M. C. 2003. The search for life on Europa: Limiting environ-

of solution-based versus laser ablation inductively cou-

mental factors. potential habitats. and earth analogues.

pled plasma mass spectrometry for analysis oflarval fish

Astrobiology 3 : 785-811 .

otolith microelemental composition. Transactions ofthe

American Fisheries Society 135: 218-231. Lundsten, 1.., Barry, J . P., Cailliet, G. M., Clague, D. A., DeVogelaere, A. P., & Geller, J . B. 2009. Benthic inverte-

Martin, A. P. 2003. Phytoplankton patchiness: the role of lateral stirring and mixing. Progress in Oceanography

57: 125-74. Martin. J. H.• Coale, K. H.• Johnson, K. S.• Fitzwater, S.

brate communities on three seamounts offsouthern and central California. USA. Marine Ecology Progress Series

E., Gordon, R. M., Tanner, S. J . et al, 2002 . Testing the

374: 23-32.

Ocean. Nature 371 : 123-129.

iron hypothesis in ecosystems of the equatorial Pacific

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Martin, S., Rodolfo-Metalpa, R., Ransome, E., Rowley, S., Buia, M-e., Gattuso, J-P., & Hall-Spencer, J . M. 2008. Effects of naturally acidified seawater on seagrass calcareous epibionts. Biology Letters 4 : 689-692. Maslanik, J . A., e. Fowler, J . Stroeve, S. Drobot, J . Zwally, D. Yi, & W. Emery. 2007. A younger, thinner Arctic ice cover: Increased potential for rapid, extensive sea-ice loss. Geophysical Research Letters 34: L24501, doi: 10. 1029/2007GL032043,2007. Masse, G., Rowland, S. J., Sicre, M. -A., Jacob, J., Jansen, E., & Belt, S. T. 2008 Abrupt climate changes for Iceland during the last millennium: Evidence from high resolution sea ice reconstructions. Earth Planetary Science Letters 269 : 564-568. Matthiessen, P., Waldock, R' Thain, J., Waite, M., & Scrope-Howe, S. 1995. Changes in periwinkle (Littorina littorea) populations following the ban on TBT-based antifoulings on small boats in the United Kingdom. Ecotoxicology and Environmental Safety 30 : 180-194. Maxwell, D., & Jennings, S. 2005 Power of monitoring programmes to detect decline and recovery of rare and vulnerable fish. Journal ofApplied Ecology 42 : 25-37. McCarthy, I. D., Fuiman, I.. A., &Alvarez, M. C. 2003. Aroclor 1254 affects growth and survival skills of Atlantic croaker Micropogonias undulates larvae . Marine Ecology Progress Series 252 : 295-301. McClain, C. R. 2009. A decade of satellite ocean color observations.Annual Review ofMarine Science 1: 19-42. McClanahan, T. R. 1992. Resource utilization. competition and predation:a model and example from coral reef grazers. Ecological Modelling 61 : 195-215. McClanahan, T. R. 1995. A coral-reef ecosystem-fisheries model-impacts of fishing intensity and catch selection on reef structure and processes. Ecological Modelling 80: 1-19. McClanahan, T. R. 2002. The near future ofcoral reefs. Environmental Conservation 29: 460-483. McClanahan, T., Polunin, N., & Done, T. 2002. Ecological states and the resilience of coral reefs. Conservation Ecology 16(2) : 18. [online] http:/ /www. conseco1.org/v016/ iss2/art18. McClanahan, T. R.• Graham, N., Maina, J., Chabanet, P.• Bruggemann, J., & Polunin, N. 2007. Influence ofinstantaneous variation in estimates of coral reef fish populations and communities . Marine Ecology Progress Series 340: 221-234. McGlade, J. M., & Metuzals, K. 2000. Options for reductions of by-catches of harbour porpoises (Phocoena phocoena) in the North Sea. In M. J. Kaiser, & S. J . de Groot (eds), J

The Effects of Fishing on Non-Target Species and Habitats Blackwell Science, Oxford, pp. 332-353. Mcivor, e. e., & Smith, T. J. 1995. Differences in the crab fauna of mangrove areas at a Southwest Florida and a Northeast Australia location: implications for leaf litter

processing. Estuaries 18: 591-597. McKinney, F. K. 1995 . One hundred million years ofcompetitive interactions between bryozoan clades:asymmetrical but not escalating. BiologicalJournal ofthe Linnean Society 56: 465-81. McKinney, F., Lidgard, S., Sepkoski, J. J., &Taylor, P. D. 1998. Decoupled temporal patterns ofevolution and ecology in two post-paleozoic clades. Science 281 : 807-809. McManus, M. A., Alldredge, A. 1.., Barnard, A. H., Boss, E., Case, J . F., Cowles, T. J . et a1. 2003. Characteristics, distribution and persistence of thin layers over a 48 hour period. Marine Ecology Progress Series 261 : 1-19. McNeill, S. E., &Fairweather, P. G. 1993. Single large or several small marine reserves? An experimental approach with seagrass fauna. Journal ofBiogeography 20: 429-40. McQueen, D. J ., Johannes, M. R. S., Post, J . R., Steward, T. J., & Lean, D. R. S. 1989. Bottom-up and top-down impacts on freshwater pelagic community structure. Ecological Monographs 59 : 289-310. McShea, D. W. 1996. Metazoan complexity and evolution: is there a trend? Evolution 50: 477-492. Medlin, I.. K., &Priddle, J . (eds) 1990. PolarMarine Diatoms. British Antarctic Survey. Natural Environment Research Council Cambridge, UK. 214 pp. Meinesz, M.• Belsher, T., Thibaut, T.• Antolic, B.• Ben Mustapha, K., Boudouresque, e. -F. et a1 2001. The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. BiologicalInvasions 3 : 201-210. Menge, B. A., & Lubchenko, J. 1981. Communityorganisation in temperate and tropical rocky intertidal habitats. Prey refuges in relation to consumer pressure gradients. Ecological Monographs 51 : 429-450. Menge, B. A., Lubchenko, J., & Ashkenas, I.. R. 1985. Diversity, heterogeneity and consumer pressure in a tropical intertidal community. Oecologia 65: 394-405. Metcalfe, J . D., &Arnold, G. P. 1997. Tracking fish with electronic tags. Nature 387: 665-666. Metcalfe, J . D., Arnold, G. P., &McDowall, P. W. 2002. Migration.ln: Handbook ofFish BiologyandFisheries, Vol 1 Fish Biology (P.J. B. Hart, &J. D. Reynolds, eds), pp. 175-199. Blackwell Publishing. Oxford. Michaud, E., Desrosiers, G., Mermillod-Blondin, F., Sundby, B., & Stora, G. 2006. The functional group approach to bioturbation: ii the effects of the macoma balthica community on fluxes of nutrients and dissolved organic carbon across the sediment-water interface. Journal of Experimental Marine Biology and Ecology 337: 178-189. Michel, e., Nielsen, T. G., Nozais, e., &Gosselin, M. 2002. Significance of sedimentation and grazing by ice micro- and meiofauna for carbon cycling in annual sea ice (northern Baffin Bay) . AquaticMicrobial Ecology 30: 57-68. Micheli, F., &Peterson, C. H.1999. Estuarine vegetated habitats as corridors for predator movements. Conservation Biology 13: 869-81 .

References Miller, P. 2004. Multi-spectral front maps for automatic detection of ocean colour features from SeaWiFS. InternationalJournal ofRemote Sensing 25 : 1437-42. Milliman, J . D. 1991 . Flux and fate of fluvial sediment and water in coastal seas. In F. C. Mantoura, J. -C. Martin. & R. Wollast (eds), Ocean Margin Processes in Global Change. John Wiley & Sons, Chichester, UK, pp. 69-89. Mitchell, J . G., Yamazaki, H., Seuront, L., Wolk, F., & Li, H. 2008. Phytoplankton patch patterns: Seascape anatamy in a turbulent ocean. Journal afMarine Systems 69: 247-253. Montagna, P., & Harper, D. E. J . 1996. Benthic infaunal long-term response to offshore production platforms in the Gulf of Mexico. Canadian Journal of Fisheries and AquaticSciences 53: 2567-88. Montagna, P. A., & Kalke, R. D. 1992. The effect of fresh-

water inflow on meiofaunal and macrofauna! populations in the Guadalupe and Nueces estuaries, Texas. Estuaries 15: 307-26. Montes-Hugo, M.• Doney, S. c.. Ducklow, H. W., Fraser, W., Martinson, D., Stammerjohn, S. E., & Schofield, o. 2009. Recent Changes in Phytoplankton Communities Associated with Rapid Regional Climate Change Along the Western Antarctic Peninsula. Science 323 : 1470-1473. Mora, C., Chittaro, P., Sale, P., Kritzer, J., & Ludsin, S. 2003 Patterns and porocesses in reeffish diversity. Nature 421 : 933-936. Moran P. J. 1986. TheAcanthasterphenomenon. Oceanography and Marine Biology: Annual Review 24: 379-48. Moran. M. A. 2008. Genomics and metagenomics of marine prokaryotes. In D. L. Kirchman (ed) Microbial Ecology of the Oceans, 2nd edn. John Wiley & sons Inc. New York, pp.91-129. Moran, M. A., & Armbrust, E. V 2007. Genomes of sea microbes. Oceanography 20: 47-55. Morin, A., Mousseau, T. A., & Roff, D. A., 1987. Accuracy and precision of secondary production estimates. Limnology and Oceanography 32: 1342-1352. Morris, R. M., Vergin K. L., Cho, J . c., Rappe, M. S., Carlson C. A., & Giovannoni, s. J . 2005. Temporal and spatial response of baeterioplankton lineages to annual convective overturn at the Bermuda Atlantic Time-series Study site. Limnology and Oceanography 50: 1687-1696. Mukai, H. 1993. Biogeography of the tropical seagrasses in the Western Pacific. Australian Journal of Manne and Freshwater Research 44: 1-17. Muller, J ., Masse, G., Stein, R., & Belt, S. T. 2009 Variability of sea ice conditions in the Fram Strait over the past 30.000 years. Nature Geoscience 2 : 772-776. Muller-Parker, G., & D'E1ia, C. F. 1997. Interactions between corals and their symbiotic algae. In C. F. Birkeland (ed.), Life and Death ofCoral Reefs Chapman & Hall, New York, pp.96-113. Mulsow, S., Landrum, P. F., & Robbins, J . A. 2002. Biologi-

cal mixing responses to sublethal concentrations of DDT in sediments by Heteromastus filiformis using a 137Cs marker layer technique. Marine Ecology Progress Series 239 : 181-9l. Mumby, P. J ., Edwards, A. J., Arias-Gonzalez, J . E.,Lindeman, K. c., Blackwell, P. G., Gall, A. et al. 2004. Mangroves enhance the biomass of coral reef fish communities in the Caribbean. Nature 427: 533-536. Murawski, S. A., 2000. Definitions of overfishing from an ecosystem perspective. ICES Journal of Marine Science 57: 649-658. Murawski, S. A. 2007 Ten myths concerning ecosystem approaches to marine resource management. Marine Policy 31 : 681-690. Murphy, E. J ., Boyd, P. W., Leakey, R. J. G., Atkinson, A., Edwards, E. S., Robinson, C. et al. 1998. Carbon flux in ice-ocean-plankton systems of the Bellingshausen Sea during a period of ice retreat. Journal ofMarine Systems 17: 207-27. Myers, A. A. 1997. Biogeographic barriers and the development of marine biodiversity. Estuarine and Coastal Shelf Science 44: 241-8. Myers, R. A., & Worm, B., 2003. Rapid worldwide depletion of predatory fish communities. Nature 423: 280-283. Naeem, S., Loreau, M., & Inchausti, P. 2002. Biodiversity and ecosystem functioning: the emergence ofa synthetic ecological framework In: (ed.) Biodiversity and Ecosystem Functioning: Synthesis and Perspectives. Oxford University Press, Oxford, pp. 3-1l. Nagata, T. 2000. Production mechanisms of dissolved organic matter. In D. L. Kirchman (ed.), Microbial Ecology of the Oceans. John Wiley & Sons, Inc. New York, Chapter 5, pp. 121-52. Nagata T. 2008. Organic matter-bacteria interactions in seawater. In D. L. Kirchman (ed) Microbial Ecology of the Oceans, 2nd edn. John Wiley & sons Inc. New York pp. 207-242. Nakano, H., Koube, H., Umezawa, S.• Momoyama, K.• Hiraoka, M., Inouye, K., & Oseko, N. 1994. Mass mortalities of cultured Kuruma shrimp, Penaeus japonicus, in Japan in 1993: Epizoological survey and infection trials. Fish Pathology 29: 135-9. Naylor, R. L., Goldburg, R., Primavera, J ., Kautsky, N., Beveridge, M. C. M., Clay, J . et al. 2000. Effect of aquaculture on world fish supply. Nature 405 : 1017-24. Nellemann, C., Corcoran. E., Duarte. C. M.• Valdes, L., De Young, c., Fonseca, L., & Grimsditch, G. 2009. Blue Carbon-The Role of Healthy Oceans in Binding Carbon. A Rapid Response Assessment. United Nations Environment Programme. GRID-Arendal, Norway. 78pp. Nelson, T. A., & Waaland, J . R. 1996. Seasonality of eelgrass, epiphyte, and grazer biomass and productivity in subtidal eelgrass meadows subject to moderate tidal amplitude. Aquatic Botany 56: 51-74.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

New, M. B., Tacon, A. G. J., & Csavas, I. 1993. Farm-made aquafeeds, FAO (Food and Agriculture Organisation of the United Nations) RAPA (Regional Office for Asia and the Pacific) ASEAN (Association of Southeast Asian Nations) Commission ofEuropean Communities, Rome . Nichols, D. S. 2006. Prokaryotes and the input of polyunsaturated fatty acids to the marine food web. FEMS Microbiology Letters 219 : 1-7. Nicol, S., & Brierley, A. S. 2010. Through a glass less darkly-New approaches for studying the distribution, abundance and biology of Euphausiids. Deep-Sea ResearchPartII 57: 496-507. Nicol, S., & de la Mare, W. K. 1993. Ecosystem management and the Antarctic krill. American Scientist 81 : 36-47. Nicol, S., Worby, A., & Leaper, R. 2008. Changes in the Antarctic sea ice ecosystem: potential effects on krill and baleen whales. Marine and Freshwater Research 59: 361-382. Nicol, S., Bowie, A. Jarman, S. Lannuzel, D., Meiners, K. M., & van der Merwe, P. 2010. Southern Ocean iron fertilization by baleen whales and Antarctic krill. Fish and Fisheries 11 : 203-209. Nixon, S. W. 2004. The artificial Nile.American Scientist 92: 158-65. Noble, C., Kadri, S., Mitchell, D. F., & Huntingford, F. A. 2008. Growth, production and fin damage in cage-held 0+ Atlantic salmon pre-smolts (Salmo salar 1..) fed either a) on-demandintraspecific competition, fin damage and growth in l +Atlantic salmon parr or b) to a fixed satiation-restriction regime: data from a commercial farm. Aquaculture 275: 163-168. Norse, E. A. (ed.) 1993. GlobalMarineBiologicalDiversity:A Strategyfor Building Conservation into Decision Making . Center for Marine Conservation. Washington. Noske, R. A. 1995. The ecology of mangrove forest birds in Peninsular Malaysia. Ibis 137: 250-263. Occhipinti-Ambrogi, A., & Savini, D. 2003. Biological invasions as a component ofglobal change in stressed marine ecosystems. Marine Pollution Bulletin 46: 542-55l. Odor, R. K. 1992. Big squid in big currents. South African

Journal of Marine Science-Suid-Afrikaanse Tydskrif Vir Seewetenskap 12: 225-235. Ojeda, F. F., & Santilices, B. 1984. Ecological dominance of Lessonia nigriscens (Phaeophyta) in Central Chile. Marine Ecology Progress Series 19: 83-9l. Oliver, J., & Babcock, R. 1992. Aspects of the fertilization ecology of boradcast spawning corals-sperm dilution effects and in situ measurements offertilization . Biological Bulletin 183: 409-417. Olsen, R. E., Henderson, R. J.• Sountama, J., Hemre, G-I. Ringe, E., Melle, W. et al. 2004 Atlantic salmon, Salmo salar, utilizes wax ester-rich oil from Calanus finmarchicus effectively. Aquaculture 240: 433-449. Olsgard, F., & Gray, J. F. 1995. A comprehensive analysis of

the effects of offshore oil and gas exploration and production on the benthic communities of the Norwegian continental shelf. Marine Ecology Progress Series 122 : 277-306. Olu, K., Duperret, A., Sibuet, M., Foucher, J. -P., & FialaMedioni, A. 1996. Structure and distribution of cold seep communities along the Peruvian active margin: relationship to geological and fluid patterns. Marine Ecology Progress Series 132: 109-125. Orr. J. c., Fabry. V. J.• Aumont, 0 ., Bopp, L.. Doney. S. C.• et a1. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686. Orth, R. J., Luckenback, M., & Moore, K. A. 1994. Seed dispersal in a marine macrophyte: implications for colonization and restoration. Ecology 75 : 1927-39. Pabi, S., van Dijken, G. 1.., & Arrigo, K. R. 2008 Primary production in the Arctic Ocean, 1998-2006. Journal of Geophysical Research 113: C08005, 10.1029/2007JC004578. Pace, M. 1.., Cole, J. J., Carpenter, S. R., & Kitchell, J . F. 1999. Trophic cascades revealed in diverse ecosystems . Trends in Ecology and Evolution 14: 483-8. Paerl, H. W. 1995. Coastal eutrophication in relation to atmospheric nitrogen deposition: current perspectives. Ophelia 41 : 237-59. Paine. R. T. 1974. Intertidal community structure, experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15: 93-120. Paine, R. T. 1980. Food webs: linkage, interaction strength and community infrastructure. Journal of Animal Ecology49: 667-85. Palmer, M. A., Reidy Liermann, C. A., Nilsson, c., Florke, M., Alcamo, J ., Lake, P. S., & Bond, N. 2008. Climate change and the world's river basins: anticipating management options. Frontiers in Ecology and Environment 6: 81-89. Palmisano. A. C., & Garrison. D. L. 1993. Microorganisms in Antarctic sea ice. In E. I. Friedman (ed .) .AntarcticMicrobiology. Wiley-Liss Inc., New York, pp. 167-218. Pandolfi, J . M. 1999. Responses of Pleistocene coral reefs to environmental change over long temporal scales.American Zoologist 39 : 113-30. Parkinson, C. L. 2004. Southern Ocean sea ice and its wider linkages: insights revealed from models and observations.AntarcticScience 16: 387-400. Pastoors, M. A., Rijnsdorp, A. D., & Van Beek, F. A., 2000. Effects ofa partially closed area in the North Sea ("plaice box") on stock development of plaice. ICES Journal of Marine Science 57: 1014-1022. Paterson, D. M., & Black, K. S. 1999. Water flow, sediment dynamics and benthic ecology. Advances in Ecological Research 29: 155-93.

References Paul, J. Scholin, C., Van den Engh, G., & Perry, M.J. 2007. In situ instrumentation. Oceanography 20: 70-78. Paulay, G. 1997. Diversity and distribution of reef organisms.ln C. Birkeland (ed.), Life and Death ofCoral Reefs. Chapman & Hall, New York, pp. 298-353. Pauly, D., & Christensen, V. 1995. Primary production required to sustain global fisheries. Nature 374: 255-257. Pauly, D., & MacLean, J . 2003. In a Perfect Ocean. The State

of Fisheries and Ecosystems in the North Atlantic Ocean. Island Press, Washington. Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., & Torres, F. 1998. Fishing down marine food webs. Science 279: 860-3. Pauly, D., Watson, R., & Alder, J. 2005 . Global trends in world fisheries : impacts on marine ecosystems and food security. Philosophical Transactions ofthe Royal Society B 360: 5-12. Paytan, A., Mackey, K. R. M., Chen, Y., Lima, I. D., Doney, S. c., Mahowald, N. et al. 2009. Toxicity of atmospheric aerosols on marine phytoplankton. Proceedings of the National Academy ofSciences USA 106: 4601-4605. Pearre, S. 2003. Eat and run? The hunger/satiation hypothesis in vertical migration: history, evidence and consequences. Biological Reviews 78: 1-79. Pearson, T., & Rosenberg, R. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology: An Annual Review 16: 229-311. Pechenik, J . A. 1999. On the advantages and disadvantages oflarval stages in benthic marine invertebrate life cycles. Marine Ecology Progress Series 177: 269-297. Peck, I.. S, Convey, P., & Barnes, D. K. A. 2006. Environmental constraints on life histories in Antarctic ecosystems: tempos, timings and predictability. Biological Reviews 81 : 75-109. Pedr6s-Ali6, C. 2006. Marine microbial diversity: can it be determined? Trends in Microbiology 14: 257-262. Pennings, S., & Callaway, R. 1992. Salt marsh plant zonation : the relative importance ofcompetition and physical factors. Ecology 73: 681-690. Pennings, S. C., Siska, E. 1.., & Bertness, M. D. 2001. Latitudinal differences in plant paltability in Atlantic coast salt marshes. Ecology 82: 1344-1359. Pennings, S. C., Ho, C. -K., Salgado, C. S.• Wil(ski. K.. Dave, N., Kunza, A. E., & Wason, E. I.. 2009. Latitudinal variation in herbivore pressure in Atlantic Coast salt marshes. Ecology 90: 183-195. Pergent, G., Boudouresque, C-F., Dumay, 0 .. PergentMartini, C., & Wyllie-Echeverria, S. 2008. Competition between the invasive macrophyte Caulerpa taxifolia and the seagrass Posidonia oceanica: contrasting strategies. BMC Eco18: 20 doi: 10.1186/1472-6785-8-20. Pershing, A. J., Wiebe, P. H., Manning, J. P., & Copley, N. J . 2001 . Evidence for vertical circulation cells in the well-

mixed area of Georges Bank and their biological implications. Deep-Sea Research Part II - Topical Studies in Oceanography 48: 283-310. Petchey, O. 1.., & Belgrano, A. 2010 Body-size distributions and size-spectra:universal indicators ofecological status? Biology Letters 6: 434-437. Peterman. R. M. 1990. Statistical power analysis can improve fisheries research and management. Canadian Journal of Fisheries and Aquatic Sciences 47: 2-15. Petersen, C. J . 1914. Valuation of the sea. ll. The animal communities of the sea bottom and their importance for marine zoogeography. Report ofthe Danish. Biological Station 21. Peterson, C. H., & Black, R. 1987. Resource depletion by active suspension feeders on tidal flats, influence of local density and tidal elevation. Limnology and Oceanography 32: 143-66. Peterson, C. H., & Black, R. 1988. Density-dependent morrality caused by physical stress interacting with biotic history.American Naturali5t 131: 257-70. Pethick J . 2001. Coastal management and sea-level rise. Catena 42: 307-322. Petz, W., Song, W., & Wilbert, N. 1995. Taxonomy and ecology of the ciliate fauna (Protozoa, Ciliophora) in the endopagial and pelagial of the Weddell Sea, Antarctica. Stapfia 40: 1-223. Pfeiffer, T. J., & Freeman, D. W. 2004. The effects of water temperature on sock grading of sub-marketable catfish, Ictalurus punctatus, in earthen ponds. J. AppliedAquaculture 16: 95-103. Phillips, M. J., Lin, C. K., & Beveridge, M. C. M. 1993. Shrimp culture and the environment: lessons from the world's most rapidly expanding warm water aquaculture sector. In Anon. (ed.), Environment and Aquaculture in Developing Countries. ICLARM Conference Proceedings. Manila, Philippines. Phillips, B., Ward, T., & Chafee, C. 2003. Eco-LabeUing in Fisheries: What Is ItAIIAbout? Blackwell Publishing. Oxford. Pickett, S. T. A., & White, P. S. 1985. Patch dynamics: a synthesis.ln S. T. A. Pickett, & P. S. White (eds), The Ecology of NaturalDi5turbance and Patch Dynamics. Academic Press, New York, pp. 371-84. Pifia-Ochoa, E., Hegslund, S., Geslin, E., Cedhagen, T., Revsbech, N. P., Nielson, I.. P. et al. 2010. Widespread occurrance of nitrate storage and denitrification among foraminifera and gromiida. Proceedings of the Natural Academy of Sciences of the United States ofAmerica 107: 1148-1153. o Pinhassi, J.• & Hagstrom A. 2000. Seasonal succession in marine bacterioplankton. Aquatic Microbial Ecology 21 : 245-256. Pitcher, T. J., & Hart, P. J. B. 1982. Fisheries Ecology. Croom Helm, Beckenham. Pitcher, T. J., Kalikoski, D., Short, K., Varkey, D., & Pramod,

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

G. 2009. An evaluation of progress in estimating ecosystem-based management of fisheries in 33 countries. Marine Policy 33: 223-232. Platt, T., Fuentes-Yaco, C., & Frank, K. T. 2003. Spring algal bloom and larval fish survival. Nature 423: 398-9. Pollard, R. T., Salter, I., Sanders, R. J ., Lucas, M.I., Moore, C. M., Mills, R. A. et al. 2009. Southern Ocean deep-water carbon export enhanced by natural iron fertilization . Nature 457: 577-581. Polunin, N. V. C. 1996. Trophodynamics of reef fisheries productivity.ln N. V. C. Polunin & C. M. Roberts (eds), Reef Fisheries. Chapman & Hall, London, pp. 113-35. Pomeroy, I.. R. 1974. The ocean's food web, a changing paradigm. Bioscience 24: 499-504. Pommier, T.• Bostrom, K' Canback, B.• Lundberg, P.• Riemann, 1.., Simu, K. et al. 2007. Global patterns ofdiversity and community structure in marine bacterioplankton. Molecular Ecology 16: 867-880. Pongthanapanich, T. 1996. Econotttic study suggests management guidelines for mangroves to derive optimal economic and social benefits. AquacultureAsia 1: 16-17. Posey, M. H. 1986. Changes in a benthic community associated with dense beds of a burrowing deposit feeder Callianassa californiensis. Marine Ecology Progress Series 31 : 15-22. Post, D. M., Taylor, J . P., Kitchell, J. E, Olson, M. H., Schindler, D. E., & Herwig, B. R. 1998. The role of tttigratory waterfowl as nutrient vectors in managed wetlands. Conservation Biology 12: 910-20. Pratchett, M.• Munday. P., Wilson. S., Graham, N.• Cinner, J., Bellwood, D. et al. 2008. Effects of climate-induced coral bleaching on coral-reef fishes ecological and economic consequences. Oceanography and Marine Biology: An Annual Review 46: 251-296. Preen, A. R. 1995. Impacts of dugong foraging on seagrass habitats: observational and experimental evidence of cultivation grazing. Marine Ecology Progress Series 124: 201-213. Priede, I. G., and Miller, P.1. 2009. A basking shark (Cetorhinus maximus) tracked by satellite together with simultaneous remotesensing II: New analysis reveals orientation to a thermal front. Fisheries Research 95: 370-372. Priede, I. G., Bagley, P., Armstrong, J. D., Smith, K. 1.., Jr., & Merrrett, N. R. 1991. Direct measurement of active dispersal of food-falls by abyssal demersal fishes. Nature 351 : 647-649. Priscu, J. C., Priscu, L. R.• Palmisano. A. C., Sullivan. C. W. 1990. Estimation of neutral lipid levels in Antarctic sea ice microalgae by nile red fluorescence. Antarctic Science 2: 149-155. Purcell, E. M. 1977. Life at low Reynolds' number. American Journal ofPhysics 45: 3-11 . Purkhold D., Pommerening-Roser A., Juretschko S., Schmid M. C., Koops H-P., & Wagner M. 2000. Phylogeny of all J

recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Applied and Environmental Microbiology 66: 5368-5382. Raffaelli, D. G. 2006. Biodiversity and ecosystem functioning: issues of scale and trophic complexity. Marine Ecology Progress Series 311 : 285-294. Raffaelli, D. G., & Hall, S. J . 1992. Comparttnents and predation in an estuarine food web. Journal ofAnimal Ecology 61 : 551-60. Raffaelli, D. G., & Hawkins, S. J . 1996. Intertidal Ecology. Chapman & Hall, London. Raffaelli, D. G., & Moller, H. 2000. Manipulative experi-

ments in animal ecology-do they promise more than they can deliver? Advances in Ecological Research 30 : 299-330. Raffaelli, D. G., & S. J . Hall 1992. Comparttnents and predation in estuarine food web. Journal ofAnimal Ecology 61 : 551-560. Raffaelli, D. G., & S. J . Hall 1995. Assessing the relative importance of trophic links in food webs. In: Food Webs: Patterru; and Process. Chapman and Hall, pp. 185-191. Raffaelli, D. G., Conacher, A., McLachlan, H ., & C. Emes

1989. The role of epibenthic crustacean predators in an eatuarine food web. Est. Coast. ShelfSci., 28: 149-160. Raffaelli, D. G., Karakassis, I., & Galloway, A. 1991. Zonation schemes on sandy shores: a multivariate approach. Journal ofExperimental Marine Biology and Ecology 148: 241-53. Raffaelli, D. G., Raven, J ., & Poole, I.. 1998. Ecological impact of green macroalgal blooms. Annual Reviews in Marine Biology and Oceanography 36: 97-125. Ragnarsson, S., &D. G. Raffaelli 1999. Effects of the mussel Mytilus edulis on the invertebrate fauna of sediments. Journal ofExperimental Marine Biology and Ecology 241 : 31-44. Rahmstorf, S. 2002. Ocean circulation and climate during the past 120,000 years. Nature 419 : 207-14. Ramage, D. 1.., & Schiel, D. R. 1998. Reproduction in the seagrass Zostera novazelandica on intertidal platforms in southern New Zealand. Marine Biology 130: 479-489. Ramsay, K., Kaiser, M. J ., & Hughes, R. N. 1997. A field study of intraspecific competition for food in hermit crabs (Pagurus bernhardus) . Estuarine Coastal and Shelf Science 44: 213-20. Randall, D. J ., & Farrell, A. P. 1997. Deep-sea Fishes, Fish Physiology Series No. 16. Academic Press. Raven J . A. 1995. Photosynthetic and non-photosynthetic roles of carbonic anhydrase in algae and cyanobacteria. Phycologia 34: 93-101. Raven. J. A. 1997. CO 2 concentrating mechanisms: a direct role for thylakoid lumen acidification? Plant, Cell and Environment 20: 147-54. Raven, J . A., & Geider, R. J . 2003. Adaptation, acclimation

References and regulation in algal photosynthesis. In A. W. D. Larkum, S. Douglas, & J . A. Raven (eds), Photosynthesis of Algae. Kluwer Academic Publishers, pp. 385-412. Raven, J ., Caldeira, K., Elderfield, H., Hoegh-Guldberg, 0 ., Liss, P., Riebesell, D. et al. 2005. Ocean acidification due to increasing atmospheric carbon dioxide . Royal Society

of London, Policy Document 12/05. 68pp. Ray, G. C. 1997. Do the metapopulation dynamics ofestuarine fishes influence the stabiliry of shelf ecosystems? Bulletin ofMarine Science 60: 1040-1049. Reid, P. C., Borges, M. D., & Svendsen, E. 2001. A regime shift in the North Sea circa 1988 linked to changes in the North Sea horse mackerel fishery. Fisheries Research 50: 163-71. Reid, P. C., Johns, D. G., Edwards, M., Starr, M., Poulin, M., & Snoeijs, P. 2007. A biological consequence of reducing Arctic ice cover: arrival of the Pacific diatom Neodenticula seminae in the North Atlantic for the first time in

800,000 years. Global Change Biology 13: 1910-1921. Reijnders, I.. 2008. Do biofuels from microalgae beat biofuels from terrestrial plants? Trends in Biotechnology 26 : 349-350. Reise, K. 1985. Tidal Flat Ecology. An ExperimentalApproach to Species Interactions. Springer Verlag, Berlin. Reise, K., Gollasch, S., & Wolff, W. J . 1999. Introduced marine species of the North Sea coasts. Helgolander Meeresuntersuchungen 52 : 219-234. Renewable Energy Centre 2007. £14 Billion Tidal Barrage Proposed for Severn Estuary. Alternative Energy eMag-

azine, August 2007 issue. http:/ /www.altenergymag. com/, Ressurreicao, A., Gibbons, J., Dentinho, T. P., Kaiser, M. J., Santos, R. S., & Edwards-Jones, G. 2010. Economicvaluarion of species loss in the open sea. Ecological Economics doi: 10.101b/j.ecolecon2010.11.009. Reusch, T. B. H., Starn, W. T., & Olsen, J . I.. 1999a. Microsatellite loci in eelgrass Zostera marina reveal marked polymorphism within and among populations. Molecular Ecology 8 : 317-321. Reusch, T. B. H., Bostrom, C., Starn, W. T., & Olsen, J . I.. 1999b. An ancient eelgrass clone in the Baltic. Marine Ecology Progress Series 183: 301-304. Rex, M. A. 1981. Community structure in the deep-sea benthos. Annual Review of Ecology and Systematics 12: 331-353. Rex. M. A., Etter. R. J., Morris. J. S., Crouse, J.• McClain, C. R., Johnson, N. A. et al. 2006. Global bathymetric patterns of standing stock and body size in the deep-sea

benthos. Marine Ecology Progress Series 317: 1-8. Rex, M. A., Stuart, C. T., Hessler, R. R., Allen, J . A., Sanders H. 1.., & Wilson, G. D. F. 1993. Global scale latitudinal patterns of species diversity in the deep-sea benthos.

Nature 365: 636-{j39. Rhoads, D. C. 1974. Organism-sediment relations on the

muddy sea floor. Oceanography and Marine Biology: An AnnualReview 12: 263-300. Rhoads, D. c., & Cande, S. 1971. Sediment profile camera for in situ study of organism-sediment relations. Limnology&Oceanography 16: 110-114. Rhoads, D. c., Boesch, D. F., Tang, Z. -C., Xu, F. -S., Huang, I.. -Q., & Nilsen, K. J . 1985. Macrobenthos and sedimentary facies on the Changjiang delta platform and adjacent continental shelf, East China Sea. Continental Shelf Research 4 : 189-213. Rice, J., & Gislason, H. 1998. Patterns of change in the size spectra of numbers and diversiry of the North Sea fish assemblage, as reflected in surveys and models. ICES Journal of Marine Science 53 : 1214-1225. Richardson, I.. I.. 1998. Coral diseases:what is really known? Trends in Ecology and Evolution 13: 438-443. Richardson, A. J., & Schoeman, D. S. 2004. Climate impact on plankton ecosystems in the Northeast Atlantic. Science 305: 1609-1612. Richardson, E. A., Kaiser M. J ., Edwards-Jones G., & Possingham H. P. 2006. Incorporating socia-economics in marine reserve design: low-resolution data results in expensive mistakes. Conservation Biology 20: 1191-

1202. Richardson, A. J ., Walne, A. W., John, A. W. G., Jonas, T. D., Lindley, J . A., Sims, D. W. et al. 2006. Using continuous plankton recorder data. Progress in Oceanography 68: 27-74. Richardson, A. J ., Bakun, A., Hays, G. c., & Gibbons, M. J. 2009. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future .

Trends in Ecology and Evolution 24: 312-322. Richmond, R. H. 1997. Reproduction and recruitment in corals: critical links in the persistence of reefs. In C. Birkeland (ed. ), Life and Death of Coral Reefs. Chapman & Hall, New York, pp. 175-97. Richmond, A. (ed.) 2004. Handbook of Microalgal Culture. Biotechnoloy and Applied Phycology. Wiley Blackwell, Oxford. Riebesell, D., Schloss, I., & Smetacek, V. 1991. Aggregation of algae released from melting sea ice : implications for

seeding and sedimentation. Polar Biology 11: 239-248. Riebesell, D., Burkhardt, S., Dauelsberg, A., & Kroon, B. 2000a. Carbon isotope fractionation by a marine diatom: dependence on the growth-rate-limiting resource.

Marine Ecology Progress Series 193: 295-303. Riebesell, D.• Zondervan, I.. Rost, B., Tortell, P. D., Zeebe, R. E., & Morel, F. M. M. 2000b. Reduced calcification of marine plankton in response to increased CO 2 , Nature 407: 364-367. Riemann, F., & Sime-Ngando, T. 1997. Note on sea ice nematodes (Monhysteroidea) from Resolute Passage, Canadian High Arctic. Polar Biology 18: 70-75. Riemann, 1.., & Middleboe, M. 2002. Stabiliry of bacterial

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

and viral community compositions in Danish coastal waters as depicted by DNA fingerprinting techniques. Aquatic Microbial Ecology 27: 219-232. Ries, B. R., Cohen, A., McCorkl, D. C. 2009. Marine calcifiers exhibit mixed respomses to C02-induced ocean acidification. Geological Society ofAmerica 37: 1131-1134. Rijnsdorp, A. D., & van Leeuwen, P. I., 1996. Changes in growth of North Sea plaice since 1950 in relation to

density, eutrophication. beam-trawl effort. and temperature.ICESJournal ofMarine Science 53: 1199-1213. Robertson, A. I. 1986. Leaf-burying crabs: their influence on energy flow and export from mixed mangrove forests (Rhizophora spp.) in northeastern Australia. Journal of Experimental Marine Biology and Ecology 102: 237-48. Robertson, A. I., Alongi, D. M., & Boto, K. G. 1992. Food chains and carbon fluxes . In A. I. Robertson, & D. M. Alongi (eds), Tropical Mangrove Ecosystems . American Geophysical Union, NY, pp. 293-326. Robinson, C., & Williams, P. J . Ie B. 2005. Respiration and its measurement in surface marine waters. In P. A. del Giorgio, & P. J . Ie B. Williams (eds), Respiration in AquaticEcosystems. Oxford University Press, Oxford, pp. 147-80. Robison, B. H. 2004. Deep pelagic biology. Journal ofExperimentalMarine Biology and Ecology 300: 253-272. Rochet, M. -J., & Trenkel, V. M., 2003. Which community indicators can measure the impact of fishing? A review and proposals. Canadian Journal ofFisheries andAquatic Sciences 60: 86-99. Rochette, R., Tetreault, F., & Himmelman, J. H. 2001. Aggregation of whelks. Buccinum undatum. near feeding predators: the role of reproductive requirements. Animal Behaviour 61 : 31-41 . Rodhouse, P. G., Elvidge, C. D., & Trathan, P. N. 2001. Remote sensing of the global light-fishing fleet: An analysis of interactions with oceanography, other fisheries and predators. Advances in Marine Biology 39: 261-303. Roelke, D. 1.., & Buyukates, Y. 2002. Dynamics of phytoplankton succession couplesd to species diversity as a system-level tool for study of Microcystis population dynamics in eutrophic lakes . Limnology and Oceanography47: 1109-18. Rogers, A. D. 2000. The role of the oceanic oxygen minima in generating biodiversity in the deep sea. Deep-Sea

Research Part II - Topical Studies in Oceanography 47: 119-148. Ropert-Coudert, Y., & Wilson, R. P. 2005. Trends and perspectives in animal-attached remote-sensing. Frontiers in Ecology and the Environment 3 : 437-444. Rose, C. D., Sharp, W. c., Kenworthy, W. J., Hunt, J . H., Lyons, W. G., Prager, E. J . et aI. 1999. Overgrazing of a large seagrass bed by the sea urchinLytechinus variegatus in outer Florida bay. Marine Ecology Progress Series 190: 211-22.

Rosenberry, R. 1994. World shrimp farming 1994. Annual Report. Shrimp News International, San Diego, California, USA. Ross, K.A., Thorpe, J . P., & Brand A. R. 2004 Biological control offouling in suspended scallop cultivation.Aquaculture 229 : 99-116. Rossello-Mora, R., & Amann R. 2001. The species concept for prokaryotes. FEMS Microbiology Reviews 25 : 39-67. Rothrock, D. A., & Zhang, J . 2005. Arctic Ocean sea ice volume : what explains its recent depletion? Journal of Geophysical Research, 110, COlO02, 10. 1029/ 2004JC002282. Rountree, R. A., & Able, K. W. 2007. Spatial and temporal habitat use patterns for salt marsh nekton: implications for ecological function. AquaticEcology 41 : 25-45. Rowden, A. A., Jones, M. B., & Morris, A. W. 1998. The role of Callianassa subterranea (Montagu) (Thalassinidia) in sediment resus pension in the North Sea. Continental ShelfResearch 18: 1365-1380. Roy, K., Jablonski, D., Valentine, J . W., & Rosenberg, G. 1998. Marine latitudinal diversity gradients : tests of causal hypotheses. Proceedings of the National Academy ofSciences USA 95: 3699-3702. Rudnick, D. 1.., & Davis, R. E. 2003. Red noise and regime shifts. Deep-Sea Research Part I- Oceanographic Research Papers 50: 691-9. Rusch, D. B., Halpern, A. 1.., Sutton, G., Heidelberg, K. B., Williamson, S., Yooseph, S. et al. 2007. The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific. PLoS Biology (USA: PublicLibraryofScience) 5: e77. doi: 10.1371/journaI. pbio. 0050077. Russ, G. R., & Alcala, A. C. 1996. Do marine reserves export adult fish biomass- evidence from Apo Island, Central Philippines. Marine Ecology Progress Series 132: 1-9. Russell, G., & Veltkamp, C. J . 1984. Epiphyte survival on skin-shedding macrophytes. Marine Ecology Progress Series 18: 149-53. Russell, G., Hawkins, S. J ., Evans, I.. c., Jones, H. D., & Holmes, G. D. 1983. Restoration of a disused dock basin as a habitat for marine benthos and fish. Journal ofApplied Ecology 20: 43-58. Ruxton, G. D., & Houston, D. C. 2004. Energetic feasibility of an obligate marine scavenger. Marine Ecology Progress Series 266: 59-63. Ryther, J. H. 1969. Potential productivityofthe sea. Science 130: 602-608. Sabine, C. 1.., Feely, R. A., Gruber, N., Key, R. M., Lee, K., Bullister, J . I.. et aI. 2004. The oceanic sink for anthropogenic CO,. Science 305 : 367-371 . Sainsbury, J. C. 1996. Commercial fishing methods: an introduction to vessels and gears. Fishing News Books, Oxford. Saintilan, N. 1997. Above- and below-ground biomasses of

References two species of mangrove on the Hawkesbury River estuary, New South Wales . Marine and Freshwater Research 48: 147-52. Sale, P. F. (ed.) 2002 . Coral ReefFishes: Dynamics and Diversity in a Complex Ecosystem . Academic Press, San Diego. Sale, R. 2006. A complete Guide to Arctic Wildlife. Christopher Helm, London. Salvat, B. 1964. Les conditions hydrodynamiques interstitielles des sediments meubles intertidaux et la repartition verticale de la faune endognee. C. R Acad. Sci. Paris 259: 1576-1579. Sandee, P., Gamborg, c., Kadri, S., & Millar, K. 2009 Balancing the needs and preferences ofhumans against concerns for fish : how to handle the emerging ethical discussions regarding capture fisheries? Journal ofFish Biology 75: 286-287. Sarmiento, J. L., Gruber, N., Brzezinski, M., & Dunne, J. P. 2004. High-latitude controls of thermocline nutrients and low latitude biological productivity. Nature 427: 56-60. Sarrazin, J ., & Juniper, S. K. 1999 Biological characteristics of a hydrothermal edifice mosaic community. Marine Ecology Progress Series 185: 1-19. Sathivel, S. 2002 Production, process design and quality characteristics of catfish visceral oil. Dissertation Abstracts International Part B: Science and Engineering, Vol. 63. Louisiana State University, Baton Rouge . Scanlan, D. J ., & West, N. J . 2002. Molecular ecology of the marine cyanobacterial genera Prochlorococcus and Synechococcus. FEMS Microbiology Ecology 40: 1-12. Schafer, W. 1972. Ecology and Palaeoecology ofMarine Environments. University of Chicago Press, Chicago. Scheffer, M., Carpenter, S., Foley, J . A., Folkes, C., & Walker, B. 2001. Catastrophic shifts in ecosystems. Nature 413 : 591-6. Schiermeier, Q. 2007. The new face of the Arctic. Nature 446: 133-135. Schmittner, A. 2005. Decline of the marine ecosystem caused by a reduction in the Atlantic overturning circulation. Nature 434: 628-633. Schnack-Schiel, S. 2003. The macrobiology of sea ice. In D. N. Thomas, & G. S. Dieckmann (eds), Sea Ie-An Introduction to its Physics, Chemistry, Biology and Geology. Blackwells Publishing. Oxford. Schnack-Schiel, S. B., Dieckmann, G. S., Gradinger, R., Melnikov, I. A., Spindler, M., & Thomas, D. N. 2001. Meiofauna in sea ice of the Weddell Sea (Antarctica) . Polar Biology 24: 724-728. Schoernann, V., Becquevort, S. Stefels, J., Rousseau, V., & Lancelot, C. 2005. Phaeocystis blooms in the global ocean and their controlling mechanisms : a review. Journal ofSea Research 53 : 43-66. Schofield, 0 ., Bergmann, T., Bissett, P., Grassle, J . F., Haidvogel, D. B., Kohut, J. et al. 2002. The long-term eco-

system observatory: An integrated coastal observatory. IEEE Journal ofOceanic Engineering 27: 146-54. Schwamborn, R., Ekau, W., Voss, M., & Saint-Paul, U. 2002. How important are mangroves as a carbon source for decapod crustacean larvae in a tropical estuary? Marine Ecology Progress Series 229: 195-205. Schwinghamer, P., Hargrave, B., Peer, D., & Hawkins, C. M., 1986. Partitioning of production and respiration among size groups of organisms in an intertidal benthic community. Marine Ecology Progress Series 31 : 131-142. Seibel, B. A., Thuesen, E. V., & Childress, J. J . 2000. Lightlimitation on predator-prey interactions: Consequences for metabolism and locomotion of deep-sea cephalopods. Biological Bulletin 198: 284-98. Sepkoski, J . J ., McKinney, F. K., & Lidgard, S. 2000. Competitive displacement among post-Paleozoic cyclostome and cheilostome bryozoans. Paleobiology 26: 7-18. Serreze, M. c., Holland, M. M., & Stroeve,J., 2007. Perspectives on the Arctic's shrinking sea-ice cover. Science 315 : 1533-1536. Sheldon, R. W., Prakash, A., & Sutcliffe, W. H. 1972. The size distribution of particles in the ocean. Limnology and Oceanography 17: 327-40. Sheppard, C. R. C. 2003. Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 425 : 294297. Sheppard, C. R. C., Price, A., & Roberts, C. M. 1992. Marine Ecology of the Arabian Region. San Diego: Academic Press . Short, F. T., Burdick, D. M., & Kaldy, J . E. 1995. Mesocosm experiments quantify the effects of eutrophication on eelgrass, Zostera marina. Limnology and Oceanography 40: 740-9. Shpigel, M., Neori, A., Popper, D. M., & Gordin, H. 1993. A proposed model for 'environmentally clean' land-based culture of fish, bivalves and seaweeds. Aquaculture 117: 115-28. Shucksmith R., Hinz H., Bergmann M., & Kaiser M. J . 2006. Using video surveys to evaluate critical habitat features for adult plaice (Pleuronectes platessa L.) . Journal ofSea Research 56: 317-328. Sievert, S. M., Kienne, R. P., & Schulz-Vogt, H. N. 2007. The sulfur cycle. Oceanography 20: 117-123. Sims, D. W., Southall, E. J., Humphries, N. E., Hays, G. C., Bradshaw, C. J . A., Pitchford, J. W. et al. 2008. Scaling laws of marine predator search behaviour. Nature 451 : 1098-Ul095. Skei, J., Larsson, P., Rosenberg, R., Jonsson, P., Olsson, M., & Broman, D. 2000. Eutrophication and contaminants in aquatic ecosystems. Ambio 29 : 184-94. Smale, M. J ., Roel, B. A., Badenborst,A., & Field, J . G. 1993. Analysis of the demersal community offish and cephalopods on the Agulhas Bank, South Africa. Journal ofFish Biology 43 : 169-191.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Smart, C. W., & Gooday, A. J. 1997. Recent benthic foraminifera in the Abyssal northeast Atlantic Ocean: Relation

to phytodetrital inputs. Journal ofForiminiferal Research 27: 85-92. Smayda, T. J. 1990. Novel and nuisance phytoplankton bolloms in the sea: evidence for a global epidemic. In E. Graneli, B. Sundstom, L. Edler, & D. M. Anderson (eds), Toxic Marine Phytoplankton. Elsevier, Amsterdam, pp. 29-40. Smetacek, V. 2008 Are declining Antarctic krill stocks a result of global warming or the decimation of the whales? In: The Impact of Global Warming on Polar Ecosystems (ed. C. Duarte). Fundacion BBVA, Spain, pp. 46-83. Smetacek, V., & Cloern, J. E. 2008. On Phytoplankton trends. Nature 319: 1346-1348. Smetacek, V., & Nicol, S. 2005. Polar ocean ecosystems in a

changing world. Nature 437: 362-368. Smetacek, V., & Passow, U. 1990. Spring bloom initiation and Sverdrup's critical-depth model. Smith, T. J . 1992. Forest Structure. In A. I. Robertson, & D. M. Alongi (eds), Tropical Mangrove Ecosystems, American Geophysical Union, New York, pp. 101-36. Smith, T. D. 1994. Scaling Fisheries: The Science of Measuring the Effeet5 of Fishing, 1855-1955. Cambridge: Cambridge University Press. Smith, C. R., & Baco, A. R. 2003. Ecology of whale falls at the deep-sea floor. Oceanographyand Marine Biology 41 : 311-354. Smith, T. J. 111. 1992. Forest Structure. In: Robertson, A. L., Alongi, D. N. Tropical Mangrove Ecosystems American Geophysical Union, Washington D.C. pp. 101-136. Smith, T. J., Boto, K. G., Frusher, S. D., & Giddins, R. L. 1991 . Keystone species and mangrove forest dynamics: the influence of burrowing by crabs on soil nutrient sta-

tus and forest productivity. Estuarine Coastal and Shelf Science 33: 419-32. Smith, R. C., Prezelin, B. B., Baker, K. S., Bidigare, R. R., Boucher, N. P., Coley, T. et al. 1992. Ozone depletionultraviolet-radiation and phytoplankton biology in antarctic waters. Science 255 : 952-959. Smith, I. P., Jensen, A. C., Collins K. J., & Mattey, E. L. 2001. Movement of wild European lobsters Homarus gammarus in natural habitat. Marine Ecology Progress Series 222: 177-86. Snelgrove, P., & Butman, C. 1994. Animal-sediment relationships revistied: cause versus effect. Oceanography and Marine Biology:An Annual Review 32: 111-177. Snowdon, P. et al. 2000. Synthesis of allometries, review of root biomass and design of future woody biomass sampiing strategies. Australian Greenhouse Office, Report No. 17. Solan. M., Germano. J.• Rhoads. D., Smith, c.. Michaud, E.• Parry, D. et al. 2003. Towards a greater understanding

of pattern. scale and process in marine benthic systems: a picture is worth a thousand worms. Journal ofExperimental Marine Biology and Ecology 285-286: 313-338. Solan, M., Cardinale, B. J., Downing, A. L., Engelhardt, K. A. M., Ruesink, J. L., & Srivastava, D. S. 2004. Extinction and ecosystem function in the marine benthos. Science 306: 1177-1180. Soloman, S. 2007. CO2 storage. The Bellona Foundation. Fact sheet: CO2 Storage. Oslo, Norway. http:/ /www.bellona.org/factsheets/1191921304.33. Somerfield, P. J., Olsgard, F., & Carr, M. 1997. A further examination of two new taxonomic distinctness measures. Marine Ecology Progress Series 154: 303-306. Sommer, U. (ed.) 1989. Plankton Ecology. Springer Verlag, Berlin. Sommer, U., Stibor, H.• Katechakis, A., Sommer. F.. & Hansen, T. 2002. Pelagic food web configurations at different levels of nutrient richness and their implications for the ratio fish production: primary production. Hydrobiologia 484: 11-20. Sendergaard, M., & Thomas, D. N. (eds.) 2004. Dissolved

Organic Matter (DOM) in Aquatic Ecosystems: A Study of European Catchments and Coastal Waters . The Domaine Project, Hillered, Denmark. 74pp. Sereide, J. E., Leu. E., Berge. J.• Graeve, M.• and FalkPetersen, S. 2010. Timing of blooms, algal food quality and Calanus glacialis reproduction and growth in a changing Arctic. Global Change Biology: doi : 10.1111/j.13652486.2010.02175.x. Sousa, W. P., Quek, S. P., & Mitchell, B. J. 2003. Regeneration of Rhizophora mangle in a Caribbean mangrove forest: interacting effects of canopy disturbance and a stem-boring beetle. Oecologia 137: 436-445. Southward, A., & Southward, E. 1978. Recolonization of rockey shores in Cornwall after use of toxic dispersants to clean up the Torrey Canyon spill. Journal ofthe Fisheries Research Board ofCanada 35: 682-706. Spalding, M. D., Ravilious, c., & Green, E. P. 2001. World Atlas ofCoral Reefs. University of California Press, Berkeley. Spindler, M. 1994. Notes on the biology of the sea ice zones in the Arctic and Antarctic. Polar Biology 14: 319-24. Spurgeon, J . P. G. 1992. The economic valuation of coral reefs. Marine Pollution Bulletin 24: 529-36. Squire. V. A., Dugan, J. P., Wadhams, P.• Rottler, P. J.• & Liu, A. K. 1995. Of ocean waves and sea-ice. Annual Reviews ofFluid Mechanics 27: 115-68. Stanhope, M. J ., Hartwick, B., & Baillie, D. 1993. Molecular phylogeographic evidence for multiple shifts in habitat preference in the diversification ofan amphipod species. Molecular Ecology 2: 99-112. Stefels, J., Steinke, M.• Turner, S., Malin. G.• & Belviso, S. 2007. Environmental contraints on the production and removal of the chemically active gas dimethylsulphide

References (DMS) and implications for ecosystem modeling. Biogeochemistry 83: 245-275. Stehli, F. G., & Wells, J . W.1971 . Diversity and age patterns in hermatypic corals. Systematic Zoology 20: 115-26. Steneck, R. S.• Graham. M. H., Bourque, B. J., Corbett. D.• Erlandson, J . M., Estes, J . A., & Tegner, M. J . 2002. Kelp forest ecosystems: biodiversity. stability. resilience and future. Environmental Conservation 29: 436-59. Stephenson, T. A., & Stephenson, A. 1949. The universal features of zonation between tidemarks on rocky coasts. Journal ofEcology 38: 289-305. Stephenson, T. A., & Stephenson, A. 1972. Life Between Tidemarks on Rocky Shores . W. H. Freeman, San Francisco. Stewart. G. B.. Kaiser. M. J'J Cote. I. M.• Halpern, B. S., Lester, S. E., Bayliss, H. R., & Pullin A. S. In press. Evaluating the effectiveness of temperate marine reserves exposes critical knowledge gaps. Conservation Letters 2 : 243-253. Stirling, I. 1998. Polar Bears. The University of Michigin Press, Ann Arbor, Michigan, USA. Stirling, I., & Parkinson, C. L. 2006. Possible effects of climate warming on selected populations of polar bears (Ursus maritimus) in the Canadian Arctic. Arctic 59 : 261-275. Stoddart, D. R. 1984. Coral reefs of Seychelles and adjacent regions. In D. R. Stoddart (ed.), Biogeography and Ecology ofthe Seychelles Islands. Dr W Junk, The Hague, pp. 63-81. Stoecker, D. K. 1999. Mixotrophy among dinoflagellates. Journal ofEukaryotic Microbiology 46: 397-401. Stramma, L., Johnson, G. c., Sprintall, J., & Mohrholz, V. 2008. Expanding oxygen-minimum zones in the tropical oceans. Science 320: 655-658. Strass, V. H., & Nothig, E. -M. 1996. Seasonal shifts in ice edge phytoplankton blooms in the Barents Sea related to the water column stability. Polar Biology 16: 409-22. Stroeve, J., Holland. M. M., Meier. W., Scarnbos, T.. & Serreze, M. 2007. Arctic sea ice decline: faster than forecast. Geophysical Research Letters 34: L09501, doi: 10.1029/2007GL029703. Strom, S. L. 2000. Bactivory: interactions between Bacteria and their Grazers. In D. L. Kirchman (ed.), Microbial Ecology ofthe Oceans. John Wiley & Sons, Inc. New York, Chapter 12, pp. 351-86. Struder-Kypke, M. c., & Montagnes, D. J . S. 2002. Development ofweb-based guides to planktonic protists. Aquatic Microbial Ecology 27: 203-7. Strzepek, R. F., and Harrison, P. J . 2004. Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431 : 689-692. Subasinghe, R., Soto, D., & Jia, J . 2009 Global aquaculture and its role in sustainable development. Reviews inAquaculture 1: 2-9. Suchanek, A. 1992. Extreme biodiversity in the marine envi-

ronment: mussel bed communities of Mytilus californianus. Northwest Environ. J. 8: 150-152. Suggett, D. J ., Oxborough, K., Baker, N. R., Maclntyre, H. L., Kana, T. M., & Geider, R. J . 2003. Fast repetition rate and pulse amplitude modulation chlorophyll-a fluorescence measurements for assessment of photosynthetic electron transport in marine phytoplankton. European Journal of Phycology 38: 371-84. Sutherland, W. J. 1996. FromlndividualBehaviourtoPopulation Ecology. Oxford University Press, Oxford. Sutherland, W. J . (ed.) 1998. Conservation Science and Action. Blackwell, Oxford. Suttle C. A. 2005. Viruses in the sea. Nature 437: 356-361. Svanstad, T., & Kristiansen, T. S. 1990. Enhancement studies of coastal cod in western Norway. Part II. Migration of reared coastal cod. Journal du Conseil International pour l'Exploration de la Mer 47: 13-22. Sverdrup, H. U. 1953. On conditions for the vernal blooming of phytoplankton. Journal du Conseil International pour l'Exploration de laMer 18: 237-295 . Takahashi, T. et al. 2009. Climatological mean and decadal change in surface ocean peo2 • and net sea-air CO2 flux over the global oceans. Deep-Sea Research, Part II 56: 554-577. Tanaka, M., & Nandakumar, K. 1994. Measurement of the degree of intransitivity in a community of sessile organisms. Journal ofExperimental Marine Biology and Ecology 182: 85-95. Tarling, G. A. 2003. Sex-dependent diel vertical migration in northern krill Meganyctiphanes norvegica and its consequences for population dynamics. Marine Ecology Progress Series 260: 173-88. Taylor, A. H., & Gangopadhyay, A. 2001. A simple model of interannual displacements of the Gulf Stream. Journal of Geophysical Research - Oceans 106: 13849-13860. Tedengren, M., Andre, c., Johannesson, K., & Kautsky, N. 1990. Genotypic and phenotypic differences between Baltic and North Sea populations of Mytilus edulis evaluated through reciprocal transplantations. Ill. Physiology. Marine Ecology Progress Series 59: 221-229. Tegner, M. J., & Dayton, P. K. 2000. Ecosystem effects offishing in kelp forest communities. ICES Journal of Marine Sciences 57: 579-589. Thayer, G. W., Bjorndal, K.A., Ogden, J. C., Williams, J . L., & Zieman, J . C. 1984. Role oflarger herbivores in seagrass communities. Estuaries 7: 351-376. Theil, H., & Schriever, G. 1990. Deep-sea mining, environmental impact and the DlSCOL project. Ambio 19: 24550. Thingstad, F. T. 2000 Control ofbacterial growth in idealized food webs. InD. L. Kirchman (ed) Microbial Ecology ofthe Oceans. John Wiley & Sons Inc. New York pp. 229-260. Thomas, D. N., & Dieckmann, G. S. 2002. Antarctic sea ice-a habitat for extremophiles. Science 295 : 641-644.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Thompson, R. C., Crowe, T. P., & Hawkins, S. J . 2002. Rocky intertidal communities: past environmental changes, present status and predictions for the next 25 years. Environmental Conservation 29: 168-191. Thompson, D., Moss, S. E. W., & Lovell, P. 2003. Foraging behaviour of South American fur seals Arctocephalus australis: extracting fine scale foraging behaviour from satellite tracks. Marine Ecology Progress Series 260 : 285-296. Thompson, R. c., Olsen, Y., Mitchell, R. P., Davis, A., Rowland, S. J ., John, A. W. G. et al. 2004. Lost at sea: Where is all the plastic? Science 304: 838-838. Thorpe, S. E., Heywood, K. J., Stevens, D. P., & Brandon, M. A. 2004. Tracking passive drifters in a high resolu-

tion ocean model: implications for interannual variability of larval krill transport to South Georgia. Deep-Sea Research Part I - Oceanographic Research Papers 51 : 909-20. Thorpe, S., Landeghem, K., Hogan, L., & Holland, P. 1997. Economic Effects on Australian Southern Bluefin Tuna Farming ofa Quarantine Ban on Imported Pilchards. Aus-

tralian Bureau ofAgricultural and Resource Economics. Canberra, Australia. Thorson, G. 1957. Bottom communities. In G. W. Hedgpeth (ed.) Treatise on Marine Ecology and Paleoecology, I Ecology. Geological Society of America, New York, pp. 461-534. Thorson, G. 1971. Life in the Sea. Weidenfield, & Nicholson, London.

Thrush, S. F.• Pridmore, R. D., Hewitt. J. E., & Cummings. V. J . 1991. Impact of ray feeding disturbances on sandflat macrobenthos: do communities dominated by polychaetes or shellfish respond differently? Marine Ecology Progress Series 69: 245-52. Tomlinson, P. B. 1986. The Botany ofMangroves . Cambridge University Press: Cambridge. Treusch, A. H., Leininger. S.• Kletzin, A., Schuster. S. C.• Klenk, H. P., & Schleper, C. 2005. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environmental Microbiology 7: 1985-1995. Trites, A. W., Miller, A. J., Maschner, H. D. G., Alexander, M. A.,Bograd, S. J ., Calder, J . A. et al. 2007. Bottom-up forcing and the decline of Steller sea lions (Eumetopias jubatus) in Alaska: assessing the ocean climate hypothesis. Fisheries Oceanography 16: 46-67. Tsukamoto, K., Nakai, I., & Tesch, W. V. 1999. Do all freshwater eels migrate? Nature 396: 635-636. Tuck, G. N., Polacheck, T., Croxall, J . P., & Weimerskirch, H. 2001 . Modelling the impact of fishery by-catches on albatross populations. Journal of Applied Ecology 38: 1182-96. Tudhope.A. W., Chilcot, C. P., McCulloch, M. T., Cook, E. R., Chappell, J ., Ellam, R. M. et al. 2001. Variability in the EI

Nino-southern oscillation through a glacial-interglacial cycle. Science 291 : 1511-1517. Tumbiolo, M. L., & Downing, J. A., 1994. An empiricalmodel for the prediction of secondary production in marine benthic invertebrate populations. Marine Ecology Progress Series 114: 165-174. Tupper, M., & Boutilier, R. G. 1995. Effects of habitat on settlement. growth. and post-settlement survival of Atlantic cod (Gadus morhua). Canadian Journal ofFi5heries and Aquatic Sciences 52 : 1834-1841. Turchini, G. M., Torstensen, B. E., & Ng, WoK. 2009. Fish oil replacment in fishfish nutrition. Reviews in Aquaculture 1: 10-57. Turner, R. E., & Rabalais, N. N. 1994. Coastal eutrophication nearthe Mississippi River delta. Nature 368: 619. Tweedley, J . R., Jackson, E. L., & Attrill, M. J . 2008. Zostera marina seagrass beds enhance the attachment of the invasive alga Sargassum muticum in soft sediments. Marine Ecology Progress Series 354: 305-309. Uchino, 0., Bojkov, R. D., Balis, D. S., Akagi, K., Hayashi M., & Kajihara, R. 1999. Essential characteristics of the Antarctic-spring ozone decline: Update to 1998. Geophysicol Research Letters 26: 1377-80. Uiblein, F., Lorance, P., Latrouite, D. 2003. Behaviour and

habitat utilisation of seven demersal fish species on the Bay of Biscay continental slope, NEAtlantic. Marine Ecology Progress Series 257: 223- 232. Underwood, A. J . 1978. A refutation of critical tidal levels as determinants of the structure of intertidal communities on British shores. Journal of Experimental Marine Biology and Ecology 33 : 261-76. Underwood, A. J . 1981. Techniques of analysis ofvariance in experimental marine biology and ecology. Oceanographyand Marine Biology:Annual Review 19: 513-605. Underwood, A. J. 1991. Beyond BACI: Experimental designs for detecting human environmental impacts on temporal variations in natural populations. Australian Journal ofMarine and Freshwater Research 42: 569-588. Underwood, A. J . 1997. Experiments in Ecology:Their Design and Interpretation UsingAnalysi5ofVariance . Cambridge University Press. Cambridge. Underwood, A. J ., & Jernakoff, P. 1981. Effects of interactions between algae and grazing gastropods on the structure of a low intertidal algal community. Oecologia 48: 221-233. UNDP 2003. Human Development Report2003. Oxford University Press, New York. US EPA 2002. Inventory of us Greenhouse Gas Emissions and Sinks: 1990-2000. US Environmental Protection Agency, Washington DC. Van der Meer, J ., 2005. Measuring the flow of energy and

matter in marine benthic animal populations. In:Eleftheriou, A., & Mcintyre, A. (eds.), Methodsfor the Study of Marine Benthos. Blackwell Science, Oxford.

References Van Dover, C. L. 2000. TheEcologyofDeep-SeaHydrothermal Vents. Princeton University Press, Princeton, NJ. Van Duren, L. A., & Videler, J .J. 2003. Escape from viscosity: the kinematics and hydrodynamics of copepod foraging and escape swimming. Journal of Experimental Biology 206: 269-279. Van Katwijk, M. M. 2003. Reintroduction ofeelgrass (Zostera marina L.) in the Dutch Wadden Sea: a research overview and management vision. In W. J. Wolff, K Essink, A. Kellerman, & M. A. van Leeuwe (eds), Challenges to the Wadden Sea . Ministry ofAgriculture, Nature Management and Fisheries, The Netherlands, pp. 173-95. Vannini, M., Cannicci, S., & Ruwa, K. 1995. Effect of light intensity on vertical migrations of the tree crab, Sesarma

leptosoma. Journal of Experimental Marine Biology and Ecology 185: 181-189. Vare, L. L., Masse, G., & Belt, S. T. 2010 A biomarker-based reconstruction ofsea ice conditions for the Barents Sea in recent centuries. The Holocene 20: 637-643. Vaughan, D., Marshall, G., Connolley, W., King, J . c., & Mulvaney, R. 2001. Climate change - Devil in the detail. Science 293: 1777-1779. Vaughan, D., Marshall, G., Connolley, W., Parkinson, c., Mulvaney, R., Hodgson, D. et al. 2003. Recent rapid regional climate warming on the Antarctic Peninsula. Climatic Change 60: 243-274. Vaughan, S. 2000. Can Antarctic sea-ice extent be determined from whaling records? Polar Record 36: 345-346. Vaughan, D., & Doake, C. 1996. Recent atmospheric warming and retreat of ice shelves on the Antarctic Peninsula. Nature 379 : 328-331. Verity, P. G., & Smetacek, V. 1996. Organism life cycles, predation, and the structure of marine pelagic ecosystems. Marine Ecology Progress Series 130: 277-93. Verity, P. G., Brussaard, C. P., Nejstgaard, J. C., van Leeuwe, M. A., Lancelot, c., & Medlin, L. K. 2007. Current understanding of Phaeocystis eclogy and biogeochemistry, and perspectives for future research. Biogeochemistry 83: 311-330. Veron, J . E. N. 2000. Corals ofthe World. Australian Institute of Marine Science Townsville. Queensland. Australia. Vincent, W. F., & Roy, S. 1993. Solar ultraviolet-B radiation and aquatic primary production: damage, protection and recovery. Environment Review 1: 1-12. Von der Heyden, S., & Cavalier-Smith, T. 2005. Culturing and environmental DNA sequencing uncover hidden kinetoplastid biodiversity and a major marine clade within ancestrally freshwater Neobodo designis. Interna-

tionalJournal ofSystematic andEvolutionaryMicrobiology 55: 2605-2621. Von Liebig, J . 1842. Chemistry in itsAppliootion to Agriculture and Physiology. Taylor & Walton, London, 409 pp. Voss, M., & Montoya, J. P. 2009. Nitrogen cycle: oceans apart. Nature 461 : 49-50.

Vrijenhoek, R. C., Shank, T., & Lutz, R. A. 1998. Gene flow and dispersal in deep-sea hydrothermal vent animals. Cahiers de Biologie Marine 39 : 363-366. Wallace, M.l., Cottier, F. R., Berge, J., Tarling, G. A., Griffiths, C., & Brierley, A. S. 2010. Comparison ofzooplankton vertical migration in an ice-free and a seasonally ice-covered Arctic fjord : An insight into the influence of sea ice cover on zooplankton behavior. Limnology and Oceanography 55: 831-845. Walsh, J. E. 2009. A comparison of Arctic and Antarctic climate change, present and future. Antarctic Science 21 : 179-188. Walther, G. -R., Post. E., Convey, P.• Menzel, A., Parmesan, c., Beebee, T. J . C. et al . 2002. Ecological response to recent climate change. Nature 416: 389-95. Waluda, C. M., Rodhouse, P. G., Podesta, G. P., Trathan, P. N., & Pierce, G. J . 2001. Surface oceanography of the inferred hatching grounds of argentinus (Cephalopoda : Ommastrephidae) and influences on recruitment variability. Marine Biology 139: 671-9. Wapnick, C. M., Precht, W. F., & Aronson, R. B. 2004. Millennial- scale dynamics of staghorn coral in Discovery Bay, Jamaica. Ecology Letters 7: 354-361. Ward B. B. 2000. Nitrification and the marine nitrogen cycle. In D. L. Kirchman (ed) Microbial Ecology of the Oceans. John Wiley & sons Inc. New York, pp. 427-453. Ward, B. B., Capone, D. G., & Zehr; J . P. 2007. What's new in the nitrogen cycle? Oceanography 20 : 101-109. Ware, D. M., & R. E. Thomson. 2005. Bottom-up ecosystem trophic dynamics determine fish production in the Northeast Pacific. Science 308: 1280-1284. Warwick, R. M. 1986. A new method for detecting pollution effects on marine macrobhenthic communities . Marine Biology 92 : 557-62. Warwick, R., & George, c., 1980. Annual macrofauna production in anAbra community. In: M. B. Collins, (ed.),

mex

Industrialised Embayments and their Environmental Problems. A Case Study ofSwansea Bay. Pergamon Press, Oxford, pp. 517-538. Warwick, R. M., & Uncles, R. J . 1980. Distribution of benthic macrofauna associations in the Bristol Channel in relation to tidal stress. Marine Ecology Progress Series 3: 97-103. Warwick, R. M., Clarke, K. R., & Gee, J. M. 1990. The effect of disturbance by soldier crabs Mictyris platycheles H. Milne Edwards on meiobenthic community structure. Journal ofExperimental Marine Biology and Ecology 135: 19-33. Watanabe, T., & Nomura, M. 1990. Current status of aquaculture in Japan. In M. Mohan Joseph (ed.), Aquaculture in Asia. Asian Fisheries Society, Indian Branch. pp. 223-53. Watson, R., & Pauly, D. 2001. Systematic distortions in world fisheries catch trends. Nature 414: 534-36. Weaver, A. J ., & Hillaire-Marcel, C. 2004. Global warming and the next ice age. Science 304: 4OQ-402.

References •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

Webb, T. J., Vanden Berghe, E., & O'Dor, R. K. 2010. Biodiversity's big wet secret: the global distribution of marine biological records reveals chronic under-exploration of the deep pelagic ocean PLOS TBP. Webster, P. J., Rowden, A. A., & Attrill, M. J. 1998. Effect of shoot density on the infaunal macroinvertebrate community within a Zostera manna seagrass bed. Estuarine Coastal and ShelfScience 47: 351-8. Weimerskirch, H., Brothers, N., & Jouventin, P. 1997. Population dynamics ofwandering albatrossDiomedea exulan.s and Amsterdam albatrossD. amsteroamensis in the Indian Ocean and their relationships with long-line fisheries: conservation implications . Biological Conservation 79 : 257-70. Weinbauer M. G., Brettar, I., & H6fle, M. G. 2003. Lysogeny and virus-induced mortality of bacterioplankton in surface, deep and anoxic marine waters. Limnology and

Oceanography48: 1457-1465. Weissenberger, J., Dieckmann, G. 5., Gradinger, R., & Spindler, M. 1992. Sea ice: a cast technique to examine and analyse brine pockets and channel structure. Limnology and Oceanography 37: 179-183. Weyer, K. M., Bush, D. R., Darzins, A., & Willson, B. D. 2009. Throretical maximum algal oil production. Bioenergy Research 1: 20-43. Whittaker, R. H. 1974. Communities andEcosystems. MacMillan, New York. Whittaker, R. H. 1975. Communities and Ecosystems, 2nd edn, pp. 1-385. The Macmillan Co., Toronto. Widdicombe,S., Austen, M. c., Kendall, M. A., Warwick, R. M.• & Jones. M. B. 2000. Bioturbation as a mechanism for setting and maintaining levels ofdiversity in subtidal macrobenthic communities. Hydrobiologia 440: 367-375. Widdows, J., Pope, N. D., Brinsley, M. D., Gascoigne, J ., & Kaiser, M. J. 2010. Influence of self-organised structures on near-bed hydrodynamics and sediment. Journal of Experimental Marine Biology, & Ecology 379: 92-100. Wiebe, P. H., & Benfield, M. C. 2003. From the Hensen net toward four-dimensional biological oceanography. Progress in Oceanography 56: 7-136. Wieneke, c., GOmez, I., & Dunton, K. 2009. Phenology and seasonal physiological performance of polar seaweeds. Botanica Marina 52: 585-592. Wiig, 0., Erik W. Born, E. W., & Pedersen, I.. T. 2003. Movements offemale polar bears (Ursus maritimus) in the East Greenland pack ice. Polar Biology 26: 509-516. Wildish, D. J., & Peer, D. 1983. Tidal current speed and production ofbenthic macrofauna in the lower Bay of Fundy.

Canadian Journal of Fisheries and Aquatic Sciences 40 (Suppl. 1): 309-321. Williams, P. J. Ie B. 1998. The balance of plankton respiration and photosynthesis in the open oceans. Nature 394: 55-57. Williams, S. 1.., & Ruckelshaus, M. H . 1993. Effects of

nitrogen availability and herbivory on eelgrass (Zostera marina) and epiphytes. Ecology 74: 904-918. Wilson, R. P. 2003. Penguins predict performance. Manne Ecology Progress Series 249 : 305-310. Wilson, R. P., Grernillet, D., Syder, J., Kierspel, M. A. M., Garthe, 5., Weimerskirch, H. et al. 2002. Remote-sensing systems and seabirds: their use and abuse and potential for monitoring marine environmental variables . Manne Ecology Progress Series 228: 241-261. Wilson. R. P.• Simeone, A., Luna-Jorquera, G.• Steinfurth, A., Jackson,S., & Fahlman, A. 2003. Patterns of respiration in diving penguins: is the last gasp based on an inspired tactic? Journal ofExpenmentalBiology 206: 1751-1763. Wilson, R. W., Millero, F. J ., Taylor, J . R., Walsh, P. J ., Christensen, V., Jennings,S., & Grosell, M. 2009. Contribution of fish to the marine inorganic carbon cycle. Science 323 : 359-362. Winter, c., Moeseneder, M. M., & Herndl, G. J. 20m . Impact of UV radiation on bacterioplankton community composition. Applied and Environmental Microbiology 67 : 665-72. Wolfe, G. V. 2000. The chemical defense ecology of marine unicellular plankton : Constraints. mechanisms. and impacts. Biological Bulletin 198: 225-244. Wolf-Gladrow D., & Riebesell D. 1997. Diffusion and reactions in the vicinity of phytoplankton. Marine Chemistry 59: 17-34. Wolf-Gladrow, D. A., Riebesell, D., Burkhardt,S., & Bijma, J . 1999 Direct effects of C02 concentration on growth and isotopic composition ofmarine plankon. Tellus B 51: 461-476. Worm, B., Lotze, H. K., Hillebrand, H., & Sommer, D. 2002. Consumer versus resource control of species diversity and ecosystem functioning. Nature 417: 848-51. Worm. B., Barbier, E. B.• Beaumont, N., Emmett Duffy, J., Folke, C., Halpern, B. S. et al. 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314: 787-790. Worm. B., Hilborn, R.• Baum, J., Branch, T., Collie, J., Costello, C. et al. 2009. Rebuilding global fisheries. Science 325: 578-585. Wotton, R. S. 2004. The essential role ofexopolymers (EPS) in aquatic ecosystems. Oceanography and Marine Biology:An Annual Review 42: 57-94. Wuchter, C.• Abbas, B., Coolen, M. J. L.. Herfort, L., van Bleijswijk, J., & Timmers, P. 2006. Archaeal nitrification in the ocean. Proceedings ofthe NationalAcademyofScience USA 103: 12317-12322. Wulff, A., Iken, K., Quartino, M., Al-Handal, A.• Wiencke. C., & Clayton, M. N. 2009. Biodiversity, biogeography and zonation of marine benthic micro- and macroalgae in the Arctic and Antarctic. BotanicaManna 52: 491-507. Yamaguchi, A.• Watanabe. Y.• Ishida. H.• Harimoto, T.,Furusawa, K., Suzuki, S. et al. 2002. Community and

References trophic structures of pelagic copepods down to greater depths in the western subarctic Pacific (WEST-COSMIC). Deep-Sea Research Part I- Oceanographic Research

Papers 49 : 1007-10025. Yates, M. G., Stillman, R. A., & Goss-Custard, J . D. 2000. Contrasting interference functions and foraging dispersion in two species of shorebird (Charadrii) . Journal of Animal Ecology 69: 314-22. Yodzis, P. 1998. Local trophodynamics and the interaction

of marine mammals and fisheries in the Benguela ecosystem. Journal ofAnimal Ecology 67: 635-658. Young, J . R., & Ziveri, P. 2000. Calculation of coccolith volume and its use in calibration of carbonate flux estimates. Deep-Sea Research, Special Part II: Topical Studies

in Oceanography Particle Fluxes and their Preservation in Deep Sea Sediments 47: 1679-1700. Zeebe, R. E., Zachos, J . C. Caldeira, K., & Tyrrell, T. 2009. Carbon emissions and acidification. Science 321 : 51-52.

Weblinks Below we have provided a selection of weblinks that will help you gain a more in-depth understanding of some of the issues we have covered in Marine Ecology: Processes, Systems, and Impacts. More importantly these websites open the door to specific regional examples of marine ecology at work, current issues, and data that you can download and use. Weblinks evolve all the time, 50 while we have tried our best to ensure all of these links are current some will

inevitably change. If they have changed, typing some of the keywords in the description text will probably take you relatively quickly to the new location. Alternatively. visit the book's online resource centre at www.oxfordtextbooks. co.uk/orc/kaiserze/ to access up-to-date URLs for all links given here. Antarctic & Arctic: There are many websites dealing with Arctic and Antarctic issues. However. by going to the fol-

lowing websites it is possible to follow links to this wealth of information and direct links to the organizations at which Polar research is conducted:

http:/ /www.antarctica.ac.uk. http:/ /www.arcus.org/index.html http:/ /nsidc.org/ index.html http:/ /www.scar.org. Antarctic living resources: This is the website of the Commission for the Conservation of Antarctic Marine Living

Resources. http:/ /www.ccamlr.org/pU/e/gen-intro. htm. It contains information on Southern Ocean ecosystems and efforts to take an ecosystem approach to management of fishery resources there.

Antarctic spring phytoplankton bloom: Part of the NASA Goddard Space Centre's web site, this provides images of the seasonal development of the spring phytoplankton bloom in the North Atlantic. It also provides information on patchiness and some of the problems this presents for sampling. http:/ /daac.gsfc.nasa.gov/CAMPAIGN_ DOCS/OCDST/nab.html. Aquaculture: The Food and Agriculture Organisation of the United Nations compiles and publishes downloadable data and figures on the cultivation ofaquatic organisms around the world http:/ /www.fao.org. To find out more about aquaculture research visit the University of

Stirling, Institute of Aquaculture website http:/ /www. aquaculture.stir.ac.uk. Benthos: The virtual handbook written by Tom Brey of the Alfred Wegener Institute is a mine of information regarding benthic ecology and production processes: this can be cited as: T. Brey 2001. Population Dynamics in Benthic Invertebrates. A Virtual Handbook . Version 01.2. http :/ /www.thomas-brey.de/science/virtualhand-

booklnavlog/index.html Alfred Wegener Institute for Polar and Marine Research, Germany. Biodiversity research: DIVERSITAS is a major international program dealing with biodiversity and eco system processes. as well as the links between eco-systern services and society. Many marine and intertidal

aspects are included in this program http :/ /www. diversitas-international.org/. Biodiversity and ecosystem function: A major website holding up-to-date literature on marine biodiversity and

ecosystem functioning can be found at http:/ /www. abdn.ac.uklecosystemibioecofunc/. Bioluminescence webpage: http :/ /www.Iifesci.ucsb. edu/biolum/, A site full of excellent information on the biology of bioluminescence with pictures and video clips. Carbon cycle: For a general introduction to the marine

carbon cycle and the links between chemistry and biology and global climate change see: http:/ /earthguide. ucsd.edu/virtualmuseum/climatechangel/06_3. shtml. Climate change: A wealth of information about global climate change can be found at the website of the Intergovernmental Panel on Climate Change: http:/ /www.ipcc. chi. The North Atlantic Oscillation website, http:/ / www.Ideo.columbia.edU/NAO/, provides everything you wanted to mow about this climate pattern. describ-

ing the underlying mechanism, plotting data and linking to other useful NAG web resources.

Coccolithophorids: For a detailed introduction into the biology, biogeochemistry, and geology of this important group of phytoplankton go to: http:/ /www.soes.soton.

ac.uk/staff/rt/. Consequences of climate change: A global analysis of the current and predicted effects of climate warming can be

found at http:/ /www.ipcc.ch.This site contains lots of informative reports and illustrations of the predicted

effects of global warming. Conservation: The website of the Society for Conservation Biology http z/ z'conbio.net/scb/ provides up-to-date access to key issues affecting the conservation of all natural resources. The Marine Conservation Society of

the United Kingdom http:/ /www.mcsuk.org and Marine Conservation Biology Institute USA http:/ /www.mcbi. org provide lots of useful links to other organizations, conservation work opportunities and projects, and scientific information on current topical issues. Coral reefs: For a global perspective on coral reefs see

http:/ /www.reefbase.org and for the International

Weblinks Society for Reef Studies webpage go to: http:/ /www. fit.edu/isrs. Deep-Sea: NOM Vents programme. http:/ /www.pme!. noaa.gov/vents/. A site dedicated to information and research on the geology and biology of hydrothermal vents, with lots of pictures and video clips. Detecting change in biological communities: For information on detecting change in communities and key considerations in experimental design, see the manual on offer at http:/ /www.primer-e.com. Diatoms: A key resource for anyone wanting to learn more about diatoms is the International Society for Diatom Research, which includes links to many other diatom

websites: http:/ /www.isdr.org/. Estuaries: The website of the Estuarine Research Federation http:/ /www.erf.org/ provides information from the world's largest estuarine science organization, including publications, education, and links. European Network of Excellence: MarBEF is a major network of European marine ecologists that involves over 80 different institutes . This is an excellent starting point for finding out what is going on in Europe and an ideal starting point for finding placement work opportunities

or employment http:/ /www.marbef.org/outreachl. Evolution & Diversity: The Tree of Life Web Project (ToL) is a collaborative effort of biologists from around the

world. On more than 3000 worldwide web pages, the project provides information about the diversity of

organisms on Earth, their evolutionary history (phylogeny), and characteristics. http:/ /tolweb.org/tree/ . Exploitation ofnon-biological resources and renewable energy: For exploitation of non-renewable offshore resources and alternative forms of energy generation such as windfarms see http:/ /www.thecrownestate. co.uk. This website has links to reports and information regarding the amount ofmaterial removed from the seabed and the potential of wind and wave energy to meet future energy requirements.

Flagellates: A website dealing with flagellates that are important in microbial processes in marine systems, and

well introduced at http:/ /tolweb.org/notesl?note_ id=50. Fisheries: Up-to-date global fisheries statistics including biological and economic information is available

through http:/ /www.fao.org. Regional information for Europe is available at http:/ /www.ices.dk where it is possible to download a database of European fisheries statistics. Current research in the US can be accessed

through http:/ /www.noaa.gov/fisheries.html which is a highly informative website with respect to current issues in fisheries and gives access to free to use photographic images . A particularly informative industry-run

website can be found at http :/ /www.fishingnj.org, which gives the fishers' angle on current issues. A more

commercial perspective is given at http:/ /www.seafish.

co.uk where you will also find excellent seafood recipes. Other informative research websites include those of the Centre for Environment. Fisheries. and Aquaculture

Science http:/ /www.cefas.co.uk, Fisheries Research Services Aberdeen http:/ /www.scotland.gov.ukltopics/marine, the Australian Institute of Marine Science http:/ /www.aims.gov.au. Visit the Worldfish Center website for more information about Asian and African

fisheries and projects http:/ /www.worldfishcenter. org. Habitat listing: The MarUN database held at the Marine Biological Association of the United Kingdom gives access to a wealth of information about intertidal and

subtidal coastal habitats with links to primary and 'grey' literature that is invaluable for learning and research

http:/ /www.marlin.ac.uk. Harmful algal blooms: Information about algal blooms and harmful algal blooms, red tides, and algal toxicity can be found at: http:/ /www.whoi.edU/science/ redtide/ as well as http:/ /www.bigelow.org/hab/ . Longterm data sets: There are a number of long-term oceanographic data sets for which biological, chemical. and physical data are collected to examine seasonal, inter-annual. and even decadal variations:

Hawaii Ocean Time-series (HOTS) http:/ /hahana.soest. hawaii.edu/hot/hotjgofs.html Bermuda Atlantic Time-series (BATS) http://bats.bios. edU/ Monterey Bay time-series study http:/ /www.mbari.org/ bog/Projects/centraicaVsummary/ts_summary.htm. VOS UnderwaypC02 Program http: www.pme!.noaa.gov/ co2/uwpco2/ Continuous Plankton Recorder Survey: http:/ /www.sahfos.ac.uk/. Mangroves: For mangroves, see http:/ /www.ncl.ac.ukl tcmweb/tcm/mglinks.htm, A site listing most of the major websites dealing with mangroves and wetlands . Maps of major marine environments:

http:/ /www.oceansatlas.org/ http :/ /www.teachers.ash.org.au/jmresources/ marine/environments.html Marine Institutes: There are a number of websites that give extensive listings of places around the world where marine research takes place:

http :/ / oceanlink.island.neVcareer/ careerlinks. html http:/ /www.skio.peachnet.edU/resources/ marinelinks.php http:/ /www.sams.ac.uklabout-us/ linksl?searchterm=links http:/ /www.marbef.org Marine systems: GLOBEC http :/ /www.pm!.ac.ukl globec/ is the International Geosphere-Biosphere

Weblinks •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••• •

Programme (IGBP) core project responsible for understanding how global change will affect the abundance,

Seagrasses: WCMC Global Seagrass Database. http :/ / www.unep-wcmc.org/marine/seagrassatlas/. Based

diversity, and productivity of marine populations. This

around the world atlas of seagrasses, the website gives some introductory information, but most interestingly has a series of online maps showing the distribution of seagrass species around the world .

web site gives summaries of recent GLOBEC-related work and access to data.

Meiofauna: The website of the International Association of Meiobenthologists and all you wanted to know about meiofauna http:/ /www.meiofauna.org/. Microbial loop: Background information about the microbialloop and why it is important can be found at: http:/ / www.bigelow.org/bacterial. Satellite imagery: The Sea-viewing Wide Field-of-view Sensor (SeaWiFS) Project http:/ /seawifs.gsfc.nasa. gov/SEAWIFS.html uses satellite observations to provide quantitative data on global ocean bio-optical properties. This website provides an overview of the project, has some excellent summary maps and even enables you

to produce mapped globes from a perspective of your choice.

Seaweeds or macroalgae: Probably the best starting point for any seaweed-related enquiries. http:/ /www.seaweed.ie. Algaebase http:/ /algaebase.org has details on 57 000 algal species, 1500 images, 33 000 bibliographic items, 104 000 distributional algal records, and a 27 ODD-word online glossary. Viruses: This website gives a good general overview of aquatic viruses and current research topics in the field,

as well as further weblinks: http:/ /library.thinkquest. org/CR0212089/halo.htm.

This page intentionally left blank

Index Locators for headings which also have subheadings refer to gene ral aspects of that topic Species appear un der their common and family names where possible

c -proteobacte ria 100-1 ,1 0 7 ABC curves 409 a bunda nce annual variations 23 bacteria 105 and body size 23, 27-8 and compe tition 24-6 deep sea 264 seasonal trends, m icrobial 11 7 a byssal plain 252-3, 256-60 a byssopelagic zone 74 , 196 ACe (Anta rctic Unipolar Curre nt) 344 acclimation 47-9 accretion , Nile delta 4 16 acid ification 57, 422-6 acoustic sa mpling 209-11 active fishing gears 364-5 activity conce pt 115 adaptations, polar regions 334 add itive effects, disturbance 403 adsorption 115 aggregate extract ion 417-9 agriculture, impact 41 4 Agu lhas leakage 203 a he rmatypic corals 30 6 Alaskan pollo ck 357 albatross, im pact of fishing 37 1 Aldabra Atoll 308 algae . see also phytoplankton; seaweed blooms 7 1, 120- 1,337- 8, 4 14 ca rbon storage 34 coralline 3 12 , 424-5 dinflagellate symbiotic 3 10 elemental composition 53 , 54-5 farming/biofuel 67,68 inorgani c nutrients 50 microbial ecology 111- 5 primary production 34-6, 64-8, 73 salinity cha nges , tolera nce 154 zonation 3, 224 alginate s 385 alien species 397, 42 1 Allee effect 163 Allen plots 130-1 allo chthonous species 99 ,260 allometric relationships, secondary production measurement 131- 3 alternative stable states 122 Alvin 255,271 Amazon es tuary 143 ammonite s, complexity 27 a m moniu m 101 , 122

amphipod, gia nt 261 Amundsen Sea 1 a nchovy, Peruvian 357 a ngios pe rms, seagrasses. see seagrass a nimal attached remote sensing 284-5 a nimal motion, te mporal/spatial patterns 203 a nnotation , genomic 102 a nnual variations. see seasonal cycles a noxia 4 14-5 . see also eutrophication anoxygenic heterotrophs 43 anoxygenic phototrophs 44 Anta rctic/Arctic comparisons 331- 2, 343-4, 350-1 Anta rctic krill 196 Anta rctic shallow waters, fauna 24 Antarctic Unipolar Curre nt (ACC) 344 a nti-fouling paint 420-1 a ntibiotics 386, 394 a nticyclon ic gyres 7 1 a photic zone 45 a ppe nd icular ians 94 aquaculture 377-8, 399 biotechnology 386-7 cages 387-9 1 conservation role 398-9 cultivation systems 387, 387- 9 1 d isease 383, 386-7,393-4, 399 environmental impacts 395-7 feed re qu irements/ constraints 37880, 385-6 further reading 400 global d istribution 383- 5 global sta tistics 38 1,385 historical account 378-8 1 methods 38 1-3 mollusc 39 5-7 offshore 39 1-3 population biology 390 sea ranching 397-8 shrim p 393-4 welfare 382, 384 aquaria, public 440 aquatic systems, primary production 73 archaea 89,97-109 Arctic/Antarctic comparisons 331- 2, 343-4,35 0-1 Arctic Ocean 331 sea-ice cha nges 339,35 1 nutrients limiting growth 340--1 a rms races, evolutionary 38, 232 , 289 Arrhenius re lationship 11

a rten -mi nim um 166 Arthrocnemum spp. 164 asse mbly, genome 102 assessm ent . see measurement Aswan High Da m 4 16 Atlantic Ocean, food webs 236 Atlantis 194 ato lls 30 7, 308- 9 a tten uation , light in water 45 aurora borealis 325 Australia conservation 444-5 Embley River estuary 161 endemism 15 Swan River estuary 156 a utochthon ous species 100, 160 a utomated aquacult ure cages 39 1- 3 a utomatic measurement devices 82-6 a utonomous un derwater veh icles (AUVs) 83, 194, 209 , 2 12,25 3,254, 336 a utotrophs net ocean productivity 74-6 season al cycles 122 zooanthellae 3 10 a utumn season 118,11 9 ,1 22,1 23 AUVs . see autonomous underwater veh icles azoic zone 265 Azores, conservation 438 Azov Sea 169 BACI (Before After Control Im pact) experimental design 4 13 bacte ria 89. see also m icrobial ecology communities 106- 7 fingerprinting methods 10 7 growth dynamics 115-8 key organism groups 97- 109 marine snow communities 108-9 oligotrophic 98 osmotrophs 93 polar regions 333 species numbers 90 Bacteroidetes 100 balla n wrasse 389- 9 1 Baltic Sea 168-9 bar-built estuaries 145 barnacles 2 , 3, 4 , 180 barrie r coral reefs 307. see also coral reefs; Great Barrie r Reef barrie r, River Thames 422 basin mangroves 278

Index basking shark 285 bathymetric distribution, lobster 266 Bathymodiolus 274 bathypelagic zone 74,75,196 bathysnacks 253-4,255 bathysnap system 253 Bay of Fundy 148, 149 beaches. see shores bears, polar 347-8,350 bedrock substrata, continental shelf 241-4 Before After Control Impact (BACI)

experimental design 413 Beggiatoa 43 belief-based science 447-8 benthic ecosystems. see seabed habitat! biota bentho-pelagic coupling 232, 343 benthos, polar regions 341-4 Big Fish Eat Little Fish picture 199-200 biodiversity

and abundance 24 conservation 439, 440 coral reefs 306,313-4 deep sea 265-7 and ecosystem function ix, 21, 22 estuaries 143, 165-8 hypersaline waters 169 index 15, 16,407,408,409

mining 419 patterns 9, 10,11,15-22 polar regions 335 seagrass meadows 292,299-300 shore communities 182, 190-1 willingness to pay for 438 biodynamics. see population dynamics bioerosion, coral reefs 309,318-20 biofuel 67 biogenic reefs, continental shelf 248-9 biogeography 9-15,203-5 bioinfonnatics 102 bio-iogging 285 biological capacity, fishe ries 360 biological pump 57,124 bioluminescence 257,258 biomass continental shelf 248 deep sea 264 definitions 232 estuaries 159- 60 fisher ies 366-8 kriil 345 microbial 90, 115--6 and ocean depth 19 7 to production ratio (P/ B) 128 and size 91 temporaVspa tial patterns 204-5 biomes 11-2,205 biota. see flora/fauna

biotechnology 386--7 biotopes, continental shelf 241,242 bioturbation . see a150 disturbance continental shelf biota 232-4 grapsid crabs 287 shores 188, 191 birds estuaries 161- 3 impact of fishing 371 polar regions 345-51 shore experiments 185 bivalve molluscs aquaculture 395-7 competition 25 experiments 181,411-2 suspended rope cultivation 397 black band disease 314 Black Sea 169 black smokers 271-2 bleaching, coral 315--6,421 blind estuaries 145, 146 blooms, piankton 71, 120-1,337-8, 414 body mass . see size BOIS database 430 bommies 307 bottom-trawling 137-9,364 bottom-up processes food web dynamics 117-8 secondary production 134 shore commun ities 181, 183, 188 boundary layer 229 Bouvet Island 11 brachiopods, competition 25 brackish water systems 168-9 Braer, oil spillage 417 breathing holes, pack ice 348-9 Brent goose 161-2 Brent Spar oil platform 446 brine channels, sea-ice 334 broadcast-spawning 23 bryozoa, secondary production 127 bubbles in w ater 45--6 buffer zone, current velocity 229 bulldozers 232 Burgess Shale 18 cages, aquaculture 387-91,391-3 calcium 54 Cambrian fauna 19 CAMERA (Community Cyberinfrastructure for Advanced Marine Microbial Ecology Research and Analysis) 102 Canada, Fraser River 155 Canadian cod 359 carbon 55-9 aigal growth 64-8 bacterial growth 116 cycles, globai 123-4

isotopes 4 0 pools 95 radiocarbon la belling 78-9 sources, estuaries 159- 61 storage, deep sea 256--7 carbon dioxide 38-41,78,422--6 carnivores 232. see also predator-prey systems carrying capacity aquaculture 380 ecosystems 12 6 oxygen 421 catches, fisheries 359,368 Caulerpa taxifolia 295-6 CCAMLR (Convention on the Conservation of Antarctic Marine Living Resources) 436 CDOM (coloured dissolved organic matter) 45--6,46, 81, 82 cell-counting, bacterial 116 Challenger 194 change. see also regime shifts detecting 408,410-1 natural 402 sea-level 144-5,151-2 charismatic species 433 chemical dispersants 4 17 chemolithotrophs 97-8,98 chemo-organotrophs 43 chemosynthesis 261,272 chemotrophs 43-4 Chesapeake Bay 145, 249, 4 26, 4 27 Chilean jack mackere l 357 choice, consumer 443-4 chlorophyll 41,51-2,204 chronic life cycles, viruses 111 chub mackerel 357 clam species (various) climate change 421 secondary production 127,128-3 1 classification of estuaries 144-8, 15 1 cleaner wrasse 322,389-91 climate change 6, 139--40,401,421. see a150 temperature acidification 422--6 carbon sinks 57 coral reefs 315 eutrophication 421 rainfali 422 sea-ice 350-1 water circulation 422 climate patterns, marine 6--7 coastal biomes 11-2,205 coastal p lain, estuaries 14 5 coastal waters, primary production 71 Coastal Zone Colour Scanner (CZCS) 10, II coccolithophorids 56 cod 238

Index •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

aquaculture 377 Canadian 359 continental shelf 244 deep-sea 254 historical account of fishing 358 polar regions 351 salinity tolerance 168 whiting impact 406 cohort-based methods 129- 31 cold seeps 273-4 colonies, and organism size 28 colour sensors 36, 195 coloured dissolved organic matter (CDOM) 45-6,81,82 Community Cyberinfrastrueture for Advanced Marine Microbial Ecology Research and Analysis (CAMERA) 102 compensation depth 48 irradiance 46 point, seagrass meadows 293 competition and abundance/biodiversity 24-6 and ammonium 122 and latitude 26 shore zonation 180 complexity 27 conservation 429-3 1,449 in action 442-7 ecolabelling 442, 443-4 economics 43 5-9, 446 ecosystem approach 432,435,436 environmental impact assessment 442- 3 evidence-based 447-8 fish communities 207 fund ing 446 further reading 449 future scenarios 448 habitat 433-5 legislation/policy 439-42 life cycle analysis 448 marine reserves 444-7 reasons for 431-2 role of aquaculture 398-9 valuing certain species over others 432-5 consumer choice 443-4 contaminants 4 19- 21. see also pollution continental shelf 1,195,217-8,249-50 biogenic reefs 248-9 biota, functional ro les 231-5,240 communities 239-41 definitions 2 18 ecosystem type 224-7 fisheries 358 food webs 235-9 fronts/production 223 further reading 250

glaciation 2 19,220-2 hard substrata 241-4 light/turbidity 223-4 primary prod uction 71 seabed habitat/biota 224-31 size, organism 227-9 specific habitats 241-9 trophic cascades 237-8 wave action/currents 219-23,229 continental slope 252 Continuous Plankton Recorder (CPR) surveys 84-5,213 Convention on Biological Biodiversity 15 Convention on the Conservation of Antarctic Marine Living Resources (CCAMLR) 436 conversion efficiency 381 conveyor belt, global 258,328-9 copepod species human impacts 139-40 parasites 161 spatial patterns 206 Cope's rule 28 coral bleaching 315--6,421 coral reefs 56, 58, 305, 323 acidification 424-5 further reading 323-4 hu man impacts 314-8,320,322-3 Impact of fishing 317, 318, 322, 363, 374-5 organisms/communities 309-11, 3 13-4,320 population dynamics 320-2 prod uctivity/food webs 311-3 reef development/distribution 305-9 reef growthlbioerosion 318-20 reproduction 3 10-11 types 307 Coriolis current 259 Coriolis force 202,223

Corophium volutator 163 CPR (Continuous Plankton Recorder) surveys 84-5,213 crab species climate change 421 d isturbance 403 food webs 237 mangrove 287-8 spawner-recruitment relationships 363 temperature effects 154 critical depth 48-9 critical tidal level 179-81 crocodiles 283 cross-section, ocean basin 252 crown-of-thorns starfish 1, 316--7 crustaceans. see also crabs; krill; lobsters; shrimps deep-sea 269-70

red coloured 197 shore 186 cryopreservation 386 cultivation systems, aquaculture 387 culture-independent genetic analysis 99 curlew 162 currents, ocean 5--6, 422 Antarctic Unipolar 344 continental shelf 2 19-23,229,246 deep sea 258-9 Gulf Stream 7 polar regions 328-9 cyanobacteria 59 Cycliophora phylum 2 cyclones 315,402 cyclonic gyres 71 CZCS (Coastal Zone Colour Scanner) 10, II

damming rivers 416--7 Darwin, Charles 307,308 data sets, long-ter m 84-6,410 DBL (diffusive boundary layer) 50, 52-3 decapod crustaceans, deep sea 269-70 decomposition 55, 89, 93-7 deep sea 251,275. see also hydrothermal vents abundance/biomass 264 abyssal plain 256--60 biodiversity 265-7 carbon storage 256--7 currents 258-9 definitions 252 dissolved organic material 261 dissolved oxygen 258 further reading 275-6 gigantism 270-1 hydrostatic p ressure 259 large food falls 261-2 light 257 major organism groups 267-70 organisms 253, 254, 255, 258, 260, 261,263-71 particulate organic material 262 produ ctivity 260-3 sampling 252-5 sediment 259--60 size, organism 264-5 species composition trends 266 temperature 257-8 timing of food inputs 262-3 zonation 263-4 Deepwater Horizon oil spillage 415, 4 17, 418 definitions biodiversity 15 biomass 232 continental shelf 2 18 deep sea 252

Index ••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

estua ries 143-4 fisheries catches/landings 359 mangroves 278-9 ontogenetic 286 pack ice 329-30 pelagic 194 pelagic ecosystems 195-7 productivity 67 seagrass meadows 290-1 secondary production 126-8 sessile organisms 286 shores 173 success 26-7 welfare 382 deforestation 414 deltas 143 density of seawater 4,198 deposition, sediment 150 depth distribution, lobster 266 determinants of zonation 179-81 detritus, marine 93~. see also marine snow nature/production 94-6 u tilization/recycling 96-7 diamond dredging 417 diapause depth 206 diatoms adaptations 195-6 frustules 37-8 lipid constituents 54 polar regions 332,333-4,340 diel vertical migration (DVM) 19, 339-40 diffusive bou ndary layer (DBl) 50, 52-3 dimethylsulphide (DMS) 6 1 dimethylsulphonioproprionate (DMSP) 60-1 dinflagellate symbiotic algae 3 10 dioecious species 297 direct economic benefits 432 disaggregation 245 discards, fisheries 359 Discovery 194 disease aquaculture 383,386-7,393-4,399 co ral reefs 3 14 dispersal, hydrothermal vent organisms 274-5 dispersants, oil spillage 417 dissipative beaches 177 dissolved organic carbon (DOC) 55, 95 dissolved organic matter (DOM) 45-6, 94-5 deep-sea 261 food webs, microbial 114 marine snow commu nities 108-9 polar regions 337 dissolved oxygen (DO). see eutrophication; oxygen distinctness, taxonomic 409

distribution, species 430 aquaculture 383-5 climate change 421 coral reefs 305-9 human impacts 407,409,430 kelp beds 244 mangroves 279 seagrass meadows 292-6 disturbance 402 ecological role 402-6 impact of fishing 371-4 intermediate disturbance hypothesis 404--{i

recovery rate 403-4 scale 402-3 shores, rocky/sandy 188,191 sources 402 diversity index IS, 16, 407,408,409. see also biod iversity DMS (d imethylsulphide) 61 DMSP (d imethylsulphonioproprionate) 60-1 DO (d issolved oxygen) . see eu trophication; oxygen DOC (dissolved organic carbon) 55,95 dolphins 213, 371,433 DOM. see dissolved organic matter dred ge netting 364 dredging 417- 9 drilling mud contamination 417 drop-frame syste ms 253-4 drought, impact on estuaries 155--6 drug resistance 386 d ugongs 301-2 dunlin 163 DVM (diel vertical migration ) 199, 339-40 dynamic viscosity of seawater 196-9 dynamite fis hing 363,374 echinoderms. see sea urchins echo-sounding 211,220,336-7 ecoclines 166, 173-9 ecolabelling 442,443-4 ecology, terrestriaVmarine comparison 277 econo mic viability, mining 419 econo mics of conservation 435-9,446 ecosystem approach to conservation 432, 435,436 to fisheries management 375--6 ecosystem-based management 360, 375-6 ecosystem engineers 237-8, 287, 319 ecosystem fun ction 15 and biodiversity Ix, 21, 22, 167-8, 190-1 and d isturbance 404 estuaries 167-8

genomics 104 mangroves 289- 90 role of microbial ecology 9 1-3 seagrass meadows 302-3 secondary p roduction 126 sediment 234-5 shores 190-1 ecosystem goods/services viii-ix and conservation 431,433,439 coral reefs 322-3 impact of fishing 375-6 ecosystems carrying capacity 126 continental shelf 224-7 secondary production 134-6 ecotones 166 ectoparasites 322 edge effects sea-ice 337-41 seagrass meadows 300 education, and conservation 439, 440 efficiency growth 91-2 trophic yield/food chain 92-3 effort controls 368 EFH (essential fish habitat) 372-4 EIA (environmental impact assessme nt) 442- 3 Ekman transport 201-2 El Nino Southern Oscillat ion (ENSO) 6-7 annual variations in abundance 23 climate change 421 coral reefs 3 15,316 primary production 204 remote sensing 81 temporal/spatial patterns 200 electrode measurement devices 79-80 eleme ntal composition, algae 53, 54-5. see also nutrients elephant seals 211 Ely sea mount 372 Embley River estuary, Australia 161 emersion, shores 174 endemism 12-5,343-4 energy, renewable 147-8, 159-60 engineers, ecosystem 237-8, 287, 319 ENSO. see EI Niflo enviro nmental grad ients, shores 173-9. see also patterns, environmental environmental impacts. see human impacts environmental variables, estuaries 148-54 epifauna 175 epifluorescence 37, 8 1, 116 epipelagic zone 74, 75, 196 epiphytes 77-8,294 EPS (exoploymeric substances) 94

Index •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

erosIOn coral reefs 309,318-20 current velocity 229 human impacts 414 sea-ice 341 error-to-mean ratio 411 essential fish habitat (EFH) 372-4 estuaries 143, 170-1 biodiversity 165-8 birds 161-3 carbo n sources 159-60 classification 144-8 definitions 143-4 dissolved oxygen 151 environmental variables 148- 54 evolution 144 fish communities 156--9 further reading 171 hypersaline waters 169-70 hyposaline seas 168-9 impact of freshwate r inflow 154-6 lagoons 170 origins of organisms 151- 3 productivity/food webs 159--65 salinity 148-9 saltmarsh systems 163-5 sediment 150, 154 stable isotope analysis 160-1 temperature changes 151, 154 zones 151 ethical responsibilities 431-2 EU. see European Union eukaryotes, species numbers 90 Eulerian sampling 211 euphotic zone 4,45 Europa 340 European Union Nature Information System (EUNIS) 241 regulations 440-2 Eurythenes (giant amphipod) 261 eutrophication 49-50,139,402,414-5, 421. see also hypoxia; oxygen evidence-based conservation 447-8 evolution, estuarine species 144, 151- 3 evolutionary arms races 38,232,289 excess production, coral reefs 312 excretion 94 Exe estuary, Devon 161 exoploymeric substances (EPS) 94 experiments acidification 425 human impacts 411-2 shore communities 180-2, 184-7, 190-1 explosive fishing 363,374 exposure, shores 174-5. see also wave action extinction 11

and abundance 23 coral reefs 3 13-4 detecting change 4 11 KT 18 and organism size 28 sea cows 429 whales 440-1 extra-o ral digestion 237 extreme environments 402 exudates 94 Exxon Valdez oil spillage 417 eye membranes, squid 196 facilitation 189 faecal pellets 338 faith-based fisheries management 369 Falkiand Isiands 11 farming, fish. see aquaculture fauna/flora. see flora/fauna fecundity, fish species 361 feeding, sioppy 94 feelings-based definitions, welfare 382 fetch 222 field experiments. see experiments finge rprinting methods, bacteria 107 fish/fish communities deep sea 270 estuaries 156--9 eutrophication 414 farming. see aquaculture mangroves 290 and primary production 135, 136, 205-7 and sea urchins 318 seagrass meadows 298-9 shores 185 size structuring 136 vertical migration 199 welfare 382, 384 fishmeal feeding, aquaculture 378-80,385-6 fisheries 357,376 ecosystem-based management 375--6 environmental impacts 370-5 fish stocks assessment 366-8 further reading 376 future scenarios 376 global 357-61 historical account 358-9 human impacts 137-8 impact on birds/mammals 371 impact on coral reefs 3 17,318,322, 363,374-5 impact on kelp beds 375 management 359-60,368-70 methods 363-5 overfishing 359--60 pelagic ecosystems 212-3 population biology 362-3,366

production 361 science 360-1 seabed impacts 371-4 stocks 361 water use impacts 416 fjords 144,1 46 Fleet Lagoon, Dorset, UK 170 flexible genomes 103 flora/fauna conservation 433 continental shelf 224-31 coral reefs 309-1 1, 313-4 deep sea 260,266,268-70 hydrothermal vents 272-3 impact of fishing 371 mangroves 286-8 microbial 97-115 polar regions 11-2, 205, 332-7, 341-51 seagrass meadows 298-301 sea ice 332 Florida, mangroves 286 flound ers 157 flow cytometry 116 fluorescence 37,81,116 foam 62 food labeliing 442,443-4 food webs/chains 91 continental shelf 235-9 coral reefs 311-3 estuaries 159--65 marine detritus recycling 97 microbial 89,114,116-8,124 pelagic ecosystems 199- 200 polar regions 334,336 secondary production 135 fossils, trace 232 fragmentation, habitat 299-300 Fraser River, Canada 155 fringing coral reefs 307 mangroves 278 fronts, bioiogical 72,204,207,223 frustules, diatoms 37-8 function-based definitions, welfare 382 functional roles, continental shelf biota 240 fund amental niches 266 funding, conservation 435-9, 446 further reading aquaculture 400 conservation 449 continental shelf 250 coral reefs 323-4 deep sea 275--6 estuaries 171 fisheries 376 human impacts 428 microbial ecology 125

Index patterns, marine environmenta l 29 pelagic ecosystems 216 polar regions 352-3 primary production 87-8 seagrass meadows/mangroves 304 secondary production 140 shores, rocky/sandy 193 future scenarios conservation 448 fisheries 376 pelagic ecosystems 214-5 shores, rocky/sandy 192 Galapagos Islands 306, 315 gastropod molluscs, biodiversity 10, 18-9, 20 gears, fishing 364-5 gene flow, hydrothermal vent organisms 274-5 genetic analysis, culture-independent 99 genetic modification, aquacultu re 386 genomics, microbial 101-4 ghost shrimp 181 gigantism deep sea 270-1 polar regions 28, 344-5 glaciation continental shelf 219, 220-2 origins of estuary organisms 152, 153, 157 global aquaculture statistics 381,385 carbon/nutrient cycles 123-4 conveyor belt 258, 328-9 d istributions. see distribution fishe ries statistics 357-8 primary production 69-76 secondary production 132-3 gold rush, shrimp 377,393-4 gonad secondary pro duction 128 Good Fish Guide (Ma rine Conservation Society) 443 goose, Brent 161-2 Gould, Stephen J. 18 government policy, greening 432,

439-42 grand cycle, p rimary production! decomposition 34,55 grazmg continental shelf biota 232 food web dynamics 116--7 mangroves 282 seagrass meadows 301-2 grease ice 329,330,332 Great Astrolabe Reef 308 Great Barrier Reef 305--6,309 h uman impacts 314 Marine Park 43 6, 444-5, 446 Great South Bay, Long Island 145

greenhouse effect 6. see also climate change greening of government policy 432, 439-42 grey mullet 157 gross photosynthesis 46 gross production, definitions 67 growth dynamics/measurement. see also nutrients microbial ecology 9 1-2, 115-8 secondary production 129-30 Guadalupe estuary 156 Guidelines for Systematic Review of Effectiveness of Interventions in Conservation and Environmental Management website 132 Gulf of Mexico 219,415,417, 418 Gulf Stream 7 Gulfwar 417 gyrotactic trapping 209 habitat/s osee also specific habitat types conservation 433-5 fragmentation 299-300 hadal zone 74 haddock 207 haloclines 4 halophytes 164,170 hard substrata, continental shelf 241-4 Hawaii Ocean Time series (HOT) 85 herbivory, fish 232 hermatypic corals 306,309-1 0,320. see also coral reefs hermit crab 237 herring 23,214 heterotrophs 43-4. see also secondary production marine snow 108-9 microbial 98, 122 net ocean productivity 74-6 high-nutrient-lew-chlorophyll (HNLC) regions 51-2,204 highly unsaturated fatty acids (HUFAs) 379 historical accounts aquaculture 378-81 fisheries 358-9 Hong Kong, sustainable fishing 447 HOT (Hawaii Ocean Time series) 85 HUFAs (highly unsaturated fatty acids) 379 human impacts 401-2,428,431. see also climate change; conservation; disturbance; pollution aquaculture 395-7 contaminants 4 19-2 1 continental shelf 2 17 coral reefs 314-8,320,322-3 current changes in sea-ice 350-1

detecting change 4 10-1 estuaries 143, 146, 155--6 eutrophication 4 14-5 experiments 411-2 fisheries 370-5 further reading 428 hydrocarbon exploitation 417, 418 indicators 408 interaction of multiple fact ors 426 measuring/assessment 406--3,442-3 mining 4 17- 9 and natural fluctuations 402 ozone holes 349-50 pelagic ecosystems 194,214-5 renewable energy generation 148 riverine input/land use 413-4 seagrass meadows 299, 300 and secondary production 136-40 shores 172,192 water use 4 16--7 humus, marine 95 hurricanes 315,402 hydrocarbon exploitation 4 17,418 hydrodynamic processes 192 hydrophilous species 291,297 hydrophytes 291 hydroponics 392 hydrostatic pressure, deep sea 259 hydrothermal vents 197, 252, 271- 5 chemosynthesis 261 organism dispersal/gene flow 274-5 organisms 272-3 productivity 272 hypersaline waters 169- 70 hyposaline seas 168-9 hypoxia. see eutrophication; oxygen IATIC (Inter-American Tropical Thna Commission) 361 ibis, scarlet 283 ice-breaking research ships 326--7 ice pancakes 329,330. see also pack ice icebergs 329, 330, 341 ICZM (integrated coastal zone management) 441-2 ideal despotis distribution 163 IDH (intermediate disturbance hypothesis) 404-6 immigration rates 11 increment summation method 130-1 indicators, environmental impacts 408 indices, biodiversity 15, 16, 407, 408, 409 Indo-West Pacific hotspot 19 induction,lytic cycles 110 industrial revolution 57 industrialization, aquaculture 378 infauna 175 inoculu m size 295 inorganic nutrients 49-53, 54

Index •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

integrated coasta l zone management (ICZM) 441-2 Inter-American Tropical Tuner Commission (IATIC) 361

latent cycles, viruses 110 lateral advection 343 latitude, and competition 26 LCA (life cycle analysis) 448

intermediate disturbance hypothesis (IDH) 404--jj

internal waves 175 International Union for Conservation of Nature (IUCN) 433,434 intertidal ecology 173. see also shores invasive species 294-6, 396 invertebrates, human impacts 137-8 Irish Sea glaciation 220 larvae dispersal 221 succession 69 iron 51-2,54 krill 341

and primary production 204-5 irradiance 46--7. see also light in water island biogeography 10--1 IUCN (International Union for Conservation of Nature) 433, 434 jack mackerel, Chilean 357 J amaica 11,316Japan 11,71 jellyfish blooms 214 Juncus spp. 164 J upiter 340 karyostrophy 48 k-ecotypes 106 kelp beds 239 continental shelf 242

global distribution/structuring 244 impact of fishing 375 primary production 76-8 keystone species 182- 3, 204, 336 kill-the-winner hypothesis 110 kinematic viscocity 112-3 kleptoparasitism 237 knees, mangroves 280 krill 19 6, 204, 341, 335-7, 345 K-seleetion 263 KT mass extinction 18 labelling food 442,443-4 lacunar systems 291

lagoons 170 Lagrangian sampling open ocean 21 1 Laguna Madre, Texas 170 land use, human impacts 413-4 Lander systems 253-4 landings, fisheries 359 Langmuir circulation 200-1 large food falls, deep sea 261-2 large oceanic gyres 71 larvae dispersal, scallop 220-1 larval viability, contaminants 419- 20

leatherback turtles 211 lecithototrophic organisms 4,274 legislation, conservation 439-42 leucine growth dynamics, bacterial 115-6 life cycle analysis (LCA) 448 life mode, continental shelf biota 230-1 life-stage, and secondary production 128 Light Detection and Ranging (UDAR) 81 light in water 44-6 acclimation 47-9 continental shelf 223-4 coral reefs 311 deep-sea 257 and photosynthesis 46--9 and primary production 70 zonation 4,45 limiting resources 117-8, 180. see also nutrients lipids 53, 54; see also HUFAs; PUFAs littoral zone 3 lobsters 266 Long Island, Great South Bay 145 long-term data sets 84-6,41 0 low latitude p lankton communities 122 low molecular weight (LMW) products 93 lugworms, experiments 187 lysogenic/lytic cycles, viruses 110 mackerel 2 12,357

Macoma balthica 168 macroalgae. see seaweeds macro-ecology 9 macrofauna, continental shelf 227-9 mammals 345-51,371,433. see also dolphins; polar bears; whales management conservation 440 ecosystem-based 360 fisheries 359-60,368-70 manatees 301-2 mangroves 164, 170, 277-8, 303 adaptations 279-81 associates 278,281-8 carbon storage 34 conservation 436--7 definitions 278-9 d istribution 279 ecosystem function 289-90 further reading 304 primary prod uction 35 reproduction 281 shrimp aquaculture 394 manipulative field experiments. see experiments

mapping, deep-sea 252 Marella 18, 19 Margalefs diversity index 15 marginal ice zone (MIZ) 337,338 Marine Conservation Society Good Fish Guide 443 marine detritus . see detritus marine humus 95 Marine Life Information Network 241, 242 Marine Protected Areas (MPAs) 446 marine reserves 440,442, 444-7 marine snow 95,96,105,107,108-9, 197 Marine Stewardship Council (MSC) 443,

444 market va lue, and conservation 432 MarXan software 435 mass balance calculation 75 mass extinction. see extinction MDS (multi-dimensional scaling) 410 mean troph ic ind ex (MTI) 408 measurement. see also below fisheries stocks 366-8 growth, bacterial 115-8 human impacts 406--13,442 secondary production 129-33 un ivariate measures 40 6--9 measurement, primary production 78-86 automatic devices 82-6 electrodes 79-80 fluorescence 8 1 oxygen 78, 79-80 radiocarbon labelling 78-9 remote sensing 8 1-3 Mediterranean Sea 120,169,257,292, 296 meiofauna 175, 227- 9 melt pools, pack ice 332 membranes, eye 196

Membranipora membranacea 12 7 mesocosms 167,190-1 mesopelagic zone 74,75,196 meta-analyses, secondary prod uction 132-3 metabolism heterotrophic 43-4 microbial ecology 89-91 metazoan zooplankton 111 methane clathrate 7 methanesulphonic acid (MSA) 338 m icrobial ecology 89, 124-5. see also bacteria algae 111-5 archaea 89,97-109 biomass 113 decomposition process 93-7 deep-sea 266

Index food web dynamics 116-8 further reading 125 genomics 101-4 global carbon/nutrient cycles 123-4 growth dynamics/measurement 115-8 growth yield 91-2 Identifying 98-9 key organism groups 97-115 metazoan zooplankton 111 organic-matter degrading species 99-104 as powerhouse of ocean 89-91 prokaryotes 97-109 protozoa 111 seasonal cycles 118-23 size 90-1 trophic structure 114 trophic yield/food chain efficiency 92-3 viruses 109- 11 wider ecological context 91-3 microbial loop 199 rnicrobiota, continental shelf 227-9 microchemistry, fish 158 microlayers 208 mid-ocean ridge 252 migration, continental shelf biota 230-1. see also vertical migration Milankovitch cycles 6 mineralization 89 mining, human impacts 417-9 missing baseline effects 213 Mississipi dead zone 415 mixed layer depth 48-9,203 mixing 70 mixotrophs 44 MIZ (marginal ice zone) 337,338 mobility continental shelf biota 230-1 deep-sea megagfau na 268-70 models, disturbance 40 5 molluscs. see also bivalves; mussels; oysters aquaculture 395-7 biodiversity 10,18-9,20 contaminants 420 monosex stocks, aquaculture 386 Monteray Bay aquarium 440 morphodynamic states, shores 174-7 morpho-species 15 mortality fishing 367-8 measurement 129-30 mosaics, patch 403 MPAs (Marine Protected Areas) 446 MSA (methanesulphonic acid) 338 MSC (Marine Stewardship Council) 443, 444

MTI (mean trophic index) 408 mudflats, estuaries 150 mudskippers 286-8 mullet 157 multibeam echosounders 21 1,220 multidimensional scaling (MDS) 4 10 multivariate measures, human impacts 409-10 mummichog 157,161 Muro-ami fishing 374 mussels 3,161,186,295-6 Mya arenaria 152, 153 myopsin, squid 196

Mytilicola intestinalis 161 nanomaterials 420-1 nanoparticles 420-1 natant organisms 270 natural fluctuations 402 nature-based definitions, welfare 382 nature reserves 440,442,444-7

Nautile 255 nekton. see fish; squid nematode worms 27

Neomysisinreger 154 neritic zone 195, 196, 252 net community/ecosystem/primary production, defi nitions 67 netting, fish 208,252-3,364 networks, shore 190-2. see also food webs/chains neustic zone 196 NGOs (non-governmental organizations) 440 niche differen tiation 283 Nile River 4 16 Nimbus satellite 10 nitrate, seasonal cycles 122 nitrifying prokaryotes, microbial 43, 97-8,101 nitrogen 54,59-60 flux, estuaries 167 isotope ratios 161 pollution 414-5 no n-governmental organizations (NGOs) 440 no n-native species 397,42 1 North America 10, I S, 155 North Atlantic right whale 440-1 North Atlantic cod 238 North Atlantic Oscillation estuarine fish communities 15 7, 159, 160 human impacts 139-40 regime shifts 213 remote sensing 81 North Sea foam 62 regime shifts 213-4

Northeast passage 35 1 Norway, fisheries science 360-1 nucleotides, labelled 115-6 number of species, deep sea 266--7. see also biodiversity nutriclines 119 nutrients/ nutrient dynamics 49--63 algal growth 64-8 Antarctic/Arctic comparisons 340-1 aquaculture 385--6 carbon 55-9, 64 coral reefs 317 cycles, global 123-4 inorganic 49-53,54 iron 51-2,54 nitrogen 54,59-60 phytoplankton 66 seagrass meadows 294 sulphur 54, 60-3 trends, global 70 obligate inhabitants, seagrass meadows 298 ocean basin cross-section 252 ocean currents. see currents oceanic carbon pools 95 oceanic conveyor 258, 328-9 oceanic zone 195,196 oceanography 4-5 offsho re aquaculture 391-3 oil platforms, disposal 446 011 spillage 415,417,418 oligotrophic species/environments 4950,98, 122,204 ontogenetic, definitions 286 ontogenic factors 269 OpenHydro Open-Centre Turbine 148 opticle particle counters (OPCs) 208 organic recycling 96--7 • • • orgamsm size. see size organisms of specific ecosystems. see flora/fa una organotrophs 97-8 osmoconforme rs 153 osmoregulation 153-4 osmotrophs 93, 98 otoliths, fish 158,362 over fishing 359--60 oxygen/oxygen levels 28. see also eutrophication abyssopelagic zone 197 carrying capacity 421 deep-sea 258 estuaries 151 hypoxia 139 mangroves 288 measurement of primary production 78,79,79-80

Index •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

polar regions 345 respiration 42-3 oxygenic heterotrophs 43 oysters 249,349-50,396,421, 426, 427 oystercatche rs 163 ozone holes 349-50 Pacific Ocea n 204,2 13-4 pack ice 326,328,329-32,346. see a150 sea-Ice palaeoecology 232 pancakes, ice 329. 330 parad ox, plankton 208 Paranais spp. 155

parasites 237 particle feeders 232, 243 particle size gradients 175- 7. see also sediment particulate organic carbon (POC) 55 particulate organic material (POM) 94-5, 96 deep-sea 260,262 food webs, microbial 114 marine snow communities 108-9 passive fishing gears 364-5 patches coral reefs 307 mosaics 4 03 patterns, marine 1-2,29. seeal.so seasonal cycles; spatial patterns; temperature; temporal patterns; zonation abundance/size 23-8 biodiversity 9,15-22,165-8 biogeography 9-15 biomes 11-2 climate 6-7 endemism 12-5 estimating past changes in sea-ice 338-9 estuaries 165-8 further reading 29 local versus regional 11 oceanography 4-5 pelagic ecosystems 200-7 polar regions 339 predator-prey systems 163 productivity 8-9 secondary production 132- 3 shore zonation causes 179- 81 PCBs (polychlorinated biphenyls) 4 19 pelagic ecosystems 194-5, 215--6 definitions 19 5-7 fisheries 212-3 further reading 2 16 future scenarios 214-5 physical processes 200-3 primary production/biogeography 203-5

regime shifts 19 5, 213-4 sampling open ocean 208-12 size, consequences 198-200 temporaVspatial patterns 200-7 penguins 284-5,346 Peruvian anchovy 134,357 pH 38-9,57,79 Phaeocystis spp. 62 phase shifts 122. see also regime shifts Philippines 436-7 phosphorus 54, 60 photic zone 45, 196 photo-acclimation, polar regions 334 photo-respiration 94 photography, wildlife 157, 253- 5, 258 photophores 258 photosynthesis 36-42. see also primary production algal growth 66 carbon dioxide 38-41 and light 46-9 pigments 4 1-2 seasonal cycles, microbial 119, 121 photosynthetic quotient (PQ) 55 phylogeography 13 physical processes continental shelf 219 coral reefs 3 11 d eep-sea 256--60 pelagic ecosystems 200-3 physics of seawater 198 physiological tolerance, and zonation 179 phytodetritus, continental shelf 223 phytoplankton. see also algae blooms 71, 120-1, 4 14 fronts, biological 223 n utrient dynamics 66 prod uctivity 8,9,35 remote sensing 8 1,82 shape 52-3 succession 69 pigments, photosynthetic 41-2 plaice continental shelf biota 230-1 hu man impacts 138-9, 373 plankton. see also phytoplankton; zooplankton larvae dispersal 220-1 paradox 208 pelagic ecosystems 198- 9 planktotrophic organisms 4 plasticity, seagrasses 292 plastochrone intervals 297 Plum Island Sound Estuary 161 pneumatocysts 77 poe (particulate organic carbon) 55 polar bear 347-8,350 polar regions 325-9, 352 Arctic!Antarctic comparisons 331-2

bentho-pelagic coupling 343 benthos 34 1-4 birds/mammals 345-51 current changes in sea-ice 350-1 endemism 343-4 estimating past changes in sea-ice 338-9 further reading 352-3 gigantism 28,344-5 organisms 11-2,205,332-7 pack ice 329-32 primary production 71 sea ice edges 337-41 policy, conservation 439-42 pollock, Alaskan 357 pollu tion and biodiversity 16 coral reefs 317 eutrophication 4 14-5 human impacts 419-21 oil spillage 4 17-8 polychlorinated biphenyls (PCBs) 419 polyculture 378,383 polyphyletic taxa, seagrasses 291 polyps, coral reef 309-10 polyunsaturated fatty acids (PUFAs) 335, 340 POM. see particulate organic material Pompeii worm 272 population biology aquaculture 390 fisheries 362-3,366 population dynamics coral reefs 320-2 krill 337 Porcupine Sea Bight 262-3,264,266 Portuguese Man '0 War 7, 196 PQ (photosynthetic quotient) 55 pravons 152, 153,269 precautionary approach to fisheries management 368 predator-prey systems. see also food webs continental shelf 23 1-2,237 estuaries 163 shores 181- 7 seagrass meadows 300 preliminary sampling 411 primary production 33-4,87 algal growth 64-8 consequences for higher trophic leve ls 205-7 continental shelf 2 17 by ecosystem type 34 and fronts, biological 223 further reading 87-8 global trends 69-76 heterotrophic metabolism 43, 43-4 inorganic nutrients 49-53 light in water 44-6, 45,46-9

Index marine plants/algae 34-6 measurement 78-86 nutrients limiting growth 53-63 pelagic ecosystems 203-5 photosynthesis 36--42,46-9 phytoplankton 35,36 polar regions 339 respiration 42,42-3 seasonal trends 69 seaweeds 76-8 and secondary production 134-5 terrestrial comparison with aquatic 73 primary space, shores 183 procedural control 288 production-to-biomass ratio (P/B) 129. see also secondary production and body mass 131- 3 human impacts 137-8 productivity/ production. see also primary; secondary production aquaculture 381,385 autochthonous 160 bacterial 116 coral reefs 3 11-3 deep sea 260-3 definitions 67 estuaries 159- 65 fisher ies 361 and fronts, biological 223 hydrothermal vents 272 patterns, marine 8-9 seagrass meadows 302 seasonal cycles, microbial 118-23 prokaryotes 97-109. see also microbial ecology propagule pressure 295 propagules, mangroves 281 proteobacteria 100-1, 107 proteomics 102 proton acceptors 42, 43 protozoa I II protozoop lankton 338 provinces 12, 205 pseudofaeces 232 PUPAs (polyunsaturated fatty acids) 335, 340 purple sulphur bacteria 43 purse seine netting 364 pycnoclines 4, 339 pyrosequencing 102

quorum sensing 10 7 radiations, evolutionary 17 radiocarbon labelling 78-9 ragworm 152, 154, 167, 186 rainfali 422 ramets 297 ranching, aquaculture 397-8

realized nich es 266 recirculation systems 391-3 recolonization/recovery rates, afte r disturbance 4 03-4 recruitment strength 183 recyciing 96-7,120,121-3 red coloured crustaceans 197 Red List (lUCN) 434 Redfield ratio 54-5 redshank 163 redundancy hypothesis, biod ivers ity 15, 22 reefs, continental shelf 248-9. see also coral reefs reference points, fisher ies 368 reflective beach es 177 regime shifts coral reefs 314 impact of fishing 375 pelagic ecosystems 195, 2 13-4 regions of freshwate r in fluen ce (ROFIs) 223 regulations, conservation 440-2 Remane diagrams 165--6 remineralization 89,334 remote sensing 195 animal attached 284-5 primary production 8 1-3 polar regions 336--7 remotely operated vehicles (ROVs) 253 ,254 renewable energy 147-8, 159-60 replacement lines, fish eries 367-8 replicates 412-3 reproduction coral reefs 310-1 mangroves 281 seagrass meadows 296-8 reptant organisms 270 research, river catchment to coast 218. see also experiments reserves, marine 440,442,444-7 resilience, ecosystem 235-7,320 resource limitation 11 7-8, 180. see also nutrients respiration 42,42-3 and decomposition process 93-4 microbial 89, 119, 121 patterns, marine 75 seasonal cycles 119, 121 vertical distribution 74 resuspension, sediment 343 Reynolds' number 112- 3, 198 ribulose biphosph ate carboxylase/ oxygenase (RUBISCO) 37,39-40 Riftia 272-4 right whale 440-1 Rio Convention on Biological Diversity 440 rippies 45-6

river disch arge, human impacts 4 13-4, 417, 423. see also individual rivers by

name riverine mangroves 278 rivet hypothesis of biodiversity 22 rocky/sandy shores. see shores rock substrata, continental shelf 241-4 ROFIs (regions of freshwater in fluen ce) 223 Roman times 378 root structures, mangroves 280 Rose Garden hydrothermal vent 2 71,274 ROVs (remotely operated veh icles) 253,254 R-selection 263 rubbish pollution 215 RUBISCO (ribulose biphosphate carboxylase/oxygenase) 37,39-40 SAHFOS (Sir Alistair Hardy Foundation for Ocean Science) 84 Salicornia spp. 164 salinity estuaries 148- 9 hyposaline seas 168 impact of freshwater inflow 154-6 lagoons 170 mangrove adaptations 279-81 pack ice 330 response of organisms 153-4 seagrass tolerance 294 shores, rocky/ sandy 176--7 zonation 4,5, 176--7 salmon aquaculture 389-91 salt-wedge effect 149 saltmarsh systems 163- 5, 277-8 sampling deep sea 252-5 measuring hu man impacts 408 open ocean 208-12 pitfalls 412-3 San Andreas fau lt 145 San Francisco Bay 145 sandpiper 161-2 sandy shores. see shores Sargasso Sea 262 satellite sampling 211 saturation irradiance 46 scale, microbial ecology 89. see also size scallops 220-1,299 scarlet ibis 283 scavengers continental shelf 23 1 deep-sea 261-2 scrence conservation 447-8 fisheries 360-1 scouring, by sea-ice 341 sea cows 301-2,429

Index •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

sea horses 398 sea-ice 328. see also pack ice biota 332 birds/ mammals 346 current changes 350-1 edges 337-41 past changes 338-9

sea level changes 7,144-5,151-2 climate change 422 coral reefs 309 glaciation 219-22 sea lice 389-91 sea mounts 252,372-3 sea ranching 397-8 sea temperature. see temperature sea urchins and acidification 425 barren grounds 239, 375 coral reefs 319 deep-sea 268-9 and fish communities 318 seabed habitats 1, 4 continental shelf 224-31 fisheries 371-4 human impacts 138- 9, 371-4 Seafood Choices Alliance 443 seagrass meadows 277,303,277-8 associated organisms 298-301 carbon storage 34 definitions 278-9,290-1 distribution 292--6 ecosystem function 302-3 further reading 304grazing 301-2 primary production 35,78 reproduction 296-8 seals 211 ,346,347,349 seasonal cycles/dynamics. see also temperature; temporal patterns abundance 23 autumn 118,119,122, 123 microbial ecology 117-23 po lar regions 326,327-8 primary production 69 secondary production 128-9 spring 118, 12G-1 , 206 summer 118,121-3 winter 118, 123 seawater, physics of 198. see also temperature seaweeds. see also kelp beds carbon storage 34 po lar regions 342-3 primary production 35,76--8 and seagrass meadows 294 SeaWiFS project 36,195 secondary production 126-8, 140 allometric re lationships 131-3 to biomass ratio 128

d rivers 134-6 further reading 140 human impacts 136-40 measurement 129-33 meta-analyses 132-3 size structuring 136 secondary space, shores 183 sedentary megafauna, deep sea 267-8 sediment continental shelf 241,245-8 coral reefs 311,317 deep sea 259-60, 268 ecosystem function 234-5 estuaries 150, 154 human impacts 413-4 influence of fauna on structure 233 manipulative experiments 190-1 and mining 4 19 resuspension 343 shores, rocky/sandy 174, 180 size gradients 175- 7 suspended 223 terrigenous 195 wave action 220 seine netting 364 self-sustaining seasonal cycles 122 sessile organisms deep-sea 267 definitions 286 Severn estuary, energy generation 14 7-8 shags, impact of fishing 371 Shannon-Weiner diversity index 15, 40 7, 409 shape, phytoplankton 52-3 shark, basking 285 shelf break 218,252 Shinkai 6500 255 shipp ing lanes 441,445 shore crab 154 shores, rocky/sandy 172,192-3 biodiversity 190-1 bottom-up processes 181, 183, 188 definitions 173 disturbance/bioturbation 188, 191 environmental gradients 173-9 experiments 181-2, 184-7, 190-1 further reading 193 future scenarios 192 organization of communities 18 1- 9 particle size gradients 175-7 primary/ secondary space 183 salinity gradients 176--7 shore networks 190-2 wave action exposure 174-5 wetness/dryness gradients 173 zonation 177-81 shotgun sequencing 102 shrimps 157,377,387,393-4 siphon cropping clam 127, 128

Sir Alistair Hardy Foundation for Ocean Science (SAHFOS) 84 sites of special scientific interest (SSSIs) 440 Sivash 169- 70 size, organism 27-8 and abundance 23 and biomass 91 continental shelf 227-9 deep sea 264-5, 27G-1 food webs 136 measuring effects of human activities 406 microbial 90-1 and P/B ratios 131-3 pelagic ecosystems 198-200 polar regions 28, 344-5 sloppy feeding 94 smelt 157 snow, marine 95,96, 105,107,108-9, 197 snowball earth 340 social circumstances, human 432,442 soft sediment, continental shelf 245-8 solubility pump 57 somatic secondary production 128 Sorcerer II 102, 103 Southern Ocean Arctic!Antarctic comparisons 332 biodiversity 20 Bouvet Island 11 diatoms 333-4 high-nutrient-low-chlorophyll regions 204 krill 335-7 nutrients limiting growth 340-1 organisms 334 sea-ice changes 339 sea temperature changes 6 southern right whale 86 Spartina spp. 164 spatial patterns biodiversity 18- 21 pelagic ecosystems 200-7 spawner-recruitment relationships 363 speciation rates 11 species richness. see biodiversity species-area relationships 11. see also biodiversity sponges 242,345 spring blooms/cycles 118, 120-1, 206 squat lobster 266 squid 196, 199,205-7,213,363 SSSIs (sites of special scientific interest) 440 stable carbon isotopes 40,160-1 stakeholders 440 starfish 1,182,237,316-7 statistics

Index aquaculture 381,385 detecting change 411 fisheries 357-8 stepping stone models 274 stickleback, three-spined 157 stipules 288 stochastic peturbations 286 stock-recruitment relationships 362-3 stocks, fisheries 361 ,366-8 Stommel diagram 200-1 storms, coral reefs 315 stratification, continental shelf 223. see also zonation stressed environments 426. see also human impacts biodiversity 15 coral reefs 310 current velocity 229 estuaries 146,168 microbial ecology 94 response of organisms 153-4 submersibles, deep sea 255 subsidized fleets, fisheries 359 substrates, chemical 39 success, definitions 26--7 succession, phytoplankton 69 Sueda spp. 164 sulphur 54,6G-3 sulphur-oxidizing/reducing bacteria 43 summer seasonal cycles 118,121-3 supply-side ecology 183 surface area and biomass 113 to volume ratios 28,90 surface currents 6 suspended rope cultivation, bivalve molluscs 396,397 suspended sediment 223 suspension feeding 232 sustainable development 431 ,435 sustainable fishing 447 Swan River estuary, Australia 156 swell 175 Symbion pandora 2 symbiosis 310, 425 synergistic effects, human impacts 426 syngnathids 399,400 tannin 289 taxonomic distinctness 15,409 diversity 15 TBT (tributyl tin ) 42G-I technical measures, fisheries management 368 tectonic estuaries 145 telemetry 285 temperature, land/ sea. see also climate change; seasonal cycles/dynamics

coral reefs 306,311,316 deep-sea 257-8 estuaries 151 polar regions 328 response of organisms to 154 temporal patterns 5, 6. see also seas onal cycles/dynamics abundancelbiodiversity 16-8, 23, 25 food inputs, deep sea 262-3 pelagic ecosystems 200-7 primary production 69 TEPs (transparent exopolymer particles) 95 terrestrial habitats carbon pools 95 and mangroves 281-5 primary production 73, 76 terrigenous sediment 195 tethering, and seagrass meadows 298 TEV (total economic value) 436 Thames, River 146,156,157,159,422 thermoclines 4,5, 118, 122 three-spined stickleback 157 thymidine, labelled 115-6 tidal energy generation 147-8 tidal-mixing 204 tidal range Bay of Fundy 149 continental shelf 222-3 estuaries 146 tidal surges 422 tide-dominated mangroves 278 timescales. see temporal patterns

Titanic 272 top-down control food web dynamics 116-7 secondary production 134 shore communities 181 topographical classification of estuaries

144, 145, 149 total economic value (TEV) 436 tourism and climate change 421 coral reefs 322-3 willingness to pay 438 trace fossils 232 Trades biome 11-2,205 transcriptomics 102 transparent exopolymer particles (TEPs)

95 trawling 137-9,252-3,364,371-4 trenches, deep sea 252 tributyl tin (TBT) 42G-I triploidy 386 trophic cascades 237-8 trophic function 16 trophic levels 12,91 secondary production 126 size str ucturing 136

trophic structure, microbial 114. see also food webs trophic yield/food chain efficiency 92-3 tropical waters, primary production 70 true mangroves 278 tube worms 186 Tubifex tubifex 155 tuna 194 aquaculture 384-5 dolphin-safe 213 fisheries 363,364,371 turbidity continental shelf 223-4 and seagrass meadows 293 turbulent eddies 229 turtles 211,301,371 type 1/11 errors 411 UK Sustainable Development Commission

148 ultraviolet (UV) light 7 adaptations to 196 algal growth 64 damage 63 ozone holes 349-50 and seagrass meadows 293 ultrahaline conditions 170 Ulva spp. 154 univariate measures 406-9 universal features, zonation 178, 179-81 uplift zones 177 upwelling 71,422,426 urchin barren grounds 239,375. see also sea urchins US Magnuson-StevensAct 372 UV. see ultra violetlight valuation, marine ecosystems 437 Van der Waals forces 245 variance, spawner-recruitment relationships 363 vertical migration 199, 339-40 vicariance hypothesis 279 viruses 109-11,116-7 vivipary 281,291 volume to surface area ratios 28, 90 vulnerability to fishing 370 walruses 347 waste/rubbish pollution 215 water circulation 422. see also currents, ocean water use, human impacts 416-7 waterlogged soils, adaptations 279 wave action coral reefs 311 patterns, marine environmental 5 shores , rocky/sandy 174-5 temporal/spatial patterns 200

Index •••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••••

wave formation 175 websites aquaculture 383,386,391 autonomous underwater vehicles 2 12 conservation 433, 443 Convention on the Conservation of

Antarctic Marine Living Resources 436 coral reefs 306, 308 fish production 135 Great Barrier Reef Marine Park 445

Guidelines for Systematic Review of Effectiveness of Interventions in Conservation and Environmental Management 132 invasive species 295 MarXan software 435

OpenHydro Open-Centre Turbine 148 photography 157,258 sea horses 399 Seafood Choices Alliance 443 Sorcerer II 103 stock-recruitment relationships 363

UK Sustainable Development Commission 148

world register of marine species 90

World Resources Institute 266 World Summit on Sustainable Development 432 welfare, fish 382, 384 Westerlies biome 11-2,205 wetness/dryness gradients, shores 173 whales 86 biogeography 204 conservation 433, 440-1 extinction 429 impact of fishing 371 polar regions 338-9, 348-9 whe lks 237 White Sea 169-70 whiting 157, 406 wildiife photography 157, 253- 5, 258 wiliingness to pay (WTP) 437,438 wind action and climate change 426 pelagic ecosystems 200,201-2 wind speed patterns 5 winter seasonal cycles 118, 123 wood, deep-sea 262 World Resources Institute 266 World Summit on Sustainable Development (WSSD) 432,440

wrasse 322,389-91 WTP (wiliingness to pay) 437,438 xenophyophores, deep-sea 270-1 Yellow River 4 14 yield-per-recruit models 367 zonation 2-4 causes 179- 8 1 continental shelf 223-4 coral reefs 31 1 estuaries 15 1 pelagic ecosystems 196--7 shores 173-9 universal features 178 zooanthellae 309,311 zooplankton coral reefs 312 metazoan III polar regions 338 productivity 8, 74, 75 vertical migration 199 Zostera spp. 294, 297-8, 300, 302

This page intentionally left blank