Respiration in Aquatic Ecosystems This page intentionally left blank Respiration in Aquatic Ecosystems EDITED BY Paul A. del Giorgio Université du Québec à Montréal, Canada Peter J. le B. Williams University of Wales, Bangor, UK 1 3 Great Clarendon Street, Oxford OX2 6DP 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 Bangkok BuenosAires Cape Town Chennai Dar es Salaam Delhi Hong Kong Istanbul Karachi Kolkata Kuala Lumpur Madrid Melbourne Mexico City Mumbai Nairobi São Paulo Shanghai Taipei Tokyo Toronto 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 2005 The moral rights of the author have been asserted Database right Oxford University Press (maker) First 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 this same condition on any acquirer A catalogue record for this title is available from the British Library Library of Congress Cataloging in Publication Data (Data available) ISBN 0 19 852709 8 (hbk) ISBN 0 19 852708 X (pbk) 10987654321 Typeset by Newgen Imaging Systems (P) Ltd., Chennai, India Printed in Great Britain on acid-free paper by Antony Rowe Ltd., Chippenham Preface Respiration, in its various biochemical manifestations, is the process by which all organisms obtain vital energy from a variety of reduced compounds, and represents the largest sink of organic matter in the bio- sphere. Although respiration is at the center of the functioning of ecosystems, much of contemporary ecology has chosen to focus attention and research on the productive processes rather than on catabolism. Almost certainly, respiration represents a major area of ignorance in out understanding the global carbon cycle. We decided to embark in this project during the 2000 ASLO meeting in Copenhagen, right after a session on aquatic respiration organized by Erik Smith and one of us. To our knowledge, it was among the first sessions entirely devoted to aquatic respiration at an international meeting, and although we had hoped to attract some interest, we never expected to fill the largest room in the conference center! It become clear that there was a tremendous interest in the topic within the aquatic scientific community, and that there was a need for synthesis and direction in this area of research. No textbook that had reviewed and synthesized the extant information on respiration in natural aquatic systems, independent of production or other traditional areas of focus. In spite of its obvious ecological and biogeochemical importance, most oceanographic and limnologi- cal textbooks usually deal with respiration superficially and only as an extension of production. We set out to fill this gap and provide the first comprehensive review of respiration in aquatic systems, with the help of an outstanding and diverse group of researchers who laid down a biochemical basis, examined the patterns and scales of respiration in diverse aquatic ecosystems. The result is a synthesis that spans the major aquatic ecosystems of the biosphere, and an in depth analysis of the current state of understanding of respiration in aquatic systems. It is our hope that this collective effort will help establish the main scientific questions and challenges that face this particular field, and more important, help bring respiration into focus as a priority area of future research. The book is mainly directed to respiration occurring in the water column of aquatic systems, because there are other excellent textbooks that extensively discuss sediment metabolism. Sediment respiration is discussed in the broader context in individual chapters, as part of the specific aim of integrating water column and benthic metabolic processes. We first (Chapters 1-5) lay down a basis to understand respiration within major categories of organisms, the photoautotrophs, the bacteria, the protozoa and the planktonic metazoa. We then (Chapters 6-12) consider the process in a series of aquatic ecosystems and the current status of attempts to model respiration in various plankton groups (Chapter 13). As the book progresses we shall seek to assess the current state of knowledge concerning respiration in aquatic ecosystems, and to address a series of questions that are key to understanding this process at the ecosystem and biospheric level. Finally, we wish to thank Hugh Ducklow, Jonathan Cole, Mike Pace, Ian Joint and Morten Søndergaard for reviewing various portion of this book. We also thank Ian Sherman and Anita Petrie of Oxford University Press for their patience and encouragement for this project, Ann Mitchel for providing a cover design and Paula Conde for help in editing manuscripts. Paul del Giorgio acknowledges the financial support of the National Science and Engineering Council of Canada. Finally, we would like to dedicate this book to Lawrence Pomeroy and to the late Robert Peters, two pioneers and visionaries who understood early on the importance of respiration in aquatic ecosystems. This page intentionally left blank Contents List of contributors ix 1 Respiration in aquatic ecosystems: history and background 1 Peter J. le B. Williams and Paul A. del Giorgio 2 Ecophysiology of microbial respiration 18 Gary M. King 3 Respiration in aquatic photolithotrophs 36 John A. Raven and John Beardall 4 Respiration in aquatic protists 47 Tom Fenchel 5 Zooplankton respiration 57 Santiago Hernández-León and Tsutomu Ikeda 6 Respiration in wetland ecosystems 83 Charlotte L. Roehm 7 Respiration in lakes 103 Michael L. Pace and Yves T. Prairie 8 Estuarine respiration: an overview of benthic, pelagic, and whole system respiration 122 Charles S. Hopkinson, Jr and Erik M. Smith 9 Respiration and its measurement in surface marine waters 147 Carol Robinson and Peter J. le B. Williams 10 Respiration in the mesopelagic and bathypelagic zones of the oceans 181 Javier Arístegui, Susana Agustí, Jack J. Middelburg, and Carlos M. Duarte 11 Respiration in coastal benthic communities 206 Jack J. Middelburg, Carlos M. Duarte, and Jean-Pierre Gattuso 12 Suboxic respiration in the oceanic water column 225 Louis A. Codispoti, Tadashi Yoshinari, and Allan H. Devol 13 Incorporating plankton respiration in models of aquatic ecosystem function 248 Kevin J. Flynn 14 The global significance of respiration in aquatic ecosystems: from single cells to the biosphere 267 Paul A. del Giorgio and Peter J. le B. Williams This page intentionally left blank List of contributors Susana Agustí Allan H. Devol IMEDEA (CSIC-UIB) School of Oceanography Grupo de Oceanografía Interdisciplinar (GOI) University of Washington Instituto Mediterráneo de Estudios Seattle, WA 98195 Avanzados, C USA Miquel Marqués, 21 Carlos M. Duarte 07190 Esporles (Mallorca) Spain IMEDEA (CSIC-UIB) Grupo de Oceanografía Interdisciplinar (GOI) Instituto Mediterráneo de Estudios Avanzados, C Javier Arístegui Miquel Marqués, 21 Facultad de Ciencias del Mar 07190 Esporles (Mallorca) Campus Universitario de Tafira Spain Universidad de las Palmas de Gran Canaria Tom Fenchel 35017 Las Palmas de Gran Canaria Marine Biological Laboratory Spain University of Copenhagen DK-3000 Helsingør John Beardall Denmark School of Biological Sciences Monash University Kevin J. Flynn Clayton Ecology Research Unit VIC 3800 University of Wales Swansea Australia Swansea SA2 8PP UK Louis A. Codispoti Jean-Pierre Gattuso University of Maryland Center for Laboratoire d’Océanographie de Villefranche Environmental Science CNRS and University of Paris 6 Horn Point Laboratory B. P. 28 P.O. Box 775 06234 Villefranche-sur-Mer Cedex Cambridge France MD 21613 USA Santiago Hernández-León Biological Oceanography Laboratory Paul A. del Giorgio Facultad de Ciencias del Mar Département des sciences biologiques Universidad de Las Palmas de Gran Canaria Université du Québec à Montréal Campus Universitario de Tafira CP 8888, Succ. Centre Ville 35017 Las Palmas de GC Montréal, Québec Canary Islands Canada H3C3P8 Spain x List of contributors Charles S. Hopkinson, Jr John A Raven Ecosystems Center Division of Environmental and Applied Biology Marine Biological Laboratory University of Dundee at SCRI Woods Hole, MA 02543 Invergowrie USA Dundee DD2 5DA UK Tsutomu Ikeda Carol Robinson Marine Biodiversity Laboratory Plymouth Marine Laboratory Graduate School of Fisheries Sciences Prospect Place Hokkaido University West Hoe 3-1-1 Minato-cho Plymouth, PL1 3DH Hakodate 041-0821 UK Japan Charlotte Roehm Gary M. King Département des sciences biologiques Darling Marine Center Université du Québec à Montréal University of Maine CP 8888, Succ. Centre Ville Walpole Montréal, Québec USA 04573 Canada H3C3P8 Jack J. Middelburg Erik M. Smith Netherlands Institute of Ecology Department of Biological Sciences (NIOO-KNAW) University of South Carolina P.O. Box 140 Columbia, SC 29208 4400 AC Yerseke USA The Netherlands