New Directions in Ecological Physiology New...

The past fifty years have witnessed major achievements in ecological physiology, the study of physiological adaptations that improve survival or permit organisms to exploit extreme environments. New Directions in Ecological Physiology outlines novel conceptual approaches to the study of physiological adaptation in animals, approaches that will stimulate the continued growth of this field.

Twenty leading ecological physiologists and evolutionary biologists have contributed critical evaluations of developments in their respective areas, highlighting major conceptual advances as well as research questions yet to be answered. The volume is organized into three parts: The first deals with comparisons of different species and populations; the second, with comparisons of individuals within a population; the last, with interacting physiological systems within individual animals.

New Directions in Ecological Physiology, by encouraging critical debate about general issues and directions of growth in this field, is intended to foster the invigoration of ecological physiology in particular and of organismal biology in general.

Martin E. Feder is Associate Professor of Anatomy and in The Committee on Evolutionary Biology, The University of Chicago; Albert F. Bennett is Professor of Developmental and Cell Biology and Professor of Ecology and Evolution, University of California, Irvine; Warren W. Burggren is Professor of Zoology, University of Massachusetts, Amherst; and Raymond B. Huey is Professor of Zoology, University of Washington, Seattle.

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NEW DIRECTIONS IN ECOLOGICAL PHYSIOLOGY






NEW DIRECTIONS IN ECOLOGICAL PHYSIOLOGY

Editors MARTIN E. FEDER The University of Chicago

ALBERT F. BENNETT University of California, Irvine

WARREN W. BURGGREN University of Massachusetts

RAYMOND B. HUEY University of Washington

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© Cambridge University Press 1987

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First published 1987

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Library of Congress Cataloguing in Publication Data

New directions in ecological physiology.Includes index.1. Adaptation (Physiology). 2. Ecology.3. Physiology. I. Feder, Martin E.QH546.N48 1987 574.5 87-24252

isbn 978-0-521-34138-7 Hardbackisbn 978-0-521-34938-3 Paperback

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Contents

Contributors and discussants Preface

1 The accomplishments of ecological physiology Albert F. Bennett

PART ONE: COMPARISONS OF SPECIES AND

page vii IX

1

POPULATIONS 9

2 Interspecific comparison as a tool for ecological physiologists 11 George A. Bartholomew

Discussion 35

3 The analysis of physiological diversity: the prospects for pattern documentation and general questions in ecological physiology 38

Martin E. Feder Discussion 71

4 Phylogeny, history, and the comparative method 76 Raymond B. Huey

Discussion 98

5 A multidisciplinary approach to the study of genetic variation within species 102

Dennis A. Powers Discussion 130

6 Comparisons of species and populations: a discussion 135 William R. Dawson

PART TWO: INTERINDIVIDUAL COMPARISONS 145

7 Interindividual variability: an underutilized resource 147 Albert F. Bennett

Discussion 166

v






vi CONTENTS

8 The importance of genetics to physiological ecology 170 Richard K. Koehn

Discussion 186

9 Genetic correlation and the evolution of physiology 189 Stevan J. Arnold

Discussion 212

10 The misuse of ratios to scale physiological data that vary allometrically with body size 216

Gary C. Packard and Thomas J. Boardman Discussion 236

11 Interindividual comparisons: a discussion 240 Douglas J. Futuyma

PART THREE: INTERACTING PHYSIOLOGICAL SYSTEMS 249

12 Invasive and noninvasive methodologies in ecological physiology: a plea for integration 251

Warren W. Burggren Discussion 272

13 The use of models in physiological studies 275 Peter Scheid

Discussion 285

14 Symmorphosis: the concept of optimal design 289 Stan L. Lindstedt and James H. Jones

Discussion 305

15 Assigning priorities among interacting physiological systems 310 Donald C. Jackson

Discussion 326

16 Physiological changes during ontogeny 328 James Metcalfe and Michael K. Stock

Discussion 340

17 Interacting physiological systems: a discussion 342 David J. Randall

18 New directions in ecological physiology: conclusion 347 Martin E. Feder

Author index 353 Subject index 360






Contributors and discussants

STEVAN J. ARNOLD, Department of Biology, The University of Chicago, 940 East 57th Street, Chicago, Illinois 60637

GEORGE A. BARTHOLOMEW, Department of Biology, University of California, Los Angeles, California 90024

ALBERT F. BENNETT, School of Biological Sciences, University of California, Irvine, California 92717

STEVEN BISHOP, Regulatory Biology Program, National Science Foundation, Washington, D.C. 20550

THOMAS J. BOARDMAN, Department of Statistics, Colorado State University, Fort Collins, Colorado 80523

WARREN W. BURGGREN, Department of Zoology, University of Massachusetts, Amherst, Massachusetts 01003

JAMES P. COLLINS, Population Biology and Physiological Ecology Program, National Science Foundation, Washington, D.C. 20550. [Present address: Department of Zoology, Arizona State University, Tempe, Arizona 85287J

MARK W. COURTNEY, Population Biology and Physiological Ecology Program, National Science Foundation, Washington, D.C. 20550

WILLIAM R. DAWSON, Division of Biological Sciences, University of Michigan, Ann Arbor, Michigan 48109

JAMES L. EDWARDS, Biological Research Resources Program, National Science Foundation, Washington, D.C. 20550

MARTIN E. FEDER, Department of Anatomy and The Committee on Evolutionary Biology, The University of Chicago, 1025 East 57th Street, Chicago, Illinois 60637

GREGORY L. FLORA NT, Department of Biology, Swarthmore College, Swarthmore, Pennsylvania 19081

DOUGLAS J. FUTUYMA, Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794

LEW I S G R E E N W A L D, Regulatory Biology Program, National Science Foundation, Washington, D.C. 20550. [Present address: Department of Zoology, Ohio State University, Columbus, Ohio 43210J

RAYMOND B. HuEY, Department of Zoology NJ-15, University of Washington, Seattle, Washington 98195

vii






viii CONTRIBUTORS AND DISCUSSANTS

DONALD C. JACKSON, Division of Biology and Medicine, Brown University, Providence, Rhode Island 02912

JAMES H. JONES, Department of Physiological Sciences, School of Veterinary Medicine, University of California, Davis, California 95616

RICHARD K. KOEHN, Department of Ecology and Evolution, State University of New York, Stony Brook, New York 11794

STAN L. LINDSTEDT, Department of Zoology and Physiology, The University of Wyoming, University Station, Box 3166, Laramie, Wyoming 82071

J AMES METCALFE, Department of Medicine, Heart Research LaboratoryL464, Oregon Health Sciences University, 3181 S.W. Sam Jackson Park

Road, Portland, Oregon 97201 GAR Y C. PACKARD, Department of Zoology, Colorado State University,

Fort Collins, Colorado 80523 DENNIS A. POWERS, Department of Biology, The Johns Hopkins Univer

sity, 3400 North Charles Street, Baltimore, Maryland 21218 [mailing address]; and Center for Marine Biotechnology, University of Maryland, Baltimore, Maryland

DA VID J. RANDALL, Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 2A9, Canada

PETER SCHEID, Institut fUr Physiologie, Ruhr-Universitat, Universitatstrasse 150, D-4630 Bochum, West Germany

MICHAEL K. STOCK, Department of Medicine, Heart Research Laboratory - L464, Oregon Health Sciences University, 3181 S.W. Sam Jackson Park Road, Portland, Oregon 97201

BRUCE L. UMMINGER, Division of Cellular Biosciences, National Science Foundation, Washington, D.C. 20550






Preface

Modern physiology has two primary objectives. The first is the understanding of the central unifying principles by which physiological function is governed. Such unifying principles transcend particular taxa, environments, developmental stages, and so on. The second is the understanding of physiological diversity in biological molecules, cells, tissues, organs, and organisms. This objective concerns the origin of physiological diversity, the constraints upon it, and its consequences for physiological function. This book is about the attempts of one subdiscipline of physiology, ecological physiology, to attain this second objective. Ecological physiology examines physiological diversity in relation to the environments in which organisms live or have lived. It is also termed "physiological ecology" and "ecologically relevant physiology"; we will use these terms interchangeably. The terms themselves, however, fail to express the breadth of the enterprise, which embraces aspects of behavior, morphology, biochemistry, and evolutionary biology, among other fields.

As summarized by the first two chapters of this volume, ecological physiology has made considerable progress in understanding physiological diversity and in establishing itself as a scientific discipline. Along with the achievements of ecological physiology, however, have come the perceptions that little of real novelty remains to be investigated. There is a sense that "the cream has been skimmed off the top" of the analysis of physiological diversity. Along with enormous increases in our understanding of physiological adaptation has come the perception that "adaptation" may be trite, flawed, or inadequate as a conceptual basis for future progress. As Albert Bennett wrote in the proposal for support of the workshop that preceded this volume:

I have frequently encountered questions concerning the significance of specific projects and the general goals and directions of the field. In my conversations with many people, I sense a real lack of perceived focus and direction in the field as a whole. People are generally aware of where we have been but not where we are going. There is no sense of movement towards general questions or goals and often a sense that these do not exist.

Whether these perceptions are accurate ones is an important question that is taken up at length in the following chapters.

This volume stemmed from a mutual conviction of the editors that eco-

ix






X PREFACE

logical physiology is very much alive and well. We were concerned, however, that misplaced perceptions of lack of directions, foci, and goals were proving increasingly inimical to the vitality of ecological physiology. Furthermore, we felt that these perceptions were often understandable because practitioners of ecological physiology seldom made explicit statements of general goals or likely avenues for future developments. We decided, therefore, that the time had come for a public discussion of goals and future directions in ecological physiology. By virtue of our own research interests, we confined the project to the ecological physiok 'y of animals.

We invited participants to a wc -kshop with the understanding that each would contribute a manuscript base,~ upon the presentation at the workshop. To set an appropriate tone for the workshop, the editors posed some conceptual questions to each participant; some of these questions are included verbatim in the following chapters. The workshop was held in late May, 1986, in Washington, D.C. Each of three morning sessions, corresponding to the three sections in this book, included four to five presentations on assigned topics. A discussion, led by assigned discussants, occupied each entire afternoon. The discussions were recorded in their entirety; the assigned discussants edited the transcripts of these recordings that appear at the end of many chapters of this book. Manuscripts based on the morning presentations were subsequently reviewed both by the editors and by reviewers who were not present at the workshop. The editors are extremely grateful for these lengthy and uniformly constructive external reviews. The workshop was supported by the National Science Foundation under Grant BSR 86-07794. Any opinions, findings, and conclusions or recommendations expressed in this publication are those of the authors and do not necessarily reflect the views of the National Science Foundation.

This book should be considered a collection of suggestions for avenues of research in ecological physiology. It conveys what a small number of ecological physiologists found compelling about their discipline in 1986. It is clearly not a comprehensive collection of suggestions, and we make no claims that the suggestions we have included will necessarily correspond to the best possible avenues for the future development of ecological physiology. As George Bartholomew has said, it is sometimes difficult to anticipate which of our contributions will be significant. We do, however, believe it important that the dialogue represented by this book be continued and expanded. Ecological physiology has indeed suffered from the lack of explicit discussion of its current and future goals. If the "new directions" contained herein are not the best ones, then the field needs to consider which directions are best. We hope that this book will promote this kind of consideration, particularly among the graduate students who will create the ecological physiology of the future. Moreover, we hope this book will intrigue practitioners of related disciplines in involving themselves in the enterprise of ecological physiology.






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