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Foraging : Behavior and Ecology / [Edited By] David W Foraging Foraging Behavior and Ecology Edited by David W. Stephens, Joel S. Brown, and Ronald C. Ydenberg The University of Chicago Press Chicago & London David W. Stephens is Professor of Ecology, Evolution, and Behavior at the University of Minnesota and author, with J. R. Krebs, of Foraging Theory. Joel S. Brown is Professor of Biology at the University of Illinois at Chicago and author, with T. L. Vincent, of Evolutionary Game Theory, Natural Selection, and Darwinian Dynamics. Ronald C. Ydenberg is Professor in the Behavioral Ecology Research Group and Director of the Centre for Wildlife Ecology at Simon Fraser University. The University of Chicago Press, Chicago 60637 The University of Chicago Press, Ltd., London C 2007 by The University of Chicago All rights reserved. Published 2007 Printed in the United States of America 16151413121110090807 12345 ISBN-13: 978-0-226-77263-9 (cloth) ISBN-13: 978-0-226-77264-6 (paper) ISBN-10: 0-226-77263-2 (cloth) ISBN-10: 0-226-77264-0 (paper) Library of Congress Cataloging-in-Publication Data Foraging : behavior and ecology / [edited by] David W. Stephens, Joel S. Brown & Ronald C. Ydenberg. p. cm. ISBN-13: 978-0-226-77263-9 (cloth : alk. paper) ISBN-13: 978-0-226-77264-6 (pbk. : alk. paper) ISBN-10: 0-226-77263-2 (cloth : alk. paper) ISBN-10: 0-226-77264-0 (pbk. : alk. paper) 1. Animals—Food. I. Stephens, David W., 1955– II. Brown, Joel S. (Joel Steven), 1959– III. Ydenberg, Ronald C. QL756.5.F665 2007 591.53—dc22 2006038724 ∞ The paper used in this publication meets the minimum requirements of the American National Standard for Information Sciences—Permanence of Paper for Printed Library Materials, ANSI Z39.48-1992. Contents Foreword ix John Krebs and Alex Kacelnik Acknowledgments xiii 1 Foraging: An Overview 1 Ronald C. Ydenberg, Joel S. Brown, and David W. Stephens Box 1.1 Prehistory: Before Foraging Met Danger Peter A. Bednekoff Box 1.2 Diving and Foraging by the Common Eider Colin W. Clark Box 1.3 A Two-Player, Symmetric, Matrix Game Box 1.4 A Two-Player Continuous Game part i Foraging and Information Processing 2 Models of Information Use 31 David W. Stephens 3 Neuroethology of Foraging 61 David F. Sherry and John B. Mitchell Box 3.1 Glossary Box 3.2 A Nobel Prize in the Molecular Basis of Memory Box 3.3 Neural Mechanisms of Reward Peter Shizgal v vi Contents 4 Cognition for Foraging 105 Melissa M. Adams-Hunt and Lucia F. Jacobs Box 4.1 Learning in the Laboratory part ii Processing, Herbivory, and Storage 5 Food Acquisition, Processing, and Digestions 141 Christopher J. Whelan and Kenneth A. Schmidt Box 5.1 Modeling Digestive Modulation in an Ecological Framework Christopher J. Whelan Box 5.2 More Than a Matter of Taste Frederick D. Provenza 6 Herbivory 175 Jonathan Newman Box 6.1 Herbivory versus Carnivory: Different Means for Similar Ends David Raubenheimer Box 6.2 Animal Farm: Food Provisioning and Abnormal Oral Behaviors in Captive Herbivores Georgia Mason 7 Energy Storage and Expenditure 221 Anders Brodin and Colin W. Clark Box 7.1 Neuroendocrine Mechanisms of Energy Regulation in Mammals Stephen C. Woods and Thomas W. Castonguay Box 7.2 Energy Stores in Migrating Birds Åke Lindstrom¨ Box 7.3 What Current Models Can and Cannot Tell Us about Adaptive Energy Storage Alasdair Houston and John McNamara part iii Modern Foraging Theory 8 Provisioning 273 Ronald C. Ydenberg Box 8.1 Effects of Social Interactions at Resource Points on Provisioning Tactics Box 8.2 Provisioning and Spatial Patterns of Resource Exploitation Box 8.3 Variance-Sensitive Provisioning Contents vii 9 Foraging in the Face of Danger 305 Peter A. Bednekoff Box 9.1 Allocation of Foraging Effort when Danger Varies over Time Box 9.2 Three Models of Information Flow in Groups 10 Foraging with Others: Games Social Foragers Play 331 Thomas A. Waite and Kristin L. Field Box 10.1 The Ideal Free Distribution Ian M. Hamilton Box 10.2 Genetic Relatedness and Group Size Box 10.3 The Rate-Maximizing Producer-Scrounger Game part iv Foraging Ecology 11 Foraging and Population Dynamics 365 Robert D. Holt and Tristan Kimbrell Box 11.1 Basic Concepts in Population Dynamics 12 Community Ecology 397 Burt P. Kotler and Joel S. Brown Box 12.1 Isolegs and Isodars 13 Foraging and the Ecology of Fear 437 Joel S. Brown and Burt P. Kotler Box 13.1 Stress Hormones and the Predation-Starvation Trade-off Vladimir V. Pravosudov Box 13.2 Giving-up Densities Joel S. Brown 14 On Foraging Theory, Humans, and the Conservation of Diversity: A Prospectus 483 Michael L. Rosenzweig Contributors 503 Literature Cited 507 Index 587 Foreword On October 1, 1975, JK wrote the following in a letter (no email in those days!) to Ric Charnov to report the pilot results of the first experimental test of the “classic” diet model under properly controlled conditions of encounter rate, handling time, and prey energy content: Here are the results—read ’em and gloat: percentage small prey in the diet predicted by: treatment random foraging prey model observed 1505047 2505037 325 00 450 02 567 09 The last three rows demonstrated the crucial counterintuitive prediction that small prey would be excluded from the diet, independently of their encounter rate, if the encounter rate with large prey were above a certain quantifiable threshold. Those were heady days! Setting aside the fact that the small prey were not totally ignored, it seemed as though a very simple, testable model, derived from a few starting assumptions about rate maximization and constraints on forag- ing,couldactuallypredicthowananimalrespondedinanexperiment.It’shard to overstate the excitement at the time. Shortly afterward, Richard Cowie’s quantitative test of the patch model appeared (Cowie 1977), and the first use of stochastic dynamic modeling ix x Foreword predicted the trade-off between sampling and exploitation of a new environ- ment (Krebs et al. 1978). It really looked as though a new quantitative the- oretical framework for behavioral ecology had been born out of the ideas of MacArthur and Pianka (1966), Emlen (1966), Charnov (1976a, 1976b), and Parker (1978). By the time Stephens and Krebs published their monograph on foraging theory in 1986, the optimal foraging industry had been in full swing for a nearly a decade, and large numbers of laboratory and field studies seemed to underline the power of the theory. But by no means everyone was convinced. At the Animal Behavior Society symposium held in Seattle in 1978 (Kamil and Sargent 1981), Reto Zach and Jamie Smith concluded their article “Optimal Foraging in Wild Birds” as fol- lows: “Most feeding problems in the wild are complex and it is therefore dif- ficult to define optima. Furthermore, optimal foraging theory cannot be tested conclusively. Optimal foraging theory is thus of limited use only. Fortunate- lythereareotherpromisingapproachestothedevelopmentalandcomparative analysis of foraging skills.” By 1984, the time of the seminal “Brown Symposium” (Kamil et al. 1987) (referring of course to the eponymous university, not the color of the re- sulting book—which was green), not only had the field of optimal foraging theory become broader, but Russell Gray and John Ollason had developed excoriating critiques of the whole enterprise. Russell Gray summarized his views in these terms: “Despite its popularity, OFT faces a long list of serious problems. These problems are generally downplayed within the OFT lit- erature and the validity of the optimality assumption is taken on faith. This faith does not seem to be particularly useful.” John Ollason was equally, if not more, astringent, commenting that when predictions of OFT and data coincide, “a labyrinthine tautology has been constructed that is based on assumption piled on assumption.” With the benefit of twenty years’ hindsight, who was right? Was it the en- thusiasticoptimistsorthecynicalcritics?Theansweris,“abitofboth.”Onone hand, there is no doubt that the initial hopes for a simple, all-embracing the- ory that paid little attention to behavioral mechanisms were soon dashed. On the other hand, as the research has matured, important insights into behavior and ecology have been fostered by optimal foraging theory. Indeed, many important questions have been asked because of optimality thinking, and asking the right questions is the basis of successful science. Furthermore, the breadth of impact of foraging theory across many disciplines is remarkable. This book shows how the field has broadened and deepened. Simplicity and coherence have been left behind, but diversity, richness of texture, and understanding have been gained. The tentacles of foraging theory, in its broadest sense, have extended to form links with neuroethology, behavioral Foreword xi economics, life histories, animal learning, game theory, and conservation biology. Perhaps most important of all, the simplistic approach to building and test- ing models of behavior that characterized some of the early foraging litera- ture has been replaced by a more sophisticated comparative analysis of models. Take risk sensitivity as an example. Caraco’s early experimental work (Caraco et al. 1980) and Stephens’s theoretical formulation (Stephens 1981) provided a beguilingly simple combination of theory and data: animals should be risk prone when their expected energy budget is negative and risk averse when it is positive. Houston and McNamara (1982) subsequently extended Stephens’s idea, using stochastic dynamic models, to predict changes in risk sensitivity de- pendingonbothenergeticstateandtimehorizon.Thetheorybecamemoreso- phisticated, but did not encompass mechanisms of decision making: its predic- tions were based on arguments about adaptation. But when mechanisms were considered, it turned out that the purely functional approach embodied in risk sensitivity theory was not the one that most successfully accounted for the experimental data. Kacelnik and Bateson (1997) compared the predictions of four kinds of models: risk sensitivity theory, short-term rate maximization, scalar utility theory, and associative learning theory.
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