Centrarchid Fishes: Diversity, Biology and Conservation

Centrarchid Fishes

Centrarchid Fishes Diversity, Biology, and Conservation

Edited by S. J. Cooke and D. P. Philipp

A John Wiley & Sons, Ltd., Publication

This edition first published 2009  2009 Blackwell Publishing Ltd. Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’s global Scientific, Technical and Medical business with Blackwell Publishing. Registered office John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, United Kingdom Editorial office John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, United Kingdom For details of our global editorial offices, for customer services and for information about how to apply for permission to reuse the copyright material in this book please see our website at www.wiley.com/wiley-blackwell. The right of the author to be identified as the author of this work has been asserted in accordance with the Copyright, Designs and Patents Act 1988. 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, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books. Designations used by companies to distinguish their products are often claimed as trademarks. All brand names and product names used in this book are trade names, service marks, trademarks or registered trademarks of their respective owners. The publisher is not associated with any product or vendor mentioned in this book. This publication is designed to provide accurate and authoritative information in regard to the subject matter covered. It is sold on the understanding that the publisher is not engaged in rendering professional services. If professional advice or other expert assistance is required, the services of a competent professional should be sought. Library of Congress Cataloging-in-Publication Data is available A catalogue record for this book is available from the British Library. Set in 9/11 Times-Roman by Laserwords Private Limited, Chennai, India Printed and bound in Singapore by Fabulous Printers Pte Ltd 1 2009

Contents

List of Contributors Acknowledgments Preface About the Editors Chapter 1

Chapter 2

Chapter 3

xi xiii xv xvii

Species diversity, phylogeny and phylogeography of Centrarchidae T. J. Near and J. B. Koppelman

1

1.1 Introduction

1

1.2 Species diversity

1

1.3 Centrarchid fossils

5

1.4 Phylogeny

12

1.5 Phylogeography

26

1.6 Conclusions and future directions

30

1.7 Acknowledgments

31

References

31

Hybridization and speciation in centrarchids D. I. Bolnick

39

2.1 Introduction

39

2.2 Incidence of hybridization in centrarchids

39

2.3 What centrarchid hybrids tell us about speciation

41

2.4 Applied value of hybrids

58

2.5 Hybrids as a conservation threat

60

2.6 Future directions

61

2.7 Conclusions and summary

62

References

62

Ecomorphology of centrarchid fishes D. C. Collar and P. C. Wainwright

70

3.1 Introduction

70

3.2 Ecomorphology of feeding

71

3.3 Ecomorphology of locomotion

81

3.4 Conclusions

85

References

85 v

vi

Contents

Chapter 4

Chapter 5

Chapter 6

Chapter 7

Alternative reproductive tactics in the Centrarchidae B. D. Neff and R. Knapp

90

4.1 Introduction

90

4.2 Alternative reproductive tactics in the Centrarchidae

92

4.3 Genetic mechanisms for alternative reproductive tactics

94

4.4 Proximate mechanisms for alternative reproductive tactics

97

4.5 Ecological and evolutionary constraints on the evolution of alternative reproductive tactics

98

4.6 Alternative reproductive tactics in other fishes

99

4.7 Future directions

100

References

100

Early life history and recruitment D. R. DeVries, J. E. Garvey, and R. A. Wright

105

5.1 Introduction

105

5.2 Definition of “early life history” and “recruitment”

105

5.3 Variation in early life history across the centrarchids

105

5.4 Meta-analysis of life history data for several centrarchids

108

5.5 Recruitment in the centrarchids

113

5.6 Some general findings from the literature review

121

5.7 Search for critical periods

121

5.8 Evidence for broad groupings within the Centrarchidae

122

5.9 Gaps in our knowledge/research and management needs

123

References

123

Population and community ecology of Centrarchidae D. D. Aday, J. J. Parkos III, and D. H. Wahl

134

6.1 Introduction

134

6.2 Population ecology of Lepomis

134

6.3 Micropterus

140

6.4 Other centrarchids

144

6.5 Community ecology

148

6.6 Conclusions

154

6.7 Current and future directions

154

References

155

Centrarchid energetics M. S. Bevelhimer and J. E. Breck

165

7.1 Introduction

165

7.2 Centrarchid bioenergetics models

166

7.3 Food consumption and feeding energetics

171

Contents

7.4 Metabolic rate

Chapter 8

Chapter 9

vii

176

7.5 Energetic wastes (egestion, excretion, and SDA)

184

7.6 Growth energetics

184

7.7 Reproductive energetics

191

7.8 Synthesis

195

7.9 Research needs

196

References

197

Physiology and organismal performance of centrarchids J. D. Kieffer and S. J. Cooke

207

8.1 Introduction

207

8.2 Baseline physiological variables

208

8.3 Physiological challenges/tolerances

208

8.4 Physiological response to stress in centrarchids

222

8.5 Cardiovascular physiology

228

8.6 Thermal biology

242

8.7 Conclusions

250

References

251

Winter biology of centrarchid fishes C. D. Suski and M. S. Ridgway

264

9.1 Introduction

264

9.2 Definition of “winter”

264

9.3 Current research

264

9.4 Temperature

265

9.5 Dissolved oxygen and winterkill

267

9.6 Physical and physiological changes

268

9.7 Swimming abilities

269

9.8 Species ranges and life history traits

270

9.9 General activity level

271

9.10 Winter movements

273

9.11 Feeding

274

9.12 Growth

276

9.13 Aggregations

277

9.14 Winter habitat

278

9.15 Photoperiod

279

9.16 Overwinter survival

279

9.17 Conclusions and future directions

282

References

284

viii

Contents

Chapter 10

Chapter 11

Chapter 12

Centrarchid aquaculture J. E. Morris and R. D. Clayton

293

10.1 Introduction

293

10.2 Historical review

293

10.3 Culture facilities

294

10.4 Lepomis culture (bluegills and their hybrids)

295

10.5 Pomoxis spp. culture

300

10.6 Micropterus spp. culture

302

10.7 Future for centrarchids as aquaculture species

305

References

307

Centrarchid fisheries S. Quinn and C. Paukert

312

11.1 Introduction

312

11.2 Historical fisheries

312

11.3 Recreational fisheries for black bass Micropterus spp.

317

11.4 Recreational fisheries for crappie Pomoxis spp.

319

11.5 Recreational fisheries for sunfish Lepomis spp.

320

11.6 Fisheries for Ambloplites spp.

322

11.7 Recreational fisheries for other centrarchids

323

11.8 Regulations

323

11.9 Future considerations in centrarchid management

326

References

330

Contemporary issues in centrarchid conservation and management S. J. Cooke, K. C. Hanson, and C. D. Suski

340

12.1 Introduction

340

12.2 Threats to centrarchid fishes and strategies for minimizing threats

340

12.3 Introduction of exotics

347

12.4 Environmental alteration and degradation

349

12.5 Stocking—mixing of populations and outbreeding

355

12.6 Parasites and diseases

355

12.7 Exotic centrarchids as threats to conservation

356

12.8 Global conservation status of centrarchids

358

12.9 Conclusion

359

References

359

Contents

Chapter 13

ix

Centrarchid identification and natural history M. L. Warren, Jr.

375

13.1 Introduction

375

13.2 Generic and species accounts

377

13.3 Acantharchus pomotis (Baird)

377

13.4 Ambloplites Rafinesque

379

13.5 Archoplites interruptus (Girard)

389

13.6 Centrarchus macropterus (Lac´ep`ede)

392

13.7 Enneacanthus Gill

393

13.8 Lepomis Rafinesque

400

13.9 Micropterus Lac´ep`ede

434

13.10 Pomoxis Rafinesque

468

13.11 Identification keys to genera and species

475

References

482

Index Color plate (between pages 334 and 335)

535

List of Contributors

D. D. Aday Department of Zoology, North Carolina State University, Raleigh, North Carolina, USA M. S. Bevelhimer Environmental Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA D. I. Bolnick Section of Integrative Biology, University of Texas at Austin, Austin, Texas, USA J. E. Breck Institute for Fisheries Research, Michigan Department of Natural Resources and University of Michigan, Ann Arbor, Michigan, USA R. D. Clayton Department of Natural Resources and Environmental Management, Iowa State University, Ames, Iowa, USA D. C. Collar Section of Evolution and Ecology, University of California, Davis, California, USA S. J. Cooke Fish Ecology and Conservation Physiology Laboratory, Department of Biology and Institute of Environmental Science, Carleton University, Ottawa, Ontario, Canada D. R. DeVries Department of Fisheries and Allied Aquacultures, Auburn University, Auburn, Alabama, USA J. E. Garvey Fisheries and Illinois Aquaculture Center and Department of Zoology, Southern Illinois University, Carbondale, Illinois, USA K. C. Hanson Fish Ecology and Conservation Physiology Laboratory, Department of Biology, Carleton University, Ottawa, Ontario, Canada J. D. Kieffer Department of Biology and Canadian Rivers Institute, University of New Brunswick, Saint John, New Brunswick, Canada R. Knapp Department of Zoology, University of Oklahoma, Norman, Oklahoma, USA J. B. Koppelman Missouri Department of Conservation, Columbia, Missouri, USA J. E. Morris Department of Natural Resources and Environmental Management, Iowa State University, Ames, Iowa, USA T. J. Near Department of Ecology and Evolutionary Biology and Peabody Museum of Natural History, Yale University, New Haven, Connecticut, USA B. D. Neff Department of Biology, University of Western Ontario, London, Ontario, Canada J. J. Parkos III Illinois Natural History Survey, Division of Ecology and Conservation Sciences, Champaign, Illinois, USA C. Paukert United States Geological Survey, Kansas Cooperative Fish and Wildlife Research Unit, Division of Biology, Kansas State University, Manhattan, Kansas, USA xi

xii

List of Contributors

D. P. Philipp Illinois Natural History Survey, Division of Ecology and Conservation Sciences, Champaign, Illinois, USA S. Quinn In-Fisherman Incorporated, Baxter, Minnesota, USA M. S. Ridgway Harkness Laboratory of Fisheries Research, Aquatic Research and Development Section, Ontario Ministry of Natural Resources and Trent University, Peterborough, Ontario, Canada C. D. Suski Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, Illinois, USA D. H. Wahl Illinois Natural History Survey, Kaskaskia Biological Station, Sullivan, Illinois, USA P. C. Wainwright Section of Evolution and Ecology, University of California, Davis, California, USA M. L. Warren, Jr. Center for Bottomland Hardwoods Research, Southern Research Station, United States Department of Agriculture Forest Service, Mississippi, USA R. A. Wright Department of Fisheries and Allied Aquacultures, Auburn University, Auburn, Alabama, USA

Acknowledgments

T. J. Near and J. B. Koppelman (Chapter 1) thank several anonymous reviewers. J. B. Koppelman was supported by the Missouri Department of Conservation. D. I. Bolnick (Chapter 2) thanks S. J. Cooke, T. J. Near, D. P. Philipp, and two anonymous reviewers for comments on early drafts of this chapter. Research for this chapter was supported by NSF grant #DEB-0412802 to D. I. Bolnick, and the University of Texas at Austin. D. C. Collar and P. C. Wainwright (Chapter 3) thank two anonymous reviewers whose comments improved their chapter. They are also grateful to D. I. Bolnick, A. Carroll, S. Day, T. Higham, and T. J. Near for their insights into centrarchid biology. D. C. Collar was supported by a U.C. Davis Center for Population Biology fellowship and NSF Grant # IOB-0444554 to P. C. Wainwright. B. D. Neff and R. Knapp (Chapter 4) thank M. R. Gross and N. Santangelo for comments on the chapter. B. D. Neff was supported by the Natural Sciences and Engineering Research Council of Canada and R. Knapp was supported by the National Science Foundation (IBN 0349449) and a University of Oklahoma Presidential International Travel Fellowship. D. R. DeVries, J. E. Garvey, and R. A. Wright (Chapter 5) would like to acknowledge the Alabama Department of Conservation and Natural Resources, Auburn University’s Department of Fisheries and Allied Aquacultures, and the Southern Illinois University at Carbondale Fisheries and Illinois Aquaculture Center for their support while they worked on this book chapter. D. D. Aday, J. J. Parkos III, and D. H. Wahl (Chapter 6) wish to thank M. Carey and L. Einfalt, both of the Illinois Natural History Survey, who assisted with the literature review and preparation of figures. This chapter was improved by the thoughtful reviews of J. R. Jackson, B. R. Robinson, and S. J. Cooke. M. S. Bevelhimer and J. E. Breck (Chapter 7) thank several anonymous reviewers. M. S. Bevelhimer works with the Oak Ridge National Laboratory, which is managed by UT-Battelle, LLC, for the US Department of Energy under contract DE-AC05–00OR22725. The work by J. E. Breck on this chapter was funded in part by Federal Aid in Sport Fish Restoration (Dingell-Johnson), Project F-80-R, and the Fish and Game Fund of the State of Michigan. J. D. Kieffer and S. J. Cooke (Chapter 8) thank J. Schreer, C. Kieffer, S. Peake, and A. Kolok for thoughtful reviews and L. Arsenault for help with preparing figures. J. D. Kieffer thanks the University of New Brunswick (Saint John) and the MADSAM fish group for their continued support. Original research reported here by J. D. Kieffer was supported by a grant from the Natural Sciences and Engineering Research Council of Canada. S. J. Cooke was supported by the Natural Sciences and Engineering Research Council of Canada, the Illinois Natural History Survey, the University of British Columbia, and Carleton University. C. D. Suski and M. S. Ridgway (Chapter 9) thank A. Danylchuk and several anonymous reviewers for comments on an earlier draft of the manuscript. C. D. Suski was supported by the Natural Sciences and Engineering Research Council of Canada, Queen’s University, the Ontario Ministry of Natural Resources, and the University of Illinois. M. S. Ridgway was supported by the Ontario Ministry of Natural Resources. J. E. Morris and R. D. Clayton (Chapter 10) thank the Department of Natural Resources and Environmental Management at Iowa State University and the North Central Regional Aquaculture Center. S. Quinn and C. Paukert (Chapter 11) thank D. Willis for thoughtful discussions on centrarchid fisheries, and acknowledge helpful editorial suggestions from S. J. Cooke, W. Wegman, and an anonymous reviewer. This work was supported by In-Fisherman, Inc. S. J. Cooke, K. C. Hanson, and C. D. Suski (Chapter 12) thank L. Thompson for help with final preparation of their chapter. S. J. Cooke was supported by the Natural Sciences and Engineering Research Council of Canada, an Izaak Walton Killam Fellowship from the University of British Columbia, and Carleton University. C. D. Suski was supported by the Ontario Ministry of Natural Resources, the Natural Sciences and Engineering Research Council of Canada, and the University of Illinois. xiii

xiv

Acknowledgments

M. L. Warren, Jr. (Chapter 13) thanks T. Darden (Enneacanthus), C. S. Schieble (Ambloplites), and P. Crain, R. Schwartz, and C. M. Woodley (Archoplites) for constructive reviews of drafts of the chapter. For sharing ongoing research, alerting him to information sources, or numerous other courtesies, he gratefully acknowledges B. M. Burr, R. C. Cashner, A. C. Commens-Carson, K. S. Cummings, T. Darden, B. Fisher, W. R. Haag, R. E. Jenkins, A. E. Keller, P. Crain, R. M. Mayden, J. G. McWhirter, M. O’Connell, K. Oswald, L. M. Page, M. S. Peterson, F. C. Rohde, C. S. Schieble, R. Schwartz, W. C. Starnes, and C. M. Woodley. L. Thompson kindly formatted the references for this chapter.

Preface

The fishes in the family Centrarchidae are more commonly known as the freshwater sunfishes, a warmwater clade with 34 extant species that are endemic to North America. This group of warmwater fishes generally consists of small to moderately sized individuals that are highly colored (like the bluegill on the cover of the book). The sunfish family includes such prominent sportfish species as the largemouth bass, Florida bass, smallmouth bass, and bluegill. The largemouth bass is the most popular recreational sportfish in North America and is the basis for a large industry. In addition, bass are the frequent quarry of anglers participating in competitive angling events. Centrarchid fishes also play important ecological roles in structuring communities. They are commonly the dominant top-level predators in the diverse lentic and lotic warmwater communities of freshwater fishes in eastern North America. They provide forage for many other species and also serve as hosts for sensitive life-stages of threatened bivalves. The reproductive strategies of centrarchid fishes are especially interesting in that the male fish provide sole parental care for offspring over periods ranging from maybe as short as 1 or 2 days (for Sacramento perch) to 4 to 5 weeks (for smallmouth bass). In addition, centrarchids have been widely introduced around the globe, leading to a number of conservation concerns. Due to the popularity of this group of fishes, state and provincial fisheries managers devote substantial efforts toward managing these species. Some regions place significant emphasis on stock enhancement using cultured fish. Although there has been a recent explosion of research on sunfish species in response to their abundance and importance, at present, this large body of literature is not supported by any comprehensive syntheses on the biology and ecology of these fishes. As managers and scientists press forward with research, management, and conservation strategies, there will be an increased need to coalesce the disparate accounts of sunfish biology. Indeed, an understanding of their physiology and behavior is essential for understanding the magnitude of the threats faced by these fishes. The tome that we have developed with our team of expert authors represents a synthesis of the current state of knowledge on sunfish biology. An overriding goal of the book is to celebrate the life-history variation evident in this group of fishes (hence the use of the word “diversity” in the title of the book). A secondary objective was to summarize the linkages between basic ecology and the applied management and conservation of centrarchid fishes. Contributors were asked both to synthesize the existing literature and to contribute novel data from unpublished or forthcoming works. For that reason, we developed a team of contributors that represent those individuals at the cutting edge of centrarchid research. Authors were asked to provide coverage of all species, not just those of economic importance. Almost every author, however, identified that the majority of the available data and research were focused on several species (largemouth bass, smallmouth bass, bluegill, pumpkinseed, rock bass, black crappie, and white crappie). Detailed species accounts (of 33 of the 34 extant species; excludes the Alabama bass, Micropterus henshalli ) and a key to the centrarchids were developed by M. Warren and can be found at the end of the book. In total, the book contains 13 chapters that cover almost all aspects of sunfish biology and management. One notable omission from the list of chapters is the one focused on the reproductive biology of the centrarchid fishes. This is intentional because various aspects of reproduction were included in all of the chapters (e.g., hybridization, early life history, population biology, energetics, culture) and are thus covered throughout the book. Alternative reproductive tactics are covered independently. The detailed species accounts at the end of the book also include summaries of reproductive biology for all of the centrarchid fishes. We are particularly excited to include a chapter on winter biology, a topic of high importance to centrarchid fishes (i.e. overwinter mortality can influence recruitment), particularly toward the northern edge of their range. To our knowledge, there are no other “taxon” specific tomes that include coverage of winter biology. Thanks to the talented authors and the many referees, we are confident that this book is THE stand-alone reference on the biology of one of the most important groups of fishes in North America. Emphasizing the diversity of centrarchid fishes and the ongoing research efforts to clarify phylogenetic relationships, during the period when the book was being typeset an additional centrarchid was elevated to the species level. That addition is Micropterus henshalli (Hubbs and Bailey 1940), the Alabama Bass (See Baker, W. H., C. E. Johnston, and xv

xvi

Preface

G. W. Folkerts, 2008. The Alabama Bass, Micropterus henshalli (Teleostei: Centrarchidae), from the Mobile River basin. Zootaxa 1861:57–67). The previously recognized subspecies of Micropterus punctulatus from the Mobile River system of Alabama, Georgia, and Mississippi has been elevated to species status on the basis of morphological evidence, but it had long been recognized as distinct according to ecological, morphometric/meristic, and genetic characters. As such, although we formally recognize 34 extant centrarchid species, only 33 of them are covered extensively in this book. We do not include a formal natural history account for Micropterus henshalli, however, details can be found under the account for Micropterus punctulatus where it is described as a subspecies. We were able to make some limited changes at the proof stage to Chapter 1 in recognition of this taxonomic change, however, the phylogenies presented exclude this species. Given the many advances in molecular genetics and taxonomy, we would expect that the number of centrarchid fish species would increase in the coming years. Hence, although an inconvenience to those of us working on this book project, this taxonomic elevation is further evidence of the diversity of centrarchid fishes. We thank the many individuals that contributed to the book either intellectually or in the form of other support. This project was initiated when Cooke was an NSERC and Killam Post-Doctoral Fellow in the Centre for Applied Conservation Research at the University of British Columbia. At the time, Cooke was mentored by Dr. S. Hinch and Dr. T. Farrell, both of whom provided the freedom and encouragement to pursue this project. In the final phases of editing, Cooke was supported by the Natural Sciences and Engineering Research Council of Canada, the Rainy Lake Fisheries Charity Trust, the Ontario Ministry of Research and Innovation (Early Researcher Award), and Carleton University. D. Philipp was supported by the Illinois Natural History Survey and the Illinois Department of Natural Resources. We recognize and appreciate tremendously that the Queen’s University Biological Station provided a stimulating, productive, and fun environment to launch the idea for the book. We are particularly indebted to A. Weckworth and L. Thompson who completed detailed technical editing to ensure consistency in format and style throughout the book. D. Ramesh, Project Manager from Laserwords Private Limited in India, provided additional technical editing and facilitated the typesetting and proof changes during the final phases of the publication process. We also thank our families for continued support and acceptance of our crazy field schedules. From Blackwell Science Publishers (UK), N. Balmforth, L. Price, and K. Nuttall provided support and continual encouragement throughout the protracted writing and editing process. We also wish to acknowledge all of the authors for providing contributions that were of high quality and incredibly comprehensive. The project took several years to complete, and our authors were extremely patient. Furthermore, we thank the many anonymous (unless declared and listed in the acknowledgments) referees for providing thoughtful reviews of the lengthy chapters. S. J. Cooke and D. P. Philipp, Eleuthera, The Bahamas, December 2, 2007

About the Editors

S. J. Cooke: Cooke received his undergraduate and M.Sc. degrees from the University of Waterloo. He completed his Ph.D. research at the University of Illinois in 2002 while working with Dr. D. P. Philipp and Dr. D. H. Wahl at the Illinois Natural History Survey. Cooke was then awarded an NSERC Post Doctoral Fellowship and Izaak Walton Killam Fellowship, which he held as a postdoctoral fellow at the University of British Columbia where he worked with Dr. S. Hinch and Dr. T. Farrell. In 2005, Cooke became an Assistant Professor in Environmental Science and Biology at Carleton University (Ottawa, Canada) where he is Director of the Fish Ecology and Conservation Physiology Laboratory. Cooke, his students, and collaborators, study how fish respond to natural and anthropogenic stressors and how individuals, populations, and species vary in their response. Cooke has published over 100 peer reviewed papers, about half on fish in the sunfish family covering topics such as the energetics of parental care, the physiological consequences of angling practices, and the consequences of outbreeding on fish performance. Cooke has been the recipient of the American Fisheries Society Award of Excellence in Fisheries Management and an Early Researcher Award from the Ontario Ministry of Innovation. He is also an editor for the journal Endangered Species Research and is on the Editorial Board for Fisheries Research. Cooke is an Affiliate Scientist with the Illinois Natural History Survey, Adjunct Professor at Queen’s University, and an Honorary Research Associate at the University of British Columbia. He and his wife currently reside in Ottawa, a region rich with centrarchid dominated fisheries. D. P. Philipp: Philipp received his undergraduate degree from Lafayette College and his Ph.D. from the University of Massachusetts in 1976. He is currently Principal Scientist at the Illinois Natural History Survey (INHS) and is a Professor in three departments at the University of Illinois at Urbana-Champaign. His research interests focus on conservation genetics and behavioral ecology with a focus on centrarchid fishes. His findings have helped to elucidate the consequences of outbreeding depression, hybridization, and fisheries exploitation on centrarchid populations. In his role at the INHS, Dr. D. P. Philipp conducts research in support of the Illinois Department of Natural Resources. He is the director of the state creel survey and responsible for assessing recreational fishery dynamics throughout Illinois. Dr. D. P. Philipp has served on a number of committees including the Independent Scientific Advisory Board of the Northwest Power and Conservation Council. He is one of the initial founders of the Fisheries Conservation Foundation (an education and outreach partner with the American Fisheries Society) and currently serves on the Foundation’s Board of Directors. He has edited several prominent books including “Black Bass Ecology and Conservation” in 2002 and has over 100 papers in peer reviewed outlets. D. P. Philipp was selected as the first touring lecturer for the Zoological Education Trust of the Canadian Society of Zoologists. He and his family reside in Champaign, Illinois, but spend the spring in Canada studying centrarchid reproduction at the Queen’s University Biology Station.

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Chapter 1

Species diversity, phylogeny and phylogeography of Centrarchidae T. J. Near and J. B. Koppelman

1.1 Introduction Centrarchidae is a clade of freshwater fishes endemic to North America, a part of the world that harbors more species of freshwater fishes than any other nontropical region on Earth (Briggs 1986; Lundberg et al . 2000). Centrarchid fishes have been of interest to biologists for a long period of time because they are commonly the dominant top-level predators in the diverse communities of freshwater fishes in eastern North America, and as such, they are among the world’s most popular freshwater sport fishes (Henshall 1881; Etnier and Starnes 1993; Philipp and Ridgway 2002). Interestingly, it is only in the last 10 years or so that comparative morphological and molecular data have been used in conjunction with objective character-based methods to investigate the phylogenetic relationships of Centrarchidae. The goal of this chapter is to review and assess previous ideas regarding the diversity and relationships of centrarchid species. We hope to provide biologists from all disciplines with a clear picture of the current and best-supported hypotheses of centrarchid phylogeny, and we intend to illustrate how many recent, cutting-edge efforts have agreed remarkably with studies published as far back as the nineteenth century. Although we realize our esoteric interests in centrarchid diversity and phylogeny, as well as our desire to understand the results of modern phylogenetic analyses in the context of the rich past of centrarchid taxonomy and systematics may be confusing to the average fish biologist or ichthyologist, we will attempt to clarify what seems like a morass of trees and classifications for biologists in need of phylogenetic hypotheses. It is our desire that both comparative biologists and conservation agencies exploit the current state of knowledge regarding centrarchid diversity and phylogenetic relationships. In this chapter we provide a discussion of the currently recognized diversity of both extant and fossil species in Centrarchidae, and we attempt to illuminate some unresolved issues in this area that need attention in future research efforts. We present an overview of previous investigations and hypotheses concerning the evolutionary relationships of Centrarchidae, including a discussion of recent efforts using morphological and molecular data in addition to those that pre-date the development of phylogenetic systematics, or cladistics (Hennig 1966). Many of the pre-cladistic ideas of centrarchid relationships discussed in this review were presented as purely taxonomic hypotheses, where the hypothesized relationships were implied from the composition and ranking of taxa. Evolutionary biologists often investigate genetic variation within a geographic context, as intraspecific gene trees often show a strong geographic pattern. Such is the science of phylogeography (Avise 2000). We provide a review and discussion of phylogeography in centrarchids, highlighting some of the problems that have made such analyses in Centrarchidae less straightforward than in species from other groups of North American freshwater fishes.

1.2 Species diversity 1.2.1 Extant species and the status of subspecies Currently, 34 extant species are recognized in Centrarchidae (Table 1.1), with the most recently described species being Ambloplites constellatus and Micropterus cataractae (Cashner and Suttkus 1977; Williams and Burgess 1999). As in 1

2

Centrarchid fishes

Table 1.1 Currently recognized centrarchid species and proposed classification. Fossil genera and species are indicated with a dagger. Centrarchidae (44 species: 33 extant, 11 extinct) Centrarchinae Acantharchus pomotis (Baird 1855) Mud sunfish Ambloplites ariommus (Viosca 1936) Shadow bass Ambloplites cavifrons (Cope 1868) Roanoke bass Ambloplites constellatus (Cashner and Suttkus 1977) Ozark bass Ambloplites ruprestris (Rafinesque 1817) Rockbass Archoplites †clarki (Smith and Miller 1985) Clarkia perch Archoplites interruptus (Girard 1854) Sacramento perch Archoplites †molarus (Smith et al. 2000) Ringold sunfish Archoplites †taylori (Miller and Smith 1967) Lake Idaho sunfish †Boreocentrarchus smithi (Schlaikjer 1937) Healy Creek sunfish ` 1801) Flier Centrarchus macropterus (Lacepede Enneacanthus chaetodon (Baird 1855) Blackbanded sunfish Enneacanthus gloriosus (Holbrook 1855) Bluespotted sunfish Enneacanthus obesus (Girard 1854) Banded sunfish †Plioplarchus septemspinosus (Cope 1889) John Day sunfish †Plioplarchus sexspinosus (Cope 1883) Sentinel Butte sunfish †Plioplarchus whitei (Cope 1883) Laramie sunfish Pomoxis annularis (Rafinesque 1818) White crappie Pomoxis †lanei (Hibbard 1936) Ogallala crappie Pomoxis nigromaculatus (Lesueur 1829) Black crappie Lepominae Lepomis auritus (L 1758) Redbreast sunfish Lepomis cyanellus (Rafinesque 1819) Green sunfish Lepomis gibbosus (L 1758) Pumpkinseed Lepomis gulosus (Cuvier 1829) Warmouth Lepomis humilis (Girard 1858) Orangespotted sunfish Lepomis †kansasensis (Hibbard 1936) Rhino Hill sunfish Lepomis macrochirus (Rafinesque 1819) Bluegill Lepomis marginatus (Holbrook 1855) Dollar sunfish Lepomis megalotis (Rafinesque 1820) Longear sunfish ¨ Lepomis microlophus (Gunther 1859) Redear sunfish Lepomis miniatus (Jordan 1877) Redspotted sunfish Lepomis peltastes (Cope 1870) Northern longear sunfish Lepomis punctatus (Valenciennes 1831) Spotted sunfish Lepomis †serratus (Smith and Lundberg 1972) Keigh sunfish Lepomis symmetricus (Forbes 1883) Bantam sunfish (continued)

Species diversity, phylogeny and phylogeography of Centrarchidae

3

Table 1.1 (continued). Centrarchidae (44 species: 33 extant, 11 extinct) Micropterinae Micropterus cataractae (Williams and Burgess 1999) shoal bass Micropterus coosae (Hubbs and Bailey 1940) Redeye bass ` Micropterus dolomieu (Lacepede 1802) smallmouth bass Micropterus floridanus (LeSueur 1822) Florida bass Micropterus henshalli (Hubbs and Bailey 1940) Micropterus notius (Bailey and Hubbs 1949), Suwannee bass Micropterus punctulatus (Rafinesque 1819) spotted bass Micropterus †relictus (Cavender and Smith 1975) Chapala bass ` 1802) largemouth bass Micropterus salmoides (Lacepede Micropterus treculi (Vaillant and Bocourt 1874) Guadalupe bass

many groups of animals, there are many more scientific names available than there are recognized species. Not including the names of valid extant species (Table 1.1), there are 118 nominal names that are considered synonyms for species in Centrarchidae. Of these, 11 were either new names for subspecies or were introduced as species names and have been used at some point to designate subspecies (Gilbert 1998). Of the 118 nominal names, 9 are based on hybrid centrarchids; all but 1 of these are the hybrid combinations of Lepomis cyanellus * L. macrochirus and L. cyanellus * L. gibbosus (Hubbs 1920; Hubbs and Hubbs 1932; Gilbert 1998). The contemporary view of species diversity in Centrarchidae was fairly well settled by the turn of the nineteenth and twentieth centuries, as the vast majority of valid centrarchid species were described between 1800 and 1883 (Table 1.1; Figure 1.1). This period was also when most of the synonymous names were introduced (Bailey 1938; Gilbert 1998). Through both the nineteenth and twentieth centuries centrarchid species have been described using very similar types of data from external morphology, including meristics (scale row and fin element counts), morphometrics (body proportions), pigmentation patterns, and coloration (Cope 1868, 1870; Hubbs and Bailey 1940; Cashner and Suttkus 1977; Williams and Burgess 1999). To date, comparative phylogenetic methods, using either morphological or molecular data, have not been used in describing new centrarchid species.

No. of valid species described

35 30 25 20 15 Ambloplites rupestris

10 5

1750

1800

1850

1900

1950

2000

Year described

Figure 1.1 Plot illustrating the growth of valid extant centrarchid species descriptions from the nineteenth through twentieth centuries. Ambloplites rupestris redrawn from Forbes and Richardson (1920).

4

Centrarchid fishes

The status of subspecies in Centrarchidae is much less resolved when compared to the 33 recognized valid extant species (Table 1.1). The use of subspecies in North American fish taxonomy has a relatively inconsistent history, and since the initial critique of subspecies, most modern workers in systematics have been moving away from using this rank (Wilson and Brown 1953; Burbrink et al . 2000). However, there remain 11 names that have been historically designated as centrarchid subspecies. We are able to categorize each of these names into three classes: (i) subspecies that do not exhibit significant variation from the nominal subspecies, (ii) subspecies that are based on hybrid specimens, and (iii) subspecies that merit elevation to species. Three centrarchid subspecies have been invalidated as it was demonstrated that they did not differ appreciably from other populations of the nominal species. Acantharchus pomotis mizelli Fowler and Enneacanthus chaetodon elizabethae were both described as subspecies in the 1940s based on six or seven specimens (Bailey 1941; Fowler 1945). In both cases, subsequent analyses that included many more specimens failed to reveal geographic variation consistent with the recognition of the subspecies proposed for each of these species (Sweeney 1972; Cashner et al . 1989). A similar situation exists for the Neosho Smallmouth Bass, Micropterus dolomieu velox Hubbs and Bailey. This subspecies was described based primarily on slight differences in counts of the second dorsal fin rays, pigmentation patterns, and dentition on the tongue (Hubbs and Bailey 1940). The validity of M. d. velox was subsequently dismissed on the basis of slight morphological differences and clinal gradation into the nominal M. dolomieu (Bailey 1956; Gilbert 1998), a conclusion supported by more recent analyses of nuclear gene encoded allozymes and mitochondrial DNA (mtDNA) sequence data (Stark and Echelle 1998; Kassler et al . 2002). At least one centrarchid subspecies has turned out to be based on hybrid specimens. Micropterus punctulatus wichitae Hubbs and Bailey was described as a subspecies from the Wichita Mountains of southwestern Oklahoma based on differences in scale row counts (Hubbs and Bailey 1940). However, this population was initially described as hybrids of M. punctulatus and M. dolomieu (Hubbs and Ortenburger 1929). Morphological data from M. p. punctulatus, M. p. wichitae, and M. dolomieu and historical records of nonnative M. dolomieu introductions near the type locality of M. p. wichitae support the hypothesis that this subspecies is based on hybrid M. punctulatus * M. dolomieu specimens (Cofer 1995). Genetic analysis of both nuclear and mtDNA in M. punctulatus populations from the Red and Arkansas River Basins did not reveal genetic divergence of the Wichita Mountain populations of M. punctulatus (Coughlin et al . 2003). Lepomis megalotis and L. macrochirus are two centrarchid species that are thought to be polytypic and contain described subspecies (Mayden et al . 1992; Gilbert 1998). Future research documenting morphological and genetic variation in these two complexes has the strong possibility to result in the recognition of additional valid centrarchid species. L. megalotis has four, and possibly seven, valid subspecies, L. m. megalotis (Rafinesque), L. m. aquilensis (Baird and Girard), L. m. breviceps (Baird and Girard), and L. m. occidentalis Meek (Bailey 1938). In addition, L. m. convexifrons (Baird and Girard), L. m. fallax (Baird and Girard), and L. m. popeii (Girard) are three additional forms from Texas that may represent other unrecognized species related to L. megalotis (Gilbert 1998). Unfortunately, there is no published analysis of morphological variation among these subspecies, but a Ph.D. dissertation had detected substantial morphometric variation among four of the described subspecies (Barlow 1980). An analysis of allozyme variation detected appreciable genetic divergence of L. m. breviceps and L. m. aquilensis relative to the other subspecies (Jennings and Philipp 1992). Based on morphometric and body size differences, L. peltastes Cope was elevated as a species from a subspecies of L. megalotis (Bailey et al . 2004). We suspect that several additional centrarchid species will be recognized as a result of analyses of geographic variation and phylogeny of the L. megalotis complex using comparative morphological and molecular data. There is a degree of uncertainty as to how many subspecies of Lepomis macrochirus are recognized. The problem centers on Pomotis speciosus described from Brownsville, Texas by Baird and Girard (1854). This species was subsequently synonymized with L. macrochirus by Hubbs (1935). At a later date, Hubbs and Lagler (1958) treated P. speciosus as a subspecies of L. macrochirus, concluding that the geographic range is throughout Texas and northeastern Mexico. Allozyme analyses did not detect genetic differentiation between L. m. macrochirus and L. m. speciosus (Kulzer and Greenbaum 1986), and subsequent treatments of centrarchid species diversity have not recognized L. m. speciosus (Gilbert 1998). The two valid subspecies of L. macrochirus present an interesting problem of nomenclature confusion, morphological and genetic divergence, an area of presumed secondary contact and introgression, and a biogeographic pattern and a timing of divergence seen in another centrarchid sister species pair. The nominal subspecies L. m. macrochirus Rafinesque is distributed across eastern North America except for the northern Atlantic Coast (Lee et al . 1980), while the other subspecies is endemic to the Florida Peninsula (Felley 1980). Initially, the subspecies found in Florida was designated as Lepomis

Species diversity, phylogeny and phylogeography of Centrarchidae

5

macrochirus purpurescens Cope under the premise that this subspecies extended from the Atlantic Coast of the Carolinas to the Florida Peninsula (Hubbs and Allen 1943; Hubbs and Lagler 1958). The type locality for Lepomis purpurescens is in the Yadkin River Drainage in North Carolina (Cope 1870). Subsequent morphological and molecular analyses demonstrate that this is far north of the range of the Florida subspecies (Avise and Smith 1974a; Felley 1980; Avise et al . 1984), and as Gilbert (1998) has pointed out, Cope described a Bluegill from Florida, Lepomis mystacalis (Cope 1877). Therefore, the appropriate name for the Florida Bluegill is L. macrochirus mystacalis. Lepomis m. macrochirus and L. m. mystacalis are morphologically and genetically distinct, but there is a presumed area of introgression through secondary contact along most of southern Georgia and South Carolina (Felley 1980; Avise et al . 1984). Another sister species pair in Centrarchidae, Micropterus salmoides and Micropterus floridanus, exhibit a very similar distribution and area of secondary contact and introgression (Bailey and Hubbs 1949; Philipp et al . 1983). Based on a fossil calibrated molecular phylogeny of Centrarchidae, the divergence time between M. salmoides and M. floridanus is approximately 2.8 million years ago (mya) (Near et al . 2003, 2005b). Lepomis m. macrochirus and L. m. mystacalis exhibit a very similar divergence time. We found mtDNA cytochrome b gene sequences in Genbank for five individuals of L. m. macrochirus and a single L. m. mystacalis (accession numbers: AY115975, AY115976, AY225667, AY828966, AY828967, and AY828968). The average genetic distance between these two subspecies was 4.5%, which translates to a divergence time of roughly 2.3 mya (Near et al . 2003). Future work should aim toward gathering sufficient morphological and molecular data to more precisely determine the geographic distribution of these two forms and assess if L. mystacalis is a valid species. Recently Micropterus henshalli (Hubbs and Bailey) was elevated as a valid species (Baker et al . 2008), but was long recognized as a subspecies of M. punctulatus (Hubbs and Bailey 1940). Micropterus henshalli is endemic to the Mobile Basin and there are slight morphological differences between populations above and below the Fall Line (Gilbert 1973; Baker et al . 2008). However, there are substantial differences in several meristic characters between M. henshalli and M. punctulatus (Gilbert 1973), and there are marked differences in body proportions and surprising life history and dietary differences between these two species (Gilbert 1973). Perhaps the most compelling evidence for the recognition of M. henshalli includes measures of genetic divergence and the results of phylogenetic analyses. Among 19 polymorphic allozyme loci surveyed for all Micropterus species, not a single allele was shared exclusively between M. henshalli and M. punctulatus, and a fixed unique allele was found in M. p. henshalli (Kassler, et al ., 2002). In a phylogenetic analysis of Micropterus species using gap coded continuous morphological characters M. henshalli and M. punctulatus did not form a clade (Harbaugh 1994), and these two species were sister lineages in frequency parsimony of allozyme alleles (Kassler et al . 2002). In addition, molecular phylogenetic analyses of mtDNA sequences from cytb and ND2 resulted in tree topologies where M. henshalli was nested within M. coosae and distantly related to M. punctulatus (Kassler et al . 2002). Given the evidence presented above, the classification of M. henshalli as a subspecies of M. punctulatus was not compelling and the recognition of this species is supported by the substantial comparative data.

1.3 Centrarchid fossils The fossil record of Centrarchidae is fairly rich and extends in geologic time from the Late Eocene to Early Oligocene of approximately 35 mya to the very early Holocene of approximately 10 years ago. Both extant centrarchid species and centrarchid fossils are found only in North America, indicating that origin and diversification of this clade did not involve other continental regions. There are 11 valid and extinct centrarchid species known only from fossil material (Table 1.1; Figures 1.2–1.17), and there are fossils of seven extant species. Despite an excitingly abundant centrarchid fossil record, at least four of the oldest fossil centrarchid species are generally unknown to science. These fossil species are undescribed and have been under study for at least three decades. Unfortunately, they have not been made available to other researchers for study, which has significantly hindered progress in understanding the evolutionary origin of Centrarchidae and its patterns of diversification. The meager information available for these four undescribed fossil species that we present here is from general synopses of the fossil record of North American freshwater fishes (Cavender 1986, 1998). The first of these four we call the High Plains Sunfish, from the northwestern part of Montana near the foothills of the Rocky Mountains. Cavender (1986, 1998) indicates that they are found in Late Eocene to Early Oligocene deposits, but more precise age estimates are unavailable. The High Plains Sunfish has three anal spines and an emarginate caudal fin. The second of these undescribed fossils is the Chadron Sunfish

6

Centrarchid fishes

Plioplarchus sexspinosus

Figure 1.2 Photos and drawings of fossil Centrarchidae species: †Plioplarchus sexspinosus Sentinel Butte Sunfish, photo redrawn from Eastman (1917).

Plioplarchus whitei

Figure 1.3 Photos and drawings of fossil Centrarchidae species: †Plioplarchus whitei Laramie Sunfish, redrawn from Cope (1884).

Plioplarchus septemspinosus

Figure 1.4 Photos and drawings of fossil Centrarchidae species: †Plioplarchus septemspinosus John Day Sunfish, photo redrawn from Eastman (1917).

Boreocentrarchus smithi

Figure 1.5 Photos and drawings of fossil Centrarchidae species: †Boreocentrarchus smithi Healy Creek Sunfish, redrawn from Schlaikjer (1937).

Species diversity, phylogeny and phylogeography of Centrarchidae

7

Pomoxis lanei

Figure 1.6 Photos and drawings of fossil Centrarchidae species: Pomoxis †lanei Ogallala Crappie, photo redrawn from Hibbard (1936).

Pomoxis sp.

Figure 1.7 Photos and drawings of fossil Centrarchidae species: Pomoxis †sp. Wakeeney Crappie, redrawn from Wilson (1968).

Archoplites clarkii

Figure 1.8 Photos and drawings of fossil Centrarchidae species: Archoplites †clarki Clarkia Perch, photo provided by Smith (1963).

Archoplites taylori

2 mm

2 mm

2 mm 2 mm

Figure 1.9 Photos and drawings of fossil Centrarchidae species: Archoplites †taylori Lake Idaho Sunfish, redrawn from Miller and Smith (1967).

8

Centrarchid fishes

Archoplites molarus

1 cm

1 cm

1 cm

1 cm

1 cm

Figure 1.10 Photos and drawings of fossil Centrarchidae species: Archoplites †molarus Ringold Sunfish, redrawn from Smith et al . (2000).

Lepomis kansasensis

Figure 1.11 Photos and drawings of fossil Centrarchidae species: Lepomis †kansasensis Rhino Hill Sunfish, photo redrawn from Hibbard (1936).

Lepomis serratus

2 mm

2 mm 2 mm

1 mm Figure 1.12 Photos and drawings of fossil Centrarchidae species: Lepomis †serratus Keigh Sunfish, redrawn from Smith and Lundberg (1972).

Species diversity, phylogeny and phylogeography of Centrarchidae

9

Lepomis sp. A

Figure 1.13 Photos and drawings of fossil Centrarchidae species: Lepomis †sp. A Valentine Sunfish, redrawn from Smith (1962).

Lepomis sp. B

Figure 1.14 Photos and drawings of fossil Centrarchidae species: Lepomis †sp. B Wakeeney Sunfish, redrawn from Wilson (1968).

Micropterus relictus

Figure 1.15 Photos and drawings of fossil Centrarchidae species: Micropterus †relictus 1975 Chapala Bass, redrawn from Smith et al . (1975).

Micropterus sp. B

Figure 1.16 Photos and drawings of fossil Centrarchidae species: Micropterus †sp. B Wakeeney Bass, redrawn from Wilson (1968).

Micropterus sp. C

Figure 1.17 Photos and drawings of fossil Centrarchidae species: Micropterus †sp. C Laverne Bass, redrawn from Smith (1962).

10

Centrarchid fishes

from Lower Oligocene limestone deposits in the South Dakota Badlands, dating this fossil to the White River group of approximately 28 to 35 mya (Tedford et al . 1987). The Chadron Sunfish has three anal spines and 27 to 28 vertebrae (Cavender 1986). The third fossil sunfish in this group of undescribed forms is from Lower Miocene deposits in South Dakota, and Cavender (1986) provides an age of approximately 25 mya. These are very similar in morphology to the Chadron Sunfish, but have 29 vertebrae (Cavender 1986). The last of the four undescribed fossils in Cavender (1986) is from Middle Miocene deposits, but no location is given. This fossil species has six or seven anal fin spines and is similar to fossils that were assigned to †Plioplarchus (Cope 1884). There are two extinct genera of Centrarchidae known from the fossil record, †Plioplarchus and †Boreocentrarchus. †Plioplarchus contains three species (Table 1.1), and is the oldest of the described centrarchid fossils (Figures 1.2–1.4). †Plioplarchus sexspinosus and †P. whitei were described from Oligocene age freshwater limestone deposits from the Sentinel Butte of North Dakota (Cope 1883) that date to approximately 30 mya (Feldman 1962) (Figures 1.2 and 1.3). †Plioplarchus sexspinosus and †P. whitei are also found in the Badlands of South Dakota in the White River Group. Specimens that are either †P. sexspinosus or †P. whitei are found at the contact between the Chadron and Brule Formations (Welzenbach 1992), and this is dated to approximately 31 mya (Tedford et al . 1987). †Plioplarchus septemspinosus was described from the John Day River in Oregon (Cope 1889) in the geological deposits that make up the John Day Fauna (Figure 1.4), and is dated between 18 and 31 mya (Tedford et al . 2004). Fossils currently assigned to †P. septemspinosus are also found in the Trout Creek Flora in Oregon and this is dated at 13 mya (Graham 1999). Morphological analyses indicate that †P. septemspinosus from the John Day and Trout Creek locations in Oregon are different from each other and both of these are quite divergent from †P. sexspinosus and †P. whitei (Schlaikjer 1937; Bailey 1938; Smith and Miller 1985). These differences were substantial enough for Bailey (1938) in his unpublished Ph.D. dissertation to describe a new genus for †P. septemspinosus. †Boreocentrarchus smithi was described from Healy Creek, Alaska in deposits that were thought to age from the Oligocene to the Early Miocene (Figure 1.5) (Schlaikjer 1937; Uyeno and Miller 1963), and a more precise estimate of this formation at 24 to 18 mya agrees with these earlier estimates (Merritt 1987). Schlaikjer (1937) argues that †B. smithi is closely related to †P. septemspinosus, but others have questioned whether †B smithi is a centrarchid (Uyeno and Miller 1963). Both †Plioplarchus and †Boreocentrarchus are classified in the Centrarchinae (Table 1.1), because these species possess more than three anal fin spines. Undescribed fossil species in this clade include one from the Horse Creek Fish Quarry in Laramie Co., Wyoming, that dates to approximately 19 mya (Cassiliano 1980), another from the Bear Valley, California (Smith and Miller 1985), and a third from the Humboldt Formation, Nevada, that dates to 9 mya (Smith and Miller 1985; Smith et al . 2002). The remaining centrarchid fossil species are classified in genera that also contain extant species (Table 1.1). Pomoxis is known from the fossil record with one described species, P . †lanei, and one undescribed fossil species. Pomoxis †lanei was found in the Rhino Hill Quarry in Logan Co., Kansas (Hibbard 1936), and age of this fossil formation is correlated with Coffee Ranch mammals that date to 6.6 mya (Wallace 1997; Passey et al . 2002). The holotype of P. †lanei is a complete and crushed skeleton (Figure 1.6). The specimen is a remarkable impression and many morphological features can be scored, counted, or measured (Hibbard 1936). The phylogenetic position of P. †lanei in Pomoxis is unresolved due to conflicting characters. The presence of seven dorsal fin spines and a long dorsal fin base supports the hypothesis that P. †lanei and P. nigromaculatus are sister species (Smith 1962). However, the hypothesis that P. nigromaculatus and P. annularis are sister species is supported by the presence of 17 to 20 anal fin rays in these species versus 12 anal fin rays in P. †lanei (Uyeno and Miller 1963). There is a second fossil species of Pomoxis that is undescribed. These fossils were found in the Wakeeney local fauna that is a part of the Ogallala Formation in Kansas (Wilson 1968). The age of this formation was placed in the lower portion of the Ash Hollow or upper Valentine Formation (Wilson 1968), and this dates to approximately 12 mya (Tedford et al . 2004). These are the oldest Pomoxis fossils and they are fragmentary, consisting of a dentary and premaxillary fragments (Figure 1.7). Archoplites contains three fossil species and only one extant species (Table 1.1). The oldest of the Archoplites fossil species is A. †clarki from the Clarkia Lake Beds in Idaho (Figure 1.8) (Smith and Miller 1985). This fossil formation has been dated at 15.5 mya (Golenberg et al . 1990; Wing 1998). Archoplites †taylori is found in seven different fossil locations in southwestern Idaho and these sites are characterized as lacustrine deposits (Figure 1.9). The oldest of the fossil sites containing A. †taylori is the Poison Creek formation and is dated at 9 mya (Smith and Cossel 2001). The youngest formation containing A. †taylori fossils is Jackass Butte, a part of the Grandview local fauna dated at 2.2 mya (Smith 1975; Lundelius et al . 1987). Archoplites †molarus was recently described from the Ringold Formation

Species diversity, phylogeny and phylogeography of Centrarchidae

11

in Washington (Figure 1.10). Fossils of A. †molarus are found at three different locations in the Ringold Formation and the ages of these deposits extend through the Pliocene. Fossils from the White Bluffs local fauna are the oldest at 4.5 mya, the Blufftop Locality and local fauna dates to 3.7 mya, and Tauton Locality dated at 2.9 mya contains the youngest A. †molarus fossils (Smith et al . 2000; Van Tassell et al . 2001). The oldest fossils assigned to the extant species Archoplites interruptus are from the Cache Formation in Lake Co., California and date to the Early Pleistocene, approximately 2.5 mya (Casteel and Rymer 1975). The youngest A. interruptus fossils are from Sacramento Co., California and date to the Pleistocene of approximately 100,000 years ago (Hansen and Begg 1970). There is the possibility of undescribed fossil species of Archoplites. Van Tassell et al . (2001) mention specimens from Grande Ronde Valley in Union Co., Oregon that date to 3.7 mya, and there are other Archoplites fossil specimens dated to the Early or Middle Pleistocene from Moses Lake in Washington (Miller 1965). There are four fossil species of Lepomis, and two of these are closely related to L. gulosus. Lepomis †kansasensis was found in the same fossil formation as P. †lanei, so it is dated at 6.6 mya (Hibbard 1936; Wallace 1997; Passey et al . 2002). The holotype is a nearly complete skeletal impression with a badly crushed head, but morphological features such as dentition can be distinguished (Figure 1.11). The presence of pterygoid teeth in L. †kansasensis led to the original classification of this species in Chaenobryttus that also contained L. gulosus (Hibbard 1936; Bailey 1938). Lepomis †serratus was described from fossils collected at the Keim Formation in the Sand Draw local fauna in Brown Co., Nebraska (Smith and Lundberg 1972). The age of this formation is dated at 3.4 mya (Repenning 1987). The Sand Draw L. †serratus fossils are dentaries, articulars, maxillae, prevomers and preopercles (Figure 1.12). Lepomis †serratus maxillae, prevomers, articulars, and preopercles, premaxillae, and dentaries are also reported from the Seneca local fauna in Hooker Co., Nebraska (Bennett 1979), and this is a younger fossil formation dated between 2.5 and 2.0 mya (Bell et al . 2004). Lepomis †serratus was classified in Chaenobryttus on the basis of morphological similarity of the preopercle with L. gulosus (Smith and Lundberg 1972). The initial classifications proposed for L. †kansasensis and L. †serratus indicate a fairly close phylogenetic affinity with L. gulosus, illustrated by the fact that at one point L. †kansasensis was synonymized with L. gulosus (Branson and Moore 1962). However, Smith and Lundberg (1972) argue that L. †kansasensis is more closely related to other Lepomis species than to L. gulosus, but concur that a definitive conclusion on this issue would result only from a more thorough analysis of the fossil material. There are at least two undescribed Lepomis fossil species. Both of these fossils are quite old and are represented by fragmentary material of the lower jaw. The first of these is referred to as L. †sp. A, and was initially identified as L. cf. microlophus (Smith 1962). The fossil comes from the Lower Valentine Formation in Brown Co., Nebraska (Figure 1.13) (Smith 1962). This fossil location was later identified as the Norden Bridge local fauna (Estes and Tihen 1964), and is dated at 13.5 mya (Tedford et al . 2004). The second undescribed Lepomis fossil species is referred to as L. †sp. B (Figure 1.14), and is found in the same fossil location as the undescribed Pomoxis fossil species discussed earlier (Wilson 1968), so this fossil also dates to approximately 12 mya. There are four fossil Micropterus species, but only one is described. Micropterus †relictus was described from and its jaw element fossils found in Late Pliocene–Early Pleistocene deposits in the Lake Chapala Basin, Mexico (Figure 1.15) (Smith et al . 1975). Micropterus †sp. A consists of fragmentary skull pieces and vertebrae from the Lower Snake Creek fauna in Sioux Co., Nebraska (Matthew 1924), and dates between 16 and 15 mya (Tedford et al . 2004). Micropterus †sp. B was originally identified as M. cf. punctulatus, and the fossil material is a lower pharyngeal jaw and a dentary fragment (Figure 1.16). The fossils were collected in the same formation as Pomoxis †sp. and Lepomis †sp. B and date to 12 mya (Wilson 1968). Micropterus †sp. C. is a dentary from the Laverne Formation in Beaver Co., Oklahoma (Figure 1.17) with an estimated age between 10.5 and 9.5 mya (Smith 1962; Tedford et al . 2004). In addition to A. interruptus discussed earlier, there are at least six extant centrarchid species present in the fossil record. The oldest formations that contain extant species are the Rexroad local fauna in Meade Co., Kansas and the Sand Draw local fauna in Brown Co., Nebraska (Smith 1962; Smith and Lundberg 1972), both dated at 3.4 mya (Bell et al . 2004). These two formations combined contain fossil specimens of Ambloplites rupestris, L. cyanellus, and L. humilis. Both L. cyanellus and L. humilis occur in numerous Pleistocene fossil deposits. Lepomis cyanellus is found in Pleistocene formations ranging in age from 2.3 mya to 10,000 years ago and these sites are spread across Kansas, Michigan, Nebraska, Oklahoma, and Texas (Smith 1954, 1958, 1963; Schultz 1965; Hibbard and Dalquest 1966; Lundberg 1967; Eshelman 1975; Neff 1975; Shoshani and Smith 1996). Pleistocene formations containing L. humilis fossils range in age from 2.5 mya to 250,000 years ago and are restricted to Kansas, Nebraska, and South Dakota (Smith 1963; Ossian 1973; Neff 1975; Bennett 1979; Cross et al . 1986). L. megalotis fossils are found at two Pleistocene fossil formations. The oldest of

12

Centrarchid fishes

these two locations is the Rita Blanca Lake Deposit in Hartley Co., Texas and this formation is dated at 2.4 mya (Anderson and Kirkland 1969; Koster 1969; Lindsay et al . 1975; Lundelius et al . 1987; Repenning 1987), whereas the Kanopolis local fauna in Ellsworth Co., Kansas has yielded much younger L. megalotis fossils dated at 300,000 years ago (Neff 1975; Repenning 1987). Micropterus salmoides fossils have been reported from Pleistocene deposits in Kansas, Michigan, and South Dakota that are dated from 300,000 to 14,000 years (Smith 1963; Wilson 1967; Ossian 1973; Neff 1975). Fossil L. gibbosus specimens are known only from a single Pleistocene locality in South Dakota (Ossian 1973).

1.4 Phylogeny 1.4.1 Pre-Cladistic concepts of centrarchid evolutionary relationships The nineteenth century was the time when most of the valid centrarchid species were described (Figure 1.1). Associated with this period of activity was the initial development of hypotheses of centrarchid relationships. In these early studies evolutionary relationships were reflected by the composition of species in particular taxonomic groups that were arranged in nested hierarchical ranks. For example, at the taxonomic rank of family, centrarchids were initially classified with Percidae (G¨unther 1859), implying a close relationship with pikeperches (Sander), perches (Perca), and darters (e.g., Etheostoma and Percina). The name Ichthelidae was applied to the centrarchids when they were first grouped apart from Percidae as a distinct family (Holbrook 1860). This family name was not used by later authors as Icthelis was regarded as a synonym (Bailey 1938). The first use of the name Centrarchidae came at a time when most of the valid species were described (Cope 1868). Subsequent studies adopted Centrarchidae as the family rank name and presented nested classifications that were meant to imply evolutionary relationships (Jordan 1877; McKay 1881; Bollman 1891). Jordan’s (1877) classification had two subfamilies with one containing Micropterus and all other genera were classified in the second subfamily, Lepominae. Within the Lepominae, the genera Ambloplites, Archoplites, Acantharchus, and Chaenobryttus (Lepomis gulosus) were grouped together. The remaining Lepomis species were classified into five genera that are no longer recognized, and Enneacanthus, Centrarchus, and Pomoxis were placed in the same grouping. The classification presented by McKay (1881) did not include taxonomic ranks above genus. Previous to this classification all Lepomis species were classified into eight genera, Chaenobryttus, Apomotis, Xenotis, Bryttus, Helioperca, Xystroplites, Eupomotis, and Lepomis. McKay (1881) placed all of these species, except for L. gulosus, into Lepomis. The classification presented by Bollman (1891) is important in that it recognized three subfamilies, Centrarchinae, Lepominae, and Micropterinae that are still in use (Table 1.1). Bollman’s (1891) proposed Centrarchinae contained Centrarchus and Pomoxis, whereas the Lepominae contained Archoplites, Ambloplites, Chaenobryttus, Acantharchus, Enneacanthus, Mesogonistius, and Lepomis. Lepomis gulosus was retained in Chaenobryttus as it was considered distantly related to other Lepomis species. The Micropterinae contained two recognized Micropterus species. After the studies of McKay (1881) and Bollman (1891), pharyngeal jaw morphology provided important information for hypotheses of relationships among Lepomis species. Hypertrophied lower pharyngeal arches were presented as evidence to remove L. gibbosus from Lepomis and into the genus Eupomotis (Richardson 1904). A later review of the pharyngeal arches resulted in an amplification of Bollman’s (1891) proposal that all species previously classified in Apomotis, Xenotis, Bryttus, Helioperca, Xystroplites, and Eupomotis were closely related and all species from these genera were placed in Lepomis (Bean and Weed 1911). However, as pointed out by Bailey (1938), some of the discussion in Richardson (1904) and Bean and Weed (1911) was based on hybrid individuals. The first representation of centrarchid relationships presented as a branching dendrogram was in Schlaikjer’s (1937) “suggestions on the phylogeny of the recent Centrarchidae.” This schematic of centrarchid relationships did not result from the current concept of a phylogenetic analysis, but was inferred from body depth, relative mouth size, and numbers of rays and spines on the dorsal and anal fins (Figure 1.18). In this “phylogeny” Centrarchus macropterus was depicted as the ancestral centrarchid species with Pomoxis and Archoplites being represented as early splits from this ancestral lineage. Elongated body shape was an important characteristic that motivated the grouping of Acantharchus, Ambloplites, and Micropterus (including the invalid Huro) (Figure 1.18). In contrast to the classifications of McKay (1881) and Bollman (1891), Schlaikjer (1937) classifies Lepomis species (except L. gulosus) into three genera (Lepomis, Apomotis, and Eupomotis) that were depicted as a group in the branching diagram (Figure 1.18). The Enneacanthus species, including

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Enneacanthus gloriosus

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Figure 1.18 Phylogeny of Centrarchidae presented in Schlaikjer (1937).

Pomoxis annularis

Eupomotis gibbosus

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Centrarchid fishes

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op litin i

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rini

pte

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ae

Archoplites interruptus

Figure 1.19 Phylogeny of Centrarchidae presented in Bailey (1938). Archoplites interruptus redrawn from Girard (1858).

the invalid Mesogonistius, were placed as closely related to Lepomis, with L. gulosus (in Chaenobryttus) outside of this group (Figure 1.18). Bailey (1938) in an unpublished Ph.D. dissertation presented a classification of Centrarchidae and a “hypothetical phylogeny” for the group that was depicted as a branching diagram (Figure 1.19). The characters used by Bailey (1938) were primarily anal fin spines, branchiostegal rays, dentition, body shape, opercle serration, scale morphology, and gill raker morphology. By classifying Centrarchus, Pomoxis, Archoplites, Acantharchus, and Ambloplites in the subfamily Centrarchinae, Bailey (1938) was the first author to propose that species in these genera are closely related (Figure 1.19). The genera Chaenobryttus (L. gulosus), Lepomis, Enneacanthus, Mesogonistius (Enneacanthus chaetodon), Micropterus, and Huro (M. salmoides) were classified together in the subfamily Lepominae (Figure 1.19). Given the uncertainty of Bailey’s (1938) placement of Enneacanthus and Mesogonistius in the phylogenetic tree (Figure 1.19), Lepomis and Chaenobryttus were depicted as the sister lineages and most closely related to Micropterus. Eight subgenera were proposed for ten recognized Lepomis species. Sister species pairs proposed within Lepomis were L. cyanellus–L. symmetricus, L. macrochirus–L. humilis, L. gibbosus–L. microlophus, and L. megalotis–L. marginatus. A detailed “phylogeny” of Lepomis species, as proposed by Bailey (1938), is given in Figure 1.20. A “theoretical phylogeny” was presented in a taxonomic revision of Micropterus that described four new species and subspecies (Figure 1.21; Hubbs and Bailey 1940). This Micropterus “phylogeny” was intuitively derived and based on character variation in scale row and fin counts, and pigmentation patterns (Figure 1.21). In this phylogeny Huro was still used as a monotypic genus to contain M. salmoides. Also, the subspecies of M. punctulatus were not presented as a group that is most closely related to one another (Figure 1.21). This is explained by the fact that Hubbs and Bailey (1940, p. 41)

Species diversity, phylogeny and phylogeography of Centrarchidae

Bailey (1938)

15

L. gulosus L. cyanellus L. symmetricus L. punctatus L. gibbosus L. microlophus L. humilis L. macrochirus L. auritus

Lepomis macrochirus

L. megalotis L. marginatus

Figure 1.20 Detailed phylogeny of Lepomis presented in Bailey (1938). Subgenera of Lepomis in Figure 1.19 were translated to species names using tables presented in Bailey (1938). Lepomis macrochirus redrawn from Forbes and Richardson (1920).

did not rule out a scenario where M. coosae originated through hybridization and introgression between M. dolomieu and M. punctulatus. This explains the “paraphyletic” depiction of M. punctulatus in their branching diagram (Figure 1.21). The phylogeny presented in Bailey (1938) was slightly modified and used to study the evolution of dorsal fin supports in percoid fishes, and particularly in Centrarchidae (Figure 1.22) (Smith and Bailey 1961). In this branching diagram Archoplites is resolved as the sister species of a group containing Pomoxis and Centrarchus (Figure 1.22). The phylogenetic position of Enneacanthus (Mesogonistius was no longer recognized) was still unresolved, but was hypothesized as closely related to Lepomis and Micropterus and not to genera in Centrarchinae (Smith and Bailey 1961). The lateralis system and osteology provided characters for inferences regarding centrarchid phylogeny (Branson and Moore 1962). In this study, relationships were proposed separately for centrarchid genera, species in Lepomis, and species in Micropterus. The “hypothetical dendography” presented as a phylogeny among centrarchid genera is quite different from the hypotheses presented in Bailey (1938) (Figure 1.19) and Smith and Bailey (1961) (Figure 1.22). In Branson and Moore’s (1962) hypothesis, Centrarchinae, as proposed by Bailey (1938), is paraphyletic relative to the Lepominae, and Chaenobryttus is nested outside of a sister group containing Lepomis and Micropterus (Figure 1.23a). Within Lepomis, Branson and Moore (1962) converge on a hypothesis of relationships that is less resolved than Bailey’s (1938) (Figure 1.20), but agree with Bailey (1938) in presenting the L. cyanellus–L. symmetricus and L. macrochirus–L. humilis species pairs (Figure 1.23b). The proposal of relationships among Micropterus species presented by Branson and Moore (1962) agrees with that of Hubbs and Bailey (1940) (Figure 1.21) in depicting M. salmoides as the sister species to all other Micropterus species. Also, Branson and Moore (1962) provide a phylogenetic hypothesis for M. treculi and M. notius (Figure 1.23c), two species that were either not recognized or not described when Hubbs and Bailey (1940) revised Micropterus. The last of the pre-cladistic hypotheses of centrarchid relationships discussed in this review was published after the development of cladistic methods, but is a verbal hypothesis of relationships among Micropterus species based primarily on pigmentation and ecological characteristics (Ramsey 1975). Three lineages in Micropterus were identified and Ramsey’s (1975) hypothesis was converted into a generally unresolved phylogeny. In this tree M. salmoides is grouped by itself, M. coosae and M. dolomieu are sister species, and M. punctulatus, M. treculi, M. notius, and M. cataractae are placed in an unresolved grouping (Figure 1.23d).

16

Centrarchid fishes

Hubbs and Bailey (1940)

Huro salmoides

M.d. dolomieu

M.d. velox

M. coosae

M.p. wichitae M.p. henshalli

M.p. punctulatus

Micropterus salmoides

Figure 1.21 Phylogeny of Micropterus presented in Hubbs and Bailey (1940). Micropterus salmoides redrawn from Forbes and Richardson (1920).

1.4.2 Phylogenetic hypotheses derived from analysis of character data The preceding section reviewed ideas about centrarchid evolutionary relationships that were intuitive, and did not utilize forms of character optimization seen in the current practice of phylogenetic systematics (Swofford et al . 1996). This section reviews more recent hypotheses of centrarchid relationships, and includes those that use a particular optimality criterion to analyze a coded character dataset. As a result of the publication of several studies and datasets over the past 30 years, Centrarchidae has come to provide an exciting system to investigate very relevant issues in systematics such as character congruence among independent molecular datasets (Near et al . 2004), the use of fossil data for calibrating molecular phylogenies (Near et al . 2005b), and the optimal use of phylogenies and divergence time estimates in comparative studies (Bolnick and Near 2005; Collar et al . 2005). The first studies of centrarchid relationships that used a defined optimality criterion to analyze a comparative data matrix were also the first studies to use genetic data in reconstructing centrarchid phylogeny. Allozymes, which are alternative forms of an enzyme produced by different alleles of a given locus that are usually detected by protein electrophoresis, were used to investigate relationships among centrarchid genera and among Lepomis species (Avise and Smith 1974b, 1977; Avise et al . 1977). In these studies allozyme variation was converted to pair-wise genetic distances, and the unweighted pair-group method (UPGMA) was used for cluster analyses that resulted in branching dendrograms. The phylogeny resulting from the UPGMA analysis that included the greatest taxon sampling among these studies is presented in Figure 1.24a (Avise and Smith 1977). These analyses agreed with earlier, pre-cladistic hypotheses by presenting Micropterus and Lepomis as sister lineages (Bailey 1938; Branson and Moore 1962), but Pomoxis grouped with this clade instead of with other

Species diversity, phylogeny and phylogeography of Centrarchidae

17

Smith and Bailey (1961) Pomoxis

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IN A

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Figure 1.22 Phylogeny of Centrarchidae presented by Smith and Bailey (1961). Enneacanthus chaetodon redrawn from Smith (1907).

Centrarchinae (Acantharchus, Archoplites, Centrarchus, and Ambloplites). However, it is important to note that the branch length for this node in the allozyme genetic distance dendrogram was very short (Avise and Smith 1977, Figure 5). The allozyme phylogenies differ from several of the earlier morphological hypotheses in having Enneacanthus closely related to genera comprising Bailey’s (1938) concept of Centrarchinae (Acantharchus, Archoplites, Centrarchus, and Ambloplites), and not Lepomis and Micropterus. Also, relationships within Lepomis were different from the hypotheses presented in Bailey (1938) and Branson and Moore (1962) (Figures 1.20 and 1.23a, b), perhaps most notable is that L. gulosus was nested well within Lepomis, and not in a separate clade that would warrant recognition of Chaenobryttus. A later allozyme study that used a distance Wagner method to construct a centrarchid phylogeny (Parker et al . 1985) resulted in a fairly similar tree (Figure 1.24b). One noticeable difference was the nonmonophyly of Lepomis, a result that may have been an artifact of the genetic distance calculations or the distance clustering method used in this study (Figure 1.24b). Characters from kidney morphology, anal fin spine counts, and olfactory organ morphology were used in the first explicit cladistic analysis of centrarchid phylogeny (Mok 1981). Two separate trees were presented, as Mok (1981) did not combine all the morphological characters for one cladistic analysis. The first phylogeny lacked resolution and was based on five characters from kidney morphology (Figure 1.25a). The presence of an extreme posterior kidney was interpreted as a shared derived character (synapomorphy) for all Centrarchidae except Micropterus. The phylogeny has a basal polytomy with the outgroup taxon (Elassoma), Micropterus, and all other centrarchid genera (Figure 1.25a). Despite the lack of phylogenetic resolution Mok’s (1981) analysis of kidney morphology resulted in a clade containing Centrarchus and Pomoxis that agreed with earlier pre-cladistic hypotheses (Bailey 1938; Smith and Bailey 1961; Branson and Moore 1962). Mok (1981) stressed that the kidney morphology does not support the previous hypotheses that presented Lepomis and Micropterus

18

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(a) Branson and Moore (1962)

(b) Branson and Moore (1962) L. cyanellus L. symmetricus

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M. coosae M. treculi M. punctulatus M. treculi

M. notius M. cataractae

Figure 1.23 (a) Phylogeny of centrarchid genera presented by Branson and Moore (1962). (b) Phylogeny of Lepomis presented by Branson and Moore (1962). (c) Phylogeny of Micropterus presented by Branson and Moore (1962). (d) Phylogeny of Micropterus converted from a verbal hypotheses presented by Ramsey (1975).

as sister taxa (Bailey 1938; Smith and Bailey 1961; Branson and Moore 1962). The second phylogeny in Mok (1981) was based on two characters, the number of anal spines and folding of the olfactory sac, as presented in Eaton (1956). This tree was also unresolved, but it did argue that more than three anal fin spines was a synapomorphy for Ambloplites, Acantharchus, Archoplites, Centrarchus, and Pomoxis (Figure 1.25b), a result that agreed closely with Bailey’s (1938) concept of Centrarchinae (Figures 1.19 and 1.25b). An undefined set of morphological characters was used for a cladistic analysis of centrarchids, and the resulting tree served as the basis for a comparative study of diet, functional feeding morphology, and behavior (Lauder 1986). The phylogeny had a basal polytomy with Micropterus, Lepomis, and clade containing Pomoxis, Centrarchus, Acantharchus, Archoplites, and Ambloplites (Figure 1.25c). Lepomis was monophyletic and L. gulosus was not closely related to Micropterus. In agreement with Bailey (1938), L. gibbosus and L. microlophus were sister species (Figures 1.20 and 1.25c) The next morphological phylogeny of Centrarchidae was presented in an unpublished Ph.D. dissertation and was based on cladistic analyses of 27 morphological characters (Chang 1988). This phylogeny was pectinate, or completely imbalanced, with Micropterus as the basal sister taxon to all other centrarchids (Figure 1.25d). One interesting aspect of this phylogeny was the placement of Enneacanthus as the sister taxon of the genera that comprise Bailey’s (1938) concept of Centrarchinae, and not closely related to Micropterus or Lepomis. Also, in agreement with several previous studies (Bailey 1938; Smith and Bailey 1961; Mok 1981; Parker et al . 1985), Centrarchus and Pomoxis were sister taxa (Figure 1.25d). Chang’s (1988) study is particularly important because it identified four morphological synapomorphies for Centrarchidae (exclusive of Elassoma), a posterior bifurcation of the swim bladder, the first hemal spine of the same length as the second, a deep groove on the first hemal spine, and contact between the first and second hemal spines.

Species diversity, phylogeny and phylogeography of Centrarchidae

(a) Avise and Smith (1977)

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Figure 1.24 (a) Allozyme inferred phylogeny of Centrarchidae presented by Avise and Smith (1977). (b) Allozyme inferred phylogeny of Centrarchidae presented by Parker et al . (1985).

In a study examining the evolutionary patterns in functional morphological aspects of feeding in centrarchids, Wainwright and Lauder (1992) used a centrarchid phylogeny that resulted from a cladistic analysis of 53 undefined morphological characters. The tree was similar to that of Chang (1988) in that Micropterus is the basal sister taxon to all other Centrarchidae (Figure 1.26a). Also, in agreement with Bailey’s (1938) concept of Centrarchinae, this phylogeny presented Acantharchus, Ambloplites, Pomoxis, Centrarchus, and Archoplites as a monophyletic group (Figure 1.26a). Archoplites interruptus and C. macropterus were recovered as sister species, a relationship that had not been proposed in any of the previous hypotheses; however, Mok (1981) presented a tree based on olfactory organ folding that had a clade containing Pomoxis, Centrarchus, and Archoplites (Figure 1.25b). Interestingly, in Wainwright and Lauder’s (1992) phylogeny, Enneacanthus was nested within Lepomis and L. gulosus was the phylogenetically basal species in this clade. Some details of the relationships in Lepomis proposed by Wainwright and Lauder (1992) are consistent with previous hypotheses (Bailey 1938; Branson and Moore 1962), and others are unique to this analysis (Figure 1.26a). Mabee (1989, 1993) presented a phylogenetic analysis of Centrarchidae using 61 morphological characters. The trees were used to study the ontogenetic criterion in phylogenetics, asking if an ontogenetic series for a particular character provided a reasonable method to polarize the character in a phylogenetic analysis (Mabee 1989, 1993). From our own reanalysis of the data matrix and other published analyses of this dataset (Mabee 1993; Patterson 1996), it is clear that parsimony analysis using outgroup rooting results in hundreds (if not thousands) of most parsimonious trees. However, a single tree from the set of most parsimonious trees was selected for purposes of Mabee’s (1989, 1993) analyses of ontogenetic character evolution (Figure 1.26b). Despite the seemingly arbitrary nature of the selection of this tree, the strict consensus of the most parsimonious trees is quite well resolved (see Patterson 1996, Figure 1a), and is completely resolute with regard to the details of the phylogenetic relationships discussed in this review.

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Figure 1.25 (a) Phylogeny of Centrarchidae based on a cladistic analysis of kidney morphology presented by Mok (1981). (b) Phylogeny of Centrarchidae based on a cladistic analysis of anal spine counts and scale morphology presented by Mok (1981). (c) Phylogeny of Centrarchidae based on a cladistic analysis of morphological characters presented by Lauder (1986). (d) Phylogeny of Centrarchidae based on a cladistic analysis of 27 morphological characters presented by Chang (1988).

The phylogeny presented by Mabee (1989, 1993) is interesting in many respects (Figure 1.26b). In agreement with two of the other morphological cladistic analyses (Chang 1988; Wainwright and Lauder 1992), Micropterus is the sister lineage of all other Centrarchidae. The relationships within Lepomis were very similar to that presented by Wainwright and Lauder (1992)—L. gulosus was the sister species to all others in the clade, and Enneacanthus was nested in Lepomis. Within Lepomis, Mabee’s (1989, 1993) phylogeny has two sister species pairs, L. megalotis–L. marginatus and L. microlophus–L. gibbosus seen in other phylogenies (Bailey 1938; Avise and Smith 1977; Lauder 1986; Wainwright and Lauder 1992); however, the sister species pairs L. macrochirus–L. humilis and L. cyanellus–L. symmetricus proposed by Bailey (1938) and Branson and Moore (1962) were not supported by these analyses (Figure 1.26b). In agreement with many of the earlier, pre-cladistic, morphological hypotheses (Bailey 1938; Branson and Moore 1962), a monophyletic Centrarchinae, exclusive of Enneacanthus, was present in the selected single tree from the pool of most parsimonious trees (Figure 1.26b). However, Acantharchus falls out of this clade in the strict consensus tree (Patterson 1996, Figure 1a). Over the past 5 years DNA data has increasingly been used in phylogenetic analyses of Centrarchidae. Three studies have focused on relationships of Micropterus species (Johnson et al . 2001; Kassler et al . 2002; Near et al . 2003) and have produced fairly congruent results; however, there are some unresolved issues with regard to species recognition in the clade that are illuminated by these molecular studies. Johnson et al . (2001) analyzed the phylogeny of Micropterus species using a maximum parsimony analysis of restriction enzyme digests of whole mtDNA genomes. The monophyly

Species diversity, phylogeny and phylogeography of Centrarchidae

(a) Wainwright and Lauder (1992) Micropterus Acantharchus Ambloplites Pomoxis Centrarchus Archoplites L. gulosus E. gloriosus E. chaetodon E. obsesus L. cyanellus L. symmetricus L. humilis L. auritus L. megalotis L. marginatus L. macrochirus L. punctatus L. microlophus L. gibbosus

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(b) Mabee (1993) M. salmoides M. dolomieu M. notius M. punctulatus M. treculi M. coosae Acantharchus P. annularis P. nigromaculatus Centrarchus Archoplites A. rupestris A. cavifrons A. ariommus A. constellatus L. gulosus L. cyanellus L. macrochirus L. symmetricus E. chaetodon E. obsesus E. gloriosus L. humilis L. auritus L. marginatus L. megalotis L. punctatus L. gibbosus L. microlophus

Figure 1.26 (a) Phylogeny of Centrarchidae based on a cladistic analysis of morphological characters presented by Wainwright and Lauder (1992). (b) Phylogeny of Centrarchidae based on a cladistic analysis of 61 morphological characters presented by Mabee (1989, 1993).

of Micropterus was not tested as only a single outgroup species was used, but the phylogeny depicts M. salmoides as the sister species to all other Micropterus (Figure 1.27a). Near et al . (2003) presented a maximum likelihood analysis of DNA sequences from two mtDNA genes, cytb and ND2 that were collected from 50 individuals sampled from 8 Micropterus species. This maximum likelihood phylogeny was similar to the tree presented by Johnson et al . (2001), but differs primarily where the root was placed. This difference was most likely a consequence of the use of a single outgroup taxon. Also, Johnson et al . (2001) did not provide support values for nodes in the phylogeny, and Near et al . (2003) presented a phylogeny that had most of the interspecific nodes supported with high bootstrap pseudoreplicate scores (Figure 1.27b). In Near et al .’s (2003) tree M. dolomieu and M. punctulatus were sister species, and this clade was sister to the remaining Micropterus species (Figure 1.27b). Differing from Johnson et al . (2001), Near et al . (2003) found M. treculi as the sister species of a clade containing M. salmoides and M. floridanus. There are two aspects of the Micropterus phylogeny presented by Near et al . (2003) that support the recognition of M. floridanus as a species distinct from M. salmoides: (i) the two species exhibit reciprocally monophyletic mtDNA haplotypes, and (ii) the intraspecific branch lengths are shorter than those subtending the interspecific node (Figure 1.27b). Kassler et al . (2002) utilized the sampling of cytb and ND2 mtDNA sequences from Near et al . (2003), but added more M. treculi specimens and included M. henshalli in the phylogenetic analyses. Also, Kassler et al . (2002) presented phylogenies that are derived from the analysis of 19 polymorphic allozyme loci. The mtDNA maximum likelihood phylogeny yielded two very surprising results. First, two distinct M. treculi mtDNA haplotypes were discovered. One of

22

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(b) Near et al. (2003) M. punctulatus

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Micropterus notius Micropterus treculi Micropterus salmoides

M. dolomieu 96 100 M. punctulatus

Micropterus floridanus 0.005 substitutions/site

Figure 1.27 (a) Phylogeny of Micropterus based on a cladistic analysis of restriction digests of whole mtDNA genomes presented by Johnson et al . (2001). (b) Phylogeny of Micropterus based on a maximum likelihood analysis of mtDNA gene sequences presented in Near et al . (2003). Outgroup species are not shown. A scale bar for the expected number of substitutions is given in the lower right, and numbers at nodes are percent recovery in a bootstrap analysis.

these was resolved as the sister taxon of the clade containing M. floridanus and M. salmoides, and the other was closely related to M. punctulatus. Second, M. henshalli was nested within the haplotypes sampled for M. coosae (Figure 1.28a). These two patterns could be attributed to mtDNA introgression, a process known to occur in fishes (Avise 2001), but the allozyme inferred phylogeny offers some important clues to the unexpected results in the mtDNA phylogeny (Figure 1.28b). In an unpublished study, we have screened 100 M. treculi from three locations within the species’ limited native range and found 49 individuals with the haplotype that is sister to the M. floridanus–M. salmoides clade, and 51 individuals with the haplotype that is closely related to M. punctulatus (Figure 1.28a). There is no geographic pattern within M. treculi as the two haplotypes were found in equal frequency within the three populations sampled. However, regardless of which of the two divergent mtDNA haplotypes are found in a given M. treculi specimen, there is virtually no intraspecific variation among allozyme alleles or DNA sequences from nuclear genes. In the allozyme phylogeny constructed using a frequency parsimony method (Swofford and Berlocher 1987), M. treculi is closely related to M. punctulatus, a result that is expected from the previous classification of M. treculi as a subspecies of M. punctulatus (Hubbs and Bailey 1942). The presence of a divergent mtDNA haplotype that is closely related to the M. floridanus–M. salmoides clade that has no counterpart in the nuclear gene phylogeny (Figure 1.28b) cannot be explained by human introductions of M. punctulatus into the native range of M. treculi. As it stands, the mystery of the two divergent mtDNA haplotypes in the background of what appears to be a homogenous nuclear genome of M. treculi will have to be solved in future studies. The case of M. henshalli, or the Alabama Spotted Bass, is equally puzzling as the pattern revealed in M. treculi. The mtDNA maximum likelihood phylogeny resolves M. p. henshalli as distantly related to M. punctulatus and the haplotypes are nested within M. coosae (Figure 1.28a). Micropterus henshalli and M. coosae are sympatric throughout the Mobile Basin (Mettee et al . 1996; Boschung and Mayden 2004) and the similarity of the mtDNA haplotypes would indicate a

Species diversity, phylogeny and phylogeography of Centrarchidae

(a) Kassler et al. (2002) (mtDNA)

23

(b) Kassler et al. (2002) (allozymes)

M. floridanus

M. coosae

M. salmoides

M. treculi M. notius M. cataractae

M. dolomieu

M. dolomieu M. floridanus

M. punctulatus

M. cataractae

M. notius

M. treculi M. henshalli M. salmoides M. henshalli M. coosae M. punctulatus 0.5 changes

M. treculi

Figure 1.28 (a) Phylogeny of Micropterus based on a maximum likelihood analysis of mtDNA gene sequences presented by Kassler et al . (2002). Outgroup species are not shown. (b) Phylogeny of Micropterus based on a frequency parsimony analysis of allozyme alleles at 19 loci presented by Kassler et al . (2002).

recent introgression of mtDNA from M. coosae to M. henshalli. The allozyme phylogeny resolves M. henshalli as the sister taxon of a clade containing M. punctulatus and M. treculi with a very long branch separating M. henshalli from this clade (Figure 1.28b). In our own work we have collected M. coosae and M. henshalli in sympatry in the upper Coosa River system. These individuals have very similar mtDNA haplotypes (1.3% uncorrected genetic distance), but despite the sympatry of these species the M. p. henshalli haplotypes cluster together exclusive of the paraphyletic M. coosae mtDNA haplotypes (Figure 1.28b). Even if mtDNA introgression is obscuring the true phylogeny of M. henshalli, it is apparent that it is quite distinct from M. punctulatus at nuclear encoded loci (Figure 1.28b) and exhibits substantial morphological divergence (Gilbert 1973). Complete coding sequences from the mtDNA cytb gene were used to examine intraspecific and interspecific relationships of Lepomis species (Harris et al . 2005). All species in the clade, except the very recently elevated L. peltastes, were sampled and multiple individuals were included from each sampled species. As reported by Harris et al . (2005), mtDNA haplotypes from five Lepomis species were not reciprocally monophyletic (Figure 1.29). However, for reasons outlined in the following text, we have found it necessary to reanalyze the cytb data from Harris et al . (2005). The phylogeny presented in this review was obtained using a Bayesian analysis similar to that used by Near et al . (2005b), and we present the phylogeny as a phylogram (Figure 1.29). Harris et al . (2005) state that introgression and the presence of cryptic species best explain the pattern of extensive nonmonophyly observed in Lepomis species. Despite a reasonable probability for this scenario, hybridization cannot be detected without genetic data from nuclear genes or morphological analyses (Neff and Smith 1979; Shaw 2002), and identification of cryptic species would minimally require some degree of assessment of morphological divergence, but such data were not presented (Harris et al . 2005). One possible explanation for the nonmonophyly of Lepomis species not

24

Centrarchid fishes

Harris et al. (2005) * *

L. auritus group A

* * *

L. punctatus L. miniatus

* L. microlophus * L. miniatus

*

L. gulosus *

Illinois Oklahoma

*

*

L. symmetricus

L. cyanellus

* L. marginatus group A *

* * L. megalotis group A * L. marginatus group B * L. megalotis group C * Maryland L. auritus group B North Carolina * Maryland L. gibbosus West Virginia Minnesota

*

*

*

* L. m. macrochirus

* 0.05 changes

L. auritus group C L. m. mystacalis L. humilis

*

Figure 1.29 Phylogeny of Lepomis based on a reanalysis of mtDNA gene sequence data presented by Harris et al . (2005). The phylogram resulted from a Bayesian mixed model analysis. Outgroup species are not shown. A scale bar for the expected number of substitutions is given in the lower left, and asterisks at nodes indicate support with significant (
0.95) Bayesian posterior probabilities.

explored by Harris et al . (2005) is misidentification of specimens. For example, the haplotype of L. symmetricus sampled from McCurtain Co., Oklahoma is very similar (low genetic divergence) to the haplotypes sampled from L. cyanellus (Figure 1.29). Given that L. cyanellus is sympatric with L. symmetricus in this region of Oklahoma (Miller and Robison 2004), specimens of L. cyanellus from the same location as this divergent L. symmetricus haplotype were not sampled, and Harris et al . (2005) do not state that they verified the identification of these specimens together, which means that specimen misidentification cannot be ruled out. The same circumstance can possibly be applied to the phylogenetic resolution of haplotypes from L. auritus group B that nests in the same clade as the sampled L. gibbosus haplotypes (Figure 1.29). The striking similarity of the haplotypes in L. auritus group B and L. gibbosus, in addition to the fact that the two species are sympatric where the L. auritus group B specimens were collected, points to a possible instance of specimen misidentification. Ancestral polymorphism was not considered as a mechanism that could result in the pattern of extensive species nonmonophyly observed in the Lepomis phylogeny (Figure 1.29). Ancestral polymorphism can result in nonmonophyly of a species’ alleles when the ancestral species is polymorphic at the locus, and the random sorting of the alleles during the splitting into multiple daughter species results in a gene tree that is incongruent with the species phylogeny (Neigel and Avise 1986; Pamilo and Nei 1988; Wu 1991; Hudson 1992; Hudson and Coyne 2002). The time to reach coalescence, when the species haplotypes are monophyletic, is proportional to the effective population size. Due to maternal inheritance, the coalescent time for mtDNA haplotypes is one quarter that expected for alleles of an autosomal locus (Moore 1995). One heuristic method to assess if ancestral polymorphism is driving a phylogenetic result is to determine if interspecific branches

Species diversity, phylogeny and phylogeography of Centrarchidae

25

(genetic distances) are longer than intraspecific branches in the phylogeny, with the assumption that long interspecific branches indicate that sufficient time has elapsed to expect coalescence and reciprocal monophyly (Moore 1995). The paraphyly of L. miniatus and L. marginatus–L. megalotis are in regions of the Lepomis phylogeny that have fairly short interspecific branch lengths relative to the intraspecific branch lengths, so ancestral polymorphism should not be ruled out as a cause for the observed paraphyly of these species. The first phylogenetic investigation among centrarchid genera using DNA sequences was an analysis of the mitochondrial cytb gene by Roe et al . (2002). The importance of this study was limited by the sampling of only one half of all centrarchid species, and by sparse phylogenetic resolution. Two recent studies have examined relationships of all extant centrarchid species, except the recently elevated L. peltastes and M. henshalli, using DNA sequences from multiple genes. Near et al . (2004) presented phylogenetic trees resulting from maximum parsimony and Bayesian analyses of a three gene data set consisting of the mtDNA, ND2, and two nuclear genes (S7 ribosomal protein intron 1 and the protein coding Tmo4C4 ). Two important conclusions were discussed in Near et al . (2004). First, separate analyses of each of the three sampled gene regions resulted in very similar phylogenies that indicated little incongruence between mtDNA and nuclear gene trees. Second, Shimodaira–Hasegawa tree topology tests indicated that 13 of 20 previous hypotheses of centrarchid relationships examined were significantly different from the best tree that resulted from the Bayesian analysis of the mitochondrial and nuclear gene dataset (Table 1.2). This allowed a unique perspective on how these earlier hypotheses compared in the context of a large set of characters that were sampled for most of the species level diversity in Centrarchidae. The phylogenies inferred from mitochondrial and nuclear gene DNA sequences demonstrated the monophyly of all polytypic genera, and in agreement with earlier studies resolved Lepomis and Micropterus as sister lineages (Bailey 1938; Smith and Bailey 1961; Branson and Moore 1962; Avise and Smith 1977), and provided strong support for a clade containing Enneacanthus Centrarchus, Archoplites, Ambloplites, and Pomoxis (Figure 1.30a, b). Other interesting relationships resolved in these analyses included Archoplites and Ambloplites as sister taxa, and the identification of two sister species pairs within Ambloplites. Relationships within Lepomis were highly resolved and most nodes received strong support in maximum parsimony bootstrap analysis or had significant Bayesian posterior probabilities (Figure 1.30a, b). The sister species pairs L. cyanellus–L. symmetricus and L. humilis–L. macrochirus, proposed by Bailey (1938) and Branson and Moore (1962) (Figures 1.20 and 1.23b), were strongly supported in the mtDNA and nuclear gene phylogenies (Figures 1.30a, b). Also, L. megalotis and L. marginatus were resolved as sister species, supporting the results from several earlier studies (Bailey 1938; Avise and Smith 1977; Mabee 1993). Previous investigations of Lepomis phylogeny have hypothesized that L. microlophus and L. gibbosus are sister species. This relationship was not supported in the mtDNA and nuclear gene phylogenies (Figure 1.30a, b). These two species are the only Lepomis species that exhibit specialized diets, feeding primarily on snails. Both L. microlophus and L. gibbosus possess morphological and behavioral specializations that function in crushing snails (Lauder 1983, 1986; Wainwright and Lauder 1992), and many of these characters had been used as evidence of common ancestry for these two species (Bailey 1938; Branson and Moore 1962; Lauder 1986; Wainwright and Lauder 1992; Mabee 1993). These phylogenies indicated that the evolution of these characters involved with molluscivory have a more complex evolutionary history than previously hypothesized. The dataset used in Near et al . (2004) was expanded to include one additional mitochondrial gene (16S ribosomal RNA) and two additional nuclear genes (calmodulin intron 4 and rhodopsin) for a total of 5553 base pairs of aligned DNA sequence data (Near et al . 2005b). The purpose of this study was to use fossil information to calibrate the molecular phylogeny to estimate divergence times in Centrarchidae. Ten centrarchid fossils were used to provide minimal age estimates for nodes in the phylogeny. Using a fossil cross-validation method (Near and Sanderson 2004; Near et al . 2005a), Near et al . (2005b) were able to identify four fossil calibrations that provided inconsistent molecular age estimates, and six consistent centrarchid fossils were used to calibrate the molecular phylogeny. Molecular divergence times of centrarchid species were estimated using penalized likelihood, a method that account for lineage specific molecular evolutionary rate heterogeneity (Sanderson 2002). The centrarchid phylogeny was presented as a chronogram, where the branch lengths are drawn to reflect estimates of absolute evolutionary ages (Figure 1.31). Given the temporal context of centrarchid diversification, Near et al . (2005b) point out that the origin of Centrarchidae at approximately 35 mya in the late Eocene–early Oligocene corresponds to a time of major global climate change to cooler conditions, and a signature in the fossil record of both lineage extinction and origination for many disparate clades across the tree of life. Another important result from the centrarchid chronogram that was exploited by later studies of functional character evolution and patterns of post-zygotic reproductive isolation was the finding that the major centrarchid lineages had

26

Centrarchid fishes

Table 1.2 Shimodaira–Hasegawa tests of alternative phylogenetic hypotheses of centrarchid fishes. Significant results are presented with an asterisk. Hypothesis

p

Three gene Bayesian phylogeny; Figure 1.30b

–

Schlaikjer (1937); Figure 1.18

<0.001*

Bailey (1938); Figure 1.19

<0.001*

Smith and Bailey (1961); Figure 1.22

<0.001*

Branson and Moore (1962); Figure 1.23a

<0.001*

Avise et al. (1977); Figure 1.24a

0.452

Mok (1981); Figure 1.25a

<0.001*

Mok (1981); Figure 1.25b

<0.001*

Parker et al. (1985); Figure 1.24b

0.002*

Lauder (1986); Figure 1.25c

0.912

Chang 1988; Figure 1.25d

0.472

Wainwright and Lauder (1992); Figure 1.26a

<0.001*

Mabee (1993); Figure 1.26b

<0.001*

Lepomis Bailey (1938); Figure 1.20 Branson and Moore (1962); Figure 1.23b

<0.001* 0.089

Micropterus Hubbs and Bailey (1940); Figure 1.21

0.014*

Branson and Moore (1962); Figure 1.23c

<0.001*

Ramsey (1975); Figure 1.23d

<0.001*

Johnson et al. (2001); Figure 1.27a

0.900

Near et al. (2003); Figure 1.27b

0.989

Kassler et al. (2002); Figure 1.28a

0.986

different ages (Bolnick and Near 2005; Collar et al . 2005; Bolnick et al . 2006). For instance, the Centrarchinae (exclusive of Acantharchus) was the oldest major centrarchid clade followed by Lepomis, then Micropterus. Interestingly, despite the fact that Lepomis and Micropterus were sister lineages, the chronogram revealed that the ages of the most recent common ancestor (MRCA) in each clade was quite different with the Lepomis MRCA being substantially older than the MRCA of Micropterus (Figure 1.31). The phylogeny inferred from the expanded mitochondrial and nuclear gene data set presented in Near et al . (2005b) is very similar to those estimated from the earlier mitochondrial and nuclear gene DNA study (Near et al . 2004) (Figures 1.30a, b and 1.31). Important differences included the resolution of Acantharchus pomotis as the sister taxon of all other Centrarchidae (Figure 1.31), where maximum parsimony and Bayesian analyses differed on the placement of this species in the phylogeny in Near et al . (2004) (Figure 1.30a, b).

1.5 Phylogeography Phylogeography investigates the relationships between phylogeny and geography for a species or group of related species. It is an approach to understanding intraspecific geographic subdivision, evolutionary pathways to that subdivision, and

Species diversity, phylogeny and phylogeography of Centrarchidae

(a) Near et al. (2004) (parsimony)

100

53

50

Acantharchus pomotis Enneacanthus chaetodon Enneacanthus gloriosus 100 Enneacanthus obesus 100 Centrarchus macropterus Archoplites interruptus 91 Ambloplites cavifrons 53 Ambloplites constellatus Ambloplites ariommus 100 100 Ambloplites rupestris Pomoxis annularis 100 Pomoxis annularis Pomoxis nigromaculatus 100 Pomoxis nigromaculatus 100 Pomoxis nigromaculatus 100 Micropterus dolomieu Micropterus dolomieu 100 Micropterus punctulatus Micropterus punctulatus 99 Micropterus notius 100 100 Micropterus notius Micropterus cataractae Micropterus coosae 62 Micropterus treculi 100 Micropterus treculi Micropterus salmoides 78 Micropterus floridanus 97 100 Micropterus floridanus Lepomis auritus 77 Lepomis marginatus 100 Lepomis megalotis 99 Lepomis megalotis 100 100 Lepomis gibbosus Lepomis microlophus 93 Lepomis punctatus 100 Lepomis miniatus 100 100 Lepomis miniatus 100 Lepomis humilis 100 Lepomis humilis Lepomis macrochirus 100 100 Lepomis macrochirus Lepomis gulosus 58 100 Lepomis gulosus Lepomis symmetricus changes 100 Lepomis cyanellus 100 100 Lepomis cyanellus

27

(b) Near et al. (2004) (Bayesian)v

* *

Centrarchus macropterus Enneacanthus chaetodon Enneacanthus gloriosus Enneacanthus obesus Archoplites interruptus Ambloplites ariommus Ambloplites rupestris Ambloplites cavifrons Ambloplites constellatus Pomoxis annularis Pomoxis annularis Pomoxis nigromaculatus Pomoxis nigromaculatus Pomoxis nigromaculatus Acantharchus pomotis Micropterus dolomieu Micropterus dolomieu Micropterus punctulatus Micropterus punctulatus Micropterus coosae Micropterus cataractae Micropterus notius Micropterus notius Micropterus treculi Micropterus treculi Micropterus salmoides Micropterus floridanus Micropterus floridanus Lepomis gulosus Lepomis gulosus Lepomis symmetricus Lepomis cyanellus Lepomis cyanellus Lepomis humilis Lepomis humilis Lepomis macrochirus Lepomis macrochirus Lepomis auritus Lepomis marginatus Lepomis megalotis Lepomis megalotis Lepomis gibbosus Lepomis microlophus Lepomis punctatus substitutions per site Lepomis miniatus Lepomis miniatus

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

*

* *

*

*

*

* *

*

0.01

*

*

*

*

Figure 1.30 (a) Phylogeny of nearly all centrarchid species based on a maximum parsimony analysis of mitochondrial and nuclear gene DNA sequences. The phylogram is a strict consensus of four most parsimonious trees. Outgroup species are not shown. A scale bar for the number of optimized changes is given in the lower left, and numbers at nodes are percent recovery in a bootstrap analysis. (b) Phylogeny of nearly all centrarchid species based on a partitioned mixed-model Bayesian analysis of mitochondrial and nuclear gene DNA sequences. Outgroup species are not shown. A scale bar for the expected number of substitutions is given in the lower left, and asterisks at nodes indicate support with significant (
0.95) Bayesian posterior probabilities.

geographic patterns of speciation. In simple terms, phylogeography involves putting phylogenies on geographic maps (Avise et al . 1987), and the term was derived to simplify the description of patterns that emerge from co-analysis of a species’ genetic diversity and the geographic framework on which that diversity is distributed. Phylogeography also involves understanding the segregation of genetic diversity under varying conditions of behavioral, physiological, and abiotic separation as they have affected gene flow (Templeton 1998). Both historic and current geographic barriers to dispersal and gene flow have shaped distributional patterns of fish species, and in many instances these patterns are evident across phylogenetically divergent lineages inhabiting the same environments and geographic regions (Avise et al . 1987; Mayden 1987; Strange and Burr 1997; Near et al . 2001). Intraspecific phylogeographic assessments are not without confounding factors. In the case of centrarchid species of recreational fishing importance, stocking over the last 100+ years has spread fish from often-distant sources across virtually all of the major watersheds in North America. Any phylogeographic analysis would have to potentially sort out the admixture of native and introduced genotypes to correctly assess the distribution of diversity. In extreme cases, the original ancestral type could be lost, leaving an anomaly in the genetic landscape (Epifanio and Philipp 2000). For example, a recent study of the distribution of alleles at two loci fixed for M. salmoides and M. floridanus concluded that the extent of mixing was so great in Virginia reservoirs that it was uncertain which species was native (Dutton et al . 2006).

28

Centrarchid fishes

Near et al. (2005)

*

* *

*

C

*

*

*

Acantharchus pomotis Centrarchus macropterus Enneacanthus chaetodon Enneacanthus gloriosus Enneacanthus obesus Pomoxis annularis Pomoxis nigromaculatus Archoplites interruptus Ambloplites ariommus Ambloplites rupestris Ambloplites cavifrons Ambloplites constellatus Micropterus dolomieu Micropterus punctulatus Micropterus cataractae Micropterus coosae Micropterus notius Micropterus treculi Micropterus salmoides Micropterus floridanus Lepomis humilis Lepomis macrochirus Lepomis gulosus Lepomis symmetricus Lepomis cyanellus Lepomis auritus Lepomis marginatus Lepomis megalotis Lepomis gibbosus Lepomis microlophus Lepomis punctatus Lepomis miniatus

*

C

*

* *

*

*

*

* *

C

C

*

*

*

*

C

*

*

C

* *

* * Eocene

Oligocene Early

33.7

Miocene

Late

28.4

Early

23.8

Middle

16.4

Late

11.2

*

* Pi

Ps

5.2 2.5

Figure 1.31 Phylogeny of nearly all centrarchid species based on a partitioned mixed-model Bayesian analysis of a seven gene dataset of mitochondrial and nuclear gene DNA sequences. The phylogeny is time-calibrated (chronogram) using six centrarchid fossils to provide minimal age estimates for nodes in the tree. Nodes calibrated with fossils are indicated with a circled ‘‘C.’’ The chronogram is calibrated against the geological time scale. Outgroup species are not shown. Asterisks at nodes indicate support with significant (
0.95) Bayesian posterior probabilities.

1.5.1 Phylogeography of Micropterus Although studies of polymorphic genetic loci had been conducted on M. salmoides (Whitt et al . 1971), Philipp et al . (1983) represented the first phylogeographic analysis of a Micropterus species. Based on fixed allelic differences at two allozyme loci, the native range of M. salmoides was divided into three areas that corresponded to M. salmoides, M. floridanus, and intergrades between the two species. Coupled with allele frequency data at two additional allozyme loci, latitudinal clines were revealed that indicate the distribution of populations follows thermal clines (Philipp et al . 1983). Additional allozyme studies on a more-local scale have had mixed results. In South Carolina, variation among sites verified that this region of the Atlantic Slope was an area of intergradation between M. salmoides and M. floridanus, and observed clinal variation appeared to correspond to mean annual temperature (Bulak et al . 1995). However, further north in Virginia, there was no geographic pattern with respect to the fixed alleles that differentiate M. salmoides and M. floridanus, and the authors concluded that this pattern was indicative of either stocking of nonnative species, or that M. salmoides is not native to the region sampled (Dutton et al . 2006). In addition to the two fixed allelic differences, there is substantial mtDNA divergence between M. salmoides and M. floridanus (Nedbal and Philipp 1994; Kassler et al . 2002; Near et al . 2003). Allozyme variation was used to investigate the phylogeography of M. dolomieu across its geographic range, but with a biased sampling of Interior Highlands (Ozark and Ouachita uplands) populations (Stark and Echelle 1998). Substantial genetic heterogeneity among sampling sites was detected (i.e. high Fst values). Multivariate analysis of genetic variation between populations identified four clusters of populations: southwestern Ozarks, northern Ozarks and upper Mississippi, and Ohio drainages, and two distinct Ouachita Highland clusters. Phylogenetic analysis using frequency

Species diversity, phylogeny and phylogeography of Centrarchidae

29

parsimony indicated that M. dolomieu populations from northern Ozark rivers were more closely related to populations sampled from the Ohio and Upper Mississippi River Basins than to other Ozark populations (Stark and Echelle 1998). Phylogeographic analysis of western populations of M. punctulatus using mtDNA sequences from the control region and allele frequencies from five microsatellite DNA loci found little genetic variation (Coughlin et al . 2003). However, it was determined that populations from the Arkansas River were more similar to Ouachita River populations, relative to Red River populations. Based on the paleogeography of the river drainages (Mayden 1985, 1988), it was expected that the Red and Ouachita River populations would be most similar genetically. Coughlin et al . (2003) hypothesized mtDNA introgession between M. punctulatus and M. dolomieu because they discovered a shared haplotype. Considering the sister species relationship and recent divergence time between M. punctulatus and M. dolomieu (Kassler et al . 2002; Near et al . 2003, 2005b), we argue that retention of ancestral polymorphism better explains this instance of mtDNA haplotype sharing. Analysis of the mtDNA cytb and ND2 has revealed extensive phylogeographic structuring among populations of the Mobile Basin endemic M. coosae. A small sample of individuals from three different sites in the eastern Mobile Basin exhibited appreciable variation at the mtDNA genes with an estimated intraspecific divergence time of approximately 1.0 mya (Near et al . 2003). Considering that the Mobile Basin is characterized by a substantial number of endemic fish species (Lydeard and Mayden 1995; Mettee et al . 1996; Boschung and Mayden 2004), the discovery of genetic differentiation among such a paltry sampling of M. coosae populations is not surprising. A more thorough phylogeographic analysis based on a sampling of M. coosae throughout its limited geographic range has potential to reveal interesting cryptic diversity.

1.5.2 Phylogeography of Lepomis Despite the fact that most Lepomis species have fairly large geographic ranges, there have been few published studies of intraspecific phylogeography. As discussed in Section 1.2.1 on subspecies, these types of studies have the potential to discover patterns of geographic variation, identify cryptic species, and test species boundaries. The first centrarchid phylogeographic study was Avise and Smith (1974a) who examined allozyme allelic variation in southern L. macrochirus populations. This study revealed an area of intergradation between two described subspecies, L. m. macrochirus and L. m. mystacalis, and genetic differentiation of Texas populations. Subsequent studies have found similar patterns resulting from analyses of mtDNA (Avise and Smith 1977; Avise et al . 1984). Phylogeography of four Lepomis species (L. miniatus, L. punctatus, L. microlophus, and L. gulosus) along the southeastern seaboard of the United States was examined with mtDNA haplotype variation (Bermingham and Avise 1986). Intraspecific patterns in two of these species exhibited phylogeographic discontinuities that were concordant with previously defined biogeographic boundaries identified from the distributional limits of other organisms (Wiley and Mayden 1985). The sister species L. miniatus and L. punctatus exhibited a pattern similar to the intraspecific-level analyses of L. gulosus and L. microlophus with a phylogeographic break at the Apalachicola River (Figure 1.32). Morphological differentiation between the sister species L. miniatus and L. punctatus and between eastern and western populations of L. microlophus is concordant with the mtDNA inferred phylogeographic breaks (Bailey 1938; Warren 1992). The phylogeographic discontinuities exhibited in L. microlophus, L. gulosus, and between L. punctatus and L. miniatus were attributed to sea-level fluctuations along the Costal Plain that had the effect of connecting and isolating costal rivers at different times during the Pliocene and Pleistocene (Bermingham and Avise 1986). The effect of water level fluctuation on the extinction and colonization dynamics of Everglades L. punctatus populations was investigated with allozyme and microsatellite markers (McElroy et al . 2003). As predicted, annual environmental fluctuations in the Everglades of Florida, in the form of water level reductions, led to increases in variation on a local level. Sampling design in this case could have resulted in a very different result if recolonization from areas with higher water levels was not considered (McElroy et al . 2003). In Section 1.2.1 on centrarchid species and subspecies, we discussed that L. megalotis contains four to possibly seven recognized subspecies. The distribution of L. megalotis includes most of the Ohio, middle and lower Mississippi river drainages, and several Gulf of Mexico drainages in Alabama, Mississippi, and Texas. The recent elevation of L. peltastes (Table 1.1; Bailey et al . 2004) based on morphological differences has only partially resolved the problem of the status of subspecies and intraspecific relationships within L. megalotis. Substantial allozyme allelic frequency differences were observed in L. megalotis with differences detected between eastern and western populations (Jennings and Philipp 1992).

30

Centrarchid fishes

Lepomis punctatus and L. miniatus

0.08

0.06

0.04

0.02

0.00

P

Lepomis punctatus Lepomis miniatus

Lepomis microlophus

0.08

0.06

0.04

0.02

0.00

P

Lepomis microlophus

Figure 1.32 Phylogeography of Lepomis punctatus, L. miniatus, and L. microlophus based on mtDNA haplotype variation (Bermingham and Avise 1986).

There were no fixed allelic differences among the populations and subspecies examined, including comparisons involving L. megalotis and L. peltastes.

1.5.3 Phylogeography of Centrarchinae A survey of allozyme variation in A. constellatus, A. rupestris, and A. ariommus came to three conclusions (Koppelman et al . 2000). First, A. constellatus exhibited substantial genetic differentiation from A. rupestris and A. ariommus and is restricted to the White River and sporadic localities in north-flowing tributaries of the upper Osage River. Second, the sister species A. rupestris and A. ariommus did not exhibit any fixed allelic differences at three polymorphic loci. Third, human introductions might have obscured the phylogeographic patterns between A. ariommus and A. rupestris, and may have been responsible for the presence of A. constellatus in the Osage basin (Koppelman et al . 2000). Recently 23 polymorphic microsatellite markers have been isolated from A. interruptus for studies to document population structure. Information on genetic variation is being collected as a prerequisite for efforts to reestablish populations in the species’ native range (Schwartz and May 2004). Given the close phylogenetic relationship between A. interruptus and the four Ambloplites species (Figures 1.30 and 1.31), these microsatellite markers may be helpful in examining the lack of coalescence observed for the allozyme markers between A. rupestris and A. ariommus.

1.6 Conclusions and future directions The vast majority of valid centrarchid species were described in the nineteenth century (Figure 1.1). Despite a long and rich history of species descriptions, taxonomic revisions, and studies aiming to resolve phylogenetic relationships of Centrarchidae, there is still much that is unresolved. Centrarchid fishes are among the most economically important group of freshwater fishes in the world, but many species remain unrecognized. In this review, we have tried to illustrate

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that many of these species are probably masquerading as subspecies. A resolution to this problem will only come from published studies that examine morphological and genetic variation within polytypic centrarchid species. With regard to the phylogeny of Centrarchidae, we argue that the analyses using both mitochondrial and nuclear gene sequences provide the best estimates of centrarchid relationships (Figure 1.31). This confidence is based on the near-complete taxon sampling that is not seen in most of the other phylogenetic analyses, a sampling of a large number of characters, congruence between the mitochondrial and nuclear gene phylogenies (Near et al . 2004), and the fact that the DNA dataset is able to reject many of the previous centrarchid phylogenetic relationships (Table 1.2). The most important question facing future phylogenetic studies of Centrarchidae involves the apparent phylogenetic incongruence of the morphological and molecular datasets. For example, the resolution of Enneacanthus as nested in Lepomis is a result in the cladistic analyses of morphology that is never resolved in the DNA inferred phylogenies (Figures 1.26a, b, 1.30a, b, and 1.31). Specifically, combined morphological and DNA character analyses may allow the identification of particular morphological character states that are convergent among centrarchid lineages, and do not reflect common ancestry. Also, it will be useful to compile the morphological characters used in the separate cladistic analyses that presumably did not share many character states (Lauder 1986; Chang 1988; Wainwright and Lauder 1992; Mabee 1993). The mitochondrial and nuclear gene DNA sequence phylogeny is not completely resolved with strongly supported nodes (Figure 1.31). It has been demonstrated that phylogenetic resolution and node support in molecular phylogenies can be increased by adding more base pairs of DNA to the dataset (de Queiroz et al . 2002). In order to increase phylogenetic resolution, we recommend the inclusion of additional mitochondrial and single-copy nuclear gene DNA sequences to the phylogenetic dataset. Given the scientific and economic importance of centrarchids, it is surprising that such little phylogeographic information is available for centrarchid species. The few published studies have provided a glimpse into the cryptic patterns of variation perhaps not readily apparent in external morphological characters.

1.7 Acknowledgments TJN thanks P. C. Wainwright for providing important mentorship and collaboration during the initiation of his centrarchid fish studies. JBK is particularly indebted to D. Philipp for past and current guidance in the conservation genetics of centrarchids. We are grateful to S. Cooke, D. Philipp, D. I. Bolnick, and D. A. Etnier for comments on earlier versions of this review. Research funding was provided by the National Science Foundation (DEB-0716155).

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Schlaikjer, E. M. 1937. New fishes from the continental Tertiary of Alaska. Bulletin of the American Museum of Natural History 74: 1–23. Schultz, G. E. 1965. Pleistocene vertebrates from the Butler Spring local fauna, Meade County, Kansas. Papers of the Michigan Academy of Science, Arts, and Letters 50: 235–265. Schwartz, R. S. and B. May. 2004. Characterization of microsatellite loci in Sacramento perch (Archoplites interruptus). Molecular Ecology Notes 4: 694–697. Shaw, K. L. 2002. Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian cricket. Proceedings of the National Academy of Sciences of the United States of America 99: 16122–16127. Shoshani, J. and G. R. Smith. 1996. Late Pleistocene fishes from the Shelton mastodon site (Oakland County, Michigan) and their ecological context. Contributions from the Museum of Paleontology University of Michigan 29: 419–433. Smith, C. L. 1954. Pleistocene fishes of the Berends Fauna of Beaver County, Oklahoma. Copeia 1954: 282–289. Smith, C. L. 1958. Additional Pleistocene and Pliocene fishes from Kansas and Oklahoma. Copeia 1958: 176–180. Smith, C. L. 1962. Some Pliocene fishes from Kansas, Oklahoma, and Nebraska. Copeia 1962: 505–520. Smith, G. R. 1963. A Late Illinoian fish fauna from southwestern Kansas and its climatic significance. Copeia 1963: 278–285. Smith, H. M. 1907. The fishes of North Carolina. North Carolina Geological and Economic Survey 2: 1–453. Smith, M. L. 1975. Fishes of the Pliocene Glenns Ferry formation, southwestern Idaho. Papers on Paleontology the Museum of Paleontology University of Michigan 14: 1–68. Smith, C. L. and R. M. Bailey. 1961. Evolution of the dorsal-fin supports of percoid fishes. Papers of the Michigan Academy of Science, Arts, and Letters 46: 345–363. Smith, G. R. and J. G. Lundberg. 1972. The Sand Draw fish fauna. Pages 40–54 in: M. F. Skinner, and C. W. Hibbard, editors. Pleistocene Preglacial and Glacial Rocks and Faunas of North Central Nebraska. American Museum of Natural History, New York. Smith, G. R. and R. R. Miller. 1985. Taxonomy of fishes from Miocene Clarkia Lake beds, Idaho. Pages 75–83 in: C. J. Smiley, editor. Late Cenozoic History of the Pacific Northwest. American Association for the Advancement of Science, San Francisco, CA. Smith, G. R. and J. Cossel, Jr. 2001. Fishes from the late Miocene Poison Creek and Chalk Hills formations, Owyhee County, Idaho. Pages 23–35 in: W. A. Akersten, M. E. Thompson, D. J. Meldrum, R. A. Raup, and H. G. McDonald, editors. And Whereas. . . Papers on the Vertebrate Paleontology of Idaho Honoring John A. White, Vol. 2. Idaho Museum of Natural History, Pocatello, ID. Smith, M. L., T. M. Cavender, and R. R. Miller. 1975. Climatic and biogeographic significance of a fish fauna from the Late Pliocene-Early Pleistocene of the Lake Chapala Basin (Jalisco, Mexico). Papers on Paleontology the Museum of Paleontology University of Michigan 12: 29–38. Smith, G. R., N. Morgan, and E. Gustafson. 2000. Fishes of the Mio-Pliocene Ringold formation, Washington: Pliocene capture of the Snake River by the Columbia River. University of Michigan Papers on Paleontology 32: 1–47. Smith, G. R., T. E. Dowling, K. W. Gobalet, T. Lugaski, D. K. Shiozawa, and R. P. Evans. 2002. Biogeography and timing of evolutionary events among Great Basin fishes. Pages 175–234 in: R. Hershler, D. B. Madsen, and D. R. Currey, editors. Great Basin Aquatic Systems History. Smithsonian Institution Press, Washington, DC. Stark, W. J. and A. A. Echelle. 1998. Genetic structure and systematics of smallmouth bass, with emphasis on Interior Highlands populations. Transactions of the American Fisheries Society 127: 393–416. Strange, R. M. and B. M. Burr. 1997. Intraspecific phylogeography of North American highland fishes: a test of the Pleistocene vicariance hypothesis. Evolution 51: 885–897. Sweeney, E. F. 1972. The systematics and distribution of the centrarchid fish tribe Enneacanthini. Ph.D. Boston University, Boston, MA. Swofford, D. L. and S. H. Berlocher. 1987. Inferring evolutionary trees from gene-frequency data under the principle of maximum parsimony. Systematic Zoology 36: 293–325. Swofford, D. L., G. J. Olsen, P. J. Waddell, and D. M. Hillis. 1996. Phylogenetic inference. Pages 407–514 in: D. M. Hillis, C. Moritz, and B. K. Mable, editors. Molecular Systematics. Sinauer, Sunderland, MA. Tedford, R. H., M. F. Skinner, R. W. Fields, J. M. Rensberger, D. P. Whistler, T. Galusha, B. E. Taylor, J. R. Macdonald, and S. D. Webb. 1987. Faunal succession and the biochronology of the Arikareean through Hemphillian interval (Late

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Oligocene through earliest Pliocene epochs) in North America. Pages 153–210 in: M. O. Woodburne, editor. Cenozoic Mammals of North America. University of California Press, Berkeley, CA. Tedford, R. H., I. L. B. Albright, A. D. Barnosky, I. Ferrusquia-Villafranca, J. R. M. Hunt, J. E. Storer, I. C. C. Swisher, M. R. Voorhies, S. D. Webb, and D. P. Whistler. 2004. Mammalian biochronology of the Arikareean through Hemphillian interval (Late Oligocene through Early Pliocene epochs). Pages 169–231 in: M. O. Woodburne, editor. Late Cretaceous and Cenozoic Mammals of North America. Columbia University Press, New York. Templeton, A. R. 1998. Species and speciation: geography, population structure, ecology, and gene trees. Pages 32–43 in: D. J. Howard, and S. H. Berlocher, editors. Endless Forms: Species and Speciation. Oxford University Press, Oxford. Uyeno, T. and R. R. Miller. 1963. Summary of Late Cenozoic freshwater fish records for North America. Occasional Papers of the Museum of Zoology The University of Michigan 631: 1–34. Van Tassell, J. L., M. Ferns, V. McConnell, and G. R. Smith. 2001. The mid-Pliocene Imbler fish fossils, Grande Ronde Valley, Union County, Oregon, and the connection between Lake Idaho and the Columbia River. Oregon Geology 63: 77–96. Wainwright, P. C. and G. V. Lauder. 1992. The evolution of feeding biology in sunfishes (Centrarchidae). Pages 472–491 in: R. L. Mayden, editor. Systematics, Historical Ecology, and North American Freshwater Fishes. Stanford University Press, Stanford, CA. Wallace, S. C. 1997. Mammals of the Rhino Hill West Local Fauna, Miocene (Hemphillian), Wallace County, Kansas. M.S. Fort Hays State University, Hays, KA. Warren, M. L., Jr. 1992. Variation of the spotted sunfish, Lepomis punctatus complex (Centrarchidae): meristics, morphometrics, pigmentation and species limits. Bulletin of the Alabama Museum of Natural History 12: 1–47 Welzenbach, L. C. 1992. Limestones in the Lower White River Group (Eocene-Oligocene), Badlands of South Dakota; Depositional Environment and Paleoclimatic Implications. M.S. Bowling Green State University, Bowling Green, OH. Whitt, G. S., W. F. Childers, and T. E. Wheat. 1971. The inheritance of tissue-specific lactate dehydrogenase isozymes in interspecific bass (Micropterus) hybrids. Biochemical Genetics 5: 257–273. Wiley, E. O. and R. L. Mayden. 1985. Species and speciation in phylogenetic systematics, with examples from the North American fish fauna. Annals of the Missouri Botanical Garden 72: 596–635. Williams, J. D. and G. H. Burgess. 1999. A new species of bass, Micropterus cataractae (Teleostei: Centrarchidae), from the Apalachicola River Basin in Alabama, Florida, and Georgia. Bulletin of the Florida Museum of Natural History 42: 80–114. Wilson, R. L. 1967. The Pleistocene vertebrates of Michigan. Papers of the Michigan Academy of Science, Arts, and Letters 52: 197–234. Wilson, R. L. 1968. Systematics and faunal analysis of a Lower Pliocene vertebrate assemblage from Trego County, Kansas. Contributions from the Museum of Paleontology University of Michigan 22: 75–126. Wilson, E. O. and W. L. Brown, Jr. 1953. The subspecies concept and its taxonomic application. Systematic Zoology 2: 97–111. Wing, S. L. 1998. Tertiary vegetation of North America as a context for mammalian evolution. Pages 37–65 in: C. M. Janis, K. M. Scott, and L. L. Jacobs, editors. Evolution of Tertiary Mammals of North America. Cambridge University Press, Cambridge. Wu, C.-I. 1991. Inferences of species phylogeny in relation to segregation of ancient polymorphisms. Genetics 127: 429–435.

Chapter 2

Hybridization and speciation in centrarchids D. I. Bolnick

2.1 Introduction Open any field guide and you will find a list of species, with brief descriptions of how to distinguish each species from other closely related species. Such field guides convey an impression of stable, cleanly delineated groups. This can lead to significant confusion when our orderly Linnean categories run into the sometimes messy reality of biology. For example, consider the recent controversy in the community of North American bird watchers. Birding, the leading magazine for bird hobbyists publishes photographic puzzles regularly, challenging its readers to identify the species. Although often the challenge is made difficult by blurry photographs, bad lighting, bad angles, or drab juvenile plumages, the editor recently published several photographs of interspecific hybrids. To Birding’s readers, who are passionately devoted to assigning each bird to a particular species, this trick was unacceptable. Angry letters poured in to the editor’s office, accusing him of staging “unfair” and “unrealistic” puzzles of “freaks.” Put on the defensive, Birding’s editor, Dr. Ted Floyd, wrote a rebuttal. He argued that far from being freaks, hybrids are a common occurrence in nature, and bird watchers’ passion for identifying everything to a species had blinded them to the animals’ biology and natural history. Hybridization is far more common among freshwater fishes than it is in birds (Campton 1987). Scribner et al . (2001) provide an extensive survey of natural hybrids in freshwater fish, documenting over 150 pairs of hybridizing species and 20% of them are drawn from within Centrarchidae. These hybrids complicate the task of identifying species in an already challenging group. Indeed, a number of hybrids were sufficiently puzzling to earn their own species names, such as Lepomis euryorus which was only later discovered to be the hybrids from matings between Lepomis cyanellus and Lepomis gibbosus (Hubbs and Hubbs 1932; Hubbs 1944). The goal of this chapter is to avoid the bird watchers’ trap, and promote the view that hybridization is not an annoying impediment to proper identification of species, but a useful window on many aspects of centrarchid biology. Hybrids are a vital tool in both academic and applied research, telling us volumes about the origin of species (Darwin devoted a whole chapter of the Origin of Species to hybridization), genetics, and development, while offering both aquacultural opportunities and conservation challenges. This chapter begins with a brief discussion of the incidence of hybridization in centrarchids, and then reviews a variety of subjects that have been illuminated, rather than clouded, by studies of centrarchid hybrids.

2.2 Incidence of hybridization in centrarchids A significant portion of the centrarchid hybrid literature is devoted to documenting the natural history of hybrids: who hybridizes, when, and how much. Much of this body of writing emphasizes the high rate of natural hybridization in centrarchids. Although this may be true relative to other groups of vertebrates, it is still striking how few pairs of species actually hybridize. The 33 described species of centrarchids could in principle produce 528 pairs of species (note that this excludes Micropterus henshalli ). This represents an overestimate of the number of possible hybrid combinations, as not all species’ ranges overlap. Not counting recently introduced populations, a brief look at range maps (Lee et al . 1981) suggests that there are approximately 250 pairs of centrarchid species with at least some geographic overlap. Only 31 of these 250 species pairs actually hybridize in nature (Table 2.1). These hybrids almost always occur among species of the same genus, though natural Centrarchus*Pomoxis hybrids are known (Burr 1974). 39

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Centrarchid fishes

Table 2.1 Species known to hybridize in nature (including disturbed and man-made habitats). The order of species names for a given pair of species does not indicate maternal or paternal status. Evidence for hybridization is morphological unless otherwise noted. References are representative, but are not meant to be exhaustive. Parent species Ambloplites cavifrons

Evidence A. rupestrus

References Cashner and Jenkins (1982)

Centrarchus macropterus Pomoxis annularis

Burr (1974)

E. gloriosus

E. obsus

Allozyme, mtDNA Graham and Felley (1985)

L. auritus

L. cyanellus

Allozyme, mtDNA Avise and Saunders (1984), Raney (1940)

L. auritus

L. gibbosus

Greeley and Bishop (1933)

L. auritus

L. gulosus

McAtee and Weed (1915)

L. auritus

L. macrochirus

L. cyanellus

L. gibbosus

L. cyanellus

L. gulosus

L. cyanellus

L. humilis

L. cyanellus

L. macrochirus

Allozyme, mtDNA Avise and Saunders (1984), Bailey and Lagler (1938)

L. cyanellus

L. megalotis

Allozyme, mtDNA Dawley (1987), Hubbs and Cooper (1935), Cross and Moore (1952)

L. cyanellus

L. microlophus

Trautman (1957)

L. gibbosus

L. gulosus

Radcliffe (1914)

L. gibbosus

L. humilis

Bailey and Lagler (1938), O’Donnell (1953), Thompson (1935)

L. gibbosus

L. macrochirus

Bailey and Lagler (1938) Allozyme

Bailey and Lagler (1938), Dawley (1987) McAtee and Weed (1915) Hubbs and Ortenberger (1929)

Allozyme

Bailey and Lagler (1938), Dawley (1987), Colgan et al. (1976), Hubbs and Hubbs (1933), Konkle and Philipp (1992)

L. gibbosus

L. megalotis

Hubbs (1926)

L. gulosus

L. macrochirus

Avise and Saunders (1984), Birdsong and Yerger (1967), Hubbs (1920)

L. gulosus

L. microlophus

Childers (1967), Childers and Bennett (1961)

L. humilis

L. macrochirus

Bailey and Lagler (1938), Cross and Moore (1952), O’Donnell (1953)

L. humilis

L. megalotis

O’Donnell (1953)

L. macrochirus

L. megalotis

Cross and Moore (1952)

L. macrochirus

L. punctatus

Childers (1967), Childers and Bennett (1961)

L. miniatus

L. punctatus

Warren (1992)

L. macrochirus

L. microlophus

Allozyme, mtDNA Avise and Saunders (1984), Bailey and Lagler (1938), Cross and Moore (1952)

M. coosae

M. dolomieu

Allozyme

M. dolomieu

M. punctulatus

Allozyme, mtDNA Pierce and Van den Avyle (1997), Koppelman et al. (2000), Avise et al. (1997)

M. dolomieu

M. salmoides

Allozyme

Whitmore and Hellier (1988)

M. dolomieu

M. treculi

Allozyme

Whitmore (1983), Morizot et al. (1991), Whitmore and Butler (1982)

M. salmoides

M. treculi

Allozyme

Morizot et al. (1991)

P. annularis

P. nigromaculatus

Allozyme

Hubbs (1955), Buck and Hooe (1986), Maceina and Greenbaum (1988), Smith et al. (1994), Near et al. (2004), Spier and Heidinger (2003), Travnichek et al. (1996), Travnichek et al. (1997)

Pipas and Bulow (1998)

Hybridization and speciation in centrarchids

41

When hybrids do occur, they generally make up a small fraction of the local centrarchid population. At two sites in Georgia, Avise and Saunders (1984) found that only 1.3% of the sampled centrarchids were hybrids. Similarly, Konkle and Philipp (1992) found hybrids comprised ∼5% of sympatric bluegill and pumpkinseed populations, and Whitmore and Hellier (1988) found Micropterus salmoides *M. dolomieu hybrids were <5% of the Micropterus population in a Texas reservoir (less than expected under random mating). Certain locations or species pairs do exhibit much higher rates of hybridization. In a few localities, Lepomis hybrids make up 75% or more of the sunfish population (Trautman 1957). Micropterus treculi have been swamped by hybridization in their native range following the introduction of M. salmoides and M. dolomieu, with hybrids comprising between 20 and 46% of Micropterus populations throughout M. treculi ’s range (Morizot et al . 1991). Hybridization with introduced M. punctulatus has effectively extirpated native M. dolomieu in a Georgia reservoir (Avise et al . 1997). Hybrids of Pomoxis nigromaculatus and Pomoxis annularis are similarly abundant, reaching frequencies of 29.3 to 54.5% at some sites (Dunham et al . 1994). However, the vast majority of sites with sympatric Pomoxis species have few or no hybrids (Hooe and Buck 1991; Dunham et al . 1994; Maceina and Greenbaum 1988; Travnichek et al . 1996). Pomoxis hybrids appear to reach exceptionally high frequencies in certain reservoirs (Weiss Lake and two reservoirs on the Coosa River; Dunham et al . 1994; Smith et al . 1994; Travnichek et al . 1996). Most estimates of hybrid abundance are based on molecular genetic analyses (statistical details reviewed in Scribner et al . 2001). One consistent lesson from these surveys is the difficulty of identifying hybrids based on morphology alone (but see Colgan et al . 1976). For instance, hybrid Pomoxis look nearly indistinguishable from P. nigromaculatus (Dunham et al . 1994). Molecular surveys thus play a key role in documenting the incidence of hybridization in wild populations (Scribner et al . 2001), but have been limited to a few locations and sets of species. Consequently, the extent of hybridization may be underestimated in some cases because hybrids are not always readily recognizable. Nonetheless, it appears safe to say that the vast majority of possible hybridizations do not occur. Both the presence and absence of hybrids can tell us a great deal about the mechanisms by which new species arise and remain distinct, as discussed in the following section.

2.3 What centrarchid hybrids tell us about speciation 2.3.1 Background on speciation When two populations are able to interbreed, any favorable new mutation occurring in one population is able to spread to the other population as well. Such gene flow inhibits genetic and morphological divergence between populations (Slatkin 1985; Garcia-Ramos and Kirkpatrick 1997; Lenormand 2002; Nosil and Crespi 2004). On the other hand, if these populations are unable to interbreed, for instance when there are geographic barriers to dispersal (Box 2.1), each population may accumulate unique genetic traits. Consequently, many systematists use interbreeding as a litmus test for whether two populations are independently evolving units. This view is codified in the most widely used definition of the term “species” in the Biological Species Concept (BSC) as follows: “species are groups of actually or potentially interbreeding populations, which are reproductively isolated from other such groups” (Mayr 1942). Under this definition, “speciation” is defined as the process by which a single species is subdivided into two reproductively isolated groups. The origin of a new species is thus linked to the loss of ability to interbreed with other populations.

Box 2.1

The geography of speciation

Geography plays a vital role in speciation. When a species is subdivided into geographically isolated (allopatric) populations with little or no gene flow, these populations may begin to accumulate genetic differences that ultimately lead to reproductive isolation (Box 2.2). These differences may accrue either due to natural or sexual selection, or by neutral processes (Coyne and Orr 2004). In theory, speciation is also possible when populations are adjoining (parapatric), if selection in different habitats is strong enough to overwhelm the homogenizing effects of gene flow (Gavrilets 2004). Sympatric speciation, in which a single population splits into two isolated species without any

42

Centrarchid fishes

geographic structure, also seems to require the action of disruptive natural selection, though its feasibility has been the subject of debate for over half a century (Ting et al . 1998; Wu 2001; Barbash et al . 2003; Coyne and Orr 2004; Dieckmann et al . 2004; Bolnick and Fitzpatrick 2007). Allopatry is generally assumed to be the default explanation for speciation, though some comparative methods have been used to evaluate the frequency of other approaches by examining the present distribution of sister species (Barraclough and Vogler 2000; Coyne and Price 2000). In centrarchids, a number of sister species have broadly overlapping ranges (L. cyanellus and L. symmetricus; Leptotyphlops humilis and Lepomis macrochirus; Lepomis marginatus and L. megalotis; Enneacanthus gloriosus, E. obesus and E. chaetodon; and the two Pomoxis), contrary to David Starr Jordan’s Rule that closely related species’ ranges do not overlap. Although this might argue in favor of sympatric speciation, the current distributions of these species may be a poor guide to their ranges at the time of speciation. Glaciations and other geological shifts have doubtless caused major changes in species’ ranges, erasing much of the historical signal of the geography of speciation. Indeed, a preliminary study (Bolnick, unpublished), suggests that current levels of sympatry between sister species are no greater than what one might expect to see by chance (when species ranges are randomly assigned on the phylogeny).

The difficulty with this definition is that the ability to interbreed is not lost instantaneously, but declines steadily and gradually as the populations diverge and accumulate genetic incompatibilities (Box 2.2). We are therefore left trying to assign a cutoff to a continuous process: how rare does hybridization have to be before we accept populations as distinct species: 5%, 1%, or 0.001%? Or do populations become species only when there are no hybrids at all? While some workers have advocated this strict interpretation of the BSC (Barton and Hewitt 1985), it often has unacceptable consequences: clearly distinct organisms that everyone intuitively considers as distinct species suddenly have to be combined because they can hybridize on a rare occasion. For example, if we collapsed all groups capable of some gene flow, we would be left with only one or a few species of Lepomis. A more satisfying solution is to abandon such arbitrary cutoffs and acknowledge that speciation is a continuous and gradual process. This is not to reject the concept of species, but to recognize that there is no precise point at which two populations become different species.

Box 2.2

Genetic incompatibilities

Why does evolutionary divergence lead to hybrid sterility or inviability? In the early part of the twentieth century, Bateson (1909), Dobzhansky (1934), and Muller (1939) proposed an answer that seems to have withstood the test of time. The basic idea is that incompatibilities arise when two loci, whose products normally interact, diverge in two populations to the point where this interaction no longer occurs correctly. Examples of such interacting (or “epistatic”) genes might include genes for two metabolic proteins that interact, structural proteins that normally form a dimer, or one gene produces a transcription factor that must bind to another gene’s regulatory site. Consider a single species with two loci, A and B, whose products interact. If the species is split into two geographically isolated populations, both with diploid genotypes AABB, new mutations arising in one population (say, A → a) will not spread to the other population. Note that this new allele a can only spread if it is compatible with both alleles A and B. Consequently, this mutation cannot by itself reduce the fitness of hybrids between populations. If a different mutation spreads in the other population (B → b), there is some chance that the two derived alleles a and b are incompatible, as they have never been tested together in a single organism. Therefore, any hybrid (AaBb) has some chance that the gene products of alleles a and b fail to work together, reducing hybrid fitness. As a single such incompatibility may be enough to cause hybrid sterility or inviability (Barbash et al . 2003; Ting et al . 1998; Wu 2001), it is also possible that this dysfunction evolves gradually as the populations incrementally build up an ever-growing collection of these incompatibilities. Such epistatic deleterious gene interactions have been identified in a few systems (Kenyon and Moraes Carlos 1997; Lewontin 1997; Presgraves 2003; Rawson and Burton 2002) and are called Dobzhansky–Muller incompatibilities.

Hybridization and speciation in centrarchids

43

One consequence of this evolutionary view of speciation is that hybrids are no longer freaks or headaches. Rather, they are an understandable reflection of the evolutionary process. At any point in time, we should expect that there would be some pairs of populations that are partway down the path toward complete speciation, and that are therefore capable of hybridizing. We can take advantage of this fact to learn a great deal about the process of speciation. With very few notable exceptions (Dobzhansky and Pavlovsky 1971; Gottlieb 1973; Carroll et al . 1997; Filchak et al . 2000; Feder et al . 2003), speciation is far too slow for biologists to follow from inception to completion within one or even few lifetimes. However, if we simultaneously consider many pairs of species that have progressed different distances down the path toward speciation, we can create a comparative transect through evolutionary time. By documenting the conditions that permit (or prevent) hybridization, we can learn what genetic changes cause speciation and how they evolve. The bulk of this chapter focuses on what the study of centrarchid hybrids tells us about reproductive isolation and speciation. As mentioned above, there are roughly 250 pairs of centrarchid species with at least partly overlapping geographic ranges. As only about 15% of those pairs are known to hybridize, there must be nongeographic barriers to interspecific mating. Dobzhansky (1951) categorized these barriers into three main types: reproductive isolation can occur when species do not spawn with each other (premating isolation), if spawning fails to produce embryos (gametic isolation), and/or if those embryos are inviable or infertile (postzygotic isolation).

2.3.2 Premating barriers to hybridization in centrarchids Each type of isolation can be further subdivided into categories that reflect a variety of causal mechanisms (Coyne and Orr 2004). For instance, premating isolation occurs when species spawn in different habitats (habitat isolation), at different times of the year (or day) (temporal isolation), or discriminate against heterospecific mates on the basis of morphology or behavior (ethological isolation). Coyne and Orr (2004, pg 182) define habitat isolation as “genetic or biological propensities to occupy different habitats when they occur in the same general area, thus preventing or limiting gene exchange through spatial separation during the breeding season. This isolation can be caused by differential adaptation, differential preference, competition, or combinations of these factors.” It is clear that centrarchids vary in their habitat preferences (Breder 1936), ranging from swamps and backwaters (Centrarchus) to deep channels of moderate to fast-flowing gravel-bottomed streams (Ambloplites ariommus) or large lakes (L. gibbosus) (Boschung and Mayden 2004). Habitat isolation may therefore play an important role in limiting hybridization, but this effect has not been tested quantitatively. Anecdotal evidence suggests that hybridization is more common in “disturbed habitats” (Hubbs 1955) where habitat isolation might have broken down. More subtle isolation can occur when species differ in nesting site within a given habitat. For example, Clark and Keenleyside (1967) note that L. gibbosus tend to build nests closer to shore and in shallower water than Lepomis macrochirus in the same pond. Although the difference was statistically significant, the distributions overlapped such that nest location was not an effective barrier to hybridization (Figure 2.1). Other co-occurring species are described as having distinct nesting preferences, but these examples are anecdotal and qualitative, making them hard to evaluate. Clark and Keenleyside (1967) also carried out one of the few quantitative studies of temporal (or allochronic) isolation. Although L. gibbosus began nesting earlier and at colder water temperatures (13–17◦ C) than L. macrochirus (17–23◦ C), both species had extended and broadly overlapping nesting seasons. Nearly all centrarchid species have extended breeding seasons, often ranging from April until August. It therefore appears unlikely that seasonal isolation plays a major role in maintaining species boundaries in centrarchids (Breder 1936). Although Clark and Keenleyside (1967) found a substantial overlap in nest timing and location of co-occurring Lepomis species, they found no phenotypically intermediate individuals. As Lepomis hybrids are generally viable, the lack of hybrids is presumably because the species did not spawn together (ethological isolation). Miller (1963) noted that L. macrochirus males would actively court conspecific females by circling their nest rim, while attacking or ignoring L. gibbosus females. Similar observations have been made for a number of other centrarchids (largely among Lepomis species), suggesting that behavioral premating isolation is an important component of reproductive isolation (Clark and Keenleyside 1967; Keenleyside 1967; Gerald 1971; Steele and Keenleyside 1971; Clark et al . 1984). For instance L. gibbosus and Lepomis megalotis females showed strong preference for conspecific males, while males of either species were unselective (Steele and Keenleyside 1971; but see Keenleyside 1967).

44

Centrarchid fishes

80

Nest depth (cm)

60 Bluegills 40 Pumpkinseeds 20

0

0

1 2 Distance from shore (m)

3

Figure 2.1 Extensive overlap in nesting habitats of bluegills (L. macrochirus) and pumpkinseeds (L. gibbosus), as measured by depth and distance from shore. The intersections represent the mean value for depth and distance for bluegill and for pumpkinseeds (21 and 44 nests, respectively). Thick lines represent ±1 s.d., thin lines represent observed range. (Adapted from Figure 10 of Clark and Keenleyside (1967) Public source Government of Canada.)

2.3.2.1 Mechanisms of species recognition For assortative mating to occur, fish must be able to distinguish between the conspecifics and heterospecifics. This requires both distinctive phenotypic signals from the prospective mates and a neurological mechanism for the recipient to detect the signal and translate that into a behavioral response. The following discussion focuses exclusively on the types of signals that differentiate species, as we are not aware of any work on the sensory ecology or neuroethology of the recipient’s side of this equation in centrarchids. Visual cues for species identification include morphological structures, sequences of courtship behaviors, and color. The sexually dimorphic opercular tabs of some Lepomis are thought to be an important morphological signal, as they are flared during courtship dances (Keenleyside 1967) and highlighted by brightly colored margins or colorful spots. These tabs are subject to sexual selection within species, as shown by an experimental study by Goddard and Mathis (1997), who manipulated the length of L. megalotis opercular tabs. Females spend more time near males with longer opercular tabs (Figure 2.2), indicating that tabs are used for selecting among conspecific males. It appears likely that this same sexual selection plays a role in species recognition, judging by an experiment in which Childers (1967) stocked two ponds with male L. microlophus and female L. macrochirus. In one pond, the males’ red opercular tabs were left intact and no hybrid fry were found later that year. In contrast, the males’ tabs were clipped in the second pond. In the absence of this visual signal, the females were willing to mate with the males of the other species, producing thousands of hybrid fry. This unreplicated experiment is still the only study to directly test whether a visual signal permits species recognition in centrarchids. Unfortunately, Childers’ experiment did not separate out the role of the tab shape from the effect of the red spot that gives L. microlophus its common name, red-ear sunfish. As far as we are aware, there have been no rigorous studies of the role of color in mate choice and reproductive isolation in centrarchids. Goddard and Mathis (1997) cited Noble (1934) as showing that “sunfishes . . . use characters such as behavior or color patterns in sex recognition,” but the cited paper provides anecdotes suggesting quite the contrary. Live females, formalin-preserved females, painted plasticine models, and leaves of approximately the same shape had the same effect. “All these objects induced the circling, butting and gentle biting characteristic of courtship” (Noble 1934, pg 153). Given the bright colors and distinctive differences among Lepomis species, it is difficult to imagine color has no impact on mate choice. Investigating color preferences (and sensory bias) in centrarchids is likely to be a highly profitable direction for future research. Species also differ in the sequence and execution of courtship behaviors. Sunfish courtship generally follows a roughly similar sequence of events (Clark et al . 1984): courtship is initiated by a female approaching a male’s nest, the male

Hybridization and speciation in centrarchids

Experiment A

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Male opercular tab length Figure 2.2 Female longear sunfish (L. megalotis) prefer males with longer opercular flaps. Females were presented with a choice between two males: artificially shortened flap versus normal flap (experiment A) or normal flap versus artificially extended flap (experiment B). Preference is measured by comparing the amount of time the female spends near each male or the number of displays to each male. (Adapted from Figure 3 of Goddard and Mathis (1997); Publisher of Ethology, Ecology & Evolution.)

leaves the nest to approach her, and she either avoids him or enters the nest. If she avoids the male, he may pursue her, returning to his nest either alone or with the female. Once in the nest, the female becomes stationary while the male circles her. Ultimately both fish circle, leading to the female tilting to present her genital opening to the male at which point spawning occurs. Quantitative comparisons of this basic sequence between L. macrochirus and L. gibbosus found important differences between the species (Ballantyne and Colgan 1978; Clark et al . 1984). L. gibbosus has a broader repertoire of actions that precedes circling. These sequences are fairly flexible, reflecting a signal–response interaction between the male and female, rather than an inflexible ritual. The species differed in their response to certain signals in the courtship sequence. Hybrids adopt some courtship sequences from each parent, producing a distinctive sequence that reduces the likelihood of backcrossing with either parent (Clark et al . 1984). This intermediate behavior in hybrids indicates that courtship sequences are at least partially heritable and able to evolve. Steele and Keenleyside (1971) tested the preference of both male and female L. gibbosus and L. megalotis for conspecific mates, and found that female L. gibbosus preferred gibbosus males even in the absence of visual cues. This is most likely a response to auditory cues: hydrophones placed near sunfish nests recorded grunts and popping sounds during mating (Figure 2.3a). The mechanical basis of these sounds is not well studied, but may result from oral (Gerald

46

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(a) B

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Figure 2.3 (a) Courtship sounds of Lepomis megalotis. The sonograph (top) displays frequency as a function of time, while the oscilloscope trace displays amplitude by time. (b) Lepomis species have distinctive courtship calls, as shown by differences in duration and pulse frequency for L. cyanellus, L. humilis, L. macrochirus, L. microlophus, L. megalotis, and L. punctulatus. Boxes represent two standard errors around the species mean. (From Figures 1 and 9 of Gerald (1971). Blackwell Publishing (1971) 25:75–87 [email protected].)

1971) or pharyngeal jaw movement (Ballantyne and Colgan 1978). These sounds accompany changes in behavior during courtship (Ballantyne and Colgan 1978) and differ among species based on pulse rates, timing, and duration (Figure 2.3b). Playback experiments to nesting males produced immediate aggressive responses, while a control playback of Grofe’s Grand Canyon Suite did not (Gerald 1971). Fish were more likely to respond to the call recorded from their own species, judging by disproportionate capture of conspecifics during playbacks to wild fish.

2.3.2.2 Breakdown of premating barriers The premating barriers discussed above can be very effective in preventing hybridization and introgression between the species. Despite these barriers, some pairs of centrarchid species do hybridize in laboratory trials and/or in nature. Natural hybrids have been documented for pairs of species that have been separated for up to about 15.5 million years (my) of independent evolution, such as L. gibbosus × L. macrochirus (Lagler and Steinmetz 1957) and L. gibbosus ×

Hybridization and speciation in centrarchids

47

L. cyanellus (Dawley 1987). Spawning can even occur between different genera, such as female Archoplites interruptus and male Ambloplites rupestris (Bolnick and Miller 2006). Incomplete premating isolation may be attributed to any of the following factors: (1) Habitat or behavioral isolation may never have been complete between the species, particularly if they have never been sympatric. Entirely allopatric species are never subject to reinforcement —natural selection favoring individuals that can recognize and avoid mating with the other species (Coyne and Orr 1998). This may explain the high rate of hybridization rate that has followed after the introduction of a species outside its native range (see Section 2.5). It may not be coincidental that the most divergent pair of centrarchid species known to voluntarily spawn (Archoplites and A. rupestris) does not occur in sympatry (Bolnick and Miller 2006). (2) Previously strong premating isolation may be diminished by environmental changes (Hubbs 1955). Both habitat and ethological isolation depend on the abiotic environment. When co-occurring species prefer different spawning locations, habitat disturbance may eliminate or degrade habitats, forcing them to nest together. When the species are isolated by visual, auditory, or olfactory cues, hybridization may result if environmental changes reduce their ability to transmit the relevant signals. The most obvious example of this is turbidity due to erosion or eutrophication, which reduces visibility in general and transmission of certain wavelengths in light, in particular, reducing the species’ ability to identify conspecific mates (Seehausen et al . 1997). Hubbs’ (1955) statement that centrarchid hybrids are more common in turbid habitats is widely cited, but this anecdotal observation has not been supported by the few rigorous tests. Travnichek et al . (1996) found no correlation between turbidity (secchi depth) and the frequency of hybrid Pomoxis in a survey of 10 lakes (see also Dallimer 1992). Olfactory and acoustic signals may be more reliable, but there is no data on how their transmission depends on environmental factors. (3) Fish may be unable to exercise their preferences. At high-population densities, both males and females may be unable to evaluate a candidate mate long enough to reach a conclusion. It has been suggested, for instance, that at high density males spend so much time defending their nest that they cannot execute a complete courting sequence, eliminating an important criterion for mate choice (Hubbs 1955). Alternative mating tactics might also bypass the normal process of mate evaluation. If sneaker males (Gross and Charnov 1980) do not discriminate among species effectively, they may steal fertilizations without giving the female an opportunity to determine that mate’s species identity. Jennings and Philipp (2002) observed sneaker male L. microlophus intruding into the nests of adjacent L. megalotis males to try to fertilize eggs. (4) Finally, species may hybridize despite complete information about their potential mate, if no alternatives are available. Laboratory studies of premating isolation can either be “choice” or “no-choice” experiments. In the former, a female (or male) is presented with two or more potential mates of different species, allowing the researcher to evaluate her (or his) preferences. In the latter, the female is presented with a single potential mate in an all-or-nothing test. In many cases, a fish with a strong preference for its own species, when given a choice, may nonetheless spawn with another species when no conspecifics are available (Childers 1967). While no-choice experiments may underestimate the strength of premating isolation under normal conditions, they may accurately reflect the natural situations in which one species is quite rare. A survey of hybrid Lepomis in Georgia has found that hybrids tend to occur when one of the parental species is rare and that rare species tends to be the female parent (Avise and Saunders 1984). This suggests that females may accept heterospecific males if no more appropriate males are available. In contrast, Pomoxis frequently hybridize even when both parental species are abundant (Travnichek et al . 1996).

2.3.3 Postmating reproductive isolation in centrarchids Premating isolation is an important and often effective barrier to hybridization. However, because mate choice depends on environmental conditions, premating isolation can be weakened or eliminated by environmental changes, as described above. Speciation by habitat or mating differences alone is thus a tenuous and potentially reversible process. When premating barriers fail, species will spawn and may produce hybrids. If these hybrids are viable and fertile, they may

48

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in turn mate with other hybrids or the parental species to create F2 and backcross hybrids. Successive generations of backcrossing can eliminate the genetic differences between the species, leading to the loss of one or both parental types, a process known as introgression. While premating barriers may be unreliable in the face of environmental change, postmating isolation can ensure irreversible divergence between emerging species. Introgression can be blocked if the two species’ gametes fail to fuse (gametic incompatibility), if the resulting hybrids are inviable, or if the surviving adult hybrids are sterile or otherwise unable to produce viable and fertile backcross or F2 progeny (postzygotic isolation).

2.3.3.1 Gametic incompatibility Mating between species does not guarantee hybrid embryos, as the species’ gametes may fail to fuse. Indeed, gametic incompatibility is a major form of reproductive isolation in some species, such as broadcast spawning in marine invertebrates (Palumbi 1999). The protein receptors involved in gamete binding and recognition are known to evolve rapidly in some species because sperm competition favors more efficient fertilization mechanisms, while eggs must evolve defenses to avoid fatal multiple fertilizations (Palumbi 1999). The resulting coevolution of interacting proteins is highly conducive to Dobzhansky–M¨uller incompatibilities, so one might expect that gametic incompatibilities would play a major role in postmating isolation. Gametic incompatibility has been tested in centrarchids through artificial fertilization experiments in which eggs and sperm are stripped from adult fish and mixed in the laboratory. Fertilization rates are measured by counting the proportion of eggs that have undergone cleavage into the two- or four-cell stage; such data have been reported for both interspecific (Smitherman and Hester 1962) and intergeneric (West and Hester 1966; Merriner 1971) crosses in centrarchids. Unfortunately, the high variance of success in artificial fertilization experiments can make these data difficult to interpret. For instance, fertilization rates ranged from 36 to 98% for 12 replicate crosses of Pomoxis * Micropterus (Merriner 1971). Although the lower end of this range might indicate gametic incompatibility, it may also reflect immature gametes or poor rearing conditions. The latter explanation is more likely, as the same study found that even within species Pomoxis crosses had variable fertilization rates (48.6–96.1%). Taking these control crosses into account, it appears that gametic incompatibility plays a minor role in reproductive isolation even among long diverged species. For instance, Lepomis gulosus has average fertilization rates of 89.3% in crosses with Micropterus, 87.7% with Pomoxis, and 85.3% with L. macrochirus, compared to an intraspecific control of 86.4% fertilization (Merriner 1971). Fertility of >90% is possible for all combinations of Pomoxis, Micropterus, and Lepomis that have been attempted (Merriner 1971). Similarly, Parker et al . (1985a) found that fertilization rates do not decline as one moved from closely to distantly related pairs of centrarchid species. Other studies have found much lower fertilization rates for similar crosses (Smitherman and Hester 1962; West and Hester 1966), but did not carry out such extensive replication. Although further tests would be helpful, we feel confident that gametic incompatibility plays a fairly minor role in reproductive isolation in centrarchids. Consequently, low hatching success of eggs from artificial fertilization experiments can be attributed to hybrid inviability.

2.3.3.2 Hybrid inviability It has long been known that hybrid viability reflects the evolutionary relationship of the two parent species. Charles Darwin (1859) commented on this relationship, though he noted that the rule is not always reliable. Later workers simply assumed that hybrid viability declines with divergence, and used hybridization success to determine membership in Linnean taxonomic ranks (Hubbs and Drewry 1959) and phylogenetic relationships (West and Hester 1966; Hester 1970; Tyus 1973). Unfortunately, this approach can yield misleading results if hybrid viability is not a perfect measure of evolutionary divergence. For instance, the warmouth (L. gulosus, formerly Chaenobryttus) yields more viable hybrids when crossed with Micropterus than with other Lepomis species (Hester 1970), despite strong evidence of the warmouth’s closer relationship to the latter (Near et al . 2004). Recently, evolutionary biologists have begun to use molecular phylogenetic data to rigorously test the relationship between reproductive isolation and evolutionary distance. This trend is often attributed to Coyne and Orr (1989), who showed that reproductive isolation among fruit fly species (Drosophila) increases with allozyme divergence. In fact, similar analyses had already been carried out in centrarchids (Parker et al . 1985a,b), albeit without some of the statistical

Hybridization and speciation in centrarchids

49

innovations introduced by Coyne and Orr. Equivalent studies have since been done for birds, frogs, butterflies, and plants, all finding similar patterns: reproductive isolation increases with divergence (Sasa et al . 1998; Presgraves 2002; Price and Bouvier 2002; Tubaro and Lijtmaer 2002; Lijtmaer et al . 2003; Mendelson 2003; Russell 2003; Moyle et al . 2004). This phenomenon has been dubbed a “speciation clock” (Coyne and Orr 1998), although this is not strictly accurate as many of these studies only examine postmating isolation, not total reproductive isolation. A recent paper by Bolnick and Near (2005) combined all available data on centrarchid hybrid viability to estimate the rate at which hybrid viability is lost with time. What set this study apart from previous papers is its use of a carefully fossil-calibrated, multigene phylogeny to measure evolutionary distance in units of time (millions of years—my; Near et al . 2005). In addition to providing the most precise estimate yet available for the rate of a speciation clock, this study led to several novel insights into the evolution of reproductive isolation. The remainder of this section reviews these findings to illustrate the kinds of general insights into speciation that can be gained through the study of centrarchid hybrids. The central result from Bolnick and Near (2005) was a regression analysis showing that hybrid viability declined linearly with the length of evolutionary time separating the parental species, at an average rate of 3.13% per my (Figure 2.4). This result was based on 130 published measurements of the hatching success of hybrid embryos from 37 pairs of centrarchid species (Smitherman and Hester 1962; West and Hester 1966; Childers 1967; Hester 1970; Merriner 1971; Tyus 1973; Philipp et al . 1983a; Philipp et al . 1983b; Parker et al . 1985a; Parker et al . 1985b; Philipp et al . 1985; Epifanio and Phillip 1994). Although larval viability data is more limited, similar analyses show that it evolves at the same rate as embryonic viability (Figure 2.5). While it is not surprising that hybrid viability declines as one moves from closely to distantly related species, this study was the first to measure the rate of this decline in units of time. More importantly, details of the rate, curvature, and scatter of this decline can shed light on the mechanisms driving the speciation. Five main insights emerged from the Bolnick and Near (2005) study. (1) Hybrid inviability is the result of many Dobzhansky–M¨uller incompatibilities of small effect. A handful of studies have identified individual genes that cause almost complete inviability in hybrids between Drosophila species (Ting et al . 1998; Barbash et al . 2003), leading some workers to posit that speciation is usually the result of one or a few Dobzhansky–M¨uller incompatibilities of large effect (Wu 2001). However, if this were the case, hybrids would be either largely viable or largely inviable. As different species pairs would make the transition between these states at different points in time, we would expect a weak correlation between hybrid inviability and divergence time. In contrast, centrarchids exhibit the tightest age–viability correlation yet documented (r = −0.85, p < 0.001). As inviability declines gradually and continuously, we can conclude that it reflects the cumulative effect of many small genetic incompatibilities.

Hybrid hatching success

120 100 80 60 40 20 0

0 10 20 30 40 Divergence between parent species (my)

Figure 2.4 The viability of hybrids declines gradually with the length of time separating the parents (p < 0.001, r 2 = 0.73). Viability is measured as the percentage of hybrid embryos that hatch, divided by the hatching rate for a within-species cross (controlling for egg viability). Divergence time is estimated from a molecular clock analysis of seven genes, calibrated with six fossils. Viabilities are averaged for all hybrid crosses for a particular divergence time, using independent contrasts to account for phylogenetic nonindependence. (Adapted from Bolnick et al ., 2008.)

Centrarchid fishes

Percentage of hybrid larvae with morphological deformities

50

80 60 40 20 0

0

10 20 30 40 Time since divergence (my)

Figure 2.5 The percentage of larvae showing visible morphological deformities increases with the divergence time separating the parent species (p = 0.047, r 2 = 0.78). Deformity frequencies are averaged for a given node in the phylogeny to account for phylogenetic nonindependence. (From Bolnick et al ., 2008.)

(2) There is a lag phase between the start of genetic divergence and when inviability begins to accrue. The linear regression in Figure 2.4 seems to predict that hybrids of species pairs with close to zero genetic divergence would have close to 120% viability—clearly a biologically spurious result. This occurs because on average, hybrid viability does not drop below 100% until the parental species have diverged for over 6 my. Hence, there is a significant delay between the start of genetic divergence between populations, and the point at which this divergence results in reduced viability. It is currently unknown whether this corresponds to a “snowball effect” in which inviability accumulates at an accelerating rate (Orr and Turelli 2001), or the temporary effects of outbreeding benefit compensating for any early loss of viability. The high incidence of heterosis in hybrids of young species argues for the latter effect. For instance, Lepomis auritus * L. macrochirus hybrids experience 20% higher hatching success than within-species crosses. (3) Speciation is driven largely by prezygotic isolation. On average, sister species in centrarchids are separated by only 4.3 my. The average time between speciation events is at most 4.66 my, shorter if we assume some past speciation events went unrecorded because one of the resulting species went extinct. Clearly, the interval between speciation events is much shorter than the time required to accumulate any hybrid inviability (or infertility, judging by what limited data exist). By process of elimination, we are forced to conclude that premating isolation plays the leading role in speciation in centrarchids. (4) Ecological divergence promotes the accumulation of genetic incompatibilities. Deviations above (or below) the regression line in Figure 2.4 represent instances of slower- (or faster-) than average loss of hybrid viability. Factors that are correlated with this residual variation may be processes that speed up or slow down the evolution of reproductive isolation (Fitzpatrick 2002). In centrarchids, body size disparity is correlated with hybrid inviability (Bolnick et al . 2006). Statistically controlling for the confounding effect of divergence time, species with greater size disparity produced less viable hybrids (Figure 2.6). As body size disparity is associated with ecological divergence and dietary differences among species, it appears likely that the natural selection for ecological divergence facilitates the evolution of reproductive isolation. This is not unexpected, as selection can speed up the rate of genetic substitutions, increasing the chances of accruing Dobzhansky–M¨uller incompatibilities. (5) Centrarchids lose hybrid viability slowly relative to other taxa. One of the long-term goals of this type of “speciation clock” study is to be able to compare the rate at which different taxonomic groups accrue reproductive isolation and explain any variation among groups. This study remains out of reach, because the various studies have used different measures of viability and of divergence. However, using certain benchmarks, we can conclude that centrarchids retain the ability to hybridize far longer than other groups studied to date. The minimum age for total hybrid inviability is 1.5 my in anurans (Sasa et al . 1998), 2 my in Drosophila (Coyne and Orr 1998), 4 my in Lepidoptera (Presgraves 2002), 5.5 my in birds (Price and Bouvier 2002; Lijtmaer et al . 2003), and 25.25 my in centrarchids (Bolnick and Near, unpublished data). This earliest instance of zero compatibility is only for one direction of crosses between L. microlophus × M. salmoides

Hybridization and speciation in centrarchids

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Residuals of hybrid viability

30 20 10 0 −10 −20 −30 −40

−2 −1 0 1 2 Residuals of body size disparity

Figure 2.6 Body size differences promote reproductive isolation between centrarchid species. As species diverge with time, they produce less viable hybrids and they diverge more in body size. Consequently, one must remove the confounding effect of divergence time in order to test whether the body size differences affect the hybrid viability. This can be done by taking the residuals of size differences (or hybrid viability) regressed against divergence time. Applying this approach to centrarchids, there is a significant relationship between the residuals (P = 0.026), indicating that the body size differences are correlated with greater hybrid inviability. (From Bolnick et al . 2006.)

(the reciprocal cross has 43% compatibility). Only three crosses (M. salmoides * A. rupestrus or either Pomoxis) yield completely inviable hybrid embryos in either direction, while 10 other crosses of the same age (28.94 my) are partially viable. Considering a different benchmark, the maximum age for heterosis is thought to be 0.5 to 1.4 my (mammals), 0.05 my (birds), 6.7 to 9.5 my (amphibians), 3 to 4.3 my (insects), or 8.3 my (crustaceans) (Edmands 2002). In contrast, heterosis has been recorded in centrarchids for a number of crosses between the taxa diverged for 12.21 my and even 13.68 my. This slower evolution of reproductive isolation is also reflected in the overall diversification rate: centrarchids have the second slowest rate of any clade of vertebrates yet investigated (after Ictalurus catfish, Bolnick and Near 2005). Why do centrarchids accrue postzygotic isolation so slowly? We can only speculate at this point, but would propose that the lack of distinct sex chromosomes in centrarchids (Roberts 1964) might contribute to this. Both theoretical work (Orr and Turelli 2001) and comparative studies in Drosophila (Turelli and Begun 1997) suggest that the species with larger X chromosomes evolve inviability faster. This is because most Dobzhansky–M¨uller incompatibilities will be recessive and only expressed when they involve a gene on a sex chromosome (see Section 2.3.3.2; Box 2.3). The larger the sex chromosome is the greater are the opportunities for gene–gene incompatibilies. As sex chromosomes are either small or absent in centrarchids, only the much rarer dominant Dobzhansky–M¨uller incompatibilities will contribute inviability, slowing the rate of reproductive isolation. The minimal size of the sex-determining region in sunfish was confirmed by a study of amplified fragment length polymorphism (AFLP) segregation in a laboratory cross of L. cyanellus, in which only 1 out of over 500 polymorphic makers was diagnostic for sex (Lopez-Fernandez and Bolnick, 2007). Interestingly, the three vertebrate clades with the slowest diversification rates all lack distinct sex chromosomes (Coyne and Orr 2004; Bolnick and Near 2005).

Box 2.3

Summary of Haldane’s rule and relevance to hybridization

Haldane’s rule states that “when in the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous [heterogametic] sex” (Haldane 1922). This generalization has been called “the most tantalizing regularity in animal speciation” (Turelli 1998), holding for 99% of the documented cases of sex-specific hybrid sterility and 90% of cases of sex-specific inviability (Laurie 1997; Barbash et al . 2003). The most general of explanation for this pattern is the “dominance theory” (Laurie 1997; Barraclough and Vogler 2000; Coyne and Orr 2004).

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Box 2.2 described how hybrids AaBb may have low viability if the derived alleles a and b fail to interact correctly. However, this assumes that the deleterious interaction between a and b is dominant. As recessive incompatibilities seem far more likely (Orr and Turelli 1996), the Dobzhansky–M¨uller incompatibilities described in Box 2.1 are likely to be rare, and accumulate slowly. However, now imagine a case where one of the genes is sex-linked (e.g., on the X chromosome of an XY male/XX female system). In this case recessive Dobzhansky–M¨uller incompatibilities will be covered by the functional dominant alleles in females (XA Xa Bb). In hemizygous males (YXa Bb) the deleterious interaction will be fully expressed, leading to sterility or inviability. Note that the larger the hemizygous chromosome is, the more genes it contains that might yield incompatibilities (Turelli and Begun 1997; Orr and Turelli 2001).

2.3.3.3 Genetic and developmental basis of hybrid dysfunction The preceding section discussed the patterns of hybrid inviability in depth, but was unclear as to the exact mechanisms causing that inviability. In fact, we do have some clues as to the nature of Dobzhansky–M¨uller incompatibilities in centrarchids. Hybrid inviability appears to be linked to developmental errors resulting in visible deformities in features such as larval eyes (Micropterus*Lepomis, Parker et al . 1985a) and jaws (Whitt et al . 1977) (Figure 2.7). Such deformities accrue at the same rate as inviability, with the same lag time (Figures 2.4 and 2.5; Bolnick and Near 2005). Even in species with viable hybrids such as the three Enneacanthus, hybrids have a higher rate of asymmetries, reflecting developmental instability (Graham and Felley 1985). It is also clear that the inviability has a genetic basis: in a hybrid cross between the green and longear sunfish (L. cyanellus and L. megalotis), slightly over half the hybrids survived to larval stage. These survivors showed a high rate of segregation distortion at AFLP genetic markers, relative to a control cross (Lopez-Fernandez and Bolnick, 2007). Such segregation distortion will occur when one or both parents are heterozygous for genes causing hybrid mortality. Markers linked to hybrid-lethal alleles disappear, resulting in an excess of markers linked to nonhybrid-lethal alleles, relative to Mendelian expectations. This cross thus indicates that at least some of the inviability in hybrids has an autosomal genetic basis, and that the responsible loci are polymorphic in natural populations. The next question is how these incompatibilities might arise. One possibility is that structural genes may be incompatible if their proteins fail to interact. For instance, in vitro assays show that hybrid copepods suffer metabolic failure because cytochrome c oxidase and cytochrome c proteins from divergent parents fail to interact correctly (Rawson and Burton 2002). Alternatively, one gene’s protein may normally be used to activate the expression of a second gene. If the regulatory protein fails to recognize the regulatory domain of the target gene, the latter may be misexpressed (Orr and Presgraves 2000; Michalak and Noor 2003). There is direct evidence for gene regulation failures in hybrid centrarchids, which show aberrant expression of allozymes during development (Figure 2.8). Most often, this entails a delayed onset of gene expression, though expression may also occur early or not at all (; Whitt et al . 1977; Philipp et al . 1983b; Parker et al . 1985b). This misexpression is not because hybrids are developmentally intermediate between the parents: in many cases the parents express the gene at the same stage of development (e.g., Ck-B, Ldh-C; Philipp et al . 1983b). The implication is that the parental species have diverged in how they turn on a gene, even while they maintained similar timing for when to turn it on (Whitt et al . 1977). Presumably a diverged regulatory gene from one species fails to efficiently activate the copy of its target gene derived from the other species, which is thus not transcribed at all, or is expressed later once the transcription factor accumulates to a high enough concentration to overcome its weakened binding efficiency (Whitt et al . 1977). These allozyme studies also point to an interesting deviation from the basic Dobzhansky–M¨uller model. The standard model (Box 2.1) assumes that incompatibilities arise between two loci within the hybrid. However, eggs are packed with maternally encoded transcription factors that govern where and when embryonic genes are turned on (Davidson 2001). Genetic divergence between species may mean that these maternal transcription factors stimulate expression of the maternally derived allele, but fail to activate the paternally derived allele from another species. In other words, Dobzhansky–M¨uller incompatibilities can arise between the maternal and embryonic loci. This appears to be the case in centrarchids: the maternal and paternal alleles were often asynchronously expressed (Parker et al . 1985a,b; Epifanio and Phillip 1994). In almost all cases it is the paternal allele, which is in an unfamiliar cytoplasmic background, that is expressed late (Figure 2.9; Gpi-B, Ldh-C, Ck-A, Mdh-B) or not at all (6-Pgdh-A, Sod-A) (Philipp et al . 1983b). It should be kept

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(a)

(b)

Figure 2.7 Photographs of L. cyanellus * L. megalotis hybrids. (a) Arrow pointing to a deformed heart that resembles a known gene mutation (‘‘heartstring’’) in zebrafish. (b) Arrow pointing to the deformed spine. Photographs by H. Lopez-Fernandez.

in mind, however, that not all delays can be ascribed to cyto–nuclear interactions, as instances do exist of symmetrical delay or misexpression of the maternal allele (e.g., L. cyanellus*M. salmoides, Philipp et al . 1983). Deviations in enzyme expression (and activity) are correlated with both hybrid viability and the genetic divergence between the parental species (Figure 2.10; Whitt et al . 1972; Philipp et al . 1983a; Parker et al . 1985b). It should be kept in mind, however, that this correlation does not prove that gene expression flaws are directly responsible for hybrid inviability. Because both structural and regulatory genes diverge with time, we cannot rule out the possibility that inviability is the result of incompatibilities at unmeasured loci (structural or regulatory) that have evolved independently but at a similar rate. We have no direct information about the developmental impact of the hybrid expression patterns and no mechanistic explanation for how allozyme expression delays affect fitness. Further progress will require experiments that isolate the effect of particular sets of genes. Even in model systems with extensive genetic tools, it has proved very difficult to

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+

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18 3

44 95 144 194 242 36 70 120 120 216 Hours after hatching

Hybrid (bass*green sunfish)

+

LNB

A(L) A(L) A(L) A(B) A(G) A(G) A(L) B(L) A(L) B(G) A(G) B(L)

GSF −

B(L) B(L) B(L) B(G) B(G) B(G)

22 14

39 70 142 218 34 44 94 170 Hours after hatching

Figure 2.8 Expression profile of creatine kinase isozymes in M. salmoides and L. cyanellus embryos during ontogeny, and of M. salmoides * L. cyanellus hybrids. The x-axis is the time after hatching and the y-axis is the electrophoretic migration distance (anodes and cathodes marked with—and + signs). In the hybrid profile, the last two lanes are samples from the parental species, for comparison (M. salmoides = largemouth bass (LMB); L. cyanellus = green sunfish (GSF). Hybrids fail to express some isozymes. (Redrawn from Figure 4 of Whitt et al . (1977). Blackwell Publishing (1977) 9:97–109 [email protected].)

identify the precise genes responsible for hybrid inviability. So far, only four genes have been found with known roles in generating hybrid dysfunction (one in Xiphophorus fish, three in Drosophila flies; Malitschek et al . 1995; Ting et al . 1998; Barbash et al . 2003; Presgraves 2003; Presgraves et al . 2003). Although great progress is being made in identifying more such genes in Drosophila (Presgraves 2003), this has required the use of advanced molecular tools for deletion mapping that are unavailable in systems like centrarchids. Another form of cytoplasm–nuclear incompatibility involves interactions between the mitochondrial and nuclear genes. In a recent theoretical model, Turelli and Moyle (2007) show that if one species undergoes accelerated mitochondrial evolution, there will be more opportunities for genetic incompatibilities when that species is the maternal parent (donating mitochondria to the hybrids) than in the reciprocal cross. Under the normal Dobzhansky–M¨uller model, hybrids would have genotype AaBb regardless of which species was the maternal parent, and therefore hybrid viability should be identical for reciprocal crosses, but the mitochondrial genes do not impose this symmetry. Thus, asymmetric viabilities can be used to test for mitochondrial-nuclear incompatibilities. This prediction was recently tested using centrarchids, which show extensive asymmetries in F1 hybrid viabilities. Of the 19 pairs of centrarchid species for which reciprocal cross data are available, 17 show significant asymmetries (Bolnick and Near 2005). In 13 out of 17 cases (significantly different from

Hybridization and speciation in centrarchids

55

Mean hatching time

Micropterus

Maternal allele Micropterus* Lepomis Paternal allele

Paternal allele Lepomis *Micropterus Maternal allele

Lepomis

0

20

40

60

80

Hours after fertilization

Figure 2.9 Timing of expression of GPI-A allozyme in pure Micropterus salmoides and Lepomis cyanellus embryos and in reciprocal hybrids. Shaded bars indicate times in which GPI-A is expressed. In hybrids, maternal and paternal allele expression timing can be distinguished electrophoretically, and are shown separately with black shading for the Micropterus allele and stippling for the Lepomis allele. The paternal allele is consistently delayed in the hybrids regardless of which species is the paternal parent. (Adapted from Whitt et al . (1977). Blackwell Publishing (1977) 9:97–109 [email protected].)

Hybrid hatching success

120 100 80 60 40 20 0 1

1.2

1.4

1.6

1.8

2

Degree of disturbance to enzymatic expression

Figure 2.10 Hybrid hatching success declines as enzyme expression is increasingly disturbed (correlation = −0.954, p < 0.05). Hybrid hatching success is relative to intraspecific controls and the enzyme expression disturbance is measured as described in Parker et al . (1985). Two caveats must be noted. First, this regression is not statistically robust: the points are not statistically independent due to phylogenetic history. Second, both variables increase with divergence time, so at least some of this correlation is a result of mutual correlation with a third variable. (Drawn from tabular data in Figure 3 of Parker et al . (1985a). Wiley (1985) 233: 451–466 [email protected].)

56

Centrarchid fishes

50%, P = 0.048), the maternal parent for the worse cross direction had higher rates of mitochondrial evolution (Bolnick et al . 2008). This provides correlative evidence that mitochondrial-nuclear incompatibilities make a significant contribution to the evolution of reproductive isolation in centrarchids.

2.3.3.4 Hybrid sterility Hybridization will only cause introgression between the parent species if the hybrids (and F2s and backcrosses) are both viable and fertile. In fact, there are many instances of centrarchid hybrids that are viable but partially or fully infertile. For instance, 99% of L. macrochirus × L. cyanellus hybrids are viable (range: 79–140% of the control cross rate; Bolnick and Near 2005). Despite this high viability, backcrosses are limited due to a biased sex ratio: 68 to 97% of the hybrids are male (Childers 1967). These males have low fertility due to a high frequency of unreduced sperm (Wills and Sheehan 2000). Consequently, the preceding discussion of hybrid viability represents an underestimate of the total postmating isolation between species. Unfortunately, there are not enough data on hybrid fertility to conduct an analogous study of the rate at which fertility is lost. What data that do exist suggest that most intrageneric hybrids are partially or fully fertile, while intergeneric hybrids are infertile. L. microlophus and L. cyanellus have diverged for approximately 14.6 my, but their hybrids are fertile and produce viable F2 progeny (Childers and Bennett 1961), as is also the case for L. gulosus*L.macrochirus (West 1970). P. annularis and P. nigromaculatus (12.0 my) have fertile F1, F2, and F3 hybrids, though fertility declines beyond the F1 generation (Hooe and Buck 1991). There do not appear to be any cases of fertile hybrids between species more than 14.6 my apart. Hybrid infertility may result from genetic incompatibilities that disrupt gonadal development. For example, L. gulosus × M. salmoides hybrids (25.25 my) fail to develop mature gonads (West 1970). Males possess small nodes of connective tissue in place of testes, and females produce few (<2%) mature oocytes (West 1970). L. gulosus *L. macrochirus males have testes ranging from “mere strands of tissue” to fully normal testes with functional spermatozoa (Birdsong and Yerger 1967). Alternatively, reduced gonad function can be due to meiotic problems. L. macrochirus × L. cyanellus hybrids (13.11 my) have intact gonads but are only semifertile due to a low frequency of unreduced 2N gametes (12%), and L. gibbosus × L. cyanellus (14.63 my) hybrids produce a small number of mostly deformed sperms (Dawley et al . 1985). Crosses of L. gulosus*M. salmoides showed abnormal meiosis 1, in which chromosomes lined up on the metaphase plate but did not migrate along the spindle, resulting in chromatin stretched among daughter cells, fragmentation of chromosomes, or unequal distribution of chromosomes among daughter cells (West 1970). These failures might reflect karyotypic differences: both M. salmoides and L. cyanellus have 46 chromosomes, compared to the usual 48 in most other centrarchids (Roberts 1964). A promising test of this hypothesis would be to compare the fertility of crosses between L. cyanellus and another Lepomis, using both 2N = 48 and 2N = 46 strains of cyanellus. Even when hybrids are fully fertile, introgression may be limited. As discussed in the section on premating isolation, hybrids may show aberrant courting behavior that reduces their ability to mate (Clark and Keenleyside 1967). When they do manage to mate, the resulting F2 or backcross progeny may themselves be inviable or infertile. L. macrochirus * L. gulosus hybrids are viable and mostly fertile, but F2 hybrids and backcrosses to macrochirus and gulosus have viabilities of only 1.1, 6.5, and 2.4%, respectively (West 1970). One explanation for this loss of viability in second-generation hybrids is chromosomal nondisjunction in the F1 hybrids. This was clearly demonstrated in a study of backcrosses from hybrid L. gibbosus and L. cyanellus. The hybrid females produce nearly 100% triploid backcross progeny with two copies of the maternal genome, because the female F1 hybrids fail to reduce oocyte ploidy during meiosis (Dawley et al . 1985). The resulting triploid progeny are viable but largely sterile, with clear milt from males. Female triploid F2s were partially fertile, but produced inviable and morphologically abnormal progeny with fragmented chromosomes (Dawley et al . 1985). So while a natural population of L. gibbosus and L. cyanellus hybrids had abundant F1s and some F2s or backcrosses, introgression did not occur between the parental species.

2.3.3.5 Hybrid sex ratios Many interspecific crosses among centrarchids yield strongly male-biased sex ratios. The lack of female hybrids can also contribute to reproductive isolation by eliminating any ability to produce F2s or certain backcrosses. There is a

Hybridization and speciation in centrarchids

57

Table 2.2 Sex ratios of hybrid crosses. The average percent male is calculated across all available published estimates. Dam

Sire

Average % male

References

L. cyanellus

L. macrochirus

97

Childers (1967)

L. macrochirus

L. cyanellus

68

Childers (1967)

L. gulosus

L. macrochirus

69

Childers (1967)

L. cyanellus

L. gulosus

84

Childers (1967)

L. gulosus

L. cyanellus

16

Childers (1967)

P. annularis

P. nigromaculatus

50

Epifanio and Philipp (2001)

L. cyanellus

L. microlophus

69

Childers (1967)

L. microlophus

L. cyanellus

48

Childers (1967)

L. gulosus

L. microlophus

55

Childers (1967)

L. macrochirus

L. microlophus

97

Childers (1967)

L. microlophus

L. macrochirus

97

Childers (1967)

significant deviation from the expected 50:50 ratio in 26 out of 30 crosses for which published sex ratio data are available (Table 2.2). In all but one case, these biases favor male hybrids (68–100% of hybrids, depending on the cross). The one counterexample is a cross of L. cyanellus*L. gulosus, yielding 16% males, though the reciprocal cross produced 84% males (Childers 1967). This case is aberrant enough that there is some question as to its reliability, particularly given the odd coincidence that the reciprocal sex ratios add to 100% (might the former ratio have been accidentally inverted?). Haldane’s Rule (Box 2.2) has been invoked to explain this consistent male bias in centrarchid hybrids. If females are the heterogametic sex (e.g., XY, whereas males are XX), then Haldane’s Rule predicts females to be sterile or inviable, the latter possibility resulting in a biased sex ratio (Krumholz 1950; Birdsong and Yerger 1967; Childers 1967). However, if the sex ratio bias arose from female inviability, any excess of males must be accompanied by a loss of hybrid survival. This does not seem to occur: viability remains high (∼100%) even when sex ratios are strongly biased. Therefore, the sex ratio bias is not due to lower female viability as required by Haldane’s Rule, which is not surprising given the lack of distinct sex chromosomes in centrarchids (Roberts 1964). Although there is some indication that males may be the heterogametic sex in centrarchids (Gomelsky et al . 2002), the sex-specific chromosomal region may be restricted to a few hundred kilobases or fewer of male-specific sequence as in some other fish species (Kondo et al . 2003; Lopez-Fernandez and Bolnick 2007). Such small sex-specific regions are probably insufficient to cause an appreciable sex bias, because males will be hemizygous for very few loci, limiting the possible number of Dobzhansky–M¨uller incompatibilities involving hemizygous genes (Turelli and Begun 1997; Orr and Turelli 2001). As Haldane’s Rule is thought to be a major cause of postzygotic isolation in many taxa, its absence in centrarchids might help explain their relatively slow evolution of reproductive isolation. If Haldane’s Rule cannot explain the sex ratio bias, what can? One hypothesis is that these male-biased populations are composed actually of genetically male and female individuals, but genetic female hybrids fail to develop normally, and appear as phenotypic males as a developmental default. This could happen if there is a Dobzhansky–M¨uller incompatibility affecting sex determination; for instance, if transcription factors that normally initiate female-specific gene expression during development fail to operate suitably in hybrids.

2.3.3.6 Ecologically dependent postmating isolation The preceding discussion of postmating reproductive isolation was largely concerned with “intrinsic” inviability or sterility arising solely from genetic incompatibilities. It is also possible for hybrid dysfunction to be variable depending on environmental conditions. Perhaps the most prominent example of this effect is in hybrids between the benthic and limnetic species of sticklebacks (Gasterosteus aculeatus spp). These hybrids are fully viable and fertile in laboratory conditions, but are unable to compete or find mates when placed in more natural settings (Hatfield and Schluter 1999).

58

Centrarchid fishes

This ecologically dependent (“extrinsic”) reproductive isolation has received little attention in centrarchids, where hybrid viability is almost always measured in the laboratory or in artificial ponds. What little evidence is available suggests that hybrids are highly competitive in stocked ponds, often growing faster than pure-species individuals (Hubbs and Hubbs 1931; Hooe and Buck 1991). For instance, L. microlophus*L. cyanellus hybrids grow faster than their reciprocal, and both hybrids outgrow either parent (Pasdar et al . 1984b). This heterosis may be environmentally dependent as there was little difference in hybrid and parental growth rates at low density, but a larger difference when competition was strong (Childers and Bennett 1961). Wheat et al . (1974) conducted one of the few studies of hybrid growth in natural environments. Backcrosses of M. salmoides*M. dolomieu hybrids with M. salmoides had lower survival than pure-species fry in natural ponds. In contrast, the backcrosses had higher survival in artificial ponds, where cannibalism was the main source of mortality. This appears to have occurred because the backcrosses grew faster than the pure species and so were the cannibals rather than the cannibalized. Further analysis of environmental dependence of hybrid viability, growth, competitiveness, predation risk, and mating success may prove very rewarding.

2.3.4 Speciation summary Studies of natural and artificial hybrids provide a vital tool for understanding speciation. Centrarchids are an exceptionally promising system for such studies, with their widespread hybridization, the ability to create artificial hybrids, and extensive variation in all these components of reproductive isolation. Although there is still much work to be done on this topic, several important conclusions are possible. First, it is clear that speciation in centrarchids is primarily a result of premating isolation. Judging by the divergence times discussed in Chapter 1, the waiting time for a newly arisen species to split by itself into daughter species is about 4.66 my. This is much shorter than the lag phase before hybrid inviability and infertility begin to accrue, indicating that postmating isolation is relatively unimportant in initiating speciation. However, premating isolation can break down under environmental change, so inviability and infertility play a vital role in buttressing the reproductive isolation of young species pairs. Postmating isolation evolves slowly, perhaps due to the lack of large hemizygous sex chromosomes, and mostly seems to reflect the cumulative action of many genetic incompatibilities of small effect (Bolnick and Near 2005), at least some of which involve cytoplasmic–nuclear incompatibilities (Whitt et al . 1977). These insights from centrarchids have been a significant contribution to our general knowledge of how new species arise.

2.4 Applied value of hybrids Understanding the evolutionary and genetic basis of reproductive isolation may ultimately have practical benefits. The patterns of hybrid viability and fertility described above will allow us to predict the outcomes of other crosses and identify new hybrid combinations that are likely to be successful and/or have desirable traits. This will have benefits for both genetic research and aquaculture.

2.4.1 Hybrids as tools for genetic analyses A century and a half after Mendel’s pioneering work on peas, the ability to make crosses between two genetic strains remains one of the most important tools in genetics. When faced with two phenotypically distinct strains (be they family groups, populations, or species), geneticists often want to identify the gene(s) that cause these differences, the dominance, pleiotropic and epistatic effects of those genes, genetic covariances between traits, and linkages between different genetic loci. Simply sequencing genes from the two strains is insufficient as they will almost always differ at many loci, making it impossible to identify the exact gene responsible for phenotypic differences. Answering such questions requires crosses to make F1 and F2 progeny. This is not a problem for studies of intraspecific variation, but has long posed a major challenge

Hybridization and speciation in centrarchids

59

for geneticists interested in understanding the genetic basis of differences between species. As fully divergent species are reproductively isolated, one cannot carry out a genetic analysis of their differences. Groups like centrarchids, which retain hybrid viability and fertility for millions of years, provide an exceptionally promising system for understanding what genetic changes make species different—behaviorally, ecologically, morphologically, and physiologically. So far there has been relatively little work done on the genetics of species differences in centrarchids. A number of studies have compared morphological or physiological traits of hybrids and their parents, but no formal quantitative genetics were applied to estimate dominance effects, number of loci, or other genetic parameters. Body condition index and growth rates of hybrid M. salmoides * M. floridanus resembled more closely the maternal parent (Maceina and Murphy 1988; Philipp 1991; Philipp and Whitt 1991), suggesting partially dominant inheritance of these traits. A number of other traits showed additive inheritance, indicated by phenotypically intermediate hybrids. Studies of enzyme activities showed that L. cyanellus * L. microlophus hybrids were intermediate between their parents (Pasdar et al . 1984b), as were most morphological traits in hybrids between L. gibbosus and L. macrochirus (Colgan et al . 1976). There is significant heterosis in both growth and viability in many hybrids between younger species pairs (Bolnick and Near In review; Hubbs 1955). The genetic basis of this is unknown, but might reflect an outbreeding benefit from increased heterozygosity covering a background genetic load of recessive deleterious alleles in the parental species. Centrarchids are a promising, but nearly untapped, resource for quantitative genetic analysis of species differences. The development of a linkage map of genetic markers for quantitative trait locus (QTL) analysis would be particularly useful, and knowledge of reproductive isolation patterns is necessary to guide the choice of species to use in developing these markers. Another promising avenue is the application of gene expression arrays to understand between-species differences, though the level of genetic divergence among centrarchids may limit cross-species comparisons of these arrays. One area where the genetic potential of hybrid centrarchids has been exploited is linkage analysis. In the 1970s and 1980s, there was an active group of researchers studying linkage between enzyme loci in Pomoxis (Epifanio and Phillip 1993) and Lepomis (Wheat et al . 1973; Whitt et al . 1976; Pasdar et al . 1984b). This research group identified a couple of sets of linked enzyme loci (e.g., G2dh, Pgk, and Sod in Lepomis (Pasdar et al . 1984c); 6 pgdh and α-Gpdh (Wheat et al . 1973)), but not enough data was collected to allow rigorous conclusions about linkage group conservation within centrarchidae or across fish families. This research program fell by the wayside, however, with the advent of more advanced genetic tools.

2.4.2 Hybrids in aquaculture Data on reproductive isolation and the genetics of species differences will, in turn, have economic applications. Centrarchids are popular among sport fishermen, who often want to stock centrarchids in both natural and man-made water bodies. The demand for fish for stocking in turn creates a market for hatchery-raised fish. As of 2000, there were approximately 485 commercial hatcheries producing Lepomis in the United States, with an emphasis on L. macrochirus and L. microlophus (Morris and Mischke 2000). Micropterus and Pomoxis are also widely raised species. These hatcheries predominantly serve the demand for stocking and sport fishing, but there is thought to be promising potential for marketing sunfish as food. There is also some thought of stocking centrarchids as biocontrol agents for pests such as mosquitoes (C. Miller, personal communication). Sunfish hatcheries in particular often raise hybrids rather than pure-strain species (about 25% of hatcheries, Morris and Mischke 2000), and hybrids are also popular among private farm owners for stocking ponds. The benefits of hybrids include: (i) faster growth or survival (heterosis), (ii) more efficient conversion of food to biomass, (iii) greater disease or stress resistance, (iv) novel combinations of phenotypes, (v) biased sex ratios can be valuable if one sex is particularly valuable, and (vi) sterility. Hybrid sterility can be further reinforced by inducing triploidy via an environmental shock (temperature or hydrostatic) early in development, a process with high survival rates yielding 90 to 100% triploids. These triploids are almost uniformly sterile but viable (Parsons and Meals 1997; Morris and Mischke 2000). In centrarchids, hybrid Lepomis and Pomoxis are known for their fast growth (Hubbs and Hubbs 1931; Krumholz 1950) (Figure 2.11). This elevated growth is associated with more aggressive feeding behavior, which facilitates raising fish on artificial food and makes it easier for anglers to catch them. Hybrid Lepomis are also more tolerant of low oxygen concentrations (Tidwell et al . 1992). Sex bias and sterility are also desirable traits for two reasons. First, stocked

60

Centrarchid fishes

100

Standard length (mm)

80

60 Hy

ds

bri

ellus

yan L. c

40

sus

ibbo

L. g

20 In aquarium

Mar 4

In fish pond

In aquarium

Oct 5

Mar 12

Dec 13 Feb 10

Date Figure 2.11 Heterosis for growth in hybrid sunfishes, comparing growth curves for a cohort of Lepomis cyanellus (formerly Apomotis), L. gibbosus (formerly Eupomotis), and their hybrids. (Redrawn from Hubbs and Hubbs (1931). Publisher no longer exists. Papers of the Michigan Academy of Sciences, Arts, and Letters.)

ponds of Lepomis and Pomoxis often experience fast population growth leading to crowding and severe stunting. The low reproductive rate of hybrid centrarchids (due to sex ratio bias or partial sterility) limits their population growth and so avoids crowding (Krumholz 1950; Hooe and Buck 1991). The partial sterility of hybrids can be reinforced by artificially inducing triploidy in the hybrids (Will et al . 1994). Second, hybrid infertility prevents interbreeding with native centrarchids. Given the high rate of introductions and stocking of centrarchids, introgression with native species is a growing conservation concern.

2.5 Hybrids as a conservation threat Hybridization poses significant risks for natural populations of centrarchids. Species with incomplete reproductive isolation are at risk of genetic mixing (“introgression”). Over successive generations of backcrossing, foreign alleles can be introduced into the parental populations, possibly replacing the original genotypes (Rhymer and Simberloff 1996; Allendorf et al . 2001). This can result in the loss of genetic diversity for selected genes (Wilson and Bernatchez 1998). In centrarchids, M. floridanus allozyme alleles have been shown to invade and persist in native populations of M. salmoides (Johnson and Fulton 1999). Persistent hybridization can lead to the ultimate extinction of both parental lineages, leaving a genetically intermediate population entirely composed of Fx hybrids (Epifanio and Philipp 2001). This appears to have occurred in several populations of centrarchids that are dominated by hybrids (Pomoxis, Dunham et al . 1994; Lepomis, Dunham et al . 1994; Micropterus, Whitmore 1983; Philipp 1991). One dramatic example is a case of introgression between M. salmoides and M. floridanus that were both introduced to a newly created reservoir in Texas (Aquilla Lake). After the dam was built

Hybridization and speciation in centrarchids

61

in 1983, hybrid Micropterus increased from ∼2% of the population in 1984 to nearly 40% in 1987, at the expense of both parent species (Maceina et al . 1988). Asymmetrical hybridization can lead to the ultimate elimination of a species. Following the introduction of M. salmoides and M. dolomieu into the native range of M. treculi, extensive hybridization has led to a decline in the native species (Whitmore 1983; Morizot et al . 1991). A genetic survey of reservoir populations in the southeast found that the introduced M. dolomieu and hybrids were swamping out the native M. punctulatus (only 2 out of 276 fish in one lake had pure punctulatus genotypes) (Pierce and Van den Avyle 1997). A similar swamping has occurred after the introduction of M. punctulatus into a reservoir with native M. dolomieu. After only 15 years, pure M. dolomieu fish comprised only 1% of the population, the remainder being hybrids or the introduced species (Avise et al . 1997). Even when hybrids are completely sterile or inviable (preventing introgression), hybridization can threaten a species with extinction (Konkle and Philipp 1992; Konishi and Takata 2004). This is because individuals may expend much of their reproductive energy on mating with another species (yielding inviable progeny), rather than with their own species. The resulting loss of fecundity can lead to extinction. Given the incomplete premating and postmating isolation in centrarchids, there is good reason to be concerned about introgression and/or extinction due to hybridization. This is particularly alarming given the high rate of stocking and anthropogenic introductions in centrarchids. Introductions should be avoided where possible, minimizing both stocking and escapees from aquaculture facilities. Where introductions are deemed necessary, care should be taken to assess hybridization potential and, if possible, use species least likely to hybridize with native fishes. Currently, there is no effective remedy for ill-conceived fish introductions and hybridization once they are established. One caveat should be added to this warning: there is emerging evidence that hybridization can result in the origin of new species, rather than in the elimination of old ones (Rieseberg et al . 1995; Coyne and Orr 2004). When hybrids are viable but reproductively isolated from either parent, they may produce a third genetically independent lineage. Eliminating all hybridization (which can be a natural process) may thus get in the way of further accumulation of biodiversity (Allendorf et al . 2001). However, as there is currently no evidence for hybrid speciation in centrarchids, it is not clear that this caveat applies to this group of fishes.

2.6 Future directions Throughout this chapter we have indicated areas where further research would be particularly valuable. Despite the long history of research on centrarchid hybrids, much of the early work was largely anecdotal. Consequently there are many topics that have been addressed in a preliminary manner, but need more rigorous documentation. Perhaps the best example is the list of factors that promote natural hybridization (Hubbs 1955), including turbidity, disturbed habitats, and unequal ratios of parental species. Although these factors may indeed make interspecific spawning more likely, there is no statistically robust evidence for such effects. Consequently, there is great mileage to be gained from just conducting more systematic surveys of the incidence of natural hybrids, viability of artificial hybrids, and levels of postzygotic isolation. A more systematic survey would require broader sampling of habitats or species pairs with sufficient replication to test particular hypotheses, and should take advantage of the recent advances in centrarchid phylogenetics that provide a comparative framework for statistical analysis. The resulting data could be used to more rigorously test hypotheses about environmental factors that facilitate hybridization, the rate at which premating and postmating isolation evolves, or other large-scale questions giving insight into the mechanisms of speciation. Rather than attempt a thorough catalogue of promising avenues for future research, we will highlight three subjects that appear particularly interesting and have received little attention. First, there is a growing recognition that ecological divergence can facilitate speciation (Schluter and Nagel 1995; Hatfield and Schluter 1999; Boughman 2001; Nosil et al . 2002; Rundle 2002). Adaptation to distinct habitats or niches can result in divergence of both ecological and mating phenotypes. Ecological differences may mean that hybrids are poorly adapted to either parental niche (Hatfield and Schluter 1999). Mating traits can also change between habitats: adaptation to different depths or water qualities may cause divergence in color signaling used to select mates, in which case ecologically divergent individuals may experience prezygotic isolation (Boughman 2001). In centrarchids, there is almost no data on ecology’s role in premating or postmating isolation, or the effects of niche divergence on mating behavior or coloration.

62

Centrarchid fishes

Second, centrarchids are a promising system for studies of reinforcement. Reinforcement occurs when previously allopatric species are brought into contact and begin to hybridize (Coyne and Orr 2004). If the hybrids have reduced fitness, the parental species will waste energy and effort by hybridizing as their efforts will not yield viable and fertile progeny. Any individual who discriminates against the other species will avoid this waste. Consequently, there is indirect selection for stronger mating discrimination (Kirkpatrick 2001), “reinforcing” the reproductive isolation between species. The reinforcement model therefore predicts that premating isolation is stronger between sympatric species than between allopatric species. Many centrarchid species have partial geographic overlap with other species, making it possible to measure premating isolation for both sympatric populations and allopatric populations for a given pair of species. For example, it is interesting to note that the greatest hybridization among Pomoxis species occurs close to where both species are allopatric (Weiss Lake) and hence may have less evolutionary history selecting for the ability to avoid hybridization (Dunham et al . 1994; Travnichek et al . 1996). Such comparisons could be made for multiple species pairs spanning a range of degrees of postmating isolation. An even more promising approach would be to document the evolution of premating isolation following anthropogenic range expansion. Humans have introduced many species beyond their native ranges, creating new areas of sympatry between species that have never interacted before. Reinforcement theory predicts that these recently sympatric populations should be in the process of evolving stronger isolation. Finally, centrarchids are a potentially valuable system for genetic analyses of the ecological, behavioral, morphological, physiological, or biomechanical differences between species. The ability to make extensive interspecific crosses is a valuable tool for understanding the genetics of species differences. The ecologically and behaviorally diverse species of Lepomis are particularly promising, given their diversity and high levels of hybrid viability. However, genetic analyses of species differences require a number of genetic tools that are currently unavailable. High-density linkage maps of genetic markers must be developed before QTL analyses are possible. Gene microarrays offer a promising avenue into the study of gene expression differences among species (and in hybrids), but they must first be evaluated for their robustness to the extensive sequence divergence among centrarchid species. Given such tools, centrarchid hybrids may make fundamental contributions to our understanding of the genetic basis of reproductive isolation and phenotypic divergence.

2.7 Conclusions and summary There is no question that natural hybridization can cause serious headaches for taxonomists and naturalists interested in species identification. But these headaches arise from imposing arbitrary boundaries on the gradual and continuous process of speciation. At any one point in time we should expect to catch some pairs of populations that are neither fully compatible nor fully isolated. This is indeed the case in the family Centrarchidae, in which various species pairs span the range from slight to complete behavioral isolation, and whose hybrids range from fully viable and fertile, to completely sterile or even inviable. This variation in reproductive isolation provides valuable opportunities to study the progress of speciation and the genetic basis of species differences. For instance, studies of centrarchid hybridization has shown that postzygotic isolation accrues very gradually in taxa without distinct sex chromosomes, suggesting that sex determination mechanisms may influence speciation rates. Isolation also appears to accrue through the gradual accumulation of many inviabilities of small effect, some of which may involve not the traditional gene–gene interactions described by Dobzhansky and M¨uller, but by failed interactions between cytoplasmic transcription factors and nuclear genes. The incomplete hybrid inviability, so useful for research (and aquaculture) has its costs as well: anthropogenic introductions threaten the genetic distinctiveness and even the existence of a number of centrarchid species. Apart from being viewed as a tool kit for academic research, economic resource, or conservation concern, hybrid centrarchids have been a rich source of biological insight, and offer promising avenues for future research.

References Allendorf, F. W., R. F. Leary, P. Spruell, and J. K. Wenburg. 2001. The problems with hybrids: setting conservation guidelines. Trends in Ecology and Evolution 16: 613–622.

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Chapter 3

Ecomorphology of centrarchid fishes D. C. Collar and P. C. Wainwright

3.1 Introduction From the ecologist’s perspective, centrarchid fishes are widely recognized as a model system for investigating the role of phenotypic variation in shaping ecological patterns. To the ichthyologist, this group is considered among the most morphologically and ecologically diverse of North America’s freshwater ichthyofauna. This chapter is intended to bring these perspectives together, highlighting the contributions of studies linking resource use patterns to morphology in order to make sense of the ecological, functional, and morphological diversity exhibited within the Centrarchidae. We review literature on feeding and on locomotion. Historically, the diversity represented within this radiation helped inspire the development of ecomorphology, a research perspective that investigates hypothesized associations between organismal design and ecology. Working independently, Werner (1974, 1977) and Keast (1978, 1985; Keast and Webb 1967) were among the first to point out a general association between head and body form and resource use in centrarchid species. Using bluegill sunfish (Lepomis macrochirus), green sunfish (Lepomis cyanellus), and largemouth bass (Micropterus salmoides) to represent the range of ecological and morphological diversity in centrarchids, Werner and coworkers developed the first mechanistic insights into the implications of variation in body and head morphology. The diversity of form and feeding habits represented by bluegill, largemouth bass, black crappie (Pomoxis nigromaculatus), and rock bass (Ambloplites rupestris) motivated Keast’s proposal that different suites of morphological features confer varying prey capture and habitat use capabilities on these species and that these differences underlie the capacity for these species to coexist in sympatry. The rationale for ecomorphology research can be seen in both Werner’s and Keast’s work: an organism’s morphology affects its capacity to perform an ecologically relevant task, and this performance capacity affects the resources available for its use. This research program was made more explicit (Werner 1977; Mittelbach 1984; Wainwright 1996) by emphasizing that researchers’ ability to explain ecological phenomena through organismal design requires focus on characters whose performance consequences are predictable. This stipulation established a primary role for functional morphology research, which investigates the morphological basis of performance variation. Moreover, the ecomorphology research perspective led to widespread recognition that the choice of an appropriate performance measure is vital to the success of studies that seek to understand the relationship between morphology and resource use. Performance variables range from proximate measures that focus on the mechanical capacities of isolated functional units, such as maximum pharyngeal jaw bite force, to more integrative measures that involve multiple functional units, like prey handling time, which is influenced by the fish’s ability to capture and process prey. In either case, the performance measure should have predictable consequences for resource use. This is not a trivial issue, as the link between any given performance measure and resource use is more frequently assumed than demonstrated. Nevertheless, studies involving centrarchid fishes provide some of the best examples of the ecomorphology research program carried out to completion. The morphological diversity of centrarchid fishes ranges between the forms exhibited by the predominant ecomorphs: piscivore/crayfish predator, zooplanktivore, molluscivore, and insectivore, which possess combinations of head and body characters that are associated with different patterns of resource use. Although these ecomorphs are named according to trophic habits, they are generally associated with habitat use patterns as well. Here, we highlight a set of morphological characters that have well-known consequences for performance and resource use. We focus on mouth gape, degree 70

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of hypertrophy of the pharyngeal jaw [as represented by the size of its primary adductor muscle, the levator posterior (LP)], and body depth as a set of morphological characters that separate the major ecomorphs in morphospace (Figure 3.1), and we discuss the work that has investigated the degree to which these characters explain ecological variation. Piscivores/crayfish predators: As typified by species of Micropterus and warmouth (Lepomis gulosus) and to a lesser degree species of Ambloplites, these fishes have large mouths, gracile pharyngeal jaws, and relatively shallow bodies. They feed mostly on fish and crayfish in the open water, with some specializing on densely vegetated habitats (e.g., warmouth). Zooplanktivores: This ecomorph is best represented by the bluegill, which is the most planktivorous centrarchid species. They are small-mouthed with gracile pharyngeal jaws and deep bodies, and they feed heavily on zooplankton in the open water or in vegetated areas. Molluscivores: The molluscivorous centrarchids are the redear sunfish (Lepomis microlophus) and the pumpkinseed (Lepomis gibbosus), which are superficially similar to the bluegill, possessing relatively small mouths and deep bodies. However, they have hypertrophied pharyngeal jaws that deliver a bite forceful enough to crush snails. Insectivores: These fishes tend to possess intermediate character values of mouth size, pharyngeal jaw robustness, and body depth. An example of an insectivore is the black crappie; however, fishes classified as insectivores display a variety of forms. They feed predominantly on aquatic immature insects in various habitats, including vegetated areas, the benthos, and the water surface.

3.2 Ecomorphology of feeding Diets of centrarchid fishes can be explained in terms of maximizing benefits obtained from a prey item (e.g., energy) relative to costs incurred in obtaining it (e.g., time and energy involved in pursuit, capture, and processing; Werner and Hall 1974; Mittelbach 1981; Werner et al . 1981; Werner et al . 1983; Osenberg and Mittelbach 1989). As prey impose different functional demands on fish predators for their capture and processing, the costs for an individual fish will vary across prey types. Fish predators vary in morphology and performance capabilities, and the cost to consume a particular prey type should vary across individuals and species. This framework for investigating diet differences, which is known as optimal foraging theory, provides a set of clearly defined performance measures that are based on the costs predators incur when foraging and includes pursuit time, success rate of capture, and handling time. In this section, we focus on the morphological variables that underlie these integrative measures of performance as well as some of the proximate, functional performance measures that contribute to them. The feeding apparatus of centrarchid fishes is composed of two functional units: the oral jaws, which are used in prey capture, and the pharyngeal jaws, which are involved in prey processing. Due to their different functional roles, we discuss these two systems separately.

3.2.1 Oral jaws and prey capture Prey capture in centrarchid fishes is accomplished by ingesting a volume of water containing a prey item. During a strike, rapid expansion of the buccal (i.e. mouth) cavity results from a linked series of movements of head elements, including elevation of the neurocranium (NC), depression of the lower jaw, depression of the floor of the mouth, and abduction of the suspensorium and operculum (Lauder 1985; Figure 3.2). As water is incompressible, the increase in volume of the buccal cavity causes water to flow into the mouth. The goal for a feeding fish is to use this flow of water to carry the prey item into its mouth. This mode of feeding is called suction feeding, and it imposes specific functional demands on the fish predator for successful prey capture. We will show that suction feeding performance is influenced by the size of the fish’s mouth, its ability to open and close its mouth rapidly, as well as its capacity to accelerate a volume of water and generate high velocity flow.

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Figure 3.1 The distribution of six centrarchid species in a schematic morphospace. Axes are size-independent morphological characters whose resource-use consequences have been well studied: oral jaw gape width, levator posterior muscle mass (an indicator of pharyngeal jaw robustness), and body depth. Placement of centrarchid species in this morphospace illustrates the suites of character values that describe the predominant ecomorphs: Lepomis macrochirus represents the planktivore ecomorph, Lepomis microlophus and Lepomis gibbosus are molluscivores, Pomoxis nigromaculatus is an example of an insectivore, and Lepomis gulosus and Micropterus salmoides are piscivore/crayfish predators.

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Figure 3.2 High-speed video images of a largemouth bass striking fish prey. Time is indicated in the lower, right corner of each frame. Frames represent (a) the initiation of the strike, (b) lower jaw depression, (c) hyoid depression (i.e. depression of the floor of the mouth cavity) and cranial elevation, (d) maximum buccal expansion and prey capture. These movements of cranial elements expand the buccal cavity and characterize suction feeding, the primary mode of prey capture for all centrarchid species.

3.2.1.1 Oral jaws gape width underlies variation in size of prey consumed As prey are ingested whole, the size of the predator’s mouth places an absolute size limit on prey that it can engulf (Werner 1974). Prey items vary in size, and so individual fish should exhibit variation in their success rate or efficiency of capture across prey types. Therefore, differences among individuals or species in mouth size should reflect variation in diet (e.g., Huskey and Turingan 2001). This simple hypothesized relationship has been thoroughly investigated and used to explain multiple ecological patterns in centrarchid species (Werner 1977; Wainwright and Richard 1995). Werner (1977) showed that the maximum and optimum sized prey for a species is at least partly a function of mouth size. Using performance trials on prey of different sizes (Daphnia and fish), Werner measured cost as the sum of pursuit and handling times for bluegill, green sunfish, and largemouth bass. When cost is given as a function of prey size, the rank order of optimum sized prey (i.e. the prey size at minimum cost) and maximum sized prey for each species correspond to the rank order of mouth size (bluegill < green sunfish < largemouth bass) (Figure 3.3). Werner extended this analysis by quantifying the distribution of prey sizes available and successfully predicted resource utilization along this axis in each species. Furthermore, he predicted that because of its intermediate position on the niche axis, green sunfish should be excluded from habitats that contain both largemouth bass and bluegill—a pattern that is generally observed in natural systems (Hubbs and Cooper 1935; Bennett 1943; Trautman 1957; Werner et al . 1977). Wainwright and Richard (1995) further demonstrated the role of mouth size in explaining variation in ontogenetic diet shifts among species. In this study, the dietary data of Keast (1985) was translated into an index of average prey size and the relationship between this variable and mouth gape was investigated in bluegill, largemouth bass, rock bass, and black crappie. Although these species exhibit extensive variation in average prey size at any given body size, this variation collapses when this diet variable is given as a function of mouth gape. Ontogenetic diet switches to larger prey items are shown to occur at approximately the same mouth gape despite occurring at different body sizes in these species. A key insight gained from this work is that the consequences of mouth gape on prey size explain ontogenetic diet shifts, a very general pattern in fish foraging ecology.

3.2.1.2 Lever mechanics of the lower jaw influence the rate of mouth opening and closing The speed with which a fish can open and close its mouth during a strike is also partly determined by the ability of the lower jaw to transmit force and velocity generated by muscles. The lower jaw can be modeled as a simple lever system.

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Log prey weight (g) Figure 3.3 Cost of prey capture (in time per unit of prey mass) as a function of prey size in bluegill (Lepomis macrochirus), green sunfish (Lepomis cyanellus), and largemouth bass (Micropterus salmoides). Cost for each species is estimated for a common body size (200 g) and is a function of pursuit and handling times measured in lab performance trials. Rank order of optimum and maximum-sized prey for each species corresponds to rank order of mouth size. (Redrawn from Werner 1977, American Naturalist, Figure 7, University of Chicago Press.)

The mandible depresses when tension in the interoperculo-mandibular ligament pulls its postero-ventral margin, which acts through a lever arm to rotate the lower jaw at the joint between the articular bone of the mandible and the quadrate bone of the suspensorium (Figure 3.4). The mouth closes when the adductor mandibulae muscle, which originates in the suspensorial fossa and inserts directly on the medial face of the mandible, contracts and works through its lever arm to rotate the lower jaw at the articular-quadrate joint (Figure 3.4). Wainwright and Shaw (1999) showed that differences in these lever arms accurately predict variation in time to open and close the mouth in bluegill, spotted sunfish (L. punctatus), and largemouth bass. As a fish’s ability to capture elusive prey is in part limited by its capacity to open and close its mouth before the prey can escape, variation in opening and closing lever arms should reflect success rate and handling time on elusive prey. Although this relationship has not been investigated in centrarchid fishes, other fish groups, such as Labridae, exhibit an association between lower jaw lever mechanics and amount of elusive prey in the diet (Westneat 1995).

3.2.1.3 Capacity to generate subambient pressure inside the mouth cavity affects forces exerted on prey Feeding performance in a suction feeding fish is also determined by its capacity to draw a volume of water containing the prey into its mouth before the prey can escape. Expansion of the buccal cavity and resultant induced flow of water into the fish’s mouth is associated with a drop in pressure inside this cavity, and the fish must be able to overcome the hydrodynamic loading exerted by the pressure gradient (Alexander 1969; Carroll et al . 2004). For an individual fish, more rapid expansion results in a greater magnitude of pressure drop (Sanford and Wainwright 2002; Svanb¨ack et al . 2002),

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Figure 3.4 (a) Skull of a bluegill with fully opened mouth. The figure highlights structures that contribute to mouth opening and closing. The mandible (i.e. lower jaw) is composed of the dentary bone, which bears the teeth, articular bone, which articulates with the quadrate bone (deep to the adductor mandibulae muscle, not shown) to form the jaw joint, and the angular bone. The interoperculo-mandibular ligament (not shown) runs from the interopercle bone to the postero-ventral margin of the lower jaw and contributes to lower-jaw depression when the operculum retracts and abducts. The adductor mandibulae muscle originates on the suspensorium and attaches to both the upper and lower jaws; it provides power for mouth closing. (b) The lever arms of the lower jaw. The in-lever for jaw opening is the distance between the point of rotation of the lower jaw (the articular-quadrate joint, indicated by the encircled X) and the insertion of the interoperculo-mandibular ligament. The in-lever for jaw closing is the distance between the rotation point of the jaw and the insertion point of the adductor mandibulae muscle. Force and motion are transmitted to the tip of the mandible through the out-lever, which is the length of the lower jaw. Jaw opening is illustrated by dashed lines. (Panel (b) redrawn from Wainwright and Shaw 1999, Journal of Experimental Biology, Figure 1, The Company of Biologists Limited.)

and thus, rate of expansion is limited by the loading a fish can resist. In addition, differences in capacity to generate a pressure gradient in front of the striking fish’s mouth are associated with differences in patterns of flow (Muller et al . 1982; Van Leeuwen 1984; Lauder and Clark 1984; Higham et al . 2006b), which affect the forces exerted on the prey. For these reasons, magnitude of the pressure drop in the buccal cavity has been used as a measure of suction feeding performance in centrarchid fishes (Norton and Brainerd 1993; Grubich and Wainwright 1997). Carroll et al . (2004) developed and empirically tested a biomechanical model that uses static morphological variables to predict the maximum capacity of individual fish to generate subambient pressure inside the buccal cavity. Rotation of the NC is a major contributor to buccal expansion and is actuated by contraction of the epaxial muscles that attach to the supraoccipital crest and posterior portion of the NC (Lauder 1980). The epaxial muscles generate force that is transmitted through a moment arm to elevate the NC and expand the buccal cavity (Figure 3.5). The model predicts the magnitude of the pressure drop based on the transmission of force from the epaxial muscles to the expanding buccal volume (see Figure 3.5 for derivation) and allows the suction performance of any individual fish to be predicted from its morphology. Using a size range of bluegill, spotted sunfish, redear sunfish, largemouth bass, and black crappie, Carroll et al . (2004) tested this model by regressing the predicted pressure based on morphology against the largest magnitude pressure drop measured for individual fish. These species span the range of morphological and trophic diversity within the group and reveal that the model has strong predictive ability (r 2 = 0.71; Figure 3.5). This model offers a mechanistic explanation for an often observed association between morphology and feeding behavior in suction feeding fishes: small-mouthed, deep-bodied fishes, such as bluegill or pumpkinseed, tend to have large magnitude pressure drops and use little body movement during a strike, whereas large-mouthed, slender-bodied fishes, such as largemouth bass, tend to have reduced pressure drops and rely more on acceleration of the body to overtake prey (Norton and Brainerd 1993). As mouth size correlates with projected area of the buccal cavity, and as body depth correlates with epaxial physiological cross sectional area (PCSA, which is proportional to its force capacity) and its moment arm, the model explains the association between these morphological characters and suction performance. Although fish with larger mouths are capable of engulfing larger prey items, they suffer a decrement in capacity to generate suction. These fishes

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Figure 3.5 (a) Model of force transmission during buccal expansion illustrated on a largemouth bass skull. At the moment of minimum subambient pressure, force generated by the epaxial muscles (Fepaxial ) acting through its moment arm (Lin ) is equal to the force due to the intra-oral pressure drop (Fpressure ) acting through its moment arm (Lout ) (1). As the force generated by the epaxial muscles is equal to the product of physiological cross-sectional area of the muscle (PCSAepaxial ; m2 ) and its specific tension (P m ) given in units of force per length squared (N/m2 ) (2), and using the definition of pressure as force over projected area of the buccal cavity (Abuccal ; m2 ) (3), the above equation can be rewritten to give a relationship that predicts the magnitude of the pressure drop (4). (b) Regression of maximum pressure magnitude measured in lab feeding performance trials against morphological potential [(PCSAepaxial * (Lin /Lout )/Abuccal )] in various centrarchid species. The model predicts a substantial amount of the variation in maximum pressure magnitude (r 2 = 0.71) and provides an accurate estimation of specific muscle tension (P m = 68.5 kPa). (Redrawn from Carroll et al . 2004, Journal of Experimental Biology, Figures 2A and 5, The Company of Biologists Limited.)

might compensate for the reduced pressure gradient by swimming to overtake their prey. On the other hand, small-mouthed fishes might be capable of using the induced flow to exert larger forces on the prey. Indeed, Collar and Wainwright (2006) found that evolutionary changes in gape width have contributed more than any other model variable to the evolution of suction performance in centrarchids. Using the centrarchid phylogeny from Near et al . (2005) and measurements of the model’s morphological variables in 28 species, this study showed that gape width independently explains more than twice as much evolutionary change in suction capacity as any other variable even though all morphological variables underlie evolutionary change in suction capacity (Collar and Wainwright 2006). These studies provide insights into the link between morphological and functional diversity, but additional research is required to determine the consequences of variation in suction capacity for resource use. Although initially thought to increase the distance from which prey can be sucked into the mouth (Norton and Brainerd 1993), buccal pressure shows no relationship with the distance between predator and prey at the time of initiation of the strike (Wainwright et al . 2001; Svanb¨ack and Wainwright 2002).

3.2.2 Pharyngeal jaws and prey processing Following capture, prey are processed in the pharyngeal jaw, a set of modified branchial arches immediately anterior to the esophagus. In centrarchids, prey processing includes both transport of prey from the mouth cavity to the gut as well as mastication of prey prior to transport. In fact, bite force of the pharyngeal jaw underlies the capacity for molluscivory in centrarchid fishes (Lauder 1983; Wainwright et al . 1991; Huckins 1997). The pharyngeal jaw bite is accomplished by depression of the upper jaw against a stabilized and slightly elevated lower jaw. Bite force is primarily generated by the LP muscle, which actuates upper jaw depression through a simple linkage system (Wainwright 1989; Galis and Drucker 1996). The LP muscle originates on the postero-lateral face of the NC and inserts on the distal region of the dorsal side of the fourth epibranchial bone (EB 4; Figure 3.6). When this muscle contracts, it causes rotation of EB 4, which articulates with the dorsal surface of the upper jaw (third pharyngobranchial

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CB 5 Figure 3.6 The snail crushing mechanism illustrated on a redear pharyngeal jaw in posterior view. The prey item (shown as a gray oval) is positioned between the upper and lower jaw tooth plates. Force for crushing the prey is generated by the levator posterior (LP) muscle, which originates on the neurocranium (NC) and inserts on the distal region of the arch-shaped fourth epibranchial (EB 4) bone. Contraction of the LP results in rotation of EB 4 about its center (indicated by the encircled X), actuating depression of the upper jaw (PB 3). This downward force is resisted by a stabilized and slightly elevated lower jaw (CB 5).

bone, PB 3), causing it to depress (Wainwright 1989; Figure 3.6). The lower jaw (fifth ceratobranchial bone, CB 5) resists this force and contributes somewhat to bite force by elevating as a result of its linkage with the distal region of EB 4 (through connection with the fourth CB; Galis and Drucker 1996). The ability of a fish to crush snails is determined by its pharyngeal jaw bite force. Snails are positioned between the upper and lower tooth plates and cracked when the compression force exceeds the strength of the snail’s shell. Molluscivorous centrarchid species, the pumpkinseed and the redear sunfish, possess hypertrophied pharyngeal jaws, including a more massive LP muscle, which is capable of generating a more forceful bite, larger bones, which transmit and resist this force, and molariform teeth (Lauder 1983). The relationships between sizes of these pharyngeal jaw elements, snail crushing performance (i.e. bite force), and percent of diet made up of snails contribute to a variety of ecological patterns within and between centrarchid species. We focus primarily on mass of the LP muscle as an indicator of pharyngeal jaw hypertrophy, but note that mass of the LP muscle correlates with a suite of pharyngeal characters, including robustness of bones, sizes of other muscles involved in the pharyngeal bite cycle, as well as tooth shape (Lauder 1983). Pumpkinseed sunfish exhibit trophic polymorphism across Michigan lakes, varying in degree of hypertrophy of their pharyngeal jaws and consumption of snails (Wainwright et al . 1991). Typically, pumpkinseed occur in lakes with a predator, largemouth bass, and competitor, bluegill. In these lakes, largemouth bass restrict juvenile pumpkinseed and bluegill to highly vegetated habitats (Mittelbach 1981; Werner et al . 1983), where they compete for their primary prey resource, zooplankton (Mittelbach 1984; Osenberg et al . 1992). The presence of both predator and competitor limits population density of pumpkinseed thereby preventing over-exploitation of their adult prey resource, snails; however, in lakes where

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largemouth bass and bluegill do not occur, pumpkinseed populations have become large enough to maintain the snail population at a density so low that snails no longer contribute substantially to their diet (Osenberg et al . 1992). Therefore, lakes vary in snail abundance, and pumpkinseed populations inhabiting these lakes differ in pharyngeal jaw morphology and diet. In lakes containing abundant snail populations, adult pumpkinseed attain competitive refuge from co-occurring bluegill because of their capacity to consume snails (Mittelbach 1984). Although both species consume only zooplankton as juveniles, pumpkinseed begin to switch to a diet of snails at about 40-mm standard length (SL). At smaller sizes, individuals exhibit poor performance (measured as handling time) on snails, but beyond 40-mm SL they are able to consume increasingly hard snails as they grow to adult size (Mittelbach 1984; Osenberg et al . 1992). This ontogenetic diet shift is associated with growth of the LP muscle. Between the size at which pumpkinseed begin to crush snails and approximately 80-mm SL, the LP muscle increases in mass, and therefore force capacity, at a greater rate than body size; however, at about 80-mm SL, pumpkinseed are capable of crushing nearly every available snail they encounter, and growth of the LP muscle slows substantially (Wainwright et al . 1991; Figure 3.7). This pattern differs markedly from growth of the LP muscle in pumpkinseed that occur in lakes devoid of snails. In these lakes, pumpkinseed possess smaller LP muscles at all body sizes and exhibit no shift in growth rate during ontogeny (Wainwright et al . 1991; Figure 3.7). As these fish do not encounter or consume snails, their pharyngeal jaws do not experience the loading regime imposed by repeated snail crushing (Wainwright et al . 1991), and the observed differences between lakes in degree of pharyngeal jaw hypertrophy have been shown to be a result of these environmental differences rather than genetic divergence between populations (Mittelbach et al . 1999). Growth of the pharyngeal jaw and snail crushing performance also explain the consequences of human-mediated introduction of redear sunfish into the range of the pumpkinseed. Although their native ranges show almost no overlap, these species have come into secondary contact in Michigan lakes. As both are molluscivores, they are expected to compete for prey resources. Redear possess more robust pharyngeal jaws than pumpkinseed (Lauder 1983) and exhibit greater crushing strength at all body sizes (Huckins 1997; Figure 3.8). Their greater snail crushing performance permits redear to shift to a diet of snails at a smaller size (Figure 3.8) and to consume harder snails at all body sizes (Huckins 1997). Because of their superior competitive ability, the introduction of redear results in decreases in pumpkinseed snail consumption, growth rate, and abundance (Huckins et al . 2000).

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Figure 3.7 Scaling of the levator posterior (LP) muscle in pumpkinseed from a lake containing abundant snails (circles) and a lake containing effectively no snails (triangles). The LP is more massive at all body sizes examined in pumpkinseed from the lake where individuals frequently encounter and consume snails. Line segments indicate two-phase scaling of LP mass with a critical point corresponding to a body size of approximately 17 g. At body sizes smaller than 17 g, the LP grows at a greater rate than body mass, but at larger sizes, it grows at a slower rate than body mass. At body sizes larger than 17 g, pumpkinseed are capable of crushing nearly every snail they encounter. This two-phase LP scaling pattern is not evident in pumpkinseed from lakes that do not contain snails. (Redrawn from Wainwright et al . 1991, Functional Ecology, Figure 3, upper left panel, Blackwell Publishing.)

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Figure 3.8 Scaling relationships of (a) percentage of diet biomass made up of snails and (b) crushing strength of co-occurring redear and pumpkinseed. Crushing strength was estimated during laboratory feeding trials as the crushing resistance of snails that have a 0.5 probability of being crushed. Redear consume more snails and crush harder snails across all body sizes. (Redrawn from Huckins 1997, Ecology, Figures 1 and 5, respectively. Ecological Society of America/Allen Press.)

Variation among centrarchid species in degree of pharyngeal jaw hypertrophy might be accounted for by a tradeoff between capacity to generate bite force and feeding performance on soft-bodied prey. Figure 3.9 shows the scaling relationships of the LP muscle for molluscivorous centrarchids and their non-molluscivorous relatives across a range of adult body sizes. At all adult sizes, molluscivores have a larger LP muscle and nonmolluscivorous centrarchids exhibit variation in LP mass (P. C. Wainwright, unpublished data). Huckins (1997) demonstrated that redear require longer handling times than pumpkinseed when feeding on aquatic insect prey. In agreement with this result, Carroll et al . (2004) found that redear exhibit a weak capacity to generate subambient pressure in their buccal cavity. Poor suction performance of redear is partly due to reduced PCSA and moment arm of the epaxial muscle and increased buccal moment arm (see Figure 3.4), which might be a result of structural modifications made to accommodate the space occupied by the hypertrophied pharyngeal jaw (Carroll et al . 2004). Furthermore, a large, robust pharyngeal jaw might constrain the size of prey a fish can consume by preventing the passage of large prey, whereas small, gracile pharyngeal jaws (as in largemouth bass) might be flexible enough to allow passage of prey that are nearly the size of the oral jaws gape (Wainwright 1988; Wainwright and Richard 1995).

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Log standard length Figure 3.9 Scaling relationships of levator posterior (LP) muscle mass in the two molluscivorous species, redear (Lepomis microlophus) and pumpkinseed (Lepomis gibbosus), as well as some nonmolluscivorous species, warmouth (Lepomis gulosus), bluegill (Lepomis macrochirus), and largemouth bass (Micropterus salmoides). Molluscivores have more massive LP muscles than the nonmolluscivores at all body sizes, but substantial variation in LP mass exists among nonmolluscivores.

3.2.3 Comparing diversity in the feeding mechanism between lineages Although ecomorphology studies have made explicit links between resource use patterns and morphological variation in a few centrarchid species, it is unclear whether these hypothesized relationships successfully predict associations between morphological and ecological diversity throughout the lineages of the centrarchid radiation. To this end, Collar et al . (2005) compared diversity in characters of the feeding apparatus in Lepomis and Micropterus. These genera are hypothesized to be sister clades with strong phylogenetic support (Near et al . 2005), but Lepomis species collectively feed on a wider range of prey resources and thus, must meet a wider range of functional demands. Using a morphological data set including species’ values for maximum total length, oral jaw gape width, lever arms of the lower jaw, extent of upper jaw protrusion, mass of the primary mouth closing muscle (the adductor mandibulae), and mass of the LP muscle, Collar et al . found that Lepomis exhibits greater variation in the feeding apparatus than Micropterus (Figure 3.10), and therefore, the difference in diet diversity is reflected in morphological diversity. Moreover, greater variation exhibited by Lepomis is not accounted for by differences in time of evolution of each group, and the feeding apparatus has evolved at a faster rate in Lepomis (Collar et al . 2005). One possible explanation for the elevated rate of trophic evolution in Lepomis is that there has been less time between species divergence events and subsequent range overlap. If the capacity for these species to co-occur is limited by morphological and diet similarity, then less time to sympatry would be associated with an elevated rate of trophic evolution. However, whether the feeding apparatus of Lepomis has evolved exceptionally fast or that of Micropterus has evolved slowly, remains an open question. These two clades are sister to a third clade that contains the centrarchid genera Ambloplites, Archoplites, Centrarchus, Enneacanthus, and Pomoxis (Near et al . 2004, 2005), and the morphological diversity within this clade will clarify whether the rate of morphological evolution has sped up in Lepomis or slowed down in Micropterus. We speculate that the species that make up this clade span the range of morphospace and diet variation of both Lepomis and Micropterus. Enneacanthus species tend to be small with relatively small, protrusible mouths, and they resemble insectivorous Lepomis species such as the dollar (Lepomis marginatus) or bantam sunfish (Lepomis symmetricus). Enneachanthus species feed on immature aquatic insects and mircrocrustacea (Schwartz 1961; Flemer and Woolcott 1966), and thus exhibit diet overlap with these Lepomis species as well. Ambloplites species as well as Archoplites interruptus attain relatively large body sizes and have large, speed-modified mouths that protrude little and would probably overlap

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L. gulosus 2 PC 2

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Figure 3.10 Distribution of Lepomis and Micropterus species in a feeding mechanism morphospace. Axes are principal components (PCs) derived from eight morphological characters that have predictable effects on feeding performance. Characters that correlate strongly with each PC are indicated on each axis. Lepomis exhibits greater variation in characters of the feeding mechanism than Micropterus and this difference corresponds with a difference in diet variation. (Modified from Collar et al . 2005, Evolution, Figure 4, Society for Study of Evolution/Allen Press.)

Micropterus in morphospace (see Figure 3.10). In addition, the diets of Ambloplites species (Keast 1965; Elrod 1981; Petrimoulx 1983; Angermeier 1985) and A. interruptus (Imler et al . 1975) are similar to those of Micropterus species and include substantial proportions of large, evasive prey like crayfish and fish. In constrast, Pomoxis species and Centrarchus macropterus differ morphologically and trophically from the rest of Centrarchidae. They have large mouths comprising gracile, highly speed-modified jaws. Although little is known about the diet of C. macropterus, Pomoxis species are known to feed on a unique combination of prey items that includes large proportions of fish, aquatic insects, and zooplankton (McCormick 1940; Clark 1943; Dendy 1946; Huish 1957; Mathur 1972; Liao et al . 2002). Therefore, we speculate that the centrarchid clade containing these genera will exhibit greater morphological and diet variations than either Lepomis or Micropterus. However, how the rate of feeding apparatus evolution in this clade compares to Lepomis and Microtperus is unclear because its lineages have been evolving independently of one another for longer than those of either Lepomis or Micropterus (Near et al . 2005).

3.3 Ecomorphology of locomotion Swimming is of paramount importance in the lives of fish. It is essential for escape from predators and movement about the habitat, and is an often-overlooked component of feeding behavior. Body form of centrarchids is diverse (Figures 3.1 and 3.11) and is thought to have important implications for their locomotor abilities, activity patterns, foraging strategies, and behavioral energetics. Although the literature on the biomechanics of swimming only sparsely samples centrarchid species, it is true that centrarchids have figured prominently in research on locomotor biomechanics (Webb 1984; Lauder and Drucker 2004). As is true for feeding, the centrarchid locomotion literature is largely focused on largemouth bass and bluegill, and much of our understanding of the implications of the body form diversity in centrarchids is therefore based on inferences largely derived from research on few species. In this section, we review the current thinking about morphology–performance relationships in centrarchid locomotion, and we consider the literature on within-species polymorphisms that has been particularly influential in shaping our understanding of the implications of morphological diversity.

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0.25 Lepomis macrochirus Enneacanthus gloriosus Anterior 0.25

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Figure 3.11 Six centrarchid species distributed in a morphospace defined by the ratio of body depth to total length (x-axis) and the distance of the first dorsal spine from the snout as a fraction of fish total length. Deep-bodied, laterally compressed phenotypes, like that exhibited by Lepomis macrochirus, have been identified as providing a relatively large surface area to maximize the thrust-generating surface during fast-start behaviors (Webb 1984; Domenici and Blake 1997). L. macrochirus has the highest accelerations in fast-starts, and Micropterus salmoides the poorest, of the few centrarchids that have been tested (summarized in Domenici and Blake 1997). In addition, the deep-bodied, laterally compressed phenotype is thought to be better for turning behaviors. Median fins also provide surface area for fast-start thrust and are used in turning behaviors and slow maneuvers (Standen and Lauder 2005). A dorsal fin located posteriorly on the dorsum is in a position to contribute well to fast-start thrust while a fin positioned more anteriorly should have greater effect in turning and other maneuvers. We hypothesize that this morphospace corresponds generally with a performance space that is oriented at 45 ◦ to the morphospace. Hence, some deep-bodied species appear better designed for maneuvering than others. Both L. macrochirus and Pomoxis nigromaculatus show features that suggest high performance in acceleration, but L. macrochirus appears to be better built for maneuverability. Although Micropterus appears in this view of locomotor space to have low performance, this body form may be relatively specialized for efficient cruising at high speeds as the shape of the body has a more optimal fineness ratio that reduces drag and the distribution of muscle on the frame may facilitate efficient swimming motion. We emphasize that most of these interpretations of swimming performance in centrarchids are hypotheses that are yet to be adequately tested.

3.3.1 Swimming performance A powerful framework for thinking about fish locomotion was provided originally by Webb (1984, 1998) who identified three dimensions of locomotor performance: cruising, acceleration, and maneuvering. Relative to the full diversity of teleosts, most centrarchids are viewed as generalists with significant abilities in all three dimensions, but with different species showing significant variation in all three dimensions of locomotor performance. As we shall see, it is not yet possible to place most centrarchid species in Webb’s performance space and herein lies a promising research program. It is useful to consider first the relevance of these performance dimensions to the biology of centrarchid fishes. Acceleration performance is a key element of the rapid escape response of fishes when encountering would be predators (Webb 1986; Blake 2004) and has been shown to directly correlate with variation in escape success among individuals

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(Walker et al . 2005). Acceleration is also significant for the abilities of sit-and-wait ambush predators, and it is likely that many centrarchids periodically use high acceleration strikes to capture elusive prey. For example, the warmouth lives and forages in heavily vegetated habitats where it often feeds on elusive prey. It is possible that acceleration is an important determinant of strike success in warmouths and other similar centrarchids, but this idea has not yet been tested. Cruising performance is about being able to sustain a high rate of speed efficiently. This will be an important element in the biology of species that make extensive swimming forays during daily activity, such as species of Micropterus (Demers et al . 1996; Sammons and Maceina 2005), and is probably a major axis of diversity in centrarchids although surprisingly little is known about the typical distances covered swimming each day by different centrarchid species. Maneuvering with the median and paired fins may have the greatest direct relevance to feeding behavior and is particularly significant for fish that feed in a spatially complex habitat, such as the vegetated littoral zone of lakes. Maneuvering performance is also likely to be a major axis of diversity in centrarchids (Webb 1984; Savino and Stein 1989). Features that are thought to enhance fast-start performance and result in relatively high accelerations include a deep body with a large lateral surface area, including large surface area of median fins, particularly toward the tail end of the fish (Webb 1984; Domenici and Blake 1997; Blake 2004). A flexible body enhances the turning radius during fast-starts and the duration of the propulsive stroke. Finally, it is expected that a large white muscle mass, relative to body mass, will characterize strong accelerators. The laterally compressed L. macrochirus has shown the highest fast-start accelerations among the few centrarchids tested, performing better than L. cyanellus, which does better than M. salmoides (Webb 1975, 1978, 1986). These three species represent a range from deep-bodied to slender with bluegill being the most deep-bodied and largemouth bass the least. It seems possible that the deep-bodied form of many Lepomis species is an anti-predator adaptation that results in relatively high fast-start performance and a wide body profile that is difficult for predators to swallow. An interesting avenue for future research will be to compare patterns of natural selection acting on body shape in populations of species such as L. macrochirus in the presence and absence of gape-limited predators. Recent observations have also suggested that the spines in the dorsal fin of Lepomis species play a prominent role in defending against predators (Januszkiewicz and Robinson 2007). High-performance cruisers are expected to have features that enhance locomotor thrust and minimize drag (Lighthill 1975; Webb 1984). The classic features associated with extremely high thrust do not occur in any centrarchids, such as a high aspect ratio lunate caudal fin, a thin caudal peduncle, or a stiff anterior body. However, compared to other centrarchids, Micropterus appears to show features that reduce drag, including a more optimal body shape (fineness ratio), and small paired fins. It is possible that Micropterus also has a relatively high mass of red muscle, and overall a high ratio of axial muscle mass to total body mass. Both energetic swimming efficiency and critical swimming speed during cruising in M. salmoides have been found to be much higher than in Pomoxis annularis (Beamish 1970; Parsons and Sylvester 1992). When fish maneuver through their environment they make extensive use of both the median fins (Standen and Lauder 2005) and the pectoral fins (Drucker and Lauder 2002; Lauder and Drucker 2004). These fins are positioned away from the fish center of mass giving them high mechanical advantage when exerting forces that turn the fish (Eidietis et al . 2002). The centrarchid body appears to be designed to be unstable and to capitalize on the varied use of these fins particularly during slow swimming behaviors. Slow swimming in L. macrochirus can be powered entirely by the pectoral fins (Drucker and Lauder 2002). Among centrarchids it can be expected that fin-based maneuvers will be enhanced by relatively large dorsal, anal, pectoral, and pelvic fin surface areas, and a deep-body shape that positions the median fins away from the fish center of mass. Although not quantified in the literature, the pectoral fins of L. macrochirus and several other Lepomis species are considerably larger than similar sized individuals of Micropterus, Ambloplites, Acantharcus, or Pomoxis. Compared to other centrarchids, Micropterus dorsal and anal fins appear to have smaller surface area. Species of Lepomis have the dorsal and anal fins extending further anteriorly than in Pomoxis. The implications of these morphological patterns lead to the predictions that species of Lepomis, especially L. macrochirus, have better maneuverability, with members of the Pomoxis/Ambloplites clade being intermediate and Micropterus showing the poorest maneuverability.

3.3.2 Insights from within-species variation Some of the most compelling arguments for the adaptive significance of morphological variation in centrarchids for their swimming ability come from studies of intra-specific variation. The power of these studies is related to a classic principle

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in comparative biology: studies that focus on close relatives minimize the number of confounding differences between the study groups when trying to understand the consequences of design differences. Members of the same population of fish that differ in body proportion or fin morphology are likely to be more similar to each other in additional traits, than they would be to any other population or species. One therefore has more confidence in attributing performance differences to specific morphological variation. Researchers at the Kellogg Biological Station in Central Michigan discovered in the late 1980s that some populations of bluegill exhibited a polymorphism in body shape and fin morphology. Individuals that foraged in the vegetated littoral zone had a deeper body form and longer pectoral fins that attached more posteriorly on the body than fish in the same lake that foraged in the open water habitat (Ehlinger and Wilson 1988). These morphological differences were associated with differences in foraging behavior in the lab; littoral zone fish hovered for longer periods of time during foraging and had a higher feeding rate in a structurally complex habitat, whereas open water fish moved more constantly and had a higher feeding rate in the open water habitat when feeding on zooplankton (Ehlinger 1990). Similar patterns of variation in bluegill across these habitats have been reported by other authors (Layzer and Clady 1987; Chipps et al . 2004). A second series of studies has shown a similar pattern of variation in numerous populations of pumpkinseed (Gillespie and Fox 2003; Jastrebski and Robinson 2004; Robinson et al . 1993, 1996, 2000). Although pumpkinseed are usually sympatric with bluegill, there are several North American drainages where pumpkinseed occur in the absence of bluegill. This has set up a situation where the well-documented competitive interaction between bluegill and pumpkinseed (Mittelbach 1984) cannot occur and pumpkinseed in these lakes frequently display an open water phenotype in addition to the usual littoral zone specialists (Robinson et al . 1993, 2000). Open water fish are sometimes less deep-bodied than littoral zone fish, and their caudal peduncle region is consistently enlarged. In addition, the pectoral fins are smaller in open water fish, and positioned higher on the sides of the fish (Robinson and Parsons 2002, Jastrebski and Robinson 2004). Limited data suggest similar patterns in Lepomis humilis and L. cyanellus (Hegrenes 1999, 2001) in response to specific dietary regimes. It is not clear whether these differences within species are due to phenotypic plasticity or to genetic variation for phenotype, but the evidence is strong that these patterns are the result of diversifying selection, and hence the functional implications of these morphological differences for locomotor behaviors are of central importance to our understanding of how selection acts on swimming structures. Behavioral studies of how bluegill feed in the open water on plankton or in vegetated habitats on benthic prey help shed light on the possible significance of these morphological differences (Ehlinger 1990). Bluegill taken from the open water habitat move through the open water more quickly as they identify, strike, and consume individual planktonic prey. Littoral zone fish in the open water habitat move more periodically, hovering for extended periods, and have a slower net rate of ingesting individual prey items. The more slender body and enlarged caudal region of the open water fish may result in more efficient cruising locomotion, while their smaller pectoral fin contributes to this by creating less drag. On the other hand, feeding in the vegetation involves greater use of maneuverability and periodic hovering. The deeper body shape of littoral zone fish may allow them to make sharper turns (Walker 2004) and the enlarged pectoral fin provides a bigger surface area for the fish that probably incurs higher drag forces as it is used to perform a variety of hovering and turning maneuvers (Webb 1984; Domenici and Blake 1997). It is worth noting that although the connections between these morphological differences and more synthetic measures of performance, such as foraging rate, have been performed, there is still a need for studies that test the expected consequences of specific morphological features for more proximate measures of performance. For example, there are no studies we are aware of that test the hypothesis that more slenderbodied, open water Lepomis are more efficient cruisers than deeper-bodied individuals, or that larger pectoral fins result in better turning performance. The open water–littoral zone pattern of within population differentiation is widespread among north-temperate lake fish (Robinson and Parsons 2002). Several species within six teleost families show the littoral zone and open water phenotypes, and there is strong evidence of convergent patterns of body form as described here for centrarchids. This phylogenetically broad distribution of the phenomenon is strong evidence of common selective forces that underlie the responses of many fish species to these habitat types (Robinson and Schluter 2000). One example is that of the Eurasian perch (Perca fluviatilis) which is known to show littoral zone and open water specialization with open water fish having a more slender body form, larger caudal peduncle, and smaller pectoral fins than littoral zone fish that have a deeper body form and larger pectoral fins (Svanb¨ack and Ekl¨ov 2002, 2003). The habitat-specific morphology found in these northern lakes appears to relate mostly to foraging patterns. Open water fish feed mostly on small mid-water crustaceans and littoral zone fish feed on a somewhat more diverse selection of benthic prey that would be plucked from their positions in the sediment or on the surface of vegetation. In addition to

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the overall body form patterns described earlier, open water fish tend to have a smaller mouth and show better foraging performance feeding on planktonic prey than littoral zone fish (Ehlinger 1990; Jastrebski and Robinson 2004). Another line of investigation has compared populations of single species that live in a river to populations that live in a lake (Brinsmead and Fox 2002). This study of A. rupestris and L. gibbosus showed that for both species, individuals in the river were more slender-bodied and had smaller pectoral fins. Thus, the pattern is similar to that seen between littoral zone and open water fish. River dwelling fish appear to be better built for efficient cruising compared to lake dwellers. This may relate to a benefit to minimizing drag induced by a deep-body form and large fins in their exposure to ambient currents.

3.3.3 Integration of feeding and locomotion: a research frontier Research on the biomechanics of feeding has generally progressed independently of research on locomotion, but fish are usually swimming as they feed and it seems likely that many of the specific adaptations for locomotion are at least partly related to performance during feeding behaviors. Although little quantitative data are available, it is known, for example, compared to bluegill, largemouth bass intercept their prey while swimming relatively fast (Norton and Brainerd 1993). The use of ram during a strike enables the fish to close the distance between itself and its prey more rapidly (Higham et al . 2005a, 2006a), and higher ram speed appears to be an adaptation to capturing elusive prey such as fishes. In contrast to largemouth bass, bluegill normally brake during the strike (Higham et al . 2005b). Probably as a result of the slower swimming speed, bluegill are more accurate than largemouth bass with their strike, as the braking bluegills show a remarkable capacity to position prey at the center of the volume of water that they ingest during the strike (Higham et al . 2006a). However, little is known of the diversity of these behaviors in centrarchids, and important questions remain. Is strike accuracy associated with a small mouth, or is it related to approach swimming speed, or are all three factors tightly linked? Finally, we note that because many of the same structures used in locomotion are also part of the feeding apparatus (e.g., the anterior epaxial muscles), responses to natural selection on locomotor performance may directly affect feeding performance. For example, selection in bluegill populations that experience high predation from largemouth bass may respond by evolving a deeper-bodied form. This deep-bodied form also tends to increase the mechanical advantage of the epaxial muscles that insert on the back of the skull and power buccal expansion during suction feeding (Carroll et al . 2004). As a result, an increasingly deep body in response to predation may indirectly increase suction feeding capacity. The dynamics of this hypothesis have not been explored in natural populations.

3.4 Conclusions The ecological and morphological diversity exhibited within Centrarchidae continues to inspire innovative research with relevance to the fields of ecology, evolution, and biomechanics. In this review, we have highlighted some unique insights provided by the ecomorphology research program carried out in centrarchids, but we also hope to have identified some promising avenues of future inquiry. Although much progress has been made by focusing on a few centrarchid species at the extremes of morphospace, centrarchid biologists are left to infer the consequences of morphological variation in other species from these few studies. For example, based on studies of trophic polymorphism in pumpkinseed, we speculate that the observed variation in pharyngeal jaw robustness (Figure 3.9) is a consequence of a trade-off between bite force and gape limitation, but this hypothesis remains untested. Additionally, the locomotor performance consequences of variation in body shape and fin placement in most centrarchids remains largely unexplored. We hope that further application of the ecomorphological research perspective to the full range of centrarchid forms will continue to elucidate both within- and between-species diversity in this fascinating group of fishes.

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Wainwright, P. C. 1988. Morphology and ecology: functional basis of feeding constraints in Caribbean labrid fishes. Ecology 69: 635–645. Wainwright, P. C. 1989. Functional morphology of the pharyngeal jaw apparatus in perciform fishes: an experimental analysis of the Haemulidae. Journal of Morphology 200: 231–245. Wainwright, P. C. 1996. Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 77: 1336–1343. Wainwright, P. C. and B. A. Richard. 1995. Predicting patterns of prey use from morphology in fishes. Environmental Biology of Fishes 44: 97–113. Wainwright, P. C. and S. S. Shaw. 1999. Morphological basis of kinematic diversity in feeding sunfishes. Journal of Experimental Biology 202: 3101–3110. Wainwright, P. C., C. W. Osenberg, and G. G. Mittelbach. 1991. Trophic polymorphism in the pumpkinseed sunfish (Lepomis gibbosus Linnaeus): effects of environment on ontogeny. Functional Ecology 5: 40–55. Wainwright, P. C., L. A. Ferry-Graham, T. B. Waltzek, A. M. Carroll, C. D. Hulsey, and J. R. Grubich. 2001. Evaluating the use of ram and suction during prey capture by cichlid fishes. Journal of Experimental Biology 204: 3039–3051. Walker, J. A. 2004. Kinematics and performance of maneuvering control surfaces in teleost fishes. IEEE Journal of Oceanic Engineering 29: 572–584. Walker, J. A., C. K. Ghalambor, O. L. Griset, D. McKenney, and D. N. Reznick. 2005. Do fast starts increase the probability of evading predators? Functional Ecology 19: 808–815. Webb, P. W. 1975. Acceleration performance of rainbow trout Salmo gairdneri and green sunfish Lepomis cyanellus. Journal of Experimental Biology 63: 451–465. Webb, P. W. 1978. Fast start performance and body form in 7 species of teleost fish. Journal of Experimental Biology 74: 211–226. Webb, P. W. 1984. Body form, locomotion and foraging in aquatic vertebrates. American Zoologist 24: 107–120. Webb, P. W. 1986. Effect of body form and response threshold on the vulnerability of four species of teleost prey attacked by largemouth bass (Micropterus salmoides). Canadian Journal of Fisheries and Aquatic Sciences 43: 763–771. Webb, P. W. 1998. Entrainment by river chub Nocomis micropogon and smallmouth bass Micropterus dolomieu on cylinders. Journal of Experimental Biology 201: 2403–2412. Werner, E. E. 1974. The fish size, prey size, handling time relation in several sunfishes and some implications. Journal of the Fisheries Research Board of Canada 31: 1531–1536. Werner, E. E. 1977. Species packing and niche complementarity in three sunfishes. American Naturalist 111: 553–578. Werner, E. E. and D. J. Hall. 1974. Optimal foraging and the size selection of prey by the bluegill sunfish (Lepomis macrochirus). Ecology 55: 1042–1052. Werner, E. E., G. G. Mittelbach, and D. J. Hall. 1981. The role of foraging profitability and experience in habitat use by the bluegill sunfish. Ecology 62: 116–125. Werner, E. E., G. G, Mittelbach, D. J. Hall, and J. F. Gilliam. 1983. Experimental tests of optimal habitat use in fish: the role of relative habitat profitability. Ecology 64: 1525–1539. Werner E. E., D. J. Hall, D. R. Laughlin, D. J. Wagner, L. A. Wilsmann, and F. C. Funk. 1977. Habitat partitioning in a freshwater fish community. Journal of the Fisheries Research Board of Canada 34: 360–370. Westneat, M. W. 1995. Feeding, function, and phylogeny: analyses of historical biomechanics in labrid fishes using comparative methods. Systematic Biology 44: 361–383.

Chapter 4

Alternative reproductive tactics in the Centrarchidae B. D. Neff and R. Knapp

4.1 Introduction Fishes show enormous diversity of reproductive behaviors including the evolution of alternative reproductive tactics (Gross 1984, 1996; Taborsky 1994, 1998; Godin 1997; Henson and Warner 1997). Alternative reproductive tactics typically involve one type of male employing a territorial, guarding tactic (“bourgeois” tactic in Taborsky 1998) and the other type of male employing a less overt tactic (“parasitic” tactic in Taborsky 1998). In many species, such alternative reproductive tactics represent discrete life histories with parasitic males maturing precociously and at a smaller body size than bourgeois males (Gross 1996). Bourgeois and parasitic tactics have been described in 140 fishes from 28 families (Table 4.1; Taborsky 1998). Such alternative reproductive tactics are widespread in fishes likely because of: (i) indeterminate growth, which results in large variation in body size; (ii) the prevalence of external fertilization in an aqueous medium, which facilitates sperm competition; and (iii) the frequency of paternal care, which adds to the benefit of an alternative noncaring tactic (Taborsky 1994, 1998; see also Neat and Locatello 2002). Bourgeois and parasitic tactics can be identified based on five approaches comprising behavior, morphology, sperm traits, endocrinology, and genetics (Taborsky 1998; Knapp 2003). First, bourgeois males use mate monopolization behavior to procure fertilizations. Monopolization behavior may include defending resources important to females such as food or shelter, or direct defence of females to limit mating access of rival males. Parasitic males, on the other hand, typically do not attempt to monopolize females, but instead exploit bourgeois males. Such exploitation behavior may include: sneak- or streak-spawning whereby a parasitic male darts into a bourgeois male’s domain during spawning, or female mimicry whereby a parasitic male accesses females by deceiving a bourgeois male. Second, bourgeois males have morphological structures that increase their ability to monopolize mates and/or resources. These structures may include large teeth and increased body size. Parasitic males typically have structures that facilitate their ability to exploit bourgeois males. These structures may include small body size to decrease conspicuousness, or female-like structures and/or coloration to facilitate deception of bourgeois males. Third, investment trade-offs are expected to lead to differences in sperm traits between bourgeois and parasitic males (Parker 1990). Specifically, because parasitic males experience a higher risk of sperm competition than bourgeois males, parasitic males are expected to invest proportionately more into sperm number or quality (Parker 1990). The gonadal somatic index (GSI) is a popular measure of relative investment into sperm and it is calculated by dividing the mass of the gonads by the mass of the total body (including gonads). Across fishes, GSI has been shown to correlate with the intensity of sperm competition (Stockley et al . 1997) and, within species, parasitic males usually have larger GSI than bourgeois males (e.g., Gross 1982; Taborsky et al . 1987). Fourth, bourgeois and parasitic males often differ in circulating levels of two major teleost androgens, testosterone and 11-ketotestosterone (11KT). Bourgeois males consistently have higher levels of 11KT than parasitic males, but the tactics do not always differ in testosterone levels (reviewed by Brantley et al . 1993). Fifth, genetic parentage analysis can be used to confirm multiple paternity within broods, and it is required to verify that parasitic males are in fact fertilizing eggs. Parentage analysis using amplification of microsatellite DNA is a common method employed to genetically detect cuckoldry and calculate that fertilization success of parasitic (and bourgeois) males (e.g., Colbourne et al . 1996).

90

Alternative reproductive tactics in the Centrarchidae

91

Table 4.1 A summary of the number of species within fish families displaying bourgeois and parasitic mating tactics. Data are from Taborsky (1998).

Family

Number of species

Acanthuridae

3

Batrachoididae

1

Belontiidae

1

Blenniidae

2

Catostomidae

5

Centrarchidae

4

Chaetodontidae Cichlidae Cyprinidae

2 16 9

Cyprinodontidae

5

Esocidae

1

Gasterosteidae

5

Gobiidae

3

Hypoptychidae Labridae

1 25

Macrorhamphosidae

1

Mochokidae

1

Monacanthidae

1

Oryziidae

1

Ostrachiidae

1

Percidae

10

Polycentridae

1

Pomacentridae

7

Salmonidae

13

Scaridae

9

Serranidae

6

Sparidae

2

Tripterygiidae

4

In this chapter, we review alternative reproductive tactics in the Centrarchidae. Specifically, we review (i) species for which bourgeois and parasitic males have been described, (ii) genetic mechanisms underlying the evolution of alternative reproductive tactics (ultimate cause), (iii) physiological mechanisms underlying the expression of alternative reproductive tactics (proximate cause), and (iv) possible ecological constraints to the evolution and expression of alternative reproductive tactics. We conclude with a brief comparison of alternative mating tactics in centrarchids to those in other species and possible future directions for research on alternative mating tactics in the Centrarchidae.

92

Centrarchid fishes

4.2 Alternative reproductive tactics in the Centrarchidae Within the Centrarchidae, bourgeois and parasitic male types have been reported in 4 (12%) of the 34 species (Table 4.2). These species all occur in the genus Lepomis and comprise bluegill (all Latin binomials for Centrarchidae are listed in Chapter 1), longear sunfish, pumpkinseed, and spotted sunfish. GSI has been determined for the male types in all four species and averages 0.9% (range = 0.5 − 1.1%) for bourgeois males and 3.3% (range = 2.3 − 4.1%) for parasitic males. Thus, parasitic males invest 3.7 (=3.3/0.9) times more of their body mass into their testes than bourgeois males. Paternity data have been reported for three of the four species and confirm that parasitic males are successful at fertilizing eggs. Indeed, one study on bluegill estimated that parasitic males fertilize about 80% of the eggs when in direct competition with bourgeois males (Fu et al . 2001). However, because bourgeois males effectively exclude parasitic males from their nests during most of the spawning (e.g., Gross 1982), bourgeois bluegill males still fertilize a majority of all eggs. Across the three species for which paternity data are available, bourgeois males fertilize an average of 85.6% (range = 77.4 − 98.7%) of the offspring, whereas parasitic males fertilize an average of 14.4% (range = 1.3 − 22.6%) of the offspring. The absence of a parasitic morph has been noted in 5 (15%) of the 34 Centrarchidae species (Table 4.3). These species are from three genera and comprise dollar sunfish, redbreast sunfish, rock bass, largemouth bass, and smallmouth bass. GSI was reported for mature males in only one of these species (dollar sunfish) and it averaged less than 1%. Paternity has been investigated in all five species, and the average paternity of nest-tending bourgeois males was 97.6% (range = 94.8–100%). The remaining offspring that were genetically inconsistent with the nest-tending bourgeois males may be attributed to nest takeovers during spawning, cuckoldry by other bourgeois males, or mutation or scoring errors in the original genetic analyses.

Table 4.2 A summary of bourgeois and parasitic mating tactics described in the Centrarchidae. Data include type of evidence supporting existence of alternative tactics (behavior, morphology, sperm traits, endocrinology, and genetic), type of parasitic morphs described (sneaker and satellite), gonadal somatic index (GSI) and mean paternity among broods for bourgeois and parasitic males.

Species

Parasitic morphs

GSI (%)

Paternity (%)

n

Bourgeois

Parasitic

Sneaker Behavior Satellite morphology sperm traits endocrinology genetic

120

1.1

4.1

Sneaker Longear sunfish Behavior Satellite morphology Lepomis sperm traits megalotis endocrinology

21

1.0

Pumpkinseed Lepomis gibbosus

Behavior morphology sperm traits genetic

Sneaker Satellite

31

Spotted sunfish Lepomis punctatus

Sperm traits genetic

Sneaker

46

Bluegill Lepomis macrochirus

Mean

Evidence

Bourgeois

Parasitic

Source

106

77.4

22.6

Gross (1979, 1982), Kindler et al. (1989), Philipp and Gross (1994), Burness et al. (2004, 2005), Fu et al. (2001), Neff (2001)

3.6

–

–

–

Keenleyside (1972), Jennings and Philipp (1992), Knapp (unpublished data)

1.0

3.2

70

80.8

19.2

Gross (1979) Rios-Cardenas and Weber (2005) Neff and Clare (2008)

0.5a

2.3a

30

98.7

1.3

0.9

3.3

85.6

14.4

a Estimated from data presented in Figure 1 in DeWoody et al. 2000a.

n

DeWoody et al. (2000a)

Alternative reproductive tactics in the Centrarchidae

93

Table 4.3 A summary of species, within the Centrarchidae, that appear lack a parasitic morph. Data include type of evidence on which the absence of the parasitic morph is based (behavioral or genetic), and the mean paternity of nest-tending bourgeois males within broods. Species

Evidence

Paternitya (%)

GSI (%)

Source b

Dollar sunfish Lepomis marginatus

Genetic

94.8 (23)

<1.0 (97)

Mackiewicz et al. (2002)

Largemouth bass Micropterus salmoides

Genetic

95.7 (26)

–

DeWoody et al. (2000b)

Redbreast sunfish Lepomis auritus

Genetic

97.3 (25)

–

DeWoody et al. (1998)

Rock bass Ambloplites rupestris

Behavioral

100 (15)

–

Gross and Nowell (1980)

Smallmouth bass Micropterus dolomieu

Genetic

100 (15)

–

Gross and Kapuscinski (1994)

97.6

–

Mean

a Sample size is denoted in parentheses. b Actual GSI data not reported, only that all males collected had GSI values <1.0%.

Parasitic spawning has also been reported in redear sunfish (Gerald 1970), but it is unclear if there is a specialized parasitic morph in this species. There are insufficient data from the remaining 23 centrachid species to draw a conclusion on the presence or absence of parasitic males. Within the Centrarchidae, alternative reproductive tactics have been best studied in bluegill, with data coming from five different sources: behavior, morphology, sperm traits, endocrinology, and genetics. Gross (1982) referred to the bourgeoistype male as “parental” and the parasitic-type male as “cuckolder.” Parentals construct nests, are highly aggressive and territorial against fish of all sizes, and have light body color with a dark yellow-orange breast. Cuckolders are referred to as either “sneaker” or “satellite” based on their behavior (Gross 1982; also see Dominey 1980). Sneakers use a rapid nest entry and exit during spawning, are nonaggressive, and have light body color with light vertical bars. Satellites use a slow nest entry during spawning, are aggressive to fish of equal size, and have dark body color with dark vertical bars (similar to a female). In Lake Opinicon (Ontario, Canada), Gross (1982) reported that sexually mature parentals were on average 8.5 years in age, 172 mm in total body length and 82 g in body mass; sneakers were on average 2.7 years of age, 73 mm in total body length and 5 g in body mass; and satellites were on average 4.2 years of age, 95 mm in total body length and 12 g in body mass. Most cuckolders mature at 2 years of age, whereas most parentals mature at 7 years of age. Thus, cuckolders mature at a much younger age than parentals. By back-calculating yearly growth rate of sneakers, satellites, and parentals (based on annual rings on scales), Gross and Charnov (1980) showed that sneakers and satellites had similar growth rates at ages 2, 3, and 4 years, whereas parentals had significantly higher growth rates at these same ages. Thus, Gross and Charnov argued that sneakers and satellites represent a single life history (i.e. sneakers grow into satellites), and that the cuckolder life history is discrete from the parental life history. Interestingly, offspring of cuckolders grow faster than offspring of parentals, at least through the end of endogenous feeding from yolk sac reserves (Neff 2004). How or whether these early differences in growth rates contribute to later yearly growth rates remains to be determined. Parentals and cuckolders also differ in several sperm traits. First, cuckolders have smaller testes than parentals: average sneaker and satellite testes masses are 0.20 ± 0.10 g and 0.62 ± 0.19 g, respectively, whereas average parental testes mass is 1.82 ± 0.56 g (Neff et al . 2003). However, cuckolders invest proportionately more of their body mass into their testes as measured by GSI: average GSI for sneakers and satellites are 3.66 and 3.74%, respectively, whereas average GSI for parentals is 1.32% (Neff et al . 2003). Sneakers and satellites also produce milt that contains higher concentrations of sperm than that of parentals (sneakers: 1.4 ± 0.2; satellites: 2.0 ± 0.4; and parentals: 0.9 ± 0.1 million/µl; Neff et al . 2003). The sperm from sneakers contains more ATP, have slightly longer flagella, and swim faster than the sperm from parentals (Burness et al . 2004; but see Burness et al . 2005 for evidence of interannual variation in swim speed). Increased swim speed may give the sperm from sneakers a competitive advantage in the race to the unfertilized egg (e.g., Gage et al .

94

Centrarchid fishes

Table 4.4 A summary of paternity analysis of nest-tending parental male bluegill in Lake Opinicon (Ontario, Canada). Data comprise the number of nests from which progeny were collected, and the mean and range of paternity of parental males. The bottom line provides the total number of nests examined and the overall nest means. Parental male paternity n 40

Mean (%)

Range (%)

75.1

41–100

Source Philipp and Gross (1994)

38

76.9

26–100

Neff (2001)

28

81.3

45–100

Fu et al. (2001)

106

77.4

26–100

2004) and may have evolved in response to the asymmetry in the risk of sperm competition experienced by cuckolders and parentals; cuckolders always experience sperm competition because the parental is present during female egg release, whereas the sperm from parentals must compete with sperm from cuckolders in only about 10–15% of female egg releases (Gross 1982; Fu et al . 2001). The ATP quantity, flagellum length, and swim speed have not yet been examined in sperm from satellites. Male bluegill practicing alternative reproductive tactics also differ in steroid hormone levels. Sneaker and satellite male bluegill have significantly lower mean circulating levels of 11KT, a major teleost androgen, on the day of spawning than do parental males (sneakers: 1.2 ± 0.1; satellites: 0.9 ± 0.4; parentals: 13.8 ± 1.7 ng/ml; Kindler et al . 1989). This same study also documented that males exhibiting the three tactics did not differ significantly in mean testosterone levels (3.5 ± 0.1, 2.6 ± 0.7, and 4.4 ± 0.4 ng/ml, respectively). Across species, 11KT has been consistently associated with the males that use a display tactic to attract females for spawning, but the role of testosterone, if any, in tactic behavioral differences is unclear (Brantley et al . 1993; Borg 1994; Knapp 2003). In this context, it is interesting that when we recently sampled males from the same population as those studied in the Kindler et al . (1989) study, cuckolders had significantly higher levels of testosterone than parental males, but again there was no difference between sneakers and satellites (Knapp and Neff, 2007). This inconsistency in relative testosterone levels among male morphs between the two studies could arise for any number of reasons, including differences in colony size (and hence frequency or intensity of male–male interactions), time of the breeding bout within the year, and even interannual variation. Further insight into potential differences among the morphs could come from knowledge of levels of the stress steroid cortisol. For example, we have found that mean plasma levels of cortisol are significantly higher in sneakers and satellites than in parental males, with no significant difference between the two parasitic morphs (Knapp and Neff, 2007). The same pattern has been found in longear sunfish (Knapp 2003). This pattern of relative cortisol levels being the inverse of tactic differences in androgen levels is consistent with the generally anti-androgenic effects of cortisol in many vertebrates (Nelson 2005). Several studies have used genetic markers to investigate the reproductive success of bluegill cuckolders and parentals (Table 4.4). All of these studies were conducted on the Lake Opinicon bluegill population. The studies show that parentals on average fertilize 77% of the eggs within their nests. Cuckolders likely fertilize most of the remaining 23% of the offsprings (parentals fertilize about 1.8% of the eggs in neighboring males’ nests; Neff 2001). The studies revealed considerable variation in paternity among parentals (26–100%), although few studies have examined ecological and phenotypic correlates of this variation. Gross (1982), for example, did find that cuckolder intrusion rates were higher in shallower versus deeper colonies.

4.3 Genetic mechanisms for alternative reproductive tactics Three prominent mechanisms have been proposed to explain the evolution of alternative reproductive tactics (Dominey 1984; Gross 1996): (i) alternative strategies; (ii) mixed strategy; and (iii) conditional strategy. Four criteria can be used

Alternative reproductive tactics in the Centrarchidae

95

Table 4.5 Three potential mechanisms underlying the evolution of alternative reproductive tactics in the Centrarchidae. Four criteria differentiate among the three mechanisms. Adapted from Gross (1996). Criteria

Alternative strategies

Mixed strategy

Conditional strategy

1. Genetics/ heritability

Polymorphism/high

Monomorphism/low

Monomorphism/low

2. Condition dependent expression

None

None

Required

3. Negatively frequency dependent selection

Required

Expected

Not required

4. Relative fitnesses of bourgeois versus parasitic males

Equal

Equal

Unequal expected

Note: A tactic is defined as a phenotype and includes physiological, morphological, and behavioral characteristics. In the Centrarchidae, three reproductive tactics have been described comprising sneak, satellite, and parental. A strategy is defined as a genetically based decision rule used to allocate somatic and reproductive effort among potential tactics.

to differentiate among these three mechanisms (see Table 4.5). For the first mechanism, alternative strategies, a genetic polymorphism is involved and therefore a system characterized by alternative strategies should display high heritability of the tactics. The simplest case of such a genetic polymorphism would involve a single locus with two alleles; one allele would lead to the expression of the bourgeois tactic, whereas the second allele would lead to the expression of the parasitic tactic (in a diploid model one allele will be dominant and the second allele will be recessive). An individual’s condition does not play a role in which the tactic is adopted. Negatively frequency dependent selection—when the fitness of a morph is negatively related to its frequency in the population—is required in such systems to ensure that the two alleles are evolutionarily stable. At the equilibrium frequency of each allele, the two tactics will have equal fitnesses and the strategies are said to exist in an evolutionarily stable state (ESSt). The second mechanism, mixed strategy, involves a genetic monomorphism (i.e. all individuals have the same decision gene) and therefore a system characterized by a mixed strategy should display low heritability of the tactics. In a mixed strategy, the decision gene leads to males adopting the bourgeois tactic with probability p and the parasitic tactic with probability 1 − p. Thus, the tactic a male uses is dependent on a stochastic event and again an individual’s condition does not influence which tactic is adopted. The probability p is determined such that the two tactics have equal fitnesses because if one tactic contributes more to fitness, an alternative strategy leading to an increased probability of expression of that tactic should invade the population (Maynard Smith and Parker 1976). Negatively frequency dependent selection is expected to operate on the tactics (Dominey 1984), but it is not required for evolutionary stability. The probability p likely will vary among populations because of, for example, differences in ecology and, when the two tactics have equal fitnesses, the corresponding strategy is said to be an evolutionarily stable strategy (ESS). Gross (1996) has argued that there are no documented cases of a mixed strategy within a sex. The third mechanism, conditional strategy, also involves a genetic monomorphism (i.e. all individuals have the same decision gene). However, unlike the mixed strategy, in a conditional strategy, the decision gene leads to males adopting the bourgeois or parasitic tactic based on some aspect of the individual’s condition. For example, a decision gene could lead to the parasitic tactic when an individual is smaller than size s and the bourgeois tactic when the individual is larger than size s. In this case, the condition is an individual’s body size and all individuals will display both tactics sometime during their life. Alternatively, a conditional strategy can lead to fixed alternative phenotypes whereby an individual displays one or the other tactic, but never both during its lifetime. Again, if the condition is an individual’s body size then individuals below the critical size s at a specific age may adopt one tactic (for life), whereas individuals above s adopt the other tactic. In either case of a conditional strategy, the tactics are not expected to have equal fitnesses, but the adopted tactic given an individual’s condition is expected to have higher fitness than the alternative tactic. For example, when small individuals

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adopt the parasitic tactic, they should have higher fitness than if the same (small) individual adopted the bourgeois tactic. Consequently, at the condition switch point the two tactics are expected to have equal fitnesses (see Box 3 in Gross 1996). When the tactics are discrete (i.e. individuals only adopt one tactic throughout their life), the tactics may display moderate heritability depending on the heritability of condition. When individuals adopt both tactics sometime during their lifetime, no heritability is expected, although the frequency with which they adopt each tactic may show heritability. Negatively frequency dependent selection is not required to ensure evolutionary stability (although it likely will operate to some degree in such systems) and, provided the conditional strategy is resilient to invasion by other strategies, the conditional strategy is said to be an ESS. Both Dominey (1984) and Gross (1996) have argued that most examples of alternative reproductive tactics represent conditional strategies. Assuming that a mixed strategy is unlikely to occur in nature (Dominey 1984; Gross 1996), determination of the relative fitnesses of bourgeois and parasitic males can differentiate between alternative strategies and a conditional strategy (see Table 4.5). Gross and Charnov (1980) developed a life history model to calculate the relative fitnesses of parental and cuckolder male bluegill and thus their model can be used to determine if the parental and cuckolder life histories represent alternative strategies or a conditional strategy. The authors show that when the life histories (parental and cuckolder) have equal fitnesses, the equilibrium proportion of males entering either life history must equal the proportion of eggs fertilized by that life history. They used population sampling over 2 years (1977 and 1978) to estimate the proportion of males entering the parental and cuckolder life history, which were 79 and 21% for the two respective life histories. Based on the data summarized here in Table 4.4, parental and cuckolder males fertilize a mean of 77.4 and 22.6%, respectively, of the eggs in a given nest. Given that parentals may fertilize an additional 1.8% of the eggs in neighboring males’ nests (Neff 2001), the total proportion of eggs fertilized by parentals is thus 79.2% (= 77.4 + 1.8%) and by cuckolders is 20.8%. These latter proportions are strikingly close to the proportions of males calculated as entering each life history and indicate that parentals and cuckolders have equal fitnesses. Equal fitnesses of the parental and cuckolder life histories are consistent with alternative strategies and not expected from a conditional strategy. Furthermore, consistent with the former mechanism, Gross (1991a) showed that negatively frequency dependent selection was operating on cuckolder males. However, artificial breeding crosses suggest that the life histories have moderate heritability—about 30% of all sons produced by parental males mature precociously (i.e. become cuckolders) and about 46% of all sons produced by cuckolder males mature precociously (Gross, unpublished data; but see Alcock 1989, p. 412; also see Dominey 1984, p. 391). Moderate heritability is more consistent with a conditional strategy (with discrete tactics) than alternative strategies. Thus, it is unclear whether the parental and cuckolder life histories in bluegill represent a conditional strategy or alternative strategies (Figure 4.1). Determining whether or not condition plays a role in which life history is adopted by individuals could help to distinguish between the conditional strategy and alternative strategies mechanisms.

Parental 0

1

2

3

4

5

6

7

8

9

10

11

Cuckolder Sneaker

Satellite

2 1. Condition dependent (ESS); or 2. Genetic dependent (ESSt)

Figure 4.1 A schematic of the alternative life histories in bluegill (Lepomis macrochirus). The numbers denote age in years and the shaded regions denote sexual maturity. Gross and Charnov (1980) used growth rate data to infer that sneakers became satellites, but that the parental and cuckolder life histories were discrete (i.e. cuckolders do not become parentals). The parental and cuckolder life histories may represent either a conditional strategy if condition determines which life history is adopted at age 2 years [evolutionarily stable strategy (ESS)], or alternative strategies if genetics determines which life history is adopted [evolutionarily stable state (ESSt)].

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4.4 Proximate mechanisms for alternative reproductive tactics The expression of alternative reproductive tactics undoubtedly derives from differences among males in the levels of particular chemical messengers at one or more particular points in time. The point(s) in time at which these chemical messengers exert their effects, and the environmental (external or internal) cues to which males respond, remain to be elucidated in centrarchids and all other teleost with alternative reproductive tactics. However, basic vertebrate physiology suggests that various hormones are likely to play central roles in morph differentiation and tactic expression. Steroid and peptide hormones are ideally suited to mediate morph differentiation and tactic expression because of their function as chemical messengers that coordinate a variety of behavioral, developmental, and physiological processes across vertebrates. Steroid hormones, in particular, are known to have permanent, organizational effects early in development that could result in the differentiation of the male phenotypes associated with the behavioral tactics (see Moore 1991; Moore et al . 1998 for reviews). Based on the phenotypic differences among the male alternative reproductive tactics in centrarchids and what is known about the role of hormones in vertebrate sexual maturation and differentiation, likely candidates for such developmental effects in centrarchids are testosterone, estradiol, cortisol, and progestins. For example, testosterone and progesterone have both been shown to alter the proportion of male tree lizards developing into territorial versus nonterritorial morphs (Hews et al . 1994, Moore et al . 1998). Estradiol masculinizes the zebra finch song system (reviewed in Wade and Arnold 2004) and some sexually dimorphic areas in rodent brains (Arnold and Gorski 1984), and mediates plumage sexual dichromatism in some species of birds (Kimball and Ligon 1999). Corticosterone (the major anuran glucocorticoid) and corticotropin releasing factor (CRF) influence the timing of metamorphosis in anurans, in part by influencing thyroid hormone levels (Denver et al . 2002). No data currently implicate cortisol (the major teleost glucocorticoid) in male morph differentiation in teleosts, but it, thyroid hormone, growth hormone, and insulin-like growth factors are all prime candidates for future studies. These hormones have general effects on growth (Power et al . 2001) and muscle development (e.g., Rescan 2005), which are two characteristics that diverge among the male reproductive phenotypes in the vast majority of teleost species with alternative reproductive tactics. Given that body condition and growth rate play a large role in the adoption of alternative tactics in salmon (see the following text) and age at maturation in smallmouth bass (Baylis et al . 1993, Wiegmann et al . 1997, 2004), we hypothesize that both of these attributes will also be important in bourgeois and parasitic tactic adoption in sunfish. Finally, differential exposure to stressors during early development is known to have profound effects on adult behavior in mammals, and these effects are mediated in part by cortisol (or corticosterone) and CRF (Plotsky and Meaney 1993). Similar effects may be occurring in teleosts with respect to alternative reproductive tactics. In addition to developmental effects, hormones can also exert acute, activational effects on behavior and morphology. Thus it is also important to consider the proximate mechanisms mediating the expression of spawning behavior in any given breeding bout or season, once males mature sexually. For example, seasonal increases in androgen levels coincide with the expression of secondary sexual characters in teleosts and other vertebrates (e.g., Borg 1994; see Nelson 2005 and Adkins-Regan 2005 for reviews). Glucocorticoids often inhibit androgen production (Nelson 2005), but these effects can be ameliorated through the enzyme 11β-hydroxysteroid dehydrogenase (11β-HSD). This can inactivate glucocorticoids at several tissues, including the testes (e.g., Monder et al . 1994). In teleosts with alternative male reproductive tactics, this enzyme may be especially important, given that the male phenotypes differ in relative levels of testosterone and 11KT, and 11β–HSD catalyzes the final step in 11KT synthesis from testosterone or androstenedione (see Knapp 2003 for further discussion). Independent of their effects on androgen levels, glucocorticoids mobilize energy stores. Thus body condition differences among the male tactics in bluegill could contribute to the observed differences in circulating cortisol levels. Conversely, differential energetic demands of the different tactics may drive the morph differences in cortisol levels that we have observed in bluegill and longear (Knapp and Neff 2007 and unpublished data). The importance of growth and body condition to age at maturity for smallmouth bass and salmon indicates that this is likely a fruitful area for future research in sunfish with respect to both morph differences and within-morph variation in behavior, especially for parental males (e.g., Magee et al . 2006). In addition to steroid hormones, several peptide hormones have been implicated in activating behavioral differences among male phenotypes in other species coincident with expression of alternative tactics (reviewed in Goodson and Bass 2001; Knapp 2003). For example, the number of neurons containing gonadotropin-releasing hormone differs between reproductive phenotypes in the grass goby (Zosterisessor ophiocephalus; Sciaggiante et al . 2004), plainfin midshipman (Porichthys notatus; Grober et al . 1994) and bluehead wrasse (Thalassoma bifasciatum; Grober et al . 1991).

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Similar morph differences in neurons containing arginine vasotocin (AVT) occur among the male morphs in plainfin midshipman (Foran and Bass 1998, 1999), bluehead wrasse (Godwin et al . 2000), and various goby and blenny species (e.g., Grober et al . 2002; Miranda et al . 2003). Isotocin (the teleost homolog of mammalian oxytocin) has differential effects on neural activity associated with reproductive tactic in the plainfin midshipman; Type I parental males are less responsive to isotocin than Type II sneaker males and females, which resemble each other in their responses (Goodson and Bass 2000). Clearly this is also a productive area for future investigation in bluegill and other centrarchids.

4.5 Ecological and evolutionary constraints on the evolution of alternative reproductive tactics Based on the current survey of alternative reproductive tactics in Centrarchidae, there are similar numbers of species with and without alternative reproductive tactics (four species with and five species without; assuming absence of evidence of alternative reproductive tactics is evidence of their absence). Given that all of the species with alternative reproductive tactics occur in the genus Lepomis, it is possible that the parasitic tactic is a derived trait in this genus (Figure 4.2). However, two species of Lepomis (L. auritus and L. marginatus) appear to lack parasitic males and thus the tactic may have been lost in these species. Interestingly, L. marginatus forms a clade with L. megalotis, which has the parasitic tactic, and the three species (L. auritus, L. marginatus, and L. megalotis) together also form a clade, indicating either multiple origins or multiple losses of the parasitic tactic within Lepomis. It has been postulated that alternative reproductive tactics are widespread in teleosts in part because indeterminate growth results in large variation in male body size (and hence competitive ability) and a high frequency of paternal care adds to the benefit of an alternative noncaring tactic (Taborsky 1994, 1998). Although paternal care (or some form of male territoriality) is a prerequisite for the evolution of a cuckolder tactic, paternal care does not explain the distribution of alternative reproductive tactics within the Centrarchidae because all species within this family display paternal care.

Lepomis humilis Lepomis macrochirus Lepomis gulosus Lepomis symmetricus Origin

Lepomis cyanellus Loss 1 Loss 2

Lepomis auritus Lepomis marginatus Lepomis megalotis Lepomis gibbosus Lepomis microlophus ? Lepomis punctatus Lepomis miniatus

Figure 4.2 A partial phylogeny of the genus Lepomis depicting the presence () and absence (×) of alternative reproductive tactics. The phylogeny is taken from Chapter 1. With the current data on alternative reproductive tactics, one parsimonious scenario is a single origin predating diversification within Lepomis and subsequent loss of the parasitic tactic in L. auritus and L. marginatus. Alternatively, if the ancestor to Lepomis lacked the parasitic morph, three independent origins could explain the current distribution of alternative reproductive tactics. Parasitic spawning has been reported in L. microlophus, but it is unclear whether or not there is a specialized parasitic morph.

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However, the energetic cost of this paternal care may be important (e.g., Coleman and Fischer 1991; Magee et al . 2006). Similarly, rates of growth, and in particular age at maturation, for bourgeois males may play a role in the evolution of alternative reproductive tactics within this family. Based on genetic analyses of paternity, the overall reproductive success of parasitic males as a group is considerably lower than that bourgeois males (see Table 4.2). However, if parasitic males have higher survivorship to maturation than bourgeois males then the relative fitnesses of the two tactics may be closer to equality and may favor the evolution of alternative tactics, particularly if the tactics represent alternative strategies (see earlier). Precocious maturation by parasitic males should provide higher survivorship for these males as compared to bourgeois males. Thus, species with late maturing bourgeois males should provide greater opportunity for precocious maturation and may be more likely to evolve a parasitic morph. Consistent with this idea, bluegill, pumpkinseed and longear sunfish all have relatively late maturing bourgeois males (≥5 years in the populations studied) and early maturing parasitic males (≤2 years). Indeed, variation in the age at maturation among populations within a species could lead to some populations evolving the parasitic tactic and others not evolving the tactic. The large latitudinal variation across populations of many sunfishes (e.g., bluegill, longear), which can lead to large variation in growth rate and age at first maturation (Carlander 1977), makes using sunfish a tractable system to test such a hypothesis about the effect that age at first maturation has on the evolution of alternative life histories. Finally, in birds it has been argued that both breeding synchrony and breeding density have roles in the evolution of cuckoldry (Stutchbury and Morton 1995; Westneat and Sherman 1997). An increase in either breeding synchrony or density should increase reproductive opportunities for parasitic males and thus the potential benefit to such a tactic. It is unlikely, however, that breeding density plays a role in the evolution of alternative reproductive tactics within the Centrarchidae because bluegill are known to nest colonially (i.e. high density of nesting males) whereas pumpkinseed nest solitarily (i.e. low density of nesting males), yet both are characterized by alternative reproductive tactics. Furthermore, redbreast sunfish are known to nest colonially whereas male largemouth bass and smallmouth bass nest solitarily, yet these three species appear to lack parasitic males. Little is known about the role synchrony plays in the evolution of alternative reproductive tactics within the centrachids. Bluegill in Lake Opinicon breed in highly synchronous bouts (Cargnelli and Gross 1996) and pumpkinseed also breed with some degree of synchrony (Neff, personal observation). However, Gerald (1970, p. 61) reported that bluegill in a creek near Austin, Texas, United States spawn such that only one male may be spawning on any given day. Thompson (1998, p. 6), working with bluegill in the same general area also reported lack of distinct breeding bouts such as those seen in Lake Opinicon, but her GSI data indicate the presence of at least two alternative male phenotypes. Interestingly, Thompson (1998, p. 7) also reported that she observed a few males exhibiting behavior consistent with that of the satellites from Lake Opinicon. Bluegill males with large GSI have also been collected in central Oklahoma (Knapp, unpublished data), but the degree of spawning synchrony in this location is currently unknown. Similarly to the bluegill, a pond population of pumpkinseed near Albany, New York, United States appears to have low breeding synchrony and the population lacks the “satellite” morph (Rios-Cardenas and Webster 2005) that has been observed in the Lake Opinicon population studied by the authors (Neff and Clare, 2008). Thus synchrony of breeding could play a role in the evolution of alternative reproductive tactics in the Centrachidae, or at least in the local presence or absence of particular tactics, perhaps in conjunction with latitude and associated variation in annual growth rates.

4.6 Alternative reproductive tactics in other fishes Alternative reproductive tactics have been extensively studied with respect to life history features in the Salmonidae (reviewed by Fleming 1998). In the Salmonidae, parasitic males are sometimes called “jack” or “parr” and bourgeois males are called “hooknose” or “anadromous” depending on the species. Jack and parr males are similar to sneaker males in the Centrarchidae in that they mature precociously and use a sneaking tactic to fertilize eggs. These males also never themselves become bourgeois males. Hooknose and anadromous males delay maturation and use a fighting and monopolization tactic to fertilize eggs. Unlike the bourgeois males in the Centrarchidae, these males provide no parental care to the offspring. In an early paper on coho salmon (Oncorhychus kisutch), Gross (1985) used survivorship to maturity data and behavioral estimates of reproductive success to estimate that jack and hooknose males had close to equal fitnesses. These data suggest that the two male tactics were therefore likely to represent alterative strategies in an ESSt. In chinook salmon (Oncorhychus tshawytscha), Heath et al . (2002) found that the jack tactic had a high, sex-linked heritable component

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(sire h2 = 0.62), which may be consistent with a genetic polymorphism and alternative strategies (see Table 4.5). However, studies in Atlantic salmon (Salmo salar) show that the developmental decision that leads to divergence in male reproductive tactic is dependent on both genetic and environmental factors (e.g., Hutchings and Myers 1994; Hutchings and Jones 1998; Aubin-Horth and Dodson 2004). In particular, a high growth rate during early life appears to lead to precocious maturation (see Gross 1991b; Hutchings and Jones 1998). These data indicate that the tactics in Atlantic salmon are condition dependent and therefore represent a conditional strategy. However, relatively few studies have explored proximate mechanisms underlying tactic expression in salmonids, but this is starting to change (e.g., Larsen et al . 2004; Aubin-Horth et al . 2005). Similarly, studies exploring endocrine and other physiological correlates and effects of social interactions in juveniles (e.g., Gilmour et al . 2005) may ultimately contribute to understanding of tactic adoption in salmonids. In contrast to our understanding of tactic adoption in salmonids, studies of other teleosts with alternative mating tactics have tended to focus on behavioral and endocrine aspects. For example, a number of studies have documented androgen and peptide hormone differences among male phenotypes (see Section 4.4 earlier). Estrogen may also be important in the expression of alternative male reproductive tactics, as morph differences in aromatase (the enzyme that converts testosterone to estradiol) has been documented in plainfin midshipman (Schlinger et al . 1999). A few studies have demonstrated effects of androgen or AVT manipulation on behavior and morphology associated with differences in male reproductive tactics (Oliveira et al . 2001; Semsar et al . 2001; Semsar and Godwin 2004; Lee and Bass 2005). However, in all of these species, little is known about the ecological and genetic factors that affect tactic expression.

4.7 Future directions In writing this review, we were surprised to find how little published information exists on the various aspects of alternative reproductive tactics in centrarchids other than bluegill. At the same time, bluegill are unique among teleosts with alternative reproductive tactics in the degree of understanding that exists across the five approaches of behavior, morphology, sperm traits, endocrinology and genetics that we have reviewed earlier. Characteristics of tractable mating systems for research on alternative reproductive tactics included ease of observation during spawning, which facilitates the collection of large data sets on behavior, morphology and sperm characteristics, and a large enough body size so that the fish can be easily sampled for various physiological measurements, including circulating levels of hormones. As these attributes are true of bluegill, they are arguably true for all of the other centrarchids. Despite what we do know about alternative reproductive tactics in bluegill, many important questions remain, particularly with respect to mechanisms. What is/are the proximate trigger(s) that influence the development of a male into a bourgeois versus a parasitic life history? Is this simply a matter of timing of maturation based on an individual male’s growth rate or do social interactions play a role (individual state versus status)? How large is the genetic component of this differential development (e.g., differential sensitivity to environmental factors)? What factors mediate the apparent transition from sneaker to satellite behavior? How do tactic differences in sperm and gonadal traits arise? Considering the Centrarchidae as a whole, an accurate assessment of the presence and absence of alternative reproductive tactics across the family is vital if we are to determine which evolutionary mechanism underlies alternative reproductive tactics in the family. In this context, additional information on the role of breeding synchrony and age at maturation of bourgeois males would be useful, especially for bluegill where we already have a considerable amount of other information. There is little doubt that the Centrarchidae represent an ideal family to study the evolution of alternative reproductive tactics.

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Kimball, R. T. and J. D. Ligon. 1999. Evolution of avian plumage dichromatism from a proximate perspective. American Naturalist 154: 182–193. Kindler, P. M., D. P. Philipp, M. R. Gross, and J. M. Bahr. 1989. Serum 11-ketotestosterone and testosterone concentrations associated with reproduction in male bluegill (Lepomis macrochirus, Centrarchidae). General and Comparative Endocrinology 75: 446–453. Knapp, R. 2003. Endocrine mediation of vertebrate alternative male reproductive phenotypes: the next generation of studies. Integrative and Comparative Biology 43: 658–668. Knapp, R. and B. D. Neff. 2007. Steroid hormones in bluegill, a species with male alternative reproductive tactics including female mimicry. Biology Letters 3: 628–631. Larsen, D. A., B. R. Beckman, K. A. Cooper, D. Barrett, M. Johnston, P. Swanson, and D. W. Dickhoff. 2004. Assessment of high rates of precocious male maturation in a spring Chinook salmon supplementation hatchery program. Transactions of the American Fisheries Society 133: 98–120. Lee, J. S. F. and A. H. Bass. 2005. Differential effects of 11-ketotestosterone on dimorphic traits in a teleost with alternative reproductive morphs. Hormones and Behavior 47: 523–531. Mackiewicz, M., D. E. Fletcher, S. D. Wilkins, J. A. DeWoody, and J. C. Avise. 2002. A genetic assessment of parentage in a natural population of dollar sunfish (Lepomis marginatus) based on microsatellite markers. Molecular Ecology 11: 1877–1883. Magee, S. E., B. D. Neff, and R. Knapp. 2006. Plasma levels of androgens and cortisol in relation to breeding behavior in parental male bluegill sunfish, Lepomis macrochirus. Hormones and Behavior 49: 598–609. Maynard Smith, J. and G. A. Parker. 1976. The logic of asymmetry contests. Animal Behaviour 24: 159–175. Miranda, J. A., R. F. Oliveira, L. A. Carneiro, R. S. Santos, and M. S. Grober. 2003. Neurochemical correlates of male polymorphism and alternative reproductive tactics in the Azoran rock-pool blenny, Parablennius parvicornis. General and Comparative Endocrinology 132: 183–189. Monder, C., Y. Miroff, A. Marandici, and M. P. Hardy. 1994. 11β-Hydroxysteroid dehydrogenase alleviates glucocorticoid-mediated inhibition of steroidogenesis in rat Leydig cells. Endocrinology 134: 1199–1204. Moore, M. C. 1991. Application of organization-activation theory to alternative male reproductive strategies: a review. Hormones and Behavior 25: 154–179. Moore, M. C., D. K. Hews, and R. Knapp. 1998. Hormonal control and evolution of alternative male phenotypes: generalizations of models for sexual differentiation. American Zoologist 38: 133–151. Neat, F. C. and L. Locatello. 2002. No reason to sneak: why males of all sizes can breed in the hole-nesting blenny, Aidablennius sphinx . Behavioral Ecology and Sociobiology 52: 66–73. Neff, B. D. 2001. Genetic paternity analysis and breeding success in bluegill sunfish (Lepomis macrochirus). Journal of Heredity 92: 111–119. Neff, B. D. 2004. Increased performance of offspring sired by parasitic males in bluegill sunfish. Behavioral Ecology 15: 327–331. Neff, B. D. and E. L. Clare. 2008. Temporal variation in cuckoldry and paternity in two sunfish species (Lepomis spp.) with alternative reproductive tactics. Canadian Journal of Zoology 86: 92–98. Neff, B. D., P. Fu, and M. R. Gross. 2003. Sperm investment and alternative mating tactics in bluegill sunfish (Lepomis macrochirus). Behavioral Ecology 14: 634–641. Nelson, R. J. 2005. An introduction to behavioral endocrinology. Third edition. Sinauer, Sunderland, MA. Oliveira, R. F., L. A. Canario, D. M. Goncalves, A. V. M. Canario, and M. S. Grober. 2001. 11-Ketotestosterone inhibits the alternative mating tactic in sneaker males of the peacock blenny, Salaria pavo. Brain, Behavior and Evolution 58: 28–37. Parker, G. A. 1990. Sperm competition games: raffles and roles. Proceedings of the Royal Society of London, Series B 242: 120–126. Philipp, D. P. and M. R. Gross. 1994. Genetic evidence for cuckoldry in bluegill (Lepomis macrochirus). Molecular Ecology 3: 563–569. Plotsky, P. M. and M. J. Meaney. 1993. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) messenger RNA, median eminence CRP content and stress-induced release in adult rats. Molecular Brain Research 18: 195–200.

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Power, D. M., L. Llewellyn, M. Faustino, M. A. Nowell, B. T. Bjornsson, I. E. Einarsdottir, A. V. M. Canario, and G. E. Sweeney. 2001. Thyroid hormones in growth and development of fish. Comparative Biochemistry and Physiology C 130: 447–459. Rescan, P. Y. 2005. Muscle growth patterns and regulation during fish ontogeny. General and Comparative Endocrinology 142: 111–116. Rios-Cardenas, O. and M. S. Webster. 2005. Paternity and paternal effort in the pumpkinseed sunfish. Behavioral Ecology 16: 914–921. Schlinger, B. A., C. Creco, and A. H. Bass. 1999. Aromatase activity in the hindbrain vocal control region of a teleost fish: divergence among males with alternative reproductive tactics. Proceedings of the Royal Society of London, Series B 266: 131–136. Sciaggiante, M., M. S. Grober, V. Lorenzi, and M. B. Rasotto. 2004. Changes along the male reproductive axis in response to social context in a gonochoristic gobiid, Zosterisessor ophiocephalus (Teleostei, Gobiidae), with alternative mating tactics. Hormones and Behavior 46: 607–617. Semsar, K., F. L. M. Kandel, and J. Godwin. 2001. Manipulations of the AVT system shift social status and related courtship and aggressive behavior in the bluehead wrasse. Hormones and Behavior 40: 21–31. Semsar, K., and J. Godwin. 2004. Multiple mechanisms of phenotype development in the bluehead wrasse. Hormones and Behavior 45: 345–353. Stockley P., M. J. G. Gage, G. A. Parker, and A. P. Møller. 1997. Sperm competition in fishes: the evolution of testis size and ejaculate characteristics. American Naturalist 149: 933–954. Stutchbury, B. J. and E. S. Morton. 1995. The effect of breeding synchrony on extra-pair mating systems in songbirds. Behaviour 132: 675–690. Taborsky, M. 1994. Sneakers, satellites, and helpers: Parasitic and cooperative behavior in fish reproduction. Advances in the Study of Behavior 23: 1–100. Taborsky, M. 1998. Sperm competition in fish: ‘bourgeois’ males and parasitic spawning. Trends in Ecology and Evolution 13: 222–227. Taborsky, M., B. Hudde, and P. Wirtz. 1987. Reproductive behaviour and ecology of Symphodus (Crenilabrus) ocellatus, a European wrasse with four types of male behaviour. Behaviour 102: 82–118. Thompson, R. L. 1998. Steroid induced immunosuppression and alternative male reproductive strategies. PhD disseration. University of Texas, Austin, Texas. Wade, J. and A. P. Arnold. 2004. Sexual differentiation of the zebra finch song system. Annals of the New York Academy of Sciences 1016: 540–559. Westneat, D. F. and P. W. Sherman. 1997. Density and extra-pair fertilizations in birds: a comparative analysis. Behavioral Ecology and Sociobiology 41: 205–215. Wiegmann, D. D., J. R. Baylis, and M. H. Hoff. 1997. Male body size, fitness and age of first reproduction in smallmouth bass, Micropterus dolomieui . Ecology 78: 111–128. Wiegmann, D. D., L. M. Angeloni, J. R. Baylis, and S. P. Newman. 2004. Negative maternal or paternal effects on tactic inheritance under a conditional strategy. Evolution 58: 1530–1535.

Chapter 5

Early life history and recruitment D. R. DeVries, J. E. Garvey, and R. A. Wright

5.1 Introduction As with most fishes, high mortality occurs during early life in centrarchids (e.g., Beard 1982; see references in Siefert 1968; Parkos and Wahl 2002). Thus, early life represents an important period determining the size of individual year classes, as well as ecological interactions influencing each year class (Garvey et al . 2003). Factors that affect survival of individuals during early life determine recruitment and eventual population size. Given the economic and ecological importance of many members of the family Centrarchidae, factors leading to small changes in early survival and resulting adult populations have important implications for a wide array of fisheries in a diverse suite of systems, and thus have formed an important focus of considerable research. In this chapter, we review the diverse array of early life history and recruitment patterns demonstrated by the Centrarchidae. We begin by defining “early life” and “recruitment,” and then describe some of the general patterns of early life histories seen in this family (as well as the variation in those patterns), and conduct a meta-analysis of early life characteristics in the Centrarchidae, leading to some broad groupings within the family. We then explore recruitment in centrarchids, describing what is known about the influence of abiotic and biotic factors, and exploring the evidence for critical periods in the early life history of centrarchids. Finally, we identify where there are important gaps in our knowledge of this important group.

5.2 Definition of “early life history” and “recruitment” We use the term “early life history” to refer to a period of time, typically during the first year of life, when mortality is highest. However, this period may last beyond the first year of life into the juvenile and subadult stages (Figure 5.1). Because mortality is highest earliest in life and typically decreases exponentially thereafter, while other factors affecting mortality are often size related, it is difficult to explicitly define what is meant by “early life history” on a purely temporal scale, and our use of this term necessarily remains a bit ambiguous. Similarly, we refer to “recruitment” as survival through the early period of high, often uncertain, mortality to a later stage when mortality is relatively lower and more predictable (i.e. through this early life history period; Figure 5.1).

5.3 Variation in early life history across the centrarchids Based on available evidence, it appears that nearly all centrarchids spawn in nests (Breder 1936; Figure 5.1) and that their larvae remain in these shallow nesting areas and begin feeding on zooplankton. The lone exception is the Sacramento perch (Archoplites interruptus), which is described to school prior to and during spawning and does not build a nest, although the males do establish and guard a territory (Murphy 1948; Matthews 1965). However, beyond the nesting stage a single model of early life history will not fit all centrarchids. The larvae of some species remain in shallow littoral zones, while others migrate between littoral and deep-water areas. Some of those migrating to the limnetic zone remain there while others return to the littoral zone after a period of foraging. Some continue to feed on zooplankton, while some feed on macroinvertebrates, and still others become piscivorous. While these patterns certainly vary among species, variation also occurs within species, both among and within populations (see Chipps et al . 2004). Out of the 34 centrarchid 105

106

Centrarchid fishes

Inter-or IntraCohort interaction

Life stage transition Egg

Gu ard ing

Hatch

Embryo Swim-up exogenous feeding offshore migration

ing rd ua

G

rding Gua mp /co

Pred p /com Pred p /com Pred p /com

Larva Inshore migration foraging shift

Juvenile Comp/pred

Recruitment overwintering

Subadult Comp

Gonads mature

Adult Comp

Figure 5.1 Suite of potential interactions and life stage events common within populations of centrarchids. Cohort interactions (left-hand side)—Arrows depict the direction of the effect. The primary interaction between adults and egg/embryo stages revolves around nest excavation and parental guarding. In some species, adult guarding continues through the larval stage. If spatial overlap between adults and larvae occurs, as in some bluegill population, intercohort competition may occur as well. Adult interactions with juveniles and subadults can be both competitive and cannibalistic. Within juvenile piscivores, intracohort cannibalism occurs. Density-dependent competition is likely important within most free-swimming life stages. Life stage transitions (right-hand side)—Arrows depict the direction of the life stage transition through time. Fertilized eggs within nests become embryos upon hatching. The transition from embryos to larvae occurs when swimming, exogenous feeding begins, and perhaps a habitat shift occurs. Switching from larval to juvenile stages is often characterized by a major foraging and perhaps habitat shift. Juveniles become subadults, and thus recruitment occurs, when variance in expected mortality declines. In many species, recruitment occurs during winter. The transition from subadults to adults occurs when gonads mature. Comp = competition; pred = predation.

species, early life research efforts have largely focused on particular species with the greatest economic importance (e.g., see later). From our review of the available literature, there appear to be three broad groupings of early life history patterns, characterized by the black basses (Micropterus spp.), the crappies (Pomoxis spp.), and the sunfishes in the genus Lepomis. We consider these three generalized patterns here.

5.3.1 Micropterus spp. Although there are currently nine species described in the genus Micropterus, the factors influencing the early life history of only largemouth bass, Micropterus salmoides (along with the recently separated species, Florida bass Micropterus floridanus), and smallmouth bass, Micropterus dolomieu, have been investigated with a sufficient number of studies to

Early life history and recruitment

107

allow us some degree of generalization. Of these two species, largemouth bass are far more studied than smallmouth bass. Our summary presented later will focus primarily on the information for largemouth bass (including both northern and Florida bass) to characterize this group. Within the littoral zone, the peak spawning of largemouth bass occurs at 16 to 18◦ C, with hatching occurring within 3 to 4 days of spawning, depending on water temperature (Kramer and Smith 1962; Chew 1974; Heidinger 1976). After hatching, larvae remain schooled inshore under the protection of the nesting/breeding male for some time (e.g., Cooke et al . 2002; see also Cooke et al . 2003 and Steinhart et al . 2005b for examples and additional references concerning parental care in smallmouth bass). Larvae begin exogenous feeding on small zooplankton, and feed on progressively larger zooplankton as they grow and their gape size increases. Eventually, they switch to feed on littoral macroinvertebrates and fish, usually within the first or second year of life. The switch to piscivory depends on several factors including relative prey and predator sizes, prey species composition, density, and availability (e.g., Applegate and Mullan 1967; Pasch 1974; Miller and Storck 1984; Gutreuter and Anderson 1985; Keast and Eadie 1985; Phillips et al . 1995; Olson 1996a,b; Cailteux et al . 1996; Garvey et al . 2000; Post 2003). As subadults and adults, black basses typically feed on a combination of fish and large, mobile invertebrates such as crayfish (Decapoda), again depending on prey availability (see Chapter 6 on Population/Community Ecology). Black basses can become piscivorous very early in their ontogeny if vulnerable sized fish are present (Garvey and Stein 1998a). Smallmouth bass follow a relatively similar pattern, albeit spawning and hatching at slightly lower water temperatures (see references in Auer 1982). Relatively little is known about spotted bass (Micropterus punctatus) or other black bass early life patterns.

5.3.2 Lepomis spp. As with the black basses only a few species within the genus Lepomis have well-studied early life histories. The information in this genus is dominated by that for bluegill, Lepomis macrochirus. Bluegill, like other Lepomis spp. sunfishes, nest in littoral areas, often forming large nesting colonies (Gross and MacMillan 1981), and spawning across a wide temperature range (17–30◦ C; Tin 1982). As with largemouth bass, bluegill hatch and their embryos remain on the nest under the protection of the nesting male, until their yolk sac is almost absorbed (Beard 1982). Spawning can occur across a wide time period, particularly at southern latitudes (e.g., Partridge and DeVries 1999). However, unlike largemouth bass, larval bluegill and some other sunfishes often migrate from the littoral areas to the limnetic zone (Faber 1967; Werner 1967; Amundrud et al . 1974; Storck et al . 1978; Beard 1982; Dimond and Storck 1985; Werner and Hall 1988; but see Garvey et al . 2002a for an example where most larval bluegill remain near the littoral zone). Migrating fish remain in the limnetic zone for varying periods of time during their first growing season, feeding on zooplankton, after which they return to the littoral zone prior to their first winter (Werner 1967; Storck et al . 1978; Dimond and Storck 1985; Werner and Hall 1988). During this second time in the littoral zone, they feed on crustacean zooplankton and macroinvertebrates (e.g., Werner and Hall 1988 and references cited therein). Juvenile bluegill remain in the littoral zone until they achieve a length where their risk of predation is reduced, at which time they can occupy and feed in any chosen habitat (Werner and Hall 1988), typically thought to be that providing the most profitable benefit/cost ratio (where benefit is equal to energetic gain and cost is predation risk; Mittelbach 1981; Werner et al . 1983). In addition to these observations for larval bluegill, pumpkinseed (Lepomis gibbosus) and rock bass (Ambloplites rupestris) larvae may also migrate to the limnetic (Faber 1967; Amundrud et al . 1974; Keast 1980; Brown 1985). Pumpkinseed are thought to exhibit similar migration patterns as bluegill (i.e. eventually back to the littoral), while rock bass larvae (considered here with Lepomis spp. relative to this migratory behavior) are thought to remain near the substrate in the limnetic zone for up to 7 weeks, after which they return to the littoral zone as described earlier (Amundrud et al . 1974; Rettig 1998). However, such migrations are not universal among Lepomis spp., given that redear sunfish (Lepomis microlophus) may not migrate (Dimond and Storck 1985).

5.3.3 Pomoxis spp. Crappies nest in beds in littoral areas in the spring, spawning when water temperatures are 14 to 24◦ C (Tin 1982). The spawning male guards the nest until shortly after the larvae hatch. Larvae remain in the littoral area for some period

108

Centrarchid fishes

of time (i.e. through absorption of the yolk sac, approximately 4–10 days; Siefert 1968), after which they migrate to the limnetic zone where they feed on crustacean zooplankton (Faber 1967; Amundrud et al . 1974; Keast 1980; O’Brien et al . 1984). As they grow, the young crappie remain in the limnetic, although the specific habitat (benthic or pelagic) is not well understood. Juveniles feed on progressively larger zooplankton, and eventually begin to feed on larger invertebrates, ultimately including fishes in their diets as well (Siefert 1968; O’Brien et al . 1984; Pine and Allen 2001). Although eventually becoming piscivorous, crappies typically do so after their first year of life.

5.3.4 Other species Among the 34 species within the Centrarchidae (Kassler et al . 2002; Nelson et al . 2004; see also Chapter 1 on Phylogenetic Relationships and Genetics), the preceding descriptions of early life history patterns are limited to approximately eight species (and only four species in any level of detail). Clearly, data limitations concerning early life stages among the Centrarchidae influence our ability to generalize further. The spatial distribution of larvae and juveniles following departure from nests will likely fall along the continuum among black basses, Lepomis sunfish, and crappies, depending on the size-dependent degree of risk and benefit afforded by residing in littoral or offshore habitats.

5.4 Meta-analysis of life history data for several centrarchids Early life ecological interactions are likely determined by factors that affect development time, nesting time, spawning time, and body size of larvae. Trade-offs likely occur among adult body size, egg size, embryo development time, and other factors that influence parental investment in larval size during the switch to independent life. To determine whether any groupings occurred in centrarchids relative to these factors, we conducted a principal components analysis (PCA) including average egg diameter (mm), hatch size (mm standard length), temperature at first spawning (◦ C), maximum adult size (mm total length), and incubation time at first spawning (days) (Table 5.1). Data that we used were largely derived from reviews conducted by Auer (1982), Carlander (1977), and Scott and Crossman (1998) (Table 1). Complete data were available for the PCA for black crappie (Pomoxis nigromaculatus), white crappie (Pomoxis annularis), bluegill, green sunfish (Lepomis cyanellus), largemouth bass, longear sunfish (Lepomis megalotis), pumpkinseed, redbreast sunfish (Lepomis auritus), rock bass, smallmouth bass, and warmouth (Lepomis gulosus). The cross-products matrix used in the PCA contained correlation coefficients among the variables. Linear regression was used to explore relationships among variables in the PCA. The first two axes explained 88% of the variance in the data set (Table 5.2; Figure 5.2). Egg diameter, spawning temperature, adult maximum size, and incubation time were highly correlated with the first axis (Table 5.2). The two large-bodied piscivores, largemouth bass and smallmouth bass, largely separated on the left side of the ordination (long incubation, large adult, early spawning, and large eggs), whereas most other species aligned to the right (short incubation, small eggs, relatively small adult, and later spawning; Figure 5.2). Separation on the second axis was correlated strongly with larval hatching size (Table 5.2), with three species that fell out as intermediate along axis one separated on the second axis (redear sunfish, redbreast sunfish, rock bass) as having large larvae (Figure 5.2). Supporting the patterns suggested by the PCA, bivariate correlations revealed that temperature at first spawn and incubation time were negatively associated (Figure 5.3). Egg diameter and size at hatching were positively related (Figure 5.4). Species with large adults spawned at the coolest temperatures (Figure 5.5). In our view, the separation on the first axis appears to reflect a tactic of first-year piscivory. Species with an eventual large adult size and first-year piscivory spawn early and, probably due to their cool spawning temperatures, have longer incubation times. Although we expected that adult investment in size of larvae would be greatest in these piscivores (i.e. to allow them an early size advantage over their eventual prey), we were surprised to discover that they fell in an intermediate position along the second axis, which we interpreted to represent early body size. Two apparent tactics arose among the sunfish in the ordination. Those species with relatively small body sizes appeared to spawn at warm temperatures, with short incubation times. Warmouth and longear sunfish fell into this category. Conversely, another grouping of sunfish appeared with relatively large adults, large larvae, and early spawning, including rock bass and redbreast sunfish.

Early life history and recruitment

Table 5.1 Early life history data and primary and review literature sources used for linear regression and multivariate analyses of some common centrarchid species. Egg diameter (mm) was first averaged within and then among literature sources. Hatch time (days) is the time required for an egg to hatch at the earliest known spawning time. Temperature (◦ C) is the earliest known spawning temperature. Adult size (mm total length) is the maximum size averaged across the oldest adult within multiple populations. Incubation time (days) is the time for an egg to develop at earliest known spawning. Species Black crappie

Parameter Egg diameter

0.9

Merriner 1971a

2.3

Merriner 1971b

Adult size

Green sunfish

2.0

Merriner 1971b Meyer 1970

Hatch time

2.6

Auer 1982a

Temperature

17.2

Stevenson et al. 1969, Snow et al. 1970

Adult size

241.0

Carlander 1977a

Incubation time

3.0

Egg diameter

1.2

Meyer 1970

Hatch time

3.6

Taubert 1977

15.6

Hunter 1963

305.0

Meyer 1970, Claussen 1991

Carlander 1977a

Incubation time

3.0

Meyer 1970

Egg diameter

1.6

Meyer 1970, Merriner 1971a, Carlander 1977

Hatch time

3.0

Heidinger 1975

Adult size

16.0 554.0

Scott and Crossman 1998 Carlander 1977a

Incubation time

5.0

Curtis 1949

Egg diameter

1.0

Meyer 1970, Scott and Crossman 1998

Hatch time

2.8

Auer 1982a

21.4

Anjard 1974

Temperature Adult size Incubation time Egg diameter Hatch time Temperature Adult size Pumpkinseed

Carlander 1977a

1.2

Temperature

Orangespotted sunfish

Breder and Rosen 1966, Goodson 1966

Egg diameter

Adult size

Longear sunfish

17.4 390.0

Incubation time

Temperature

Largemouth bass

Sources

Hatch time Temperature

Bluegill

Value

178.0

Carlander 1977a

3.0

Scott and Crossman 1998

1.0

Barney and Anson 1922

N/A 18.4 137.0

Barney and Anson 1923 Carlander 1977a

Incubation time

5.0

Barney and Anson 1923

Egg diameter

1.0

Anjard 1974

Hatch time

2.8

Temperature

20.0

Anjard 1974, Taubert 1977 Miller 1963, Scott and Crossman 1998 (continued)

109

110

Centrarchid fishes

Table 5.1 (continued). Species

Parameter

Value

Adult size

274.0

Incubation time Redbreast sunfish

2.1

Buynak and Mohr 1978

4.9

Buynak and Mohr 1978

3.0

Buynak and Mohr 1978

1.5

Meyer 1970

Hatch time

5.0

Auer 1982a

306.0

Lopinot 1961 Carlander 1977a

3.0

Meyer 1970

Egg diameter

2.1

Powles et al. 1980

Hatch time

5.2

Powles et al. 1980

Adult size

15.6 216.0

Scott and Crossman 1998 Carlander 1977a

Incubation time

3.0

Breder 1936

Egg diameter

2.3

Tester 1930, Meyer 1970, Scott and Crossman 1998

Hatch time

4.6

Reighard 1906

Temperature Adult size

12.8 501.0

Scott and Crossman 1998 Carlander 1977a

Incubation time

6.0

Scott and Crossman 1998

Egg diameter

1.1

Larimore 1957, Merriner 1971b

Hatch time Temperature Adult size Incubation time

2.6

Larimore 1957

21.1

Merriner 1971b

274.0

Carlander 1977a

2.0

Merriner 1971b

Egg diameter

0.9

Hansen 1943, 1951

Hatch

1.9

Morgan 1954

Temperature Adult size Incubation time a Averages data from multiple sources.

Note: N/A = Not available

20.0

Incubation time

Temperature

White crappie

Buynak and Mohr 1978 Carlander 1977a

Egg diameter

Adult size

Warmouth

20.0 239.0

Incubation time

Temperature

Smallmouth bass

Breder 1936

Egg diameter

Adult size

Rock bass

Carlander 1977a

Hatch time Temperature

Redear sunfish

3.0

Sources

14.0 478.0 4.0

Scott and Crossman 1998 Carlander 1977a Siefert 1968

Early life history and recruitment

111

Table 5.2 Principal components analysis (PCA) results for 12 centrarchid taxa including black crappie, bluegill, green sunfish, white crappie, largemouth bass, longear sunfish, pumpkinseed, redbreast sunfish, redear sunfish, rock bass, smallmouth bass, and warmouth. Eigenvector Variable

PC axis 1

Kendall’s r

PC axis 2

PC axis 1

PC axis 2

Egg diameter

−0.43

0.51

−0.71

Hatch length

−0.27

0.66

−0.44

0.87

0.49

0.26

0.81

0.34

Max adult size

−0.43

−0.47

−0.71

−0.61

Incubation time

−0.56

−0.13

−0.91

−0.17

Spawn temperature

Large at hatch

3 RBR RBSS

2

RE

1 PC2

0.68

SMB

0

LE GS BG PS WM

-1 LMB -2 Small at hatch

Cumulative variance explained: 88%

BC WC

-3 -5

-4

-3

-2

-1

0

1

2

3

PC1 Large egg Cool spawn Large adults Long incubation

Small egg Warm spawn Small adults Short incubation

Figure 5.2 The first two axes from a principal components analysis (PCA) of factors thought to affect early life interactions in centrarchids. Data derived from reviews conducted by Auer (1982) and Carlander (1977). Variables loading high on PCA axes 1 or 2 are indicated at the ends of the axes. Abbreviations are, BC = black crappie, WC = white crappie, BG = bluegill, GS = green sunfish, LMB = largemouth bass, LE = longear sunfish, PS = pumpkinseed, RBR = redbreast sunfish, RBSS = rock bass, RE = redear, SMB = smallmouth bass, and WM = warmouth. Broken-stick eigenvalues for PC1 (2.66) and PC2 (1.73) were less than the actual eigenvectors (PC1 = 2.28, PC2 = 1.28), revealing that the PCA explained more information than expected by chance.

Although speculative, it appears that the three general tactics are related to piscivory and maximum adult body size. The first implies that piscivorous species spawn early in the season and have large adults. The two tactics in the typically nonpiscivorous sunfishes involve an apparent trade-off between the size of young produced and timing of spawning. For example, early spawning likely requires larger, precocial offspring to ensure survival during variable spring temperatures (Garvey et al . 2002a); adults of these species must be sufficiently large to make the necessary energetic reproductive investment in large offspring. Conversely, late-spawning sunfish have altricial larvae that can be produced by small adults; small initial larval size may be mitigated by faster development at warm temperatures (Garvey et al . 2002a). Fecundity data are lacking for most of these species, so the trade-offs among egg production, egg size, and adult

112

Centrarchid fishes

7

Incubation time (days)

6

5

4

3

2

1 12

14

16

18

20

22

Temperature at first spawn (οC)

Figure 5.3 Association between average temperature at first spawning (◦ C) and early incubation time (days) in black crappie, bluegill, green sunfish, white crappie, largemouth bass, longear sunfish, pumpkinseed, redbreast sunfish, redear sunfish, rock bass, smallmouth bass, warmouth, and orangespotted sunfish. R2 = 0.28, slope = −0.25, intercept = 7.95, p = 0.04.

5.5 5.0

Size at hatch (mm)

4.5 4.0 3.5 3.0 2.5 2.0 1.5 0.6

0.8

1.0

1.2

1.4

1.6

1.8

2.0

2.2

2.4

Egg diameter (mm)

Figure 5.4 Relationship between egg diameter (mm) and larval size at hatching (mm) for black crappie, bluegill, green sunfish, white crappie, largemouth bass, longear sunfish, pumpkinseed, redbreast sunfish, redear sunfish, rock bass, smallmouth bass, and warmouth. R2 = 0.71, slope = 2.0, intercept = 0.66, p = 0.0004.

size cannot be explored. Winemiller and Rose (1992) placed reproductive tactics among many diverse North American taxa into the context of the timing and duration of reproduction. Unfortunately, so little is known about the reproductive behavior of most centrarchids (e.g., whether spawning is protracted or punctuated) that it is impossible to determine the adaptive significance (if any) of these apparent tactics in this context. However, this analysis does suggest that the early life history of species at the extremes of the ordination such as smallmouth bass, white crappie, redbreast sunfish, and longear sunfish may provide interesting insight into the significance of adult investment, spawning timing, and offspring size on early life history interactions in centrarchids.

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Maximum adult size (mm total length)

600

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100 12

14

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ο

Temperature at first spawn ( C)

Figure 5.5 Relationship between average temperature at first spawning (◦ C) and maximum adult body size (mm total length) in black crappie, bluegill, green sunfish, white crappie, largemouth bass, longear sunfish, pumpkinseed, redbreast sunfish, redear sunfish, rock bass, smallmouth bass, warmouth, and orangespotted sunfish. R2 = 0.36, slope = −30, intercept = 844, p = 0.02.

5.5 Recruitment in the centrarchids We reviewed the literature to identify the factors that have been studied and noted as important for the survival (or factors related to survival) and eventual recruitment of species within the Centrarchidae. In the more than 200 papers from which we obtained information concerning factors affecting recruitment in centrarchids, a number of generalizable abiotic and biotic factors arose. We first consider the limited evidence for stock–recruitment relationships in centrarchids, after which we consider the direct influences of abiotic and biotic factors on centrarchid recruitment, and some examples of the potential interactions among these factors. Finally, we discuss some patterns from these publications relative to these factors across centrarchid species.

5.5.1 Stock–recruitment relationships The functional relationship between the density and size structure of the adult spawning stock and recruitment (i.e. yearclass strength) is important for understanding and predicting variation in populations, often affecting our ability to manage fish populations. However, although important from both theoretical and management perspectives, only rarely have such relationships been demonstrated in centrarchids. For example, largemouth bass and smallmouth bass populations in most systems do not show a significant relationship between adult densities and the recruits they produce (Garvey et al . 2002a; Parkos and Wahl 2002; Shuter and Ridgway 2002), although in systems with abundant largemouth bass, cannibalism (both by adults and previous cohorts within the same year class) may limit recruitment of juveniles (Post et al . 1998). For crappies, recruitment varies greatly, which is typically related to environmental conditions independent of adult density (Beam 1983; Dubuc and DeVries 2002; Sammons et al . 2002; Maceina 2003). However, one recent study, Bunnell et al . (2006), found that models including functions for both adult density and chlorophyll concentration generated the best predictors of recruitment of combined white crappie and black crappie in 11 Ohio reservoirs. Recruitment success is often related to adult size structure (c.f., adult abundance) in several species of centrarchids, including Lepomis spp. (Aday et al . 2002; Garvey et al . 2002a; Knuth 2006), smallmouth bass (Baylis et al . 1993), and

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largemouth bass (Miranda and Muncy 1987; Goodgame and Miranda 1993), with large adults producing larvae earlier than small counterparts, often leading to proportionally more juveniles and juveniles with greater recruitment probability. However, this process may be more complex than once thought, depending on stage-dependent patterns of growth and survival. Knuth (2006) found that the high densities of sunfish larvae produced in lakes with proportionally more large adult sunfish led to poor density-dependent larval growth and high larval mortality. Although scarce by fall, the surviving juveniles in these lakes were released from density-dependent competition, grew rapidly, and thus successfully recruited, maintaining the large adults in the population. In general, it appears that recruitment in centrarchids is rarely limited by the abundances of adult spawning stock that typically occur. Adult size structure may be more important than abundance by affecting the timing and duration of spawning, thereby strongly influencing patterns of larval and juvenile growth and survival. As a consequence, research has focused on those biotic and abiotic factors that affect the growth and survival of centrarchid early life stages (as reviewed later).

5.5.2 Abiotic factors 5.5.2.1 Temperature It is clear that temperature can be important for recruitment in centrarchids, as is the case with most fishes, during at least three time periods. First is during the incubation period, which determines how long eggs remain in the nest before they hatch, and how much yolk they contain upon hatching (i.e. how long they can maintain endogenous feeding). Second is the temperature during the growing season, which controls the entire energetics of the fish, and eventually the balance between consumption and growth. Finally, is the temperature during the first overwinter period, which can influence growth and survival. Temperature likely controls when young of various centrarchid species are present, given the differences among species in spawning temperatures (see e.g., Mettee et al . 1996; Boschung et al . 2004). For example, although it may be the leaststudied centrarchid, the mud sunfish (Acantharchus pomotis) is distributed across a broad area of the Atlantic coast from New York to Florida. It is likely the earliest spawning centrarchid, with evidence from one study indicating spawning at 6 to 10◦ C (Pardue 1993), which likely puts their larvae into a different environment or set of environmental circumstances (and potentially allowing them to exploit other habitats) than other centrarchids, which typically spawn at higher temperatures and later times. Variation in spawning time occurs within species as well. Largemouth bass spawn at different times, with individuals that hatch earlier typically having an advantage in growth and survival compared to later-spawned individuals (Miller and Storck 1984; Miranda and Muncy 1987; Goodgame and Miranda 1993; Ludsin and DeVries 1997). However, for crappie, early hatching sometimes leads to increased mortality (Pine and Allen 2001). For bluegill and pumpkinseed, variation in hatch date has led to different conclusions, with some studies showing early hatching to be best (Beard 1982; Cargnelli and Gross 1996), and others finding later-hatched fish to have better recruitment (Garvey et al . 2002a; Santucci and Wahl 2003). In largemouth bass, early hatched fish have been found to experience better recruitment (Phillips et al . 1995), although for these eventual piscivores, the relative timing of their spawning versus their eventual prey may be more important than the actual spawning time itself (Pasch 1974; Miller and Storck 1984; Adams and DeAngelis 1987; Ludsin and DeVries 1997; Garvey et al . 2002b). Changes in temperature also can affect centrarchid early life stages, such as the reduced swimming ability of smallmouth bass fry due to a sharp temperature drop (Larimore and Duever 1968). Several studies have documented increased recruitment with increased temperatures (measured at various times, including before and during spawning, and during the growing season), likely related to increased growth rates or earlier hatch date, although it is not always clear what life stages are affected (e.g., crappie, Siefert 1968; Pope and Willis 1998; Pine and Allen 2001; smallmouth bass, Fry and Watt 1955; Clady 1975). Finally, temperature during the first winter has been suggested to be important for recruitment in a number of centrarchids, including bluegill, green sunfish, white crappie (P. annularis), smallmouth bass, and largemouth bass (Aggus and Elliott 1975; Toneys and Coble 1979; Oliver et al . 1979; Gutreuter and Anderson 1985; Miranda and Hubbard 1994a; Ludsin and DeVries 1997; Garvey et al . 1998a; Wright et al . 1999; Fullerton et al . 2000; McCollum et al . 2003; see recent reviews in Garvey et al . 2002a,b; Parkos and Wahl 2002). The overall conclusion from these studies of overwinter

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mortality appears to be that fishes that are larger as they enter their first winter are more likely to survive through their first winter than their smaller counterparts, and that these differences are due to diet differences during their first year of life, and the subsequent lipid stores that fish have accumulated during their first growing season (Ludsin and DeVries 1997; Garvey et al . 2002b). However, while these relationships are relatively clear for black basses, they are not as clear for Lepomis spp., perhaps influenced by both body size and population density (Bernard and Fox 1997). Temperature, growth, and size during winter may interact with biotic factors such as predation to further influence recruitment strength (Garvey et al . 2004). Temperatures vary substantially across the range of many centrarchid species, potentially affecting patterns of growth and survival during early life. For juvenile largemouth bass, origin affected growth and survival during simulated experimental winters (Fullerton et al . 2000), with most young fish from southern (Alabama) US latitudes being unable to survive under simulated northern (Wisconsin) winter conditions. Fish from the northern latitude grew more on the same ration during winter than southern counterparts (Fullerton et al . 2000). The temperature-dependent length of the growing season also may affect the first-year size of largemouth bass in the fall, with individuals being smaller on average at northern latitudes (Garvey et al . 2003). Understanding how the influence of temperature varies along broad environmental gradients is likely the key for understanding the population dynamics and ultimately community interactions of centrarchids.

5.5.2.2 Dissolved oxygen As has been shown with other species, low dissolved oxygen (DO) concentrations have a negative effect on behavior, growth, and survival of several centrarchid species. Fontenot et al . (2001) found that larval centrarchids were not present in hypoxic limnetic areas in the Atchafalaya River Basin, Louisiana, until the DO concentration rose to 2.0 mg l−1 . They speculated that these larvae remained in oxygenated littoral areas and only migrated into the limnetic when the DO concentration was suitable. For largemouth bass, hatching, first feeding, and larval growth all were negatively affected by low DO concentrations (Carlson and Siefert 1974; Dudley and Eipper 1975), and in smallmouth bass, Siefert et al . (1974) found that while fish hatched, they were too weak to swim up at low DO concentrations. These results suggest that the primary effects of low DO concentrations are on the earliest life stages. Furmisky et al . (2003) found a marked difference in blood oxygen content of adult largemouth bass versus smallmouth bass under hypoxia, with smallmouth bass being more sensitive to hypoxia than largemouth bass. These differences in tolerance likely occur among early life stages of these taxa as well, suggesting that, along a gradient of oxygen conditions, centrarchid assemblages may be shaped by their relative DO tolerances. Clearly low DO concentrations can have a negative effect on centrarchid early life stages, and ultimately on recruitment.

5.5.2.3 Turbidity and wind Although they can have distinct effects, turbidity and wind are often correlated, particularly in their effects on recruitment. For example, Mitzner (1987, 1991) found that larval crappie abundance was negatively affected by wind and that up to 50% of the variability in larval crappie abundance was explained by turbidity. Similarly, Kramer and Smith (1960, 1962) found wind to be the most important single factor affecting largemouth bass year-class strength via nest destruction and Popiel et al . (1996) found that nest success in pumpkinseed was affected by the turbulence caused by wind in two lakes. However, Pope et al . (1996) found a positive relationship between age-0 black crappie CPUE and wind speed, which they suggested to be due to the negative effects of wind on a potential competitor (yellow perch, Perca flavescens). The influence of turbidity may be more complex due to interactions with light intensity. In larval bluegill there was a strong negative relationship between turbidity and consumption at low light intensities, while a positive relationship occurred at higher light intensities (Miner and Stein 1993). The often negative influence of wind and turbidity appears to be exerted across life stages, although the most dramatic effects may be at the vulnerable early life stages, including the nesting stage of centrarchids.

5.5.2.4 Habitat structure and vegetation Although habitat structure and vegetation influence young fish feeding rates, prey availability, and predation risk, their role in affecting recruitment is less well defined. Crowder and Cooper (1979, 1982) showed that foraging efficiency and

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prey availability, which vary in contrast to one another with macrophyte density, predicted maximum predator feeding rates at intermediate macrophyte density (see also Wiley et al . 1984), although fish condition may not be negatively affected until extremely high macrophyte densities are present (Colle and Shireman 1980). Foraging ability of piscivores also declines with plant density such that predation risk to young Lepomis spp. declines with increasing macrophyte density (Mittelbach 1981; Savino and Stein 1982; Werner et al . 1983; Werner and Hall 1988). However, even in systems without vegetation, DeVries (1990) found bluegill to use shallow littoral areas as a refuge from predation. In addition to plant density, macrophyte architecture can be an important determinant, with different effects of gaps or open areas within the macrophytes (Savino and Stein 1989a,b; Dibble and Harrel 1997; Valley and Bremigan 2002). Juvenile largemouth bass become piscivorous earlier at lower vegetation densities (Bettoli et al . 1992; Cailteux et al . 1996), and may experience increased oversummer (Moxley and Langford 1982) and overwinter (Miranda and Pugh 1997) survival at higher vegetation densities. These conflicting influences of vegetation for juvenile largemouth bass (i.e. decreased risk of predation and decreased ability to capture prey both associated with increased vegetation abundance) likely represent a complex role of vegetation for largemouth bass recruitment. A similar importance of substrate (i.e. cobble versus vegetation) was found to determine relative feeding rate and predation risk for juvenile smallmouth bass and juvenile largemouth bass (Olson et al . 2003). To make the issue more complex, habitat structure that helps to reduce predation risk for small centrarchids also crowds them into these lower-risk habitats, increasing the risk of nest predation (e.g., Hunt et al . 2002). Clearly, mortality as affected by vulnerability and availability to piscivores can dramatically influence recruitment; habitat structure appears to be important both for survival on the nests, as well as later in life (i.e. during the juvenile stages) for these centrarchids. There remains a trade-off between the effects of vegetation on predation risk and the ability to capture prey.

5.5.2.5 Salinity Given the wide distribution and physiological tolerances of centrarchids, they commonly occur in coastal areas, and thus can be exposed to variations in salinity. Some centrarchids can be present in salinity up to 10 ppt (Peterson and Ross 1991), and in fact, salinity up to 10 ppt did not affect juvenile bluegill growth (Musselman et al . 1995). Juvenile bluegill did not exhibit any strong preference for salinity (Peterson et al . 1993), although their swimming speed increased with increasing salinity, and they may actually use small fluctuations in salinity as a directional cue (Peterson et al . 1987). In fact, a salinity of 2 to 4 ppt was metabolically less costly than either freshwater or higher salinities (8 ppt; Peterson et al . 1987). Largemouth bass young-of-year preferred a salinity of 0 ppt when given a choice, although they did not move away from increased salinity in the field (Meador and Kelso 1989). Several studies have shown reduced survival of youngof-year largemouth bass when exposed to increased salinity (Renfro 1959; Tebo and McCoy 1964; Susanto and Peterson 1996). Peterson et al . (1993) suggested that largemouth bass is physiologically less able to tolerate increased salinity than is bluegill. While Tebo and McCoy’s (1964) work was with eggs and fry, the other studies have been limited to older and larger young-of-year fishes, suggesting that salinity effects may provide a continuing influence through growth and development. In a relatively comprehensive study of the first year of life in a coastal largemouth bass population, Peer et al . (2006) found that first-year growth was faster at brackish sites than at freshwater sites, due to a greater degree of piscivory in brackish sites, suggesting that advantages of fish prey availability may outweigh any negative effects of osmoregulatory costs. Coastal areas where salinity varies represent a dynamic environment in which centrarchids regularly occur and can be abundant, although no clear patterns exist relative to the overall influence of salinity on early life and recruitment.

5.5.2.6 Floods The primary influence of floods on centrarchids appears to be to destroy nests and displace fry downstream. Negative effects have been documented for centrarchids in general (Surber 1939), green sunfish and longear sunfish (Harvey 1987), and smallmouth bass (Surber 1939; Larimore 1975; Winemiller and Taylor 1982). In contrast, high spring floods have been shown to be positively correlated with strong year classes in largemouth bass, presumably due to the increased nesting habitat provided in the floodplain (Raibley et al . 1997). The effects of floods on centrarchids appear to be directed at the nesting and early life stages across species, yielding both positive and negative effects depending on where the effects are expressed (e.g., floodplain versus main channel).

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5.5.2.7 Hydrology and precipitation Closely related to flooding is the influence of hydrology on centrarchid recruitment. While increased flow during nesting has been shown to be negative to nesting success of rock bass, redbreast sunfish, and longear sunfish (Noltie and Keenleyside 1986; Andress 2002), orangespotted sunfish (Lepomis humilis) and green sunfish were found to be more abundant in years with higher water levels (Martin et al . 1981). For crappie, although the mechanisms remain unclear, there appears to be a relatively strong relationship between winter and post-winter water levels and year-class strength (Mitzner 1981; Martin et al . 1981; Maceina and Stimpert 1998; Sammons et al . 2002; Maceina 2003; but see Pope et al . 1996 for an example of a negative relationship between precipitation and age-0 catch-per-unit-effort). For smallmouth bass, low water levels appear to be good for year-class production, as the strongest year class was produced during a drought (Funk and Fleener 1974). The influence of hydrology on largemouth bass recruitment appears more variable, with studies documenting a positive influence of stable water levels (Garvey et al . 2000), dry post-hatch period (Maceina and Bettoli 1998), and higher water levels (Martin et al . 1981). In a Montana reservoir, flow was important, but only as related to spring runoff and its effects on water temperature as a control on spawning time (Saffel 2003). While it is not clear at what life stage(s) the influence of hydrology and water levels is being expressed across the Centrarchidae, there is no question that hydrology and water level is important for centrarchid recruitment. However, note that all but one of the studies cited earlier were conducted in reservoirs, with the only one noting a negative relationship between precipitation and abundance being conducted in a natural lake (Pope et al . 1996). Based on our review of the literature, we suggest the following conceptual model for the influence of hydrology on growth and abundance of centrarchids, particularly as related to largemouth bass and common Lepomis species (Figure 5.6). We consider the influence of discharge on fish in systems with two different hydrological patterns: systems that have dramatic variation in flow (i.e. “flashy”) and those with less variable flows where changes between high and low flows are more subtle. In systems with low variation in discharge, or more gradual rises and declines in flow, we expect that the availability of nesting areas (e.g., in the floodplain) will influence centrarchid density and growth such that both density

Density

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Discharge Figure 5.6 Conceptual model of the influence of hydrology on centrarchid density (left panels) and growth (right panels). The top panels represent expected relationships between both density and growth versus discharge for systems that experience relatively low variation in discharge from low- to high-flow events (i.e. systems with a gradual rise and fall). The bottom panels represent expected relationships between both density and growth versus discharge for ‘‘flashy’’ systems that experience high variability in discharge between low- and high-flow events.

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and growth are positively related to discharge. Increased flow leads to increased availability of nesting sites and areas in which to forage. In contrast, for flashy systems with a greater variation in discharge, we expect that density will be negatively related to discharge, as the influence of the high discharge events themselves will limit recruitment and hence density (likely a curvilinear relationship, governed by the dramatic forces of flow). Growth in this case will be density dependent. While this model may not reflect all of the patterns observed for centrarchids, we believe that it represents a model that can be tested in future work. It is clear that these patterns apply for systems such as reservoirs or lotic systems, and hydrology may not influence centrarchids in natural lakes as much. In addition, while hydrology has been shown to be important for crappie recruitment, our lack of understanding of the limnetic larval stage of crappie clearly leaves us without a mechanistic understanding of any hydrological influences.

5.5.3 Biotic factors 5.5.3.1 Horizontal migration It has been well established that at least some larval bluegill migrate from the littoral to the limnetic at some point after hatching and schooling dispersal (Faber 1967; Werner 1967, 1969; Storck et al . 1978; Keast 1980; Beard 1982; Werner and Hall 1988; Rettig 1998). In addition to bluegill, larval pumpkinseed and larval green sunfish have also been shown to exhibit this offshore migration (Keast 1980; Rettig 1998) as well as larval crappie (Nelson et al . 1967; Siefert 1968; Keast 1980). However, while this has generally been accepted as the normal early life habitat use pattern, not all larval bluegill migrate, with some remaining in the littoral zone (Werner 1967, 1969; Garvey et al . 2002). In addition, work with longear sunfish and redear sunfish have shown that their larvae remain in the littoral zone and do not migrate to the limnetic (Boyer 1967; Dimond and Storck 1985). Largemouth bass do not exhibit any such offshore migration (e.g., Hirst and DeVries 1994). While larval bluegill, pumpkinseed, and green sunfish move back to the littoral zone at a time and/or fish size that is not clearly understood, crappie remain in the limnetic zone and do not return to the littoral. Why such spatial partitioning occurs among species as well as between life stages within species is speculative, but is likely related to avoidance of intraspecific resource overlap, intracohort cannibalism, or piscivory. Currently the influence of migration to recruitment is not known. Life in the limnetic zone carries different costs and benefits than does life in the littoral zone, likely differentially affecting recruitment among species and life stages.

5.5.3.2 Intraspecific competition/density dependence Competition has been suggested to be an important influence on centrarchid recruitment at several different points during the first year of life. Relative to intraspecific interactions, both inter- and intracohort interactions are common. For a number of centrarchids, the availability of zooplankton appears to be limiting during the larval and early juvenile stages, with a positive relationship between larval bluegill growth and zooplankton density (Dai 1997; Welker et al . 1994; Claramunt and Wahl 2000) and negative relationship between bluegill density and zooplankton density (Partridge and DeVries 1999; Rettig 2003). Poor growth of juvenile sunfishes also occurs when they are forced into vegetated habitats to avoid predation (Mittelbach 1984; Osenberg et al . 1988; Breck 1993; Welker et al . 1994; Olson et al . 1995; but see Werner et al . 1996). Intracohort competition also is likely to occur when spatial overlap occurs between life stages that rely on similar resources. For example, Rettig and Mittelbach (2002) conducted experiments with bluegill demonstrating competition for zooplankton between limnetic larvae and adults. This pattern may be similar in many centrarchids with multiple life stages that forage on similar-sized zooplankton. Similarly, crappie larvae and zooplankton are linked (Siefert 1968; O’Brien et al . 1984; DeVries et al . 1998; Claramunt and Wahl 2000; Pine and Allen 2001), with first-year growth strongly related to zooplankton abundance (Lemly and Dimmick 1982; Bunnell et al . 2003) although larval crappie density is not necessarily related to system productivity (Dubuc and DeVries 2002; see Hoxmeier and DeVries 1998 for an example of a negative relationship between system productivity and larval crappie density). For young largemouth bass in Ohio reservoirs, dense, strong year classes led to small fall lengths relative to poor year classes (Garvey et al . 2000), although this is not always the case (e.g., 1994 results in Post et al . 1997).

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5.5.3.3 Interspecific competition Because centrarchids are often the dominant fish resident of small lakes and streams, they are likely to compete between species as well as within populations. Given the importance of zooplankton during the larval stage, larval bluegill are likely to compete with other planktivores at this time. In fact, larval bluegill have been shown to compete with larval gizzard shad and larval threadfin shad in midwestern impoundments during the time when they co-occur in the limnetic zone (DeVries et al . 1991; DeVries and Stein 1992; Stein et al . 1995; Garvey et al . 1998b), with the magnitude of the competitive effect dependent on the relative timing of spawning and appearance in the limnetic zone of these species (Garvey and Stein 1998b). However, such competitive interactions are not always expressed, as has been shown in southern systems where larval bluegill densities are often greater than larval shad densities (Kim and DeVries 2000; Irwin et al . 2003; Watson et al . 2003; Michaletz and Bonneau 2005). Interactions similar to those for larval bluegill would be expected to occur between larval crappie and other zooplanktivores, given their migration to the limnetic zone after hatching. In fact, negative interactions have been quantified between larval crappie and larval shad (Guest et al . 1990), although competition with larval shad is not always the case (e.g., Pope and DeVries 1994), likely due to variation in the relative timing of crappie and shad spawning, both of whom spawn relatively early in the spring. Little work has dealt with competition in larval largemouth bass; in one study there was no evidence of direct competition between larval largemouth bass and larval gizzard shad (Hirst and DeVries 1994). Although zooplanktivorous for a short period of time, larval largemouth bass switch relatively rapidly to larger prey (e.g., Chew 1974). Some evidence suggests that zooplankton composition is important for largemouth bass survival (Lemly and Dimmick 1982), although much more attention has been given to the importance of when juvenile largemouth bass transition to a piscivorous diet (Timmons et al . 1980; Janssen 1992; Phillips et al . 1995; Olson 1996a,b; Ludsin and DeVries 1997; Allen et al . 1999; Micucci et al . 2003). The only evidence for competition at this stage is a negative effect of competition with juvenile bluegill, where juvenile largemouth bass were negatively affected by juvenile bluegill more than juvenile largemouth bass affected juvenile bluegill (Gilliam 1982; Olson et al . 1995; Brenden and Murphy 2004). Given the potential widespread nature of the size-structured interactions described earlier (both intraspecific and interspecific), the relative abundance of cohorts, as well as the relative contributions of cohorts to year-class strength will dramatically affect centrarchid population dynamics.

5.5.3.4 Predation Predation can potentially affect all early life stages in centrarchids. Nest predation can influence eggs and small larvae and can be due to both other fishes (e.g., Steinhart et al . 2004, 2005a) and other benthic organisms (e.g., crayfish: Dorn and Mittelbach 2004). Predation on larval fishes is difficult to detect, given the small body size and rapid digestion of larvae (Crowder 1980; Bowen 1996; Kim and DeVries 2001). In fact, Kim and DeVries (2001) found that stomach content analysis of adult fishes was insufficient for quantifying predation rates on larval bluegill in southern US systems, and that experimental approaches may be required. In a field experiment, Rettig and Mittelbach (2002) suggested that cannibalism by older bluegill was responsible for reduced larval bluegill survival at the highest adult bluegill density. In the littoral zone, Hydra have been shown to be a potential source of high mortality for larval bluegill, at least when reaching high densities (Elliott et al . 1997). Intracohort cannibalism may be important for littoral age-0 largemouth bass during summer (DeAngelis et al . 1980; Johnson and Post 1996) and winter (Miranda and Hubbard 1994b; Garvey et al . 2004). Once migrating to the limnetic, larval Lepomis spp. and crappie are vulnerable to adult fishes (e.g., bluegill and crappie), with potentially high mortality rates occurring at this stage (Kim and DeVries 2001). Predation has been shown to have important consequences for juvenile Lepomis spp., although not necessarily directly related to survival (but see Santucci and Wahl 2003). After spending some time in the limnetic, juvenile bluegill migrate back to the littoral zone, where they stay for varying lengths of time, depending on system-specific predation risk (Werner and Hall 1988). It is clear that predation on age-0 bluegill is a potentially important source of mortality (Werner et al . 1983; Werner and Hall 1988), although this risk is typically mediated by choice of less risky habitats by juvenile bluegill (Savino and Stein 1982; Gotceitas and Colgan 1987, 1990; DeVries 1990; Gotceitas 1990). Because they are selecting habitats based primarily on predation risk at this point in their life history, juveniles of several centrarchid species combine in

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the littoral, leading to competition among them (Mittelbach 1984, 1988). It is this predatory control of juvenile bluegill that is central to the management of largemouth bass and bluegill in small impoundments (Swingle 1950). Predation can obviously have important negative consequences for recruitment; however, while these are difficult to document for larvae, they are well established for juvenile centrarchids.

5.5.4 Combination of abiotic and biotic factors We expect that in most cases recruitment is not set by a single factor or a single class of factors (i.e. by abiotic or by biotic factors only). Here we consider three examples of centrarchids whose early life and recruitment patterns are perhaps the best studied among freshwater fishes. (1) In a multi-lake study in Illinois, Claramunt and Wahl (2000) quantified among-lake variation in growth rates of larval crappies and larval bluegill. Interestingly, they found that biotic variables (e.g., zooplankton abundance, larval fish density) explained more variation in larval bluegill growth rates than in larval crappie growth rates (c.f., results in the following section). Factors important for larval crappie growth rates included percent littoral volume, water temperature, and zooplankton, while for bluegill the important factors were reservoir surface area, conductivity, zooplankton, and larval fish density. Similarly, Allen and Miranda (2001) found that a combination of environmental variability and density dependence (i.e. biotic factors, possibly including cannibalism, Thompson 1941) produced quasi-cycles in crappie populations that were similar to the cyclic production of strong year classes seen every 2 to 5 years. Clearly, a combination of abiotic and biotic factors is important in determining larval fish growth rates and eventual year-class strength, and the relative importance of these factors likely differs among centrarchids. (2) Bluegill, gizzard shad, and largemouth bass interact in complex ways that directly influence recruitment of bluegill and eventually that of largemouth bass as well (Stein et al . 1995). Interactions include habitat overlap/segregation, and size-structured competition and predation, and are influenced by water temperatures (e.g., through its effect on relative timing of appearance of their larvae). Larval bluegill and gizzard shad can compete for zooplankton once they move to the limnetic (DeVries and Stein 1992; Garvey and Stein 1998b). While there is a weak negative relationship between the abundance of limnetic larval gizzard shad and limnetic larval bluegill, there is a strong negative relationship between the abundance of limnetic larval gizzard shad and the abundance of bluegill returning to the littoral zone (Garvey et al . 1998b; Garvey and Stein 1998b). This reduced abundance of littoral age-0 bluegill limits their availability as prey for piscivores, including age-0 largemouth bass. (3) The process of recruitment in largemouth bass is perhaps better studied than that in any other centrarchid, with studies having been conducted in the diverse systems where they occur (e.g., farm ponds, streams, reservoirs, lakes, and low salinity estuaries). Consistently across all of these system types, recruitment in largemouth bass is size dependent (Parkos and Wahl 2002; Garvey et al . 2003). As a gape-limited predator even small increases in size can result in dramatic increases in food availability and ultimately growth (Davies et al . 1982; Hambright 1991). Fastergrowing individuals become less vulnerable to predators and can accumulate sufficient energy stores, reducing the mortality associated with periods of starvation (e.g., the first overwinter period), particularly at latitudes with extreme winters (Ludsin and DeVries 1997; Fullerton et al . 2000). This size dependency interacts with biotic and abiotic factors through the effects of temperature on growth and the onset and duration of spawning for both largemouth bass and fish species that could eventually become their prey (Gilliam 1982; Adams and DeAngelis 1987). Timing of hatch of largemouth bass larvae could determine if the juveniles could reach the appropriate size to make a transition to piscivory. The nature of this complex interaction becomes clear when one explores a typical foodweb of dominant warmwater species found in a midwestern or southeastern US reservoir (e.g., Figure 2 in Garvey et al . 2002b). As juvenile largemouth bass in these systems grow, they may become piscivorous, often feeding on juvenile bluegill or gizzard shad. If competition occurs between gizzard shad and bluegill (as described earlier), fewer juvenile bluegill will return to the littoral zone as potential prey for juvenile largemouth bass. Further, when gizzard shad spawn early relative to largemouth bass, they may also be unavailable as prey (Adams and DeAngelis 1987), leading to reduced growth and survival of juvenile largemouth bass. Alternatively, if largemouth bass spawn early enough relative to

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gizzard shad or if gizzard shad grow slowly, then juvenile bass may be able to feed on gizzard shad during the first year of life, grow rapidly, and enjoy good survival. Clearly, the complex interactions described earlier are strongly influenced by the differential influence of increasing temperature and day length in the spring on the timing of spawning and the productivity of the ecosystem. In addition, given the widespread distribution of largemouth bass and bluegill (as their primary prey), the predator–prey interaction between their age-0 can be influenced heavily by temperature. In fact, Garvey et al . (2003) found that first-year growth of bluegill did not vary across latitudes while that of largemouth bass declined with latitude, further complicating the nature of these size-dependent competitive and predator–prey interactions between them. Clearly, a diverse and complex suite of factors and interactions ultimately controls interactions between bluegill and largemouth bass.

5.6 Some general findings from the literature review In our review of the literature concerning early life history and recruitment in the Centrarchidae, for each paper we identified what species was/were being studied, and whether the study was related to abiotic factors, biotic factors, or both. Of the 201 papers that we reviewed, 35% dealt with studies of largemouth bass, 25% dealt with studies of bluegill, 14% dealt with crappie, 12% dealt with smallmouth bass, and the other 14% dealt with the remaining centrarchid species. Within largemouth bass, roughly half of the studies dealt with abiotic and biotic factors (abiotic = 55%, biotic = 45%), while for bluegill, 89% dealt with biotic factors with only 11% dealing with abiotic factors. For crappie, 68% dealt with abiotic factors, while for smallmouth bass 50% dealt with abiotic and biotic factors. These results were significantly different from those expected based on a χ 2 contingency table analysis (χ 2 = 35.11, P < 0.005, df = 3), with most of the difference due to an overrepresentation of studies of biotic factors for bluegill and of abiotic factors for crappie.

5.7 Search for critical periods Although much early research in fish recruitment dealt with the search for a critical period (Hjort 1914), more recent work, particularly in freshwater systems where fish larvae are typically larger than in marine systems, has focused on interrelated factors affecting fishes across a number of early life stages (e.g., Ludsin and DeVries 1997; Parkos and Wahl 2002; Garvey et al . 2002b). We use a similar approach here to explore what is known about potential critical periods or bottlenecks for the Centrarchidae based on our review of the literature (Table 5.3; Figure 5.1). For largemouth bass,

Table 5.3 Suggested indication of the potential importance of factors or periods influencing recruitment and eventual year-class strength in four groups of centrarchids. An ‘‘X’’ indicates that evidence supports the importance of the factor or period, while a ‘‘???’’ indicates that the evidence for the importance of the factor or period is unclear or not compelling, and a ‘‘–’’ indicates that the particular factor or period is not important for recruitment or does not apply to that species. Largemouth bass

Smallmouth bass

Bluegill

Crappie

Spawning

X

X

X

X

Hatch date

X

???

X

X

Offshore migration

–

–

X

X ???

Limnetic residence

–

–

X

Littoral migration

–

–

???

–

Transition to piscivory

X

???

–

???

First winter

X

X

X

???

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most of the literature suggesting any critical period indicates survival through the first winter as the most important bottleneck [Toneys and Coble 1979; Miranda and Hubbard 1994a,b; Garvey et al . 1998a; Post et al . 1998; Wright et al . 1999; Fullerton et al . 2000; Brenden and Murphy 2004; see also Oliver et al . (1979) and Shuter et al . (1980) for smallmouth bass], with some evidence of the importance of hatch date, physical conditions at spawning, and the transition to a piscivorous diet (Wicker and Johnson 1987; Trebitz 1991; Ludsin and DeVries 1997; Post 2003). For bluegill and other Lepomis spp. there is evidence of important bottlenecks potentially occurring at dispersion (Toetz 1966), during the larval stage (Partridge and DeVries 1999), and during the first winter period (Toneys and Coble 1979; Santucci and Wahl 2003). However, there is no clear consensus for the general importance of any of these periods for eventual bluegill recruitment. Finally, for crappies, the spawning period appears important, given the important role of hydrology in determining crappie year-class strength (see earlier), as well as the larval stage in general (Pope and Willis 1998) and the first winter period (Toneys and Coble 1979). Although little information exists concerning the period when age-0 crappie occur limnetic (but see Pine and Allen 2001), there is some evidence that recruitment is set by the time larval crappie are present (McDonough and Buchanan 1991; Sammons and Bettoli 1998; but see Slipke et al . 1998 for an example where the critical period may be during the first summer of life). As with Lepomis spp., there does not appear to be any general consensus as to what early life periods might be most important for crappie recruitment.

5.8 Evidence for broad groupings within the Centrarchidae At the outset of this chapter, we described three broad groups of centrarchids based on our understanding of their early life. Here we present three additional pieces of evidence supporting that these groupings are important for the overall understanding of early life and recruitment within the Centrarchidae. First, as described earlier, we used a PCA to analyze relatively fixed characteristics (i.e. temperature at spawning, egg size, adult body size, etc.), with the results suggesting groupings among species within the Centrarchidae. Those groups were (i) those becoming piscivorous in their first year of life (e.g., Micropterus spp.), (ii) those becoming piscivorous in their second year of life (e.g., Pomoxis spp.), and (iii) sporadic piscivores (e.g., Lepomis spp.) (see Figure 5.2). Second, although little work has examined behavior of centrarchid early life stages, some evidence of differences among species does exist. Brown (1985), Brown and Colgan (1984, 1985a, b), and Sabo et al . (1996) quantified behavior of largemouth bass, smallmouth bass, rock bass, bluegill, pumpkinseed, and black crappie, and found that behavioral differences existed among species becoming piscivorous as age-0 (largemouth bass, smallmouth bass), those becoming piscivorous as age-1 (rock bass, crappie), and those with only sporadic piscivory (bluegill, pumpkinseed). Those species without parental care after larvae swim up (e.g., bluegill, pumpkinseed, rock bass) exhibited agonistic behavior earlier than those species with parental care (e.g., largemouth bass, smallmouth bass), thought to be important relative to dispersal of those species without parental care to safer habitats (i.e. to the limnetic). Those species with parental care remained relatively safe from predators in the littoral zone, being protected by the guarding male. When quantifying agonistic behaviors, those of bluegill and pumpkinseed were found to be similar, while those of largemouth bass and rock bass were most different (Brown and Colgan 1985a). In general, Brown and Colgan concluded across these studies that the ontogeny of behaviors that were expressed both in the field and laboratory were primarily related to size, and served to enhance survival of the young with these varying early life behavioral patterns. Finally, in a recent study, Near et al . (2004) used both mitochondrial and nuclear DNA sequences to conduct a phylogenetic analysis of the entire centrarchid family. They identified four major lineages using two approaches (maximum parsimony analysis, Bayesian maximum likelihood analysis). In general, they found these groups to include (i) the mud sunfish, (ii) Micropterus spp. black bass, (iii) Lepomis spp. sunfishes, and (iv) a combined group including the Pomoxis spp. crappies, rock bass and other Ambloplites, the Sacramento perch (A. pomotis), the flier (Centrarchus macropterus), and Enneacanthus spp. (blackbanded sunfish E. chaetodon, bluespotted sunfish E. gloriosus, and banded sunfish E. obesus). Although there are some differences among the groupings we defined (e.g., Pomoxis spp. with rock bass), we find it interesting that these four groups are reasonably similar to ours. The combination of these three pieces of evidence leads to the suggestion that the groupings that we generated at the outset of this chapter may have broader ecological and evolutionary implications within the Centrarchidae.

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5.9 Gaps in our knowledge/research and management needs Our review of the literature has identified gaps in our knowledge and areas in which additional research is needed relative to improving our understanding of the early life history and recruitment in the Centrarchidae as well as to allow for improved management of this diverse family. Here we identify these gaps (in no particular order). (1) Clearly, our understanding of the early life history of centrarchids is dominated by information from relatively few species. The importance of the fisheries for those species as well as their economic impact has certainly been influential in driving the research on recruitment processes. Largemouth bass, the crappies, and bluegill have been studied in many systems. While information about the variety of species in the sunfish family might prove interesting, it is those animals representing the extremes of body size (i.e. Enneacanthus spp.) or behavioral strategy (e.g., mud sunfish) in particular that would challenge the patterns of reproductive investment into larval size revealed by our multivariate analysis. (2) In addition to greater breadth of study of species within the Centrarchidae, work is required in a greater diversity of system types. For example, more work is required for lotic species, for estuarine populations, in natural lakes for crappie, and across latitudes. (3) We require more information on movements of larval fishes, including both additional information for those species that have been relatively well studied (e.g., do all bluegill move to the limnetic as larvae, what influences the differential movement offshore within species, what triggers the movement back to the littoral), as well as any information concerning other centrarchids that have not yet been studied (e.g., do these other lesser-studied species move offshore as larvae, how does their movement or lack of movement compare with other centrarchids). Such results would help to identify evolutionary causes for such behaviors. Work is also needed relative to movement patterns of larval centrarchids in system types other than ponds and small lakes, such as lotic systems. (4) As was clear from the literature review, there have been biases in the distribution of studies investigating abiotic versus biotic factors among centrarchid species. Why are abiotic factors more important (or studied more often) in crappies, while biotic factors are studied more often in bluegill? Is this a bias of our science, or does it reflect actual differences in controlling influences across the centrarchids? (5) Interestingly, although crappies are an important sport fish species, and much research has been conducted relative to demonstrating that hydrological factors affect their early life and recruitment, we remain unable to explain how these hydrological factors exert their influence. There is a great deal that is not known about crappie early life history, which is an area in which research is needed. (6) Although much information about mechanisms influencing centrarchids during specific critical periods is available, it is still imperative that investigators understand the interplay among life stages as well as their eventual population-level consequences (e.g., Ludsin and DeVries 1997). In this chapter, we have compiled a relatively comprehensive summary of the information available concerning those early life stages we identified as being important (see earlier). However, few studies have identified the specific life stage or stages that are most important in determining eventual cohort strength. We suggest that work explicitly addressing this in the centrarchids is needed.

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Chapter 6

Population and community ecology of Centrarchidae D. D. Aday, J. J. Parkos III, and D. H. Wahl

6.1 Introduction Although our chapter is titled “Population and community ecology of centrarchids,” clearly all of the chapters in this volume address some aspect of this broad theme. Our approach, therefore, was to isolate the factors or issues that seem to have a disproportionate influence on the populations or communities of these common freshwater species that have received little or no attention in the other chapters. In some cases, our ideas segue into those of other chapters, and in these instances we generally introduce the topic and then reference the appropriate chapter. Because of the species and life-history diversity within Centrarchidae, each of our subsections are built around different themes. What unifies the ideas presented in the population section is a focus on the interface between basic and applied ecology, that is, the ways in which theory can be applied to the management of these often important sportfish species. We begin by considering the population ecology of the genus Lepomis (Section 6.2). In this section we focus on issues associated with habitat use and reproduction, two factors that have particularly strong influence on the population ecology of these species, and emphasize body size as a unifying theme. Next, we cover the Micropterus species (Section 6.3), and focus on their role as top predators and how that influences individual life histories and population ecology. In addition, we address the widespread introduction of Micropterus species outside of their native ranges by examining their ecology in novel environments and the ecological consequences of these introductions. Although there are other interesting and important centrarchids, much less information is available for these species and, therefore, much less text is devoted to their coverage. In Section 6.4, we focus on the species that have received most of the attention in the literature—rock bass (Latin binomials for centrarchids listed in Chapter 1) and crappie. After the sections on population ecology, we move to community considerations (Section 6.5) and attempt to synthesize the published literature on topics that most influence the freshwater communities that centrarchids often dominate. In the community section, we specifically consider the influence of competition and predation on community structure, food-web dynamics, and trophic cascades. We conclude the chapter with a summary of the important issues and look to the future of investigations involving centrarchids. Because of the sheer volume (and diversity) of literature associated with the better-studied members of this family, our approach is to highlight trends and themes in an effort to avoid overwhelming the reader with detail. Though we emphasize some specifics, our review is intended for a general audience. For those interested in additional detail, we provide some direction by referencing other chapters in this volume as well as pertinent primary literature.

6.2 Population ecology of Lepomis Lepomis is the largest genus of the family Centrarchidae. Although much interspecific diversity in life-history strategies occurs within the genus, in this section we provide an overview of various aspects of lepomid life histories while drawing

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attention to instances of obvious divergence. We then present information specific to the species (e.g., bluegill, Lepomis macrochirus, and pumpkinseed, Lepomis gibbosus) that are best studied. One point to be emphasized is that, despite the important role these species are often presumed to play in the communities they inhabit, relevant information for many in this genus is depauperate at best and completely lacking in certain instances. We suggest, therefore, that there is substantial need for additional studies on fundamental aspects of the ecology and life histories of many of these common freshwater species. Of the 13 species (Chapter 1) in the genus Lepomis, most are colonial spawners that inhabit lentic systems. Typically, adult individuals range in size from 100 to 250 mm (total length), tolerate a range of habitats, are omnivorous, and are distributed primarily east of the Rocky Mountains (summarized in Robinson and Buchanan 1992; Jenkins and Burkhead 1993; Table 6.1). Lepomids generally exhibit relatively rapid growth, early maturation, and short lives. However, in describing the “general lepomid” it is important to recognize the diversity that exists both within and among species. For example, there are several species that exhibit much smaller body size than others in the genus, such as the orangespotted (Lepomis humilis) and bantam (Lepomis symmetricus) sunfish, which rarely exceed 100 mm in total length as adults (Table 6.1). Further, the spotted sunfish (Lepomis punctatus) appears to be a solitary rather than colonial spawner, and the redear (Lepomis microlophus) and pumpkinseed sunfish feed more extensively on crustaceans than do other members of the genus (Table 6.1). Even within species, there is often considerable population-specific variation in growth rate, body size, and timing of maturation (e.g., Fox 1994; Cargnelli and Gross 1996; Aday et al . 2002, 2003a). However, as a general rule, lepomids appear to exist primarily at the intermediate trophic level in most of the systems they inhabit, serving as important predators on invertebrates and fish, and as prey resources for piscivorous predators.

Table 6.1 Summary of life-history aspects of the 13 members of the genus Lepomis.

Common name

Scientific name

Habitat

Diet

Maximum adult body size (TL, mm)

Redbreast sunfisha

Lepomis auritus

Primarily lotic

Omnivorous

>200

Green sunfisha

Lepomis cyanellus

Lotic and lentic

Omnivorous

>200

Pumpkinseeda

Lepomis gibbosus

Lentic and lotic

Omnivorous; primarily mollusks

>200

Lepomis gulosus

Lotic and lentic

Omnivorous

>200

Orangespotted sunfish

Lepomis humilis

Lotic and lentic

Omnivorous

<150

Bluegilla

Lepomis macrochirus

Lentic and lotic

Omnivorous

>200

Dollar sunfishb

Lepomis marginatus

Lotic and lentic

Omnivorous

<150

Longear sunfishb

Lepomis megalotis

Lotic and lentic

Omnivorous

<200

Redear sunfish

Lepomis microlophus

Lentic and lotic

Omnivorous; primarily mollusks

>200

Redspotted sunfishb

Lepomis miniatus

Primarily lotic

Omnivorous

>200

Northern longear sunfish

Lepomis peltastes

New species classification—data unavailable

–

Spotted sunfishb

Lepomis punctatus

Primarily lotic

Omnivorous

>200

Lepomis symmetricus

Lotic and lentic

Omnivorous

<100

Warmoutha b

a

Bantam sunfish

b

a Information summarized in Jenkins and Burkhead (1993) b Information summarized in Robinson and Buchanan (1992)

Note: Characteristics listed for each species are for typical individuals in most populations

–

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Centrarchid fishes

6.2.1 Population structure and body size: linking basic and applied research Many of the factors that influence population structure of lepomids are given coverage in other chapters of this volume. For example, reproductive behaviors, alternative reproductive tactics (Chapter 4), and early life histories (Chapter 5) all play important roles in structuring lepomid populations. Rather than reiterating that material, therefore, in this section we focus on aspects of lepomid ecology that are not specifically emphasized in other sections of this volume, but that still have significant influence on population structure. The most widely studied species in the genus Lepomis are bluegill and pumpkinseed. As a tremendous diversity of information is available for these two species, we have chosen to focus on aspects of population ecology that seem to be most widely investigated, and that would likely be applicable to other, less studied members of the genus. Theoretical aspects of individual life histories and population structures and applied approaches to managing these often-exploited species are prevalent themes in the peer-reviewed literature. In this section, we discuss habitat considerations as well as reproductive strategies and behaviors. Unifying these topics is a focus on body size, and the ways in which size-structured interactions influence the life histories of individuals and the structure of populations. Body size is both a fundamental determinant of an organism’s ecology (Werner and Gilliam 1984) and, from an applied perspective, often the primary response variable in investigations or management initiatives associated with recreational harvest.

6.2.1.1 Habitat considerations The population ecology of lepomids, like that of other species, can be influenced to a significant degree by habitat, through its influence on factors such as prey availability (Werner et al . 1983; Ehlinger 1989), predation (e.g., Mittelbach 1986; Werner and Hall 1988; Savino and Stein 1989), and competitive interactions (e.g., Persson 1983; Fischer 2000). A number of investigations have indicated the importance of habitat considerations to the life histories, population dynamics, and community ecology of centrarchids in general and lepomids specifically. Although a number of mechanisms could conceivably be associated with habitat selection by lepomids, much research has been conducted on the following: ontogenetic diet and habit shifts, predation risk, prey availability and foraging considerations, and competition. Even though many of these underlying mechanisms are issues of community (rather than population) ecology, ontogentic habitat shifts and optimal foraging can have considerable influence on lepomid populations. Further discussion can be found in the community section of this chapter (Section 6.5). Ontogenetic habitat shifts have been well studied in lepomids, and a number of investigations have indicated that bluegill undergo a series of diet changes. Mittelbach (1981) used a foraging model and field experiment to show that bluegill undergo an important niche shift at approximately 100-mm standard length (SL), whereby those larger than 100 mm become highly selective and those smaller are restricted in their habitat use. In a separate experiment, Mittelbach (1984) concluded that small bluegill (this time < 75-mm SL) and small pumpkinseed both were restricted to vegetated habitat and, by extension, vegetation-associated prey items. For larger individuals of both species, however, a distinct habitat shift occurred, and large bluegill began foraging in the open water on zooplankton while large pumpkinseed foraged specifically on gastropods. In a seminal 1988 paper, Werner and Hall examined bluegill habitat shifts and, within the context of predation risk, argued that bluegill in fact make several distinct shifts, first from the littoral zone to the pelagic zone as fry, then from the pelagic zone back to the littoral zone as juveniles, finally returning to the pelagic zone again after growing to a size at which predation risk is reduced. The timing of these habitat shifts by individuals can have considerable influence on population structure. Directly associated with these ontogenetic habitat shifts (and habitat selection by other lepomids as well) is optimal foraging theory (Emlen 1966; MacArthur and Pianka 1966) and predictions about diet selection for, in this instance, remarkably omnivorous sunfish. Although many of these species can and do consume a wide variety of food types, one can predict which would produce the greatest return based on the handling time and energetic value of the prey (i.e. which would be optimal forage). These relationships explain the specialization in many habitats of bluegill on large-bodied zooplankton (e.g., Daphnia pulex ; e.g., Mittelbach 1983, 1984; Werner et al . 1983) and adult pumpkinseed on gastropods (e.g., Mittelbach 1984). As Mittelbach (1983) demonstrated, foraging in a way that maximizes net energy intake can have a tremendous influence on growth and energy gain of individuals, again with implications at the population level. The question then becomes, why not always forage optimally? The answer, in many cases, is that foraging options coincide with habitat selection, which can be driven by prey availability, predation risk, and competition.

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Perhaps the most basic consideration for an organism selecting a particular habitat in which to forage is prey availability and, in the absence of predators or competitors, individuals would be expected to forage such that they maximize net energy intake. For bluegill in a laboratory setting, Ehlinger (1990) found that individuals generally foraged in areas that provided them with the greatest return. Likewise, in the absence of predators, other investigations have found that bluegill choose to forage in patches that maximize energy intake per unit time (Gotceitas 1990) or in those that have the highest initial prey densities (Gotceitas and Colgan 1990). Werner et al . (1983) used optimal foraging theory to predict habitat selection based on profitability (maximizing feeding rates and energy return) and found that bluegill habitat use in the field corresponded nicely to their predictions. However, it is often the case that constraints will be placed on habitat selection and foraging due to the presence of other biotic or abiotic factors, most importantly predation and competition. A final habitat consideration that has received attention in the literature is the morphological change that can sometimes be connected to habitat-specific foraging. The foraging ecology and functional morphology associated with habitat specialization has been relatively well studied for lepomids (Wainwright 1996). Ehlinger and Wilson (1988) described adaptive variation in both morphology and behavior for bluegill foraging in littoral or pelagic zones. In a follow-up study, Ehlinger (1990) showed that bluegill differed in their habitat selection (vegetated versus open water), and that modified foraging behaviors and morphology (size of pectoral fins) were associated with variation in habitat choice and foraging abilities. Chipps et al . (2004) compared predator evasiveness among bluegill with littoral and limnetic morphologies and found that differences in body type and behavior between the two groups was linked to predation susceptibility in both vegetated and open-water habitats. Similar polymorphisms have been demonstrated in pumpkinseed as well (e.g., Robinson et al . 2000). To test mechanisms associated with foraging polymorphisms, Hegrenes (2001) raised young-of-the-year (YOY) orangespotted sunfish on different diets, which led to differences in feeding morphology. For pumpkinseed, Robinson and Wilson (1996) found that both genetic differences and phenotypic plasticity contributed to the development of trophic polymorphisms. Finally, in an interesting tie-in with competition considerations, Robinson et al . (2000) found that the presence of bluegill limited pumpkinseed divergence. This may be a function of lack of pumpkinseed foraging in limnetic habitat, where bluegill were frequently observed and captured, preventing the formation of the open-water morphology (Robinson et al . 2000). Clearly, habitat selection and its association with foraging behaviors can have significant consequences for lepomid populations. Individuals seeking to maximize energy intake and growth can be limited by prey availability, predators, and competitors, which can lead to a variety of physical and ecological changes, all of which can influence the life histories of individuals and, by extension, population structure and dynamics. As such, habitat availability and use underlies virtually all of the biotic interactions that shape the population ecology of centrarchids in general and lepomids specifically. Issues associated with habitat are also connected directly to body size, the unifying theme for this section on population ecology of lepomids. Within species, body size plays an important role in habitat selection and foraging behavior, and is the principal factor in predator-mediated habitat shifts and competitive interactions, each of which is covered in the community section of this chapter. It is also a central theme in reproductive strategies and behaviors, which we discuss next.

6.2.1.2 Reproductive strategies and behaviors Reproductive strategies and behaviors of lepomids have received considerable attention in the literature, perhaps due to their relatively unique life histories, and it is clear that reproductive issues can have a significant influence on population structure. For lepomids, reproductive strategies and success can be based on a number of individual factors and biotic interactions, including body size, sex, and morphology, as well as male–male competition and female choice. In addition, their temporally protracted spawning season (with individuals potentially spawning multiple times) influences individual reproductive strategies. A significant underlying consideration is that most lepomids are colonial, with males providing parental care to eggs and developing fry (e.g., Avila 1976; Gross 1982). Colonial reproduction may have arisen in response to predation, as groups of individuals seem to experience less nest predation than solitary spawners (Dominey 1981; Gross and MacMillan 1981). Regardless of the mechanism for its origination, this aggregate spawning behavior leads to interactions among individuals that influence size- and sex-specific reproductive strategies and, hence, population structure. Size may be the single factor with the greatest influence on lepomid reproductive strategies, influencing (though perhaps through different mechanisms) both males and females. It has both a direct influence on males and females individually, as well as an influence on inter- and intrasexual interactions. For males, body size plays a role in an individual’s ability

138

Centrarchid fishes

to compete for access to spawning sites within a colony, attract a mate, and defend his brood. For females, because body size is often directly related to fecundity (Roff 1984; Fox 1994), strategies regarding energy acquisition and timing of sexual maturation are often size-specific. For both sexes, size-based interactions can influence the timing and quantity of energy allocation to reproduction as well as reproductive success. We consider here the size- and sex-specific reproductive strategies, focusing greater attention on males due to the importance of their behavioral interactions for individual lifehistory strategies and population structure. For males, body size is a fundamental determinant of reproductive strategy. It is the basis of alternative reproductive behaviors found in many male lepomids (small males cuckolding larger parental males; Chapter 4), and structures interactions within colonies that lead to variation in individual timing of maturation and reproductive success. At the population level, size-based behavioral interactions appear to be particularly important in structuring bluegill populations. Bluegill exhibit social inhibition of maturation whereby the presence of large, parental male bluegill inhibits maturation of smaller juvenile males (Jennings et al . 1997; Aday et al . 2003a,b; Aday et al . 2006). This social inhibition of maturation is a common phenomenon in fish populations, and is often manifested as large males inhibiting maturation of smaller males. In particular, much research has been conducted on members of the genus Xiphophorus. For example, Borowsky (1978, 1987) showed that large male platyfish (Xiphophorus variatus; either mature or immature) could suppress the maturation of smaller males. Other investigations have indicated similar results in fathead minnows (Pimephales promelas; Danylchuk and Tonn 2001), mosquito fish (Gambusia affinis; Hughes 1985), and the swordtail characin (Corynopoma riisei ; Bushman and Burns 1994). In centrarchids, Jennings et al . (1997) first documented social inhibition of maturation in bluegill by quantifying gonadal investment of male bluegill in ponds with different size structures. Following that study, Aday et al . (2003a) determined that individuals from isolated populations responded similarly to social interactions (i.e. juvenile males from separate populations delayed or initiated maturation based on the presence or absence of large males), confirming the importance of size-based social interactions to male-maturation schedules, and suggesting that bluegill likely have extremely plastic life histories. Subsequent investigations have provided further evidence that social interactions are of primary importance in determining maturation schedules of juveniles; even when resources are abundant and growth rates are relatively high, juvenile males delay maturation in the presence of larger males (Aday et al . 2006). It may be that an olfactory cue mediates male–male interactions (Aday et al . 2003b), however, additional research will be necessary to determine exactly how these size-based relations take place. Regardless, size-based interactions clearly have important implications for shaping individual life histories and for the size structure of bluegill populations (see the section on management considerations presented later). Beyond reproductive strategies associated with timing of maturation, body size has a direct influence on the reproductive success of male lepomids. In bluegill, Aday et al . (2002) showed that larger males had greater nesting success (i.e. greater number of eggs per nest) than smaller, stunted males in ponds. Similarly, Jennings and Philipp (1992) found a direct relationship between the size of longear males and their nesting success. Unlike with bluegill, however, they found that solitary nesting longear were more successful than those that nested in colonies, with the latter being more likely to be cuckolded than those that nested alone. The greater reproductive success of larger males is likely a function of female choice, indicating the importance of body size in both intrasexual (male–male interactions, presented earlier) and intersexual interactions. Female lepomids have been shown to spawn preferentially with larger males (Claussen 1991; Jennings and Philipp 1992). Females may be making these choices based on attributes of the larger males such as the size of their opercular flaps. Goddard and Mathis (1997) experimentally manipulated opercular flap size in spawning male longears and found that females spent more time with, and displayed more to, males with larger flap size. Alternatively, choice may be based on where or when males build their nests. Dupuis and Keenleyside (1988) found that, among longear nesting in groups, females preferred to spawn with males that nested early in centrally located positions within colonies (which might decrease the predation risk to their eggs from predators that must enter the colony from the periphery; Dominey 1981, Gross and MacMillan 1981). Body size also influences male reproductive success vis-`a-vis alternative reproductive strategies (Chapter 4), through the influence of reproductive parasites on the reproductive success of “parental” male centrarchids. It appears that conspecific nest parasitism is common to a number of lepomids, and this sometimes occurs when small individuals adopt a morphologically specific life-history strategy and steal fertilizations from larger males. A number of studies using genetic techniques such as microsatellite markers have revealed the influence of these nest parasites on the reproductive success of spawning males. In the spotted sunfish, for example, only 57% of the nests examined contained eggs fertilized exclusively by the guardian male (DeWoody et al . 2000). Philipp and Gross (1994) demonstrated that the fertilization success of

Population and community ecology of Centrarchidae

139

parental male bluegill in Lake Opinicon, Ontario, Canada, varied from 41 to 100%, based on the density of cuckolder males present near the colonies. Interestingly, in cases in which the guardian males and the cuckolders were homomorphic, the success of the cuckolders was significantly reduced; in dollar sunfish, more than 95% of the nests contained eggs fertilized exclusively by the guarding male (Mackiewicz et al . 2002), and in redbreast sunfish the number was greater than 90% (DeWoody et al . 1998). Clearly, body size influences the reproductive success of males displaying alternative reproductive strategies—for both the guarding males and the cuckolders. Size-specific reproductive patterns have also been shown to be important for female lepomids. Unlike males, which often appear to be limited by access to females, reproductive investment of females in many species is thought to be resource limited (e.g., Bateman 1948; Trivers 1972; Whiteman 1997). Research on female pumpkinseed suggests that body size and resource availability can influence their reproductive strategies. For example, Danylchuk and Fox (1994) found a relationship between size and age structure and the proportion of females spawning in certain populations, and suggested that differences in spawning times between small and large females was a consequence of difference in energy reserves. In bluegill, females in experimental ponds with high levels of food resources became reproductively mature at twice the rate of females in ponds with lower resource levels (Aday et al . 2006). It is not clear whether social interactions play a role in female reproductive decisions in the same way that they do for males. In the same pond experiment, female bluegill showed no response to the presence or absence of large parental males. In a number of fish species, behavioral interactions have been shown to be fundamentally important for female life histories, even causing sex change (e.g., Ross et al . 1990; Francis and Barlow 1993; St. Mary 1994; Kuwamura et al . 1994). Further research on female centrarchids will be necessary to determine what influence, if any, inter- or intrasexual behavioral interactions have on female reproductive strategies and success. For both males and females, the relationship between body size and reproductive strategies can be somewhat circular; body size can influence the timing of sexual maturation and, in turn, timing of maturation can influence body size. The mechanism underlying the latter relationship is a central tenet of life-history theory, that is, a presumed trade-off between growth and maturity in which energetic resources devoted to reproduction (including the building of gonad material and, in the case of male centrarchids, the energetically costly building and defending of nests) cause a decrease in somatic growth (e.g., Williams 1966; Gadgil and Bossert 1970; Bell 1980; Partridge and Harvey 1988). This makes achieving a relatively large body size prior to sexual maturation important for most lepomids due to the relationship between body size and fecundity for females and, for males, the need to attract females and defend their offspring. The consequences of energetic trade-offs between growth and maturation for individual body size and population size structure are discussed in the section on management considerations.

6.2.2 Historical context and management considerations Although Lepomis is a diverse genera containing many nonexploited members, a number of lepomid species are widely targeted by recreational anglers. Undoubtedly, it is bluegill that receive the most angling pressure in the group (Chapter 11) and, consequently, they are the subject of numerous management initiatives aimed at understanding population dynamics and maximizing size structure. Indeed, each of the themes described earlier (habitat use, diet shifts, and life-history decisions related to reproduction) can be considered in the context of bluegill population dynamics, a subject that has been a central theme in applied fisheries management for more than a half century. Early studies of bluegill tended to focus on fishery-related issues such as production and mortality. This was particularly true of work in small impoundments, where much of the early work on bluegill appeared. Homer Swingle and E.V. Smith, among others, contributed much to the understanding of stocking rates and production for bluegill and other centrarchids (e.g., Swingle and Smith 1943; Swingle 1946, 1950a), and their research considered both population dynamics and community-level interactions, particularly those between largemouth bass and their prey (Swingle 1946). Around the same period, classic studies on bluegill mortality were being carried out. Ricker (1945) analyzed three Indiana ponds to determine total annual mortality and fishing mortality of bluegill over a range of sizes and ages. Gerking (e.g., 1952, 1962) followed with extensive studies on bluegill growth, prey selection, production, and mortality. These early investigations provided the framework on which contemporary studies of population dynamics and community structure (for both centrarchids and other species) are built.

140

Centrarchid fishes

Bluegill populations and their dynamics continue to be studied in a variety of settings. One theme that has generated particular interest has been the phenomenon of stunting, a condition in which members of a population remain small relative to conspecifics in other populations. Though the traditional view of stunting is that it is the result of poor growth (e.g., El-Shamy 1978), recent research provides an alternative explanation. In essence, this alternative hypothesis focuses on the growth–maturation trade-off discussed earlier in this chapter, and suggests that stunting may be associated with early maturation (e.g., Mann and McCart 1981; Jansen 1996). Evidence supporting this explanation can be found in research focused on lepomids. For example, a survey of bluegill populations across Illinois indicated that population size structure was inversely related to age-at-maturation (Julie Claussen, Illinois Natural History Survey, personal communication). Aday et al . (2006) found that social interactions inhibited maturation of juvenile males regardless of resource availability, suggesting that socially mediated timing of maturation has a significant influence on adult body size of males regardless of growth rates. There are a number of mechanisms that might lead to, if not stunting, variation in adult body size among populations, and these mechanisms might work in concert. Clearly, further research will be necessary to describe additional mechanisms and pathways associated with variation in body size and population size structure (see Aday 2009). Nevertheless, we suggest that traditional, single-dimension paradigms are often not robust enough to explain stunting in fish populations. Instead, we recommend that management investigations and initiatives consider the complexity of ecological and evolutionary pathways that can shape individual life histories and population size structure.

6.3 Micropterus Micropterus species (black basses) are probably best known for their ecological role as top predators in many freshwater systems. Species such as largemouth bass (M. salmoides) often become piscivorous during their first year of life. The importance of the black basses both to the structure of aquatic communities and as game species derives largely from their predatory ecology. As top predators, these species must achieve fast growth rates to overcome any gape limitations relative to their prey. The need to achieve relatively large body size also has led these species to evolve life-history strategies involving high-quality offspring (versus quantity), delayed maturity, and parental care of their reproductive investment. Micropterus life history is intermediate between a periodic strategy with delayed maturity and synchronous reproduction and an equilibrium strategy with large eggs and parental care (as defined in Winemiller and Rose 1992). We focus this section on how the population ecology of black basses is influenced by their role as top predators in aquatic ecosystems. First, we discuss how the reproductive behaviors of black bass provide opportunities for piscivory by their offspring and the consequences of these behaviors for intraspecific competition. Next, we describe the influence of parental care on the population ecology of black basses. Chapter 5 provides in-depth coverage of bass recruitment, and so we focus on the relationship between predatory behaviors, such as cannibalism, and recruitment. We then review general patterns of population dynamics observed and expected for black basses and how trophic relationships may be responsible for these dynamics. We also describe the population ecology of black bass species at the edges of their native ranges. Some black bass species, such as largemouth bass and smallmouth bass, (M. dolomieu), are the targets of intensive sport fisheries and, due to their popularity, have been widely introduced outside of their native ranges. We conclude our section on the population ecology of Micropterus species by examining the effects of this fishing pressure and reviewing the ecological consequences of these introductions, as well as the ecology of black bass in novel environments.

6.3.1 Population ecology of a top predator Typical of piscivores, black basses exhibit reproductive behaviors that maximize foraging opportunities for their offspring. All fish species must either time their reproduction to the availability of food for their offspring or face high losses due to starvation (Cushing 1990: Match/Mismatch hypothesis). Species such as largemouth bass, for whom fish compose the majority of their diet by age-1, must not only have an ample supply of plankton prey available upon absorption of their yolk-sac, but must also successfully make the transition to piscivory during their first growing season. The offspring of

Population and community ecology of Centrarchidae

200 180

70

160 60

140

50

120 100

40

80

30

60

20

40 20

10 0 4/1

Lepomis larvae (N/m3)

Percentage of total bass nests

80

141

0 5/1

6/1

7/1

8/1

9/1

10/1

Figure 6.1 Number of new largemouth bass nests as percentage of the total number observed by date (vertical bars) and density of larval lepomids (solid line) through time in Lincoln Trail Lake, IL during 2003.

these early-switching piscivores that do not make this transition during their first growing season often have decreased growth and survival (Mittelbach and Persson 1998). For centrarchids that are not primary piscivores, such as Lepomis species, reproduction can be protracted in order to increase offspring success in variable environments (Garvey et al . 2002). In contrast, primary piscivores must time their reproduction such that their offspring are developed enough (e.g., sensory systems, gape size) to take advantage of the seasonal emergence of fish prey. The need for YOY piscivory has resulted in black basses having, on average, earlier spawning times than the primary fish prey of their offspring (Phillips et al . 1995; Figure 6.1). Micropterus species typically spawn in spring when water temperatures are 15 to 25◦ C, with most reproductive activity being initiated at 15◦ C (Carlander 1977). During a given year, differences in male age and size lead to variation among individuals in the timing of reproduction, with older, larger males spawning earlier in the year than smaller, younger males (Ridgway and Friesen 1992; Baylis et al . 1993). This variation in timing of reproduction can lead to differences in growth among early- and late-hatched cohorts (Isely et al . 1987; Maceina et al . 1988; Phillips et al . 1995; Ludsin and DeVries 1997; Sammons et al . 1999). Due to the importance of timing of reproduction for offspring growth and survival, black basses need to concentrate their reproductive activity within a relatively compressed time frame. Micropterus species are characterized by relatively synchronous spawning bouts, with almost all spawning taking place within a month (Figure 6.1). One implication of synchronous spawning behavior is that environmental events occurring during a relatively short time frame can affect cohort success. Abiotic conditions (e.g., temperature and rainfall) during the spring, when black basses spawn, are often variable, and extreme conditions can have a large influence on nest success and overall recruitment within a population (Parkos and Wahl 2002). The synchronous nature of black bass spawning also could heighten competition for limited nest sites (Iguchi et al . 2004). Territoriality and nest site fidelity are black bass behaviors that increase the potential for intrasexual competition. For example, smallmouth bass exhibit strong nest site fidelity (Ridgway et al . 1991). One outcome of intrasexual competition is that a relatively small proportion of sexually mature males may spawn in a given year (Raffeto et al . 1990). For smallmouth bass, the number of nesting males appears to be the result of a negative density-dependent relationship, whereby reduced growth of juveniles during conditions of heightened competition results in fewer individuals recruiting into the breeding population (juvenile transition hypothesis of Ridgway et al . 2002). Micropterus species typically mature at ages 2 to 4, with most females not maturing until age 3 or 4 (Carlander 1977). In some smallmouth bass populations, size- and agedependent timing of maturity has led to alternating life-history patterns. The earlier-hatched offspring of old, large males gain enough of a growth advantage over the later spawned offspring of young, small males that they become sexually mature at smaller sizes and younger ages and, therefore, spawn later in spring. This pattern repeats itself such that there is a negative covariance between parental males and their male offspring in age of sexual maturation (Baylis et al . 1993).

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Centrarchid fishes

Pumpkinseed

Green sunfish

Bluegill sunfish

White crappie

Redear sunfish

Redeye bass

Black crappie

Smallmouth bass

Spotted bass

200 180 160 140 120 100 80 60 40 20 0 Largemouth bass

Total length (mm) at age-1

Micropterus, like all centrarchids, provide parental care to the most vulnerable life stages of their offspring. Care is provided by the male and consists of nest fanning and guarding. Guarding is especially important to protect eggs and larvae from cannibals and other centrarchids (Eipper 1975; Post et al . 1998). Patterns of parental care in largemouth and smallmouth bass consist of guarding behavior extending through the free-swimming stage of development. For many fish species, mortality during the earliest life stages creates “critical periods” of recruitment, such that year class strength is set by losses of embryos and larvae to predators, starvation, and extreme abiotic conditions (Houde 1994). Parental protection of developing eggs and larvae minimizes these losses, thereby pushing back the critical period for recruitment to later stages of development. Factors such as extreme abiotic conditions and angling pressure that interfere with parental care behavior may negatively influence year class strength by shifting recruitment bottlenecks back to the nesting period of development (Ridgway and Shuter 1997; Parkos and Wahl 2002). Recruitment is a critical process in the dynamics and persistence of fish populations. Variation in recruitment may be due to the quality or quantity of spawning stock, environmental conditions (i.e. abiotic factors), food abundance, and predation (Ricker 1954; Houde 1987; Miller et al . 1988; Cowan et al . 2000). The relationship between stock and recruitment in largemouth bass and smallmouth bass populations appears to be complex, and has so far defied the identification of any simple correlative patterns (Parkos and Wahl 2002). A more accurate connection between mature individuals and recruitment may be nest success, and variable nest success appears to be closely related to size of parental males; larger parental males may provide more effective defense against nest predators than smaller, younger males (Suski and Philipp 2004). If environmental conditions such as water temperature and wave action are extreme or variable during nesting, recruitment may be closely tied to abiotic factors in the spring (Parkos and Wahl 2002). Multi-year studies in systems at both high and low latitudes have identified mortality during pre-dispersal life stages as determinants of recruitment strength (Kramer and Smith 1962; Jackson and Noble 2000). If spring conditions are less extreme, growth during the summer and winter mortality may be the crucial factors affecting recruitment (Chapter 5). The success of YOY as predators is also important for black bass recruitment. Growth is higher for piscivorous YOY than for those individuals still foraging on invertebrates (Olson 1996). This difference in growth rate is important for both first-year survival and for the effectiveness of YOY as predators on larger invertebrates and other fish (Olson 1996; Ludsin and DeVries 1997). Indicative of their ecological role as top predators, Micropterus have larger body sizes relative to other centrarchid species that are less piscivorous (Figure 6.2; data from Carlander 1977). Predation is often considered to be an important source of mortality for YOY fish, and bass are no exception. The effectiveness of black basses as piscivores can be a threat to their own YOY as yearling bass represent a significant source of predation mortality (Post et al . 1998). Once protection by the parental male has ended, YOY bass must risk independent foraging for larger invertebrates and smaller fish. During these foraging bouts, YOY bass are highly susceptible to attack by cannibalistic bass. Predation

Figure 6.2 Size at age-1 (total length, mm) for representative Micropterus (open bars), Pomoxis (closed bars), and Lepomis (gray bars). Sizes are averages of reported values from populations near the center of the native range of each species. Values from Carlander (1977).

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during the winter can also negatively influence YOY bass survival (Miranda and Hubbard 1994; Garvey et al . 1998a). Above-average growth would benefit YOY bass during the winter by reducing their susceptibility to both predators and starvation (Chapter 5). Density-dependent regulation of growth and survival due to, for example, size-dependent starvation during winter and cannibalism maintains largemouth bass populations near a dynamic equilibrium. Long-term records of largemouth bass and smallmouth bass populations support the idea that Micropterus populations fluctuate around an equilibrium density (Inskip and Magnuson 1983). Ample evidence suggests that largemouth bass and smallmouth bass exhibit densitydependent responses in both growth and survival. High densities of YOY fish increase intraspecific competition, lower spring and summer growth, and lead to lower winter survival (DeAngelis et al . 1991; Schramm et al . 1995; Garvey et al . 1998a). Increased winter mortality of YOY due to smaller body sizes results in a negative association between high densities and recruitment. Losses of smaller fish to cannibalism also appear to be a potential mechanism of population regulation at high abundances (Swenson 2002). Density-dependent responses may be stronger in productive systems that attain higher abundances of fish (Beamesderfer and North 1995). Any potential for black bass populations to exhibit complex dynamics would likely be due to close connections between YOY bass piscivory, growth, and survival. Trophic relationships appear to be responsible for the majority of the cases of complex population dynamics (Turchin 2003). Any variation in prey fish abundance due to competition, stochastic environmental factors, or predation would influence bass growth and survival. Depending on how long it takes for predator numbers to respond (lag time) to changes in prey abundance, population cycles may become unstable (Turchin 2003). A potential intrinsic, though trophic, mechanism that could induce population cycles in largemouth bass would be heavy losses of subsequent cohorts of YOY to cannibals from the previous year class (Dong and Polis 1992). Populations of black basses at high latitudes may be more susceptible to abiotic factors such as water temperature and, therefore, may exhibit more chaotic dynamics if environmental conditions are sufficiently variable among years (Schramm et al . 1995). Dynamics of black bass populations in lotic environments are strongly influenced by among-year variation in discharge, and so may also have chaotic-seeming patterns in abundance (Swenson et al . 2002). Overall, Micropterus populations appear to be relatively stable in age structure and abundance due to strong density-dependent responses and medium potential growth rates. Any fluctuations about carrying capacity are likely due to fluctuations in prey abundance, stochastic environmental factors, or cannibalism. At the edges of their native ranges, black basses may inhabit environments that lead to significant differences in their population ecology relative to populations in more typical conditions. For example, smallmouth bass populations in Canada, near the northern extent of their range, are strongly influenced by water temperatures, with recruitment and survival dependent on summer and winter temperatures (Shuter et al . 1980). Largemouth bass populations have adapted to brackish environments at the southern edge of their range. These populations are characterized by reduced growth, smaller length at age, and stouter morphology (Meador and Kelso 1990).

6.3.2 Human impacts and management considerations Micropterus are generally highly prized as sportfish species. They have been introduced widely outside their native range and can be subject to fairly intensive fishing pressure (Noble 2002). Due to their higher levels of aggression, larger parental males that have high reproductive success and exhibit the most effective parental care of offspring are more vulnerable to capture by anglers (Suski and Philipp 2004) than smaller, less aggressive males. Anthropogenic effects that selectively influence the most reproductively successful members of a population could have large consequences for recruitment and subsequent population dynamics. If the larger, more reproductively successful males are also older individuals, this target effect of spring angling may also shift the age of maturity to younger, smaller males (Conover and Munch 2002). Cases in which fishing rates are relaxed have shown changes in age structure from dominance by younger age classes to increased abundance of older age classes (Swenson 2002). One approach to minimizing any negative effects of angling on black bass reproductive success is to establish spawning sanctuaries (Suski et al . 2002). Most of the research on effects of angling on Micropterus nest success and efficacy of spawning sanctuaries has been performed on populations at high latitudes (e.g., Ontario, Canada and Wisconsin, USA); therefore, further research is needed for populations at more southerly latitudes where factors influencing recruitment and fishing mortality rates could differ.

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Numerous introductions of Micropterus species outside of their native ranges, combined with concerns over the potential negative effects of these introductions, have led to studies of bass populations outside of their typical environments. In Japan, limited availability of nesting sites in a lake where smallmouth bass had been introduced led to altered patterns of size-specific reproductive success due to increased male–male competition (Iguchi et al . 2004). In a tropical reservoir in Puerto Rico, largemouth bass displayed temporally protracted and erratic spawning seasons (Waters and Noble 2004). Largemouth bass populations in tropical environments, such as Africa and Puerto Rico, have faster growth, higher mortality, younger age structure, and younger age at first reproduction than populations in temperate environments (Mozambique: Weyl and Hecht 1999; Puerto Rico: Waters and Noble 2004). This acceleration of typical largemouth bass life history would likely result in less stable populations characterized by rapid turnover. A long-term creel survey at Lake Opeongo in Ontario, Canada, provides a view of three phases of population growth following introduction of smallmouth bass into a novel environment. Smallmouth bass went through establishment (slow rate of increase), expansion (rapid rate of increase), and accommodation (reduced rate of increase) patterns of abundance following introduction (Shuter and Ridgway 2002). Black basses are effective top predators and, therefore, outside of their native range they represent a threat to native diversity (Jackson 2002). Human-facilitated spread of Micropterus species also results in contact between previously separate black bass species. This contact can result in either competitive displacement or hybridization. The coexistence of some black basses, such as Suwannee bass (Micropterus notius), and largemouth bass, is hypothesized to be due to partitioning of habitat and food sources (Schramm and Maceina 1986). However, in systems where previously separated species come into contact, such as redeye bass (Micropterus coosae), and spotted bass (Micropterus punctulatus), one species usually declines in abundance (Barwick and Moore 1983). Some declines may be due to hybridization between Micropterus species. For instance, Guadalupe bass (Micropterus treculi ), an endemic of central Texas, is threatened by hybridization with introduced smallmouth bass (Koppelman and Garrett 2002). Hybridization not only threatens the integrity of a native gene pool, but may also result in loss of fitness (Philipp et al . 2002).

6.4 Other centrarchids Of the 12 other members of the centrarchid family, only crappie (Pomoxis sp.) and rock bass (Ambloplites rupestris) have received much direct attention in the literature. Several species have single or few studies describing their behavior, life history, or ecology, including the mud sunfish (Acantharchus pomotis; Pardue 1993), Roanoke bass (Ambloplites cavifrons; Petrimoulx 1983), Ozark bass (Ambloplites constellatus; Walters et al . 2000), and the bluespotted sunfish (Enneacanthus gloriosus; Peterson and VanderKooy 1997; Snyder and Peterson 1999). Interesting work has been done on various aspects of green sunfish ecology and physiology. Though no particular theme emerges, one aspect that has received attention is the influence of chemical alarm signals on the behavior of individuals (e.g., Brown and Brennan 2000; Golub and Brown 2003). The banded sunfish (Enneacanthus obesus) was the subject of a number of interesting investigations involving predatory affects on anurans. For example, Chalcraft and Resetarits (2004) investigated the impact of banded sunfish populations on Southern leopard frogs (Rana shenocephala) and found that biomass and density (and their interaction) had an influence on the predatory effects of this sunfish on anuran prey. Similarly, Binckley and Resetarits (2003) and Resetarits and Wilbur (1991) found that anurans avoided ponds that contained banded sunfish predators. Similar effects of banded sunfish on other anurans have been documented (e.g., Lawler 1989). As only crappie and rock bass have been extensively studied, however, we focus on those species and again draw attention to the need for more detailed information on other members of this family.

6.4.1 Rock bass Although there have been a number of papers published on rock bass, there is no consistent theme in the literature. To summarize the important points, therefore, we have grouped the research into areas that have received the most attention, including rock bass ecology and physiology, reproductive behavior, and predatory effects, and we summarize the research accordingly.

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The first area of research concentration relates to the ecology and physiology of rock bass. One focus has been the comparison of lentic versus lotic populations. Brinsmead and Fox (2002) found that there were differences in external morphology between stream- and lake-dwelling rock bass, with stream fish exhibiting a more slender body and more anterior placement of lateral fins. Putman et al . (1995) studied stream populations of rock bass and reported evidence of individuals undergoing ontogenetic diet shifts, similar to those in lake populations. Perhaps because of mercury contamination and acidification in many of the systems this species inhabits, a number of studies have investigated the physiological effects of these factors on rock bass. For example, Bidwell and Heath (1993) and Scheuhammer and Graham (1999) consider the influence of mercury contamination and pH problems on rock bass populations. McCormick et al . (1989) considered acidification problems, finding that rock bass could osmoregulate and survive extended periods even at a relatively low pH (4.5), but substantial mortality occurred as levels continued to drop. Additional considerations related to pollution effects on centrarchids can be found in Chapter 8. Other studies have considered parental care and reproductive behavior of rock bass. Noltie and Keenleyside (1986) examined the reproductive success of male rock bass in the Middle Thames River, London, Ontario, and found that large males had greater reproductive success than smaller males, and that both water temperature and flow rates influenced reproductive success. Similar to studies with bluegill, the authors also noted that females spawned preferentially with larger males. Interestingly, they also noted that large males renested more frequently than smaller males. Sabat (1994) used rock bass to test a fundamental question in behavioral ecology, that enhancement of offspring survival due to parental care comes at a cost to the parent. In this study, the author manipulated broods in nests and determined that males lost more mass when guarding larger broods, and that parental body size influenced both mass loss (nonlinear) and offspring survival (better survival with larger parent). The following reproductive season, the recapture probability for parental males decreased in proportion to mass loss the previous season, further indicating the costs of parental care behavior (Sabat 1994). Perhaps the largest area of research on rock bass relates to their role as a predatory species in aquatic systems and subsequent effects on prey items. Rock bass can be important predators on a number of prey, thus the relatively common occurrence of papers examining predatory effects on specific species. For example, Grossman et al . (1995) examined the effects of rock bass on microhabitat shifts in mottled sculpin (Cottus bairdi ). They concluded that rock bass influenced the sculpins’ nighttime foraging behavior, but did not have strong effects on their habitat use. Rock bass often consume a wide variety of fish prey, and Angermeier (1992) quantified rock bass predation on stream fishes to determine the influence of specific habitat variables. In his investigation, rock bass consumed fish such as pumpkinseed, fantail darters (Etheostoma flabellare), and central stonerollers (Campostoma anomalum), and the influence of water depth and cover on predation rates were species-specific. Rock bass have also been shown to be efficient predators on invertebrates. Rabeni (1992) showed that centrarchids in general consumed more than 33% of crayfish produced in an Ozark stream, and concluded that rock bass (among other centrarchids) have significant influence on crayfish population dynamics, mortality, and energy flow. On a final note, an examination of the influence of climate on growth of stream fish and trees in the Ozarks provided some interesting observations. In this investigation, Guyette and Rabeni (1995) found a strong correlation between variation in growth increments of rock bass and four tree species, white oak, post oak, shortleaf pine, and eastern red cedar over a 22-year period. Based on this fascinating result, the authors conclude that, “The magnitude and significance of correlations among growth increments from fish and trees imply that conditions such as topography, stream gradient, organism age, and the distribution of a population relative to its geographic range can influence the climatic response of an organism.” Clearly, rock bass are important members of the systems they inhabit, and have the potential to influence habitat use by prey species and aquatic community structure. Continued research on factors that influence its population structure and dynamics, such as climate, habitat, and biotic interactions, will be necessary to fully understand the ecological role of this species in both lotic and lentic systems.

6.4.2 Crappie Ecologically, black crappie (Pomoxis nigromaculatus) and white crappie (Pomoxis annularis) are intermediate between lepomids and black basses. Crappie size at age-1 (Figure 6.2), later onset of piscivory, and early spawn dates are similar to black basses, whereas duration of parental care (relative to developmental stage of offspring), age-at-maturity (ages 2–3; Carlander 1977), and planktivory as YOY are more similar to lepomids. The population ecology of crappies is

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characterized by large variation in growth and recruitment, and this variation has been the subject of most of the research on this group. The main factors explored by past research on growth and recruitment variability of crappies have been zooplankton abundance, water conditions (level, temperature, and turbidity), and timing of hatch. Differences in hatch time appear to play more of a role than stock abundance in causing variation among cohorts in growth and survival. The proposed stock–recruitment relationship for crappie populations is dome-shaped, with low survival at extremely small and large spawner densities (Allen and Miranda 2001). However, the evidence for a stock–recruitment relationship is equivocal, with some evidence for (Dockendorf and Allen 2005) and against (Dubuc and DeVries 2002; McKeown and Mooradian 2002) a significant effect of spawning stock abundance. Among years, earlier hatches result in better growth rates on average than years with later hatches; however, within years earlier-hatched individuals have higher mortality and slower growth rates than individuals hatched later in the spring (Pine and Allen 2001; Sammons et al . 2001; Dubuc and DeVries 2002). These differences in growth and mortality among different hatch times may be related to differences in prey availability, predation pressure, water temperature, and overall environmental variability in early versus late spring. The high level of variation observed in crappie growth and recruitment may in fact be a consequence of variable abiotic conditions, such as temperature and turbidity (Allen and Miranda 2001). Many crappie populations are found in impoundments, systems often characterized by high turbidity and variable water levels. Increasing water levels during the spring appear to act as a cue for crappie reproduction (Sammons et al . 2001). In reservoirs, strong recruitment occurs in years with high discharge rates during the pre-spawn period followed by long retention times during and after the spawn (Maceina 2003). The importance of high discharge during the pre-spawn period may be system-dependent, but stable water level during and after the spawn appears to be consistently associated with strong year classes (Mitzner 1991; McDonough and Buchanan 1991; Slipke et al . 1998). Winter mortality is another factor often hypothesized to influence variation in year class strength of freshwater fishes. However, winter mortality does not appear to be important in setting recruitment strength (McKeown and Mooradian 2002), unless the winters are very severe (McCollum et al . 2003). Another environmental factor that may influence crappie recruitment is turbidity (Mitzner 1991), perhaps by interfering with their foraging efficiency on zooplankton (Ellison 1984; Dockendorf and Allen 2005). Pomoxis species are primarily planktivorous throughout their first year of life (Mathur and Robbins 1971; Ellison 1984; O’Brien et al . 1984), therefore, differences in zooplankton abundance have been considered to be a potential source of variation in growth and recruitment. As planktivores, crappies appear to primarily select for either Daphnia or the smallest crustacean zooplankton available (O’Brien et al . 1984; Dubuc and DeVries 2002). Despite some evidence for a positive effect of zooplankton abundance on growth (Claramunt and Wahl 2000; Sammons et al . 2001), other studies have found no effect on growth beyond the first-feeding larval stage (Allen et al . 1998; Bunnell et al . 2003; Dockendorf and Allen 2005). Evidence for a strong effect of zooplankton abundance on either crappie abundance or survival is also equivocal (Allen et al . 1998; Dubuc and DeVries 2002; Bunnell et al . 2003; Dockendorf and Allen 2005). A decline in foraging success due to high turbidity may have more of an effect on first-year growth and survival than the overall abundance of zooplankton per se (Ellison 1984; Dockendorf and Allen 2005), and black crappie may be more sensitive to high levels of turbidity than white crappie (Ellison 1984; Egertson and Downing 2004). Interestingly, turbidity may mediate the outcome of ecological interactions between black and white crappie. These species coexist in many systems and, based on their similar life histories, morphology, and diets, they likely compete with one another. However, differences between these two species in sensitivity to turbidity may result in the dominance of black crappie in clear water, macrophyte-dominated systems and white crappie in more turbid environments (McDonough and Buchanan 1991; Egertson and Downing 2004). McDonough and Buchanan (1991) documented a shift in dominance from white crappie to black crappie in a Tennessee reservoir that was experiencing increased aquatic macrophyte abundance, while Egertson and Downing (2004) found that higher abundances of common carp Cyprinus carpio were associated with lower abundances of black crappie and higher abundances of white crappie. In both studies, the authors documented a shift in the dominance of one Pomoxis species over the other due to changes in environmental conditions likely to affect turbidity. Aquatic macrophytes often play an important role in stabilizing sediments and increasing water clarity (Scheffer et al . 1993), while common carp are large benthivores often associated with loss of aquatic macrophytes and increased turbidity (Parkos et al . 2003). Aquatic macrophytes would also affect the availability of particular food resources, potentially also influencing the dominance of one or the other crappie species. Turbidity would still be important due to its effect on aquatic macrophyte abundance and potential species-specific differences in foraging capabilities under turbid conditions. In a lake with both crappie species, only white crappie switched from a diet of invertebrates to piscivory. This

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difference in diets may be due to niche partitioning among these competing species, but the author of this particular study concluded that high turbidity played a role by limiting the effectiveness of black crappie foraging (Ellison 1984). Turbidity may also weaken the reproductive barrier between black crappie and white crappie. Both crappie species have been known to hybridize in systems where they co-occur (Hubbs 1955; Buck and Hooe 1986; Dunham et al . 1994; Travnichek et al . 1996b). F1 hybrids achieve faster growth than their parental types, and this difference manifests itself just after hatching, with hybrid larvae having earlier swim-up dates (Travnichek et al . 1996a). Most records of black crappie × white crappie hybrids are from southeastern impoundments where hybridization rates range from 0 to 55% (Dunham et al . 1994; Smith et al . 1994; Travnichek et al . 1996b). Hybridization appears to be symmetrical between these two species and F1 hybrids are viable (Travnichek et al . 1997; Epifanio et al . 1999). However, few Fx individuals are found in the wild (Travnichek et al . 1997), perhaps due to lower reproductive success of F2 individuals (Epifanio et al . 1999). It is not clear if the lower numbers of Fx individuals are due to pre- or post-zygotic isolating mechanisms, but assortative mating between these two species does suggest that pre-zygotic barriers may limit hybridization under natural conditions (Epifanio et al . 1999). Turbidity may play a role in the extent and occurrence of hybridization between black and white crappie. High levels of turbidity have weakened reproductive barriers in cichlids found in African lakes because these fish rely in part on visual cues for mate selection (Seehausen et al . 1997). Crappies are often found in impoundments where turbidity can be quite high, and previous authors have suggested that crappie hybridization may be related to habitat disturbance. However, as far as we know, no one has investigated if hybridization rates of Pomoxis are correlated with any environmental factors. We provide additional discussion on crappie in Section 6.5 (on community ecology) of this chapter.

6.4.3 Human impacts and need for further research Fishing pressure can have important effects on crappie population dynamics. Fisheries for crappie often represent a large portion of total angler effort, especially in impoundments (Colvin 1991a; Webb and Ott 1991). Unlike the high proportion of catch-and-release angling in the fishery for Micropterus species (Quinn 1996; Noble 2002), crappies are typically harvested by anglers (Allen and Miranda 1996). Under conditions of strong fishing pressure, age and size structure of crappie populations can become truncated due to removal of older, larger individuals (Colvin 1991a). Stunted crappie populations were often thought to be the result of high densities from strong recruitment. However, high fishing pressure on smaller fish could prevent the recruitment of individuals to older ages and larger sizes, resulting in growth overfishing (Webb and Ott 1991). Removal of older age classes can result in more variable population dynamics (and hence, fishery yields), because recruitment of age-0 cohorts, often a highly variable process in space and time, makes up a relatively larger portion of the total population (Colvin 1991a). A potential outcome of fishing pressure on older, larger individuals being sustained over long enough periods of time is that age and size at maturation may shift down, resulting in stunted size structure and reduced fishing yields (Conover and Munch 2002). Bag and size limits have been used successfully to protect smaller individuals in order to allow more fish to survive to older age classes (Colvin 1991b; Webb and Ott 1991). However, differences among populations in growth rates and natural mortality can add variability to effects of size limits on crappie fisheries (Bister et al . 2002; Isermann et al . 2002). Crappie species are similar to other centrarchids in that nesting males provide parental protection to their offspring (Siefert 1968), therefore, removal of parental males would presumably have a detrimental effect on nest success. The impact of fishing pressure on nest success might be even stronger than the effects documented for Micropterus species, because unlike bass, crappie are not typically released after capture. At the same time, the relatively compressed time frame of crappie parental care may reduce time of vulnerability. As far as we know, the effects of angling parental males off nests on offspring survival and cohort recruitment have not been examined. Beyond rock bass and crappie, there are a variety of interesting species in this group of “other centrarchids” that remain to be fully or even partially studied. Based on investigations into the life histories, population dynamics, and communitylevel interactions of other centrarchids, it seems reasonable to conclude that each of the relatively unstudied species could play important ecological roles in the aquatic systems they inhabit. In addition, for any of these species facing habitat-related threats, more basic biological and ecological information will be needed for effective protection and conservation. The Sacramento perch (Archoplites interruptus) provides an example of both the potential for ecological harm from indiscriminate introductions of nonnative centrarchids and of the need for more research on the nongame species of

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Centrarchidae. The Sacramento perch is the only native centrarchid west of the Rocky Mountains and is thought to contain ancestral traits from the family (Aceituno and Nicola 1976). The decline of this species in the early twentieth century coincided with both the introduction of nonnative centrarchids (black crappie, bluegill, largemouth bass) and the manipulation of the natural hydrologic regime of various streams and rivers in the Sacramento perch’s range (Marchetti 1999). Sacramento perch are adapted to rivers with variable hydrologic regimes and, therefore, they have a wide physiological tolerance for conditions such as alkalinity. However, Sacramento perch are less aggressive than centrarchids such as bluegill and have been shown to be competitively inferior to these species (Marchetti 1999). Furthermore, Sacramento perch may not have the appropriate behaviors to cope with either nest predation by bluegill (Murphy 1948) or predation on juveniles and adults by largemouth bass (Marchetti 1999). Disruption of patterns of natural hydrologic disturbance may have allowed nonnative centrarchids to establish and out-compete Sacramento perch, resulting in local extirpations within its native range, such that mainly transplanted populations remain today. Evolutionarily, the Sacramento perch occupies a unique position in the family due to its historic isolation, and the extinction of this species in its native range would represent a tremendous loss. We argue that the story of this species should serve as a wake-up call to deepen our understanding of the relatively unstudied representatives of Centrarchidae before they face similar threats to their persistence or, worse, are gone before we can fully understand their ecological roles and evolutionary legacies. In particular, we recommend increased effort toward study of centrarchids that occupy restricted geographic ranges or unique ecological niches relative to other members of this family (e.g., bantam sunfish, Roanoke bass, Guadalupe bass) as these species represent significant evolutionary developments and are often the most at risk of extinction.

6.5 Community ecology Competition and predation are two important biological interactions that can structure ecological communities, and we address each here for centrarchids. We start by examining the role of competition in determining community organization and some of the important work done in these areas with Lepomis spp. Next, we explore the general ways in which predation can structure communities, through size-selective processes and both direct and indirect effects. Finally, we discuss dynamics and control of food webs. Within these food webs, ontogenetic diet shifts can dramatically change the role of a fish species within a community; species can operate at times as competitors and at other times as predators. Gulland (1982) observed that “fish have no direct terrestrial counterparts—a fox or lion does not start competing with mice.” First, larval fish are one component of a complex plankton community that compete with one another (Frank and Leggett 1994), and aggregation of species according to trophic levels is clearly inappropriate at this stage. However, as they grow, some species switch to piscivory and many interactions within communities become size-dependent. Often, competition and predation can interact with habitat to determine community structure. One important caveat should be mentioned: although these processes have proven to be extremely important in shaping community structure, an increasing number of studies have suggested that communities are not determined solely by interactions among component species. Rather, environmental variation may reduce the local abundances of many populations, decreasing the opportunity for competition and other interactions between species (Wiens 1977). In these situations, local assemblages of species may be more influenced by environmental or autecological factors than by species interactions. Understanding the relative importance of predation, competition, and stochastic effects in determining communities continues to be an important focus of ecology in general, as well as specifically for centrarchids.

6.5.1 Competition Centrarchids have played an important role in the development of competition theory. Early work, for example, focused on examination of food habits and diet overlap of sunfish species in Lake Opinicon (Keast and Welsh 1968; Keast 1978). Subsequent studies found evidence for competition as a process shaping communities by examining resource utilization of three sunfish species—bluegill, green sunfish, and pumpkinseed. In one study, ecological changes (niche shifts) were observed for the three species when grown in combination (Werner and Hall 1976). In this study, all three species

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preferred foraging in vegetation when alone, reflecting the rich resource base in that habitat. When together, however, green sunfish continued to concentrate in this area, bluegill switched to open-water areas, and pumpkinseed switched to benthic habitats. As such, a niche separation occurred as bluegill and pumpkinseed opted for different habitats and prey types due to competitive pressures, each choosing the environment more suited to its morphology and behavior. A strong asymmetry in the competition between green sunfish and bluegill sunfish was also found, favoring green sunfish in vegetated habitat (Werner and Hall 1977). Open-water habitat, which contains smaller prey, provides a competitive refuge for bluegill that handle smaller items more efficiently. In general, bluegill are more flexible in their habitat and prey utilization, whereas green sunfish are more aggressive and make fewer changes in the presence of congeners. It is important to note that the intensity of competitive interactions among sunfish is seasonally dynamic, with overlap in habitats among species determined by the relationship between resource levels and foraging efficiencies; as resources decline competitive pressures increase, and habitat shifts are likely to occur within these fish communities. Competition among sunfishes is also influenced by sometimes complex interactions with habitat and other fish species within the community, especially centrarchid predators (Mittelbach 1984, 1986; Osenberg et al . 1988). These topics will be covered further in the section on food-web dynamics.

6.5.2 Predator effects 6.5.2.1 Size-selective predation The size-selective nature of fish predation and its direct effects on zooplankton and fish are well understood (e.g., Brooks and Dodson 1965; O’Brien et al . 1976). As with many zooplanktivores, bluegill generally select the largest zooplankton available and can drive larger species to extinction. Declines in the larger individuals within populations of coexisting cladocerans can increase food resources (phytoplankton) for remaining zooplankters (Vanni 1987). In some cases, the increase in fitness of remaining individuals compensates for predator loss, the net result being that predation has little effect on prey population density. Largmouth bass are also size-selective predators (Lawrence 1957), but gape limitations often complicate interpretation of field data. As a result, it is often unclear whether diet composition is the result of a passive or active process for many piscivores. Largemouth bass and bluegill are commonly found together in the littoral zone of freshwater lakes and ponds throughout North America. Juvenile bluegill seek refuge in littoral habitats until they attain a large enough size (around 75-mm total length) to release them from gape-limited, size-selective predators like largemouth bass (Werner and Hall, 1988). Sizeselective predation by largemouth bass has been shown to differentially affect survival of bluegill cohorts, with higher mortality on early-spawned fish (Santucci and Wahl 2003). This may set up a trade-off in sunfish timing of reproduction; earlier spawners may have offspring that face high predation, and later spawners may produce larvae with poorer overwinter survival prospects. In a mid-latitude lake, overwinter mortality was not important (Santucci and Wahl 2003), but these effects could be important at other latitudes. Studies with other prey of largemouth bass (e.g., gizzard shad, Dorosoma cepedianum, and threadfin shad, D. patenense) have shown how spring water temperature and resulting spawning time can also affect predator–prey interactions (Adams and DeAngelis 1987). If spring water temperatures and spawning allow largemouth bass to gain a size advantage on young shad, then bass can maintain high growth rates. If spawning is delayed, YOY bass can be too small to feed on shad when they become available. Bass growth on non-fish prey such as benthic invertebrates and zooplankton is slowed, ultimately leading to poor overwinter survival and low recruitment. In some studies, overwinter mortality has been shown to be sizedependent for both smallmouth (Shuter et al . 1980) and largemouth bass (Adams et al . 1982), with large fish surviving better than small ones. Others have found that postwinter abundance of largemouth bass is not related to prewinter size, but rather dictated by the abundance of age-0 bass at the end of the first growing season, regardless of size (Fuhr et al . 2002).

6.5.2.2 Direct and indirect effects Some of the earliest attempts to understand predator–prey relationships in centrarchid communities examined interactions in small ponds. Swingle (1950b) developed the concept of balance in largemouth bass and bluegill populations. He

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proposed relationships between the weight of piscivores (largemouth bass) and forage fish (bluegill) that would occur in balanced (ratio of 1:3 or 1:4) and unbalanced populations. Balanced populations were those that could be repeatedly harvested at some level on an annual basis and maintain a preferred size structure. These hypotheses assumed a direct predator–prey relationship between largemouth bass and bluegill (Bennett 1954). As largemouth bass can be relatively omnivorous, Bennett (1951) found that bass populations could attain good population structure in the absence of bluegill prey. These early studies suggested some of the complex interactions that have subsequently been shown to occur within centrarchid communities (see the section on food-web dynamics). Predators can also have important effects on growth and recruitment of prey populations. For example, crappie growth is strongly density-dependent, and populations can be characterized as having either high recruitment with small size structure or low recruitment with large size structure (Guy and Willis 1995). A number of predators including northern pike (Esox lucius), largemouth bass, walleye (Sander vitreus), and saugeye (sauger Sander canadensis × walleye) have been associated with decreased recruitment and increased growth of crappie (Gabelhouse 1984; Willis et al . 1984; Boxrucker 2002; McKeown and Mooradian 2002; Galinat et al . 2002). However, the influence of predator abundance on mortality of YOY crappie can vary based on the availability of other, more vulnerable prey (McKeown and Mooradian 2002). In addition to direct effects, predators can influence prey through indirect pathways. Small centrarchids often alter their habitat choice or activity levels in the presence of predators (Werner and Gilliam 1984). Bluegill and pumpkinseed will often occupy littoral vegetation as a refuge from predation by largemouth bass, and congregation in these habitats can lead to increased competition (Mittelbach 1984; Mittelbach and Chesson 1987). These indirect predatory effects can result in competitive elimination of pumpkinseed, even if the adults of these two species use separate resources. The net impact of predators within communities has traditionally been viewed as the sum of pair-wise effects of individual predators on prey. However, studies on effects of multiple predators have more recently begun to address indirect effects. These combined effects on prey can be additive (Van Buskirk 1988) or nonadditive (Soluk 1993). Behavioral responses of prey appear to be an essential component in generating nonadditive effects. Prey behaviors that increase encounter rates with one of the two predators generally result in consumption greater than expected (“net facilitation”) whereas behaviors that decrease encounter rate with one or both predators lower consumption (“net interference”). Aquatic food webs also commonly contain both vertebrate and invertebrate predators that interact through direct and indirect pathways. Within stream communities, multiple predators are known to have potentially strong interactive effects on prey abundances (Soluk and Collins 1988; Soluk 1993). In these systems, interactions between fish and invertebrate prey can be nonadditive and can vary across prey densities and among prey taxa. These interactions were explored in lentic systems using juvenile bluegill (a searching predator), larval odonates (an ambush predator), and their mayfly larval prey (Figure 6.3; Swisher et al . 1998). In that investigation, sunfish and dragonfly predation exceeded additivity at low habitat complexity, but were additive at higher levels of complexity. At low habitat complexity, sunfish captured more mayfly larvae than expected in the presence of dragonflies than in their absence, while mayfly consumption by dragonflies was unchanged in the presence of fish. Mayflies escape capture during attacks by dragonflies by swimming away and this movement likely attracts attention and attacks by bluegill. Both the behavioral attributes of the predators and prey, as well

Indirect effects Sunfish (search predator)

Larval odonates (ambush predator)

Mayfly larvae

+

Figure 6.3 Example of indirect interactions among two predators (sunfish, larval odonates) with differing foraging strategies and their common prey (mayfly larvae). Solid lines point in the direction of energy transfer and the dashed line indicates indirect effects.

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as the structural complexity of their habitat affected the encounter rates, and thus their net interaction. Prey density and habitat complexity affect individual predators, but they may also affect interactions between multiple predators and thus their relative importance in shaping communities.

6.5.2.3 Bioenergetics Bioenergetic modeling (Chapter 7) can be an important tool for examining the implications of predation in aquatic communities. Estimates of growth and diets, along with water temperature data, can be used to predict food consumption rates of predators. These estimates of consumption from bioenergetic models can be used to assess predatory demand on prey populations (Ney 1993) and to understand a variety of predator–prey interactions within aquatic communities. As an example, Santucci and Wahl (2003) used bioenergetic simulations combined with field sampling to show that bluegill that spawned early in the season suffered higher mortality from largemouth bass than those that spawned later, suggesting that predation is an important mechanism regulating recruitment. As shown in this example, bioenergetic models can be used to help understand the effects of predators on aquatic communities and to provide insight into size-structured interactions. This topic is covered extensively in Chapter 7 of this volume.

6.5.3 Food-web dynamics Examining food-web dynamics provides a useful way to understand the combined effects of competition and predation within a community. Both predation and competition can regulate relationships between trophic levels within food webs and may, therefore, work in concert to structure aquatic communities. We start this section by discussing some of the community-level processes associated with ontogenetic diet and habitat shifts of centrarchids, focusing specifically on the influence of predation. We then describe some of the many ways in which fishes can control food webs, including both top-down and bottom-up processes.

6.5.3.1 Ontogenetic diet shifts and predatory effects Predation risk is a major factor associated with ontogentic diet and habitat shifts (and associated foraging abilities) of most lepomids, primarily due to the fact that their relatively small body size renders them vulnerable to piscivores throughout much (if not all) of their ontogeny. For bluegill, a number of investigations have clearly indicated that foraging behaviors and habitat use change when predators are present. Gotceitas (1990) showed that, when exposed to largemouth bass predators, bluegill changed their foraging strategy from one that maximized net energy intake to one that minimized the ratio of mortality risk to foraging rate gains (which he termed /f). Werner and Hall (1988) showed that ontogenetic habitat shifts by bluegill were largely driven by predation risk; they suggest that pelagic foraging on zooplankton is the most profitable for all size classes, but that individuals of intermediate size (and thus vulnerable to piscine predators) are restricted to suboptimal vegetated habitat to reduce predation risk. Many additional investigations have reached the conclusion that small sunfish are forced by predation risk into suboptimal vegetated habitats (e.g., Werner and Hall 1977; Mittelbach 1981, 1984). Food-web dynamics (the subject of this subsection) become particularly important at this point, as predatory effects lead to competitive interactions, which can further influence habitat selection by sunfish. Ample evidence supports the conclusion that sunfish refuging in vegetated areas are forced into competitive interactions that can also influence their life histories and population structure. For example, bluegill and pumpkinseed show significant dietary overlap as juveniles despite habitat separation as adults (Mittelbach 1984). Overlap at the small sizes is due, at least in part, to piscivorous predators forcing both species to share vegetated habitat (Mittelbach 1984). The results of these competitive interactions can cause decreases in growth rates for both species at the juvenile stage (Mittelbach 1986, 1988; Osenberg et al . 1988), which can be associated with other life-history changes such as timing of maturation and body size. Ontogenetic change in diet and habitat use is a good illustration of how crappies are ecologically intermediate between black basses and lepomids. Bluegill have pelagic larvae that feed on zooplankton until, as juveniles, they migrate inshore to

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Largemouth bass, walleye, muskellunge, channel catfish

Humans

Bluegill

Gizzard shad

Zooplankton

Benthic invertebrates

Phytoplankton

Aquatic plants Nutrient

Figure 6.4 Example of complex food–web interactions common in many lake ecosystems among top predators (piscivores and humans), secondary consumers (bluegill and gizzard shad), primary consumers (zooplankton and benthic invertebrates), primary producers (phytoplankton and aquatic plants), and nutrients.

the littoral zone and feed on invertebrates. Largemouth bass YOY stay in the littoral zone throughout development where they have a brief planktivory phase, transition quickly to larger invertebrates (mainly insect larvae), and become piscivorous before the end of their first growing season. Crappies are similar to bluegill in that they make a transition from the pelagic to the littoral zone as larger juveniles, yet they are also similar to largemouth bass because they develop a piscivorous diet (Ellison 1984; O’Brien et al . 1984). Crappies differ from other centrarchids in that they spend a larger portion of their early life history feeding in the pelagic zone on zooplankton (Mathur and Robbins 1971; O’Brien et al . 1984). Complex interactions among Micropterus species and their prey are common (Figure 6.4), and lepomids can influence piscivorous predators at early life stages. In fact, the most important predators on bass nests are often the same lepomids whose offspring will in turn be prey for the surviving YOY bass (Heidinger 1975; Colgan and Brown 1988). Patterns of growth and survival that result from differences in the timing of ontogenetic diet shifts by largemouth bass are, to a large degree, dictated by the influence of other members of the community. Largemouth bass begin exogenous feeding by preying upon zooplankton. Differences in the timing of zooplankton peak abundances and variation in zooplankton community composition could influence bass growth and survival, but this issue has not been closely studied. However, largemouth bass typically incorporate larger invertebrates (macro invertebrates), such as insect larvae, into their diets very quickly in their development. Variation in the composition and abundance of the macro-invertebrate community leads to variation in YOY largemouth bass growth, with a subsequent effect on the timing of age-0 bass shifts to piscivory (Olson 1996). Fish species that are the primary prey of piscivorous bass (such as lepomids) also compete with age-0 bass for these same invertebrate prey items. Competition with species that will be its future prey results in a complex pattern of delayed piscivory due to reduced growth and, potentially, recruitment bottlenecks due to increased size-specific mortality (Olson et al . 1995). More than just prey for bass, species such as bluegill are also important competitors that can shape ontogenetic shifts in bass.

6.5.3.2 Control of food webs and trophic cascades One explanation for the role of fish predation in regulating aquatic food webs that has received much attention in the literature is the concept of trophic cascades. Cascading trophic interactions have been used to explain differences in productivity among lakes with similar nutrient supplies but different food webs. The trophic cascade hypothesis can be broken down into two components—top-down and bottom-up effects. Top-down effects can be instigated by an increase in piscivore biomass that influences subsequent levels in an alternating fashion (lower planktivore, higher zooplankton,

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Bottom-up

Middle-out

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Top-down

Piscivore

; Planktivore

; Herbivore

; Phytoplankton

; Nutrients Figure 6.5 Bottom-up, middle-out, and top-down control of trophic interactions in aquatic food webs. Arrows indicate biomass responses of each trophic level within the food web.

and lower phytoplankton biomasses; Carpenter et al . 1985, Figure 6.5). Bottom-up effects can also be propagated through the food web, but rather than alternating among trophic levels, effects are observed in the same direction (i.e. increased productivity results in increased biomass at each trophic level). Several early demonstrations of trophic cascades examined effects of largemouth bass on lake ecosystems. However, many of the experiments conducted have involved extreme manipulations of predation in relatively artificial systems (fish compared to no fish; high densities of piscivores relative to planktivores; Crowder et al . 1988). In addition, prey species examined in these studies have been highly vulnerable (cyprinids or conspecifics), rather than less susceptible prey species such as centrarchids or clupeids (Wahl and Stein 1988; Einfalt and Wahl 1997). As a result, it is not clear if the predator effects observed can be sustained over a long period of time (Crowder et al . 1988). Top-down effects are expected to be strong at the top of the food web and weaken toward the bottom, whereas bottom-up strength should weaken toward the top of the food web. In a field study, McQueen et al . (1989) examined correlations between adjacent trophic levels, and found a negative correlation between number of piscivores and planktivores, a weaker correlation between number of planktivores and zooplankton biomass, no correlation between zooplankton biomass and chlorophyll a concentration, and a strong correlation between chlorophyll a and phosphorus. The lack of correlation between zooplankton and chlorophyll a suggests the trophic cascade uncouples at the zooplankton–phytoplankton link and must be taken into account whenever these principles are used to manage centrarchid communities (DeMelo et al . 1992). Middle-out regulation by species such as gizzard shad has also been suggested for some aquatic communities (Stein et al . 1995). Because of their high fecundity and low vulnerability, shad are not typically controlled by fish predators. In addition, their omnivorous feeding habits allow them to switch from zooplankton prey to detritus and phytoplankton depending on prey profitabilities. These factors, combined with their high reproductive potential, often make gizzard shad the dominant fish species (in terms of biomass) in reservoir ecosystems (Vanni et al . 2005). As a result, gizzard shad can regulate community composition rather than being regulated by top-down or bottom-up processes (Figure 6.5). The presence of these strong interactors can also have important effects on the population ecology of centrarchids. Age-0 gizzard shad can be important prey items for largemouth bass, but gizzard shad tend to have a small window of vulnerability due to rapid growth rates. Adult gizzard shad and older juveniles feed on detritus, and this interaction with bottom sediments typically results in high turbidity and increased nutrient availability through recycling to phytoplankton (Schaus and Vanni 2000). The result of this bottom-processing behavior is that dense gizzard shad populations can reduce the abundance of submerged vegetation used by both adult largemouth bass (for spawning and foraging) and YOY bass (for nursery areas and foraging and refuging). As bass are visual predators, the increased turbidity can also impair their foraging efficiency. Complex community-based interactions among gizzard shad, bluegill, crappie, and largemouth bass can result from the direct and indirect effects of predation and from the outcome of sized-based competition. Larval gizzard shad can reduce the abundance of zooplankton prey required by larval bluegill (Welker et al . 1994), resulting in fewer juvenile bluegill migrating inshore where they are preyed upon by largemouth bass. This reduction in juvenile bluegill abundance can result

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in lower growth rates for YOY largemouth bass (Garvey et al . 1998b). In contrast, evidence for a negative effect of shad abundance on crappie growth and survival has been inconsistent (McDonough and Buchanan 1991; McInerny and Degan 1991; Slipke et al . 1998). Differential foraging behavior of bluegill and gizzard shad as juveniles can structure zooplankton and benthos communities and influence growth of juvenile largemouth bass. In mesocosm experiments, juvenile largemouth bass lost weight in the presence of juvenile bluegill, but grew at similar rates with gizzard shad and fishless controls (Aday et al . 2005). Results of that experiment led the authors to suggest that bluegill compete with juvenile largemouth bass for preferred prey items, thereby limiting largemouth bass growth. As a result, larger gizzard shad may not have the negative effects on piscivores that have been observed with smaller individuals. The presence of gizzard shad can also reduce adult bluegill growth rates and size structure (Aday et al . 2003c). Higher turbidity and lower benthic invertebrate densities in systems with gizzard shad may reduce foraging success and growth of adult bluegill. In addition, the presence of gizzard shad as alternate prey for largemouth bass can result in higher bluegill densities and slower growth. These complex effects of gizzard shad on adult bluegill can occur through mechanisms other than competition for food resources (Aday et al . 2003c). Knowledge of size-structured interactions within these fish communities provides valuable information for developing initiatives aimed at maximizing growth of important sportfish such as bluegill and largemouth bass.

6.6 Conclusions The diversity of species in the family Centrarchidae is evident in the myriad factors that shape the population structures and ecological interactions of each. Despite the presence of 34 species in the family, clearly the vast majority of research has been directed at only a few of the members, primarily bluegill, pumpkinseed, crappie, largemouth, and smallmouth bass. For the lepomids, data have been collected on their reproductive behaviors, habitat and prey use, life histories and associated growth rates and size structures. For bluegill, in particular, that information has included the elucidation of interesting social interactions that have the potential to influence individual life histories, population dynamics, and community structure. For the Micropterinae, we now understand much about the predatory role that they play in aquatic systems, and the ways in which their life histories are organized around this ecological niche. To achieve a size advantage over important prey species, Micropterus species have developed patterns of life history and behavior that include synchronous reproduction, delayed maturity, parental care, and precocious piscivory, a life-history pattern intermediate between that of equilibrium and periodic strategists (as defined in Winemiller and Rose 1992). At the community level, we now understand much about the processes that shape predator–prey dynamics and food-web structure. Competition among sunfish can be influenced by predatory bass, and bass life histories can be shaped by early competition with species that ultimately become their prey. Ontogenetic diet and habitat shifts of centrarchids in many populations are influenced by complex interactions with competitors and predators. These interactions are clearly beginning to have an effect on species distributions and aquatic communities at the ecosystem and even global scale, as continued introductions of centrarchids outside of their indigenous range impact the biota of native flora and fauna. Despite our understanding of many aspects of the population and community ecology of centrarchids, a great deal of work remains for many of the family’s less-studied species (28 of the 34 species). For populations of all centrarchids, understanding mechanisms associated with population, community, and ecosystem ecology will play a central role in their management.

6.7 Current and future directions To manage centrarchid populations more effectively, scientists and managers have been forced to expand their perspectives on the factors that influence population- and community-level processes. Watershed-level features (such as land use) and regional-level variation in environmental conditions (such as discharge) can influence nutrient subsidies and energy flow patterns with subsequent effects on centrarchid life histories (Garvey et al . 2000; Vanni et al . 2005), and must be considered in future investigations and management initiatives. An important change in approach to the study of fish populations has been to investigate the influences of individuals, populations, and communities on ecosystem-level processes (Miranda and Dibble 2002). On an individual level, the

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behavior, physiology, growth and, ultimately, fitness of individuals determines the fate of populations. The difficulty lies in translating the relative influence of individual variation up to population-level effects. Typically, population ecologists and fishery managers must summarize and simplify individual variation into population-level averages because of the challenge in determining the importance of individual traits for population-level processes. Beyond this challenge is the importance of considering community- and ecosystem-level effects. In many ways, a community-based approach to studying fish populations has been used for a long time. For example, tracking the abundance of important prey species, competitors, and predators is an approach that tacitly acknowledges the need to understand individual interactions as we attempt to quantify population and community dynamics. The main challenge of community-based approaches has been the difficulty in producing generalities that can guide management, due to the high degree of among-community variation in trophic structure, and the identity and strength of among-species interactions. Focusing on ecosystem processes is currently a highly favored approach in fisheries ecology. This approach encompasses watershed and region-level processes such as nutrient dynamics and energy flow. An ecosystem-based approach to the study of population dynamics has many challenges. From a management perspective, the difficulty lies in coordinating the cooperation of all agencies and affected user groups within the region/ecosystem that the population of interest is embedded. From a scientific perspective, difficulties include defining the appropriate boundaries of the ecosystem (e.g., lakeshore, riparian zones of all tributaries in watershed, ecoregion) and understanding the actual mechanisms involved in translating ecosystem-level processes to population-level effects. Despite the challenges posed by all of these approaches, investigations into the operation of lower- and higher-order processes on the ecology of fishes represent a significant development in our understanding of centrarchid ecology and management. Centrarchids should continue to serve as a model system for understanding individual variation as well as population- and community-level processes, and this system should provide a strong foundation and continued opportunities for expanding investigations to the watershed and ecosystem levels.

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Travnichek, V. H., M. J. Maceina, and R. A. Dunham. 1996a. Hatching time and early growth of age-0 black crappies, white crappies, and their naturally produced F1 hybrids in Weiss Lake, Alabama. Transactions of the American Fisheries Society 125: 334–337. Travnichek, V. H., M. J. Maceina, S. M. Smith, and R. A. Dunham. 1996b. Natural hybridization between black and white crappies (Pomoxis) in 10 Alabama reservoirs. American Midland Naturalist 135: 310–316. Travnichek, V. H., M. J. Maceina, M. C. Wooten, and R. A. Dunham. 1997. Symmetrical hybridization between black crappie and white crappie in an Alabama reservoir based on analysis of the cytochrome-b gene. Transactions of the American Fisheries Society 126: 127–132. Trivers, R. L. 1972. Parental investment and sexual selection. Pages 136–179 in B. Campbell, editor. Sexual Selection and the Descent of Man. Aldine-Atherton, Chicago, IL. Turchin, P. 2003. Complex Population Dynamics: A Theoretical/Empirical Synthesis. Princeton University Press, Princeton, NJ. Van Buskirk, J. 1988. Interactive effects of dragonfly predation in experimental pond communities. Ecology 69: 857–867. Vanni, M. J. 1987. Indirect effect of predators on age-structured prey populations: planktivorous fish and zoolplankton. Pages 149–160 in E. C. Kerfoot and A. Sih, editors. Predation: Direct and Indirect Impacts on Aquatic Communities. University Press of New England, Dartmouth, New Hampshire. Vanni, M. J., K. K. Arend, M. T. Bremigan, D. B. Bunnell, J. E. Garvey, M. J. Gonzalez, W. H. Renwick, P. A. Soranno, and R. A. Stein. 2005. Linking landscapes and food webs: effects of omnivorous fish and watersheds on reservoir ecosystems. Bioscience 55: 155–167. Wahl, D. H. and R. A. Stein. 1988. Selective predation by three esocids: the role of prey behavior and morphology. Transactions of the American Fisheries Society 117: 142–151. Walters, J., C. Annett, and G. Siegwarth. 2000. Breeding ecology and behavior of Ozark bass Ambloplites constellatus. American Midland Naturalist 144: 423–427. Waters, D. S. and R. L. Noble. 2004. Spawning season and nest fidelity of largemouth bass in a tropical reservoir. North American Journal of Fisheries Management 24: 1240–1251. Wainwright, P. C. 1996. Ecological explanation through functional morphology: the feeding biology of sunfishes. Ecology 77: 1336–1343. Webb, M. A. and R. A. Ott, Jr. 1991. Effects of length and bag limits on population structure and harvest of white crappies in three Texas reservoirs. North American Journal of Fisheries Management 11: 614–622. Welker, M. T., C. L. Pierce, and D. H. Wahl. 1994. Growth and survival of larval fishes: the roles of competition and zooplankton abundance. Transactions of the American Fisheries Society 123: 703–717. Werner, E. E. and D. J. Hall. 1976. Niche shifts in sunfishes: experimental evidence and significance. Science 191: 404–406. Werner, E. E. and D. J. Hall. 1977. Competition and habitat shift in two sunfishes (Centrachidae). Ecology 58: 869–876. Werner, E. E. and J. F. Gilliam. 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology and Systemmatics 15: 393–425. Werner, E. E. and D. J. Hall. 1988. Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off. Ecology 69: 1352–1366. Werner, E. E., G. G. Mittelbach, D. J. Hall, and J. F. Gilliam. 1983. Experimental tests of optimal habitat use in fish: the role of relative habitat profitability. Ecology 64: 1525–1539. Weyl, O. and T. Hecht. 1999. A successful population of largemouth bass, Micropterus salmoides, in a subtropical lake in Mozambique. Environmental Biology of Fishes 54: 53–66. Whiteman, H. H. 1997. Maintenance of polymorphism promoted by sex-specific fitness payoffs. Evolution 51: 2039–2044. Wiens, J. A. 1977. On competition and variable environments. American Scientist 65: 590–597. Williams, G. C. 1966. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. American Naturalist 100: 687–690. Willis, D. W., J. F. Smeltzer, and S. A. Flickinger. 1984. Characteristics of a crappie population in an unfished small impoundment containing northern pike. North American Journal of Fisheries Management 4: 385–389. Winemiller, K. O. and K. A. Rose. 1992. Patterns of life-history diversification in North American fishes: implications for population regulation. Canadian Journal of Fisheries and Aquatic Sciences 49: 2196–2218.

Chapter 7

Centrarchid energetics M. S. Bevelhimer and J. E. Breck

7.1 Introduction The ability to understand the uptake and utilization of energy by fish is crucial to many aspects of fisheries management and conservation. Thus, it is no wonder that studies at all scales of bioenergetics investigation are now common in the scientific literature. Whereas investigations of various components of fish bioenergetics (such as oxygen consumption and growth efficiency) have been undertaken for decades, the integration of these individual components into a holistic view of individual and population energetics has only become common in the past 20 years or so. Because bioenergetics is intertwined with many of the chapter subjects throughout this book (such as growth and reproduction), we defer to those chapters for detailed discussion. In this chapter we present the importance of energetics to understanding centrarchid ecology and management, discuss the use of bioenergetics models as a tool for research and management of centrarchid species, describe bioenergetics model development and parameter derivation, compare bioenergetics among centrarchid species, and identify knowledge gaps in centrarchid energetics. The study of fish bioenergetics includes research into various aspects of energy utilization as either energetic costs associated with metabolism, waste products, and activity, or the assimilation of energy into tissue (somatic and gonadal). Bioenergetics models have been developed as a mathematical means to balance energy uptake and loss for the purpose of predicting an unknown component of the equation, such as growth or food consumption, when the other components are known. These models, in one form or another, have been used sporadically in fisheries science since early descriptions by Winberg (1956) and others. In the mid-1970s, Kitchell et al . (1977) developed the first bioenergetics model for bluegill (Lepomis macrochirus) as part of research sponsored by the Eastern Deciduous Forest Biome, part of the U.S. International Biological Program. Although not the first paper to present a fish bioenergetics model, Kitchell et al . (1974) did encourage other researchers (particularly in North America) to develop and apply bioenergetics models for a variety of fisheries applications. Models that followed in the same architecture as that of Kitchell et al . (1974) have come to be known as the “Wisconsin” bioenergetics models (though they could just as easily have been called the “Oak Ridge” model given that half of the six authors were from Oak Ridge National Laboratory). Hewett and Johnson (1987) produced an easy-to-use software package based on the “Wisconsin” model that made bioenergetics models for a variety of species available to fisheries managers and researchers. This package has been released twice since in updated versions (Hewett and Johnson 1992; Hanson et al . 1997). However, given the simplicity of the basic model, many researchers still prefer to code their own models in a variety of modeling platforms with modifications to meet specific needs. Adams and Breck (1990) and Hansen (1993) provide informative reviews on the development and application of bioenergetics models in fisheries science. The recent increase in the development of bioenergetics models stems from (i) the development of better techniques and technology for understanding individual energetic components, (ii) the development of faster computers and user friendly software and programming platforms, and (iii) a realization by researchers and managers that models provide a means to investigate questions that are often difficult to answer with field studies. Bioenergetics models have been used to investigate a variety of fish management issues including stocking strategies, prey availability and utilization, environmental effects on growth rates, and habitat selection.

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Warren and Davis (1967) presented and Adams and Breck (1990) summarized a generalized form of the bioenergetics model that is the basis for most modeling efforts today: Consumption = metabolism + waste + growth or C = (Mr + Ma + SDA) + (F + U ) + (Gs + Gg ) where C, energy consumption; Mr , standard metabolism, Ma , increase in metabolism (above standard) due to activity; SDA, increase in metabolism due to specific dynamic action; F , waste loss due to egestion (feces); U , waste loss due to excretion (urine); Gs , somatic growth; and Gg , gonadal growth. All of these terms are rates that have dimensions of energy per unit time, such as kJ min−1 or kcal day−1 . In the following sections of this chapter we review the development of bioenergetics models for centrarchid species followed by a discussion of major components of fish energetics that affect fish growth and energy use. In particular, we discuss empirically derived relationships among energetic functions (i.e. consumption, metabolism, excretion, egestion, and growth) and the factors that affect them (e.g., size, temperature, dissolved oxygen, and activity).

7.2 Centrarchid bioenergetics models 7.2.1 Typical model applications The earliest centrarchid energy budgets are those presented for largemouth bass (Micropterus salmoides; Niimi and Beamish 1974) and bluegill (Kitchell et al . 1974). These studies combined the results from a variety of empirical studies on those aspects of fish energetics described earlier. Most of the bioenergetics models of centrarchid fishes are for three species—bluegill, largemouth bass, and smallmouth bass (M. dolomieui ). During our literature review, we also found one incidence each of models for white crappie (Pomoxis annularis), spotted bass (M. punctulatus), Sacramento perch (Archoplites interruptus), and a sunfish hybrid [green sunfish (L. cyanellus) × bluegill cross]. However, the sunfish hybrid model was merely a copy of a bluegill model, and the spotted bass model was really a borrowed smallmouth model. Published bioenergetics models for centrarchid species are summarized in Table 7.1. Bluegill bioenergetics models have been used to investigate a variety of questions including the effects on growth and food consumption of bluegill density, food availability, temperature, DO (dissolved oxygen), and pH. Usually these factors were investigated individually, but some studies looked at combinations of factors. Neill et al . (2004) recently published a model called “Ecophys.Fish” that evaluates simultaneously the effects of temporal variation in food, oxygen, temperature, pH, and salinity on fish growth. In the Ecophys.Fish model, the authors have coupled FEJ Fry’s concepts of “physiological classification of environment” and “metabolic scope for activity” with conventional bioenergetics. Model inputs include initial fish size and time series of temperature, pH, DO concentration, salinity, food availability, and energy content. Model outputs are food consumption, oxygen consumption, waste production, energy content of fish biomass, and growth. The model has been parameterized for two species, bluegill and red drum (Sciaenops ocellatus), and is available online. The first two models for largemouth bass were produced almost simultaneously to investigate energy partitioning and overwinter survival (Adams et al . 1982) and seasonal changes in condition (Rice 1981; Rice et al . 1983). These two models not only contained several common components based on laboratory studies of Beamish (1970, 1972, 1974), but also differed in many aspects. Researchers studying largemouth bass biology have used bioenergetics models to investigate the seasonality of prey abundance and bass growth, overwinter survival, seasonal changes in condition, individual- and population-level food consumption, juvenile survival and recruitment, thermal effects, latitudinal stock differences, and predatory effects on prey populations (Table 7.1).

7.2.2 Other model applications Aside from the normal applications of growth and food consumption evaluations, bioenergetics models have also been used for some not so common applications. Zweifel et al . (1999) and Slaughter et al . (2004) used bioenergetics models to

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Table 7.1 Summary of published application of bioenergetics models for centrarchid fishes. Species

Modeling summary

Source

Bluegill

Simulated effects of temperature and prey availability on seasonal growth compared to long-term laboratory and field observations

Kitchell et al. (1974)

Evaluated effects of increased YOY (young-of-year) mortality (decreased density) as a result of macrophyte harvesting on food consumption and growth

Breck and Kitchell (1979)

Effects of fry density and food availability on growth using IBM with bioenergetics component

Breck (1993)

Effects of food availability and temperature on habitat choice using IBM with bioenergetics component

Wildhaber and Lamberson (2004)

Effects of food availability, temperature, DO, and pH on food consumption and growth

Neill et al. (2004)

Hybrid sunfish (Green sunfish × bluegill)

Tested model predictions of growth and food consumption under feeding regimes that elicited compensatory growth responses (copy of bluegill model)

Whitledge et al. (1998)

Largemouth bass

Original construction and application of model

Rice (1981)

Investigated effects of seasonally fluctuating prey base on the seasonal allocation of consumed energy

Adams et al. (1982)

Estimated daily ration and cumulative food over a single season with several intervals of measured growth

Cochran and Rice (1982)

Investigation of seasonal changes in condition factor (i.e. weight loss) reveals that likely explanation is seasonal variation in consumption

Rice et al. (1983)

Field validation of model for adult largemouth bass; predicted food consumption using observed growth compared to observed consumption estimates

Rice and Cochran (1984)

Sensitivity analysis of model parameters

Bartell et al. (1986)

Demonstration of model use for estimating population-level lake-wide consumption rates

Carline (1987)

Investigated importance of spawning timing to growth and survival of juveniles, and recruitment to adult stages using IBM with bioenergetics component

Trebitz (1991)

Used laboratory results of adult growth at two temperatures and two rations to corroborate model

Whitledge and Hayward (1997)

Compared performance of two models to evaluate winter energy depletion in YOY as simulated in laboratory experiments

Wright et al. (1999)

Estimated long-term consumption rates for 100+ individuals based on individual growth rates measured in the field

Essington et al. (2000)

Investigated differences in consumed prey and growth in adults among lakes with different temperature regimes and prey bases

Yako et al. (2000)

Evaluated effects of consumption by predator population on numbers of stocked prey species

Paukert et al. (2003)

Compared estimates of annual prey consumption to that of conspecifics based on field observations

Raborn et al. (2003)

Evaluated potential for adults to control abundance of prey populations in small impoundments

Irwin et al. (2003) (continued)

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Table 7.1 (continued). Species

Modeling summary

Source

Tested model predictions of growth against lab results for juveniles from different latitudes at different rations and temperatures

Slaughter et al. (2004)

Sacramento perch

Developed to test the effects of various environmental stressors (e.g., temperature, DO, pH, and salinity) on growth for the purpose of assessing habitat quality

Woodley (PhD research; personal communication with Christa Woodley, UC Davis)

Smallmouth bass

Evaluated implications of climate change on overwinter survival and latitudinal distribution

Shuter and Post (1990)

Investigated effects of initial density and size-dependent predation on recruitment of YOY to yearling stage using IBM with bioenergetics component

DeAngelis et al. (1991)

Effects of alternative flow regimes on adult reproduction and juvenile growth and recruitment using IBM with bioenergetics component

Jager et al. (1993)

Modeled a multi-predator system to examine potential for top-down control on invasive prey species

Mayo et al. (1998)

Compared ability of models derived for different life stages (YOY, juvenile, adult) to predict growth and food consumption

Whitledge et al. (2003)

Evaluated increased food consumption demands to meet higher than expected activity levels measured with field telemetry

Cooke et al. (2001)

Compared estimates of annual prey consumption to that of conspecifics based on field observations

Raborn et al. (2003)

Modeled growth effects of summer stream temperatures as affected by riparian shading and groundwater input

Whitledge et al. (2006a)

Compared estimates of annual prey consumption to that of conspecifics based on field observations (copy of smallmouth bass model)

Raborn et al. (2003)

Spotted bass

White crappie

Original construction and application of model

Zweifel (2000)

Model predictions of consumption and growth compared to lab results to investigate presence of systematic errors in bioenergetics models

Bajer et al. (2004a)

Simulated effects of diet quality and interannual and inter-lake variation in warm water exposure during summer on growth

Bajer (2005)

assess variation in temperature-mediated growth and geographic distribution of smallmouth and largemouth bass. Slaughter et al . (2004) found that the largemouth bass bioenergetics model provided inaccurate predictions of growth for largemouth bass from different origins—Wisconsin, Alabama, and Florida. Woodley and Cech (personal communication with Christa Woodley, University of California at Davis) have recently developed a bioenergetics model for Sacramento perch to assess the quality of currently available habitat for this rare species and are investigating how individual time and energy budgets might translate into population changes. Rice (1990) used a largemouth bass model to demonstrate how it can be used to detect energetic deficiencies in fish that have been exposed to environmental stressors. He proposed two approaches. The first was to use a “healthy fish” model as a null hypothesis to determine whether an observed growth pattern can be explained by natural causes without stressor effects that alter the energy-budgeting process. The second approach was to incorporate known effects of a stressor on feeding, metabolic rate, or other energetic component to simulate indirect effects of the environmental stressor on growth.

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For some studies, the bioenergetics model is just a component of a larger model. For example, the growth component of many individual-based models (IBMs) is usually the standard bioenergetics model (DeAngelis et al . 1991; Trebitz 1991; Breck 1993; Jager et al . 1993). IBMs are used to model population dynamics by simulating habitat selection, feeding, reproduction, mortality, and growth of individual members of the population. The bioenergetics parameters in an IBM described in Breck (1993) came from those in Hewett and Johnson (1987), most of which were originally derived from Breck and Kitchell (1979). Breck’s IBM estimated daily growth of individual age-0 bluegill fry that foraged stochastically for prey in open-water or benthic habitats, and then grew according to the bioenergetics submodel. The model operated on a daily time-step and simulated growth through the first summer of life. In addition to growth, the bluegill IBM simulated foraging, prey dynamics, and natural mortality. Model predictions of the relationship between bluegill fry density and summer growth rate were verified with observations from pond experiments.

7.2.3 Model evolution and parameter borrowing A genealogy of largemouth bass models provides an interesting look at the progression of a species-specific set of models (Figure 7.1). The first largemouth bass model was developed as part of a Masters thesis (Rice 1981) and applied in various

Rice (1981) Adams et al. (1982) Rice et al. (1983) Cochran & Rice (1982) Rice & Cochran (1984) Bartell et al. (1986) Carline (1987) Essington et al. (2000)

Hewett & Johnson (19871)

Trebitz (1991)

Hewett & Johnson (19921) Wright et al. (1999)

Hanson et al.

(19971)

Whitledge & Hayward (1997) Wright et al. (1999) Yako et al. (2000)

Raborn et al. (2003) Irwin et al. (2003) Paukert et al. (2003) Slaughter et al. (2004) 1

Versions 1, 2, and 3 of the fish bioenergetics software published by Wisconsin Sea Grant

Figure 7.1 Lineage of largemouth bass bioenergetics models. Arrows connect studies to those from which equations were borrowed.

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ways as described in several follow-up publications by the original author and colleagues (Cochran and Rice 1982; Rice et al . 1983; Rice and Cochran 1984). The Rice et al . (1983) model was subsequently used by several other investigators (Bartell et al . 1986; Carline 1987; Trebitz 1991; Essington et al . 2000) and ultimately incorporated into the software produced by Hewett and Johnson (1987). Trebitz (1991) made modifications to the model, incorporating new parameter values to better simulate growth for juvenile fish and at cold temperatures. Some of Trebitz’s modifications were later included in the second version of the fish bioenergetics software (Hewett and Johnson 1992). Several studies were published using the largemouth bass model in version two of the software. The third version of the software (Hanson et al . 1997) included new species and other revisions, but the parameters for largemouth bass remained the same, and this version has been used in several studies since. Adams et al .’s (1982) model stands alone as the only largemouth bass derived independently of the Rice model. Wright et al . (1999) provide a comparison of two of the models—Trebitz (1991) and Hewett and Johnson (1992), which we discuss later in this chapter. Although fewer in number than largemouth bass models, most smallmouth bass models have been based on the first model by Shuter and Post (1990), which was developed to simulate the growth of age-0 fish. Hanson et al . (1997) used the parameters from Shuter and Post (1990) for age-0 smallmouth bass to develop a bioenergetics model that was included in version 3 of the fish bioenergetics software and erroneously listed as applicable for adult smallmouth bass. Whitledge et al . (2003) compared the Hanson model with the one they developed with empirical data for subadult and adult fish. Not surprisingly, they found the model that used adult-derived parameters more accurately simulated observed consumption and growth of older fish than the original model. The model developed by Whitledge et al . (2003) was subsequently used to evaluate summer growth of smallmouth bass in the field exposed to different natural thermal regimes (Whitledge et al . 2006a). Bioenergetics models are rarely developed by the same researcher or laboratory group that generated the original empirical data upon which model parameters are based. Researchers at the University of Missouri have developed a white crappie model based on metabolic and food consumption relationships determined within their own laboratory (Zweifel 2000). In subsequent years the original model was tested with additional experimental data and revised to address errors in parameter derivation and model development (Bajer et al . 2004a; Bajer 2005). Because their model was developed from empirical data on the same general stock of white crappie and has undergone such scrutiny and validation, we suspect it is one of the most accurate models developed. However, this model may still have trouble accurately simulating growth or consumption in stocks of different geographic or genetic origin. The question of whether bioenergetics models can be transferred to populations other than those from which parameters were derived is largely unanswered. A common occurrence in the development of bioenergetics modeling is the borrowing of parameter values from other species when values for the species of interest are not available. This is likely true to a small extent for all models, particularly for parameters related to egestion, excretion, and the cost of activity for which there is little species-specific data. At the other extreme are instances where nearly all parameters are borrowed, usually from species of the same genus. For example, Raborn et al . (2003) used a modeling approach to compare estimates of annual prey consumption among largemouth, smallmouth, and spotted bass. Because no model parameters were available for spotted bass, Raborn et al . (2003) used the same parameters for spotted bass that they used for smallmouth bass. Parameters they used for smallmouth bass were mostly different from largemouth bass parameters except those for egestion, excretion, and energy density.

7.2.4 Model evaluation A primary objective of several published studies was to evaluate model performance. Rice and Cochran (1984) corroborated the original Rice largemouth bass model by comparing observed consumption estimates from the field to predicted food consumption based on observed growth. Whitledge and Hayward (1997) used the results of controlled laboratory experiments to assess the accuracy of a largemouth bass model for adults exposed to two temperatures and two levels of feeding. Their statistical analysis indicated no significant deviations between predicted and observed mass at the end of each week of a 9-week experiment. Cumulative food consumption was underpredicted by about 9%, and the model performed better under normal ration than under ad libitum feeding. Similarly, Wright et al . (1999) used controlled growth studies to compare model predictions for largemouth bass and also found model accuracy varied with environmental conditions; the greatest growth underestimation occurred under high-latitude winter conditions.

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The finding of larger discrepancies between observed and modeled growth for winter periods compared to summer periods is a common one. Potential explanations are numerous. Incorrect parameters or functions for the effects of temperature on respiration and consumption can cause overestimates of respiration or underestimates of consumption for low temperatures. The models’ omission of seasonal variation in metabolic rate can cause modeled respiration rate in winter to be too high (Wohlschlag and Juliano 1959; Roberts 1964, 1966, 1967; Evans 1984). Models generally do not account for a reduction in metabolic rate as starvation proceeds (Glass 1968; Broekhuizen et al . 1994), as can occur during winter. Errors in estimates from field data can increase the discrepancy between modeled and measured growth. Field estimates of consumption during winter can be greatly influenced by the presence or absence in gut samples of a few large prey items. Lastly, a rare, large prey item could mean the difference between an increase and decrease in fish weight during a winter month, yet the frequency of rare diet items is difficult to measure accurately without large sample sizes (Diana 1987). More recently, Bajer et al . (2004b) used three centrarchid bioenergetics models (largemouth bass, smallmouth bass, and bluegill) and results from laboratory experiments to evaluate commonly occurring errors in model predictions. They concluded that bioenergetics models often contain consumption-dependent systematic errors that result in underestimated growth at low food consumption levels and overestimated growth at high levels. Bartell et al . (1986) performed a sensitivity analysis on all parameters of the model to identify those parameters that are most likely to cause uncertainty or error in model predictions of growth and consumption rates for three species including largemouth bass. Monte Carlo simulations and statistical analyses were used to rank parameter importance. They found that the order of parameter importance was model specific, but were able to generalize that those parameters with a high potential to introduce error included the realized fraction of maximum consumption rate (P value) and the allometric parameters (i.e. the weight-dependent exponent) for consumption and respiration. Studies, such as the above, designed specifically to evaluate bioenergetics models are crucial to developing a model framework with proper parameterization that can be useful for addressing fisheries management and conservation questions. The fact that many of these studies are finding common and recurring errors is not surprising given that some of the mechanistic relationships are still not entirely understood and a number of model parameters are often borrowed from other species or are crudely estimated. Fish physiologists and model developers should continue model and parameter evaluations such that fish bioenergetics are better understood and, whenever possible, make model revisions through mechanistic corrections instead of simply applying a correction factor.

7.3 Food consumption and feeding energetics 7.3.1 Food consumption rate Early studies indicated that temperature and body size influence food consumption of fishes. Pearse (1924) measured the weight of food consumed by three species of centrarchids (rock bass Ambloplites rupestris, pumpkinseed L. gibbosus, and largemouth bass). He recognized that smaller individuals consume a larger amount in relation to their body size than larger individuals. Hathaway (1927) seems to be the first to have demonstrated experimentally that three species of centrarchids (pumpkinseed, bluegill, and largemouth bass) consume more food (live earthworms) at 20◦ C than at 10◦ C. So, it was known very early that body size and temperature are the major factors influencing food consumption of fishes, including centrarchids. Markus (1932) measured voluntary consumption of minnows by largemouth bass over three consecutive 30-day periods during winter months; temperature was not tightly controlled. He noted that bass “take little or no food” when the temperature is around 4◦ C. Hunt (1960) measured voluntary food consumption for Florida bass (M. floridanus; which he called largemouth bass) and warmouth (L. gulosus), although temperature was not controlled. Additional studies of food consumption by largemouth bass include Lee (1966), Lewis et al . (1974), and Niimi and Beamish (1974), discussed later. In the first energetics model for bluegill growth, Kitchell et al . (1974) used the following function, derived by O’Neill et al . (1972), to account for temperature dependence of consumption: f (T ) = V X e(X(1 − V ))

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where V = (TM − T )/(TM − TO ); TM is the maximum temperature for feeding; TO is the optimal temperature for feeding, where the function reaches a maximum value; X = (Z 2 (1 + (1 + 40/Y )0.5 )2 )/400; Z = ln(θ )(TM − TO ); Y = ln(θ )(TM − TO + 2); and θ is a parameter similar to Q10 . This function first increases nearly exponentially with increasing temperature, similar to a Q10 relationship, then slowly increases to the maximum value of 1.0 at a temperature of TO , then declines steeply at high temperatures. They reported the following values for the temperature dependence of consumption by bluegill (Kitchell et al . 1974; see also Beitinger 1974): θ = 2.3; for juveniles TO = 31◦ C, TM = 37◦ C; for adults TO = 27◦ C, TM = 36◦ C. These values are included in Hanson et al . (1997). Hayward and Arnold (1996) measured the maximum daily consumption rate of adult white crappie (164–532 g) at 18, 21, 24, and 27◦ C. Consumption increased from 18 to 24◦ C, then decreased sharply at 27◦ C. The general pattern is qualitatively similar to the above temperature function. Hayward and Arnold (1996) note that the white crappie feeding response to temperature is more similar to that of coolwater species such as yellow perch (Perca flavescens) than to bluegill and largemouth bass, even though these latter two are also centrarchids. Niimi and Beamish (1974) determined consumption rate of different sizes of largemouth bass (8–150 g) at three different temperatures (18, 25, and 30◦ C) and three to seven feeding levels, including satiation level. They also measured changes in proximate composition. Rice et al . (1983) used these data with the following equation from Kitchell et al . (1977) that includes both temperature and body mass as independent variables: C = Cmax Pf (T ) where C is the weight-specific consumption rate; Cmax = a·W b (g·g−1 d−1 ); W is fish weight (g); a, b are regression constants; P is the proportion of maximum rations consumed; and f (T ) is a function that relates consumption to temperature. Zweifel et al . (1999) compared consumption rates for two black bass species at four temperatures (18, 22, 26, and 30◦ C) and found maximum consumption for smallmouth bass peaked at 22◦ C (nearly 8% of wet body weight) and for largemouth bass at 22 to 26◦ C (nearly 5%). McComish (1971) conducted ad libitum feeding experiments with a range of sizes of bluegill held at 20◦ C. Breck and Kitchell (1979) used these data to estimate Cmax for bluegill: Cmax = 0.182W −0.274 These values for Cmax are included in Hanson et al . (1997). Breck (1993) modified this for his application to very small juvenile bluegill, increasing the coefficient 50% from 0.182 to 0.273 g·g−1 d−1 so that simulated fry would show growth. The modification was probably required due to extrapolating to fish sizes smaller than the range of sizes used in the original experiments. Alternatively, adjustments to Cmax for effective daphnid energy density may be needed for fish consuming zooplankton prey because some species of fish can reduce the water content of certain zooplankton prey after ingestion, increasing the effective energy density (Luecke and Brandt 1993; Stockwell et al . 1999). Additional sources of information on consumption rate of bluegill include Gerking (1955, 1971), Anderson (1959), and Schneider (1973). Gerking (1952) reported on laboratory experiments on consumption, growth, and protein metabolism of longear sunfish (L. megalotis) and green sunfish fed mealworms (Tenebrio molitor). Food consumption can also be influenced by oxygen concentration. Warren and Davis (1967) cite Stewart’s (1962) work on largemouth bass and mention results of several other studies that indicate that food consumption and growth of fishes declines when oxygen concentration declines appreciably below saturation levels. The bluegill model of Kitchell et al . (1974) included the effects of low oxygen concentration on mortality rate but not on consumption or growth.

7.3.2 Defining Cmax There are two general ways in which Cmax has been measured, and these reflect two different types of constraints on consumption and different parts of the complex system controlling food intake (e.g., Di Marzo and Matias 2005). These two types of Cmax are the “instantaneous satiation” and “integrated satiation” used by Essington et al . (2000), which they describe as reflecting the constraints of storage and digestion, respectively. The first type of Cmax (binge-feeding Cmax or “instantaneous satiation”; Essington et al . 2000) measures the maximum amount of food that an organism can ingest

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in 1 day and reflects a combination of stomach capacity and 1-day digestion; this is like measuring human consumption at a big Thanksgiving-Day meal or at a pie-eating contest. The second type of Cmax (“integrated satiation”; Essington et al . 2000) measures the long-term average consumption for fish that are offered food ad libitum. The first type of Cmax will always be larger than the second type. Because fitted P -values (daily consumption expressed as a proportion of Cmax ) depend on Cmax , the interpretation of P -values must be different depending on which type of Cmax is used in the computation. Binge-feeding Cmax is typically measured by starving fish for one or more days, then offering food multiple times during the day until the fish ingests no more. Alternatively, food is offered in excess and Cmax is measured as the total offered minus the uneaten remainder at the end of the day. This Cmax can be measured in 1 day (following several days of preparation). The details of the method used are important, because several factors can influence the resulting measured value. It has been known for some time that feeding multiple meals per day results in a larger daily ration, probably because stomach fullness can signal the end of a meal and additional meals can occur as gastric evacuation proceeds. It is important, therefore, to offer food multiple times per day when estimating Cmax . As Hayward et al . (1997) have shown, the maximum amount consumed on the first day following a period of food deprivation depends on the length of time without food. Hybrid sunfish deprived of food for 14 days consumed an initial daily ration 3 to 4 times the size of the ration of control fish fed ad libitum every day; on subsequent days of feeding the food-deprived fish decreased their hyperphagia until their consumption rate was similar to the control group (Hayward et al . 1997). This type of short-term variation in Cmax may reflect the operation of hormones released by the stomach, pancreas and intestine as well as neural signals from the gut (Murphy and Bloom 2006). In mammals, at least, this information from the gastrointestinal (GI) tract is integrated with other information on the body’s lipid level, which changes on a longer time scale, in order to regulate food intake and energy expenditure (Rosen and Spiegelman 2006). Integrated-satiation type Cmax reflects the maximum sustainable consumption rate. This is typically measured by allowing fish to consume an ad libitum ration over a period of several days, and then determining the average daily consumption rate (Niimi and Beamish 1974; Hayward and Arnold 1996). It is important that the measurements be carried out over more than a few days, because a larger ration on 1 day is often followed by a smaller meal on the next day (Smagula and Adelman 1982; Hayward et al . 1997). Further, Hayward et al . (1997) have shown that the average daily ration becomes smaller over time, asymptotically approaching a steady-state value. This may be due to slow adjustments in the fish’s lipid level (energy density and condition) in response to level of feeding (see Rosen and Spiegelman 2006). The choice of Cmax type does not make a great difference when the bioenergetics model is used to fit observed growth. The fitted P -value will differ accordingly, but the goodness of fit will not be affected. The interpretation of the P -value will be affected, however. For example, if the model is fitted to growth during a 1-month period, the P -value could be 0.6 relative to an integrated-satiation type Cmax , but the fitted value could be 0.4 relative to an instantaneous-satiation type Cmax . Based on data from Hayward et al . (1997), differences could be even larger than this. The choice of Cmax is much more important when the bioenergetics approach is used in dynamic simulations involving predators and prey, because Cmax is generally used as the upper limit to daily ration (Essington et al . 2000). In such a case, when simulated prey abundance is high, the simulated ingestion and growth rates for a predator would be much higher based on the instantaneous- versus an integrated-satiation type Cmax . This could produce quite a different growth during simulation periods when prey availability is high; there would be no effect of choice of Cmax as long as prey availability results in less-than-maximum daily rations. Depending on the questions being addressed in the simulation, it might be important to have both types of Cmax considered in the model—the first type for cases where it is important to allow the predator to ingest a big meal (e.g., Diana 1987), and the second type for cases where it is important to have fish consume a reasonable ration over an extended period of time without excessive growth. Essington et al . (2000) studied such situations. They concluded that satiation may be rare for piscivores. In general, the temporal scale of Cmax estimates should be matched with the temporal scale of the application.

7.3.3 Compensatory growth As part of their ongoing crappie model development and evaluation, R. Hayward’s research group at the University of Missouri have incorporated aspects of fish growth that are rare in most other bioenergetics models such as compensatory

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growth and growth in length. For example, suppose two groups of fish are initially offered food in excess, then one group is starved (or fed restricted rations) for some period of time (as short as a few days; Hayward et al . 1997) while the other group continues to be fed ad libitum rations. If both groups are subsequently given food in excess, the group that had been on restricted rations is likely to experience faster, compensatory growth so that they eventually catch up (or nearly so) to the size of the group that had always received full rations. Compensatory or catch-up growth can be defined as “the process of achieving normal body weight and composition following nutritional restriction” (Bull and Metcalfe 1997, p. 498). Growth overcompensation has also been documented where a previously starved fish not only catches but also exceeds the growth of continuously fed fish (Hayward et al . 1997). Compensatory growth commonly (perhaps always) involves a period of hyperphagia (increased food intake) when more food becomes available (Jobling 1994; Hayward et al . 1997; Wang et al . 1998). Increased food conversion efficiency may also be involved; this has been observed on some occasions when it has been studied (e.g., Miglavs and Jobling 1989a,b; Russell and Wootton 1992; Wang et al . 1998). Hayward et al . (1997) speculated that reduction in metabolic rate during low-ration periods (e.g., Glass 1968) may also contribute to increased growth efficiency. Ali and Wootton (2000) reported that compensatory responses allowed female three-spined sticklebacks (Gasterosteus aculeatus) experiencing variable food availability to have growth and reproductive performance equivalent to females with constant food availability. Compensatory growth has been investigated in aquaculture settings as a means to enhance production for many species (Byamungu et al . 2001; Chatakondi and Yant 2001; Xie et al . 2001) including hybrid sunfish (Hayward et al . 2000). In order to successfully simulate compensatory growth, a bioenergetics model would need to include a mechanism to allow temporal variation in Cmax . Such variation might be in response, for example, to changes in body condition or nutritional status. The model might also need to incorporate condition-dependent changes in growth efficiency, such as changes in fraction of consumed energy lost as waste, changes in respiration rate, or dynamic changes in energy density. Whitledge et al . (2006b) took a more simplistic approach by applying an empirically based correction factor to consumption and relative growth parameters in a bioenergetics model that simulated compensatory growth in a hybrid sunfish. Broekhuizen et al . (1994) developed a model for compensatory growth in fishes based on two key assumptions. First, that an individual partition net assimilates between two tissue types: those that can and those that cannot be remobilized once laid down. Second, that the individual modulates its behavior and physiology in response to the instantaneous ratio of mobilizable to nonmobilizable tissues (Broekhuizen et al . 1994, p. 770). When the ratio is low, then relatively more energy is allocated to mobilizable reserves, and body condition improves. When the ratio is high, then relatively more energy is allocated to nonmobilizable structure, and the fish growth in length and condition may decline. When the ratio is at the nominal level, energy is allocated so that the fish grows just enough in length that the ratio remains the same and condition remains constant. They also proposed that an individual fish can be in one of three nutritional states, depending on the relative level of reserves: healthy, hungry, and torpid. As reserves decline, a fish changes state from healthy to hungry, and maximum ingestion rate increases by a fixed proportion (e.g., hungry ingestion rate = 2.0 × healthy ingestion rate). As reserves decline still further, a fish changes state from hungry to torpid, maximum ingestion rate falls below the level for a healthy fish (e.g., torpid ingestion rate = 0.8 × healthy ingestion rate), and respiration rate changes by a fixed proportion (e.g., torpid respiration rate = 0.3 × healthy respiration rate). The model did a good job of fitting the results of several compensatory growth experiments with salmonids. Breck (1998) used the general approach of Broekhuizen et al . (1994) to model energy allocation for growth in length and weight of bluegill and largemouth bass. Because this approach was used for growth throughout the fish life cycle, it was necessary to allow the nominal ratio of reserve to structural energy to increase with body size so that adults would tend to have relatively larger reserves than small juveniles. Additional work is needed to successfully model the changes in body condition that occur as ration level changes. Hyperphagia in hybrid sunfish following periods of starvation was clearly demonstrated by Hayward et al . (1997). Their results show a fast-responding component and a slow-responding component influencing daily ration, and by implication, appetite and Cmax . By the fast component we mean a strong tendency for a higher level of consumption to be followed the next day by a lower level (especially the high first feeding after starvation and the low level the following day), and vice versa. This daily variation in level of consumption is also suggested in the hybrid sunfish data of Wang et al . (1998) and the largemouth bass data of Smagula and Adelman (1982) and Whitledge and Hayward (1997). By the slow component, we mean a gradual decrease in the magnitude of hyperphagia. The results for hybrid sunfish show that when food is available in excess the magnitude of hyperphagia (relative to controls fed ad libitum) decreases gradually (perhaps 50% in

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about 10 days) (Hayward et al . 1997); this is very different than the on–off type of hyperphagia assumed by Broekhuizen et al . (1994). There are several interesting questions raised by the phenomenon of compensatory growth. First, what is the proximate mechanism responsible for this phenomenon in centrarchids? Is it the level of body lipid that regulates hyperphagia (and Cmax ), as suggested by the experiments of Bull and Metcalfe (1997) with overwintering juvenile Atlantic salmon? A recent review notes that lipid cells (adipocytes) play a major role in regulating energy balance and the total amount of body fat, at least in mammals (Rosen and Spiegelman 2006). Second, why is Cmax not larger than that observed for individuals that remain on ad libitum rations? If individuals that have endured a period of restricted rations can consume a “larger-thannormal” daily ration when food is again made available, at least for a while, why do not the individuals stay at that higher level of consumption? They could then continue to grow faster or store even more energy. Stated another way, what are the trade-offs that determine the optimum level of consumption, and consequently, the optimum level of growth? Finally, there are implications for the determination of Cmax as used in bioenergetics models. From the above discussion, it seems clear that Cmax not only varies with fish size, but also depends on the nutritional status of the fish. This suggests that the protocol for measuring Cmax will influence the value obtained. Cmax is expected to be larger when fish are starved for a longer time before feeding, and Cmax is expected to be lower when more days of feeding are included in the average, because hyperphagia is expected to diminish. Additionally, the influence of longer term preexperimental feeding (i.e. prior weeks and months) on Cmax determination is largely untested, but likely important.

7.3.4 Prey energy density Prey energy density has a large effect on predator growth. A predator that ingests a 10-g prey will grow much faster if the prey contains 4000 J g−1 than if the prey contains 500 J g−1 . The significance of prey energy density to estimates of fish growth has probably been underappreciated, perhaps because prey energy density was not explicitly included in the early sensitivity analyses that identified critical parameters in bioenergetics models (Kitchell et al . 1977; Rice and Cochran 1984; Bartell et al . 1986). Rand et al . (1994) noted that substantial variations occur in the mean sizes and energy densities of pelagic forage fish in Lake Ontario. For example, the energy density of alewives (Alosa pseudoharengus) varies more than twofold during the year, from peak values in the fall to low values in spring or summer. They used a bioenergetics model to show that the seasonal changes in alewife energy density, differences in energy density between rainbow smelt and alewives, and changes in mean sizes of these prey fish would be expected to produce noticeable changes in Chinook salmon (Oncorhynchus tshawytscha) growth in Lake Ontario. Cummins and Wuycheck (1971) produced a large compendium (158 pages) of energy values for a wide range of animals and plants, both aquatic and terrestrial. They reported energy density per gram dry weight and per gram wet weight when the information was available. But only a modest amount of information was available at that time on energy density of aquatic arthropods and fish. Hanson et al . (1997) compiled information on energy density of common taxa of invertebrate prey commonly used in bioenergetics models. As noted in Section 7.3.1, rainbow trout (Oncorhynchus mykiss) and kokanee salmon (Oncorhynchus nerka) can reduce the water content of ingested daphnid zooplankton, increasing the effective energy density of these prey items (Luecke and Brandt 1993; Stockwell et al . 1999). It would be interesting to know if centrarchids can also do this, because zooplankton can be important diet items for small centrarchids generally and adult bluegill in particular (Mittelbach and Osenberg 1993).

7.3.5 Digestion/gastric evacuation rate Rate of food digestion is one factor that may limit daily ration of fish. As temperature increases, the rate of digestion increases, such that more food can be processed in a day. Gastric evacuation rate has been used to estimate field consumption rate from data on stomach contents (Elliott and Persson 1978; Adams and Breck 1990). The approach may be complicated

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if there are multiple meals (Persson 1984). Bromley (1994) and Cort´es (1997) have both critically reviewed the use of gastric evacuation rate for estimating the consumption rate of fish. DeAngelis et al . (1984), Tudor (2001), and Finstad (2005) used a simulation modeling approach to estimate the effects of sampling interval, water temperature, and other factors on the accuracy of such estimates. Whitledge and Hayward (2000) tested the influence of sampling interval on precision of in situ estimates of cumulative food consumption by stream-dwelling green sunfish and reservoir bluegill and found that a sample interval of less than 5 days was necessary to prevent significant error in the estimate. Hunt (1960) reported digestion rates of Florida bass (which he called largemouth bass) and warmouth. He force-fed the experimental fish and did not control temperature, so the digestion rates are difficult to compare with later results. Cochran and Adelman (1982), Hayward and Bushmann (1994), and Wetzel and Kohler (2005) all published information on gastric evacuation rate of largemouth bass as did Rogers and Burley (1991) for smallmouth bass. Windell (1966) carefully investigated the rate of gastric evacuation for bluegill. At 21◦ C, natural food organisms were about 50% digested after 6 hours and completely evacuated from the stomach in 17 to 19 hours. He observed modest differences in gastric evacuation rate for different prey types; prey types with larger amounts of chitin were not digested more slowly. Windell noted a very large effect of starvation, which caused a slowing of gastric evacuation rate. For three control groups (15 fish each), the fraction remaining in the stomach after 22 hours was 4.4, 10.5, and 0%. For groups starved for 7, 14, and 25 days, the fraction remaining after 22 hours was 24.3, 46.1, and 51.1%, respectively. To help explain this effect of starvation time, he noted striking changes in the condition of the pyloric caeca; these were “definitely shrunken after 7 days, and the condition became progressively advanced with time” (Windell 1966, p. 201). Kitchell and Windell (1968) measured the rate of gastric evacuation by pumpkinseed. After 6 hours at about 21◦ C, approximately 37% of the digestible organic matter remained in the stomach, and essentially all had left the stomach by 14 hours after feeding. Richardson and Nickol (1998) determined that gastric evacuation in green sunfish at 21◦ C occurred from 24 to 32 hours postfeeding, with approximately 25% evacuation by 4 hours and 50% by 12 hours. Time required for a meal to pass completely through the alimentary canal ranged from 41 to more than 61 hours. Feeding level influences assimilation efficiency and the fraction of ingested food that is egested. The general pattern in fishes is that food conversion efficiency decreases at high ration levels (Paloheimo and Dickie 1966; Warren and Davis 1967; Brett et al . 1969; Kerr 1971; Brett and Groves 1979). The work of Elliott (1976) on brown trout (Salmo trutta) carefully documented that the proportion of food assimilated declined as ration increased, when ration was expressed as a fraction of maximum ration. To our knowledge no comparable study involving combinations of fish size, water temperature, and feeding level has been done on centrarchids. In mammals, hormones in the ghrelin–motilin receptor family modulate both appetite and GI motility (Nogueiras and Tsch¨op 2005; Murphy and Bloom 2006). The hormone ghrelin increases food intake and body weight, whereas the newly identified hormone obestatin does the opposite, and also “decelerates gastric emptying and decreases intestinal contractility in mice, both of which counteract the well-defined effects of ghrelin” (Nogueiras and Tsch¨op 2005, p. 985). If this type of regulatory system also occurs in fish, then GI motility might correlate with food intake, and assimilation efficiency would be expected to decrease with increasing GI motility. That is, at higher levels of GI motility, food is present in the GI tract for a shorter time, and a smaller proportion of the food (the most readily digested and absorbed proportion) is assimilated. The advantage to the organism is that this increases the overall rate at which energy and materials are assimilated. So as consumption rate increases, a greater proportion of ingested food would be lost as feces. This would be consistent with the decrease in gross growth efficiency with increasing ration level described in the reviews by Paloheimo and Dickie (1966) and Kerr (1971), and the extensive lab studies by Brett et al . (1969) and Elliott (1976). It would also help explain the systematic error in bioenergetics models observed by Bajer et al . (2004a, 2004b). At low rations fish might assimilate more food than predicted by the models so that the models would underpredict growth at low consumption rates. At high rations fish might assimilate a lower fraction of the food than predicted by the models so that the models would overpredict growth at high consumption rates.

7.4 Metabolic rate The metabolic rate of fish is a measure of the rate of energy expenditure and is commonly estimated by measuring respiration rate often expressed in units of oxygen consumed per unit weight of fish per unit time (e.g., mg O2 g−1 h−1 ).

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Of the various types of energy expenditure, the highest priority for an organism is that of basal metabolism, that is, the minimum amount of energy necessary to keep an animal alive. Because measurement of basal metabolism requires that a fish be totally immobile, more commonly reported measures are standard or routine metabolism. Standard metabolism normally refers to measures of metabolism extrapolated to zero activity from measures at a series of activity levels. Routine metabolism refers to the metabolic rate during normal, spontaneous activity. Active metabolism on the other hand is measured while fish are subjected to periods of continuous swimming. Fry (1957) and Brett and Groves (1979) provide excellent summaries of these various measures of metabolism and the factors that influence them. Metabolic rate measured as the rate of oxygen consumption has been determined for several centrarchid species (Table 7.2). The studies we found often subjected test fish to a variety of environmental conditions to determine their effect on metabolic rate. The effects of temperature, size, activity, DO concentration, turbidity, contaminants, and social interaction are discussed later.

Table 7.2 Summary of factors evaluated in studies on metabolic rate of centrarchid fishes. Factors evaluated Species

Temperature

Size

Activity

Food

Other

Source

Bluegill

X

X

X

–

–

Wohlschlag and Juliano (1959)

X

X

–

–

Hypoxia

Moss and Scott (1961)

X –

X

–

–

–

O’Hara (1968)

–

–

–

Schooling

Parker (1973)

–

–

–

X

–

Pierce and Wissing (1974)

–

–

–

X

–

Schalles and Wissing (1976)

Green sunfish

–

–

–

–

Turbidity

Horkel and Pearson (1976)

Largemouth bass

X X

X –

– X

– –

Hypoxia, pH –

Wiebe and Fuller (1933) Johnson and Charlton (1960)

X

X

–

–

Hypoxia

Moss and Scott (1961)

X

X

X

–

–

Beamish (1970)

X

X

X

X

–

Glass (1971)

–

–

–

–

Schooling

Parker (1973)

–

–

–

X

–

Beamish (1974)

X

–

–

–

Hypoxia

Cech et al. (1979)

X

–

–

–

–

Diana (1983)

Pumpkinseed sunfish

– X

– X

X –

– –

– –

Brett and Sutherland (1965) O’Hara (1968)

X

X

–

–

Season

Evans (1984)

Redbreast sunfish

X

X

–

–

Contaminants

Shepard (1988)

Sacramento perch

X

X

–

–

–

Woodley (PhD research; personal communication with Christa Woodley, UC Davis)

Smallmouth bass

X

X

–

–

–

Whitledge et al. (2002)

White crappie

X

X

–

–

–

Zweifel (2000)

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7.4.1 Temperature and size Temperature and size are two of the most often evaluated factors affecting metabolic rate and are often evaluated together. The relationship between metabolic rate (M, mg O2 per unit time) and fish weight (W ) is often described by the following exponential relationship: M = aW b where log(a) is the intercept for the relationship between log(M) and log(W ), and b the slope. The b exponent is a useful descriptive value and a particularly sensitive parameter in bioenergetics models (Rice 1983; Bartell et al . 1986). The relationship between metabolic rate and temperature is often described as exponential in nature and can be modeled in combination with weight as: M = aW b ecT where T is temperature and c is a regression constant. Wiebe and Fuller (1933) was possibly the first published study on centrarchid metabolism. They tested largemouth bass ranging in size from about 13.5 to 67.3 g at temperatures of 15, 20, 25, and 26◦ C. Their results suggest a nearly threefold increase in largemouth bass metabolic rate from 15 to 26◦ C, and they found the typical metabolic relationship of decreasing weight-specific metabolic rate with increasing size. We performed a regression analysis on the data of Wiebe and Fuller, which produced a weight-dependent exponent b value of 0.742. Although the study by Wiebe and Fuller (1933) is the earliest published we found on centrarchid metabolism, the authors also mention a study at about the same time by “Mr. Burdick,” a student in the Department of Zoology at the University of Iowa, where these experiments were performed, but do not provide a complete citation. Additional sleuthing on our part found the following partial reference—“The oxygen consumption of the white crappie (P. annularis, Raf.) and the black bullhead (Ameiurus melas, Raf.)” by H. C. Burdick, State University of Iowa. This is perhaps a student thesis on another centrarchid species completed during the same period. Wohlschlag and Juliano (1959) studied seasonal changes in respiration rates of bluegill relative to seasonal limnological changes. They tested fish four times over the course of a year immediately after capture in the field and found various seasonal differences that they ascribed to seasonal variation in acclimation temperature, general condition, reproductive condition, and activity. They summarized their findings in equations for each season that regress metabolic rate as a function of temperature (range 8.2–26.5◦ C), weight (range of mean weights 52–324 g), and swimming velocity (range 0–14 m min−1 ). The weight-dependent exponent b for the spring, fall, and winter regressions ranged from 0.80 to 0.86, and for summer 1.06. The authors suggest that the uncharacteristically high summer value occurred because the larger fish in the sample were in spawning condition, whereas the smaller fish had already spawned. Moss and Scott (1961) determined standard metabolic rates for juvenile bluegill and largemouth bass at three temperatures. They found little difference in standard rates among tests at 25, 30, and 35◦ C for either species. Bluegill and largemouth bass weighing more than 15 g (up to 48 g for bluegill and 78 g for largemouth bass) showed no difference in metabolic rate with increasing size, but below this weight, metabolic rate increased with decreasing weight. O’Hara (1968) measured routine respiration rates for bluegill and pumpkinseed sunfish ranging in weight from 1.4 to 116 g at 25 and 30◦ C. He found that bluegill are slightly better adapted for high temperatures (i.e. bluegill had a lower metabolic rate at 30◦ C). The weight exponent, b, differed slightly between the two temperatures, but was similar for the two species: b = 0.75 and 0.79 for bluegill and pumpkinseed at 30◦ C, and b = 0.72 and 0.71, respectively, at 25◦ C. Evans (1984) produced the most complete analysis of the effects of temperature on metabolic rate of a centrarchid fish. Routine metabolic rates of pumpkinseed sunfish were measured at temperatures from 8 to 32◦ C during all four seasons. He also found a significant seasonal effect such that routine metabolic rates were lowest in winter and highest in spring independent of acclimation temperature. For example, a 100-g fish acclimated to 20◦ C in spring had a higher metabolic rate than a similarly conditioned fish in winter. The increase in metabolic rate in spring begins independent of the vernal rise in temperature and is perhaps related to increased metabolic demands of spawning or in anticipation of increasing food availability. The lowering of rates in the winter is suggestive of a metabolic strategy similar to hibernation. At 20◦ C, the weight exponent, b (based on weight range of 1–194 g) was similar for all four seasons ranging from 0.72 to 0.75.

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Respiration rate (mg O2 g−1 d−1)

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Bluegill; c = 0.0391 (Wohlschlag & Juliano 1959) Bluegill; c = 0.0519 (O'Hara 1968) Pumpkinseed; c = 0.0589 (Evans 1984) Redbreast; c = 0.0568 (Shepard 1988) Figure 7.2 Relationship between temperature and respiration rate for three Lepomis species standardized for a 100-g fish. Symbols indicate the lowest and highest temperatures used in the experiments.

A comparison of the measured routine rates and the estimated standard rates presented in Evans (1984) suggests that, on average, routine rates are about 1.43 times greater than standard rates. Shepard (1988) found significant effects of both temperature and weight on the metabolic rate of redbreast sunfish L. auritus (34–183 g). Standard metabolic rates were measured in a continuous flow respirometer at 12, 18, 22, and 28◦ C. The regression model used to describe the relationship produced a weight exponent, b, of 0.66. Relationships that describe the dependence of metabolic rate on temperature and weight for Lepomis species are compared in Figures 7.2 and 7.3 for Shepard (1988), Evans (1984), O’Hara (1968), and Wohlschlag and Juliano (1959). This comparison suggests some differences among species with respect to the dependence of metabolic rate on temperature and size, but simultaneous experiments with multiple species tested under the same conditions are needed to determine whether these differences are real. In addition to studies by Wiebe and Fuller (1933) and Moss and Scott (1961), there are a handful of other published studies on the effects of temperature and size on metabolism of Micropterus species. Johnson and Charlton (1960) measured both standard and active rates of fingerling largemouth bass at five temperatures from 5 to 29◦ C. Beamish (1970) determined oxygen consumption rates for largemouth bass (40–400 g) over a range of temperatures (10–34◦ C) and swimming speeds (20–60 cm s−1 ). The average size-dependent coefficient, b, in experiments by Beamish was about 0.64. Glass (1971) presents routine metabolic rate data for largemouth bass over a wide range of both temperature (12–25◦ C) and size (10–320 g). Regression equations fit to data for each of three temperatures produced an average b value of 0.77. Cech et al . (1979) measured routine metabolic rates of subadult largemouth bass (230–470 g) at 20, 25, and 30◦ C. All fish were tested at all three temperatures on the same day after being held at acclimation temperatures of 18 to 20◦ C. These results provided the basis for further tests by the authors on the effects of hypoxia, which are discussed later in this chapter. Diana (1983) compared the routine metabolic rates of largemouth bass (95–260 g) exposed to constant cool (15◦ C), constant warm (30◦ C), and a fluctuating thermal regime with a diel cycle of 20 hours at 15◦ C and 4 hours at 30◦ C. The fluctuating regime was chosen to simulate the conditions experienced by a fish in summer that would reside in cool water

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Weight (g) Bluegill; b = .96 (Wohlschlag & Juliano 1959) Bluegill; b = 0.72 (O'Hara 1968) Pumpkinseed; b = 0.73 (Evans 1984) Redbreast; b = 0.34 (Shepard 1988)

Figure 7.3 Relationship between size and respiration rate for three Lepomis species standardized for 25◦ C. Symbols indicate the smallest and largest sizes of fish used in the experiments.

just above the thermocline for most of the day and move into warm shallow areas for brief periods to feed. Under constant thermal regimes, the metabolic rate at 30◦ C was about twice that at 15◦ C. Under the cyclic regime, the metabolic rates during the period at 15 and 30◦ C were nearly the same as under the respective temperatures under the constant regimes, indicating that within this temperature range, largemouth bass probably encounter little or no metabolic stress when exposed to this kind of temperature fluctuation. Largemouth bass and most other centrarchids are considered temperature eurytherms (Magnuson et al . 1979) and are regularly exposed to seasonal fluctuations of 1 to >30◦ C. Based on Diana’s results with largemouth bass, one might expect that other centrarchids would have similar tolerance for moderate diel fluctuations. Whitledge et al . (2002) measured routine metabolism for two size classes of smallmouth bass (50–100 g and 150–280 g) at 18, 22, 26, and 30◦ C. They found the general trends that others have found with respect to weight and temperature. Specifically, they revealed little difference between rates at 22 and 26◦ C for both size classes, an outcome observed in other studies that is somewhat contrary to the strict exponential relationship normally expected (Kitchell et al . 1977). Regression models developed for each temperature produced weight-dependent exponents (b values) from 0.53 to 0.86. Zweifel (2000) measured routine metabolic rate for white crappie ranging from 50 to 300 g at 18, 21, 24, 27, and 30◦ C. Bajer et al . (2004a) performed regression analysis on the Zweifel data to develop a metabolic rate model as a function of temperature and weight (b = 0.377; this value is much lower than the range of other studies of about 0.6–0.9). In more recent work, Bajer (2005) determined that the weight coefficient for white crappie to be a more reasonable 0.70. Woodley and Cech (personal communication with Christa Woodley, University of California at Davis) have been investigating metabolic rates and other physiological responses of Sacramento perch to high temperature and other environmental stressors (e.g., DO, pH, and salinity). Based on the habitat in which they historically resided, it is believed that Sacramento perch have a high tolerance for extreme temperatures. From laboratory and field observations they were able to determine optimal temperatures for various life stages (larvae, juvenile, and adults) and found significant ontogenetic differences. The exponential function has often been used to describe the relationship between fish metabolic rate and temperature (Figure 7.2), but other relationships have also been used. In recently published work, Gillooly et al . (2002) discuss how metabolic rate is expected to vary with temperature as well as body size. They use the Boltzmann factor, also known as

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the Van’t Hoff-Arrhenius relation, to express how rates of chemical reactions that combine to determine metabolic rate are expected to vary with changes in absolute temperature: M ∝ e−E/kT where M is metabolic rate, the symbol ∝ means “is proportional to,” E is the activation energy of the chemical reaction [about 0.63 eV (electron volts)], k is Boltzmann’s constant (8.6173 × 10−5 eV K−1 ), and T is absolute temperature (K). Gillooly et al . (2002) recommend the use of the Boltzmann factor to account for the effects of temperature on metabolic rate. They propose a form in which the temperature adjustment is expressed relative to that at some reference temperature. Over a typical range of biological temperatures (0–35◦ C), the effects of temperature as expressed in the Boltzmann factor are similar to those predicted by an exponential function of temperature (Figure 7.4). Brown et al . (2004) presented an outline of a metabolic theory of ecology. They showed how the effects of body size and temperature on metabolic rate could provide an explanation for a wide range of phenomena in ecology, from the individual level to the population and ecosystem levels. Brown et al . (2004) do not mention the substantial amount of work in fish bioenergetics that had come to the same conclusion about the importance of body size and temperature as major factors affecting metabolic rate (Kitchell et al . 1977 and subsequent work). West et al . (1997, 1999) provided an explanation for quarter-power allometric scaling of metabolic rate in animals, why metabolic rate per individual should be proportional to mass raised to the three-fourth power. They considered the transport of nutrients and other essential materials through fractal-like branching networks of tubes that service the entire body of an animal. Essential materials need to be exchanged with all cells in the body to keep them alive. They assume that natural selection has minimized the energy required to transport essential materials throughout the body, minimizing transport distances and times. They also assume that the size of the terminal tubes in the transport network is the same in all organisms (e.g., blood capillaries are the same size in mice and whales). They assume that natural selection has acted to maximize metabolic capacity. They reason that this leads to maximizing the total effective biological surface area through which essential materials are exchanged with all cells. The branching distribution network that creates this exchange area is volume-filling, leading to the consequence that “the area of the effective exchange surface scales as if it were a volume” (West et al . 1999, p. 1679). The fractal-like distribution network thus adds another dimension to living things, so that effective surface area scales as if it operated in three dimensions, and the corresponding biological volume scales as if it operated in four spatial dimensions. This is the reason that metabolic rate scales as mass raised to the three-fourth power, and why we should expect b = 0.75. For metabolic rate the exponent of mass is expected to be very close to b = 0.75 (West et al . 1997, 1999; Brown et al . 2004). Deviations far from this value should be regarded with suspicion. Large deviations may be due to statistical estimation problems caused by an insufficient range in body sizes. For example, in Figure 7.3, a large deviation from b = 0.75 is observed in the data from Shepard (1988), who used fish that differed in size by less than one order of magnitude. The deviation from b = 0.75 observed in the data from Wohlschlag and Juliano (1959) in Figure 7.3 is probably due to methodological issues. They measured wild-caught bluegill soon after capture, and if the stress and recovery from capture is size related, it could produce a stronger effect on the metabolic rate of larger fish and a deviation from b = 0.75. The theoretical basis provided by West et al . (1997, 1999) provides a strong justification, in our opinion, for using b = 0.75 as a standard value in fish bioenergetics models. This should also be the reference value against which to judge experimentally measured estimates.

7.4.2 Activity The effect of activity on metabolic rate has been investigated for a number of centrarchid species and is a significant factor in the development of an energy budget. The results of these studies can be used to derive activity multipliers or swimming dependent functions for respiration rate equations in bioenergetics models. Inclusion of an activity parameter in the standard metabolic rate equation is often accomplished in one of two ways. One way is by capturing the effect of activity as a simple multiplier of the routine (or standard) metabolic rate: M = aW b ecT ACT

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0 ln(I, Watts) Linear ln(I, Watts)

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Figure 7.4 The effect of temperature on metabolic rate (M, in watts) as predicted by (i) the Boltzmann factor (also known as the Van’t Hoff–Arrhenius relation) and (ii) a simple exponential relation, M = a · exp(0.0867 · T), where a = exp(−4.7797) watts. The parameters of the exponential relation were estimated by linear regression of loge (M) on T.

where ACT is an activity multiplier usually between 1 and 2 (Hanson et al . 1997). Alternatively, active metabolism can be modeled as a function of swimming velocity: M = aW b ecT edV where V is swimming velocity (usually in either centimeter per second or body lengths per second) and d is a regression constant. Hanson et al . (1997) present an alternative formulation for incorporating swimming speed which is more complex, but not necessarily any more accurate. In their early studies on metabolic rates of bluegill, Wohlschlag and Juliano (1959) included level of activity as a factor in addition to temperature and fish size. The level of activity during the experiments varied from 0 to 24 cm s−1 . They derived mathematical models of metabolic rate by regressing log oxygen consumption on log body weight, swimming speed, and temperature. Data from Johnson and Charlton (1960) indicate that increased activity elevated respiration rate by a factor of about 1.5 for fingerling largemouth bass. They tested fish at predetermined temperature-specific maximum cruising speeds between 10 cm s−1 (5◦ C) and 40 cm s−1 (22◦ C). For tests at 5, 12, 17, 22, and 29◦ C, active metabolism exceeded standard metabolism by an average factor (i.e. ACT) of 1.54. Brett and Sutherland (1965) measured active metabolism of pumpkinseed sunfish in a tunnel respirometer to evaluate the relation between oxygen consumption and swimming speed. Tests were performed at several velocities between 3 and 37 cm s−1 . They found that for a 45-g fish at 20◦ C the active metabolic rate at the 60-min fatigue swimming speed of 37 cm s−1 was about nine times greater than the standard rate. Glass (1971) tested the effects of activity on four size classes of largemouth bass at a range of velocities ranging from a mean minimum of 7.4 cm s−1 to a mean maximum of 46.8 cm s−1 . The highest metabolic rate occurred at the higher velocities and exceeded that of fish at slower velocities by a factor of 4.2 for the smallest size class (30–40 g) and by a factor of 1.9 for the largest size class (88–95 g). Recent work by Bajer (2005) produced an updated metabolic rate equation for white crappie that includes weight, temperature, and activity as dependent variables in the form described earlier: M = 5.37 · W −0.296 e0.0606T e0.785V Cooke et al . (2001) tracked smallmouth bass with electromyogram transmitters that measured muscle activity to evaluate daily activity costs relative to the same estimates from mark-recapture and conventional telemetry studies. Their results indicate that smallmouth bass may travel nearly 100 times more than previously expected. They further concluded that based on bioenergetics modeling, this higher level of activity would require a 37% increase in daily food consumption to meet energetic requirements.

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Similar to increases in “voluntary” activity are energetic expenditures related to escape from predation. Cooke et al . (2003) investigated heightened stress in largemouth bass associated with fright-or-flight responses following simulated predation by avian predator models. They found elevated cardiac response, heart rate, and stroke volume of largemouth bass when presented with avian models and that this response was size-dependent. These nonlethal costs might need to be considered in bioenergetics models when predation avoidance is a significant factor. A recent review of studies using electromyogram telemetry lists 10 studies that included either smallmouth or largemouth bass (Cooke et al . 2004).

7.4.3 Hypoxia Metabolic rate is often affected by exposure to environmental stressors, such as low dissolved oxygen, turbidity, pH, and exposure to toxicants. One of the most common stressors experienced by warmwater fish and therefore one that is frequently studied is low dissolved oxygen or hypoxia. Cech et al . (1979) found a significant reduction in routine metabolic rate of adult largemouth bass as dissolved oxygen partial pressures declined. Critical oxygen tensions were achieved at progressively higher levels as temperatures increased from 20 to 30◦ C. To minimize largemouth bass mortalities in the wild, these results suggest that dissolved oxygen concentrations need to be maintained above 2.60 mg l−1 at 25◦ C and above 2.85 mg l−1 at 30◦ C. Moss and Scott (1961) exposed juvenile bluegill and largemouth bass to progressively lower dissolved oxygen concentrations while monitoring oxygen uptake rate to determine the critical dissolved oxygen level (i.e. concentration at which respiration rate decreased relative to a control) at 25, 30, and 35◦ C. They found critical levels increased from about 0.7 mg l−1 at 25◦ C to 1.0 mg l−1 at 35◦ C for bluegill and from about 0.8 mg l−1 at 25◦ C to 1.2 mg l−1 at 35◦ C for largemouth bass.

7.4.4 Turbidity Horkel and Pearson (1976) measured the effects of turbidity on ventilation rate and oxygen consumption of green sunfish at four temperatures (5, 15, 25, and 35◦ C) and several levels of turbidity. Ventilation rates eventually increased at all temperatures in response to elevated turbidity, with a response occurring at lower turbidities as temperature increased. However, oxygen consumption rates did not change over the range of turbidities tested at any of the four temperatures.

7.4.5 Environmental stressors Fish exposed to sublethal levels of environmental contaminants and other stressors often exhibit physiological and or biochemical responses. Shepard (1988) investigated the potential for using metabolic rate as an indicator of contaminant exposure in redbreast sunfish. Although fish exposed to sublethal levels of suspended contaminated sediment showed no difference in metabolic rate, those exposed to stream water with industrial effluent did have reduced metabolic rates. The author suggests this effect may have been a result of gill damage due to chlorine exposure and not a direct metabolic effect.

7.4.6 Schooling Just as there are conditions that result in suboptimal metabolic rates, there are also conditions that support a healthy metabolism. From the studies referred to earlier in this chapter one might generalize that optimal conditions for low metabolic rates include low temperatures, high dissolved oxygen, low turbidity, and minimal activity. There are other less obvious factors that affect metabolism. Parker (1973) investigated the relationship between metabolic rate and induced schooling for bluegill and largemouth bass (along with 13 other non-centrarchid species). He found that respiration

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rates for bluegill, but not for largemouth bass, were significantly lower when fish were grouped with conspecifics than when tested individually. These results correspond with what we know about the social behavior of these two species (i.e. bluegill commonly school and largemouth bass are more solitary). To the contrary, Wohlschlag and Juliano (1959) found grouped bluegill had a higher average metabolic rate than individuals in spring but no differences in summer. They suggest that this might be explained by relaxation of competitive spawning interactions.

7.5 Energetic wastes (egestion, excretion, and SDA) Egestion, excretion, and specific dynamic action (SDA) are energetic costs associated with digestion and processing of consumed food. Egestion represents the loss of energy in that portion of consumed food that is not digestible, passes through the gut without absorption, and is defecated. Excretion represents energy loss in the form of ammonia/ammonium and urea when proteins are broken down for energy production or storage. SDA is the common name given to the increase in metabolic rate that is associated with digestion and processing of a recently consumed meal. Gerking (1971 and earlier works) and Savitz (1971) performed many of the early experiments on nitrogen excretion in centrarchid fishes. They investigated the relationships between nitrogen excretion and fish size and ration for bluegill. Beamish (1972) estimated both excretion and egestion rates for largemouth bass as a percentage of total energy consumed. Although it has been demonstrated that egestion and excretion are both functions of temperature and ration level (Elliott 1976), the sum of the two remains fairly constant (Kitchell et al . 1977). Therefore, in lieu of detailed data, both are usually estimated as a set proportion of consumed energy in most bioenergetics models. Rice et al . (1983) and Adams et al . (1982) derived their estimates of egestion (10.4% of consumed food) and excretion (7.9% of consumed food) from empirical studies by Beamish (1972). For a bluegill bioenergetics model, Breck (1993) adopted nonspecific values from Brett and Groves (1979) of 0.168 and 0.0841 as the proportion of ingested energy accounted for by egestion and excretion, respectively. Hanson et al . (1997) used values of 10.4% for egestion and 6.8% for excretion for adult largemouth and smallmouth bass. Although rare in bioenergetics models, Breck and Kitchell (1979) and Hanson et al . (1997) calculated both egestion and excretion as functions of temperature and ration for bluegill. In bioenergetics models, SDA is typically represented as a constant proportion of the energy consumed, although Beamish and Trippel (1990) argue that many studies show that this is not the case and doing so may result in inaccurate model outputs. Similar studies by Beamish (1974) and Tandler and Beamish (1981) reported slightly different mean apparent SDAs for largemouth bass, 14.2 and 11.3% of energy ingested, respectively. Both studies found the typical temporal pattern of a relatively rapid rise in oxygen consumption after feeding, reaching a maximum around 2 hours postfeeding and then a gradual decline back to baseline that may take 1 to 3 days. The period of elevated metabolic rate depended on fish size and meal size, but the energy demand relative to energy ingested was mostly unaffected by meal size or fish size. Pierce and Wissing (1974) found a mean energy cost of food utilization for bluegill of 12.7% when they were fed mayfly nymphs (Hexagenia limbata). Schalles and Wissing (1976) in a similar study found an SDA value for bluegill when fed a dry pellet diet to be about 14.9% of consumed energy. The original bluegill bioenergetics model of Kitchell et al . (1974) adopted the 13% value from Pierce and Wissing. In the original largemouth bass models, Rice (1981) and Adams et al . (1982) both used the value of 14.2% derived by Beamish (1974). The SDA values used in the latest version of the Fish Bioenergetics (3.0) software (0.172 for bluegill, 0.163 for largemouth bass, and 0.16 for smallmouth bass; Hanson et al . 1997) are not consistent with the earlier studies and their origin is unclear.

7.6 Growth energetics 7.6.1 Energy density and body composition Fish energy density can have a large effect on growth rate. Suppose two fish each have 2 kcal of energy (consumption minus losses) available for growth. If one fish has an energy density of 1 kcal g−1 then it can add 2 g of weight. If the

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other fish has an energy density of 2 kcal g−1 then it can add only 1 g of weight and keep the same energy density. Fish energy density was not explicitly included as a parameter in the sensitivity analyses of Kitchell et al . (1977) or Bartell et al . (1986), but it can have a large influence on predicted growth (Hartman and Brandt 1995). Bioenergetics models often do their accounting in terms of energy, keeping track of energy input, energy losses, and change in total body energy content, considering energy density of the food and the fish. When considering changes in energy density or the corresponding changes in proximate body composition, the issue arises of conversion from one chemical type to another. In particular, protein could be converted to lipid following deamination and further conversion, but lipid cannot be converted into protein without addition of nitrogen. This sets some limitations on the conversion of one chemical class into the other. But it is generally the case that fish growth is limited by available energy, not a shortage of nitrogen or phosphorus (Schindler and Eby 1997). Fish energy density depends on body composition, which is related to percent dry weight and proximate composition. Brett and Groves (1979) summarize much literature about fish energetics, including the energy values of body components such as lipid, protein, and carbohydrate. For mammals, the familiar value for heat of combustion of lipid is 9.45 kcal g−1 (or 39.55 kJ g−1 , where 1 kcal = 4.1855 kJ). Brett and Groves note that for fish, which have lipids that are more unsaturated than mammals, the corresponding value for lipid is lower: 8.66 kcal g−1 (36.25 kJ g−1 ). The heat of combustion of protein is considered the same for mammals and fish: 5.65 kcal g−1 (23.65 kJ g−1 ). When body protein is used as an energy source, as during starvation, the metabolizable energy is only 4.80 kcal g−1 (20.1 kJ g−1 ) because some energy is lost with the nitrogen excreted as ammonia. Brett and Groves give a value of 4.10 kcal g−1 (17.16 kJ g−1 ) for mammal and fish carbohydrate. However, the carbohydrate content of fish is usually much less than 1% of wet weight, so this component is often omitted in analysis of fish energy density. Recent work is showing differences in fatty acid composition among species and among sizes of fish within species, probably related to differences in diets (e.g., Iverson et al . 2002), and this would contribute to variation in the mean energy value of lipid. Fish total energy content (E, kJ) can be calculated from the energy values of the component tissues. Let F represent the gram of lipid (fat) and P represent the gram of protein in a fish. The total body energy will be given by the following equation, where Df is the energy density of lipid (kJ g−1 lipid) and Dp is the energy density of protein (kJ g−1 protein). E = F Df + P Dp Fish energy density (d = E/W , kJ g−1 ) can be calculated by dividing E by total wet weight (W , g). Let f = F /W represent lipid content as a fraction of total weight, and p = P /W represent protein content as a fraction of total weight. d = f Df + pDp From these equations it is clear that fish energy density depends on proximate composition. Energy density is expected to be linearly related to the fraction lipid, and therefore, energy density is expected to change with body condition. Fish in better condition generally have higher levels of lipid, which translates into higher energy density. Fish percent dry weight changes with ontogeny. Larval fish have a much higher percentage of water and a lower energy density compared to older and larger fish. Breck (1993) reported that bluegill smaller than 6 mm were about 10% dry weight, and the median value for fish from 8 to 31 mm was 18% dry weight. McComish (1974) measured percent dry weight in 100 bluegill ranging from 35 to 192 mm and observed a range from about 24 to 33% dry weight. When bluegill data for small individuals (4.4–31.2 mm TL; Breck unpublished) are combined with the data of McComish (1971, 1974) for larger individuals (37–192 mm TL), one can observe a clear trend for percent dry weight to increase with body length (Figure 7.5). Typical body composition and energy density of bluegill in relation to fish length can be estimated from the regression equations shown in Figure 7.5 and additional data and information from McComish (1971, 1974). Fraction water (h) was estimated from the regression equations shown in Figure 7.5 for wet weight (W ) and dry weight (Wd ) in relation to length (L). h = 1 − Wd /W log10 (Wd /W ) = −1.060 − 0.255 log10 (L). Analysis of McComish’s (1971) data for grams of water (H = hW ) and grams of protein (P ) revealed a very strong relationship: loge (P ) = aP + bP loge (H )

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Length (mm) Figure 7.5 Wet weight and dry weight of bluegill over most of the common length range for this species. Data for individuals from 37 to 192 mm (N = 100) are from McComish (1971); data for individuals from 4.4 to 31.2 mm (N = 141) are from Breck (unpublished). Regressions use the equation: log10 (W ) = a + b log10 (L), N = 241. For wet weight, a = −5.416 (95% CL: ±0.026), b = 3.331 (±0.016), R2 = 0.999; for dry weight, a = −6.476 (±0.034), b = 3.586 (±0.021), R2 = 0.998. For reference, the equation for bluegill standard weight is shown as a dotted line (a = −5.374, b = 3.316). Because the slope for dry weight (3.586) is larger than the slope for wet weight (3.331), longer fish tend to have higher fraction dry weight and lower fraction water than smaller fish.

where aP = −1.535 ± 0.016, bP = 1.040 ± 0.006; N = 100, R 2 = 0.999, so water content can be used to estimate protein content. McComish (1974) reported a very strong relationship between grams of ash (A) and length: loge (A) = aA + bA loge (L) where aA = −16.674, bA = 3.540; N = 100; R 2 = 0.99. Therefore, length can be used to estimate wet weight and dry weight (Figure 7.5), fraction water and grams of water, and grams of ash. Water content (H ) can be used to estimate protein (P ). Grams of lipid (F ) can be estimated by subtracting water, protein, and ash from wet weight. Proximate composition can then be expressed as fractions of body weight and plotted in relation to fish length (Figure 7.6). The fractions of protein and lipid can be used to calculate energy density, which decreases as fraction water increases (Figure 7.7). These figures show the general pattern of body composition as bluegill increase in length. Individuals that are heavier at a given length would be expected to have a smaller fraction water and a larger fraction protein and lipid. Fish percent dry weight typically changes with body condition. Anderson (1959) and McComish (1974) both found a significant positive correlation with condition factor (K = 105 · W/L3 ) in bluegill. Fish energy density can have a strong seasonal component, often highest in the fall and lowest at the end of winter. This has been noted in largemouth bass (Brown and Murphy 1995) and white crappie (Bunnell and Marschall 2003). The effect of such seasonal changes on bioenergetics model predictions depends on the question being asked. Stewart and Binkowski (1986) used their bioenergetics model of alewife to compare simulations that included seasonal changes in alewife energy density to simulations using a constant energy density. They found that estimates of annual production and consumption differed by less than 10%, but there were larger differences in the seasonal estimates of production and consumption. The studies of centrarchid life history by Bunnell and Marschall (2003) and Garvey and Marschall (2003) suggest that a seasonal pattern of energy storage can contribute to fitness.

Fraction water, protein, lipid, ash

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1.0 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0

50

100

150

200

Length (mm) Water

Protein

Lipid

Ash

Figure 7.6 Body composition of bluegill in relation to fish length, estimated from data of McComish (1971).

There are two common observations regarding energy density and body composition. The first is that percent lipid declines as percent water increases; the second and related observation is that energy density (J g−1 wet weight) declines linearly as percent water increases (Brett et al . 1969; Henderson and Ward 1978; Rottiers and Tucker 1978; Love 1980; Weatherley and Gill 1983; Van Pelt et al . 1997). Breck (1998, 2008) proposed an explanation for these observations based on a mass-balance constraint and the hypothesis that a certain amount of water is associated with each gram of protein, and another smaller amount is associated with each gram of lipid in the body. If these amounts of water per gram protein and water per gram lipid are constant (e.g., for a specific size of fish and outside the range of starvation), then it can be shown that percent lipid will vary linearly with percent water, and that energy density will be a linear function of percent water. Because percent water changes with body size (Figure 7.6), these expected linear relationships for lipid and energy

10.0

0.16

7.5

0.12 5.0 0.08 2.5

0.04 0.00 0.65

0.70

0.75

Energy density (kJ g−1)

Fraction of protein, lipid, ash

0.20

0.0 0.80

Fraction of water Protein

Lipid

Ash

Energy density

Figure 7.7 Body composition and calculated energy density of bluegill in relation to fraction water, estimated from the data of McComish (1971). Energy density calculations assume 36.25 kJ g−1 lipid and 23.65 kJ g−1 protein.

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density can appear noisy or even curvilinear if data from a wide size range of fish are combined; including log(W ) in the analysis can reduce the unexplained variation (Breck 2008). Pearse (1924) was apparently the first to measure the body composition of entire fishes. Earlier workers had measured edible portions or other parts. Working at the University of Wisconsin, Pearse also seems to have been the first to measure the body composition of centrarchids (largemouth bass and pumpkinseed), which he captured in Lake Mendota. His sample sizes were very small. He fed two juveniles a variety of invertebrates and other foods for 63 days and compared them with one juvenile that was starved for 63 days and another that was just caught from the lake. The two fed fish approximately doubled their weight (initial mass: 15.0 and 27.1 g; final mass: 36.94 and 62.84 g), had a relatively modest amount of water (73.72 and 71.31%), a relatively modest amount of fat (2.88 and 6.53% wet mass), and a modest amount of ash (4.13 and 4.11%), compared to the fish that starved (from 60 to 46.3 g), which had 75.73% water, 7.24% ash, and 0.51% fat. The fish caught fresh from the lake on August 20 was 25.71 g, 77.11% water, 3.78% ash, and 1.46% fat. He also compared two starved pumpkinseed with one fed and one caught fresh in the lake. The one starved fish decreased from 75.3 to 55.82 g in 62 days, with a final 76.01% water, 6.93% ash, and 0.42% fat; the other starved fish decreased from 70 to 37.89 g in 72 days, with a final 73.39% water, 9.53% ash, and 0.44% fat (this fish was dead when measured, but was alive the previous day). The fish fed for 84 days had a final mass of 26.37 g, had 72.75% water, 4.39% ash, and 5.64% fat. The fresh-caught fish weighed 52.68 g, had 74.44% water, 4.96% ash, and 2.35% fat. Note that the increased percentage of ash in the starved fish was almost certainly due to a reduced amount of other material with a constant mass of ash, not an increase in the mass of ash. These data are consistent with more recent information (Gerking 1955; Lee 1966; Savitz 1971; Niimi 1972; Garvey et al . 1998; McCollum et al . 2003). Together they suggest that centrarchids have a relatively low amount of fat and a high amount of ash compared to salmonids (e.g., Rottiers and Tucker 1978). Gerking (1955) studied the influence of consumption rate on body composition and protein metabolism of bluegill. Bluegill fed mealworms at higher rates grew at higher rates and developed higher levels of lipid. Savitz (1971) studied nitrogen excretion and protein consumption by bluegill. Niimi (1972) described the changes in body composition of largemouth bass during starvation, and Savitz (1971) did the same for bluegill. They both found that lipid level decreased with starvation. Niimi (1974) described the relationship between ash content and body weight in largemouth bass (and two other species). McComish (1974) developed regression models to predict the proximate body composition of bluegills. Consumption rate’s influence on body composition and energy density probably provides part of the explanation for the consumption-dependent errors recently identified in bioenergetics models (see Sections 7.2.4 and 7.3.5). Stock fish placed on reduced rations would be expected to reduce their energy density over several days; a bioenergetics model that used a higher value of energy density appropriate for the initial stock fish would tend to underestimate growth (or overestimate weight loss). Similarly, stock fish placed on increased rations would be expected to increase their energy density and lipid level over several days; a model that used the (lower) level of energy density of the stock fish would tend to overestimate growth. These are the directions of model errors identified by Bajer et al . (2004b). Careful measurements of energy density before and after such experiments would indicate how much of the model error could be explained by such expected dynamic changes in energy density. Hartman and Brandt (1995) describe methods of estimating energy density of fish. One recent method uses inductance, which varies with the proportion of water in the body, to estimate body composition. Lipid content has a large influence on fish energy density. The measured value for lipid content can depend significantly on the chemical method used to extract the lipid (Randall et al . 1991). Standard methods are important. Few energetics models have tracked body composition in addition to weight. An early model that incorporated body composition was developed for the African catfish Clarias gariepinus (Machiels and Henken 1986, 1987). Garvey and Marschall (2003) modeled seasonal energy allocation to growth, fat, and gonad for largemouth bass populations at low and high latitudes, and Bunnell and Marschall (2003) developed a similar model for white crappie. Schindler and Eby (1997) considered the stoichiometry of fishes and their food and asked whether fish growth was likely to be limited by nitrogen or phosphorus. They note that in the unusually rapid growth in some aquaculture situations, fish growth can be limited by the availability of N or P in the food. Their analysis of 28 populations and 18 species revealed that growth was almost always limited by energy and not by N. In only 3 of 186 cases examined (1.6%) was growth limited by P.

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7.6.2 Maximum sizes In contrast to birds and mammals, fish have plastic or indeterminate growth. Growth continues as long as energy intake exceeds energy expenditure. For some fish species, there is a limit to the number and size of muscle fibers in the body (Weatherly and Gill 1987). For these species, growth in size can continue until this limit is reached. There are an increasing number of suggestions that the optimum growth rate for fish may be less than the maximum possible growth rate (see Section 7.3.3). If these suggestions turn out to be correct, then it may be rare that fish approach a maximum size for the species. Under the Von Bertalanffy model, all fish approach a maximum specified size for that population.

7.6.3 Condition indices The related topics of fish condition and growth in length are areas where recent progress has been made and where further development and application of bioenergetics models would be helpful. Fish condition refers to relative plumpness, fish weight in relation to length, hence simulating changes in fish condition require simulating changes in fish length as well as weight. Proximate body composition and energy density are also involved. Fish in good condition generally have higher levels of lipid, higher energy density, and are more resistant to starvation than fish in poor condition. Female bluegills in poorer condition have lower fecundity than females in good condition (Breck 1996). Recent work on white crappie demonstrates that condition influences the rate of growth in length (Bajer 2005; Bajer and Hayward 2006). For a given increase in weight, fish in poor condition allocate more of the new tissue to improving condition and consequently grow less in length than fish in good condition (Bajer and Hayward 2006). Fish condition thus affects survival, reproduction and growth in length. Many different condition indices have been used on centrarchid fishes and here we briefly summarize some of those indices as well as centrarchid bioenergetics models involving changes in condition. Heidinger and Crawford (1977) showed that the liver-somatic index (liver weight as a percentage of wet weight) of largemouth bass varied with temperature and feeding rate. The relative size of the liver was shown to be an index of the average feeding rate over the past several days. Wege and Anderson (1978) introduced relative weight (Wr ) as a new index of condition. Standard weight (Ws ) reflects a reference weight for fish of a particular length (L) (Wege and Anderson 1978): Ws = aLb where a and b are constants for a given species. Relative weight (Wr ) expresses fish weight (W ) as a proportion (or percentage) of standard weight, and is an indication of the relative plumpness or condition of an individual compared to the standard. W Wr = Ws Murphy et al . (1991) proposed standard weight equations for several game fishes, including several centrarchids. Smith et al . (2005) used the changes in body shape that occur with starvation to devise a morphological index of nutritional status for larval largemouth bass (8.0–15.4 mm SL). They developed a multivariate index based on 23 characters that was able to correctly classify 92% of fed and 78% of unfed individuals. Most of the differences between fed and unfed fish occurred along the vertical body dimension, especially near the abdomen. A much simpler index, based on the ratio of body depth at the anus to standard length, was almost as effective, correctly classifying 83% of fed and 79% of unfed fish for the 7 days of the experiment. As expected, the magnitude of difference between fed and unfed fish increased with days of starvation. Weber et al . (2003) discuss several biochemical indices of condition in juvenile fishes. They discuss whole-body total lipids, whole-body triglycerides, muscle RNA:DNA ratio, and muscle protein. The novel aspect of their study is that all indices were measured for each individual fish. This permits analysis of how the suite of indices changes over time, for example, in comparing fed versus starved individuals. They give recommendations of methods for each biochemical

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index. For a starved group of juvenile rainbow trout, the RNA:DNA ratio decreased after just a few days, and whole-body lipids and triglycerides decreased to very low levels by day 18; however, mortalities did not begin until day 32 of their experiment. One early application of a bioenergetics model (Figure 7.1) was to a largemouth bass population in a power-plant cooling pond, where the model was used to better understand the factors that might be responsible for the poor condition (extreme thinness) of the bass at certain times of the year (Rice et al . 1983). Van Winkle et al . (1997) developed a model that included dynamic changes in body condition. Bajer (2005) and Bajer and Hayward (2006) showed very nicely that, for a given increase in weight, growth in length depends on relative condition. For the same level of consumption, fish in good condition had a greater rate of growth in length than fish in poor condition. They presented a method for estimating growth in both length and weight in white crappie using a modified bioenergetics model.

7.6.4 Stunting Stunting occurs in many centrarchid species, notably bluegill, black crappie, and largemouth bass. Stunted fish are small for their age, and their growth rates are low relative to some standard. Not all populations of small fish are stunted; if mortality rate is high, a population may have predominantly small fish despite rapid growth. The following comments are directed toward the issue of stunting, not small size per se. Several hypotheses have been advanced to explain stunting in centrarchids, including genetics, food availability per fish, and social influence of size at maturity of male bluegill. The energetics of growth are involved in several but not all of these hypotheses. The proximate cause of stunting is a low amount of energy used for growth. The more ultimate cause of such low energy is selection for life history strategies that maximize contribution of offspring to the next generation. This can result from high recruitment, without sufficient mortality to produce a good-growing density. One hypothesis is that genetic differences cause some populations to grow at a slower rate. This can definitely occur, as shown in common garden experiments involving young striped bass (Morone saxatilis) from various locations reared in identical conditions (Conover et al . 1997). However, in most cases of stunting in centrarchid populations, genetics seems unlikely to be the major cause of slow growth (e.g., pumpkinseed; Heath and Roff 1987). Similarly, the genetic hypothesis for stunting has been studied—and rejected—in fish populations from other fish families (e.g., yellow perch; Heath and Roff 1987). The major cause of stunting in centrarchid populations is a high density of juveniles, resulting in a reduced availability of food per individual. Evidence for this comes from observations and experiments. Fish increase their growth rate when moved from stunted populations to conditions with more food (Bennett et al . 1940, cited in Parker 1958). When the density of stunted populations is sufficiently reduced, either by winterkill (Beckman 1950) or experimental or management action (Parker 1958; Schneider and Lockwood 2002), the growth rate increases significantly. The effects of such actions or events typically last only a few years; growth rate slows over time, and the size structure returns to the stunted condition as the population biomass of fish increases (Schneider and Lockwood 2002). Similar responses occur in other fishes (e.g., roach Rutilus rutilus, Burrough and Kennedy 1979; bream Abramis brama, Wright 1990; white sucker Catostomus commersoni , Brodeur et al . 2001; Arctic charr Salvelinus alpinus, Amundsen et al . 2007). The growth rate of male bluegills depends in part on the size structure of the population. In bluegill, where there is strong female preference to mate with larger males, the sizes of males that are successful at mating depend on the size structure of the male population (see Chapter 5). If large male bluegills are sufficiently abundant in the nesting colony, then smaller males will be unsuccessful at mating (Jennings et al . 1997), so it is to their advantage to allocate more energy toward growth rather than reproduction until they attain a larger size. If large male bluegills are sufficiently rare or absent, then there may be a decline in male size at age as more male fish allocate a larger proportion of available energy to reproduction instead of growth. An experiment is currently underway in Illinois to examine the social hypothesis for fish maturing at a small size (see Chapter 5). Growth rate of juvenile centrarchids in the littoral zone can be independent of the growth rate of adults (Osenberg et al . 1992; Mittelbach and Osenberg 1993). Mittelbach and Chesson (1987) presented a two-stage population model for bluegills.

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7.6.5 Overwinter survival Growth can influence overwinter survival of centrarchid fishes in several ways. Growth during summer and fall influences fish body size as winter begins, and therefore affects the vulnerability to size-dependent predation. There also appears to be size dependence in the ability of some species to tolerate low temperature (Oliver et al . 1979). Growth influences the amount of energy reserves available to sustain the fish until food availability increases in the spring. Because of the allometry of respiration rate, larger fish use energy at a lower weight-specific rate than do smaller fish. In long-term controlled experiments that simulated exposure to typical winter temperature regimes, Oliver et al . (1979) found that young-of-year (YOY) smallmouth bass overwinter survival was directly related to size and body composition. Long fish survived better than short fish, and the ratios of mean dry weight to wet weight and ignitable weight to dry weight appear to be useful for differentiating between survivors and those that succumb to prolonged cold exposure. The standard fisheries approach to modeling survival is to account for natural mortality and fishing mortality, usually with constant age-dependent instantaneous rates (Ricker 1975). Although this is a useful approach for fisheries assessment, it can need modification when applied to bioenergetics models that focus on dynamic individual and population responses within a year. For example, bioenergetics models that account for changes in condition, or energy reserves permit the modeling of starvation mortality as an increased probability of death as condition declines or energy reserves are exhausted (Rice et al . 1983; Breck 1993, 1998; Kooijman 2000). Wright et al . (1999) concluded that the bioenergetics models they tested made poorer predictions for winter conditions than for summer. Adams et al . (1982) used a bioenergetics model of adult largemouth bass to evaluate the dynamics of food consumption, somatic and gonadal growth, energy storage, and activity throughout the year with emphasis on the overwinter period when prey abundance is lowest. They found that in a Tennessee reservoir during the winter, consumption and standard metabolism were low and no growth or energy storage occurred. During these periods of low food consumption, lipids were probably utilized from both the body and the viscera. Their modeling suggested that winter energy demands were greater than that which could be accounted for by catabolism of body tissue alone, and thus some consumption occurred throughout the winter at reservoir temperatures of 6 to 10◦ C. Garvey et al . (1998) used a combination of reservoir surveys of natural responses and experimental manipulation in reservoirs, ponds, and artificial pools to assess size-related overwinter survival of largemouth bass. They determined that the lower survival rate of the smaller individuals was more likely due to greater susceptibility to predation than for energetic reasons such as a lower amount of stored energy reserves. From field and laboratory observations with age-0 white crappie, McCollum et al . (2003) found that winter severity was a better indicator of overwinter survival than size, feeding level, or energy depletion. In laboratory studies, only 47% of all white crappies survived a simulated severe winter, whereas 97% survived a simulated mild winter. In severe winter, neither of the indicators listed earlier influenced mortality. They suggest that osmoregulatory failure as a result of exposure to temperatures colder than 4◦ C for at least 1 week may be responsible for high mortality rates.

7.7 Reproductive energetics There are several aspects of reproduction that have important energetic ramifications, including energetic costs of gonad development, nest building, and parental care. Most bioenergetics models do not account for somatic and gonadal growth separately, but typically include both in a single compartment. Increased activity costs due to spawning, and parental care also are rarely included in bioenergetics models.

7.7.1 Gonad development costs A bioenergetics model for centrarchids needs to account for the energy costs of reproduction, including gonad development and parental care. As in all fishes, reproductive costs of gonad development are much greater for females than for males. To the contrary, reproductive costs of parental care for centrarchids are much greater for males, because it is the males

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that make the nest, guard the eggs and larvae, and, in black bass, guard the fry for several weeks after they leave the nest. In bluegill, a variable proportion of young males become mature precocially (sneakers), allocating some energy to reproduction instead of growth, and probably foregoing some foraging during reproductive bouts. Species that spawn in early or late spring (e.g., largemouth bass, smallmouth bass, black crappie, and white crappie) tend to begin accumulating energy for reproduction in autumn, whereas species that spawn in summer (e.g., bluegill) can wait until spring to allocate energy to reproduction (James 1946; Morgan 1951a, 1951b; Adams et al . 1982; Bunnell and Marschall 2003; Garvey and Marschall 2003). Morgan (1951a, 1951b) measured the gonadosomatic index (GSI, gonad mass as a percentage of body mass) for bluegill, black crappie, and white crappie in Buckeye Lake, Ohio, from mid-March to late August, usually at intervals of 3 to 7 days (note: actually, he reported the ratio of body mass to ovary mass, which is the inverse of GSI—here, we have expressed his results in terms of the more familiar GSI). He observed that female bluegill GSI was very low (average GSI about 1.1–1.7%) during March and April, increased rapidly to about 7.7% between May 5 and May 14, 1949, remained high through the summer (average GSI from 6.6 to 12.5%), and decreased in late August back to very low levels. In contrast, black crappie increased their GSI during late summer and fall, with the level in November similar to the level the next March, hence, based on gonad size, he speculated that their gonads are ready to spawn with little additional energy needed. What determines the seasonal pattern of allocation to reproduction? Bunnell and Marschall (2003) combined dynamic programming with an IBM to examine optimal timing of energy allocation to reproduction in white crappie. The dynamic programming model for largemouth bass developed by Garvey and Marschall (2003) suggests that fish should begin storing energy for reproduction in the fall to prepare for reproduction in early spring. The costs of gonad development depend on the size of the gonads and their energy content. Female ovaries are much larger than male testes (James 1946). Ovary size varies with available energy. Breck’s (1996) pond experiments with bluegill showed that female GSI in June varied inversely with stocking density for fish stocked in April, but the number of eggs per gram of bluegill ovary was not significantly different among the stocking-density treatments. Energy content of ovaries is higher than the whole-body average, due to the relatively large amount of lipid in eggs. Bunnell and Marschall (2003) reported that ovaries of white crappie are about 1.33 times the energy density of somatic tissue. For bluegill and pumpkinseed, eggs in the ovary can be in different stages of development, and an individual female can deposit eggs at several times during the late spring and summer (James 1946; Fox and Crivelli 1998). This is in contrast to largemouth bass, in which eggs tend to develop at the same time and females deposit all their eggs in a short period (James 1946).

7.7.2 Nest building and guarding Nests are made by males using strong movements of the caudal fin directed downward toward the sediment, combined with compensatory movements by the pectoral fins to minimize forward motion of the fish. When a nest is built in very shallow water, some of the energy directed at excavating the nest is lost in making waves on the surface of the water. To our knowledge, the energy costs of nest building have not been measured. In all centrarchids, males guard nests from spawning through the swim-up stage. The period of guarding is of longer duration in black bass, because the males guard fry for several weeks after they have left the nest. Cooke et al . (2002) monitored male smallmouth and largemouth bass as they guarded nests at about 18◦ C and reported that the duration of stages at that water temperature was 3 days for the egg stage, 2 days for egg-sac fry, 2 days for swim-up fry, and 15 days for free-swimming fry, for a total of 22 days of guarding. For both smallmouth bass and bluegill, larger individuals tend to nest and spawn earlier than smaller adults and tend to be in better condition than smaller bluegill (Ridgway et al . 1991; Baylis et al . 1993; Lukas and Orth 1995; Cargnelli and Gross 1997; Wiegmann et al . 1997). A similar pattern has been observed for largemouth bass in pond experiments (Goodgame and Miranda 1993), but was not observed in Ohio reservoirs (Garvey et al . 1988). Energy costs of guarding are due to lack of feeding, and increased respiration rate due to increased activity. Most of the cost of nest guarding appears to be due to the foregoing of foraging. Male centrarchids do not leave the nest to forage in order to protect eggs and fry, which can be attacked by nest predators within seconds or minutes. This means that, apart

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from rare opportunistic feeding at the nest (Hinch and Collins 1991), the male must survive the guarding period using stored energy. Cooke et al . (2002) monitored the activity level of guarding black bass using radio transmitters with implanted electrodes that indicated activity of axial red muscles. They found that nesting males had elevated activity compared to nonnesting bass, that activity was elevated during both day and night, and that activity level varied with developmental stage of the brood. For example, for male largemouth bass, they determined average swimming activity of about 43 km d−1 (0.50 m s−1 ) during their offspring’s egg stage, 58 km d−1 (0.67 m s−1 ) during the egg-sac fry stage, 37 km d−1 (0.43 m s−1 ) during the swim-up fry stage, and 52 km d−1 (0.60 m s−1 ) during the free-swimming fry stage. Relatively long periods of low activity, including fanning the eggs, are interrupted by short periods of high activity that indicate rapid movements to drive away potential nest predators. They estimated that the activity level of nesting males was about double than that of nonnesting fish. The instantaneous activity level for free-swimming, nonnesting smallmouth bass was estimated to be 0.317 m s−1 , based on a similar study conducted in Lake Erie. Cooke et al . (2002) used the Wisconsin Bioenergetics Model 3.0 with parameters from Rice et al . (1983) to simulate energy expenditure of 1000 g nesting and nonnesting largemouth and smallmouth bass. They used activity levels that varied with the developmental stage of the offspring, as measured in the field. Over a 22-day nesting period, and accounting for variations in male activity level among brood developmental stages, they estimated that a nesting, nonfeeding largemouth bass would lose 125 g, whereas a nonnesting, nonfeeding male would lose 83 g in 22 days. A nesting, nonfeeding smallmouth bass would lose 115 g, whereas a nonnesting, nonfeeding male would lose 98 g. Based on these values, 66% of the mass lost by nesting largemouth bass is due to foregoing feeding, and 34% is due to increased activity. For nesting smallmouth bass, 85% of the mass lost is due to foregoing feeding, and 15% is due to increased activity. Costs of reproduction are high enough that males of most centrarchid species probably do not renest in the same year. In some systems, the cost of reproduction can significantly reduce survival of male smallmouth bass. Ridgway and Shuter (1994) provided supplemental food to parental smallmouth bass and found that this improved male survival in 1 year, compared to unfed males; in the second year it improved care duration and reproductive success but decreased survival. Wiegmann and Baylis (1995) had evidence that few male smallmouth bass were repeat spawners in the northern lake they studied. Apparently, the cost of reproducing was sufficiently high that the population they were studying was nearly semelparous, with up to 94% of males dying after their first reproduction.

7.7.3 Egg development time Egg development time can be included in an energetics model of a centrarchid full life cycle. Egg development time is also important in determining the duration of male parental care, thereby affecting the cost of parental care and the duration of high vulnerability to angling. Trebitz (1991) developed the following equation for time to hatch (th , day) for eggs of largemouth bass as a function of average water temperature (Tave ,◦ C), based on data in Heidinger (1976). e9.88 T −1.88 24 Gillooly et al . (2002) recently derived a model from first principles of allometry and biochemical kinetics that explains the general pattern across taxonomic groups: egg development time is predominantly a function of temperature and egg size. The time to hatch is shorter at higher temperatures and for smaller eggs. Their model explained 83% of the variance in a data set of 59 values for fish egg size, temperature, and time to hatch (Gillooly and Dodson 2000; Gillooly et al . 2002, their Figure 1). Their general model was fitted to data for both aquatic ectotherms (including fishes and amphibians) and birds: 4m1/4 th = a(Tc ) where th is the time (day) to hatch, m is the egg mass (g), and a(Tc ) is a function that expresses the temperature dependence of development:  
 αTc + yint a(Tc ) = 4 exp − 1 + Tc /T0 th =

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40 2.00 mm, smallmouth bass 1.67 mm, largemouth bass Time to hatch (d)

30

1.45 mm, redear sunfish 1.20 mm, bluegill 1.05 mm, pumpkinseed

20

0.89 mm, white crappie 10

0 10

15

20

25

30

Temperature (°C) Figure 7.8 Predicted time to hatch (days) increases with egg diameter (millimeter, converted to mass, gram) and decreases with temperature (Gillooly et al . 2002). Egg diameters are representative of several common centrarchid species.

where α = −0.12 per degree Celsius is the slope, and yint = 6 is the intercept of the regression of mass-adjusted time to hatch versus scaled temperature, T0 = 273 Kelvin is the freezing point of water, and Tc is the temperature (◦ C) to which the eggs are exposed. Gillooly et al . (2002) also indicate how to compute the time to hatch for fluctuating temperatures. Winemiller and Rose (1992) compiled life history characteristics for many North American fishes, including 16 species of centrarchids. In their compilation, mean ovum size in centrarchids varies from 0.89 mm in white crappie, to 1.20 mm in bluegill, to 2.00 mm in smallmouth bass. According to the model of Gillooly et al . (2002), the egg-size effect would result in faster development times in white crappie than smallmouth bass, with bluegill intermediate. Because smallmouth bass spawn at cooler temperatures (15 or 16◦ C) than bluegill (about 20◦ C), the temperature effect would result in faster development times for bluegill. Figure 7.8 shows the predicted effect of temperature and egg size on time to hatch for several egg sizes, selected to represent the range of centrarchid egg sizes in the compilation by Winemiller and Rose (1992). These predicted hatching times, based on the broad biological pattern across many taxa, are probably overestimates for centrarchids. However, the general relationships presented may encourage others to measure these data and estimate α and yint specifically for centrarchids and consider the possible consequences of egg mass, temperature, and hatching time for evolution of life history traits, including the trade-off between egg size and egg number (Gillooly and Dodson 2000).

7.7.4 Modeling energetics of reproduction Modeling energetics of reproduction has grown increasingly sophisticated, particularly in addressing questions involving reproduction. In early bioenergetics models, including the first and second versions of the Wisconsin software package (Hewett and Johnson 1987, 1992), fish biomass (W ) was the only state variable, and reproduction was incorporated by decrementing W once per year by the average reproductive loss (G). For example, on the specified annual date of reproduction, if average reproductive losses were 10% of body mass, then W would be decremented by G = 0.10 ∗ W . Using this same basic approach, separate model runs can be done for males and females, to account for differences in gonad mass lost at spawning. Adjustments can also be made to account for the energy density of eggs and milt relative to that of the rest of the body. The standard model can be used to estimate the costs of male guarding of offspring, by increasing fish metabolic rate (by increasing the simulated swim speed) and setting consumption to zero during the guarding period. Cooke et al . (2002) used this approach to estimate the energy costs of parental care by male largemouth bass and smallmouth bass, as described earlier.

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Bunnell and Marschall (2003) used a dynamic programming approach to determine optimal allocation of energy between growth in length and growth of gonads during a year for different feeding conditions. Length and gonad mass were tracked separately for the fish, a change from the Wisconsin model. The optimal allocation pattern was the one that maximized lifetime fitness of modeled fish, with fitness evaluated as the expected number of larvae produced. Their analysis of white crappie in Ohio reservoirs indicated that some energy should be allocated to gonad development as early as fall if feeding conditions might not be favorable in the spring. Interestingly, the benefit of allocating energy to ovary development in the fall was strongly dependent on the likely feeding conditions the following spring, not on feeding conditions earlier in the summer. Garvey and Marschall (2003) developed a model to analyze energy allocation patterns of largemouth bass for different feeding conditions and different latitudes. Their model separately tracked allocation of energy to somatic growth (increase in length), fat, and reproductive tissue. Their question required the model to include these separate compartments. A theoretical reciprocal transplant experiment allowed them to compare the success of fish with an optimal northern strategy “transplanted” to a southern environment versus the success of fish with an optimal southern strategy “transplanted” to a northern environment. The southern strategy was not successful in the north because they did not allocate sufficient energy to fat reserves prior to winter and did not begin early enough to allocate energy to ovary development.

7.8 Synthesis Because rapid growth and high reproductive output are highly selected for in most fishes, behaviors that result in maximizing net energy gain should be commonly observed. Such behaviors include both habitat selection and feeding choices. One feature of habitat choice that has been described for several centrarchid species is temperature preference (see related discussion in Chapter 8 of this book). Fish typically prefer a narrow range of temperatures within which physiological processes, such as digestion, energy assimilation, and growth, are presumed to be most efficient (Reynolds 1977; Magnuson and Beitinger 1978; Jobling 1981). Several laboratory studies have demonstrated the ability of centrarchid species (bluegill, rock bass, black crappie, smallmouth bass, and largemouth bass) to maintain their temperatures within a few degree range in shuttle-box test chambers (Neill and Magnuson 1974; Reynolds and Casterlin 1978; Wildhaber and Crowder 1990). Centrarchid species have also been observed exhibiting thermoregulatory behavior in the field (Zimmerman et al . 1989). As with choice of thermal habitat, the type of feeding strategy exhibited also has energetic consequences. Several investigators have used centrarchid species as experimental subjects to test predictions of optimal foraging theory. Werner (1974) and Werner and Hall (1974) used theoretical modeling and laboratory experimentation with bluegill to show that prey size selection is related to the optimal allocation of time spent searching for and handling prey. Stein (1977) similarly found that smallmouth bass size-selectivity on crayfish prey resulted in maximizing net energy intake by balancing handling and pursuit time with prey caloric content. To the contrary, Stein et al . (1984) found that prey selection by redear sunfish on various snail species in the laboratory was not consistent with optimal foraging predictions. Crowder and Cooper (1982) and Savino et al . (1992) both studied the relationship between vegetation density and the ability of bluegill to choose prey that maximized net energy intake. The experimental results of Savino et al . (1992) did not find a difference in growth rate (i.e. net energy intake) at different plant densities as predicted by Crowder and Cooper (1982). Manatunge and Asaeda (1999) developed a model to predict the feeding selectivity of white crappie and bluegill based on the caloric benefit and energetic cost of searching for and consuming different sized zooplankton. A comparison of stomach samples from fish in the field to the available prey base at the same location demonstrated that the fish were selecting prey as predicted by the model, which matched predictions of optimal foraging theory. Living an energetically efficient life in the wild, however, is rarely as simple as selecting the right temperature or consuming the perfect size prey. More often than not these choices are entangled in consideration of several factors in combination. For example, Neil and Magnuson (1974) tested the effect of food availability on behavioral thermoregulation and found that bluegill would spend increased time at temperatures above the preferred temperature to acquire food. Bevelhimer (1996) found similar results in laboratory studies where smallmouth bass altered the amount of time they spent at higher than preferred temperatures depending on food availability. Smallmouth bass were willing to spend significant time at an energetically costly temperature in exchange for foraging opportunities, especially when the available ration was less than satiation; when satiated, smallmouth bass returned to cooler, lower cost temperatures.

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Energetic trade-offs also occur in habitat choices related to things other than food availability. Energy efficiency is sometimes compromised for survival as shown in studies that demonstrated how risk of predation can cause fish to exhibit less than optimal feeding strategies (Werner et al . 1983; Mittelbach 1984). Similarly, Bevelhimer (1995, 1996) demonstrated that, in both field and laboratory settings, smallmouth bass would forego habitats with more energetically favorable thermal conditions in favor of those with physical cover and suboptimal temperatures. Because the standard bioenergetics models are not able to handle the energetic consequences of predator avoidance and many habitat choices, some researchers have instead used IBMs mentioned earlier to incorporate factors that directly and indirectly affect fish energetics. These models have been used to investigate smallmouth bass YOY recruitment (DeAngelis et al . 1991), largemouth bass juvenile survival and recruitment (Trebitz 1991), bluegill fry density and growth relationships (Breck 1993), and the effects of alternate river flow regimes on smallmouth bass populations (Jager et al . 1993).

7.9 Research needs Like many other fundamental aspects of fish biology, basic studies on fish energetics seem to have become pass´e to many researchers. Analytical methods and instruments that can be used to measure various aspects of fish physiology and biochemistry are no doubt much more advanced than 10 or 20 years ago, but the volume of empirical studies on fish energetics seems to not have kept up with the technology. Basic energetic relationships have not been determined for most centrarchid species. In the absence of species-specific data for parameters used in bioenergetics models, researchers resort to borrowing parameters from other species to construct new models. For closely related species with similar life histories (e.g., diet, body shape, and behavior), one might expect to find similar physiological energetics. Unfortunately, few simultaneous studies have been performed with multiple species to determine the degree of similarity among congeneric species. The only such study we found for centrarchids is O’Hara (1968) who determined metabolic rates for bluegill and pumpkinseed sunfish. A good example of such a study is Bevelhimer et al . (1985) who simultaneously determined rates of metabolism, food consumption, and growth for two esocid species and a hybrid. Along these lines, there is a great need for detailed studies on the bioenergetic differences between largemouth bass and Florida bass given the economic and recreational importance of these species. Other than for largemouth bass, there are no studies on geographic variation in bioenergetics parameters within other species. Virtually nothing is known of the energetics of the smallest centrarchids, such as the Enneacanthus species. There are several aspects of fish energetics that are still poorly understood, not just for Centrarchidae but for other families as well. General areas in need of more research include costs associated with activity and reproduction, allometry of feeding and respiration (i.e. the size-dependent coefficients in explanatory equations), and the effects of ration or nutritional status on energetic processes including compensatory growth. For example, the need for improvement in the ability of a largemouth bass model to handle fish of different sizes was demonstrated in a study with juvenile largemouth bass by Slaughter et al . (2004). Recent advances in understanding compensatory growth of centrarchid species are promising and have significant relevance to fish biology in general as discussed earlier. Of the 33 centrarchid species, we found published bioenergetics models for only 5 species (see Table 7.1; we did not count the spotted bass model which was a copy of a smallmouth model or the hybrid sunfish model which was a copy of a bluegill model). This area of research is wide-open for further development. Unfortunately, the development of models for new species usually depends on some management or conservation need and not so much on a basic quest to fill gaps in knowledge. An alternative to developing individual models for a variety of similar species would be the development of a reliable generic model that could be used interchangeably. Simultaneous laboratory studies would first be needed to define the degree of similarity among different genera and species. For some model parameters, differences among species are either nonexistent or so small that the same value may be representative of all species. For parameters where significant differences are observed, it might be possible to use adjustable parameters that are applied automatically based on various life history parameters, such as shape, diet, feeding mode, maximum size, level of activity, latitudinal distribution, etc. The general shape and magnitude of the relationships between some parameters (e.g., metabolic rate and feeding rate) and temperature may be applicable to several species by simple adjustment to the left or right along the temperature axis to account for

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different thermal optima. A comprehensive comparison of bioenergetics parameters for centrarchid species to those of other families (such as salmonids) would provide useful insight into the degree of within-family differences relative to amongfamily differences. Such an analysis would certainly add perspective to the importance or lack of species-specific models. More model validation and testing are desperately needed. A significant deficiency in bioenergetics modeling to date for all species has been the scarcity of studies with independent evaluations. Depending on the type of application, the level (or lack thereof) of model validation dictates the level of confidence one can have in the results. The greater the number of parameters borrowed from other studies, stocks, or species, the greater the need for model validation and testing. This is also the case when models are applied beyond the conditions (e.g., temperature, fish size, and ration), under which parameters were derived. Due to the lack of that one comprehensive and fully tested study that defines all the energetic parameters for a single species, there are many scientists and managers that will continue to view bioenergetics models with a great deal of suspicion. Centrarchid species, perhaps second only to salmonids in North America, have been the subject of a plethora of physiological studies and bioenergetics analyses for many years. The knowledge base derived from these studies has made possible the development of energy budgets and bioenergetics models that have been used to address a variety of fisheries management and conservation questions. The bioenergetics approach to investigating fish behavior, foraging, and growth is based on solid theory and has been proven to be a sound approach in fisheries science. However, our knowledge of fish energetics and our application of that knowledge in the form of bioenergetics models are still fraught with uncertainty and probably at least a little misunderstanding. As we continue to use bioenergetics models, we must also continue performing the basic experiments to continue to refine the underlying knowledge base. When specific metabolic functions and relationships become better understood and bioenergetics models are continually tested and improved, we can expect the use of such models and other energetic-based approaches to become more common and more useful in the management and conservation of centrarchid species.

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Chapter 8

Physiology and organismal performance of centrarchids J. D. Kieffer and S. J. Cooke

8.1 Introduction The relationship between fish and their environment represents some of the most fascinating examples of physiological adaptations among the animal kingdom. This is particularly the case for temperate fishes that experience distinct seasons that can include both harsh and cold winters and hot summers. With a few exceptions, most fish are ectotherms and therefore, their physiological processes and organismal performance, including swimming ability, metabolic rates, and enzyme activity are often dictated by water temperature. Furthermore, many freshwater fish live in a heterogeneous environment where oxygen concentrations vary extensively, making aerobic respiration a challenge. Individuals, populations, and species exhibit different tolerances to environmental conditions such as hypoxia (low oxygen) and temperature. When exposed to stressors, be it anthropogenic (e.g., angling, handling) or natural (e.g., winter, predation attempt, hypoxia), fish also exhibit variation in how they respond. Much of the existing research on the physiology, performance, and environmental tolerances of fishes involves the use of a salmonid model, and most frequently the rainbow trout. Aside from several other unique examples, such as tuna, Arctic fish, and desert fish, that have been well studied because they live in extreme environments or have special adaptations, we know less about the physiology of other fish groups, such as the centrarchids (sunfish). However, centrarchids have been studied because of their use in culture facilities, their hardiness in the laboratory, their wide availability in natural systems, and their importance in recreational fisheries. In addition, centrarchid fishes have value for use as physiological models because of their large variation in life history, both within and among species. Centrarchid fishes occupy a number of different niches and habitats and vary extensively in body size. The behavioral ecology and natural history of several species of centrarchids (e.g., bluegill, Lepomis macrochirus, largemouth bass, Micropterus salmoides) have been well studied (Miller 1975; Keast 1978; Gross 1980) such that this information can be used to form interesting hypotheses. Despite this background information and apparent value in studying centrarchid biology, there is a relative paucity of research on the physiology and performance of these fishes. In fact, most accounts on this group of fishes are rather disparate with no cohesive synthesis on an individual species or the family. For this reason, it has not been possible to develop a more general understanding of centrarchid physiology and performance. For the first time, we synthesize existing information on the physiology of centrarchid fishes. The specific objective of this chapter is to provide a detailed overview of the physiology of centrarchid fishes, with particular emphasis on how they cope with environmental (e.g., temperature, hypoxia) and biological (e.g., swimming, exercise) challenges. We adopt a comparative approach and discuss the relevance of centrarchid physiology to ecology, behavior and, when appropriate, management. Because of the wealth of knowledge on the physiology of salmonids, we also provide some direct comparisons between the physiology and performance of those fishes and the centrarchids. We conclude by providing a general discussion of the physiological patterns evident among the centrarchids focusing on both general patterns and variation. Issues that are applied are also covered in detail in other chapters (e.g., swimming performance relative to fishway design; sublethal impacts of catch-and-release angling). Other information relative to fish physiology and performance can also be found in the chapter of this volume on bioenergetics (Chapter 7).

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8.2 Baseline physiological variables A compilation of baseline physiological values for oxygen consumption rates, ventilation rates, blood variables, such as ion concentrations, energy reserves (e.g., protein and glucose), plasma hormone concentrations, and muscle enzyme and metabolite levels of various centrarchids is found in Table 8.1. We have also included in the table information about the size of the fish and the water temperature. As with any data compilation, it is important to recognize that factors such as sampling method and sampling time can significantly affect baseline physiology. McDonald and Milligan (1992) discuss some of these general issues and provide an excellent review of the chemical properties of the blood of fish (mainly salmonids). From Table 8.1, it is interesting to note that most of the baseline physiological data exist for only a few of the 32 species of centrarchid fishes. In fact, for more than 20 of the centrarchid species, there is simply no published physiological data at all. As noted for other species of fish [e.g., rainbow trout, Kieffer et al . (1998); tilapia, Oreochromis niliticus, Alsop et al . (1999); sockeye salmon, Oncorhynchus nerka and coho salmon, Oncorhynchus kisutch, Lee et al . (2003a)], temperature strongly affects baseline oxygen consumption rates in various centrarchids (see Figure 8.1a). In addition to these temperature related effects, there are differences in oxygen consumption rates between species of centrarchids (Figure 8.1a). From the available data, bluegill (L. macrochirus) and longear sunfish (Lepomis megalotis) appear to have higher resting metabolic rates across temperatures relative to largemouth bass and pumpkinseed sunfish (Lepomis gibbosus). Whether this variation represents true species differences or is the result of different methodologies is not certain. However, there are clear differences in routine oxygen consumption rates across temperatures among different stocks of largemouth bass (Cooke et al . 2001a; see Figure 8.1b). These intraspecific findings have also been noted for Arctic charr (Salvelinus alpinus) (Giles 1991). Overall, the values noted for centrarchids are in line with those of other species, such as sockeye and coho salmon (Brett 1995; Lee et al . 2003a) and brown trout (Salmo trutta) (Sloman et al . 2000). In addition to temperature, baseline oxygen consumption rates are also significantly influenced by the levels of oxygen in the water (Cech et al . 1979; Figure 8.1c). These effects are particularly noticeable at higher (i.e. 30◦ C) temperatures (Figure 8.1c). Cech et al . (1979) discuss these findings with respect to oxygen levels required for largemouth bass (see Section 8.4.4 on hypoxia for more detail). Ventilation rates are variable among centrarchid species (26–75 beats min−1 ; Table 8.1). It appears that this variation is largely related to body size and water temperature. However, these rates are consistent with ventilation rates noted for other species of fish, including shortnose (Acipenser brevirostrum) and Atlantic (Acipenser oxyrhinchus oxyrhinchus) sturgeon (Baker et al . 2005) and rainbow trout (Oncorhynchus mykiss; Bindon et al . 1994). Blood hemoglobin and hematocrit (Hct) are within the normal ranges for other fishes (Table 8.1; reviewed in Gallaugher and Farrell 1998), suggesting that centrarchids have adequate oxygen transport capacities. Resting ion levels (Na+, K+, Cl− ) and osmolality (a measure of the total concentration of ions in the blood) are within the ranges noted for other freshwater fishes (McDonald and Milligan 1992) and are probably sensitive to a wide variety of abiotic (e.g., salinity, pollutants) and biotic (e.g., stress) influences (see Section 8.4). Of all the muscle and blood variables noted in Table 8.1, the greatest difference between centrarchids and other species is the muscle lactate dehydrogenase (LDH) concentration. This enzyme is important in the conversion of pyruvate to lactate during anaerobic metabolism. Overall, centrarchids have relatively low levels of LDH in their muscle relative to Atlantic salmon (Salmo salar) (McDonald et al .1998) and sea lamprey (Petromyzon marinus) (Boutilier et al . 1993, Wilkie et al . 2001). This lower LDH level (∼ one-fifth to one-tenth of the levels of Atlantic salmon and sea lamprey, depending on the temperature) would imply that the anaerobic capacity of centrarchids is significantly lower compared to other species. Indeed, this is the case as centrarchids generally produce less lactate than other species of fish following certain stress (e.g., exhaustive exercise, hypoxia; see Table 8.2).

8.3 Physiological challenges/tolerances 8.3.1 Swimming capacity For various practical and physiological reasons, most of the research on the swimming capacity in fish has focused on salmonids (Brett 1964, Davison 1989). Levels of swimming performance in fish are traditionally defined in terms of duration of swimming (Beamish 1978) and whether the exercise depends on the presence of oxygen (i.e. aerobic

Physiology and organismal performance of centrarchids

209

Table 8.1 Baseline physiological variables of various centrarchid fish species. Physiological variable and species Oxygen consumption Pumpkinseed

Pumpkinseed

Bluegill

Smallmouth bass

Variable specific units −1

mg kg

hr

Banded sunfish Longear sunfish

White crappie

Source

−1

8

100 g

Evans 1984

45

16

100 g

Evans 1984

45

20

45 g

Brett and Sutherland 1965

70

24

100 g

Evans 1984

81

28

100 g

Evans 1984

117

32

100 g

Evans 1984

∼40

15

MA Population

∼43

15

NC Population

Roberts 1967

∼70

25

MA Population

Roberts 1967

Roberts 1967

∼90

25

NC Population

Roberts 1967

111.9

10

9.74 cm (31 g)

Dent and Lutterschmidt 2003

143.6

20

10.3 cm (36 g)

100

25

118 g

223.4

30

9.83 cm (31 g)

86.7

–

32 cm

74.7 nmol g

Green sunfish

Size of fish (various units)

30

−1

Largemouth bass

Water temperature (◦ C)

min

−1

26.6

Dent and Lutterschmidt 2003 Marvin and Heath 1968 Dent and Lutterschmidt 2003 S. Peake, unpublished data

18

15 g

5

6–10 g/8.3–9.7 cm

Johnson and Charlton 1960

Gonzalez and McDonald 1994

91

12

6–10 g/8.3–9.7 cm

Johnson and Charlton 1960

93.8

17

6–10 g/8.3–9.7 cm

Johnson and Charlton 1960

129.5

22

6–10 g/8.3–9.7 cm

Johnson and Charlton 1960

224

29

6–10 g/8.3–9.7 cm

Johnson and Charlton 1960

∼78

10

150 g/22.5 cm

Beamish 1970

∼95

15

150 g/22.5 cm

Beamish 1970

∼110

20

150 g/22.5 cm

Beamish 1970

∼125

25

150 g/22.5 cm

Beamish 1970

∼150

30

150 g/22.5 cm

Beamish 1970

∼160

34

150 g/22.5 cm

67.7

20

230–470 g

Cech et al. 1979

102.9

25

230–470 g

Cech et al. 1979

173.2

30

230–470 g

Cech et al. 1979

130

15

4.9–15.8 g

41.3 nmol g−1 min−1

18

–

Beamish 1970

Horkel and Pearson 1976 Gonzalez and McDonald 1994

126.7

10

8.9 cm (22 g)

Dent and Lutterschmidt 2003

169.2

20

9.44 cm (30 g)

Dent and Lutterschmidt 2003

187.7

30

9.36 cm (25 g)

Dent and Lutterschmidt 2003

121.5

25

∼90 g

Parsons and Sylvester 1992 (continued)

210

Centrarchid fishes

Table 8.1 (continued). Physiological variable and species Ventilation rate Green sunfish Largemouth bass Smallmouth bass Bluegill Pumpkinseed

Variable specific units vents min

−1

Water temperature (◦ C)

Size of fish (various units)

Source

–

–

26

15

6–10.5 cm/5–16 g

∼65

20

422 g

∼120

20–22

16–20 cm

∼75

20

389 g

Furimsky et al. 2003

70

25

118 g

Marvin and Heath 1968

∼40

15

MA Population

Horkel and Pearson 1976 Furimsky et al. 2003 C. Suski, unpublished data

Roberts 1967

∼25

15

NC Population

Roberts 1967

∼50

25

MA Population

Roberts 1967 Roberts 1967

∼52

25

NC Population

G dl−1

–

–

Bluegill

9.07

20–22

∼33 g

Heath 1991

Largemouth bass

8.1

–

115 g

Black 1955

6.2

–

1–4 yr

5.72–7.87

over seasons

–

White crappie

6.1

22

7.5 cm

Rock bass

5.85

–

–

7

9

14.2–18.4 cm

Bidwell and Heath 1993 Bidwell and Heath 1993

Hemoglobin

Redear sunfish

6.5 Hematocrit (%) Bluegill

Smallmouth bass

Largemouth bass

7

14.2–18.4 cm

–

–

Clark et al. 1979 Atkinson and Judd 1978 Parsons 1993 Coburn 1970 in Atkinson and Judd 1978

30%

23

–

Musselman et al. 1995

35%

–

–

Coburn 1970 in Atkinson and Judd 1978

37%

20

5–7 cm

Lemly 1993

25%

–

32 cm

S. Peake, unpublished data

19.20%

20

–

Furimsky et al. 2003

33%

12, 16, and 20

–

J. Schreer, unpublished data

35%

–

1–4 yr

16.70%

20

–

Furimsky et al. 2003

∼40%

over seasons

–

Atkinson and Judd 1978

31%

–

–

Coburn 1970 in Atkinson and Judd 1978

27%

22

7.5 cm

Black crappie

23%

–

–

Coburn 1970 in Atkinson and Judd 1978

Rock bass

30%

–

–

Coburn 1970 in Atkinson and Judd 1978

Redear sunfish White crappie

Clark et al. 1979

Parsons 1993

35%

9

14.2–18.4 cm

Bidwell and Heath 1993

32%

7

14.2–18.4 cm

Bidwell and Heath 1993 (continued)

Physiology and organismal performance of centrarchids

211

Table 8.1 (continued). Physiological variable and species Plasma sodium

Variable specific units

Size of fish (various units)

Source

–

–

Bluegill

∼144

20–22

∼33 g

Heath 1991

Smallmouth bass

∼173

22

25 cm

Carmichael et al. 1983

149

12, 16, and 20

–

J. Schreer, unpublished data

Largemouth bass

125

–

–

Suski et al. 2003

Plasma chloride

mequiv l−1

–

–

∼110

20–22

∼33 g

112

22

25 cm

101

12, 16, and 20

–

Bluegill Smallmouth bass Largemouth bass

mequiv l

−1

Water temperature (◦ C)

∼100

–

–

101–115

–

150 g

Heath 1991 Carmichael et al. 1983 J. Schreer, unpublished data Suski et al. 2003 Williamson and Carmichael 1986

106

23

13–23 cm

mequiv l−1

–

–

Bluegill

∼5.5

20–22

∼33 g

Smallmouth bass

∼2.5

22

25 cm

2.99

12, 16, and 20

–

J. Schreer, unpublished data

∼2.5

–

–

Suski et al. 2003

MOsm

–

–

Plasma potassium

Largemouth bass Plasma osmolarity Rockbass

Carmichael et al. 1984a Heath 1991 Carmichael et al. 1983

325

9

14.2–18.4 cm

Bidwell and Heath 1993

∼280

7

14.2–18.4 cm

Bidwell and Heath 1993

293

–

3.2 g

McCormick et al. 1989

Bluegill

∼300

23

–

Musselman et al. 1995

Largemouth bass

∼300

22–24

33 cm

286

23

5–6 cm

294

23

13–23 cm

g dl−1

–

–

Black crappie

Plasma protein Rock bass

Suski et al. 2004 Susanto and Peterson 1996 Carmichael et al. 1984a

6

9

14.2–18.4 cm

∼5.5

7

14.2–18.4 cm

Largemouth bass

7

–

1–4 yr

Clark et al. 1979

6.97

–

51–2382 g

Clark et al. 1979

Plasma glucose

mg dl−1

–

–

Largemouth bass

Smallmouth bass

100

–

–

161.2

–

1–4 yr

53

23

13–23 cm

68–74

–

150 g

157.8

N/A

51–2382 g

∼90

22

25 cm

48

12, 16, and 20

–

Bidwell and Heath 1993 Bidwell and Heath 1993

´ Sepulveda et al. 2004 Clark et al. 1979 Carmichael et al. 1984a Williamson and Carmichael 1986 Clark et al. 1979 Carmichael et al. 1983 J. Schreer, unpublished data (continued)

212

Centrarchid fishes

Table 8.1 (continued). Physiological variable and species

Variable specific units

Water temperature (◦ C)

Size of fish (various units)

Bluegill sunfish

∼50

20–22

∼33 g

Rockbass

∼50

9

14.2–18.4 cm

Bidwell and Heath 1993

∼50

7

14.2–18.4 cm

Bidwell and Heath 1993

Source Heath 1991

Muscle cytochrome oxidase

umol min−1 g−1

White crappie

∼5

5

–

Tschantz et al. 2002

∼8

25

–

Tschantz et al. 2002

Black crappie

∼35

25

–

Tschantz et al. 2002

Bluegill sunfish

∼3

5

–

Tschantz et al. 2002

∼1

25

–

Tschantz et al. 2002

∼2

5

–

Tschantz et al. 2002

∼4

25

–

Tschantz et al. 2002

∼2

5

–

Tschantz et al. 2002

∼2

25

–

Tschantz et al. 2002

Green sunfish Largemouth bass Muscle lactate dehydrogenase White crappie Black crappie Bluegill sunfish Green sunfish Largemouth bass

umol min−1 g−1 ∼30

5

–

Tschantz et al. 2002

∼75

25

–

Tschantz et al. 2002

∼25

5

–

Tschantz et al. 2002

∼100

25

–

Tschantz et al. 2002

∼25

5

–

Tschantz et al. 2002

∼40

25

–

Tschantz et al. 2002

∼38

5

–

Tschantz et al. 2002

∼80

25

–

Tschantz et al. 2002

∼38

5

–

Tschantz et al. 2002

∼100

25

–

Tschantz et al. 2002

Muscle phosphocreatine PCr

umol g−1

Largemouth bass

∼3

–

–

∼15

22–24

33 cm

Suski et al. 2005

Smallmouth bass Muscle ATP Largemouth bass

Smallmouth bass

Dehn and Schirf 1986

∼16

–

–

Suski et al. 2003

∼15

16

32 cm

Kieffer et al. 1995

−1

umol g ∼4

–

–

∼7

22–24

33 cm

Suski et al. 2005

∼7

–

–

Suski et al. 2003

∼6

16

32 cm

Kieffer et al. 1995

Dehn and Schirf 1986

(continued)

Physiology and organismal performance of centrarchids

213

Table 8.1 (continued). Physiological variable and species Plasma cortisol Largemouth bass

Plasma adrenaline

Variable specific units ng ml

Water temperature (◦ C)

Size of fish (various units)

Source

−1

16

21

–

Davis and Parker 1986

∼20

–

–

Suski et al. 2003

∼50

22–24

33 cm

Suski et al. 2005

nmol l−1

Largemouth bass

1

20

–

Furimsky et al. 2003

Smallmouth bass

∼1

20

–

Furimsky et al. 2003

Plasma noradrenaline

nmol l

−1

Largemouth bass

∼6

20

–

Furimsky et al. 2003

Smallmouth bass

∼2

20

–

Furimsky et al. 2003

Note: Values may be estimated.

versus anaerobic). Researchers have categorized swimming in fish into three broad categories: sustained, prolonged, and burst-type swimming (see Brett 1964; Beamish 1978; Hammer 1995; Plaut 2001, for details). Sustained exercise is powered exclusively by aerobic metabolism and, in fish, this type of exercise is referred to as cruising. Sustained swimming performance includes those speeds that can be maintained for long periods of time (typically greater than 200 min) without resulting in muscular fatigue (Beamish 1978). Prolonged exercise can last between 2 and 200 minutes and, depending on the swimming speed, is terminated by exhaustion. A third type of exercise, intense burst activity, relies almost exclusively on anaerobic metabolism within the white muscle and can only be maintained for short periods of time (typically less than 20 s). This type of exercise results in a significant reduction of intracellular energy supplies or by the accumulation of waste products (Kieffer 2000).

8.3.2 Tests to measure swimming performance in fish (methodological approaches) Different methods have been developed to quantify exercise performance in fish. Common laboratory tests include: (i) fixed velocity (fatigue) tests and (ii) increased (incremental) velocity tests (Brett 1964; Beamish 1978; Hammer 1995, for a review). Fixed velocity tests involve placing fish in a swim tunnel (or long raceway) and after an adjustment period, swimming speed is increased (steadily, in small steps, or abruptly) until the test velocity is achieved, after which the velocity is constant. At this point, time to swimming failure at the test speed is measured. An increased velocity test (also known as the UCrit, or the critical velocity test; Brett 1964) involves forcing fish against a known current. Unlike that of the fixed velocity tests, fish are exposed to increasing velocity increments (e.g., 10 cm s−1 ) and duration (ranges from 5 to 60 min; see Farlinger and Beamish 1977) until exhaustion is reached (see Brett 1964; Farlinger and Beamish 1977; Beamish 1978; Hammer 1995; Kolok 1999, for details and methodological considerations). Much of the earlier work on swimming in centrarchids has been documented in an excellent review by Beamish (1978). Recent research on swimming performance in centrarchids has focused on critical swimming capacity and fixed velocity performance. Some research has also focused on the metabolic costs (i.e. oxygen consumption) associated with swimming (see later).

8.3.3 Critical swimming (UCrit) performance Critical swimming speeds [UCrit, typically measured as body lengths (BLs) per second, BL s−1 ] for many species of centrarchid fish, such as largemouth bass, smallmouth bass (Micropterus dolomieu), pumpkinseed sunfish, bluegill sunfish

214

Centrarchid fishes

(a)

250 200 150 100 50 0 0

5

10

15

20

25

30

35

Oxygen consumption (mg O2 Kg−1 h−1)

Temperature (°C) (b)

200 160 120 80 40 0

6

12

18

Temperature (°C) (c)

160

30°C

120 25°C 80 20°C 40 0 30

40

50 60 70 80 90 100 110 120 130 140 150 160 Partial pressure of oxygen in water (mmHg)

Figure 8.1 (a) Baseline metabolic rates of various centrarchids as a function of water temperature. Closed circles represent longear sunfish (Dent and Lutterschmidt 2003), closed squares represent bluegill sunfish (Marvin and Heath 1968; Dent and Lutterschmidt 2003), open triangles represent largemouth bass (Johnson and Charlton 1960), open circles represent largemouth bass (Beamish 1964) and closed diamonds represent pumpkinseed sunfish (Brett and Sutherland 1965; Evans 1984). (b) Effects of water temperature and stock on the baseline oxygen consumption rates of largemouth bass. Closed squares represent central Illinois pure stock (IL), closed triangles represent southeastern Wisconsin stock (WI), closed circles represent WI × IL stock and open squares represent IL × WI stock (see Cooke et al . 2001a, for details). (c) Effects of ambient oxygen concentrations on the baseline metabolic rates in largemouth bass at 20◦ C (closed circles), 25◦ C (closed triangles), and 30◦ C (closed squares). (Redrawn from Cech et al . 1979. American Fisheries Society.)

and white crappie (Pomoxis annularis) exist. The published results for critical swimming speeds show that considerable variation exists within the Centrarchidae (see Table 8.3). For example, values for UCrit typically range from between 2 and 3.5 BL s−1 for smallmouth bass (McDonald et al . 1991; Cooke and Bunt 2001; Peake 2004, but see Larimore and Duever 1968 for work on juveniles), about 3 BL s−1 for bluegill (Kelsch 1996), 2 BL s−1 for white crappie (Parsons and Smiley 2003), 3 BL s−1 for pumpkinseeds (Brett and Sutherland 1965) and as high as 3.5–8 BL s−1 for largemouth bass (Dahlberg et al . 1968; Hocutt 1973; Farlinger and Beamish 1977; Farlinger and Beamish 1978, but see Ostrand et al .

Physiology and organismal performance of centrarchids

215

Table 8.2 Maximum muscle lactate concentrations (umol g−1 wet tissue) following exhaustive exercise stress in various centrarchid and noncentrarchid species of fish. Species

Muscle lactate (umol g−1 wet tissue)

Largemouth bass (adult) Smallmouth bass (adult) Rainbow trout (adult)

Source

∼20

Kieffer et al. 1996

∼15

Suski et al. 2004

∼18

Kieffer et al. 1995a

∼30

Peake and Farrell 2004

41

Schulte et al. 1992

∼30

Kieffer et al. 1994

Coho salmon

∼45

Farrell et al. 2001b

Atlantic salmon (adult)

∼45

Wilkie et al. 1996

Brook charr (adult)

∼33

Kieffer et al. 1996

Sea lamprey (adult)

∼25

Boutilier et al. 1993

Yellow perch

∼24

Schwalme and Mackay 1991

Atlantic sturgeon (juvenile)

∼6

Kieffer et al. 2001

a indicates post-angling lactate levels. b indicates lactate levels following capture by commercial fishers.

2005, for exceptions on juveniles). Critical swimming speeds of centrarchids are similar to those for other freshwater and marine fish species, including: brown trout (UCrit ∼1.8; Altimiras et al . 2002), rainbow trout (UCrit ∼3.0; Kieffer et al . 1998; UCrit ∼1.5; Jain and Farrell 2003), common snook (Centropomus undecimalis; UCrit ∼2.2–8.9 BL s−1 , depending on size; Tolley and Torres 2002), cut-throat trout (Oncorhynchus clarki clarki ; UCrit ∼4; MacNutt et al . 2004), coho salmon (UCrit 1.5–2.5; Lee et al . 2003a), and walleye (Sander vitreus; UCrit ∼0.8–1.2; Peake et al . 2000). Although differences in UCrit values between centrarchid species may reflect differences in the methodology(ies) used to determine critical swimming speeds (e.g., size of fish, time increments for testing; Farlinger and Beamish 1977; Peake et al . 2000), it is highly possible that the variability in these values reflects various abiotic and biotic factors (see Section 8.3.4) or differences in life history and ecology of the various centrarchid species (see Chapter 13).

8.3.4 Effects of abiotic factors on UCrit 8.3.4.1 Temperature effects The effects of temperature on swimming performance in fish are well known (Brett 1964; Hocutt 1973; Randall and Brauner 1991; Keen and Farrell 1994; Kieffer et al . 1998; Myrick and Cech 2000; Cooke et al . 2001a; Lee et al . 2003a,b; MacNutt et al . 2004; O’Steen and Bennett 2003). In general, increases in temperature to an optimum improve swimming performance by enhancing biochemical rates (Franklin 1998), skeletal muscle contractility (Rome et al . 1990), and cardiac performance (Kolok and Farrell 1994a,b). In an early study by Larimore and Duever (1968), groups of smallmouth bass fry were acclimated to water temperatures ranging from 5 to 35◦ C. The maximum swimming speed for fish acclimated to a particular temperature increased with successively higher test temperatures until 30◦ C (see Figure 8.2), with fry acclimated to 30◦ C achieving a maximum swimming speed twice that of fry acclimated to 5◦ C. These authors also acutely challenged acclimated animals to different temperatures (i.e. 5◦ C acclimated fish tested at 10, 15, and 20◦ C) and found that critical swimming speeds also increased with increases in temperature, but the range of performance changed in comparison in the response of acclimated fish. For example, only fish acclimated to 5 or 10◦ C performed well at 5◦ C and only fish conditioned to 35◦ C performed well at 35◦ C. Hocutt (1973) measured the swimming performance of largemouth bass exposed to a rapid temperature change (temperature range: 15–35◦ C) and also noted positive correlations between increasing temperature and swimming performance.

216

Centrarchid fishes

Table 8.3 Critical swimming (UCrit) values for various species of centrarchids. Species

Size (length/mass)

Temperature (◦ C)

UCrit (cm s−1 )

UCrit (Bl s−1 )

Source

13.5–17.5 cm

13

–

∼2.4

Kelsch 1996

13.5–17.5 cm

25

–

∼3

Kelsch 1996

13.5–17.5 cm

30

–

∼2.8

Kelsch 1996

Pumpkinseed

12.7 cm

20

–

3.01

Brett and Sutherland 1965

White crappie

16.5–17.5 cm

25

34.7

–

8.01 cm

5

6.16

0.76

Smiley and Parsons 1997c

7.63 cm

15

13.59

1.78

Smiley and Parsons 1997c

8.00 cm

25

13.86

1.73

Smiley and Parsons 1997c

Bluegill

Largemouth bass

Parsons and Sylvester 1992

5–10 cm

5–7

∼10

–

Parsons and Smiley 2003

5–10 cm

15–18

∼16

–

Parsons and Smiley 2003

5–10 cm

24–27

∼20

–

Parsons and Smiley 2003

10–15 cm

5–7

∼11

–

Parsons and Smiley 2003

10–15 cm

15–18

∼20

–

Parsons and Smiley 2003

10–15 cm

24–27

∼28

–

Parsons and Smiley 2003

15–20 cm

5–7

∼10

–

Parsons and Smiley 2003

15–20 cm

15–18

∼15

–

Parsons and Smiley 2003

15–20 cm

24–27

∼30

–

Parsons and Smiley 2003

20–25 cm

5–7

∼15

–

Parsons and Smiley 2003

20–25 cm

15–18

∼20

–

Parsons and Smiley 2003

20–25 cm

24–27

∼30

–

Parsons and Smiley 2003

25–30 cm

5–7

∼15

–

Parsons and Smiley 2003

25–30 cm

15–18

∼20

–

Parsons and Smiley 2003

25–30 cm

24–27

∼25

–

Parsons and Smiley 2003

9.3–12.8 cm 9.3–12.8 cm

5 5

– –

∼2.2 ∼1.7

Kolok 1991d Kolok 1991e

9.3–12.8 cm

5

–

∼1.5

Kolok 1991f

9.3–12.8 cm

10

–

∼2.9

Kolok 1991g

9.3–12.8 cm

10

–

∼2.8

Kolok 1991h

9.3–12.8 cm

10

–

∼2.3

Kolok 1991i

10.1 cm

5

20

1.98

Kolok 1992

9.7 cm

20

35.7

3.68

Kolok 1992

15.9 cm

6

30.1

1.90

Cooke et al. 2001a

17.0 cm

12

34.6

2.06

Cooke et al. 2001a

16.6 cm

18

35.2

2.01

Cooke et al. 2001a

8.6 cm

20

∼60–70

∼7.2–8.4

Ostrand et al. 2004a

12.2 cm

25

41.63

3.41

10.4 cm

25

–

∼3.5

Farlinger and Beamish 1978 Farlinger and Beamish 1978

5.2–6.4 cm

30

29.81

8.08

Hocutt 1973 (continued)

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217

Table 8.3 (continued). Species Smallmouth bass

Size (length/mass)

Temperature (◦ C)

UCrit (cm s−1 )

UCrit (Bl s−1 )

2.2 cm 2.2 cm

5 10

– –

2.2 4.7

Larimore and Duever 1968b Larimore and Duever 1968b

2.2 cm

15

–

6.8

Larimore and Duever 1968b

2.2 cm

20

–

10.2

Larimore and Duever 1968b

2.2 cm

25

–

11.8

Larimore and Duever 1968b

2.2 cm

30

–

13.6

Larimore and Duever 1968b

2.2 cm

35

–

11.5

Larimore and Duever 1968b

Source

10.1 g

16

–

2.0

McDonald et al. 1991

∼30 cm

–

83.75

2.79

S. Peake, unpublished data

31.0 cm

17

111.3

3.59

26.2–37.8 cm

15–20

50–118

–

Bunt et al. 1999

42.1–48.9 cm

20–24

47–69

–

Bunt 1999

Cooke and Bunt 2001

a Values depend on diet. See Ostrand et al. (2005), for details. b Fry were swum in groups of 20. c Fish held under 12:12 (L:D) photoperiod. See Smiley and Parsons (1997) for additional details and UCrit values. d Winter acclimatized (5◦ C) fish. ◦ e

Laboratory acclimated to 5 C, photoperiod 9:15 L:D.

f Laboratory acclimated to 5◦ C, photoperiod 12:12 L:D. g Spring acclimatized (10◦ C) fish. h Laboratory acclimated to 10◦ C, photoperiod 9:15 L:D. ◦ i

Laboratory acclimated to 10 C, photoperiod 12:12 L:D.

Smallmouth bass

16 UCrit (cm s −1)

14 12 10 8 6 4 2 0 5

10

15

20

25

30

35

Temperature (°C) Figure 8.2 Mean critical swimming speed of groups of smallmouth bass fry acclimated to various temperatures (data from Larimore and Duever 1968. American Fisheries Society).

Parsons and Smiley (2003) measured critical swimming speeds in white crappie that were seasonally acclimatized to winter (5–7◦ C), spring (15–18◦ C), and summer (24–27◦ C) temperatures. These authors noted the typical pattern that UCrit values increased in fish at the higher temperatures (see earlier and Figure 8.2). They also documented that the highest number of nonperforming fish (those with UCrits <5 cm s−1 ) was observed among the winter-acclimatized fish. Parsons and Smiley (2003) also examined the effect of rapidly decreasing temperature (either 15◦ C-acclimated fish tested at 5◦ C or 25◦ C-acclimated fish tested at 15◦ C) and found that UCrit values were significantly altered. For example, warm-acclimated

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Centrarchid fishes

(25◦ C) fish exposed to 15◦ C had significantly decreased swimming performance compared to 25◦ C-acclimatized fish. These trends were similar to those noted for yellow perch (Otto and Rice 1974) and coho salmon (Griffiths and Alderdice 1972). The UCrit of 15◦ C-acclimated fish acutely exposed to 5◦ C, however, were not different when compared to 15◦ C-acclimated fish. Lastly, Parsons and Smiley (2003) found that there was no difference in UCrit values of white crappie measured during the day and night for any of the three temperature groups. The trend of decreasing swimming performance with decreasing water temperatures has also been documented for subadult largemouth bass (Beamish 1970; Kolok 1991, 1992; Cooke et al . 2001a) of various stocks (Cooke et al . 2001a). For largemouth bass, these findings are not surprising because it has been noted that as water temperatures approach 5◦ C, largemouth bass often become quiescent (Lemons and Crawshaw 1985; Kolok 1992). Taken together, the effects of temperature on the UCrit values of centrarchids are apparent, and these results clearly support the idea of temperature being a “controlling variable” for swimming performance in fish (i.e. Fry 1947). Temperature may also explain the large intraspecific variability in the UCrit values for a given centrarchid species (see Table 8.3). Thus, to make UCrit values comparable between studies, abiotic factors such as temperature have to be controlled or at least documented within the study.

8.3.4.2 Photoperiod effects It has long been argued that when measuring whole animal processes (i.e. swimming performance), it is important to recognize the importance of other environmental factors (Kolok 1991). For example, and as noted earlier, temperature has an enormous impact on the swimming performance of many fish species. However, other variables, such as photoperiod, may confound results, especially if researchers are using wild fish in laboratory studies. Kolok (1991) carried out landmark experiments to test the effects of prolonged exposure to photoperiods on the UCrit of largemouth bass. These experiments were repeated at 5, 10, 15, or 19◦ C. Photoperiod [either 12:12, light:dark (L:D) or 9:15, light:dark] had significant effects on UCrit of bass at 5 and 10◦ C, but not at 15 or 19◦ C (see Kolok 1991, for details). More specifically, in early winter, largemouth bass acclimated to 5◦ C and to 12:12 (L:D) had reduced performance compared to field-acclimatized fish at 5◦ C. A similar trend was noted for bass acclimated to and tested at 10◦ C. Kolok (1991) concluded that photoperiod may bias UCrit measurements in fish acclimated to colder temperatures, but this bias does not affect fish held at warmer temperatures (see Kolok 1991 for additional details). In a more recent study, Smiley and Parsons (1997) acclimated white crappie to one of five photoperiods, ranging from 24-hour light to 24-hour dark (see Figure 8.3), and determined the effect of these photoperiod regimes on UCrit. At the three temperatures tested (5, 15, and 25◦ C), the highest mean swimming performance occurred with the 8L:16D photoperiod, regardless of temperature (Figure 8.3). When swimming speeds for all photoperiod treatments were combined, fish tested at the coldest temperature swam significantly slower than fish tested at either 15 or 25◦ C. It should be noted that

30

Ucrit (cm s −1)

25 20 15

15°C

10

25°C

5

5°C

0 24:0

16:8

12:12

8:16

0:24

Photoperiod (L:D) Figure 8.3 Mean critical swimming speed of white crappie at various photoperiods and temperatures (5◦ C, closed circles; 15◦ C, closed squares; 25◦ C, closed triangles). [Data from Smiley and Parsons (1997). American Fisheries Society.]

Physiology and organismal performance of centrarchids

219

no combined effect of photoperiod and temperature occurred in the study by Smiley and Parsons (1997). The results of this study and that of Kolok (1991) indicate that photoperiod is an important determinant of the swimming performance of fish, and that species differences in the response may exist. Future studies should address the importance, if any, of the potential interactive effects between temperature and photoperiod.

8.3.4.3 Oxygen effects Relative to that of temperature and photoperiod, less is known about the effects of oxygen on the critical swimming ability of fish in general (Dahlberg et al . 1968). With respect to centrarchids, even less is known about the impacts of oxygen and/or carbon dioxide levels on exercise performance. Swimming speed decreased significantly with a reduction of dissolved oxygen below 5 or 6 mg l−1 in largemouth bass (Dahlberg et al . 1968). At oxygen levels above 6 mg l−1 , performance of bass was independent of oxygen concentration. Although these results suggest that largemouth bass are highly tolerant to low oxygen levels (see Section 8.4.4 on hypoxia), more work is required to determine the effects of hypoxia on swimming performance in other species of centrarchids.

8.3.5 Biotic effects on swimming performance 8.3.5.1 Body size effects In general, relative performance at critical swimming speeds favors the smaller individuals of a species (Beamish 1978; Peake et al . 2000). For smallmouth bass, Larimore and Duever (1968) found that fry (2.5 cm) had a UCrit of about 6.8 BL s−1 (at 15◦ C) whereas McDonald et al . (1991) found this value to be about 2 BL s−1 (for 12-cm fish). A similar pattern was noted by Parsons and Smiley (2003) for summer acclimatized white crappie, where small fish (5–10 cm) had UCrits of about 2–4 BL s−1 compared to UCrits of about 1.5 BL s−1 for larger fish (20–25 cm). These studies demonstrate that size influences swimming performance, but they do not illustrate whether this relationship is linear or nonlinear. Nor can they predict the metabolic cost of fish swimming at these speeds. To effectively answer this question, researchers need to carry out studies on various sizes of fish [as in Peake et al . (2000), for walleye]. This may be methodologically challenging to get extremely small fish (<1 cm, for example) to swim in a flume for the time required to get accurate UCrit measurements.

8.3.5.2 Training effects It has been known for decades that physical conditioning impacts many physiological processes, including swimming in fish (Davison 1997; Kieffer 2000). Most studies on training in fish have been carried out on salmonids (see Davison 1997). The literature on the effects of training on swimming performance is generally lacking for centrarchids (MacLeod 1967; Beamish 1970; Farlinger and Beamish 1978). Of the few published works, studies have focused on the maximum swimming performance in largemouth bass. Farlinger and Beamish (1978) provide additional details of the changes in blood chemistry that may accompany the critical swimming speed. These authors noted a significant impact of a 30-day training regime on UCrit values (values for trained fish were about 15% higher than untrained bass). Hemoglobin levels increased significantly with conditioning, suggesting an increased aerobic capacity. Farlinger and Beamish (1978) also measured levels of LDH. Conditioning of largemouth bass did not lead to an enhanced production of LDH; whether or not conditioning affects metabolic recovery from exercise in bass is not known, but it has been shown in rainbow trout (Pearson et al . 1990). Using an open-topped oval channel, MacLeod (1967) showed that fingerling largemouth bass showed a marked increase in maximum swimming speeds after 3 days of training. Swimming performance was not significantly affected by feeding status (i.e. being fed or not). The impact of training on physiological aspects of swimming in fish is highly variable (Kieffer 2000). Thus, it is not entirely clear how training affected largemouth bass swimming. It is possible that conditioned fish may have more hemoglobin (citing Hochachka 1961) or could tolerate higher levels of lactate following exercise (citing Hammond and Hickman 1966). Overall, the impact of training on swimming capacity needs to be addressed in all fish species, including centrarchids.

220

Centrarchid fishes

8.3.5.3 Feeding status/food type The ability of fish to exercise is affected by the amount of on-board energy reserves (Scarabello et al . 1991; Kieffer 2000). Ostrand et al . (2005) conducted a large-scale experiment that investigated the effects of common over-wintering prey assemblages [either natural invertebrate forage, fathead minnows (Pimephales promelas) and natural invertebrate forage, and bluegill and nature invertebrate forage] on fish condition and swimming ability (i.e. UCrit) of largemouth bass. The hypothesis tested was that fish that emerge from the winter in better condition may have an enhanced UCrit, which could affect their ability to evade predators. Each pond (three for each diet) was stocked with small age-0 largemouth bass in the fall and the fish were allowed to forage under these conditions from late fall until early April. At that time, condition factor and mortality rates were determined (no differences between diet groups were noted). A subsample of smaller fish from each diet regime was exposed to UCrit swimming challenges (see Ostrand et al . 2005 for details). Overall, there were significant effects of prey treatment on UCrit. Fish that were fed only invertebrates had the highest UCrit (∼8.4 BL s−1 ), whereas the fish that were fed bluegill and natural invertebrates had the lowest UCrit (∼7.2 BL s−1 ). These authors provide several explanations for why this relationship exists, such as the effects of differing protein levels and fatty acid compositions on swimming performance (e.g., Beamish et al . 1989; McKenzie et al . 1998).

8.3.5.4 Individual differences The underlying mechanisms for differences in swimming capacity of centrarchid species are lacking. Even less information is available to address the enormous variability of responses within individual fish (i.e. individual variation) in centrarchids. To address the importance of individual variation of swimming performance in fish, Kolok (1992) addressed the possible relationship(s) between morphology and physiological performance of largemouth bass (see Kolok 1999 for a review on this subject). He measured many physiological (e.g., liver glycogen and LDH activity) and morphological (e.g., length, mass, gill filament density and lamellar density) traits of each fish and conducted correlations among these traits. His experiments showed that seasonality (winter versus summer) influenced these traits, and the performance of winter-acclimatized fish was influenced more significantly by the morphological and physiological traits compared with the warm-acclimatized bass. Additional information on the importance of inter-individual variation on swimming performance of other species is reviewed in Kolok (1999).

8.3.6 Endurance swimming performance Although not as prevalent as studies on prolonged swimming, a body of literature on endurance (sustained) swimming exists for many centrarchid species (see Beamish 1978 for a detailed review of the early literature). Studies on endurance swimming, however, can be difficult to interpret because researchers have examined either maximum swimming speeds (MacLeod 1967; Dahlberg et al . 1968), time to exhaustion at lower speeds (Parsons and Sylvester 1992; Schaefer et al . 1999), or the amount of time swimming and spontaneous swimming (Tschantz et al . 2002). Other authors have assessed the kinematics of swimming (Gibb et al . 1994; Jayne and Lauder 1995a,b; Drucker et al . 2006), properties of locomotion (Jayne and Lauder 1994; Lauder 2005), acceleration performance (e.g., Webb 1975), or power output during swimming (Coughlin 2000, 2002) in centrarchids. In addition, only a few studies have measured the metabolic cost (e.g., oxygen consumption rates) of swimming in centrarchids. Although we are aware of these limitations, we have combined all the available studies on endurance swimming in an attempt to provide information and some general conclusions.

8.3.7 Metabolic costs of swimming: interspecific differences Because of the technical considerations of measuring swimming performance and metabolic costs (i.e. oxygen consumption) in fish, there are few studies for centrarchids, compared to the broad literature base for salmonids (Brett 1964; Kieffer et al . 1998; see Brett 1995 for review), that have examined the swimming efficiency and metabolic costs. The results

Oxygen consumption rate (mg O2 kg−1 h−1)

Physiology and organismal performance of centrarchids

221

600 400 200 0 0

30

60

swimming speed (cm −1

90 s−1)

−1

Figure 8.4 Oxygen consumption rates (mg O2 kg h ) of centrarchid fish in relationship to sustained swimming speed. Open circles represent white crappie (Parsons and Sylvester 1992), closed squares represent largemouth bass (Beamish 1970), open triangles represent pumpkinseed sunfish (Brett and Sutherland 1965), and closed circles represent smallmouth bass (Cooke, unpublished data).

of some studies are presented in Figure 8.4. Overall, these findings indicate that the metabolic cost of swimming in centrarchids is different among species. For example, the cost of swimming in largemouth bass appears to be lower than that of smallmouth bass across most swimming speeds (Figure 8.4). These may be true species differences but could also be related to fish size, temperature, and other variables. Parsons and Sylvester (1992) measured oxygen consumption at various swimming speeds and estimated standard and active metabolic rates and swimming efficiency [using cost of transport (COT) analysis] of white crappie. As was noted for other centrarchid and noncentrarchid species (Beamish 1970; Brett 1995; Tolley and Torres 2002; see Figure 8.4), the metabolic rate (mg O2 kg−1 h−1 ) of white crappie increased with increases in swimming speed. An unexpected finding for white crappie, however, was that the metabolic cost and COT decreased between 20 and 25 cm s−1 . The authors observed that at the lower swimming speeds, crappie hold the body rigid (using the relatively long pectoral fins) and persist to swim in the labriform mode (rowing/flapping action of pectoral fins for forward motion). The importance of the pectoral fins for locomotion in fish is fairly well known (for examples, see Gibb et al . 1994; Wilga and Lauder 1999). At higher speeds, Parsons and Sylvester noted that white crappie changed to caudal fin propulsion. It was suggested that this change in swimming mode might contribute to the reduction in energy expenditure at intermediate swimming speeds. Thus, swimming “strategy” may change with changes in water velocity (see Section 8.3.8 on behavioral correlates of swimming). Earlier research on pumpkinseed sunfish by Brett and Sutherland (1965) also showed that oxygen consumption rates increased with increases in swimming speed (Figure 8.4). However, these authors noted that the range of responses in metabolic rate reported within the study appeared unusually large for a centrarchid, the active rate being about nine times the standard rate. Of interest is that these authors compared the 20◦ C response of pumpkinseeds to the 5◦ C response of sockeye salmon and noted that the oxygen consumption rate versus swimming speed of these two species nearly lie on top of each other. This study illustrates the need to examine/establish these relationships in other species and to determine whether body morphology (i.e. being laterally compressed) affects the COT and swimming efficiency (see Videler 1993, for COT values of various fish species). To examine interspecific differences in swimming capacities, Schaefer et al . (1999) compared the swimming endurance of longear (L. megalotis) and bluegill sunfishes at 10◦ C. In this study, swimming endurance was defined as the time to exhaustion while forced to swim at 30 cm s−1 (fish averaged about 100 mm in standard length). There was considerable variation in the endurance time of both species (∼20–180 s). With body length effects removed, however, these authors found that the longear sunfish had a lower hydrodynamic drag and higher mean endurance times than bluegill sunfish (∼97 versus ∼81s). These differences in endurance led to a decreased ability of bluegill sunfish to forage successfully in feeding trials. Recently, Tschantz et al . (2002) examined the physiological strategy for acclimating to low body temperature in largemouth bass, green sunfish (Lepomis cyanellus), bluegill sunfish, black crappie (Pomoxis nigromaculatus), and white

222

Centrarchid fishes

crappie. As part of this study, the authors also examined the swimming activity of these fish. Although a relatively crude measure of swimming (number of times a fish crossed the center line of the tank in a 5-min interval), these authors found that largemouth bass, green sunfish, and bluegill sunfish all decreased average swimming movements (in 5 min) by more than an order of magnitude when 5◦ C-acclimated fish were compared to 25◦ C-acclimated fish. In black crappie, however, there was no significant difference in mean activity between cold (5◦ C) and warm (25◦ C)-acclimated fish. The authors suggested that these differences might be related to over-wintering strategies between species. In a similar study on largemouth bass, Cooke et al . (2001a) found that the swimming activity (proportion of time swimming) and turning rate (turns h−1 ) typically decreased with reduction in temperature (fish tested at 6, 12, or 18◦ C). There were clear effects of fish stock on these relationships (Cooke et al . 2001a). Lastly, Stevens (1979) noted a significant relationship between tail-beat frequency and swimming speed and stride length (swim speed divided by tail-beat frequency to get the fraction of length traveled per tail beat) and swimming speed in largemouth bass swum at different temperatures.

8.3.8 Behavioural correlates with swimming Most of the research conducted on swimming in fish has been obtained through the use of swim tunnels (or respirometers). The use of swim tunnels provides a means to gain data on the metabolic costs of swimming in fish; however, they have certain limitations. One in particular is that behavioral aspects of swimming (i.e. gait recruitment, steady versus unsteady swimming strategies) are more difficult to assess while fish swim in the confined spaces of a tunnel. Recently, Peake and Farrell (2004) examined the locomotory behavior of smallmouth bass during a voluntary ascent through a 25-m raceway, against water velocities ranging from about 50 to 100 cm s−1 . More specifically, they were interested in whether the behavioral aspects of swimming correlated with the physiology in free-swimming bass. The authors found that bass switched between steady and unsteady swimming styles at intermediate speeds. This transition suggested that fish were switching to anaerobic swimming (i.e. contractility of the white musculature). These behavioral findings were supported by the observation that unsteady swimming fish showed significantly lower muscle glycogen levels and higher muscle and plasma lactate levels (i.e. a greater physiological disturbance during unsteady swimming). Therefore, this study and that of Peake and Farrell (2005) provided good evidence that the findings of laboratory studies using swim tunnels may not be applicable to free-swimming individuals. Additional studies directly comparing the locomotor physiology and behavior of confined and free-swimming fish are clearly warranted (see Peake and Farrell 2005).

8.4 Physiological response to stress in centrarchids Over the past 20 to 30 years, a large body of literature has addressed the study of stress in fish. There are many excellent reviews on the basic concepts of stress in fish (e.g., Pickering 1981; Wendellar Bonga 1997; Barton et al . 2002); only a general overview is provided here.

8.4.1 Stress response defined The stress response is broadly grouped as primary, secondary, or tertiary (Barton et al . 2002). The primary stress response is hormonal, and involves an increase in plasma catecholamine (e.g., epinephrine and norepinephrine) and corticosteroid (e.g., cortisol) levels. The catecholamines (predominantly epinephrine) are the first hormones to be released in teleost fish following a stressful situation (Barton et al . 2002). The principal roles of catecholamines are to facilitate oxygen delivery to tissues and mobilization of energy reserves in response to stress (Kieffer 2000). The release of cortisol is delayed (peaks in 1–2 h) relative to catecholamine release. Cortisol has been shown to have several functions in fish including effects on metabolism, osmoregulation, and immune function (see Mommsen et al . 1999 for a review). Increases in catecholamines and cortisol levels can induce changes in metabolic, hydromineral, hematological, immunological, cardiovascular, and respiratory functions. These changes are referred to as the secondary stress response (Barton et al . 2002). Compared with the primary response, the secondary response is slightly delayed and may

Physiology and organismal performance of centrarchids

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be sustained for longer periods of time (Kieffer 2000). Because of this delay, many researchers have examined stress in fish by measuring secondary stress response indices. The secondary response is mainly an attempt to meet the increased energy and oxygen demands placed on the stressed animal (Barton et al . 2002), and to reinstate homeostasis. There are many secondary stress indicators, such as plasma glucose, lactate, tissue glycogen, plasma chloride, sodium and osmolality (a measure of the total concentration of ions in the blood), hematocrit, and hemoglobin, which have been used to assess the stress response in fish (see Barton et al . 2002 for the advantages and disadvantages of each measurement). The tertiary stress response reflects whole animal performance or behavioral changes following primary and secondary indices (Barton et al . 2002). Specifically, these included changes in growth rate, swimming capacity, disease resistance effects, and reproductive functions, all of which ultimately influence the survival of the organism. Most of the research on stress responses of centrarchids has focused on the primary (e.g., Furimsky et al . 2003) or secondary (e.g., Gustaveson et al . 1991; Suski et al . 2004) response.

8.4.2 Handling, hauling, and confinement stresses With respect to fisheries and aquaculture events, it has long been known that mortality is often associated with handling and transporting (hauling) of fishes. To assess the potential causes of mortality in fish following handling and hauling, many researchers have focused on the physiological responses to these types of stressors (Carmichael et al . 1984a,b for example). With respect to centrarchids, most of the emphasis has been placed on the largemouth bass, smallmouth bass, and Florida largemouth bass (Micropterus floridanus), as these species are major game fish that are cultured intensively and transported long distances (Carmichael et al . 1984b). In smallmouth bass, ranging in size from 215 to 300 mm, Carmichael and colleagues (1983) assessed the immediate physiological effects of handling and crowding and the time needed for bass to recuperate from these stressors. Handling and hauling caused a significant increase in blood glucose levels. Compared to baseline levels, glucose increased about four times following a 21/2-hour hauling stress. Although plasma glucose levels had returned to baseline levels by the end of the 4- to 5-day recovery period, plasma ion (sodium and chloride) levels remained low following this period. The hypochloremia (low chloride levels) suggested that smallmouth bass might be more sensitive to hauling stress than previously realized. In a subsequent study, Carmichael et al . (1984a) examined the importance of fish sex and body size, and time of day on the physiological response to confinement stress. Confinement stress was evaluated by placing largemouth bass in small dip-nets immersed in tanks. Fish were confined for up to 48 hours and recovery was monitored periodically for up to 28 days following confinement. Net confinement, for up to 48 hours, caused elevations in glucose and corticosteroids and reductions in chloride levels and osmolality. About 14 days were required for glucocorticoids, osmolality, and glucose levels to return to baseline; whereas chloride levels required nearly the entire 28 days to recover. Similar to that of smallmouth bass (Carmichael et al . 1983), ionoregulatory effects seem to persist following stress, and thus plasma ions are a relatively accurate measure of metabolic recovery in bass. These findings for plasma ions also indicate that more than one stress descriptor/variable should be monitored. Recent work by Suski et al . (2004) showed that exercise stress did not cause significant chloride losses in largemouth bass. The differences between these two studies may reflect differences between prolonged (e.g., hauling stress) and acute (chasing stress) stressors. Carmichael et al . (1984a) also showed that the physiological response to confinement did not appear to be influenced either by fish sex or size. However, in a 30-minute net confinement stress test, time of day had a significant effect. In particular, glucose levels were higher in fish sampled at 1600 than at 2400 and 0400 hours. Lastly, it was noted that the stress response was reduced at lower temperatures (10◦ C) versus warmer (23◦ C) temperatures. This study, in particular, identified the need for researchers to control for (or at least include) the impact of endogenous and exogenous factors on the physiological responses to stress in bass. As part of a larger comparative study, Davis and Parker (1986) examined the corticosteroid stress response of several species of warm-water fish, including largemouth bass and crappie, to transportation/hauling stress. Fish were electro-shocked, blood samples immediately taken, and the fish were held in live wells. After about 1 hour in the live wells, fish were transferred to a laboratory where a second blood sample was taken. Plasma corticosteroid levels increased significantly during transportation in 13 of the 14 species tested. Of the two centrarchid species, largemouth bass had a much lower corticosteroid response (about 1/2) compared with crappie. Since largemouth bass are intensively cultured and widely stocked in temperate and subtropical waters, research into the importance of fish stock/subspecies has been emphasized in earlier literature. The physiological response to hauling stress of

224

Centrarchid fishes

Florida, northern, and hybrid largemouth bass was investigated by Williamson and Carmichael (1986). Fish were spawned to produce four experimental progeny—Florida (F × F), northern (N × N), and two reciprocal crosses (N × F and F × N, the female parent represented first). Groups of largemouth bass of each strain (now known to be species) were confined for up to 24 hours in a net and sampled at a known time. Other experiments were conducted to examine the recovery times and mortality levels of the various strains of fish. Resting concentrations of plasma glucose and chloride did not significantly differ among strains. As noted in other studies (see earlier sections), the confinement stress significantly modified the glucose and chloride levels in all fish. Strain differences occurred within the first 3 hours of net confinement. After 6 hours of confinement, glucose levels remained high and chloride levels decreased, as has been shown in previous studies (Carmichael et al . 1983, 1984a,b). The northern species (i.e. largemouth bass) had smaller changes in their plasma variables and fewer fish died compared to the Florida largemouth bass. These species-specific differences to a stress or challenge imply real genetic physiological differences that need to be recognized by researchers and fish culturists. For example, if one species of bass is more susceptible to stress (largemouth versus Florida largemouth; Williamson and Carmichael 1986), this could have a serious impact on mortality rates of popular game fish during competitive fishing tournaments.

8.4.3 Burst exercise and angling stress The physiological and biochemical responses to burst exercise stress in fish have been well described over the past 50 years (see Wood 1991; Milligan 1996; Kieffer 2000, for reviews). Much of this research has focused on salmonids (Kieffer 2000), mainly because of their large capacity for burst activity. Despite valuable information acquired by studying a single group, research comparing the physiological response to burst exercise of different groups has revealed other important information about exercise-related mechanisms (Wood 1991). Because of their importance as game fish, most research on exercise and angling stress in centrarchids has been carried out on fish in the genus Micropterus (Gustaveson et al . 1991; Kieffer et al . 1995; Suski et al . 2003, 2004). Most work on burst exercise stress in centrarchids has focused on cardiovascular physiology (see Section 8.5) or muscle physiology as indicators of stress. To evaluate the physiological response to exercise/angling stress, many researchers have measured changes in muscle and/or blood lactate. Overall, the maximum post-exercise muscle lactate levels are generally lower for centrarchids compared to some other fish species (see Table 8.3). One of the earliest studies to examine exercise stress in centrarchids came from the pioneering work of Edgar Black. Black (1955) examined burst exercise stress in six freshwater species, including the largemouth bass. Black (1955) exercised fish by manual chasing for about 15 minutes and then assessed the blood for changes in hemoglobin (Hb) and lactate. Of all the species tested, only largemouth bass showed a significant increase in Hb (about a doubling from baseline concentrations) levels following the exercise stress. Blood lactate levels increased from 9.9 mg dl−1 (1 mmol l−1 ) at rest to about 76 mg dl−1 (8.4 mmol l−1 ) following the exercise stress. Compared with the other species of fish studied, Black (1955) showed that the levels of lactate produced by bass were not as high as noted for trout and not as low as for black catfish (Ameiurus melas melas), fine-scaled sucker (Catostomus catostomus), and carp (Cyprinus carpio). Black suggested that the order of lactate accumulation might be related to upper lethal temperature of each species. Other investigators have noted similar plasma lactate levels in largemouth bass following 1 minute of exercise (∼5 mmol l−1 ; Suski et al . 2004) or following an angling tournament (∼10 mmol l−1 ; Suski et al . 2003). Despite the rapid increase in lactate levels following exercise stress, levels decreased to resting conditions within 4 hours (Suski et al . 2006). Heath and Pritchard (1962) examined the physiological response, measured as oxygen consumption and blood lactic acid production, of bluegill following an 11-minute exercise bout (range 5–45 min) at 20◦ C. Similar to that of largemouth bass, bluegill had resting blood lactate levels of about 10 mg dl−1 (∼1 mmol l−1 ). These levels increased to 77 mg dl−1 (∼8.5 mmol l−1 ) immediately after exercise and they peaked at 100 mg dl−1 (∼11 mmol l−1 ) at 1 hour. Unlike that for largemouth bass (Suski et al . 2006), clearance of lactate was much slower (∼6–10 h) for bluegill. This may be related to differences in temperature between these studies (e.g., see Kieffer et al . 1994, for rainbow trout).

8.4.3.1 Effects of angling stress duration Gustaveson et al . (1991) examined the physiological response to angling duration (1–5 min) in largemouth bass. Of the many measurements made in the study, blood lactate concentrations increased directly with angling time. Plasma osmolality

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also increased with increases in angling time. Gustaveson et al . (1991) also showed that these increases were greater in fish angled in warmer water (23–26◦ C) compared to colder water (11–13◦ C). A similar study was carried out by Kieffer et al . (1995) to examine the effects of angling stress on nesting male smallmouth bass. Bass were hooked and played either briefly (<20 s) or to exhaustion (∼2 min) and the white muscle metabolite energy status and lactate concentrations were used as indicators of the physiological disturbance. Similar to that for largemouth bass (Gustaveson et al . 1991), the physiological disturbance was greater in smallmouth bass angled for 2 minutes relative to 20 seconds. Levels of white muscle energy fuels (e.g., phosphocreatine, PCr, and ATP) were lower in smallmouth bass that were angled for longer periods of time. White muscle pH was also lower (6.9 versus 7.0) and muscle lactate levels were significantly higher (∼18 µmol g−1 versus 12 µmol g−1 ) in bass angled for 2 minutes compared to 20 seconds, respectively. In addition to examining the physiological response to exercise, Kieffer et al . (1995) also examined the ability of bass to return to their nests following an angling bout. Fish played for 2 minutes took 4 times longer to return to their nests than did fish played for ∼20 seconds. This more lengthy disruption in the parental care activities of the exhaustively played group of fish resulted in an increase in the incidence of nest predation (see Kieffer et al . 1995 for additional details).

8.4.3.2 Body size effects Over the past decade, researchers have become interested in the relationship between body size and the stress response in fish (Goolish 1991, 1995). Most work has focused on salmonids (Goolish 1991; Ferguson et al . 1993; Kieffer et al . 1996; McDonald et al . 1998; Wakefield et al . 2004), but some work has been conducted on centrarchids. In a comparative study, Kieffer et al . (1996) examined the physiological response to exercise stress in two sizes of largemouth bass and brook trout (Salvelinus fontinalis). They found that a strong positive relationship between body size and the postexercise response in brook trout exists [also noted for salmon: Wakefield et al . (2004) and rainbow trout: Ferguson et al . (1993), see Figure 8.5b and 8.5a, respectively]. In contrast, Kieffer et al . (1996) did not observe the same trend for largemouth bass (see Figure 8.5c). In fact, it appeared that there was a slight negative relationship between lactate production and body (c) Largemouth bass 45

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Figure 8.5 The relationship between fish length and the maximum level of white muscle lactate in (a) rainbow trout (Ferguson et al . 1993, Kieffer et al . 1994), (b) Atlantic salmon (Wakefield and Kieffer, unpublished data; Booth et al . 1995, Wilkie et al . 1996, 1997, Galloway and Kieffer 2003, Rossiter, unpublished data), (c) largemouth bass (Kieffer et al . 1996; Suski et al . 2006), and (d) smallmouth bass (McDonald et al . 1991 for 12-cm fish; Kieffer et al . 1996 and Peake and Farrell 2004 for 31-cm fish).

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size (see Figure 8.5d). It was suggested that the differences in the physiological response between trout and bass could be related to lifestyle differences. For example, because bass are sit-and-wait predators that attack their prey from short distances, one might expect that large and small bass would not require different levels of anaerobic power. This contrasts that of active species, such as trout and salmon, which must maintain burst speeds over longer distances; therefore, large and small individuals of a given active species may require different anaerobic capacities to overcome the increases in frictional drag and to maintain size-independent capacities for burst swimming. Although comparative studies are lacking to specifically address the relationship between body size and exercise stress response in centrarchids, conclusions may be obtained by combining various data sets for smallmouth bass (see Figure 8.5d). Although these data are from various sources, it appears that the relationship between smallmouth bass size and lactate production follows a trend similar to that of the salmonids, rather than that of largemouth bass (Figure 8.5c). A potential explanation for this would be that smallmouth bass are a more riverine species compared to largemouth bass, and the same constraints that exist for other riverine species (i.e. anaerobic power issues mentioned earlier) exist for smallmouth bass. Future work should identify the effects of body size on stress/exercise physiology of centrarchids.

8.4.3.3 Time course for recovery Although the physiological response to chasing stress has been studied in some species of centrarchids, very little information has been collected on the time course for physiological recovery. Recently, Suski et al . (2005) examined the physiological recovery of largemouth bass to a 1-minute chasing stress. The response of largemouth bass to exercise was typical of other fish species examined (i.e. decreases in white muscle energy reserves, accumulation of lactate in muscle and blood). Unlike that for species of salmonids (see Milligan 1996; Kieffer 2000), however, the physiological disturbances associated with exercise stress were corrected by 2 to 4 hours when fish were held in well-aerated water. Suski et al . (2005) also exercised largemouth bass at acclimation temperature (26◦ C) and allowed the fish to recover for 2 hours in environments with either elevated temperature (32◦ C), reduced temperature (14◦ C), low oxygen levels (hypoxia), or high oxygen levels (hyperoxia). These authors noted that cold environments significantly impaired metabolic recovery of muscle lactate, a result that has also been recently shown for Atlantic salmon (Galloway and Kieffer 2003). Interesting, however, was that recovery at warmer temperatures also negatively impacted recovery of bass. Although no mortalities were noted in this study, it is highly possible that the warmer temperatures approached the upper lethal of bass, which potentially has a negative effect on recovery time. Similarly, a 50% reduction in oxygen levels impeded recovery of the metabolic disturbances in this species following exhaustive exercise. In comparison to the other recovery environments used in this study, hyperoxic water had much less of an impact on the physiological variables examined. Most notably, hyperoxia did not impair the recovery of muscle lactate. Again, future studies need to examine the impact of different oxygen levels on the postexercise stress response in centrarchids. As noted earlier, exhaustive exercise has pronounced effects on muscle and blood physiology in fish. It is also apparent that there are species-specific responses in the magnitude of the disturbance and the time required for full metabolic recovery. Based on a limited data set (i.e. Suski et al . 2006), it is apparent that some abiotic factors (i.e. temperature and oxygen levels) negatively impact the recovery process in largemouth bass. In fact, most studies examining the postexercise recovery process in fish have limited their studies to abiotic factors (Kieffer 2000). Recently, researchers have examined the impact of slow velocity swimming on the time required to recover from exhaustive exercise. Milligan et al . (2000) and Farrell et al . (2001), for example, have shown that slow aerobic swimming hastened the recovery of several physiological variables in salmonids relative to fish recovered in static water. Given that rainbow trout and coho salmon are migratory, these findings may not be surprising. Centrarchids, on the other hand, are generally considered to be quiescent relative to salmonids. Thus, whether the results noted for salmonids (Milligan et al . 2000; Farrell et al . 2001) are comparable to nonsalmonid species is not fully understood. To address this question, Suski et al . (2007) exercised largemouth bass to exhaustion and allowed half the fish to recover from exercise in static water or in water flowing at 0.5 BL s−1 . Various blood (cortisol, lactate), muscle (lactate, phosphocreatine, ATP), and cardiac (stroke volume, heart rate, cardiac output) variables were assessed over a 4-hour period. Overall, few of the variables measured over the 4-hour recovery period recovered faster in bass with access to flow. These findings for bass may reflect the fact that largemouth bass are “sit-and-wait” ambush-type predators and do not routinely engage in long-distance swimming (Demers et al . 1996). Additional studies are warranted to address these intriguing questions.

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8.4.4 Environmental hypoxia Fish experience large variations in the physical and chemical properties of their natural aquatic environments, including changes in dissolved oxygen levels. Reduced levels of dissolved oxygen (hypoxia) in aquatic environments occur as a result of natural phenomena; however, more commonly they are caused by anthropogenic input of nutrients and organic matter into water with poor circulation. Reduced dissolved oxygen is an environmental problem frequently encountered in many water bodies. Changes in water oxygen levels can affect the physiology and behavior of fish, and it can influence fish distribution, migration, growth, reproduction, and survival.

8.4.4.1 Responses to hypoxia When fish encounter hypoxic environments, a behavioral response, such as escaping, is the easiest and least expensive way of coping with the situation (Jensen et al . 1993). However, there are situations in which escape is neither possible (e.g., widespread hypoxia in a lake) nor necessary. In these cases, fish may use a combination of behavioral or physiological strategies to cope with the conditions. Initially, fish attempt to maintain oxygen delivery to the tissues, which can be accomplished by increasing ventilation volume (Perry and Gilmour 1999), oxygen transport capacity (e.g., increasing the number of red blood cells, Nikinmaa 1990), or oxygen binding capacity of hemoglobin (Nikinmaa 1990). Fish can survive hypoxia through metabolic depression or through the activation of alternative metabolic strategies, such as utilization of anaerobic pathways to produce ATP (Boutilier et al . 1988). The responses and tolerance to hypoxia have been well documented in some freshwater species of fish, such as salmonids, carp, goldfish (Carassius auratus), and sturgeon species (Dunn and Hochachka 1986; Boutilier et al . 1988; Van Raaij et al . 1996; Baker et al . 2005). Some research has been conducted on centrarchids, including behavioral and physiological responses to hypoxia.

8.4.4.2 Behavioral responses to hypoxia Using a 5-m-long oxygen gradient ranging from 10 to 95% air saturation, Burleson et al . (2001) examined the behavioral response of small (23–500 g) and large (1000–3000 g) largemouth bass to hypoxia. Observations of the fish within the gradient were used to determine whether bass showed oxygen selection, hypoxic avoidance, or changed their activity. The position of the fish in the gradient was compared between control (no gradient) and experimental (oxygen gradient) periods. When the gradient was formed, fish rarely visited the most hypoxic (<20% saturation) areas; if fish swam through these low oxygen areas, they typically turned around and swam back into water with higher oxygen tensions. These results suggested that bass actively avoided oxygen levels <27% air saturation. Activity levels were not significantly different between control and experimental groups, but the authors suggested that smaller fish had broader hypoxic tolerance limits than the larger fish. Although bass generally avoided oxygen levels of <27%, some animals did venture into the areas with the lowest oxygen. Thus, largemouth bass have the ability to briefly tolerate hypoxic exposure (see later for physiological responses).

8.4.4.3 Physiological responses to hypoxia The physiological response to hypoxia in centrarchids is limited to studies on bluegill, smallmouth bass, and largemouth bass. Most of these studies have subjected fish to gradually induced environmental hypoxia. Studies have focused on either respiratory physiology (Cech et al . 1979; O’Hara 1971; Furimsky et al . 2003) or metabolic changes (Heath 1991; Furimsky et al . 2003) associated with hypoxia.

8.4.4.4 Respiratory physiology Cech et al . (1979) examined how the oxygen consumption patterns changed before (oxygen saturated, partial pressure of oxygen, PO2 >130 mmHg) and following a hypoxic challenge (partial pressure of oxygen at 40 mmHg). At 25 and 30◦ C, oxygen consumption rates dropped about 14 and 46% after the hypoxic exposure, respectively. This pattern was not noted

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at 20◦ C (see Figure 8.1c). In a separate experiment, Cech et al . (1979) determined that the critical PO2 for largemouth bass at 20◦ C is below 40 mmHg, between 40 and 50 mmHg at 25◦ C, and between 50 and 60 mmHg at 30◦ C (see Figure 8.1c). Ventilation frequency was not measured in Cech et al . (1979), but recently Furimsky et al . (2003) measured the ventilation rate of largemouth and smallmouth bass over a range of oxygen tensions. They found that the ventilation rate increased by about 25% at the first level of hypoxia (90 mmHg) in smallmouth bass and remained elevated as oxygen tensions in the water decreased. Ventilation rate following hypoxia also increased in largemouth bass, but oxygen tensions were lower (i.e. 60 mmHg). Overall, the ventilation rate of largemouth bass was much lower compared to smallmouth bass, again suggesting the relatively high hypoxic tolerance of largemouth bass. Increases in ventilation rates with decreases in PO2 have been noted for other species, including shortnose and Atlantic sturgeon (Baker et al . 2005), and flounder (Platichthys flesus) (Steffensen et al . 1982). Spitzer et al . (1969) examined the effects of reduced oxygen levels on the oxygen consumption and ventilation rates in bluegill acclimated to 13, 25, and 30◦ C. As hypoxia was induced, fish at the warmest temperature showed an immediate and continued decline in oxygen consumption rates below an oxygen tension of 122 mmHg. In contrast, at 13◦ C, bluegill showed a high degree of oxygen independence until 60 to 70 mmHg; oxygen consumption rates were significantly reduced below these oxygen tensions. Fish acclimated to 25◦ C had a response that was intermediate to 13 and 30◦ C. Ventilation rates increased at both 13 and 25◦ C as oxygen tension decreased. At 25◦ C, however, ventilation rates could not be maintained at oxygen tensions below about 50 mmHg. Fish acclimated to 30◦ C could not increase ventilation rates with increasing hypoxia. In fact, ventilation rate dropped off significantly at about 60 mmHg. Overall, these findings indicate that the physiological response to hypoxia in bluegill is significantly influenced by environmental temperature. In particular, fish at 13◦ C have a high degree of oxygen independence compared to fish at warmer temperatures.

8.4.4.5 Metabolic physiology In addition to respiratory adaptations, fish also show metabolic changes following hypoxic stress. Of the limited data, studies on centrarchids have focused on hormonal, hematological, and ionic changes associated with hypoxia. Heath (1991) exposed bluegill to air-saturated water (∼8 mg l−1 ) and then a 1.3 mg l−1 hypoxic challenge. Blood samples were taken before and immediately following the hypoxic stress or after 4- and 24-hour recovery in normoxic water. Overall, hypoxia did not cause any significant changes in hemoglobin levels or blood ions (Na+ , Cl− , or K+ ). In contrast, there were elevations in blood glucose and lactate concentrations (i.e. a stress response) following hypoxia. Lactate recovered within 4 hours after the fish were returned to normoxic water. In a detailed study, Furimsky et al . (2003) examined several arterial blood respiratory variables, ventilation rate, cardiac output, and hematological responses in largemouth and smallmouth bass to graded levels of hypoxia. Reductions in water oxygen tension caused a similar decrease in arterial partial pressure of oxygen in both species. Largemouth bass typically had blood with a higher affinity for oxygen, which signifies that largemouth bass hemoglobin can bind more oxygen at a lower arterial oxygen pressure. Severe reductions in oxygen caused significant increases in blood catecholamine levels of smallmouth bass only. Catecholamines are normally released during severe hypoxia to initiate a variety of physiological mechanisms that will enhance blood oxygen transport (e.g., release of red blood cells from spleen, increase the gill surface area to enhance oxygen uptake; see Perry and Reid 1992 for review). Lactate levels were typically higher for smallmouth compared to largemouth bass, indicating that smallmouth bass activated anaerobic pathways to generate ATP for cellular processes. Although these two species are closely related, these results suggest overall that, largemouth bass are less sensitive to low oxygen levels than smallmouth bass. Some important interspecific differences were also observed in these experiments during the posthypoxia recovery period. For example, all the variables measured in this study had returned to control normoxia values within 12 hours in largemouth bass but not smallmouth bass. In addition, all of the largemouth bass used in the study survived, whereas some of the smallmouth bass died.

8.5 Cardiovascular physiology Details on the form and function of the fish cardiovascular system are provided by Satchell (1991) and Farrell and Jones (1992). In general, the cardiovascular system in teleost fishes, including the centrarchids, is similar to other vertebrates

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in that it is the primary means of delivering oxygen obtained from the gills to body tissues (Jones and Randall 1978). In addition, the circulatory system serves a number of other key transport functions. This includes the transport of carbon dioxide to the gills (and skin in some species) where it is expelled to the environmental water, the transport of the soluble digestion products from the alimentary canal to the liver, the transport of hormones and vitamins, as well as ions that are essential for osmoregulation (Satchell 1991). The generalized teleost circulatory system comprises a pump (the heart) and a continuous system of branching arteries, arterioles, capillaries, and veins (Satchell 1992). These branching tubes form a closed system such that all blood leaving the heart is returned at a later time. One of the most robust indicators of metabolic rate in fish is cardiac output (the product of heart rate and stroke volume; Farrell and Jones 1992). Cardiac output is perhaps the most fundamental quantitative measure of cardiac function. The relative contribution of the two constituents—heart rate and stroke volume—determines whether a certain species is regarded as a frequency modulator (when heart rate increases and stroke volume decreases) or volume modulator (when stroke volume increases and heart rate decreases; Farrell 1991). The prevailing belief is that volume modulation is the most common strategy (e.g., salmonids; Farrell 1991). Methods for quantifying and describing cardiac function are covered in detail elsewhere (Satchell 1992) but include Doppler and transonic flow probes (Schreer et al . 2001), electrocardiography (Spitzer et al . 1969), heart rate telemetry (Priede 1983), and indirect thermodilution methods (Reynolds and Casterlin 1978b). There is a large body of work on the cardiovascular physiology of teleost fishes owing in large part to the extensive work conducted using rainbow trout and other salmonid models (e.g., Satchell 1991; Farrell and Jones 1992). Many of the current paradigms in fish cardiovascular physiology are based on the assumption that the circulatory system of salmonids are representative of the broader teleost classes of fishes. In recent years, it has become apparent that there is extensive interspecific variation in cardiovascular performance (Farrell 1991). More recently, efforts have focused on evaluating the extent of cardiovascular plasticity and intraspecific variation (Gamperl and Farrell 2004). Despite being abundant components of the North American ichthyofauna, historically centrarchid fishes were rarely used as models in cardiovascular research. Researchers began to focus on centrarchids, and in particular those of the Micropterus genera, in the late 1990s. This research actually grew out of an interest in applying tools in cardiovascular physiology to understand pressing issues in fisheries conservation and management, especially with respect to catch-and-release angling (Cooke et al . 2002b,c,d). As this research attempted to provide information of an applied nature, it also quickly became apparent that centrarchid fishes were fascinating models for exploring more basic questions in comparative cardiovascular performance and physiological diversity (see Schreer et al . 2002). Here, we summarize the cardiovascular physiology of centrarchid fishes in the context of their performance, behavior, and ecology. We also consider the recent contributions of centrarchid cardiovascular physiology to the broader field of fish circulation, especially in relation to salmonids.

8.5.1 Stress and cardiovascular alterations Stress can arise from different sources ranging from the environmental heterogeneity, biological interactions, and anthropogenic disturbances (see Adams 2002). Cardiovascular physiology has only recently been used as a proxy for the assessment of stress responses in fish, with the majority of effort focused on centrarchid fishes. Cardiovascular variables are inextricably linked to the metabolic rates of fish and their physical performance, and thus can be used to monitor how fish respond to different stressors (Farrell and Jones 1992; Thorarensen et al . 1996; Brodeur et al . 2001). Researchers have used cardiovascular performance as an indicator of how fish respond to variations in environmental conditions such as salinity (Claireaux et al . 1995) or oxygen (Randall 1982). Here we evaluate cardiovascular responses to a number of natural and anthropogenic stressors including predation threat, air exposure, silt, exercise, hypoxia, and water temperature.

8.5.1.1 Ecological stressors An ecologically relevant stressor faced by many fish, including centrarchids, is the threat of avian predation. Cooke et al . (2003c) simulated avian predation attempts on largemouth bass using the models great blue heron Ardea herodias and osprey Pandion haliaetus to quantify the nonlethal energetic costs of predation. The researchers evaluated largemouth bass cardiac response across in fish ranging in length from 200 to 450 mm using Doppler flow probes. The response exhibited by all fish to simulated predation was an immediate bradycardia (i.e. massive reduction in heart rate), possibly due to the

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psychological stress of fear or anticipation. The extent of the bradycardia during the 30-second predation attempt varied depending upon the size of the fish and the type of predator. The magnitude of the bradycardia decreased with increasing size of the fish. Maximal cardiac disturbance following simulated predation attempts by osprey was consistent among size classes of bass. However, Cooke et al . (2003c) reported that the magnitude of the disturbance following heron predation attempts was reduced as the size of fish increased. Size-specific trends for largemouth bass exposed to simulated avian predation attempts were even more extreme for cardiac recovery durations. Largemouth bass of all sizes exposed to osprey predation attempts required ∼40 minutes for cardiac output and heart rate, and ∼30 minutes for stroke volume to return to predisturbance levels (Figure 8.6). Although smaller bass exposed to heron predation attempts required recovery times similar to fish exposed to the osprey, as the size of largemouth bass exposed to the heron model increased above ∼300 mm,

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the recovery time decreased significantly (Figure 8.6). The authors concluded that the size-specific response of largemouth bass to different predators is reflective of their ability to assess the risk posed by different predators. Furthermore, the nonlethal costs of predation can be substantial and should be considered in future bioenergetics models. Interestingly, this was the first study to assess all components of cardiac output rather than just heart rate (e.g., Atlantic salmon, Johnsson et al . 2001) when assessing the nonlethal costs of predation. Fish also will respond to social interactions through changes in cardiovascular function. Cooke et al . (2002a) used heart rate transmitters on free-swimming largemouth bass and reported that heart rate increased in response to both conspecifics and potential prey. Perhaps these changes are anticipatory as has been proposed for lingcod (Farrell 1981).

8.5.1.2 Handling stressors Air exposure represents a similar type of stressor to hypoxia in that the cardiorespiratory systems become compromised. In centrarchid fishes, air exposure occurs as a result of catch-and-release recreational angling and fishing tournaments (Suski et al . 2004). In a study of rock bass (Ambloplites ruprestris), Cooke et al . (2001b) revealed that longer air exposure durations resulted in longer cardiac disturbance times. Fish were held at 16◦ C and were chased for 30 seconds prior to experimentation. When exposed to air for 30 seconds, cardiac variables recovered in ∼100 minutes whereas when exposed to air for 180 seconds, recovery took longer than 200 minutes. During air exposure, fish experienced severe bradycardia similar to responses observed from simulated predation attempts as discussed earlier. Cooke et al . (2002c) reported the same pattern of longer recovery associated with longer air exposure duration for smallmouth bass across a broader suite of air exposure durations (0, 30, 120, 240 s). All fish were chased for 60 seconds at 12◦ C prior to an air exposure “treatment.” Time required for cardiac variables to recover increased from 60 minutes for fish not exposed to air to 160 minutes for fish exposed for 240 seconds (Cooke et al . 2002c). Cooke et al . (2002c) and Suski et al . (2004) evaluated the air exposure component (livewell weigh-in) of fishing tournaments for smallmouth bass and largemouth bass, respectively. Air exposure during the weigh-in procedure was determined to be the single greatest stressor, elevating cardiac output and heart rate more than exercise alone. Indeed, in a parallel study (i.e. Suski et al . 2004) where fish were weighed in water or air, it was even more apparent that air exposure caused massive physiological disturbances (suite of metabolic changes), including cardiovascular alterations. Anthropogenic stressors can also arise due to husbandry and handling. A recent study by Cooke et al . (2004c) used largemouth bass as a model to evaluate the cardiovascular consequences of truck transport and the potential for low concentrations of the anesthetic clove oil to mitigate stress. When exposed to clove oil of any concentration, an initial bradycardia occurred in bass, followed by increases in both cardiac output and heart rate. Fish exposed to low levels of clove oil recovered these variables rapidly when returned to fresh water, but those exposed to higher concentrations exhibited protracted cardiovascular recovery. In addition, fish that were exposed to shallow (i.e. sedating) anesthesia recovered more rapidly than nonanesthetized control fish. Although crowding was likely not an issue in that study due to the use of low densities of fish, previous research on smallmouth bass indicated that crowding is indeed stressful. Cooke et al . (2002c) held smallmouth bass in live wells to simulate tournament fishing conditions with either 1, 2, 4, or 6 fish per livewell at 25◦ C and monitored their cardiovascular activity after a brief handling disturbance. The authors reported that when fish were held individually, cardiac variables returned to resting levels within 1 hour. However, fish held at densities of 2, 4, or 6 fish/livewell showed different recovery trends. This was particularly evident for fish held in the highest two densities where cardiac output, heart rate, and stroke volume remained elevated and were highly variable throughout the entire 6-hour experiment. Thus, crowding, and likely associated interactions among individuals, resulted in stress that was manifested in cardiovascular disturbance.

8.5.1.3 Environmental stressors To date, relatively few environmental variables have been evaluated in the context of centrarchid cardiovascular responses to stress. The several exceptions are for responses to silt and hypoxia, which are discussed here, and temperature, which is discussed in extensive detail in its own section later. Bunt et al . (2004) conducted an assessment of silt responses using rock bass (equipped with Doppler flow probes) from both riverine and lacustrine populations (see discussion on intraspecific variation later). After recovery from surgery, replicated treatment groups were exposed to incremental increases in silt load

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(made from a bentonite slurry). Lacustrine rock bass responded significantly to low concentrations of silt [10 Nephelometric Turbidity Units (NTU)] as evidenced by inconsistent and highly variable cardiovascular function. However, the response by riverine rock bass was muted with little interindividual variation. Results indicated that compensatory mechanisms to minimize cardiorespiratory disruption associated with increases in suspended silt appear to be inherent in rock bass of riverine origin, and these fish appear to fully compensate for interference in gas exchange at the gill surfaces 60 minutes after initial exposure. Hypoxia is a widespread stressor experienced by many fish species including centrarchids (Aday et al . 1999). The most comprehensive assessment of hypoxia on centrachid cardiovascular physiology is in Furimsky et al . (2003), where they contrasted smallmouth bass and largemouth bass responses to graded hypoxia (reduction in water PO2 from 150 to 45 torr). The authors reported that increases in ventilation rate (54%) and decreases in cardiac output (27%) during hypoxia were more pronounced in smallmouth bass than in largemouth bass. These findings are indicative of a bradycardia during hypoxia and are consistent with salmonid literature (e.g., Randall 1982). These observations were also consistent with the greater acid-base disturbance and lower oxygen affinity for smallmouth bass relative to largemouth bass. After a 24-hour recovery period, largemouth bass cardiovascular variables had returned to baseline levels. Conversely, smallmouth bass cardiovascular performance was still altered (i.e. erratic), possibly indicating permanent tissue damage. The authors concluded that smallmouth bass were more sensitive to hypoxia than largemouth bass providing implications for situations in which these two bass species may be exposed to periods of hypoxia, such as during live-release angling events. Similarly, periods of winter hypoxia may also be more stressful to smallmouth bass rather than largemouth bass, but this has not been addressed in the literature. The only other centrarchid cardiovascular physiology research on hypoxia focused on bluegill using electrodes to monitor the electrocardiogram. Marvin and Heath (1968) exposed bluegill held at 25◦ C to gradually progressive hypoxia. Resting heart rate was ∼90 BPM and increased when oxygen concentrations were reduced from 100% saturation to 80% saturation, reaching a maximum of ∼100 BPM. Interestingly, ventilation rates did not reach maximal values (i.e. 110 ventilations/min) until ∼40% saturation. There is a near one-to-one relationship between heart rate and ventilation rate in largemouth bass (Reynolds 1977a) held in normoxic water (but at a range of water temperatures). As saturation levels dropped below 80%, Marvin and Heath (1968) noted that bluegill experienced a bradycardia (to a low of 15 BPM) and near zero ventilation at 15% saturation. Below 15% saturation, oxygen concentrations were lethal leading to cardiorespiratory failure. Spitzer et al . (1969) conducted similar experiments on bluegill; however, they evaluated hypoxic responses at three temperatures (13, 25, and 30◦ C). Cardiac responses to hypoxia differed markedly across water temperatures. At 30◦ C, heart rate decreased linearly (from 100 BPM) with decreasing oxygen concentrations. Responses at 25◦ C were identical to those reported in Marvin and Heath (1968) (i.e. tachycardia followed by later bradycardia). At 13◦ C, heart rate actually increased gradually from ∼25 BPM with decreasing oxygen concentrations until reaching a maximum at 75 mmHg. This was followed by a gradual bradycardia. Ventilation rates also remained steady at 13◦ C until below 90 mmHg when they gradually increased by ∼50%. Conversely, ventilation rates for fish held at 25 and 30◦ C decreased dramatically at a PO2 of about 75 mmHg. These two studies provided early insight into the cardiovascular physiology of fishes during hypoxia, and decades later, they still represent more than half of this work focused on centrarchids.

8.5.1.4 Water temperature as a stressor and mediating factor As with most physiological processes, cardiovascular performance is intimately linked to water temperature. Increases in metabolic rate tend to produce a proportional increase in cardiac output (Mirkovic and Rombough 1998). In general, resting heart rate and cardiac output are usually lower at cold temperatures and higher at warmer temperatures (Farrell 1996; Farrell 2002; see Table 8.4). Indeed, this pattern seems to be evident among largemouth bass. Interestingly, largemouth bass cardiovascular performance has been evaluated across one of the largest ranges (3–26◦ C) of water temperature for any fish species [this range is actually larger if one includes just heart rate data— Reynolds (1977a) monitored heart rate up to 32◦ C with electrocardiogram apparatus]. When all of these data for largemouth bass collected with Doppler probes are plotted on a single figure, the temperature dependence of resting heart rate and cardiac output becomes apparent (Table 8.4; Figure 8.7). For smallmouth bass across a narrower range of temperatures (12 to 20◦ C), Q10 rates for resting fish were around 2 indicating temperature conformity. Other species of centrarchid fish also show positive relationships between temperature and both heart rate and cardiac output (e.g., smallmouth bass, bluegill, pumpkinseed,

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Cooke et al. 2003c

Cooke et al. 2003c

Cooke et al. 2003c

Cooke et al. 2003c

Citation

129

134

135

134

140

2

2

3

42

20

38

39

Cardiac recovery time (min)

Table 8.4 Summary of centrarchid cardiac responses to a variety of different stressors. This table is focused on heart rate responses as there are more papers that have measured heart rate than cardiac output. Data provide opportunity to compare resting levels of heart rate, responses to different stressors, and recovery times across a range of water temperatures and species. Several different methods were used to generate values; D, Doppler flow probes, T, heart rate telemetry, E, electrocardiography, O, thermodilution. Readers are encouraged to consult original sources for additional detail on each study.

234

Smallmouth bass

Species

Table 8.4 (continued).

D D D D D D D D

D

D

D

D

D

18 12 12 16 16 20 20 12

12

12

12

25

25

E

32 D

O

12

21

Method

Water temperature (◦ C)

Confinement over 6 h (density 2 fish)

Confinement over 6 hours (density 1 fish)

Exhaustive exercise and 240-s air exposure

Exhaustive exercise and 120-s air exposure

Exhaustive exercise and 30-s air exposure

Exhaustive exercise and 0-s air exposure

Exhaustive exercise

Brief exercise

Exhaustive exercise

Brief exercise

Exhaustive exercise

Brief exercise

Exhaustive exercise

Graded hypoxia followed by normoxia

Resting

Resting

Stressor/Activity

63

36

26.7

58.1

58.1

26.7

26.7

26.7

26.7

52.8

52.8

34.5

34.5

26.7

NA NA

Schreer et al. 2001

Cooke et al. 2002c

Cooke et al. 2002c

Cooke et al. 2002c

Cooke et al. 2002c

∼60

∼120

∼130

∼155

NA

NA

∼180

NA

110a

140a

NA

NA

NA

Schreer et al. 2001

∼30 ∼130

∼165

Schreer et al. 2001

Cooke et al. 2002c

Cooke et al. 2002c

Schreer et al. 2001

Schreer et al. 2001

∼28 ∼100

Schreer et al. 2001

∼220

∼200

Cooke 2002

Furimsky et al. 2003

Reynolds 1977a

Reynolds and Casterlin 1978b

Citation

∼220

∼50 ∼115

∼150

72

NA

∼70

NA

Cardiac recovery time (min)

233

NA

∼30

37.4

Relative change in heart rate (% of resting)

Resting heart rate (beats min−1 )

235

D

E

25

D

E

25

3

E

15

18

E

D

18 15

E

25

D

E

13

18

E

25

D

18 E

D

16

30

D

16

D

25

a Mean over a 6-h period. b At oxygen tension of 120 mmHg.

Black crappie

Pumpkinseed

Bluegill

Rock bass

D

25

Exhaustive exercise

Exhaustive exercise

Resting (North Carolina population)

Resting (Massachusetts population)

Resting (North Carolina population)

Resting (Massachusetts population)

Exhaustive exercise

Exhaustive exercise

Response to graded hypoxia

Response to graded hypoxia

Response to graded hypoxia

Response to graded hypoxia

Exhaustive exercise

Exercise and 180-s air exposure

Exercise and 30-s air exposure

Confinement over 6 h (density 6 fish)

Confinement over 6 h (density 4 fish)

∼20

∼90

NA NA NA

∼30 ∼50 ∼60

13.3

250

212

NA

∼38

33.9

183

52.6

171

NA

∼50

∼ 32b

59.4

NA

∼20

∼ 95b

103

81

NA

NA

NA

NA

77

65

NA

79 NA

228 ∼25

203

39.8

180

101

NA

130a 148

NA

140a

∼ 100b

48.7

48.7

58.1

58.1

Cooke et al. 2003a

Cooke 2002

Roberts 1967

Roberts 1967

Roberts 1967

Roberts 1967

Cooke 2002

Cooke 2002

Marvin and Heath 1968

Spitzer et al. 1969

Spitzer et al. 1969

Spitzer et al. 1969

Cooke 2002

Cooke et al. 2001b

Cooke et al. 2001b

Cooke et al. 2002c

Cooke et al. 2002c

Centrarchid fishes

Cardiac output (ml min−1 kg−1)

236

80 70 60 50 40 30 20 10 0

RT LMB?

140 Heart rate (beats min−1)

120 100 80 ∗

60 40 20 0

Stroke volume (ml min−1)

1.4 1.2 1.0 0.8 0.6 0.4 0.2

0

5

10

15

20

25

30

35

Water temperature (°C)

Figure 8.7 Effects of water temperature on resting and maximum cardiac output and its components, heart rate, and stroke volume. Data are for largemouth bass. Squares are maximal values and circles are resting values from data taken from Cooke et al . (2003a,b). Additional data are extracted from Cooke and Philipp (2005); only data from pure Illinois fish were used from this paper. The asterisk represents a single warmer resting heart rate point for largemouth bass taken from Reynolds (1977a). Note that following exercise, cardiac output and heart rate increase, whereas stroke volume decreases. Thus, stroke volume values represent maximal change (decrease) from resting levels. Data from rainbow trout cardiac output are included for comparison at 10 (open triangle, maximum, filled triangle, minimum; from Kiceniuk and Jones 1977) and 15◦ C (open inverted triangle, maximum, filled inverted triangle, minimum; from Neumann et al . 1983). The dashed line drawn on the cardiac output panel is a general schematics generated from the idea that rainbow trout (RT) reach a maximal cardiac output and beyond a threshold temperature, cardiac scope is reduced (as presented by Farrell 1996; 2002). The schematic dashed line presented for largemouth bass (LMB) has not been verified experimentally.

rock bass; Cooke 2002). Interestingly, most centrarchid studies have found that resting stroke volume was not affected by temperature (e.g., smallmouth bass, Schreer et al . 2001; largemouth bass, Cooke et al . 2003b). However, when data from a larger temperature range (including low temperatures) are included, there is an inverse relationship between temperature and stroke volume (e.g., largemouth bass in Figure 8.7). This pattern is consistent with noncentrarchid fishes (e.g., Driedzic et al . 1996). At present, some of the lowest resting heart beats recorded for teleost fish exist for largemouth bass (7.6 beats min−1 ) and black crappie (13.3 beats min−1 ), collected at 3◦ C (Cooke et al . 2003a). Both of these species exhibit ventricular hypertrophy and increase stroke volume at low temperatures to apparently maintain cardiac output (see discussion of cardiac morphology later). Exposing fish to changing temperatures—rather than stable temperatures as described earlier—can also provide valuable information on cardiovascular performance. The first study of that nature involved exposing individual largemouth bass

Physiology and organismal performance of centrarchids

237

to both increasing and decreasing temperatures over short periods (less than 1 h; Reynolds 1977a). The authors noted that heart rate (and ventilation rate) was greater for a given temperature during heating than cooling, suggesting a hysteresis. The hysteresis effect was most evident during use of the broadest temperature range (i.e. 12–32◦ C) and less so over narrower temperature ranges (i.e. 22–32◦ C, 17–32◦ C, and 12–22◦ C). Schreer and Cooke (2002) used cardiovascular approaches to understand how smallmouth bass responded to dynamic thermal conditions in a power-plant thermal effluent, and also revealed interesting findings relevant to basic cardiovascular physiology. The researchers determined that cardiac output was strongly coupled with water temperature and that these changes were driven almost entirely by heart rate. In fact, when temperature and heart rate are plotted over time, heart rate appears to mimic the same pattern of temperature (see Figure 8.6 in Schreer and Cooke 2002). To simulate fish swimming into and out of the effluent, the researchers switched the tank water supplies. Fish acclimated to the variable and high discharge water and exposed to effluent water exhibited stronger relationships between water temperature and both cardiac output and heart rate than fish from the thermally stable lake exposed to the effluent water. Additional experiments were conducted across four different ranges of temperature (4–14, 12–22, 12–26, and 18–28◦ C). The relationship between cardiac output and heart rate was strongest for fish in the lowest three temperature ranges. Interestingly, at the highest temperature range (i.e. 18–28◦ C), the relationship between cardiac variables and temperature became variable and independent. The authors concluded that the water temperatures had exceeded the thermal tolerances (i.e.> ∼24◦ C) of the smallmouth bass to the point that they were no longer able to physiologically adjust to thermal variation (but were still less than the thermal preferenda; see thermal biology later). The smallmouth bass were likely near maximal cardiac output and heart rate (∼120 BPM). In fact, the highest heart rate recorded for any centrarchid to date is just below 130 BPM (Cooke, unpublished data), consistent with salmonid literature and most other temperate fishes (Farrell and Jones 1992).

8.5.1.5 Exercise and cardiovascular performance

Oxygen consumption (mg kg−1 min−1)

Anaerobic exercise for fish results in a series of physiological changes that includes alterations in cardiovascular performance (Randall 1982; Kieffer 2000). In fact, these alterations are adaptive changes that are intended to provide oxygen to tissues and to accommodate the excess postexercise oxygen consumption. Exercise at sub maximal levels (i.e. aerobic) also results in increased cardiac output to deliver oxygen to working tissues as has been observed for smallmouth bass (Figures 8.8, 8.9; Cooke, unpublished data). In fact, Farrell suggests that exercise and organismal performance are limited by the ability of the myocardial oxygen supply and thus the ability of the heart to provide oxygen to working tissues (Farrell 1996, 2002; Farrell et al . 1996). Water temperature results in both an elevated resting cardiac output and heart rate, and it also affects organismal performance metrics, including swimming ability (Farrell 2002). As such, we will further explore the role of water temperature and exercise on cardiovascular physiology in centrarchids. When undergoing anaerobic exercise, both smallmouth bass (Schreer et al . 2001) and largemouth bass (Cooke et al . 2003b) exhibit a brief initial bradycardia followed by tachycardia. In these two species, cardiac output is increased primarily

12 10 8 6 4 2 0 40

45

50

55

60

65

70

75

Cardiac output (ml kg−1 min−1)

80 60

70

80

90

100

110

Heart rate (beats min−1)

120 0.4

0.5

0.6

0.7

0.8

0.9

Stroke volume (ml kg−1)

Figure 8.8 Relationship between cardiovascular activity and oxygen consumption for smallmouth bass exposed to forced swim trials at 24◦ C. Experiments were conducted on five adult smallmouth bass in Illinois. Fish were affixed with Doppler flow probes and introduced to a respirometer. Fish were exposed to a series of stepwise velocity increments during which time oxygen consumption and cardiovascular activity were monitored (Cooke, unpublished data).

Centrarchid fishes

80

120

70

110

60

100

50

90

0.80

Cardiac Output Heart Rate Stroke Volume

40

80 70

10

20

30

40

50

60

0.65 0.60 0.55 0.50 0.45

30 0

0.70

Stroke volume (m /kg−1)

0.75 Heart rate (beats min−1)

Cardiac output (ml min−1 kg−1)

238

70

0.40

80

Swimming speed (cm s−1)

Figure 8.9 Relationship between cardiovascular activity and swimming speeds for smallmouth bass exposed to forced swim trials at 24◦ C. Experiments were conducted on five adult smallmouth bass in Illinois. Fish were affixed with Doppler flow probes and introduced to a respirometer. Fish were exposed to a series of stepwise velocity increments during which time cardiovascular activity was monitored (Cooke, unpublished data).

due to increases in heart rate. In fact, stroke volume generally decreases. Elevated cardiac output during and after exercise can occur due to elevations in one or both of its components (Farrell and Jones 1992). Farrell (1991) suggested that there is an evolutionary trend from volume-modulated to frequency-modulated cardiac output. Evidence to date for centrarchid fishes suggests that they are frequency modulators, but to varying degrees. Cooke et al . (2003a) explored the evolutionary basis for frequency modulation through a comparison of white bass (Morone chrysops, a moronid), black crappie, and largemouth bass—largemouth bass increased cardiac output through a massive increase in heart rate (∼425%) despite a reduction in stroke volume; black crappie increased heart rate (∼225%), although stroke volume did not change; white bass increased heart rate to a lesser extent (∼140%), but stroke volume increased more (∼150%). These same changes are also evident during aerobic swimming trials (Figure 8.9; Cooke, unpublished data). Here, it is evident how smallmouth bass increase cardiac output in response to elevated heart rate, even though stroke volume decreases (Figure 8.9; Cooke, unpublished data). The magnitude of the reduction in stroke volume found in largemouth bass, black crappie, and smallmouth bass in response to anaerobic exercise is unique relative to salmonids and several other fishes (Farrell 1991). The majority of fish have a 40 to 60% contribution from stroke volume (Farrell and Jones 1992). Data from centrarchid fishes provides evidence that frequency modulation may be ubiquitous within the Centrarchidae family. Interestingly, the white bass that are classified taxonomically in the Percichthyidae (temperate bass family) are also members of the same order as the Centrarchidae [i.e. Order Perciformes (Percomorphi)], yet do not appear to be frequency modulators. In addition to the experiments conducted in laboratory settings, researchers have used heart rate telemetry transmitters to assess the response of free-swimming largemouth bass to exercise resulting from angling (Cooke et al . 2004a). In the laboratory, fish tend to be confined and are inactive (Cooke, personal observation). For this reason, field studies are more realistic because the fish are operating at basal levels and cardiac scopes that are reflections of routine metabolic rate, not standard metabolic rate as in the laboratory. Indeed, resting heart rates from largemouth bass in the field (i.e. Cooke et al . 2004a) were consistently higher than laboratory values collected by Cooke et al . (2003b), with the disparity as high as 44% (Figure 8.10). These data, which are rare for teleost fishes, suggest that greater efforts must be made to move from the laboratory to the field using biotelemetry techniques.

8.5.1.6 Summary of stressors The magnitude of cardiac disturbance associated with different stressors varies widely. Of course, rarely are study designs sufficiently compatible to enable direct comparisons. Nonetheless, here we briefly discuss the relative magnitude of different stressors on both the magnitude of cardiac disturbance (using heart rate) and cardiac recovery time (also using

Physiology and organismal performance of centrarchids

239

100 Doppler probes in lab

Heart rate (beats min−1)

80 60 40 20 100 Telemetry in field 80 60 40 20

0

60

120

180

240

300

Time (min)

Figure 8.10 Cardiovascular responses of adult largemouth bass exposed to exhaustive exercise and brief air exposure in either a laboratory or field environment. In the laboratory, heart rate was measured using Doppler flow probes (Data adapted from Cooke et al . 2003b; See photo of bass during the surgical procedure when the Doppler flow probe is attached; S. Cooke, Photo Credit). In the field, heart rate was measured using heart rate telemetry (Data adapted from Cooke et al . 2004a; See photo of telemetered fish, Credit S. Cooke). Additional detail on telemetry techniques can be found in Cooke et al . 2002a. The arrows on the graphs illustrate the time when the angling took place. (Blackwell Science—Journal of Applied Ichthyology).

heart rate). Comparisons of all resting cardiovascular variables for six centrarchid species for which cardiac data exist reveal the large degree of interspecific diversity (Table 8.4). In this case, resting rates vary by nearly 100% and responses to stressors range from depressions in heart rate (e.g., hypoxia) through to massive increases (e.g., low temperature exercise; Table 8.4). Similarly, recovery rates range from a few minutes to multiple hours (Table 8.4). In general, the level of interspecific variation at the generic or familial level in centrarchids is consistent with the level of variation observed in other noncentrarchid models such as salmonids (Farrell and Jones 1992). Most of the stressors that resulted in the highest disturbance magnitudes and longest recovery periods are stressors/ activities that are faced by fish on rare occasions. In the field, centrarchids may experience such levels of exhaustive exercise during riverine migrations, negotiation of fishways or obstructions, or when angled. Air exposure was also consistently one of the most deleterious stressors. Localized intermediate swimming activity, social interactions, and predator encounters are activities that are experienced more regularly by fish and elicited less extreme stress responses (as indicated by cardiovascular disturbance). Although avian predation attempts only require intermediate recovery periods relative to exhaustive exercise, predation attempts would likely be encountered more frequently. Although social interactions and low-speed swimming also elicit cardiac responses, the fish are able to recover very rapidly compared to predator attacks.

8.5.2 Cardiac morphology, histology, and biochemistry Little work has been carried out on the cardiovascular morphology of centrarchid fishes. The largemouth bass and smallmouth bass definitely possess a coronary artery and hence coronary circulation (Cooke, unpublished data). It is likely that this feature is ubiquitous within the centrarchid family. Superficially the heart appears to be of similar shape, size, and configuration to that of the well-studied salmonid heart (e.g., Farrell and Jones 1992). Also like salmonids (e.g., Driedzic et al . 1996), centrarchids experience ventricular hypertrophy (increased cell sizes) when acclimated to cold waters for extended periods. For example, Kent et al . (1988) studied the response of the hearts of green sunfish to different temperatures and revealed substantial ventricular hypertrophy as temperatures decreased (i.e. heart somatic

240

Centrarchid fishes

index = 0.065% at 25◦ C increasing to 0.090% at 15◦ C), coupled with an increase in protein content but not concentration. Conversely, when water temperatures were raised from 15 to 25◦ C, heart somatic index fell. More recently, Cooke et al . (2003a) revealed that relative ventricular mass was similar between black crappie and largemouth bass (∼0.1% of total body mass) at 3◦ C. Data from fish held at warmer temperatures (i.e. >12◦ C) reveal that relative ventricular mass for both these species tends to decrease to ∼0.07 to ∼0.08% of total body mass (Cooke et al . 2003b; Cooke 2002). Interestingly, Kolok (1992) observed that largemouth bass held at 5◦ C had lower heart somatic indices than did fish held at 20◦ C, and attributed this disparity to rapid somatic growth during the summer. He also reported that green sunfish did not exhibit ventricular hypertrophy (Kolok 1991). However, earlier studies by Kolok (1991) and Sephton and Driedzic (1991) revealed that smallmouth bass did exhibit ventricular hypertrophy during the winter. With the number of different species of centrarchids, unfortunately, it can be difficult to draw conclusions from different studies using disparate methodologies. To reduce the potential for this problem, Tschantz et al . (2002) tested the hypothesis that the physiological strategy for acclimating to low body temperature is similar among five centrarchids. Using largemouth bass, green sunfish, bluegill, black crappie, and white crappie acclimated to 5 and 25◦ C, they contrasted relative ventricular mass. All species exhibited ventricular hypertrophy but it was most evident in the two crappie species. Although there is sufficient evidence that centrarchids exhibit increases in relative ventricular mass with cold temperature (see exception in Kolok 1991), empirical evidence for the anticipated increase in stroke volume to maintain cardiac output is still somewhat rare. Perhaps the most compelling data are for largemouth bass where studies of cardiovascular function have been conducted at multiple temperatures ranging from 3 to 25◦ C. Indeed, such a pattern is observed and is presumed to be an important strategy to maintain cardiac output in the face of low heart rates (Farrell et al . 1996).

8.5.3 Intraspecific variation and cardiac plasticity There is a paucity of research on intraspecific variation in the cardiovascular physiology of fishes focusing on population level differences (see recent review by Gamperl and Farrell 2004). Interestingly, the only four published studies of any fish species that include direct analyses of population level differences in cardiovascular performance are for the pumpkinseed (Roberts 1967), largemouth bass (Cooke et al . 2003b; Cooke and Philipp 2005), and rock bass (Bunt et al . 2004). The first evidence for intraspecific variation in cardiovascular physiology was for pumpkinseed sunfish, using fish from a population in North Carolina and a population in Massachusetts (Roberts 1967). Roberts acclimated fish to water temperatures from 10 to 25◦ C and revealed that at low water temperatures (i.e. <20◦ C) heart rate was higher in fish from the northern population but at higher temperatures (i.e. >20◦ C) heart rate was higher in fish from the southern population. These data were preliminary and there is insufficient detail in the Roberts (1967) publication to provide rationale interpretation. A more recent assessment of intraspecific variation was presented by Cooke et al . (2003b), when they evaluated cardiovascular responses of largemouth bass to exercise across four water temperatures. The authors used fish from central Illinois for the two lowest temperatures (13 and 17◦ C) and fish from eastern Ontario for the two highest temperatures (21 and 25◦ C). Population (or site) was determined to contribute significantly to variation in resting heart rate and cardiac output and was used as a covariate in analyses. Bunt et al . (2004) contrasted the cardiovascular response of rock bass to graded silt concentrations and revealed that fish from a lacustrine population had a more variable response than a riverine population that was used to frequent silt pulses. However, neither of these two studies was explicitly designed to assess intraspecific variation. More recently, Cooke and Philipp (2005) provided data from a common garden experiment designed to explicitly evaluate the role of local adaptation in basic cardiovascular function, using two genetically distinct stocks of largemouth bass and their reciprocal hybrids. In that study, the cardiovascular response to exhaustive exercise among differentiated stocks of largemouth bass was compared at 10 and 20◦ C to assess phenotypic plasticity. In addition, the impact that interstock hybridization had on adaptive differences was assessed using F1 hybrids. To accomplish these assessments, four genetically distinct stocks of fish were produced using adults from two regions in the midwestern United States identified as distinct conservation management units (central Illinois, IL and southeastern Wisconsin, WI): both P1 stocks and both reciprocal F1 interstock hybrids. Cardiac variables (both resting and maximal) were consistently lowest for the IL × IL stock relative to the WI × WI stock and both F1 interstock hybrids. Interestingly, however, all groups of fish were able to maintain similar levels of cardiac scope. All fish responded to exercise by increasing heart rate and decreasing stroke

Physiology and organismal performance of centrarchids

241

volume, consistent with the notion that largemouth bass modulate cardiac output via frequency. After exercise, cardiac variables returned to resting levels about 30% more rapidly for IL × IL fish relative to all other groups at 20◦ C. At 10◦ C, recovery rates for both P1 stocks were similar but were more rapid than the interstock hybrids. Collectively, these results indicate that the locally adapted stock (IL × IL) exhibited cardiovascular adaptations that enabled rapid cardiovascular recovery and maintenance of low resting cardiac output and heart rate. Conversely, the translocated stock (WI × WI) and the interstock hybrids required longer for cardiovascular variables to recover after exercise and exhibited higher resting levels of cardiac output and heart rate. Their study provided the first evidence of clear intraspecific variation in cardiovascular performance. In addition to exploring variation in cardiovascular performance among populations, sex also represents another opportunity to explore intraspecific variation. To date, there have been few attempts to quantify sex-specific differences in cardiovascular physiology and even fewer that have revealed sex-specific variation (reviewed in Burggren 1999). In fact, most assessments have focused on morphological differences. The only quantitative sex-specific assessment among teleost fishes evaluating resting cardiovascular activity was by Cooke (2004). In that study, Cooke (2004) contrasted the resting cardiovascular performance (using Doppler flow probes) of male and female largemouth bass across three seasons and different reproductive states, including the spring when nesting males provide sole parental care. During the spring when largemouth bass were engaged in reproduction (at 21◦ C), parental male nesting fish had heightened resting cardiovascular rates (both cardiac output and heart rate) relative to nonnesting males and females. In the summer at slightly higher water temperatures (24◦ C), and in the autumn at water temperatures similar to the reproductive period (21◦ C), resting cardiovascular variables were similar among sex. The author concluded that although sex-specific differences in resting cardiac variables were evident it was not consistent across seasons. Differences were apparent during the reproductive period, and in particular for male fish actively engaged in the nesting phase of parental care, indicating a likely role of the endocrine system. The most striking pattern was that nesting male bass had elevated cardiac output and heart rate relative to both females and nonnesting males. Elevated cardiac output for nesting male bass would be advantageous during a period when fish are engaged in highintensity locomotory activity associated with defense and aeration (Cooke 2002). Elevated cardiac output may enhance the ability of parental male bass to respond rapidly to threats, provide enhanced oxygen delivery, and expedite clearance of metabolic by-products. Earlier comparative data from Cooke (2002) provided a comparison of six species of centrarchid fishes, focusing on nesting and nonnesting males (Figure 8.11). These data highlight the clear intraspecific differences evident for nesting and nonnesting fish (i.e. reproductive status). Similar to the detailed analysis of largemouth bass by Cooke (2004), nesting fish consistently had higher resting heart rates. These data also highlight the level of interspecific variation in resting heart rate evident among species, in this case corrected for the covariate water temperature to enable direct comparisons. As an example, nonnesting black crappie had resting heart rates that were roughly half that of nonnesting bluegill (Figure 8.11).

Resting heart rate (beats min−1)

120 Non-nesting Nesting 90

60

30 BC SMB RB

LMB

PS

BG

Figure 8.11 Comparison of temperature standardized resting heart rates of six species of nesting and nonnesting male centrarchid fishes: smallmouth bass (SMB), largemouth bass (LMB), rock bass (RB), pumpkinseed (PS), bluegill (BG), black crappie (BC). Data are adapted from Cooke (2002). Means (± SEs) were generated using ANCOVA using temperature as a covariate.

242

Centrarchid fishes

Variation in fish size within a species is another important component of intraspecific variation. In fishes, there have been few quantitative assessments of fish size when conducting studies on fish cardiovascular performance. Such analyses were imperative for the simulated predation experiment conducted by Cooke et al . (2003c) as they needed to determine if baseline cardiovascular function varied across fish of different sizes. When the authors plotted total length by resting cardiovascular variables (corrected to body size for cardiac output), they revealed that indeed there were no size-specific differences. Although a simple assessment, similar analyses do not exist for other fishes as most efforts have attempted to standardize sizes.

8.6 Thermal biology Since fish are ectothermic, changes in ambient water temperatures are realized throughout the animal, and can have pronounced impacts on cellular function (Prosser 1991), protein structure (Somero 1995), enzyme activity, diffusion rates, and metabolism (Fry 1971; Brett and Groves 1979; Farrell 1996; Kieffer et al . 1998). Temperature is also an important determinant of many behavioral attributes (Fry 1971; Ultsch 1989) and overall organismal performance. For centrarchids and other fishes, it also influences factors such as geographic range, spawning date (see Chapter 13), food consumption (Hathaway 1927; see Chapter 7), digestion rates (F¨ange and Grove 1979), growth (see Chapter 7), swimming abilities (see earlier) and activity (Malizia et al . 1984; Demers et al . 1996), winter biology (see Chapter 9), and habitat selection, and distribution (Neill and Magnuson 1974; Neill 1979; Armour 1993). Temperature can also be lethal at both low and high extremes. In fact, temperature plays such an important role that it has been termed the abiotic “master factor” (Brett 1971) and is typically viewed as an “ecological resource” and a fundamental component of an animal’s niche (Magnuson et al . 1979). Magnuson et al . (1979) contend that fish actually compete for temperature as a resource. With such extensive natural distributions, it is not surprising that centrarchid fishes have served as models for much research on thermal biology. Concern that arose from the proliferation of utilities that generated thermal effluent in the 1970s also spurred much research on this group of fishes (Beitinger et al . 2000). In fact, the vast majority of work on thermal relations of centrarchids is from that era (e.g., Coutant 1970, 1975b, 1977). Most chapters in this book discuss the role of water temperature to some extent. Here, we focus on aspects of thermal biology that are not discussed elsewhere in this book. We focus on the role of water temperature as the principal factor in determining how the centrarchid fishes interact with their environment and ultimately how temperature affects survival, fitness, and distribution.

8.6.1 Thermal tolerances and the Fry paradigm As outlined by Coutant (1975a), the responses of fish to temperature vary across different life stages (e.g., eggs, larvae, adults), so no single temperature can be viewed as good or bad. Instead, the temperature must be viewed in the context of the life stage as well as the activities that the organism is trying to perform. Early life history relationships between water temperature and survival are presented elsewhere in this book (see Chapter 5). Here, we focus on adult thermal tolerances. We use the Fry paradigm to generally structure our discussion. Fry classified physical and chemical aspects of fish habitat as (i) lethal, (ii) controlling, or (iii) directive, based on how they influence fish (Fry 1947, 1971). In this context, extreme temperatures can kill fish and would be viewed as lethal. When not at extremes, temperature can control developmental and physiological rates and processes (i.e. metabolism) of fish. Temperature can also direct the position or habitat preference of an individual fish (i.e. orientation response). Fry’s paradigm also included another group of factors commonly referred to as “limiting” such as those that are in short supply (e.g., oxygen) or others that are “masking” the influence of other environmental factors. The Fry paradigm has become an important component of fisheries management (Loftus 1976).

8.6.2 Lethal temperatures In general, survival in response to extreme temperatures (either high or low) depends on three primary factors. (i) the initial acclimation or holding temperature, (ii) the exact test temperature, and (iii) the duration of exposure to the test

Physiology and organismal performance of centrarchids

243

temperature (Hart 1952). Other factors such as individual variation in energy stores, parasite/disease burdens, reproductive state, and so on can also play a role in temperature related mortality but these effects are typically manifested over longer periods (see Chapter 9 on Winter Biology as an example). Obviously when acting as a lethal factor, temperature has the most dramatic effects (Fry 1947). This area of research is replete with examples for numerous marine and freshwater species, including many of the centrarchid fishes. Methods used to determine thermal tolerances are critically reviewed in Becker and Genoway (1979) and Beitinger et al . (2000). Briefly, the three most common techniques used are the incipient lethal temperature (ILT), critical thermal (CTM) and chronic lethal (CLM) methods. They all involve time and temperature as major test variables but they do not quantify the same response. The ILT technique involves plunging fish from a variety of acclimation temperatures into a series of constant test temperatures near the estimated upper and lower limits for the species (Fry 1947). Mortality is the endpoint and recorded over time, usually looking at when 50% of fish are moribund. CTM involves exposing fish that are usually acclimated to specific temperature(s) to a constant linear change in temperature until a near lethal endpoint is reached. The endpoint is determined when locomotory movements are impaired and represents the CTminima or CTmaxima. The CLM involves exposing fish to dynamic temperature changes of 1◦ C/day or slower until death is observed. All methods can be conducted to determine the maximum or minimum tolerances. The different methods generate disparate but generally similar values. Using data for largemouth bass (i.e. Currie et al . 1998), Beitinger et al . (2000) suggest the following general sequence for upper tolerances: ILT < CLM < CTM. Overall, CTM measurements are generally regarded as the most realistic and have other advantages relative to CLM and ILT (Beitinger et al . 2000). In their review, Beitinger et al . (2000) provided a synthesis of CLM and CTM studies and concluded that 22 species or hybrids had CTmaxima that exceeded 40◦ C, of which five were centrarchids (bluegill, Florida largemouth bass, largemouth bass) and their hybrids (M. floridanus × M. salmoides and their reciprocal cross). Since then, longear sunfish have also been determined to fall into this category (see Dent and Luttershmidt 2003). We also located CTmaxima data for three species that were not included in the review of Beitinger et al . (2000; i.e. rock bass, white crappie, and black crappie—all reported in Reutter and Herdendorf 1976). To date, CTmaxima have been experimentally determined for only 13 species, 2 subspecies (of which Florida largemouth bass have now been elevated to species status), and on 2 hybrids. This compares with only one species examined for CLM. CTmaxima values range from a low of 29.2◦ C for largemouth bass to a high of 41.8◦ C for Florida largemouth bass (Figure 8.12). Interestingly, the CTmaxima of fish in the family Centrarchidae span a range of 12.6◦ C compared to a range of 8.1◦ C for the family Salmonidae. In fact, the highest CTmaxima for all salmonids is about one-third that of the family Centrarchidae. CTminima has also been determined on an infrequent basis (only two species) relative to CTmaxima. In both cases, CTminima varied extensively with acclimation temperature and were as low as 1.7◦ C for bluegill acclimated to 15◦ C (Becker et al . 1977), and 3.2◦ C for largemouth bass acclimated to 20◦ C (Currie et al . 1998). In some cases, fish acclimated to cold temperatures and then provided with a thermal gradient explore temperatures that are beyond their CTmaxima resulting in mortality, particularly among juveniles. Such patterns have been observed for smallmouth bass (Barans and Tubb 1973) and bluegill (Beitinger and Magnuson 1976) and this phenomenon is referred to as “low thermal responsiveness.” We have not listed all of the thermal tolerances for centrarchid fishes and instead refer readers to the synthesis of Beitinger et al . (2000) and more importantly, the original sources. We must reiterate that although CTM approaches were used in all cases, differences in acclimation temperature and test endpoints can influence findings. Similarly, the sample sizes (both within studies and total number of studies) vary extensively among species. Thus, consultation of original sources is essential, especially if data are being used for regulatory or policy purposes. There are only three thermal tolerance studies of centrarchids with which we are familiar that have been published since the Beitinger et al . (2000) review. Schaefer et al . (1999) contrasted CTmaxima of longear and bluegill sunfish during both summer and winter. In the summer, bluegill consistently had CTmaxima higher than longear sunfish—which were all higher than CTmaxima recorded in the winter. In the winter, differences between species were less apparent. In another study on the same two species, Dent and Lutterschmidt (2003) found no interspecific differences in CTmaxima, but bluegill tended to have greater thermal plasticity (i.e. variance). The final study on this topic published since Beitinger et al . (2000) was by Currie et al . (2004). The researchers exposed some largemouth bass to a 10◦ C-diel thermoperiod and others to stable temperatures. The researchers determined that the diel thermoperiod CTminima and maxima were more similar to those determined at intermediate acclimation temperatures than to the lowest or highest acclimation period. Overall, exposure to diel thermoperiod did not enhance thermal tolerances as hypothesized by the authors.

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P. nigromaculatus Salmonidae

Figure 8.12 Critical thermal maxima data for centrarchid fishes. The lines for each species extend from the extremes (i.e. highest CTMax and lowest CTMax) for all data that we could locate. Data were compiled from a number of syntheses and original sources. Grouped salmonid data are also provided for comparison. [Data sources: Spotila et al . (1979), Reutter and Herdendorf (1976), Schaefer et al . (1999), Dent and Lutterschmidt (2003), Currie et al . (1998), Wismer and Christie (1987), Beitinger et al . (2000), Fields et al . (1987).]

Some attempts have been made to develop generic temperature tolerance criteria, which in practice may be helpful in cases where data are deficient. For example, Mathur et al . (1983) developed a statistical analysis from laboratory data to predict avoidance temperatures of fish including seven species of centrarchids. The authors determined that species within each family (including centrarchids) showed similar avoidance temperatures and that acclimation temperature was the most significant predictor variable. However, this approach fails to consider that there may be substantial intraspecific variation. For example, Fields et al . (1987) reported that critical and chronic thermal maxima varied among genetically distinct populations of largemouth bass.

8.6.3 Preferred temperatures Centrarchid fishes have long been the focus of work on thermal preferences. Unfortunately, the data are rather sporadic and tend to provide few opportunities for direct comparisons. When exposed to a gradient of thermal conditions for a short period (hours), fish will select a specific set of temperatures known as the preferred temperature (Wismer and Christie 1987). These short-term preferences for temperature are highly dependent upon acclimation temperature (Cherry et al . 1977). If provided with an infinite temperature gradient and if monitored for long periods (days to weeks), fish select a temperature that is known as the final temperature preferendum (Fry 1947; Giattina and Garton 1982). Due to the longerterm nature of final temperature preferenda, acclimation temperature is not as important as when determining short-term thermal preferences. Due to differences in methodology among studies, it is sometimes unclear whether data reported as final preferenda are indeed that, or are simply a temperature preference point for a single acclimation temperature. Because of the strong dependence of thermal preferences on acclimation temperature, it is very difficult to draw comparisons among species unless their preferences are examined across the same range of acclimation temperatures and provided with the same thermal selection gradient. In addition, variation in thermal preferences can be associated with experimental apparatus, age of fish, and seasonal conditions (Coutant 1975b). Data on thermal preferenda are more common that–quantitative data on

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lethal temperatures. In fact, even some of the less economically valuable species of centrarchid fishes have experimentally determined values (e.g., bluespotted sunfish, Enneacanthus gloriosus; Casterlin and Reynolds 1979; Stauffer 1981). One of the few studies that provides comparative data for several centrarchid (and salmonid) species is Cherry et al . (1977). The authors exposed rock bass, bluegill, spotted bass (Micropterus punctulatus), and smallmouth bass to a range of standardized acclimation temperatures and thermal gradients. In general, thermal preferences increased with acclimation temperatures until acclimation temperatures reached 30◦ C. As the fish approached lethal temperatures (i.e. >30◦ C), preferences decreased. For all the centrarchids the authors evaluated, final thermal preferenda were near 30◦ C. In the same study, the authors found that salmonids (i.e. rainbow trout, brook trout, and brown trout) all had final thermal preferenda that were more than 10◦ C lower (i.e. <20◦ C) than centrarchids. We generated a figure that illustrates the range of final thermal preferenda for all centrarchid fish for which they exist (see Figure 8.13). In general, the final thermal preferenda are between 28 and 32◦ C with few exceptions. This contrasts with the substantially lower thermal preferenda of salmonids (see Figure 8.13). What is particularly interesting is the general conformity of all species to a rather narrow range of preferred temperatures. There are of course several exceptions (e.g., bluegill and pumpkinseed, both >6◦ C range), which is actually unusual among all fishes. Perhaps this is because these species have had thermal preferenda determined more times than the other species. Magnuson and Beitinger (1978) also concluded that temperature preference of centrarchids represented a species-specific characteristic that varies little within the family. In fact, some researchers have concluded that final preferendum is a stable characteristic for each species, suggesting strong regulation by natural selection (Beitinger and Fitzpatrick 1979). For centrarchid fishes, there tends to be a positive correlation between acclimation and selected temperatures (Hill et al . 1975), not just final preferenda. Although relatively minor, much of the variation observed in the existing final thermal preferenda data tend to reflect differences associated with how the values were determined (in particular acclimation temperatures and methods of measurement). The variation may also reflect inter- (and even intra-) specific differences in thermal tolerances and optima, but at present there are few studies (but see Cherry et al . 1977) that enable this to be explicitly determined (despite the conclusions of Beitinger and Fitzpatrick 1979 and Magnuson and Beitinger 1978). Early research suggested that species

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Figure 8.13 Final thermal preferenda data for centrarchid fishes. The lines for each species extend from the extremes (i.e. highest final preferenda and lowest final preferenda) for all data that we could locate. Data were compiled from a number of syntheses and original sources. Only studies in which fish were provided with ample time to determine final preferenda were utilized. We excluded all but adults. Note that final preferenda for some species are for very few fish and/or a single study (e.g., white crappie). Grouped salmonid data are also provided for comparison. [Data sources: Spotila et al . (1979), Reutter and Herdendorf (1976), Beitinger and Magnuson (1976), Cherry et al . (1975), Cherry et al . (1977), Neill and Magnuson (1974), Casterlin and Reynolds (1979), Reynolds and Casterlin (1976), Magnuson and Beitinger (1978), Wismer and Christie (1987), Koppelman et al . (1986), Bennett (1965).]

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with wide geographic distributions, such as bluegill and largemouth bass exhibit constant laboratory final preferenda regardless of their geographic origin or thermal histories (Beitinger and Fitzpatrick 1979; Reynolds and Casterlin 1979; Danzmann et al . 1991). Indeed, research has generally confirmed this pattern. For example, largemouth bass populations from different geographic regions did not exhibit differences in thermal preferenda (Koppelman et al . 1988) despite fish from these same populations having different chronic thermal maxima (Fields et al . 1987; see earlier). Mathur et al . (1981) found strong similarities among the thermal preferenda of many freshwater fish including centrarchids. Within the centrarchids, there was a remarkable relationship between preferenda of different species. Although this is informative, there is much room for additional research on thermal plasticity and intraspecific variation in thermal preferenda. It is not possible to fully appreciate whether generalities are appropriate for centrarchids or other species of fish due to the scarcity of data. Individual differences in thermal preferenda have also been noted (e.g., Beitinger et al . 1975) but are rarely reported (e.g., usually means and error estimate rather than range). Despite being of similar size and exposed to similar experimental conditions, Beitinger et al . (1975) noted a range of 3C among individual preferenda for green sunfish. Other factors can also affect thermal preferenda including sociobiology, fish size, season, and photoperiod. In a study of social dominance, Beitinger and Magnuson (1975) found that social rank influenced temperature selection of bluegills. Dominant individuals selected warmer temperatures near their thermal preferenda while subordinate individuals were relegated to cooler temperatures. A similar study on bluegill by Medvick et al . (1981) yielded similar results and the authors concluded that temperature can influence selection of bluegill territories, and at low densities social behaviors can exclude subordinate fish from preferred water temperatures. Several studies have evaluated the role of fish size on thermal preferences with disparate results. Beitinger and Magnuson (1975) found no relationship between length and final preferenda for bluegill. However, Barans and Tubb (1973) found size-specific differences in thermal preferenda for smallmouth bass. It is also well known that thermal preferenda can vary among seasons (e.g., Barans and Tubb 1973), emphasizing the importance of acclimation temperature and conditions when determining final preferenda. For some species (e.g., largemouth bass and smallmouth bass), thermal preferenda vary on a diel basis (Reynolds and Casterlin 1978a), but for others such as bluespotted sunfish (Reynolds and Casterlin 1979) and green sunfish (Beitinger et al . 1975), they do not. Reynolds and Casterlin (1978a) determined that the thermoregulatory rhythms of largemouth bass and smallmouth bass differed over the diel photoperiod (12:12) cycle. While smallmouth bass exhibited a peak in thermal preference at the end of the photophase, that time coincided to the lowest thermal preference for largemouth bass. The authors conclude that this may serve to segregate niches of these often sympatric species in support of the thermal niche concept proposed by Magnuson et al . (1979).

8.6.3.1 Correlates of preferred temperature Preferred temperatures, as discussed earlier, tend to be stable within species suggesting strong regulation by natural selection (Beitinger and Fitzpatrick 1979). It is therefore not surprising that there are a number of clear ecological correlates of preferred temperature (Magnuson et al . 1979). In fact, for the well-studied sockeye salmon, Brett (1971) has demonstrated that the majority of physiological processes are optimized at the final thermal preferenda. More recent work on centrarchid fishes has revealed that this is also the case for centrarchids. Coutant (1975a) suggested that feeding rate, growth rate, metabolism, and swimming speed of largemouth bass are all maximal between 25 and 30◦ C, coinciding with their thermal preferendum. The same patterns were also evident for smallmouth bass, but there were fewer data available. Also interesting is the observation that in the wild, some species spend very little of their time at temperatures that fall within their preferred temperature ranges as a function of constraint from available temperatures. Magnuson and DeStasio (1996) illustrated this succinctly for largemouth bass across the United States. The authors concluded that largemouth bass occupy suboptimal thermal habitats for much of the year. In fact, in some regions, fish may not ever experience preferred temperatures. Here, we briefly summarize the correlates of preferred temperature in centrarchids, as well as explore the factors that can lead to the selection of suboptimal thermal environments in favor of some other resource. Growth rates assuming no feeding limitations tend to be higher at or below thermal preferenda (e.g., bluegill, Beitinger and Magnuson 1979). When provided with near unlimited food resources, centrarchids will typically select temperatures that exceed their thermal preferenda (e.g., Bevelhimer 1996). Consistent with this finding, Danzmann et al . (1991) reported that the catchability of five of six species (bluegill, pumpkinseed, black crappie, largemouth bass, smallmouth bass, exception was rock bass) of centrarchids that they studied in Lake St Clair was greatest in water warmer than their thermal preferenda. The relationship between water temperature and growth is complex and is discussed in more detail

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in the chapter on bioenergetics (see Chapter 7). Sometimes centrarchids will occupy areas that are beyond their thermal preferenda and approaching their thermal maxima in favor of other factors. For example, in South Carolina, dying and dead bluegills from a heated reservoir were eaten by largemouth bass, which swim into effluent temperatures as high as 46◦ C to consume these easily caught prey items (Janssen and Giesy 1984). Thus, largemouth bass distributions are affected by the presence of food rather than by temperature. Cooke et al . (2000, 2004b) found a similar pattern in smallmouth bass in Lake Erie where fish resided in a thermally challenging environment (i.e. thermal effluent) but did so because the effluent provided complex habitat features and abundant forage. Although both food and habitat can influence thermal habitat selection of centrarchids (Neill and Magnuson 1974), Beitinger and Magnuson (1975) conclude that social factors (i.e. intraspecific agonistic behaviors) can be more important in determining centrarchid distribution in the wild. Fish are believed to exhibit their highest critical swimming speeds at their preferred temperatures and this has been documented for both salmonids (e.g., Farrell 1996, 2002; Lee et al . 2004) and centrarchids (Kelsch and Neill 1990). Researchers have been interested for some time in discovering as to why fish select temperatures that are optimal for performance. Research on salmonids suggests that consistent with preferred temperatures and optimal swimming performance is maximum aerobic scope (i.e. the position on the scope for activity where there is the largest disparity between standard metabolic rate and maximal metabolic rate; Fry 1947). Not only does this hold across species (e.g., rainbow trout, Farrell 2002), but it can also be found among different populations (e.g., sockeye salmon; Lee et al . 2003a,b). Below and particularly above the preferred temperature, performance is constrained. As discussed in the section on cardiovascular physiology, it is believed that myocardial oxygen supply becomes limited above preferred temperatures and is responsible for constrained performance in salmonids (Farrell 2002). Unfortunately, there is not as complete a picture for centrarchids or any other group of fishes relative to the salmonids. Kelsch (1996) proposed a similar explanation to explain why fish perform optimally at preferred temperatures using bluegill as a model. Although he used the terminology “available power” (Ware 1982), he was in essence also attempting to correlate performance with maximum scope. Indeed, he noted that critical swimming speeds of bluegill reflected the frequency with which temperatures were selected. Earlier modeling exercises using bluegill also suggested that preferred temperatures were those that maximized surplus power (or scope; Bryan et al . 1990). Coutant (1975a) perhaps developed the most complete picture of the relationship between metabolic scope, performance, and temperature by visualizing data on largemouth bass from several researchers. He clearly illustrated that fish performance was maximal near the final thermal preferendum where scope was also highest. Above that temperature, scope and performance declined. Research on other organ systems is also suggestive of the fact that physiological processes tend to be optimal at or near the final preferendum. For example, Fuhrman et al . (1944) determined that the metabolism of the brain of exercised largemouth bass was optimal at 35◦ C, a temperature near their thermal preferendum. Above 35◦ C, the brain oxygen requirements fell perhaps associated with the limitations in cardiovascular performance identified by Farrell (2002). Fuhrman et al . (1944) also measured ammonia levels in the brain and revealed that as temperature rose above 35◦ C, ammonia concentrations production rose dramatically. In another example, swim bladder inflation and associated buoyancy regulation may also exhibit optimal performance near the final preferendum. McNabb and Mecham (1971) reported that swimbladder oxygen secretion rates (for filling) increased with increasing temperatures up to 32◦ C for bluegill. Interestingly, total gas secretion was temperature independent. This obviously is also connected to the cardiorespiratory system and gas transport dynamics.

8.6.4 Behavioral thermoregulation One of the remarkable findings is that fish possess acute thermal discrimination abilities and will adjust their behavior to avoid hostile areas in favor of more hospitable areas provided they exist (Neill and Magnuson 1974). In fact, research has suggested that some fish are capable of detecting differences in temperature as subtle as 0.03◦ C (Bull 1936). Much of the research that determined precisely how fish were able to detect differences and behaviorally thermoregulate (i.e. select temperatures and associated microenvironments that are less variable than the ambient water temperature) was done using centrarchid fish as models. Thermoregulatory behavior requires peripheral and central thermoreceptors to monitor sensory input (Crawshaw et al . 1990), which is processed and integrated in the preoptic anterior hypothalamus (Crawshaw 1980). Indeed, preoptic neuronal recordings from green sunfish revealed that 17% of cells were warm-sensitive whereas only 2% were cold-sensitive and

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that the cells were randomly dispersed (Nelson and Prosser 1981a,b). In another experiment, Nelson and Prosser (1979) used green sunfish acclimated to 5, 15, and 25◦ C. When placed in a horizontal temperature gradient from 2 to 30◦ C where they could swim freely, the fish tended to behaviorally select temperatures near their acclimation temperature and maintain relatively constant body temperatures. The researchers then created bilateral medial and lateral preoptic lesions that led to random fish distribution and variable body temperatures confirming the important role of this part of the neural anatomy of the fishes for thermoregulation. When fish detect changes in temperature, they often respond behaviorally by moving to other regions with more favorable thermal conditions (Neill and Magnuson 1974). Under natural scenarios, these temperature changes are usually sufficiently slow that fish can acclimate (e.g., seasonal changes as discussed later). However, water is not always well mixed (e.g., in a lotic system) or is stratified (e.g., in a lentic system). Furthermore, human influence in the form of point source pollution (e.g., thermal generating station effluents) can also expose fish to thermal variation and rapid temperature change. All of these scenarios can provide fish the opportunity to choose the specific thermal environment that they wish to occupy. Obviously, these thermal resources change both spatially and temporally. If temperature changes too quickly and fish are unable to locate appropriate thermal refugia, sublethal physiological disturbances or mortality can occur. For example, Power and Todd (1976) used territorial groups of pumpkinseed and exposed them to increasing water temperatures. The authors noted that social behavior remained unchanged until temperature approached lethal temperatures (30–38◦ C). On the other hand, ritualized behaviors increased in frequency with rising temperature but decreased near lethal temperatures. Seasonal influences on organismal physiology are largely influenced by water temperature and require acclimatization. There are a reasonable number of studies that evaluate seasonal changes in metabolic rate (see discussions earlier) and general activity. Here, we focus briefly on topics not specific to bioenergetics or winter as they are discussed elsewhere. For example, Shaklee et al . (1977) monitored enzyme activity and isozyme patterns of green sunfish exposed to seasonal differences in temperature to understand the molecular aspects of temperature acclimation. The authors determined that there were few changes in isozyme repertories, which accompanied the thermoacclimatory responses of green sunfish. In another example, Dehn et al . (1992) evaluated seasonal adenylate energy metabolism in redear sunfish. Levels of muscle and liver adenylates, phosphocreatine, total adenylates, and the adenylate energy charge exhibited significant seasonal changes in the redear sunfish.

8.6.5 Body temperature Being ectothermic organisms, it is reasonable to assume that the body temperatures of centrarchid fishes are a direct function of water temperature. However, as we learn more about the thermal biology, it has become clear that the body temperature of fish in stable water temperatures is anywhere from 0.1 to 1.0◦ C warmer than ambient water temperatures. This disparity between fish temperature and water temperature is referred to as “excess temperature” (Stevens and Fry 1970). Such relationships have now been documented for largemouth bass (Cooke, unpublished data). In regions with variable temperatures, body temperatures of fish can vary widely. Some of the most complete data on body temperatures of fish are generated using centrarchid models. This topic is relevant to behavioral thermoregulation because Neill and Magnuson (1974) suggested that thermoregulatory behaviors of fish in response to spatial and temporal temperature variations are based upon sensory capabilities that compare external ambient thermal conditions to core body temperature. Early studies measured body temperatures of fish following capture. For example, Bennett (1979) measured the internal body temperatures of largemouth bass in a heated effluent in a reservoir and contrasted those with temperatures recorded from bass in a nonheated region. Not surprisingly, bass from the heated area had body temperatures that were ∼10◦ C higher than that of the bass from the nonheated area during December through March. Thermal disparities in the spring and early summer were about 1 to 3◦ C in heated areas, whereas in the summer body temperatures were similar between areas. The highest body temperatures reported by Bennett (1979) were 36.2◦ C in heated and 31.4◦ C in nonheated areas. Telemetry techniques have provided more detailed information on body temperatures of fish in the wild. For example, Siler and Clugston (1975) monitored body temperatures of free-swimming largemouth bass in a heated reservoir using tempsensing ultrasonic and on one occasion recorded a body temperature as high as 35.6◦ C. Earlier work by Coutant (1975b) also provided information on the distribution and thermal biology of largemouth bass.

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Information on relationships between biological characteristics and thermal biology may be useful for understanding responses or exposure to thermal pollution and general environmental relations. However, it is well known that the body temperature of a fish is not an effective measure of residency time in different thermal environments (such as a thermal effluent) because the time for temperature equilibrium is influenced by a number of factors. One of the most obvious factors associated with body temperature of fish is body size. Cox (1974) reported that large bluegill lost equilibrium when exposed to high temperatures more rapidly and at lower temperatures, than small bluegill. Similarly, Fechhelm and Neill (1982) reported no significant relationship between body size and lag time for bluegill. The finding of Cox (1974) and Fechhelm and Neill (1982) on bluegill contrasts with more recent data on largemouth bass that suggest that there are clearly lags in body temperature equilibration with water temperature, particularly in larger-bodied individuals (e.g., Reynolds 1977a; Bennett 1979; Weller et al . 1984). For example, Bennett (1979) reported that body weight was negatively correlated with body temperatures of largemouth bass from heated and nonheated areas of a thermal cooling reservoir. Condition factor was also negatively correlated with body temperature but only in the heated area. A series of modeling exercises have also been attempted to understand the role of size on body temperature better. The first was by Erskine and Spotila (1977) who conducted a heat energy budget analysis for largemouth bass. Their efforts focused on studying the role of conductance on heat transfer and concluded that direct heat transfer between the body surface and the water was the primary avenue for change in body temperature. Interestingly, they did not observe an effect of body size, but only used aluminum castings of largemouth bass body shapes. Kubb et al . (1980) developed a timedependent model for describing heat transfer in largemouth bass. Model sensitivity analysis indicated that body diameter, insulation thickness, and tissue thermal conductivity were controlling variables in the transfer of heat between a fish and water. Interestingly, fish metabolic rate and water velocity across fish surfaces did not appreciably affect heat transfer rates in their experiments. Kubb et al . (1980) also found that the midgut region exchanged heat at the slowest rate and the heart region exchanged heat at the fastest rate. A more recent model of heat exchange rates was developed by Weller et al . (1984), also for largemouth bass. That model incorporated an initial time lag into Newton’s law of cooling. Although the authors found significant relationships between body size and rate of temperature exchange, nearly 20% of the variance was unexplained suggesting that there are indeed other variables beyond body size, such as the role of the circulatory system, that contribute to determine thermal exchange characteristics. Indeed, the cardiovascular physiology/activity of the individual fish has been recognized as an important characteristic in influencing the body temperature of bluegill (Stauffer et al . 1975). Overall, it appears that body size is important, but not the sole predictor of heat transfer rates or body temperature in fish. Other factors can also affect body temperature of fish. For example, diel rhythms of body temperature are common in most vertebrates including largemouth bass (Reynolds et al . 1976). However, other research on the confamilial bluegill revealed that they do not exhibit such rhythms (Reynolds and Casterlin 1976). A more detailed study placed bluegill in a thermal gradient and exposed them to a natural photoperiod (Crawshaw 1975). Dorsal muscle temperatures of bluegill exhibited relatively constant body temperature (independent of photic conditions) despite being more active during the day (Crawshaw 1975). The direction of temperature change can also influence body temperature and the rates of thermal exchange. For example, Weller et al . (1984) reported that largemouth bass exchanged heat at a faster rate while warming than when cooling and their argument was supported by other field and laboratory experiments (e.g., Stauffer et al . 1975, bluegill; Reynolds 1977a, largemouth bass). Interestingly, this finding was contrary to the modeling results reported for largemouth bass by Kubb et al . (1980). Some bacterial diseases change the thermoregulatory behavior of centrarchids by increasing their thermal preference and hence body temperature (e.g., bluegill; Reynolds 1977b). Presumably this “behavioral fever” may enhance their immune response to pathogens (Kluger 1978).

8.6.6 Synergistic effects of temperature Temperature has been widely recognized as having strong interactive effects with other stressors. On its own, the temperature or other stressor may not be overly deleterious. But when these factors interact, they can have more dire consequences and magnified effects. To date, much of the research on this topic has occurred using rainbow trout and has focused on the interactive effects of water temperature and other pollutants. In a review, Morgan et al . (2001) reported that when rainbow trout were nearing their CTmaxima, they were more succeptible to minor toxicant challenges. In fact, temperature can not

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only magnify effects of pollutants, but can also lead to more rapid clearance or change the actual properties of the pollutant. At present, there have been comparatively few studies on the interactive effects of water temperature and pollutants on centrarchids (but see brief review on black bass by Bulkley 1975). Cember et al . (1978) evaluated mercury bioconcentration in bluegill relative to different water temperatures and mercury concentrations. Interestingly, the bioconcentration factor increased exponentially with water temperature but not with mercury concentration in the water. In a review of the interactive effects of chlorinated biocides on fish in the Laurentian Great Lakes, Cooke and Schreer (2001) determined that temperature played a key role in chlorine toxicity for centrarchid fishes. For example, Seegert et al . (1979) reported that there was an inverse relationship between temperature and median lethal (LC50) concentrations of monochloramine for bluegill. In fact, LC50 values decreased by a factor of two as the exposure temperature increased from 10 to 30◦ C. Such synergistic relationships are rather common between temperature and contaminants, but more detailed examination is beyond the scope of this chapter.

8.7 Conclusions This contribution represents the first synthesis on the physiology, performance, and environmental tolerances of the centrarchid fishes. Although we were able to find several examples on most of the key topics we wished to cover, rarely were we able to find sufficient information to develop the level of understanding that exists for other fishes, such as the salmonids. This means that there is ample opportunity for greatly expanded research on centrarchid species. It is our hope that synthesizing the available information will help to elucidate future questions. Furthermore, we hope that this contribution will provide context and baseline information that will make it easier for those considering using centrarchid models. There are a number of general patterns that are evident within the centrarchid fishes. In fact, the most substantial and poignant pattern was that it was quite difficult to make generalizations because centrarchids are so diverse. There is extensive variation at all physiologically relevant levels. For example, interindividual differences in swimming performance (Kolok 1992) and resting cardiac output (Cooke 2004) are evident for centrarcid fishes. We also observe extensive intraspecific variation among populations. For example, largemouth bass populations are locally adapted and exhibit differences in cardiovascular physiology (e.g., largemouth bass; Cooke and Philipp 2005), swimming performance (e.g., largemouth bass; Cooke et al . 2001a), stress response (rock bass; Bunt et al . 2004), and critical thermal maxima (Florida largemouth bass, largemouth bass; Fields et al . 1987). Among animal biology, centrarchid fishes have also been used as a classic example to contrast differences at the subspecies level. For many years it was believed that Florida largemouth bass was a subspecies of the northern largemouth bass (Williamson and Carmichael 1990) with many comparative studies of stress responses (Williamson and Carmichael 1986), thermal tolerance (Carmichael et al . 1988), and hypoxia tolerance (Carmichael et al . 1988). More recently, however, it has become evident that Florida largemouth are actually a distinct species (Kassler et al . 2002) and thus these data provide information on interspecific differences. There are other comparative studies at the species level that focus on comparisons within and among genera. For example, there has been some work conducted on the physiological performance of sympatric lepomids, such as longear and bluegill sunfish (Schaefer et al . 1999). One of our objectives was to draw comparisons among the salmonid and centrarchid fishes where appropriate. This approach yielded some fascinating insight. For example, the thermal preferences (i.e. final thermal preferenda) and thermal tolerances (i.e. critical thermal maxima) are substantially lower for salmonids than centrarchids. In fact, the salmonid and centrarchid values barely overlap. Another important difference among centrarchid and salmonid fishes is how they regulate cardiac output. Centrarchids appear to be primarily cardiac frequency modulators (e.g., Schreer et al . 2002) whereas salmonids are volume modulators (Farrell 1991). Interestingly, centrarchid fishes and salmonid fishes have comparable swimming performance. This is surprising considering that salmonids are often considered the athletes among the fish world. Although it is unlikely that any of the centrarchid fishes will ever replace the rainbow trout and become the “white rat” of the fish physiology world, it is reasonable to think that work on these fishes will expand. As early as the 1960s, green sunfish were being used as a model for work on thermal ecology and enzyme activity (see Shaklee et al . 1977). In the 1970s, bluegill became a popular model for pollution assessments (see Mayer and Ellersieck 1986), and are actually

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one of two standard models for toxicological testing of pesticides in Canada and the United States (interestingly rainbow trout is the coldwater model). In today’s interdisciplinary research environment, we see much opportunity for ecologists, behavioralists, and physiologists to work collectively on centrarchid model systems. In fact, with a growing recognition that there is a direct link between physiology and life history (Ricklefs and Wikelski 2002), centrarchids may in fact serve as a key model. Furthermore, fisheries managers are becoming more dependent on the type of information that physiology can provide on topics such as the sublethal effects of catch and release (e.g., Gustaveson et al . 1991; Kieffer et al . 1995) or minimizing stress of cultured fish transported for release from supplementation programs (e.g., Carmichael et al . 1983, 1984b).

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Spotila, J., K. Terpin, R. Koons, and R. Bonati. 1979. Temperature requirements of fishes from eastern Lake Erie and upper Niagara River: a review of the literature. Environmental Biology of Fishes 4: 281–307. Stauffer, J. R., Jr. 1981. Temperature behavior of the bluespotted sunfish Enneacanthus gloriosus (Holbrook), with an evaluation of the interpretation of thermal behavior data. Water Resources Bulletin 17: 504–507. Stauffer, J. R., K. L. Dickson, A. G. Heath, G. W. Lane, and J. Cairns, Jr. 1975. Body temperature change of bluegill sunfish subjected to thermal shock. The Progressive Fish Culturist 37: 90–92. Steffensen, J. F., J. P. Lomholt, and K. Johansen. 1982. Gill ventilation and O2 extraction during graded hypoxia in two ecologically distinct species of flatfish, the flounder (Platichthys flesus) and the plaice (Pleuronectes platessa). Environmental Biology of Fishes 7: 157–163. Stevens, E. D. 1979. The effect of temperature on tail beat frequency of fish swimming at constant velocity. Canadian Journal of Zoology 57: 1628–1635. Stevens, E. D. and F. E. J. Fry. 1970. The rate of thermal exchange in a teleost, Tilapia mossambica. Canadian Journal of Zoology 48: 221–226. Susanto, G. N. and M. S. Peterson. 1996. Survival, osmoregulation and oxygen consumption of YOY coastal largemouth bass, Micropterus salmoides exposed to saline media. Hydrobiologia 323: 119–127. Suski, C. D., S. S. Killen, M. B. Morrissey, S. G. Lund, and B. L. Tufts. 2003. Physiological changes in largemouth bass caused by live-release angling tournaments in Southeastern Ontario. North American Journal of Fisheries Management 23: 760–769. Suski, C. D., S. S. Killen, S. J., Cooke, J. D. Kieffer, D. P. Philipp, and B. L. Tufts. 2004. Physiological significance of the weigh-in during live-release angling tournaments for largemouth bass. Transactions of the American Fisheries Society 133: 1291–1303. Suski, C. D., S. S. Killen, J. D. Kieffer, and B. L. Tufts. 2006. The influence of environmental temperature and oxygen concentration on the recovery of largemouth bass from exercise: implications for live-release angling tournaments. Journal of Fish Biology 68: 120–136. Suski, C. D., S. J. Cooke, and B. L. Tufts. 2007. Failure of low-velocity swimming to enhance recovery from exhaustive exercise in largemouth bass (Micropterus salmoides). Physiological and Biochemical Zoology 80: 78–87. Thorarensen, H., P. E. Gallaugher, and A. P. Farrell. 1996. The limitations of heart rate as a predictor of metabolic rate in fish. Journal of Fish Biology 49: 226–236. Tolley, S. G. and J. J. Torres. 2002. Energetics of swimming in juvenile common snook, Centropomus undecimalis. Environmental Biology of Fishes 63: 427–433. Tschantz, D. R., E. L. Crockett, P. H. Niewiarowski, and R. L. Londraville. 2002. Cold acclimation strategy is highly variable among the sunfishes (Centrarchidae). Physiological and Biochemical Zoology 75: 544–556. Ultsch, G. R. 1989. Ecology and physiology of hibernation and overwintering among freshwater fishes, turtles, and snakes. Biological Reviews 64: 435–516. Van Raaij, M., D. Pit, P. Balm, A. Steffens, and G. van den Thillart. 1996. Behavioral strategy and the physiological stress response in rainbow trout exposed to severe hypoxia. Hormones and Behaviour 30: 85–92. Videler, J. J. 1993. Fish Swimming. Chapman Hall, London, UK. Wakefield, A. M., R. A. Cunjak, and J. D. Kieffer. 2004. Metabolic recovery in Atlantic salmon fry and parr following forced activity. Journal of Fish Biology 65: 920–932. Ware, D. M. 1982. Power and evolutionary fitness of teleosts. Canadian Journal of Fisheries and Aquatic Sciences 39: 3–13. Webb, P. W. 1975. Acceleration performance of rainbow trout Salmo gairdneri and green sunfish Lepomis cyanellus. Journal of Experimental Biology 63: 451–465. Wendellar Bonga, S. E. W. 1997. The stress response in fish. Physiological Reviews 77: 591–625. Wilga, C. D. and G. V. Lauder. 1999. Locomotion in sturgeon: function of the pectoral fins. Journal of Experimental Biology 202: 2413–2432. Wilkie, M. P., K. Davidson, M. A. Brobbel, J. D. Kieffer, R. K. Booth, A. T. Bielak, and B. L. Tufts. 1996. Physiology and survival of wild Atlantic salmon following angling in warm summer waters. Transactions of the American Fisheries Society 125: 572–580. Wilkie, M. P., M. A. Brobbel, K. Davidson, L. Forsyth, and B. L. Tufts. 1997. Influences of temperature upon the postexercise physiology of Atlantic salmon (Salmo salar). Canadian Journal of Fisheries and Aquatic Sciences 54: 503–511.

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Wilkie, M. P., P. G Bradshaw, V. Joanis, J. F. Claude, and S. S. Swindell. 2001. Rapid metabolic recovery following vigorous exercise in burrow-dwelling larval sea lampreys (Petromyzon marinus). Physiological and Biochemical Zoology 74: 261–272. Williamson, J. H. and G. J. Carmichael. 1986. Differential response to handling stress by Florida, northern, and hybrid largemouth bass. Transactions of the American Fisheries Society 115: 756–761. Williamson, J. H. and G. J. Carmichael. 1990. An aquacultural evaluation of Florida, northern, and hybrid largemouth bass, Micropterus salmoides. Aquaculture 85: 247–257. Wismer, D. A. and A. E. Christie. 1987. Temperature Relationships of Great Lakes Fishes: A Data Compilation. Great Lakes Fisheries Commission Report. Ann Arbor, MI. Weller, D. E., D. J. Anderson, D. L. DeAngelis, and C. C. Coutant. 1984. Rates of heat exchange in largemouth bass: experiment and model. Physiological Zoology 57: 413–427. Wood, C. M. 1991. Acid-base and ion balance, metabolism, and their interactions, after exhaustive exercise in fish. Journal of Experimental Biology 160: 285–308.

Chapter 9

Winter biology of centrarchid fishes C. D. Suski and M. S. Ridgway

9.1 Introduction Temperate latitudes experience a predictable annual cycle of alternating warm and cold periods that can result in below freezing conditions, ice cover, and alterations to aquatic habitats that persist for a substantial portion of a year. Winter represents a very interesting and challenging time of the year that exerts a strong selective pressure on individual survival, community structure, and year class strength for centrarchid fishes. Despite the impact of this time on both individuals and populations, we are only beginning to comprehend how this period of the year can influence centrarchid fishes. The purpose of this chapter is to summarize the current literature that defines the ecological, behavioral, and physiological alterations experienced by centrarchid fishes both prior to and during winter. Because of the paucity of information on winter biology of centrarchid fishes, this chapter has been written in a general format whereby studies of different centrarchid fishes have been pooled to identify trends that exist across the entire family. Where appropriate, exceptions to these general trends have been noted. A general over-arching question does emerge from work to date despite the lack of broad research coverage in many areas of centrarchid winter biology: What physiological and ecological changes occur to ensure survival prior to and during a period of reduced energy intake?

9.2 Definition of “winter” We define “winter” as the period of the year between the autumnal equinox and prior to the onset of spawning in centrarchid fishes. This definition encompasses the suite of physical, biochemical, and structural changes to both water and fish that result from reduced water temperature and day length, and allows for the onset and termination of the “winter” period that varies with latitude. Centrarchids can experience a broad range of climatic conditions during winter across their range. Pronounced latitudinal gradients in winter conditions exist with growing degree days and summer temperatures both declining with latitude, whereas both winter severity (i.e. lower daily temperatures) and winter length increase with latitude. Centrarchids residing in Alabama farm ponds, for example, may briefly experience winter water temperatures that range from 4 to 13◦ C (Swingle 1952), whereas water temperatures for centrarchids at the northern edge of their range may be near freezing for several consecutive months. This latitudinal variation in winter severity has several pronounced implications for many of the ecological, physiological, and geographic characteristics observed within this family.

9.3 Current research One trend that emerged while writing this chapter was the paucity of research that has been conducted on the winter ecology and physiology of centrarchid fishes. To illustrate this, we used three common academic search engines (Fish and Fisheries Abstracts, Web of Science, and CISTI Source) to perform literature searches and collect reference materials. The search terms used were truncations designed to maximize the number of potential hits associated with winter conditions. 264

Winter biology of centrarchid fishes

265

Table 9.1 Results of literature searches using three academic search engines to locate reference materials. Fish and fisheries worldwide

Web of science

4178

4918

132

22

7

Micropt* and (ice or snow or winter)

94

63

39

Lepom* and (ice or snow or winter)

63

42

14

Pomox* and (ice or snow or winter)

Search string Fish* and (ice or snow or winter) Centrarch* and (ice or snow or winter)

CISTI source 2074

33

10

7

Ambloplit* and (ice or snow or winter)

9

3

2

Enneacan* and (ice or snow or winter)

2

1

0

Archoplit* and (ice or snow or winter)

0

0

0

Centrarch* and habitat*

1019

102

28

Centrarch* and reprod*

515

69

16

*Truncated search strings are shown here, and searches were set up to scan entire articles for the truncated search strings.

Searches scanned entire articles for keywords, and the keywords used included all of the different genera in the centrarchid family (See Chapter 1 in this volume) as well as the terms ice, snow, and winter. Results from these searches are shown in Table 9.1 and highlight the lack of studies focusing on centrarchids in winter. When a general search string such as [Fish* and (ice or snow or winter)] was queried, several thousand hits were generated for each of the three search engines used (Table 9.1). Similar research focusing on centrarchid fishes, however, is proportionally scarce with only 161 total references generated for all three search engines combined when the search string [centrarch* and (ice or snow or winter)] was run (Table 9.1). In contrast, for topics such as centrarchid habitat, there were approximately five times more citations listed than for winter ecology (Table 9.1). This lack of information can likely be attributed to the numerous inherent challenges associated with studying fish in winter, including: difficulty in fish collections through ice, safety issues concerning ice and cold water, as well as the obvious discomfort of outdoor work during cold temperatures. Despite these challenges, however, sufficient studies have been performed to provide a general understanding of the impact of winter on centrarchid fishes.

9.4 Temperature One of the most significant impacts of winter conditions on centrarchid fishes is a reduction in ambient water temperature brought about by changes in solar radiation. Temperature affects almost all levels of biological organization including molecular diffusion rates, membrane structure, organ function, and respiration rates. Both calendar date and latitude have a significant impact on the amount of solar radiation (Gates 1962; Figure 9.1). Both the amount of radiation and the angle at which it strikes the Earth decrease as months advance from the summer solstice and as latitudes increase (Gates 1962). Less solar radiation is transferred to water and more radiation is reflected by the water surface during winter periods in temperate regions.

9.4.1 Ice Ice formation on lakes results from a predictable pattern based on latitude, volume, and fetch (Shuter et al . 1983). Ice can be intermittent throughout the winter or it can accumulate to thicknesses approaching 1 m or more in certain northern

266

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Solar radiation (cal cm−2 day−1)

1000 0 10 20

800

0 10 20

30

400 200

0

30

40

600

J

F

40

50

50

60

60

70

70

80

80

M −2

A

M

J

J

A

S

O

N

D

−1

Figure 9.1 Amount of solar radiation (cal·cm ·day ) received on a horizontal surface for different latitudes at various times of the year. Latitude is presented in 10◦ intervals and abbreviated calendar month is shown on the x- axis beginning on the left with January (J, January; F, February; M, March, etc.). Figure from Wetzel (1983), Elsevier [(Harcourt Publishers) http://www.thomsonrights.com/permissions/action/start].

locations and persist for several months. As snow is added on top of ice or if ice is not transparent, both albedo (Grenfell and Maykut 1977) and light attenuation increase and light levels can fall to near zero <1 m below the surface (Welch et al . 1987). This can have important implications for photosynthetic and aerobic organisms throughout a waterbody. In streams and rivers, the energy of flowing water may be sufficient to prevent formation of surface ice despite cold temperatures. Despite this lack of ice cover, flowing water at high latitudes only warms a few hundredths of a degree above freezing during winter except in locations of groundwater inflow, input from tributaries, or at gaps in ice formation (Belatos et al . 1993). Super-cooled water in turbulent areas can form frazil ice crystals that can remain suspended in the water or possibly coat objects in the river (Belatos et al . 1993; Prowse 1994). Frazil ice can accumulate on virtually any underwater surface with significant accumulations being termed anchor ice (Benson 1955; Belatos et al . 1993; Prowse 1994). Although anchor ice may float downstream without any consequences to fishes, it can contain sand, gravel, organic materials, and benthic invertebrates (Benson 1955), and accumulations on the substrate can create a false bottom causing the river to rise above its normal depth (Belatos et al . 1993). Anchor ice, coupled with the growth of surface ice in slower river reaches, can extend the entire depth of the water column effectively removing large portions of backwater lotic habitats (Prowse 1994; Gent et al . 1995). The full extent of ice on stream erosion, stream flow, dissolved oxygen levels, and lotic fishes is not fully understood (Prowse 1994). The extent to which most of these processes can affect lotic centrarchids in rivers and streams has not been well studied.

9.4.2 Photosynthesis Primary productivity in temperate latitudes follows the annual cycle of solar radiation discussed earlier. During winter, the amount of emergent macrophytes (Miranda and Pugh 1997), submergent macrophytes, phytoplankton (Wetzel 2001), and epilithic algae (Harrison and Hildrew 1998) all decline in abundance, with more pronounced decreases occurring at high latitudes. This seasonal decline in primary producers is largely due to a reduction in water temperature (Rooney and Kalff 2000), but also appears to be associated with reduced light levels (Welch and Kalff 1974). Phytoplankton adapted to low temperature and reduced light conditions can survive under ice (Philips and Fawley 2002) and may continue to photosynthesize, with this activity typically occurring in the upper portions of a waterbody (Wetzel 2001). In general, however, aquatic dissolved oxygen concentrations decrease in winter as a result of reductions in photosynthetic macrophytes and phytoplankton, elimination of atmospheric oxygen exchange because of ice, decomposition in the benthos, and inputs

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267

of oxygen-poor groundwater (Schreier et al . 1980; Prowse 1994). This reduction in dissolved oxygen may be responsible for several behavioral modifications for centrarchid fishes during winter and can result in mortality.

9.5 Dissolved oxygen and winterkill A reduction in dissolved oxygen under ice during winter is a common occurrence and has been reported for many different waterbodies at high latitudes. Extensive fish mortality can result if hypoxic conditions persist for extended periods and escalate to the depletion of oxygen within the water (Greenbank 1945; Fox and Keast 1990). Depletion of oxygen can occur for many reasons such as a lack of photosynthesizing vegetation, oxygen consumption through benthic decomposition, and ice cover preventing the exchange of oxygen with the environment (Danylchuk and Tonn 2003). The potential to develop hypoxic conditions in northern waterbodies can be predicted (Jackson and Lasenby 1982) and is influenced by factors such as waterbody depth, trophic status, basin morphometry, degree of water mixing, macrophyte abundance, percent littoral area, and total phosphorous (Mathias and Barica 1980; Meding and Jackson 2003). Shallow, eutrophic waters rich in phosphorous and littoral macrophytes at northern latitudes appear to be the most prone to winter hypoxia (Mathias and Barica 1980; Meding and Jackson 2003), and the quantity of dissolved oxygen within a waterbody can vary across winters (Greenbank 1945; Danylchuk and Tonn 2003). Winterkill can occur on a local scale such as in an isolated lake or pond, and studies have shown that such events can result in the loss of 85% of pumpkinseed from the population (Fox and Keast 1990). Winterkill can also occur at a landscape scale as a result of severe winters, such as described in Greenbank (1945) who documented “a considerable number of lakes in Southern Michigan” that experienced winterkill in the winter of 1935–1936 resulting in the deaths of hundreds of thousands of fish, with centrarchids likely included. Declines in large numbers of fish as a result of winterkill can have repercussions that cascade throughout an ecosystem. Changes as a result of winterkill influence the relative abundance of individuals or species (composition), and can affect age of first maturity, species richness, ecosystem biomass, or food web dynamics (Shuter and Koonce 1977; Micheli et al . 1999). Laboratory investigations examining the oxygen tolerances of centrarchid fishes have focused on only a few species with results consistently showing a profound resilience to hypoxic conditions. Laboratory studies with bluegill showed that, at 25◦ C, fish could survive for 24 h in dissolved oxygen concentrations that had been reduced to 0.7 mg/l (Moss and Scott 1961). Laboratory studies have also shown that largemouth bass held at 23.7◦ C will avoid waters with dissolved oxygen concentrations below 2.4 mg/l and show preference for water at or above 4 mg/l (Burleson et al . 2001), but can survive dissolved oxygen concentrations below 1.0 mg/l (Moss and Scott 1961). Field studies during winter tend to corroborate these lab investigations and suggest that many centrarchid fishes are quite tolerant to hypoxic conditions. Lethal dissolved oxygen concentrations have been reported as ranging between 0.4 and 2.0 mg/l for pumpkinseed, bluegill, and black crappie during winter conditions (Moore 1942; Cooper and Washburn 1949). Cooper and Washburn (1949) and Johnson (1965) reported that significant winterkill of centrarchid fishes was unlikely provided dissolved oxygen concentrations remained above 1.0 mg/l, while Knights et al . (1995) recommended 2–3 mg/l dissolved oxygen for overwintering bluegill and black crappie. Cooper and Washburn (1949) also observed live bluegill and pumpkinseed congregating at holes cut in the ice of a Michigan lake despite the fact that dissolved oxygen in the lake had been below 1.0 mg/l for over a week, and was 0.4 mg/l when fish were observed. Prolonged exposure to dissolved oxygen concentrations below 2.6 mg/l in a winter simulation experiment did not influence spawning activity in black crappie (Carlson and Herman 1978). Finally, Moore (1942) noted that smaller centrarchid fishes were more likely to die during periods of oxygen depletion, likely because of elevated metabolic rates relative to larger fish. It is believed that the reduced metabolic rate (Section 9.6) and activity levels (Section 9.9) of overwintering fish allow survival at low-oxygen tensions. Laboratory and field studies suggest that, with the onset of hypoxia under ice, fish exhibit several predictable behavioral responses in an attempt to survive low-oxygen conditions. First, laboratory studies with bluegill documented that dissolved oxygen levels below 2.0 mg/l resulted in increased ventilation rates as fish attempt to increase the flow of water over their gills and maximize oxygen uptake (Petrosky and Magnuson 1973). Hypoxic conditions have also been shown to increase activity levels in bluegill, likely as fish attempted to search for more oxygenated waters (Petrosky and Maguson 1973). Next, many species such as yellow perch (Perca flavescens), northern pike (Esox lucius), and several small-bodied minnows all showed an increased association with the ice/water interface during hypoxia because dissolved oxygen levels in this depth zone are often elevated relative to other areas of a waterbody (Magnuson and Karlen 1970; Magnuson et al . 1985;

268

Centrarchid fishes

Petrosky and Magnuson 1973). Bluegill do not appear to associate with the ice/water interface during hypoxia, and, as a result, died from hypoxic exposure prior to other fishes in experimental conditions (Petrosky and Magnuson 1973). Finally, studies with small-bodied minnows showed that declining oxygen levels motivate fish to migrate to more oxygen-rich waters thereby avoiding hypoxic conditions (Magnuson et al . 1985); similar studies involving centrarchid fish are somewhat conflicting. Some studies report the movements of centrarchids in response to low dissolved oxygen, whereas others note either a reluctance or inability to move despite near hypoxic waters. Greenbank (1945), for example, noted dead and dying fish crowded in an area with dissolved oxygen concentrations of only 0.4 mg/l, while only 13 m away, dissolved oxygen concentrations were 2.8 mg/l—unfortunately, fish species were not named in that study. More specifically, Knights et al . (1995) showed that dissolved oxygen concentrations influenced habitat decisions by overwintering bluegill and black crappie, and a drop in oxygen concentrations below 2 mg/l caused fish to seek higher dissolved oxygen concentrations even though this subjected them to temperatures below 1◦ C and increased current velocities. Both Raibley et al . (1997) and Gent et al . (1995) documented that overwintering largemouth bass were active and roamed throughout backwater habitats despite dissolved oxygen concentrations of 1–2 and 3–6 mg/l, respectively, but avoided more oxygenated main channel areas. While main channel areas may contain increased levels of dissolved oxygen relative to hypoxic backwater areas, main channel waters are also colder than back water areas and have increased current velocity. Thus, fish inhabiting main channel areas would experience increased activity levels, a reduction in swimming ability (Section 9.7), and a concomitant increase in energy consumption. All of these factors would increase the rate of energy consumption, and possibly mortality. In addition to the immediate population-level impacts of mortality from winterkill, repeated bouts of winterkill are suspected to have altered the life history and species composition of resident fishes and populations. Pumpkinseed that reside in ponds with frequent winterkill were shown to display a more “r-selected” life history with smaller body sizes, smaller length at maturity, higher gonadal investment, and higher fecundity relative to conspecifics from stable lake environments (Fox and Keast 1990; Fox and Keast 1991).

9.6 Physical and physiological changes The internal temperature of a fish seldom deviates from that of its surroundings because of the relatively large surface area of gills and the close contact between blood and water (Reynolds et al . 1976; Hazel 1993). Reductions in water temperature that accompany winter are experienced throughout an entire fish and are accompanied by a suite of physiological changes that can be seen at the cellular, tissue, and individual levels. In general, decreases in temperature of 10◦ C result in reductions in the rate of reactions by a factor of 2 or 3. Consequently, both the standard metabolic rate and the active metabolic rate of fishes decline at low temperatures such that oxygen consumption and scope for activity are lowest with reduced water temperature (Beamish 1970; Cech et al . 1979; Robinson et al . 1983; Clarke and Fraser 2004). This relationship has been established for several centrarchid species including largemouth bass (Johnson and Charlton 1960; Lemons and Crawshaw 1985) and bluegill (Wohlschlag and Juliano 1959). The term “metabolic rate,” however, encompasses the sum of a suite of physical and chemical processes involved in anabolism, catabolism, and cell energetics, all of which are influenced by temperature (Randall et al . 1997). Cold temperatures, for example, slow the activity of enzymes, ion pumps, and ion channels (Somero 1995; Hochachka 1988) and will alter the phase state, rate of motion, and packing arrangement of cellular membranes (Hazel 1993). Cold temperatures also produce changes in neural function in poikilothermic vertebrates, and virtually all neural processes (synaptic gain, conduction velocity, refractory period) are slowed with cooler temperatures (Montgomery and MacDonald 1990). The degree to which this cooling affects the performance of individuals and populations, however, will depend on the species in question and the actual temperatures involved (Montgomery and MacDonald 1990). The extent to which cold temperatures affect the nervous system of centrarchid fishes is unknown as two reviews on this subject (Prosser and Nelson 1981; Montgomery and MacDonald 1990) did not mention any centrarchid species. Low temperatures slow the digestion rates of many fish species including largemouth bass (Markus 1932; Moln´ar and T¨olg 1962; F¨ange and Grove 1979), and also lowers the cardiac performance of fish (Driedzic 1992). Many eurythermal fish species experience modifications in internal physiology in an attempt to combat the reductions in reaction rates and physiological processes that accompany cold water temperatures. Studies of this nature have been conducted using centrarchid fishes, but the paucity of data and disparity between studies preclude clear identification

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of trends or strategies both within and among species. For example, winter-acclimated fish often increase metabolismrelated enzyme levels to improve their ability to utilize metabolic pathways despite reduced temperatures (Hazel and Prosser 1974; Driedzic et al . 1996). This trend was documented by Kolok (1991a) who showed significant increases in the activity of heart citrate synthase from cold-acclimated smallmouth bass suggesting an increased ability to maintain performance despite cold temperatures. In contrast, studies by Sephton and Driedzic (1991) documented that acclimation to 5◦ C did not alter the activity rate of citrate synthase in smallmouth bass hearts suggesting a decrease in performance for cardiac tissue during winter. Shaklee et al . (1977) noted similar within-species discrepancies for winter acclimation strategies for green sunfish (Lepomis cyanellus). These authors showed that enzymes from different metabolic pathways (aerobic, anaerobic, etc.) often exhibited different up- or down-regulation both across and within tissues (Shaklee et al . 1977) and called for additional studies to elucidate tissue-specific responses to cold acclimation. Furthermore, Tschantz et al . (2002) documented significant differences in the activity levels of several different aerobic and anaerobic enzymes for five different centrarchid species during winter acclimation (largemouth bass, green sunfish, bluegill, black crappie, and white crappie) both across species and tissues. No clear trend related to phylogeny could be determined by these authors, further emphasizing that the metabolic strategies employed by centrarchid fishes in dealing with winter conditions vary significantly across species, tissues, and enzymes. Similarly, acclimation to winter conditions often results in an increase in heart (ventricle) mass relative to body mass (often called the heart somatic index), and it is believed that this occurs to maintain swimming capacity in cold conditions (Driedzic et al . 1996). Across several centrarchid species, an increase in ventricular mass during winter was reported for black crappie, white crappie, and smallmouth bass, but not for green sunfish, bluegill, or largemouth bass suggesting species-specific differences in winter performance following acclimation (Kolok 1991a; Sephton and Driedzic 1991; Tschantz et al . 2002). Discrepancies across studies may result from the sizes/ages of fish used, latitude (severity of winter), or photoperiod (Section 9.15), and further work in this area is required to elucidate trends.

9.7 Swimming abilities For all fish, swimming speeds can be categorized as sustained, prolonged, and burst (Hoar and Randall 1978). While sustained and prolonged swimming represent slow-speed aerobic activity that can typically be maintained for extended time periods, burst swimming represents high-intensity, anaerobic activity that can only be maintained for short durations such as during prey capture or predator avoidance (Hoar and Randall 1978). As a result of reductions in water temperature that accompany winter, fish experience several biochemical and physiological changes within their muscle tissue that reduce their capacity to maintain swimming performance relative to summer levels. Low temperature reduces the force generated by muscle, the rate of force development, and maximum power output for the muscle of poikilothermic organisms, although few studies have examined these trends specifically in fishes (Rall and Woledge 1990). Across a range of fish species, however, studies have shown that low water temperatures increase the amount of time required for muscle to contract, while reducing maximum tail beat frequency, therefore lowering maximum swimming speed (Wardle 1980). In addition, reduced temperature impairs the locomotory capacity of fishes by reducing the shortening velocity and power output of muscle (Rome 1990; Hazel 1993). In addition to limitations in swimming performance driven by muscle, reductions in the scope for activity may be driven by a reduced scope for cardiac output at low temperatures (Kolok et al . 1983) or a decline in the ability of organisms to uptake and transport oxygen (P¨ortner 2002). These physiological limitations in muscle are reflected in studies of winter swimming performance, including several involving centrarchid fishes; reductions in water temperature result in a decline in the prolonged swimming speed of several centrarchid species including largemouth bass, smallmouth bass (Beamish 1978; Hanson et al . 2007; Figure 9.2), and white crappie (Parsons and Smiley 2003). Additionally, the swimming performance of largemouth bass acclimated to 20◦ C was significantly higher than the fish acclimated to 5◦ C (Kolok 1992), and Larimore and Duever (1968) noted a significant decline in the swimming ability of smallmouth bass fry (21–23 TL in mm) below 10◦ C. To compensate for impairments in muscle capacity associated with low temperatures, many studies have reported alterations to fish muscle properties that attempt to maintain performance. For example, studies involving rainbow trout (Oncorhynchus mykiss) report that mitochondrial density, membrane structure, and aerobic capacity in red muscle all show cold-induced alterations intended to enhance the ability of muscle to respire aerobically despite low water temperatures

270

Centrarchid fishes

100

Oncorhynchus nerka Prolonged swimming speed (cm s −1)

80

Salvelinus namaycush

60

Micropterus salmoides

40

Carassius auratus

Oncorhynchus kisutch Micropterus dolomieu

20 Trematornus borchgrevinki 0

0

10

20 Temperature °C

30

40

Figure 9.2 Prolonged swimming speed of various fish species across a range of temperatures. Figure from Beamish (1978) [Elsevier (Academic Press, New York) http://www.elsevier.com/wps/find/obtainpermissionform.cws home/ obtainpermissionform].

(P¨ortner 2002; Guderly 2004). Evidence also exists to suggest that many of the contractile properties of fish muscle can acclimate to cold temperatures potentially permitting a return to near-normal swimming performance (Johnston et al . 1990). A study by Kolok (1991a) documented that the cross-sectional area of red muscle in the caudle peduncle of smallmouth bass and green sunfish increased with cold acclimation, suggesting the potential for increased swimming performance in winter for these species. To date, a few studies have examined the influence of temperature on burst swimming, but results suggest that burst speed is independent of temperature effects (Beamish 1978), although low temperatures will prolong the time to recovery from such activity (Cooke et al . 2003).

9.8 Species ranges and life history traits Magnuson et al . (1979) proposed that temperature was an ecological resource similar to food or habitat, and that fish compete for access to appropriate thermal resources to maximize their performance and fitness. Along with Magnuson et al . (1979), several additional authors have described lethal (Fry 1971), tolerance (Brett 1970), and performance (Fry 1971) factors associated with temperature gradients that interact to define the thermal niche of fishes, with the geographical limits of the thermal conditions within this niche defining a fish’s range and distribution. This theory of temperaturedefined species distributions has proved correct for many fishes. Studies by Brandt et al . (1980) revealed that fishes in Lake Michigan partitioned habitat according to thermal boundaries, while both Meisner et al . (1987) and Shuter and Post (1990) showed that the geographical limits of many Ontario fishes could be delineated by climatic contours associated with temperature and growing season (Figure 9.3). Furthermore, many fish species are confined to southerly regions despite the absence of physical barriers, possibly because of restrictions in thermal niches and reduced performance at higher

Winter biology of centrarchid fishes

140° 70 °

110°

80°

271

50°

60

A

°

B C

A B

50

°

C

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Figure 9.3 Distribution of smallmouth bass in North America (shaded area) and northern limit predicted by computer modeling based on mortality with high food availability (Line A) and low food availability (Line B). Dashed line (C) represents the latitude at which winter starvation likely begins to influence population behavior. Figure from Shuter and Post (1990) [The American Fisheries Society (1990)119:314–336].

latitudes (Meisner et al . 1987; Shuter and Post 1990; P¨ortner 2002), in part explaining the reduction in species diversity observed at high latitudes (McAllister et al . 1986; Allen et al . 2002). Latitude and climate clines (i.e. the extent and duration of winter conditions) can also impact life history characteristics of centrarchid fishes. Latitude has been shown to influence the growth rates of largemouth bass (Carlander 1979; Modde and Scalet 1985) and bluegill (Modde and Scalet 1985) and other fish species [e.g., brown trout Salmo trutta (Jensen et al . 2000)]. Record adult size for largemouth bass declines with increasing latitude (Modde and Scalet 1985). In a review of age and growth patterns for largemouth bass and smallmouth bass in North America, Beamsderfer and North (1995) found clear evidence for the effect of growing season on life history parameters (Figure 9.4). Increasing latitude results in older ages at 30.0 and 28.0 cm TL for largemouth and smallmouth bass, respectively. Similarly, increasing average air temperature results in faster growth to young adult size for both species. For largemouth bass, Beamsderfer and North (1995) found a significant negative correlation between natural mortality and latitude as well as degree days above 10◦ C, a measure of growing season duration for bass (Figure 9.4). Mean air temperature was positively correlated with natural mortality in largemouth bass. Taken together, the latitudinal clines in life history for largemouth and smallmouth bass found in Beamsderfer and North’s (1995) survey certainly reflect growing season, and its corollary, winter duration. Trade-offs between allocation of energy to growth or reproduction lie at the heart of life history variation in fish (Danylchuk and Fox 1994; Lester et al . 2004), so factors influencing this allocation process, such as winter duration, appear to be essential in understanding life history variation in centrarchid fishes. The ecological and physiological alterations to individuals and ecosystems associated with the onset of winter interact to influence the abundance, range, distribution, and life history characteristics of centrarchids.

9.9 General activity level Consistent with the impairments to physiological performance listed in Section 9.6, laboratory studies all document a reduction in the activity level of centrarchid fishes during winter conditions relative to summer, but species-specific

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differences do exist. For example, activity levels of largemouth bass in laboratory experiments remained constant despite reductions in water temperature until approximately 7◦ C, at which point activity levels diminished (Crawshaw 1984; Lemons and Crawshaw 1985; Figure 9.5). Similarly, laboratory studies by Tschantz et al . (2002) documented a reduction in swimming activity of largemouth bass, green sunfish, bluegill, and black crappie to near dormant at cold temperatures, while the swimming activity of white crappie was not affected by cold. Existing evidence indicates that the activity levels and movement rates of centrarchid fishes are reduced considerably in winter, but are not completely eliminated. It is not clear if this reduced activity is necessitated through reduced food intake,

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a temperature-induced reduction in metabolism and performance, or a combination of these factors. Conversely, it has been proposed that the reductions in activity levels exhibited by centrarchid fishes are facultative rather than obligate (Kolok 1991a). This hypothesis has resulted from several lines of evidence listed earlier including the observation that several centrarchid species appear to continue feeding during winter (Moffett and Hunt 1943; Gent et al . 1995). Centrarchids have the capability of substantial swimming bouts despite near freezing temperatures (Lyons and Kanehl 2002; Karchesky and Bennett 2004). Multiple compensatory physiological changes have been noted to cardiac tissue, muscle tissue, and metabolic enzymes that would suggest an ability to maintain performance during winter conditions (Kolok 1991a; Tschantz 2002). Furthermore, these compensatory alterations were similar for a reportedly “winter quiescent” species (smallmouth bass) and a “winter active” species (green sunfish) (Kolok 1991a). Thus, evidence exists to suggest that winter quiescence in some species of centrarchids may be facultative rather than obligate, and this reduction in activity level may function to minimize maintenance costs at times of reduced food availability.

9.10 Winter movements Although the results of laboratory studies generally agree in classifying many overwintering centrarchids as dormant, results from several field investigations would suggest otherwise. Field studies investigating the movements of centrarchid fishes during winter all document reductions relative to summer (Warden and Lorio 1975; Hubert and Lackey 1980; Todd and Rabeni 1989; Horton and Guy 2002) and researchers have labeled some radio-tagged centrarchids as “inactive” during winter periods (Munther 1970; Warden and Lorio 1975). Also, studies involving a whole-lake telemetry array revealed that the distribution of fish within the lake was constricted considerably during winter periods relative to summer (Caleb Hasler, unpublished data, Figure 9.6; Hasler et al . 2007). However, for many studies, movements by centrarchid fishes during winter are quite common. Karchesky and Bennett (2004), for example, documented travel of some largemouth bass between two overwintering areas despite water temperatures of 3◦ C, while Greenbank (1956) noted considerable winter movements of several fish species, especially black crappie, to and from an ice-covered backwater area of the Mississippi River. Despite water temperatures of 4◦ C, Todd and Rabeni (1989) documented movements of stream-dwelling smallmouth bass in Missouri of 120 m/day, while Lyons and Kanehl (2002) reported that overwintering smallmouth bass in Wisconsin exhibited regular movements of 100–200 m/week in water temperatures less than 1◦ C. Thus, while laboratory studies would suggest that centrarchids are dormant during winter, several field investigations document movement and activity levels in centrarchids during this period.

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A recent synthesis by Lyons and Kanehl (2002) suggested that the magnitude of downstream movements by smallmouth bass to larger water bodies may be correlated with winter severity. Studies of smallmouth bass movements prior to winter in Idaho (Munther 1970) and Missouri (Todd and Rabeni 1989), where winters were mild, documented winter downstream migration of fish <1 km. In Wisconsin, where winters are more severe, smallmouth bass migrated between 6.5 and 69 km to downstream wintering areas during late fall (Langhurst and Schoenike 1990; Lyons and Kanehl 2002), highlighting the influence of river conditions during winter on this behavior. Despite an apparent general reduction in activity during winter, further research is needed to assess winter activity among centrarchid species. Sorting through proximate causes (e.g., impaired neuronal transmission capabilities, reduced muscle performance) and ultimate causes (e.g., lowered metabolic rates, lowered food availability, reduced need for movements) behind reduced activity during winter is an important area for future research. Activity levels during winter are believed to be influenced by prey assemblages, water temperature, energy stores, and the presence of predators, but a clear influence of these variables on activity level has not yet been established (Micucci et al . 2003; Garvey et al . 2004).

9.11 Feeding A common assumption is that feeding ceases during winter for centrarchid fishes. This idea stems from several laboratory studies suggesting inactivity during winter (Crawshaw 1984; Lemons and Crawshaw 1985), and several studies listed below showing a little or no winter feeding. In contrast, current theory for coolwater fishes suggests that winter feeding occurs, but only to permit individuals to maintain minimal activity rates and routine metabolism rather than to fuel growth or gonadal development, and that feeding only occurs when energy stores decline to a critical level (McCauley and Kilgour 1990; Conover 1992; Metcalfe and Thorpe 1992; although see Post and Parkinson 2001). This theory was highlighted in winter simulation experiments by Metcalfe and Thorpe (1992) who showed that juvenile Atlantic salmon

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(Salmo salar) above a certain nutritional threshold would refuse all food presented to them. If food was withheld and the nutritional status of the fish fell, feeding would resume until the nutritional status was re-established (Figure 9.7). This theory of periodic feeding to defend energy levels has not been tested explicitly with centrarchid fishes, but both modeling simulations (Garvey et al . 2004) and laboratory/field studies listed below indirectly support this hypothesis.

9.11.1 Laboratory studies Laboratory feeding studies involving overwintering fish typically present individuals with prey items ad libitum, reducing the need for energetically expensive foraging bouts or prey searching. Across all studies, results show that, under simulated winter conditions, the feeding rates of centrarchid fishes are reduced relative to warmer water temperatures (Hathaway 1927; Markus 1932; Coble 1975; Oliver et al . 1979; Johnson and Charlton 1960). For species such as largemouth bass and smallmouth bass, cessation of feeding was documented when water temperatures fell below 3–10◦ C (Markus 1932; Coble 1975; Johnson and Charlton 1960; Lemons and Crawshaw 1985) and 7.1◦ C (Oliver et al . 1979), respectively. In contrast, however, Hathaway (1927) showed a decrease in food consumption rates of bluegill, pumpkinseed, and largemouth bass when water temperatures were cooled to 10◦ C, but all three species continued to consume food as winter simulations continued. Although results from laboratory studies show that feeding by centrarchid fishes is reduced at low temperatures, the cessation of feeding does not appear to be universal suggesting that feeding in winter can occur in the field for some or all species.

9.11.2 Feeding in the wild Feeding by centrachids can be greatly reduced, but does not appear to cease completely during winter—even at high latitudes. Snyder and Peterson (1999) documented that bluespotted sunfish (Enneacanthus gloriosus) in Mississippi fed

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Figure 9.8 Largemouth bass collected by angling thorough ice in Ontario, Canada.

during winter, and VanderKooy et al . (2000) noted that bluegill (Lepomis macrochirus), redspotted sunfish (Lepomis miniatus), and redear sunfish (Lepomis microlophus) across a range of sizes sampled from a Mississippi estuary all continued feeding during winter, primarily on invertebrate prey. Collections of fish through the ice in Ontario by Keast (1968) noted that rock bass (Ambloplites rupestris), bluegill, smallmouth bass, and largemouth bass collected at water temperatures between 6.5 and 8.5◦ C appeared to have not eaten for several weeks. In contrast to these field studies, however, collections of bluegill by hook-and-line angling through the ice in Michigan revealed that 83% of individuals caught had food in their stomachs consisting mainly of invertebrates such as Cladocera and Ostracods, although feeding rates were reduced relative to summer food intake (Moffett and Hunt 1943). Similarly, Bulow et al . (1981) reported that the stomach fullness of bluegill sampled in the winter was reduced relative to summer levels, but the fish still had food in their stomachs. Food consumption during winter is certainly implied when anglers are able to catch fish. Studies by Rach and Meyer (1982) estimated that anglers fishing through the ice in Wisconsin harvested 2.41 bluegill per hour over a 17-week winter fishery. Gent et al . (1995) documented the winter harvest of largemouth bass outfitted with radio transmitters suggesting that this species also feeds during winter (Figure 9.8), and Knights et al . (1995) noted that anglers caught black crappies when fishing through the ice. Experiments by Garvey et al . (2004) showed that if predatory largemouth bass were absent, energy reserves for overwintering small (<94 mm) largemouth bass could increase because of foraging. Thus, both laboratory and field investigations agree that winter feeding in centrarchid fishes is reduced relative to summer levels. Even at high latitudes, however, some centrarchid fishes continue to feed during winter, and fish are therefore not completely dormant at this time.

9.12 Growth Winter growth appears to virtually stop for fishes at high latitudes, and is decreased substantially for lower-latitude centrarchids (Hoxmeier et al . 2001). Pessah and Powles (1974), for example, documented no growth in Ontario pumpkinseed held at 5◦ C, slow growth in fish at 10◦ C, and substantial growth for fish held at higher temperatures. Bluegill ceased to grow during winter weather in several Indiana lakes (Gerking 1966) and Alabama ponds (Smith and Swingle 1940), and within a population of largemouth bass, smaller individuals appear to cease growing before larger individuals (Miranda and Hubbard 1994a). Ratios of the quantity of RNA/DNA can be used to indicate recent growth rates in fish (Bulow 1970), and studies of bluegill in Tennessee showed a reduction in RNA/DNA ratios in the winter indicating a reduction in growth. A more heuristic approach to considerations of centrarchid growth during winter is to regard growth as an energy allocation strategy during a time period of reduced energy intake. Modeling experiments by Garvey and Marschall (2003)

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and Garvey et al . (2004) revealed that, during winter when food availability and fat reserves are low, small individuals invested in growth more than larger individuals in an effort to increase fat stores and reduce energetic demands, whereas larger individuals prioritized energy investment into gonadal tissue rather than growth.

9.12.1 Energy allocation Latitudinal clines in age, growth, and life history reflect differing energy allocation patterns between somatic growth and reproduction as a function of growing season and winter duration. This is clearly present in largemouth bass and smallmouth bass (Beamsderfer and North 1995; Figure 9.4; Section 9.8). Because feeding stops or is greatly reduced during winter (Section 9.11), the energy allocation strategy ought to reflect the seasonal shifts in feeding behaviors. The period of highest energy storage for adult male smallmouth bass is in the fall prior to the winter period (Mackereth et al . 1999). During winter, approximately two-thirds of this stored energy is utilized prior to the open water (ice-out) spring period (Mackereth et al . 1999). We believe the pattern of large energy stores established in the fall to meet energy demands during reduced energy intake in winter is a common centrarchid energy allocation strategy. Energy storage for winter survival versus allocating energy to somatic growth will be a function of winter duration and the selective pressures facing individuals. Selective pressures on individuals could, in turn, affect growth in the juvenile stage, maximum attained size, and the age of maturation (Lester et al . 2004).

9.13 Aggregations One of the most curious and understudied aspects of centrarchid ecology is the formation and maintenance of aggregations of individuals during winter. The formation of aggregations during winter conditions has been reported for some, but not for all centrarchid fishes, although studies involving numerous species have yet to be undertaken. Breder and Nigrelli (1935) held 10 centrarchid species under identical laboratory condition, and noted that true “aggregations” formed only in smallmouth bass and redbreast sunfish (Lepomis auritus), while black crappie formed loose clusters of multiple individuals. The other six centrarchid species examined [bluegill, green sunfish, pumpkinseed, warmouth (Lepomis gulosus), rock bass, and bluespotted sunfish] preferred to remain solitary during winter simulations, and often migrated to nonflowing water (Breder and Nigrelli 1935). Webster (1954) documented the formation of winter aggregations of smallmouth bass in Cayuga Lake and noted both the propensity of aggregations to repeatedly and predictably form in the same location in the lake and that smaller fish arrive at wintering areas prior to larger individuals. Karchesky and Bennett (2004) documented two aggregations of overwintering largemouth bass in an Idaho river that contained 95% of 19 tagged individuals, while Carlson (1992) reported that 59% of the largemouth bass fishery ≥ 305 mm estimated to be in the Hudson River overwintered at five different sites. Langlois (1936) documented the formation of winter aggregations of spotted bass in Ohio ponds. Langhurst and Schoenike (1990) showed that smallmouth bass migrated 69–87 km downstream in the Embarrass River system to reach their overwinter site. The stimulus for the formation of winter aggregations for wild centrarchids has been attributed to water temperatures below 16–10◦ C, reductions in day length, and die off aquatic macrophytes (Langlois 1936; Webster 1954; Savitz et al . 1993; Karchesky and Bennett 2004). In laboratory studies of the redbreast sunfish, Breder and Nigrelli (1935) noted that fish swam independently at 9◦ C, formed feeble aggregations at 7◦ C, and formed a quiescent resting school at 5◦ C. Furthermore, Breder and Nigrelli (1935) noted that such aggregations were only present during conditions of daylight; when lights in the laboratory were turned off or if the flow of water to the tank was stopped, the fish dispersed. The aggregation was re-formed, however, when lights were turned on and current was re-established indicating the importance of visual cues for aggregation formation and maintenance. A similar propensity for aggregations to occur only during daylight hours was observed in largemouth bass by Hasler et al . (2007). Finally, Breder and Nigrelli (1935) noted that redbreast sunfish re-formed aggregations to remain facing into the current if the location of the current was changed, and a variety of aggregation shapes and dimensions could be formed by varying the velocity of water entering the tank. The formation of winter aggregations or loose associations of individual fish is an intriguing component of the life history of many centrarchid species. Winter aggregations are especially interesting when one considers the extent of research

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on habitat selection by centrarchid fishes and the trade-off between foraging profitability and minimizing mortality risk that drives habitat selection (Mittelbach 2002). Habitat selection in centrarchids during the growing season is fairly well understood in the context of this trade-off (Stein 1979; Mittelbach 2002). How this trade-off drives habitat selection during winter is an important research question. Foraging is reduced or ceases, aggregations or loose associations of individuals develop at long distances from summer home ranges, and minimizing energetic costs appears to be paramount. Indeed, macrophyte areas that are important structural components of habitat selection for many centrarchid fishes in the growing season (Stein 1979; Savino and Stein 1982; Tonn and Magnuson 1982; Eadie and Keast 1984; Persson and Ekl¨ov 1995) die back during the winter and therefore cannot provide refuge. What trade-offs in habitat selection are present that promote the formation of aggregations in some of the largest species of centrarchid fishes, smallmouth and largemouth bass? Day/night changes in the grouping behavior, where individuals are aggregated at night and only loosely associated during the day, adds additional complexity to questions of habitat selection. In the case of Micropterus species, aggregations may simply represent habitat selection by individuals seeking to minimize physiological maintenance costs while maximizing oxygen uptake or limited foraging opportunities. Formation of aggregations in Micropterus spp., however, points to added benefits from forming social groupings of top predators.

9.14 Winter habitat Both Chapman (1966) and Cunjak (1996) proposed that habitat is the main factor regulating fish populations during winter because low water temperatures reduce metabolic costs and minimize the need to feed and defend territories. Cunjak (1996) also proposed minimizing energy expenditure by fish during winter (e.g., obtaining sufficient oxygen, protection from winter freshet, and access to refugia) was more important than was protection from predators and access to food resources. Despite this importance of refugia during winter, little is currently known about the winter habitat requirements of the majority of centrarchid fishes. Centrarchid fishes prefer to overwinter in water that is deeper and slower-moving relative to their summer habitat, although the deepest portions of a waterbody are not necessarily occupied (Lyons and Kanehl 2002). This may simply mean moving offshore into deeper regions of the lake or reservoir where they currently reside (Lewis and Flickinger 1967; Kraai et al . 1991; Savitz et al . 1993; Curry et al . 2005). In large lakes, movements to wintering areas can involve large-scale movements of many individuals to relatively few traditional overwintering locations (Webster 1954). In stream and river ecosystems, movements to overwintering areas involve fish seeking out larger, deeper sections of a river/stream or the confluence of streams. This phenomenon has been documented for smallmouth bass (Munther 1970; Langhurst and Schoenike 1990; Bunt et al . 2002), largemouth bass (Carlson 1992), redeye bass (Micropterus coosae) (Parsons 1953), and spotted bass (Trautman 1981). Lateral movements to slow-moving or backwater areas of large rivers have also been documented for bluegill (Knights et al . 1995), black crappie (Knights et al . 1995), and largemouth bass (Raibley et al . 1997; Karchesky and Bennett 2004). These winter migrations appear to begin when water temperatures fall below approximately 8–16◦ C (Munther 1970; Paragamian 1981; Langhurst and Schoenike 1990; Karchesky and Bennett 2004) or with reductions in daylight (Webster 1954). Habitats with deep, slow-moving waters are likely desirable to centrarchids as they provide cover and shelter from excessive flow thereby minimizing energy expenditure. Access to warm water relative to cooler main channel areas may also be important (Bodensteiner and Lewis 1994). Deep pools may also allow fish to avoid capture from potential mammalian (Alexander 1979; Carss et al . 1990) and avian predators (Sayler and Lagler 1940). Two notable exceptions to this trend include a stream-dwelling population of smallmouth bass in Missouri that showed no seasonal change in depth from summer to winter (Todd and Rabeni 1989) and a portion of a stream-dwelling population of smallmouth bass in Ontario that overwintered in a riverine environment rather than migrate downstream to a common overwinter site in a lake (Barthel 2004). Winter habitat selection by overwintering centrarchids may also be influenced by dissolved oxygen concentrations, and this is discussed in Sections 9.4.2 and 9.5. Surprisingly little work has been done to quantify the habitat requirements of overwintering centrarchids at small spatial scales. Furthermore, the paucity of studies and the occasional conflict in results precludes identification of species-wide trends. For example, Paragamian (1981) showed a preference of river-dwelling smallmouth bass for gravel and cobble substrate (≤256 mm) rather than boulders during winter. In contrast, Todd and Rabeni (1989) reported that stream-dwelling smallmouth bass associated with boulders almost exclusively during winter. Furthermore, Hubert and Lackey (1980) found

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no difference in seasonal habitat use for smallmouth bass in a Tennessee reservoir with fish using structures such as overbanks, river channels and dropoffs consistently throughout the year. Even within a single waterbody, Webster (1954) noted that overwintering smallmouth bass could be associated with boulders, crevices, or no structure at all. Although these differences may simply represent site- or population-specific preferences, they also suggest that the stimulus for aggregation formation at a site is based more on location than on the microhabitat features that have been quantified to date. Other studies have shown overwintering largemouth bass associated with vegetation, boulders, and rock ridges (Carlson 1992; Karchesky and Bennett 2004), overwintering bluegill associated with submerged vegetation (Cunjak 1996), whereas overwintering pumpkinseed preferred woody debris, cobble-boulders, as well as vegetation Cunjak (1996). The lack of any clear, detectable pattern of preferred habitat at small scales points to a stronger watershed perspective for understanding habitat selection at larger scales. The relatively few studies of wintering habitat selection in rivers (e.g., Langhurst and Schoenike 1990; Carlson 1992) reinforce the need to consider larger watershed scales when examining winter habitat for centrarchid fishes. Winter habitat studies employing telemetry focus on centarchid adults because of the lower size limits imposed by the technology. Winter habitat selection by juvenile centrarchids is therefore an area of research that is largely unexplored. Given the importance of first year survival in centrarchid populations, habitat selection during the critical winter months is an important area for investigation.

9.15 Photoperiod While many of the changes in behavior and physiology described earlier can likely be attributed to reductions in water temperature during winter, some studies have suggested that numerous changes arise independent of ambient water temperatures and are linked to photoperiod. For example, studies have shown that temperature preference (Otto et al . 1976) and swimming activity (Sandstr¨om 1983) can both fluctuate seasonally in fish as a result of photoperiod variation. Additionally, Beamish (1964) showed that the metabolic rate of brook trout (Salvelinus fontinalis) and white suckers (Catastoumus commersoni ) declined within 3 days as a result of starvation, even though water temperature remained constant. In centrarchid fishes, Mischke and Morris (1997) reported that spawning in captive bluegill could be initiated by reducing photoperiod without exposing fish to prolonged winter water temperatures. Laboratory experiments with green sunfish documented that food consumption, food conversion efficiency, and growth all declined with reduced photoperiod when fish were held at constant temperatures (Gross et al . 1965), and work by Petit et al . (2003) revealed that food consumption in largemouth bass was also influenced by photoperiod. Kolok (1991b) showed that the swimming performance of largemouth bass at cold water temperatures was reduced with seasonally inappropriate photoperiod regimes relative to fish experiencing similar temperatures but natural photoperiod regimes. Finally, Evans (1984) showed that pumpkinseed exhibited a temperature-independent drop in metabolic rate associated with reductions in photoperiod, and studies of rainbow trout (Dickson 1971), threespined stickleback (Gasterosteus aculeatus) (Meakins 1975), brook trout (Beamish 1964), and brown trout (Beamish 1964) have all documented a similar seasonal fluctuation in metabolic rate that is not dependant on temperature. Evans (1984) hypothesized that temperature-independent variation in metabolism may be related to predictable winter conditions and designed to reduce maintenance costs when food resources are scarce, thereby increasing the likelihood of overwinter survival. Thus, it is not clear if the observed changes in behavior and physiology exhibited by centrarchid fishes in the winter can be attributed exclusively to water temperature, or if factors associated with variation in photoperiod are also responsible. Kaya and Hasler (1972), for example, suggest that a combination of elevated water temperatures and increased day length is necessary to stimulate gonadal development in green sunfish following exposure to winter conditions.

9.16 Overwinter survival Numerous studies have concluded that survival during the first winter of life represents a “critical period” for many centrarchid fishes often exerting a strong influence on year class strength (Shuter et al . 1980; Parkos and Wahl 2002). Curry et al . (2005) showed that winter mortality for age-0 smallmouth bass in New Brunswick can exceed 78% of the population

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highlighting how large winter-induced mortality can occur at the population level. Currently it is believed that overwinter survival is primarily governed by two processes that are not mutually exclusive: starvation and predation.

9.16.1 Starvation The “classic” theory of overwinter survival for young-of-the-year centrarchids suggests that fish rely on lipid reserves accumulated in summer and fall for overwinter fuel, and mortality results when these lipid stores have been depleted. This reliance on energy stores occurs because winter feeding rates at cold temperatures appear to be significantly reduced (Section 9.11) and many prey items, especially for smaller fishes, are no longer present. As latitude and the degree of winter severity increase, it is hypothesized that this accumulation of lipids for overwinter survival increases in magnitude and importance relative to lower latitudes (Shuter et al . 1980; Schultz and Conover 1997). Lipids represent an efficient, easily deposited, and stable method of energy storage containing 8.0 kcal/g of energy compared with 1.6 kcal/g for carbohydrates and 3.9 kcal/g for protein (Phillips 1969). Currently it is believed that decreasing water temperature stimulates lipid accumulation (Hazel and Prosser 1974; Shul’man 1974), lipid deposits in aerobic muscle (Egginton and Sidell 1989), and increased lipid metabolism (Hazel and Prosser 1974), all to facilitate overwinter survival. Consequently, prior to the onset of winter, lipid levels in wild adult smallmouth bass (Mackereth et al . 1999) and age-0 largemouth bass (Miranda and Hubbard 1994a; Ludsin and DeVries 1997) were at their highest, and were lower during spring sampling—a result corroborated by laboratory studies simulating winter conditions for juvenile largemouth bass (Toneys and Coble 1979) and juvenile smallmouth bass (Oliver et al . 1979). Niimi (1972) noted that largemouth bass starved for 40 days at 25◦ C consumed protein and lipid in a ratio of 60:40, while Savitz (1971) noted that bluegill catabolized both fat and protein to obtain energy during a 29-day starvation experiment at 23.9◦ C.

9.16.2 Allometry Size appears to play an important role in determining lipid stores and energy utilization (and therefore overwinter survival) based on three relationships. First, larger fish store a greater mass-specific quantity of lipids than do the smaller individuals (Shul’man 1974; Shuter et al . 1980; Adams et al . 1982; Shuter and Post 1990; Schultz and Conover 1999; Curry et al . 2005). An allometric accumulation of fat reserves has been shown for several centrarchid species including smallmouth bass (Shuter et al . 1980; Mackereth et al . 1999; Curry et al . 2005), largemouth bass (Adams et al . 1982), and bluegill (Cargnelli and Gross 1997). Two rare exceptions to this trend, however, include Miranda and Hubbard (1994a) and Bernard and Fox (1997) who did not document an allometric relationship for the accumulation of lipids for largemouth bass and pumpkinseed, respectively, potentially as a result of interannual variation in lipid accumulation within a population. Second, the mass-specific metabolic rate of larger fish is lower than smaller individuals (Brett 1965; Brett and Groves 1979). Third, smaller individuals have a greater energetic cost of swimming than do larger fish (Schmidt-Nielsen 1972). Larger fish therefore accumulate more energy stores than do smaller fish, use the accumulated energy at a slower rate, and spend less energy when swimming, thereby increasing their probability of surviving conditions of reduced food intake during winter (Shuter et al . 1980; Schultz and Conover 1999). Most models therefore propose that smaller centrarchid fishes experience increased overwinter mortality relative to larger individuals because of starvation resulting from reduced food intake and elevated energy consumption. This sizeselective mortality hypothesis has been corroborated by both laboratory and field collection studies that pair fall and spring fish collections (Johnson 1965; Oliver et al . 1979; Shuter et al . 1980; Adams et al . 1982; Miranda and Hubbard 1994b; Bernard and Fox 1997; Post et al . 1998; Curry et al . 2005), and in the case of smallmouth bass, this mechanism can account for its northern limit in the biogeographic range of the species (Shuter et al . 1980; Shuter and Post 1990). Experiments that increase ration availability to overwintering largemouth bass permit individuals to maintain energy stores resulting in increased survival (Garvey et al . 1998; Fullerton et al . 2000). Recently, studies have suggested that size-selective starvation may not be the only factor governing overwinter survival in centrarchid fishes. Several studies (Shirley and Andrews 1977; Toneys and Coble 1979; Kohler et al . 1993) report little evidence for size-dependent overwinter mortality among overwintering centrarchids. Additionally, both Adams et al .

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(1982) and Miranda and Hubbard (1994b) reported size-selective overwinter mortality of largemouth bass in Tennessee and Mississippi, respectively, with Kohler et al . (1993) reporting no size-selective overwinter mortality for largemouth bass in Illinois. If the sole factor governing overwinter survival of centrarchid fishes was the interaction between energy stores, temperature, and body size, then one would expect an inverse linear relationship to exist between overwinter survival of small centrarchid fishes and latitude as a result of more severe and prolonged winter conditions at high latitudes (Garvey et al . 1998). In fact, in a literature review by Garvey et al . (1998) examining overwinter survival of largemouth bass, higher survival of large individuals at high latitudes was not consistent among studies (Table 9.2). Additionally, using hatchery ponds in Wisconsin, Toneys and Coble (1979) did not report size-selective overwinter mortality for green sunfish, but noted size-selective mortality for one-third of the bluegill populations and one-half of largemouth bass populations sampled. While this lack of size-dependant mortality may have been observed because the populations examined did not include the extreme northern edge species ranges (Shuter and Post 1990), they do suggest that factors in addition to starvation may be involved in controlling overwinter survival, increasing the complexity associated with overwinter mortality of centrarchid fishes.

9.16.3 Predation Predation is believed to be a second factor that can influence overwinter survival for centrarchids, especially at lower latitudes. As with starvation, predation is more likely to increase winter mortality for smaller fish, as smaller fish may be forced

Table 9.2 Summary of studies examining the effect of size on overwinter survival of largemouth bass.

Source

Latitude (◦ )

Did large age-0 largemouth bass have greater overwinter survival relative to smaller largemouth bass?

Ludsin and DeVries 1997

33

Yesa

Miranda and Hubbard 1994a

34

Yesa

Miranda and Hubbard 1994b

34

Sometimesb

Adams et al. 1982

36

Yesa

Boxrucker 1982

36

Yesa

Shirley and Andrews 1977

36

No

Aggus and Elliott 1975

37

Yesa

Chang 1971

38

No

Isley 1981

38

No

Kohler et al. 1993

40

No

Garvey et al. 1998

40

Sometimesb

Green 1982

43

Yesb

Toneys and Coble 1979

43

Sometimesc

Kolander 1992

45

No

Wright 1993

46

No

Studies are arranged in the order of increasing latitude. Table from Garvey et al. (1998) [NRC Research Press ([email protected]) (CJFAS)]. a In these studies, differential mortality likely resulted from energy reserve depletion during winter. b Mortality of smaller largemouth bass was attributed to predation. c Size-selective mortality occurred in lake studies where predators were present, and did not occur in hatchery pond experiments without predators.

282

Centrarchid fishes

to forage before larger individuals, because of the increased energetic costs described earlier. Both Micucci et al . (2003) and Miranda and Hubbard (1994b) demonstrated that predation was the proximate source of size-dependant overwinter mortality in midlatitude and southern largemouth bass populations, respectively. Predation during winter conditions may either create or mask size-dependant mortality described earlier based on predator abundance and prey availability (Garvey et al . 2004). For example, if prey abundance is low and predators are present, smaller fish may need to forage thereby exposing themselves to predators. Conversely, if prey availability is increased, fish of all sizes can reduce the frequency of foraging bouts, possibly eliminating size-selective mortality despite low water temperatures (Garvey et al . 2004). Finally, the impacts of both starvation and predation on winter mortality appear to be exacerbated at colder temperatures and/or higher latitudes (Garvey et al . 1998; Table 9.2).

9.16.4 Other potential mechanisms for overwinter mortality While starvation and predation are two prominent causes of mortality for overwintering centrarchids, additional reasons for mortality have been suggested. Specifically, during winter conditions, centrarchid fishes may be more susceptible to sub-lethal stressors than at other times of the year, possibly because of reduced energy stores. For example, studies have shown that young-of-the-year largemouth bass are vulnerable to low pH levels during winter leading to mortality because of gill damage (Leino and McCormick 1993; Parkos and Wahl 2002) or osmoregulatory dysfunction in smallmouth bass (Cunningham and Shuter 1986). Peles et al . (2000) showed that radiocesium (137 Cs) levels in largemouth bass peaked in winter/spring months possibly increasing the likelihood of mortality, while Lemly (1993) suggested that winter stress syndrome (WSS) results in greater overwinter mortality for warmwater fishes. Mortality from WSS results from lipid depletion that occurs when external stressors (such as parasites, selenium, or wastewater) increase the energetic demands of fish, but the combination of reduced photoperiod and low water temperatures inhibit feeding to replenish energy stores, thus accelerating death by starvation (Lemly 1993; Lemly 1996). Additionally, Raibley et al . (1997) noted that, when river levels fall during winter, fish are often forced to abandon their preferred still, backwater overwinter habitats for main channel areas. While main channel areas may contain increased levels of dissolved oxygen relative to hypoxic backwater areas, main channel waters are also colder than back water areas and have increased current velocity. Thus, fish inhabiting main channel areas would experience increased activity levels, a reduction in swimming ability (Section 9.7), and a concomitant increase in energy consumption.

9.17 Conclusions and future directions Over 70 years ago Hubbs and Trautman (1935) recognized the importance of winter conditions for the survival of fish and called for an end to the annual indoor migration of fisheries scientists during winter. In particular, Hubbs and Trautman (1935) highlighted investigations of winter habitat requirements and the impacts of winter water levels and ice damage on fish populations as important areas for future research. Little work has been done to quantify winter habitat requirements of most centrarchid species, regardless of age, sex, size distribution, or latitudinal variation. Indeed, ecological research during winter has generally received little attention relative to warmer seasons (Campbell et al . 2005). In general, the strategy for winter survival for centrarchid fishes appears to center around the conservation of lipid stores accumulated during the summer and fall. This can occur through reductions in metabolic rates and reductions in activity levels as fish seek shelter from current and energetically expensive environmental conditions. The physiological strategies employed by centrarchid fishes for overwinter survival currently appear to vary by species, tissue, and enzyme examined, and further study is required before clear trends in this area can be identified. These generalizations, however, are based primarily on the studies of largemouth bass and bluegill, with few studies occurring at the true northern extreme of the species ranges. Ultimately, the ability of a species to tolerate prolonged winter conditions appears to dictate their distribution and range, emphasizing the control of winter conditions on centrarchids. Understanding the physiological, behavioral and ecological responses of centrarchid fishes of all life stages to winter conditions is important.

Winter biology of centrarchid fishes

283

The debate concerning the prevalence of size-selective mortality (e.g., Table 9.2) is in part a debate about ecological processes across a latitudinal gradient ranging from the northern limits of centrarchid distribution to its southern limits. Life history variation detected at latitudinal scales reflects changes in selective process on physiological rates and tolerances across the geographic range of any centrarchid species. Winter (or its corollary, summer growing season) is a very important period in the life history of centrarchid fish. A comparative, latitudinal approach to understanding life history trade-offs (growth versus reproduction) and physiological characteristics of different populations subjected to different winter severities is an important research area for the future. In addition, it is important to examine the winter habitat selection of centrarchid fishes at various life stages. The formation of wintering aggregations, possibly with fish from widely dispersed locations, is an important element of this effort. Entire populations of some species may be located in small areas for extended periods of each year. The impact of land use and habitat destruction on the summer survival and reproduction of many fishes has been documented resulting in management plans and recommended conservation strategies (i.e. maintenance of riparian habitats for lotic fishes). To date, we know very little about the overwintering habitat requirements of the majority of centrarchid fishes (preferred flow rates, dissolved oxygen requirements, water depths, etc.) making successful management decisions challenging. For example, land use activities such as dams or water draw down that reduce winter stream flow will reduce available habitat and access to certain areas for centrarchid fishes and the extent to which these practices affect survival and recruitment has not been adequately quantified (Maceina 2003). Backwater habitats important to the overwinter survival of centrarchids are being lost due to sedimentation and athropogenic disturbances, but the impact of this habitat loss on overwinter survival and recruitment of centrarchids needs to be quantified (Karr et al . 1985; Gent et al . 1995; Knights et al . 1995). Although dredging of backwater areas has shown potential to provide suitable overwinter habitat for largemouth bass, if dissolved oxygen levels are not maintained and flow rates are not optimized, fish will leave the backwater areas for the main channel where flows are greater resulting in an increased probability of mortality (Gent et al . 1995). Recent climate models suggest that global warming will increase North American air temperatures resulting in a corresponding increase in aquatic temperatures (Meisner et al . 1987; Eaton and Scheller 1996; DeStasio et al . 1996; Fang and Stefan 1998). This is expected to be more pronounced for higher latitudes relative to lower latitudes (DeAngelis and Cushman 1990; Fang and Stefan 1998). Accurate predictions regarding the potential cascade of responses by aquatic communities to climate changes are difficult because of unpredictable responses by variables such as dissolved oxygen, wind patterns, macrophyte abundance, watershed connectivity, precipitation patterns, and zooplankton abundance (Chen and Folt 1996; Magnuson and DeStasio 1996; DeStasio et al . 1996). In general, however, it is believed that the predicted increases in ambient temperatures will reduce the severity of winters at high latitudes possibly leading to a northward range expansion of more southerly centrarchid species (Meisner et al . 1987; Regier et al . 1989; Shuter and Post 1990). The relative abundance of various fish species will also likely be affected by temperature change as a result of alterations in thermal niches, prey availability, and oxygen conditions (Meisner et al . 1987). To date, little attention has been paid to the responses of small centrarchid fishes to increased water temperatures (Regier et al . 1989) and relatively little work has focused on the response of southern centrarchids to elevated temperatures. Because of the pronounced impact of winter conditions on the distribution and abundance of centrarchid fishes, the effect of global warming on this family cannot be accurately predicted without a solid understanding of winter ecology. Finally, we must obtain greater understanding of winter ecology of centrarchids to better inform bioenergetics modeling. Currently, many bioenergetics models for overwintering centrarchid fishes assume that individuals stop feeding during winter and often fail to acknowledge the role of predation in influencing overwinter survival (Shuter et al . 1980; Lyons 1997). Studies by Wright et al . (1999) showed that existing bioenergetics models fare poorly in predicting the responses of largemouth bass to winter conditions (possibly because models to date have underestimated the role of predation and feeding in overwinter survival), emphasizing the need to improve our understanding of this period of the year. Winter conditions, and the changes that they bring, represent an interesting, challenging, and important time of the year for centrarchid fishes. Continued research and study should reveal the role of winter on population structure, individual survival, life history variation, and year class strength. Winter field work is accompanied by several inherent challenges, but further study will aid in the management and conservation of this valuable family of fishes.

284

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Chapter 10

Centrarchid aquaculture J. E. Morris and R. D. Clayton

10.1 Introduction Centrarchids have been cultured for stocking for fishery management and more recently as potential commercial culture species. Although these fishes have been cultured since the early 1900s, there is a limited amount of information available for the culturists to produce fish for the food fish market. Expansion of centrarchid aquaculture is limited by the lack of proven, profitable, and sustainable production technologies. Knowledge on basic centrarchid biology is needed to develop aquaculture methodology for the wide variety of centrarchid species.

10.2 Historical review The term “sunfish” refers to any of the 34 species now included in the Centrarchidae family (Chapter 1). Centrarchids are strictly a North American fish family that include, in part, sunfish or bream (Lepomis spp.), crappie (Pomoxis spp.), and bass (Micropterus spp.; Pflieger 1975). Although there are 34 species of centrarchids, the available fish culture literature is limited to those species that have historically been used in fishery management [e.g., primarily bluegill (Lepomis macrochirus) and largemouth bass (Micropterus salmoides), and secondarily black crappie (Pomoxis nigromaculatus)]. Much of the basic production practices should be similar to other centrarchids especially those within the same genera. Centrarchid culture practices date back to the 1930s when federal and state hatcheries first produced warm water fishes in large quantities, focusing on centrarchids and percids (Regier 1962). Culture of Micropterus spp. began around 1890 and continued to grow especially after the 1940s with their use for stocking farm ponds (Snow 1975). In conjunction with pond studies conducted in the 1940s, the combination of largemouth bass and bluegills resulted in the continued growth of centrarchid aquaculture that exists today.

10.2.1 History of centrarchids being used for pond fisheries Both largemouth bass and bluegills have been the principal species used in farm ponds through the United States, bluegills serving both as prey for largemouth bass as well as an alternative sport fish for the fishery. Much of the original impetus for this fish combination can be traced to work done by researchers at Auburn University (Swingle and Smith 1938; Swingle 1946, 1951). Although the initial research arose from southern studies, this species combination has continued to be used today, with minor modifications related to stocking rates, in other regions of the United States, such as the Midwest (Gabelhouse et al . 1982; Morris and Whitcomb 1999).

10.2.2 History of Lepomis spp. hybrids Lepomis spp. are extremely fecund, each female producing an average of 80,000 eggs/year in several successive spawns, which often leads to stunted populations (Carlander 1977). To control the excessive populations of Lepomis spp., 293

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investigators developed Lepomis hybrids because they have reduced reproductive potential as a result of skewed sex ratios (predominately males) or abnormal reproductive behavior (Krumholz 1949; Childers and Bennett 1961; Lewis and Heidinger 1971; Heidinger and Lewis 1972). Becker (1983) notes that Lepomis spp. readily produce hybrids if given the right environmental conditions. Lepomis hybrids also exhibit hybrid vigor with improved growth rates (Childers 1967; Kurzawski and Heidinger 1982; Brunson and Robinette 1983; Engelhardt 1985), high acceptance of artificial feeds (Lewis and Heidinger 1971; Brunson and Robinette 1983; Tidwell et al . 1992), greater tolerance to cooler water temperatures and poor environmental conditions (Heidinger 1975; Brunson and Robinette 1983), and high vulnerability to angling (Kurzawski and Heidinger 1982; Engelhardt 1985; Brunson and Robinette 1986). The earliest research on stocking hybrid sunfish for population control was done by Ricker (1948). Ricker indicated that hybrids between female redear sunfish (M. microlophus) × male bluegill (R × B) had skewed sex ratios, that is, only 2% were females, and were considered as potential stockers for small ponds. Krumholz (1949) found that these hybrids exhibited faster growth and were relatively heavier for their length when compared to parental stocks in small ponds. Childers and Bennett (1961) made all possible crosses among bluegill, redear sunfish, and green sunfish (L. cyanelus). They found that only female bluegill × male green sunfish (B × G), and female green sunfish × male redear sunfish (G × R) hybrids produced significant numbers of F1 offspring naturally. Only female redear sunfish × male green sunfish (R × G) F1 hybrids exhibited a 50:50 sex ratio; all other crosses produced more than 70% males. The following hybrids did not successfully reproduce in later culture periods: female green sunfish × male bluegill (G × B), R × B, and the female bluegill × male redear sunfish (B × R) F1 . Heidinger (1975) investigated the growth of G × B hybrids at low temperatures, below 15◦ C, when stocked with channel catfish (Ictalurus punctatus). G × B hybrids gained weight, while channel catfish lost weight at these temperatures; Heidinger thereby concluded that these hybrids were better adapted for colder climates than channel catfish. Brunson and Robinette (1983) also investigated the growth of hybrid sunfish at low temperatures, 112-day culture period with an average temperature of 10.4◦ C in Mississippi. Winter growth of young-of-the-year bluegill was compared to that of the G × B hybrid. Hybrids increased weight and length compared to bluegill; they outgrew the bluegill by a ratio of approximately 2:1. The intermediate nature of hybrids has been reported in several studies. Etnier (1971) collected female green sunfish × male pumpkinseed (Lepomis gibosus) hybrids, G × B hybrids and their parental species from three lakes in north-central Minnesota. Both hybrids had larger mouths and consumed larger food organisms than bluegill or pumpkinseed, but not green sunfish. Additionally, R × B hybrids raised in ponds with no competition were found to be relatively larger, heavier, and longer than individuals of the same age group in either of the parent species (Ricker 1945; Krumholz 1949; Childers 1967). This increased growth rate is primarily attributed to the reduced fertility or sterility of hybrids (Krumholz 1949; Childers 1967), less energy being diverted to reproduction allows for more energy for growth. Some F1 hybrids have been found to be fertile (Ricker 1945; Laarman 1973), but they typically showed low fecundity and highly skewed sex ratios, which limits their reproductive potential. The fecundity of bluegill females has been reported to be 280 times greater than G × BF1 hybrid females (Laarman 1973). As reported by Kleinsasser et al . (1990), Bailey and Hubbs (1949) recognized two subspecies of largemouth bass; the first subspecies being the northern largemouth bass, M. S. salmoides, which have been used in most fisheries throughout the United States, and the Florida largemouth bass, M. S. floridanus, located originally in Florida. Subsequent information from Chapter 1 now lists two taxa as separate species, M. salmoides and M. floridanus. In a direct comparison between the parental stocks and the F1 hybrids, the female northern largemouth bass × male Florida bass F1 hybrid was found to be the faster growing taxa (Kleinsasser et al . 1990).

10.3 Culture facilities Most of the aquacultural production of centrarchids to date has been through the utilization of small ponds and lakes, whereby adults are stocked and allowed to spawn. Generally, young are raised in the same ponds as the adults (Simco et al . 1986). Ponds used for production of a particular sunfish species should not be contaminated with other centrarchids, because interbreeding is common in this family. Surface water sources must be filtered (e.g., using Saran sock) to prevent introduction of undesirable fish. Some aquaculturists prefer to use ponds with a maximum depth of 0.9 to 1.5 m with some

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shallow areas 0.3-m deep (Higgenbotham et al . 1983). When utilizing pond culture techniques, most brood fish are able to get much of their food requirements from natural production of the pond (e.g., insects and zooplankton). However, brood fish can be fed supplemental commercial feed 3.2 to 6.2 mm in diameter; catfish diet may be used (Dupree and Huner 1984). In areas where regular pond culture is not practical, cage culture of centrarchids might be a viable option. Irregularly shaped ponds, quarry pits, or other bodies of water that cannot be seined easily are all possible areas. Additionally, harvesting and observation of fish is also greatly simplified. Cage culture requires a relatively low initial investment and allows the use of the pond for sport fishing or culture of other species (Masser 1988; Beveridge 1996). Another advantage of cage culture is that it can manage centrarchid reproduction. The suspension of cages off the pond bottom will prevent centrarchids from spawning. Also, cages can be used to control spawning activity to a limited number of spawning cycles; adults are removed from site once initial spawning occurs. Missouri Department of Conservation as well as Iowa Department of Natural Resources hatchery staff, have used cages to hold the brood fish in plastic-lined ponds; spawning trays are placed into each cage (Jim Mainner, Missouri Department of Conservation, personal communication; Andy Moore, Iowa Department of Natural Resources, personal communication). Once newly hatched fry are observed, cages are removed along with the brood fish leaving the fry to grow. When food fish are grown in cages, they are able to utilize some of the pond’s natural productivity, but not nearly as much as free-roaming fish. Therefore, the protein requirement for cage-cultured sunfish is between that of pond-cultured fish and fish cultured in recirculating systems. Best results probably occur when first year stocking densities are reduced for second year final grow-out. Centrarchids can also be cultured using tanks that are either flow-through or closed reuse systems. Most reuse systems are located indoors, which allows the grower to maintain control over the water quality parameters (e.g., water pH, alkalinity, and temperature). The actual production level of indoor tanks depends on water quality parameters as well as flow rates; high flows of high-quality water naturally result in increased fish production. General fish production rates in closed reuse systems vary considerably depending on the type of system and the user’s expertise. Yields can range from 0.03 to 0.10 kg/l for some species, although these figures can be misleading. Also, recirculating systems require a higher level of management than pond production systems (Losordo et al . 1992).

10.4 Lepomis culture (bluegills and their hybrids) 10.4.1 Brood fish Brood fish can be collected using electrofishing equipment, trap nets, seine nets, or other types of nets, if proper collection permits are acquired from appropriate natural resource agency. If fish are captured in some type of net, they should be immediately anesthetized using a governmental approved agent. In the United States, applications of 80 ppm of tricaine methanesulfonate (e.g., Finquel, Argent Chemical Laboratories, Redmond, Washington), has proven to be useful for Lepomis brood fish. If fish are captured by electrofishing, they should be put in fresh water and allowed to recover from the stress of electrofishing for about half an hour before being anesthetized. After being captured, brood fish can then be stripped of gametes and released or kept for future brood fish. Since there is a 21-day withdrawal time for fish anesthetized with Finquel before they can be consumed, they will need to be held for that time period (i.e. 21 days) prior to being released into a fishery. Other anesthesia agents have been used for fin fish. For instance, Peake (1998) found that applications of 2.66-g sodium bicarbonate/l or 60-mg clove oil/l were optimal as anesthetics for use on walleyes (Sander vitreus) at 10◦ C; actual application rate for centrarchids has not yet been determined. Wagner and Cooke’s (2005) review of procedures for transmitter implantation for fish noted that tricaine methanesulfonate was used most often (47%), followed by clove oil (32%). Additional anesthetics used included benzocaine, 2-phenoxy-ethanol, metomidate hydrochloride, and carbon dioxide. If fish are to be stripped of gametes on-site, they should be removed from the anesthetic and their urogenital pore dried with a soft cloth to prevent the anesthetic from interfering with fertilization. Eggs can then be stripped from the ripe female, using gentle pressure on the abdomen, and placed into a damp glass petri dish. Eggs should be fertilized immediately by stripping the milt from one or more males directly onto the eggs. After stripping the eggs and milt, return the fish to the pond and mix the gametes by swirling the petri dish vigorously. Childers and Bennett (1961) present additional information about spawning Lepomis spp. using this technique.

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If the adult Lepomis spp. are kept for future brood fish, then care must be taken in their transport and in acclimation to their new environment. Fish should be transported in water with plenty of oxygen and 1% NaCl (uniodized salt) to reduce osmoregulatory (physiological regulation of internal water/solute concentration) stress. Once fish arrive at the holding facilities, they must be acclimated to the different water chemistry and temperature. This can be done by slowly exchanging hauling water with system water. When producing hybrids, sexing brood fish is critical for stocking proper male to female ratios. The ease of sexing brood fish is a function of the time of year. As with most fish species, Lepomis spp. are more easily sexed during the breeding season. As the spawning period nears, the males take on distinctive, brilliant spawning colors, and milt is usually easy to express from the vent (Dupree and Huner 1984). Females have a much fuller and rounder abdomen than males during the breeding season. With bluegill, a mature male’s urogenital opening usually terminates in a small, funnel-shaped pore (McComish 1968). The area around the opening tends to be darkly pigmented. Other characteristics of males include a square and heavily pigmented opercular lobe, black pigmented gular area, a general dark cast to the body, and a definitive spot at the posterior base of the dorsal fin (Brauhn 1972). The female’s urogenital opening resembles a small, swollen doughnut-like ring, probably the result of a slight eversion of the urogenital tract (McComish 1968). Other characteristics of females include a rounded, less pigmented opercular lobe; a yellow-pigmented gular area; a general light appearance to the body; and a reduced spot at the posterior base of the dorsal fin (Brauhn 1972). Another method of sexing brood fish is probing for eggs. First, use gentle pressure on the abdomen, palpating from the middle of the abdomen back to the vent. If milt is expelled from the urogenital opening, the fish is obviously a male. If no milt appears, the fish is probably a female but needs to be checked with a capillary tube to be certain. Hold the fish upside down and gently insert the capillary tube, 1.1- to 1.2-mm wide and 5- to 10-cm long, through the urogenital opening. Once the capillary tube is inserted into the urogenital sinus, angle it back toward the tail and slightly to one side. When the tube is inserted, place a finger over the end of the tube and remove it. If eggs are seen in the tube, the fish is a female. If no eggs are present and no milt was seen from palpation of the abdomen, then a certain sex determination cannot be made, and the fish should not be used. Brood fish are often maintained on-site of the aquaculture operation or collected from public or private waters. Private aquaculturists will need to obtain the proper collection permits if they care for collecting stock from waters not owned by them. Although most culturists use brood fish from local sources, there has been an increased interest in specific strains of bluegills. In addition to bluegills, copper-nose bluegills (L. M. purpuresens) are sometimes produced for southern ponds and lakes. Engelhardt and McCarty (1990) indicated that cultivation of the copper-nose subspecies coincided with the increased production of the Florida largemouth bass; this strain was noted as having larger body size and improved growth compared to the common bluegill. This interest in strain preference also extends to hybrids. Stinefelt et al . (2004) compared the growth performance of a proprietary of G × B hybrid, Georgia Giant with the standard hybrid. In a direct comparison, the proprietary strain outperformed the standard hybrid, exemplifying the role of strains in culture potential. Bluegills and redear sunfish should be at least 2 years old and 110 to 225 g for maximum productivity (Brunson and Morris 2000). If smaller bluegills and redears are used for spawning, they should be stocked at higher rates to compensate for reduced fecundity and greater variability of spawn size, consistency, and success. Most culturists agree that brood fish should be stocked in the winter, or at least by early spring, at the rate of 50 to 100 pairs/ha. Sex ratios of brood fish in spawning ponds are typically 1:1.

10.4.2 Species selection and hybridization It is very important to be able to identify different species of sunfish, especially when trying to produce hybrids. Pflieger (1975) and Tomelleri and Eberle (1990) provide keys, descriptions, and illustrations for a more definite identification of different sunfish species. Identification of hybrid sunfish can be difficult because hybridization results in animals with multiple species characteristics. Given the high degree of hybridization often seen in Lepomis species, there is a need to be certain as to the purity of stocks being cultured both in single species culture (e.g., bluegills) as well as their hybrids.

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There are two methods that are used to produce hybrid sunfish: stripping and fertilizing eggs in the laboratory, or stocking parent species and allowing them to spawn, usually in ponds. Childers and Bennett (1961) and Smitherman and Hester (1962) described the following methods for stripping and fertilizing eggs in the laboratory. First, select females of the desired sunfish species containing mature gametes, and hand spawn them into damp, glass petri dishes. When milt and eggs are stripped, they should be mixed by vigorously swirling the petri dish. After mixing the milt and eggs, add dechlorinated water and allow 2 minutes for fertilization to occur. Then, place fertilized eggs into clean glass petri dishes containing aged tap water and allow the eggs to become water hardened (∼15 min). After fertilized eggs are water hardened, wash them by raising and lowering the petri dish several times in a container of aged tap water. Fertilized eggs will adhere to the petri dishes, whereas nonfertilized eggs will not. Place the petri dishes of fertilized eggs into aerated aquaria. The eggs should hatch from 41 to 46 hours after fertilization, depending on the photoperiod and temperature. As the amount of light and temperature are increased, hatching time is decreased (Toetz 1966). The second method of producing hybrid sunfish is to stock parent species in fish-free ponds. To prevent contamination with undesirable sunfish, dry the spawning pond thoroughly and treat all depressions with approved fish toxicants before filling and stocking with brood fish. Water from surface sources must be filtered to prevent introduction of undesirable fish. The filter material should have approximately the same size mesh as mosquito netting to prevent admission of larval fish; because of the small mesh size, daily to weekly cleaning is required (McLarney 1987). According to Dupree and Huner (1984), ponds less than 0.4 ha in area are preferred for production of hybrids. After the pond has been properly prepared, select mature male and female sunfish and stock them into the ponds.

10.4.3 Hatchery methods A very important aspect of management of sunfish brood fish is holding brood fish in ponds that are not contaminated with other sunfish; interbreeding is common in this fish family. Before filling and stocking brood fish ponds, ponds should be dried thoroughly and all depressions should be treated with an appropriate fish toxicant. The preferred depth of brood fish ponds is from 0.9 to 1.5 m with some shallow areas 0.3-m deep, whereby nests are constructed and protected by the males (Higgenbotham et al . 1983). Fish should be stocked at a ratio of one male to one female (Dupree and Huner 1984; Engelhardt 1985; Simco et al . 1986). Suggested stocking rates for Lepomis spp. vary with size; 100 pairs/ha for small fish and 75 pairs/ha for larger fish. Spawning activity will begin when the water temperature reaches 21◦ C for green sunfish, 24◦ C for redear sunfish, and 27◦ C for bluegill, and will continue as long as temperatures remain above these levels (Dupree and Huner 1984). Fry are left in the ponds with the adults for 30 to 40 days post hatch, at which time they are harvested from the ponds and distributed. Fry are sometimes stocked into separate ponds to continue their growth. Krumholz (1949) stocked fry at 6200 to 800 000 fish/ha resulting in highly variable survival and growth; research pointed out the need for a sound pond fertilization program. It is important for brood fish to be in good physical condition for maximum spawning success. Fish bioenergetics become critical at this time as investment of the female into yolk production is of critical importance for fry (Jobling 1994). High quality commercial feeds should be fed several times daily. According to Dupree and Huner (1984), when more than 225 kg/ha standing crop is maintained, brood fish should be offered a pelleted feed 3.2 to 6.2 mm in diameter to supplement available natural feed; catfish diet may be appropriate. A floating feed is preferred to a sinking feed because floating feed allows the producer to observe fish on a regular basis. The amount of feed to be fed depends on the water temperature. Feed brood fish five to seven times per week at a rate of 3% of the standing crop when temperatures are above 21◦ C. At temperatures from 13 to 21◦ C, feed the brood fish on alternate days at a rate of 1 to 2% of the standing crop; and when water temperatures are less than 13◦ C do not feed the brood fish (Dupree and Huner 1984). It is also important to increase a pond’s natural fertility to improve fry survival; Lepomis spp. fry consume a wide variety of invertebrates during the larval stage. Numerous authors have suggested amounts of fertilizers needed to support fingerling culture (Dobbins and Boyd 1976; Lichtkoppler and Boyd 1977). These fertilization regimes include inorganic fertilizers, nitrogenous and phosphorus compounds, as well as organic fertilizers that are often in abundance in the local area (e.g., cottonseed meal in southern states and alfalfa meal in Midwestern states). These regimes include both the application of prescribed amounts of fertilizers as well as nutrient ratios (Rogge et al . 2003). Even though past production of sunfish has been mostly extensively in ponds, there has been success in obtaining fry with some intensive laboratory culture methods. Regardless of where sunfish brood, fish are held in ponds, cages, or

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tanks, and their gametes can be stripped and fertilized in the laboratory. Childers and Bennett (1961) hand spawned mature gametes from fish into petri dishes. Toetz (1966) obtained fertilization rates exceeding 70% by mixing spawns from wild female bluegills with a suspension consisting of extracted and macerated testis combined with water. Childers and Bennett (1961) successfully induced bluegill and their hybrids to produce gametes by manipulation of temperature and photoperiod. Banner and Hyatt (1975) also induced bluegill to spawn by manipulating temperature and photoperiod, along with presentation of conspecifics. Bluegill exposed to a-16 hours light: 8 hours dark photoperiod at 25◦ C released gametes when stripped. The presence of male bluegill greatly increased female ovarian development. Also, nest-digging activities increased when a sharp fluctuation in temperature interrupted ambient conditions appropriate for spawning. Other experiments have also been successful in artificially reproducing sunfish using similar methods (Smitherman and Hester 1962; Merriner 1971; Smith 1975). Bryan et al . (1994) manipulated temperature and photoperiod along with artificial spawning nests to induce bluegill courtship and spawning in the laboratory. After spawning, males were allowed to defend the nests for 12 hours. Nests were then removed and placed into 38-l flow-through aquaria. At 26◦ C, eggs hatched in 36 hours. Larval sunfish were transferred to rearing chambers at 3 days post-hatch and fed Artificial Plankton Microcapsules (AP, Argent Chemical Laboratories, Redmond, Washington). At 9 days post hatch, brine shrimp (Artemia) were fed to the fish three times daily. No survival rates were given. Mischke and Morris (1997) developed a protocol for handling brood fish and out-of-season spawning for intensive culture of sunfish through manipulation of temperature and photoperiod. After spawning, the nests were removed, eggs were allowed to hatch, and fry transferred to aquaria for swim-up. Mischke and Morris (1998) transferred larval bluegill to rearing chambers at 7 days post-hatch and conducted several feeding studies. They found that larval bluegill would not digest commercial feeds at the onset of exogenous feeding. However, by feeding brine shrimp nauplii (newly hatched brine shrimp) for 14 days and then weaning larvae to Fry Feed Kyowa B-250 (Biokyowa, Incorporated, Tokyo, Japan), survival rates of about 43% were obtained. Mischke et al . (2001) determined that the combination of using brine shrimp for G × B hybrids for at least 7 days followed by a commercial diet allowed for a survival rate of approximately 40%. If Lepomis fry are held in aquaria while they absorb their yolk sacs, they should be siphoned from the aquaria before they reach swim-up; bluegill larvae reach swim-up at 7 days post-hatch (Mischke 1995). After being siphoned from the aquaria, larvae may be transferred to rearing chambers or tanks held at 25◦ C, the preferred growth temperature of larval bluegill (Beitinger and Magnuson 1979; Bryan et al . 1994), and feed offered. The 4 to 9 days post-hatch is the critical stage in larvae Lepomis development, as they switch from endogenous (energy is derived internally from the yolk sac) to exogenous (external) feeding (Toetz 1966; Smith 1975). During this critical stage, nutrients from the yolk sac are utilized and the sunfish’s mouth opens; fry will die if they do not begin feeding at this critical stage. Proper feed for larval sunfish must be small enough so that the fish can physically handle it. Toetz (1966) reported the mouth gape of larval bluegill at the onset of exogenous feeding to be 230 to 270 µm. The mouth gapes of redear sunfish and pumpkinseeds are probably very close to that of the bluegill; the mouth gapes of green sunfish are probably larger. If the sunfish survive the critical stage and begin feeding in the wild, their first food consists of small zooplankton (e.g., rotifers and copepod nauplii). Sunfish growth is rapid and will select increasing larger prey (Siefert 1972). When intensively culturing sunfish fry, a commercial feed smaller than 250 µm should be used as the first feed, and progressively larger feeds should be offered as the sunfish grow. When changing to larger feeds, mix the larger feed with the smaller sized feed for a couple of feedings to allow the fish to adapt to the larger feed size.

10.4.4 Use of triploid technology Induced polyploidy in Lepomis culture could potentially overcome many impediments to their development for the food fish market in the Midwest (Mischke and Morris 2003). Polyploidy refers to the condition of having three or more full sets of chromosomes instead of two found in normal diploids thereby decreasing reproductive potential. In a project funded by the North Central Regional Aquaculture Center, Michigan State University and Southern Illinois University, Carbondale investigators developed methods for inducing and evaluating polyploidy in bluegill sunfish and G × B hybrids. Triploid and tetraploid bluegills were produced using cold shocks. Hydrostatic pressure shocks were superior

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to temperature shocks, because high survival (>90%), 100% triploidy, and no deformed individuals were produced (Wills et al . 1994).

10.4.5 Grow-out methods Producers often depend on natural organisms such as zooplankton and benthic organisms as the main food source. However, as these natural food sources can be quickly depleted at high stocking densities, producers should consider using supplemental diets to enhance growth in high-density sunfish pond production. The stocking rate for grow-out of G × B hybrids is 12,355 to 17,279 fish/ha (NCRAC 1999). As the accepted food size for sunfish is 227 to 340 g, Lepomis spp. require 2+ years to reach this size. Best production is often gained by stocking a higher density during the first year of production followed by decreased stocking numbers in the subsequent years. There is a difference between Lepomis taxa in pond culture. Lane and Morris (2002) compared the feed utilization and fish growth between bluegills and G × B hybrids. The G × B hybrid made better use of the commercial diet (36% protein) whereby they had better growth than bluegills under identical culture conditions. Unlike pond production, a truly complete diet is required for sunfish in recirculation. Crude protein levels required for recirculating culture are estimated to be >40% (NCRAC 1999). Stocking densities for sunfish in recirculating systems have not been adequately determined at this time. Lepomis spp. fingerlings are stocked at 10 cm or larger and graded for uniformity in size. Five hundred sunfish fingerlings can be stocked in a 0.12 × 0.12 × 0.12-m square cage; 2000 sunfish can be stocked in a 0.24 × 0.24 × 0.12-m cage (Masser 1988). NCRAC (1998) gives the guideline of 200 fish/m3 for cage culture. As with pond culture, best results probably occur when first year stocking densities are reduced for second year final grow-out. Commercial producers will often use a commercial channel catfish diet to feed fish in cages, 36% protein with 4 to 6% lipid.

10.4.6 Nutrition Tidwell et al . (1992) suggested that using higher protein feeds (35% or greater) may improve growth and production potential of G × B hybrids. Hybrids fed three diets, 40, 44, and 48% protein, had higher whole-body protein and lower whole-body lipids than hybrids fed 35% protein diet (Webster et al . 1992). For both bluegills and G × B hybrids, fish fed commercial trout diets (40–44% protein, 10–11% lipid) outperformed those fed commercial channel catfish diets (32–36% protein, 4–6% lipid) (Twibell et al . 2003). Stinefelt et al . (2004) also noted that G × B hybrids grew best using a diet that had 42% protein and 16% lipid. Work with hybrids in recirculating systems and in ponds suggests that when the formulated diet supplies virtually all the nutrition, best growth was obtained using feeds containing 44% protein and 8% lipids (Hoagland et al . 2003). In a study investigating the use of three commercially available high-protein (>45% protein) diets, age-1 redear sunfish accepted all diets after a 3-week training period (Cook and Scurlock 1998). Fish fed Ziegler Salmon Starter #4 (Zeigler Brothers, Inc., Gardners, PA) had food conversion rates (FCR) of 1.33 compared to FCR values of 3.28 and 3.21 for Biodiet Starter Diet #3 (Bio-Oregon, Inc., Warrenton, OR) and Fry Feed Kyowa B-250 (BioKyowa Inc., Tokyo), respectively. Tidwell et al . (1992) and Webster et al . (1992) reported specific growth rate (SGR) values of 1.98 and 2.6, respectively, using small fish (3 to 5 g). Webster et al . (1997) and Tidwell et al . (1994) both noted lower SGR values for larger fish. Webster et al . (1992) reported FCR values of 3.72 and 3.87 at 32 and 38% crude protein, respectively, using smaller fish (3–4 g). Webster et al . (1997) obtained slightly higher FCR values for larger fish. High FCR values were reported for large fish stocked in ponds for the summer growing season (Tidwell et al . 1994; Lovshin and Mathewa 2003). Alternative feeding schedules, which elicit compensatory growth, have been used to substantially increase growth rates of juvenile Lepomis hybrids sunfish using mealworms (Tenebrio molitor; Hayward et al . 1997). The best results occurred for fish fed on continuous cycles of 2 days off feed followed by 6 days of unrestricted feeding. The larger sizes were achieved with no loss of feed conversion, and body composition appeared no different than for normally fed controls. Further work has shown that this very rapid growth from compensatory growth occurs only under certain conditions (Hayward et al . 1999; Hayward and Wang 2002).

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Other factors, such as: whether fish are held individually or in groups (social costs), time of year, fish age, and food type, may affect the outcome of compensatory growth. Wang et al . (1998) studied the effects of daily feeding frequency on growth rates of juvenile G × B hybrids. Results indicate that three daily feedings produce the highest growth rates, but knowledge of how much to feed at each time is important to avoid overfeeding and underfeeding. Webster and Tidwell (2002) present detailed information regarding Lepomis nutrition under a variety of culture conditions as well as life stages. Additional information includes feeding regimes as well as vitamin and amino acid profiles.

10.4.7 Environmental conditions Several authors have reported the optimal temperature range for Lepomis spp. to be from 20 to 30◦ C (Breder 1936; Banner and Hyatt 1975; Carlander 1977). Additionally, most sunfish will spawn when temperatures are within this range (Carlander 1977). Growth rates of sunfish will generally increase as temperatures increase up to approximately 30◦ C, and then decrease as temperatures increase above 30◦ C (Carlander 1977; Lemke 1977; Beitinger and Magnuson 1979). Lemke (1977) reported the highest mean SGR values, 2.35% per day, to occur at 30◦ C from bluegill grown for 30 days at 2◦ C temperature increments from 20 to 36◦ C. Beitinger and Magnuson (1979) reported growth of bluegill to be greatest at 31◦ C, but not significantly different from fish at 25◦ , 28◦ , and 31◦ C. Temperature not only affects growth of sunfish, but also has an effect on survival. Bluegill eggs will hatch at temperatures ranging from 23 to 34◦ C. Banner and Van Arman (1973) hatched bluegill eggs at 34◦ C; however, 50% mortality occurred. They also reported eggs at different temperatures; maximum hatch rate occurred at 22◦ C in one experiment and at 24◦ C in a second experiment. Fry have a greater thermal tolerance range than eggs; juveniles have a greater thermal tolerance than fry and eggs (Banner and Van Arman 1973). Wrenn et al . (1979) found a hatching success mean of 95% for bluegill eggs within the 23 to 34◦ C temperature range.

10.4.8 Harvesting and processing Fingerling harvest is often limited to fish of at least 50 mm, a size often used in pond and lake stocking programs (Brunson and Morris 2000). Fingerling transportation is best postponed to fall, whereby the cooler water temperatures help to minimize hauling stress. In addition, bluegills are most often stocked into waters in the fall followed by spring stocking of largemouth bass. Pond harvest is commonly done using a soft mesh seine; 8-mm mesh for 37+ mm fingerlings and 12-mm mesh for larger fish. It is best to use nontarred seines as this mesh is less harmful to these delicate fish. To date, there is little information as to the actual processing of Lepomis fishes. Lane (2001) investigated the culture of both bluegills and G × B hybrids in ponds. There are significant differences in both skin-on fillets and in-the-round percentages with bluegills having the best percentages. Bluegills had 36% skin-on fillet compared to 32% for the hybrid sunfish and 62% in the round compared to 58% for the hybrid sunfish.

10.5 Pomoxis spp. culture 10.5.1 Brood fish To date, there are limited reports that discuss black crappie, also called calico bass (Harper 1938) or white crappie (P. annularis) brood fish. Stocking rates for brood fish vary widely. Higginbotham (1988) suggested a rate of 7 to 20 pairs/ha for black crappie. Dupree and Huner (1984) reported a rate of 99 pairs/ha stocked with equal sex ratios. Stocking rates of 250 adults/ha actually limited fish production (Martin 1988; Smeltzer and Flickinger 1991). Smeltzer (1981) as reported by Simco et al . (1986) indicated that the best fingerling production was obtained by stocking brood fish at 125 adults/ha.

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Harper (1938) noted that black crappie were hardier than white crappie and suggested a stocking rate of 7 to 12 pairs/ha; this stocking rate produced over 12 939 fingerlings/ha. Myers and Rowe III (2001) suggested a brood fish sex ratio skewed toward more males. Fathead minnows (Pimephales promelas) are commonly provided for forage. However, threadfin (Dorosoma petenense) and gizzard shad (D. cepedianum) have also been used (Stickney 2000). Similar to the high incidence in hybridization exhibited by Lepomis spp., crappie can naturally hybridize (Buck and Hooe 1986; Dunham et al . 1994). The black crappie and both hybrids had better body condition and growth than did the white crappie. As with other centrarchids, brood fish are often maintained on-site of the aquaculture operation or collected from public or private water using electrofishing equipment, trap nets, seine nets, or other types of nets. Private aquaculturists will need to obtain the proper collection permits if they collect stock from waters not owned by them. Black crappie brood fish can spawn at 1 year of age; however, most producers use 2-year-old fish (Stickney 2000). Martin (1988) used age-3 crappies for brood fish. Stickney also stated that the two species may also be stocked in the same pond. Smeltzer and Flickinger (1991) restricted their brood fish to >200 mm total length (TL) while Higginbotham (1988) noted that most culturists prefer brood fish that range in size from 454 to 567 g. Smeltzer and Flickinger (1991) used four criteria for sex determination: (i) body coloration (males being darker just prior to spawning), (ii) gametes if present, (iii) urogenital morphology, and (iv) abdominal distention (females being visibly swollen with eggs). Males had a urogenital area entirely scaled that was round to oval. If the scaleless area was shaped more like a teardrop or pear, and the posterior genital opening was swollen like a doughnut, it was a female—similar to McComish’s (1968) information for bluegills. As with other fish, many of these sexual characteristics were more prevalent closer to the actual spawning season.

10.5.2 Hatchery methods As previously noted, the stocking rates for brood fish are highly variable, ranging from less than 10 pairs/ha to a maximum of 250 adults/ha, which often results in variable fish production (Higginbotham 1988; Smeltzer and Flickinger 1991). Smeltzer and Flickinger (1991) determined that brood fish stocked at densities of 100 to 125 fish/ha with sex ratios close to 1:1 resulted in the greatest fingerling production. Although private culturists will often place additional structure into culture ponds, this study found additional brush did not enhance fish production. Myers and Rowe III (2001) found that black crappie production was highly variable but averaged 52 681 fish/ha. After a 11-month culture period, the fish had a mean TL of 76 to 219 mm. As with the culture of Lepomis spp., a fertilization regime needs to be established for ponds used in crappie production (Martin 1988). This regime can include both organic and inorganic fertilizers as well as nutrient ratio modifications. In contrast to Lepomis culture, there is a limited amount of information on the hatching of crappie indoors.

10.5.3 Grow-out methods Black, white, and hybrid crappie are more difficult to habituate to prepared diets and they do not feed as aggressively as hybrid bluegill in indoor tanks, especially at lower water temperatures; black crappie were the best performing crappie taxa under these conditions (NCRAC 1996). Pond production methods suitable for hybrid sunfish are not suitable for black crappie (NCRAC 2000). Black crappie had poor growth and survival, and appeared to be subsisting on the natural food supply rather than the production diet. To date, there have been few studies that have cultured either crappie species to the food fish stage indoors. There have been a limited number of studies that describe feed training for black crappie. Smeltzer (1981) had the best success feed training black crappie, up to 95%, using a 7-day program, carp egg to Bio-diet sequence. The use of smaller fish, <3.8 cm, and small troughs with some horizontal water movement yields the best results. Smeltzer and Flickinger (1991) recommended similar strategies using a soft-textured terminal diet as well as a culture tank that promotes food particle suspension. To date, there is no published literature that describes crappie culture in cages that the authors are aware of.

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10.5.4 Nutrition To date, the authors are not aware of any published literature that describes crappie nutrition in detail. Given the similarity between these fish and other members of the centrarchid family, it is anticipated that these fish would do well when fed a commercial diet consisting of at least 40% protein and ca. 8% lipid.

10.5.5 Role of stress in handling Strategies for handling black crappies without causing stress-induced loss have been developed (Smeltzer 1981; Smeltzer and Flickinger 1991; Stickney 2000). Often there is an incidence in Columnaris as well as Saprolegnia diseases in these fish soon after they have been handled (Stickney 2000).

10.5.6 Harvesting and processing Fish are often cultured until they reach 7.6 mm, which is most often in the fall when the water temperatures are cool. To reduce stress in crappies, fingerlings are harvested using a soft-mesh uncoated seine similar to that used for other centrarchids. In addition, crappies need to be transported in tanks using salt as well as oxygen (Higginbotham 1988; Stickney 2000). The use of chilled water is more stressful than using ambient water for transport (NCRAC 1999). The use of an isotonic concentration of salt (NaCl) appears to be most beneficial for transporting crappies.

10.6 Micropterus spp. culture 10.6.1 Brood fish There are two recognized species of largemouth bass; the northern largemouth bass, M. salmoides, and the Florida largemouth bass, M. floridanus (Chapter 1). Florida largemouth bass are limited to the southern region of the United States due to their limited survival in cold winter temperatures. Both the Florida largemouth bass and the F1 hybrid (northern largemouth bass female × male Florida largemouth bass) are cultured in the southern United States for use in fisheries due to their improved growth. Micropterus spp. brood fish will often lose 10 to 30% of their body weight during their spawning period (Simco et al . 1986). Supplemental feeding of these fish is possible using live baitfish; 3:1 baitfish to brood fish weight. However, Dupree and Huner (1984) noted that the ratio of forage to brood fish biomass should be closer to 6:1. Forage should also be excluded from the spawning ponds. Baitfish may include fathead minnows or golden shiners (Notemigonus crysoleucas). As previously noted, Florida largemouth bass has been identified as an excellent alternative to the northern largemouth bass in southern fisheries. Williamson and Carmichael (1990) did a direct comparison of the different subspecies of largemouth bass and their hybrids to determine their utility in aquaculture operations. Based on food trainability, growth, survival, and stress response, the northern largemouth bass was identified as having the best potential for aquaculture. As with other centrarchids, Micropterus brood fish are often maintained on-site of the aquaculture operation or collected from public or private water using electrofishing equipment, trap nets, seine nets, or other types of nets. Private aquaculturists will need to obtain the proper collection permits if they are collecting stock from waters not owned by them. Most largemouth bass are sexually mature at 1 year but may not reach sexual maturity until their second year when they are experiencing slow growth (Moorman 1957; Regier 1962 as noted in Carlander 1977). Largemouth bass reach sexual maturity in 1 year in southern states and may take 3 to 4 years in more northern states. Fecundity of this species is estimated and is highly variable but averages 8800 eggs/kg of female (Nickum 2004). Spawning often occurs when water temperatures reach 15.5◦ C; males build nests in depths that range from 0.3 to 2 m (Carlander 1977).

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Smallmouth bass will usually become sexually mature at 3 to 4 years and like other centrarchids, their maturity can be extended due to environmental conditions (Carlander 1977). Brood fish are typically 0.4 to 1.0 kg (Hutson 1983). The number of eggs per female range from 15 000 to 18 000 eggs/kg; body size influences number of spawnings as well as number of fry produced. However, Carlander (1977) notes that often the number of eggs is not related to size of female. Smallmouth bass spawn earlier than most centrarchids (Hubbs and Bailey 1938 as reported by Carlander 1977); spawning starts when water temperature reaches 13◦ C with spawning taking place at 15◦ C. Nests are often constructed in sandy-rock locations. As indicated earlier, sexual maturity depends more on size than age (Moorman 1957). Females and males mature when they reach 25 and 22 cm, respectively (Heidinger 2000). Brood fish are often replaced when they reach 1.8 to 2.3 kg or 4 to 5 years of age (Heidinger 2000).

10.6.2 Hatchery methods In preparation for the upcoming culture season, largemouth bass brood fish are often held in holding ponds. Fish can be held in these ponds at 336 to 448 kg/ha (White 1988). Brood fish may be either fed a commercial diet, 3% of their biomass except in the winter when they are fed 1%, or a live diet, 3 kg of prey per kilogram stocked for maintenance or 5 kg/kg of bass for growth (Heidinger 2000). Smallmouth bass are sometimes fed using 5- to 7-cm goldfish at a rate of 5 to 7 kg/kg of brood fish (Hutson 1983). Depending on production goals for the hatchery, the actual number of brood fish as well as their genetics is important to the fish culturist. Largemouth bass fingerlings may be cultured using two types of methods. The first is sometimes referred to as spawning-rearing system whereby the adults are left in the pond with the fingerlings until fish are harvested. The second type of culture system is referred to as fry-transfer system (Snow 1975). In the spawning-rearing system largemouth bass brood fish should be stocked at 25 to 100 fish/ha (Snow 1975; Heidinger 2000). Fingerlings are harvested after a culture period of 40 to 65 days. Snow (1975) notes this system had no control over stocking density of fingerlings other than controlling number of brood fish as well as the possible predation by the adults upon the young fish. In the fry-transfer system, Snow (1975) recommends stocking brood fish at 99 to 247 fish/ha and that more males than females be used. Using these stocking rates, as many as 1 235 000 fry/ha could be obtained, but often the average numbers are less than half of this number. Lock (1988) suggests that up to 140 kg/ha of brood fish can be stocked when fry are transferred to separate rearing ponds. Fry are often stocked into nursery ponds at 99 000 to 198 000 fry/ha (Heidinger 2000). Actual numbers were estimated using weight/volume estimations. As with other fishes, ponds used for fingerling production are often fertilized using a combination of fertilizers to allow for increased aquatic invertebrate production; increased amounts of invertebrate prey improve fingerling production. Largemouth bass fry, 4-day, initially consume rotifers switching to copepods and later cladocerans soon thereafter (Wickstrom and Applegate 1989). Fish then switch to larger invertebrates (e.g., insect larvae). Insect larvae become increasing important in smallmouth bass diets once they reach 20-mm TL (Farquhar and Guest 1991). Largemouth bass brood fish are stocked into ponds prior to spawning season. These ponds can be 0.2 to 1.2 ha and should be free of rooted vegetation and be constructed to allow for adequate fish harvest (Dupree and Huner 1984). A good ratio of female:male is 3:2. Once fry hatch, they may be removed using an 8-mm soft-mesh seine while they are still in a school and placed into a rearing pond, which has been fertilized. Male largemouth bass may guard their fry during their school stage, 2 weeks or less. Ponds can be stocked at 100 000 to 200 000 fry/ha (Nickum 2004). In contrast to largemouth bass fry, smallmouth bass fry are collected before they leave their nest (Dupree and Huner 1984). In this paper, the authors describe a cylindrical frame 0.9-m diameter and 1.0-m deep, covered with window screen, placed over each nest prior to fry leaving it. In a similar fashion, Texas culturists used portable nests, one box contained into a larger box whereby fry are removed using the small box and placed into wire boxes until swim-up (Hutson 1983). Fry are then collected from each enclosed area as they leave their nest and stocked into fertilized culture ponds. Another means of collecting centrarchid fry from individual nests is the use of a portable underwater suction device similar to a modified air-lift pump (Vogele et al . 1971). Eggs and larvae of both largemouth and smallmouth bass can be collected in approximately 30 minutes from an individual nest.

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Fingerlings are often harvested when they reach 4 to 5 mm in length, as this is the size that they will begin to cannibalize (White 1988; Heidinger 2000). Fish are then either marketed or stocked into ponds as part of a fishery or retained and cultured until they reach 15 to 20 cm in length, a size highly desirable for pond and lake stockings (Heidinger 2000). To date, there is a limited amount of information on Micropterus culture in indoor systems although there have been some private producers culturing these fishes indoors. Sparrow and Barkoh (2002) described intensive culture of smallmouth bass. Eggs are removed from the spawning trays used in plastic-line production ponds using 1.5% sodium sulfite solution. Eggs are then placed into McDonald hatching jars at 40 000 to 80 000 eggs/jar. Care is taken during the initial 24 hours after stocking as smallmouth bass are extremely vulnerable to disturbance at this time (Inslee 1975).

10.6.3 Feed training The production of largemouth bass to 15 to 20 cm length using commercial diets can be historically traced to the 1960s to Jack Snow, U.S. Fish and Wildlife Service (Snow 1968; Snow and Maxwell 1970; Tidwell et al . 2000). Refinement of this technique has continued for both the public and private fish culturists. The concept of feed training of fishes, especially piscivorous species, requires the transition of fish from a natural diet to a commercial diet. Given the well-known nature of largemouth bass to cannibalize, the initial feeding training regime starts with fingerlings being harvested at 4 to 5 cm from fingerling ponds and graded for uniform sizes (Tidwell et al . 2000). Fish are then stocked into flow-through tanks at 7100 to 18,000 fish/m3 , actual density being dependent on water flow. Heidinger (2000) indicated that the initial stocking be 3013 fish/l or 5 to 7 g/l with this group sorted using a bar grader several times over a 7- to 10-day training period. Fish are then offered a variety of transition feeds that can include freeze-dried krill, ground fish flesh, fish eggs, or even beef liver. The palatable diets are gradually mixed with the commercial diet, usually a salmonid diet, over a 7- to 14-day period (Willis and Flickinger 1981; Kubitza and Lovshin 1997a; Heidinger 2000; Tidwell et al . 2000). Feed-trained fish can easily been sorted out due to their pronounced bellies. About 80 to 90% of the fish should accept commercial diets under optimal conditions; moist and semimoist diets work best. Heidinger (2000) indicates that it is often easier to train offspring of previously trained fish relative to na¨ıve individuals. Both hand and mechanical feeding as well as supplemental lighting can be used during this training period. In addition to the numerous publications on feed training of largemouth bass, Flickinger et al . (1975) investigated feed training smallmouth bass. Best success was obtained using 5 mm fish being fed a training diet similar to largemouth bass as well as using moist diets.

10.6.4 Grow-out methods Following this initial training period, fish are then stocked out into ponds and cultured until they reach the desirable 15- to 20 cm market size as advanced fingerlings for sport fish stocking. Fish are stocked at 37 000 to 74 000 fish/ha (Heidinger 2000; Tidwell et al . 2000). The culturist can expect a 40 to 50% retention rate of the feed training. This percentage improves from 90 to 95% if the feed-trained fingerlings are confined to cages or areas of a pond for 7 to 10 days during their initial culture period. Fish are fed 2 to 3 times daily using a 40 to 48% protein diet with 8 to 10% fat. Although largemouth bass have been cultured using commercial diets since the 1960s, their feeding activity is often influenced by variable water temperatures and environmental conditions. Largemouth bass will often reach 15 to 20 cm during their first fall. At this time, these fish can be used for stocking in the fall or retained for the following culture period. In the next culture period, fish are often stocked out at 3700 to 4940 fish/ha and fed a high protein salmonid diet (Heidinger 2000; Tidwell et al . 2000). Tidwell et al . (1996 and 2000) note that these fish can be stocked at levels approaching 12 355 fish/ha, fed 46 to 48% protein diet with 6 to 8% lipid in one daily feeding to satiation with production levels reaching 5000 kg/ha. FCR of largemouth bass ranged from 1.07 for juveniles to 1.42–1.46 for food fish (Kubitza and Lovshin 1997b). Florida largemouth bass reared on pellets grew faster and had larger mesenteric fat and gonadal somatic indices at all times of the year compared to largemouth bass (Rosenblum et al . 1994). As with the nursery stage, there is a limited amount of information about culture of these fish in indoor systems. Similarly, in contrast to Lepomis spp., there is no published literature on Micropterus spp. culture to food size in cages.

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10.6.5 Nutrition As with other centrarchids, Micropterus spp. required higher protein feeds than other fishes such as channel catfish (Tidwell et al . 1998; Bright et al . 2005). A diet containing 7 to 16% lipid is sufficient for fish growth in juvenile largemouth bass when they fed on a diet containing 40% protein. Food fish can be produced using a commercial diet containing at least 44% protein. Ashley (1974) and Goodwin et al . (2002) report that juvenile largemouth bass fed diets with excess carbohydrate (>25%), have livers with hepatic lesions. Goodwin et al . (2002) report that livers with gross lesions were enlarged by glycogen, but with translucent pale areas and pink nodules on the surface. Histological examination showed that translucent regions of the liver contained few hepatocytes, and were composed of granulomas. The pink nodules were areas of regeneration of hepatocytes. They concluded that bass livers were accumulating glycogen in their hepatocytes to explain the massive necrosis (i.e. cell death of the liver). Fish fed a diet with 45% protein and <25% carbohydrate not only did not have this problem, but also grew faster.

10.6.6 Environmental conditions As with other centrarchids, Micropterus spp. are somewhat tolerant of varying water quality conditions, including water pH and ammonia levels. This tolerance is between salmonids and ictalurids (Heidinger 2000).

10.6.7 Harvesting and processing Fish should be harvested under cool temperatures and overcast days if possible. As with other centrarchids, bass fry can be harvested using a seine consisting of soft netting. Williamson et al . (1993) presented detailed information on harvesting and transport strategies. Fry can be shipped using plastic bags filled one-fourth with water, and oxygen and stocked with 2000 to 12,000 fry/l (Heidinger 2000). In addition, juvenile largemouth bass can be transported in tanks for 4 to 6 hours when water temperature is less than 20◦ C, at stocking rates of 26 to 53 fish/l.

10.7 Future for centrarchids as aquaculture species Although there is some basic culture information about individual centrarchid taxa, there are basic guidelines missing that exist for other culture species (e.g., channel catfish; Table 10.1). This information includes genetics related to domestication, controlled reproduction as well as feeds actually formatted for that specific taxa. In the authors’ opinion, centrarchid taxa that have the highest culture potential include bluegill Lepomis spp. hybrids and largemouth bass (Table 10.2). The potential other centrarchid taxa is dependent on new research as well as market potential.

10.7.1 Economic concerns As centrarchid aquaculture is relatively new and spread throughout the United States, there is very little information on marketing and economics of these species (Morris et al . 2006). In 1999, personnel from the NCRAC Publications Office at Iowa State University conducted a survey of state aquaculture specialists and aquaculture coordinators in the United States to determine the number of producers, species of sunfish cultured, and the primary markets utilized. There are an estimated 400+ producers of sunfish nationally; Texas and Wisconsin reported the greatest numbers of producers. Idaho is the only western state that reported commercial sunfish producers. The most commonly produced sunfish taxa is the bluegill followed by miscellaneous Lepomis spp. hybrids and redear sunfish. The primary markets for sunfish are sport-fish stocking and fee-fishing operations. In the Midwest, it is estimated that 74% of the producers utilize the sport-fish market for sale of their sunfish; approximately 20% of the producers utilize fee-fishing as a market. Detailed

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Table 10.1 Known information on commonly cultured centrarchid species. Stocking rates Brood fish Species

No./ha Ratioa

Bluegill

50–100

1/1

No. of fry/ha

Spawning temperature (◦ C)

6200–800,000

27

Diet requirements

Harvest techniques

Floating feed

Soft mesh seine

+35% protein Redear sunfish

50–100

1/1

6200–800,000

24

Floating feed

Soft mesh seine

+35% protein White crappie Black crappie

7–125

1/>1

Northern Largemouth bass 25–100

2/3

10,000–200,000

Florida largemouth bass

15.5

40% protein

Soft mesh seine

40–44%

Soft mesh seine

15.5

Smallmouth bass

13

a Ratio is number of females to males.

Table 10.2 Culture potential of selected centrarchid species. Culture potential noted by authors’ viewpoints. Species

Food fish

Pond stocking

Culture potential

Bluegill

X

X

High

hybrid (L. cyanellus × L. macrochirus)

X

–

High

Redear sunfish

–

X

High

White crappie

–

X

Low

Black crappie

–

X

Low

Northern Largemouth bass

X

X

High

Florida largemouth bass

–

X

Low

Smallmouth bass

–

X

Low

summaries of sunfish markets and marketing are needed, as presently, there is no sound data to indicate how broad the markets are for either pure sunfish or hybrids. In some states, it is not legal to raise largemouth bass for food or stocking (Heidinger 2000). Given this legality, the interstate transport of centrarchids is best taken with a thorough understanding of individual state regulations as they are related to both the stocking and transportation of sport fish.

10.7.2 Use for centrarchids beyond pond fisheries and food fish Beyond the conventional use of cultured centrarchids for fisheries or food-fish purposes, there are additional reasons the culture of selected centrarchids may be desirable. For example, redear sunfish can be used for the control of snail populations in ponds needed to curb parasitic outbreaks. Digenetic trematodes (class Trematoda) often plague pond-reared fishes. Whereas most digenetic trematodes are not a serious threat to fish health, their mere appearance often renders the fish undesirable by consumers. The black grub (Uvulifer ambloplitis), white grub (Posthodiplostomum minimum), and

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yellow grub (Clinostomum complanatum) are commonly seen digenetic trematodes in fish in earthen ponds (Olsen 1962; Lane and Morris 2002). In addition to searching for chemical control of snails in aquaculture ponds (Mitchell and Hobbs 2003), other researchers have sought biological control of snails using fish (e.g., known for their consumption of snails). Redears are well known to consume snails and have been called “shellcrackers” (Huish 1957 as described byPflieger 1975). Wang et al . (2003) investigated the use of redear sunfish for controlling Physa and Helosoma populations. Their results noted that redear sunfish larger than 15-cm total length can consume all sizes of Physa gyrina. However, only larger redear sunfish, larger than 32 cm, are capable of consuming the full range size of Helisoma trivolis. In addition to their uses for fisheries and aquaculture, some centrarchid species have recently been used for the ornamental trade industry. A desirable ornamental species is one that retains a small size, is easily reproduced, colorful, and is tolerant of limited water conditions. The orangespotted sunfish (L. humilis, Girard) is one species that meets this criteria, although to date, such opportunities have not been exploited. Small centrarchids (where legal) are often used to populate personal ornamental tanks, although there is no industry per se associated with this activity (i.e. members of the public collecting fish from the wild and putting them in fish tanks).

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NCRAC (North Central Regional Aquaculture Center). 1996. Sunfish project component termination report. Pages 51–54. In: NCRAC Annual Progress Report 1994–95. NCRAC, Michigan State University, East Lansing, MI. NCRAC (North Central Regional Aquaculture Center). 1998. Sunfish progress report. Pages 65–76. In: NCRAC Annual Progress Report 1996–97. NCRAC, Michigan State University, East Lansing, MI. NCRAC (North Central Regional Aquaculture Center). 1999. Sunfish progress report. Pages 45–53. In: NCRAC Annual Progress Report 1997–98. NCRAC, Michigan State University, East Lansing, MI. NCRAC (North Central Regional Aquaculture Center). 2000. Sunfish progress report. Pages 35–41. In: NCRAC Annual Progress Report 1998–99. NCRAC, Michigan State University, East Lansing, MI. Nickum, M. 2004. An overview of largemouth bass breeding and culture, part 1. Aquaculture Magazine 30: 19–24. Olsen, O. W. 1962. Animal Parasites. Burgess Publishing Company. Minneapolis, MN. Peake, S. 1998. Sodium bicarbonate and clove oil as potential anesthetics for nonsalmonid fishes. North American Journal of Fisheries Management 18(4): 919–924. Pflieger, W. 1975. The Fishes of Missouri. Missouri Department of Conservation, Columbia, MO. Regier, H. A. 1962. On the evolution of bass-bluegill stocking policies and management recommendations. The Progressive Fish-Culturist 24(3): 99–111. Ricker, W. E. 1948. Hybrid sunfish for stocking small ponds. Transactions of the American Fisheries Society 75: 84–96. Rogge, M. L., A. A. Moore, and J. E. Morris. 2003. Organic and mixed organic–inorganic fertilization of plastic-lined ponds for fingerling walleye culture. North American Journal of Aquaculture 65: 179–190. Rosenblum, P. M., T. M. Brandt, K. B. Mayers, and P. Hutson. 1994. Annual cycles of growth and reproduction in hatchery-reared Florida largemouth bass, Micropterus salmoides floridanus, raised on forage and pelleted diets. Journal of Fish Biology 44: 1045–1059. Siefert, R. E. 1972. First food of larval yellow perch, white sucker, bluegill, emerald shiner, and rainbow smelt. Transactions of the American Fisheries Society 101: 219–225. Simco, B. A., J. H. Williamson, G. J. Carmichael, and J. R. Tomasso. 1986. Centrarchids. Pages 73–89. In: R. R. Stickney, editor. Culture of Nonsalmonid Freshwater Fishes. CRC Press, Inc., Baco Raton, FL. Smeltzer, J. F. 1981. Culture, Handling, and Feeding Techniques for Black Crappie Fingerlings. Master’s thesis, Colorado State University, Fort Collins, CO. Smeltzer, J. F. and S. A. Flickinger. 1991. Culture, handling, and feeding techniques for black crappie fingerlings. North American Journal of Fisheries Management 11: 485–491. Smith, W. E. 1975. Breeding and culture of two sunfish, Lepomis cyanellus and L. megalotis, in the laboratory. The Progressive Fish-Culturist 37: 227–229. Smitherman, R. O. and R. E. Hester. 1962. Artificial propagation of sunfishes, with meristic comparisons of three species of Lepomis and five of their hybrids. Transactions of the American Fisheries Society 91: 333–341. Snow, J. R. 1968. Production of six- to eight-inch largemouth bass for special purposes. The Progressive Fish-Culturist 30: 144–152. Snow, J. R. 1975. Hatchery propagation of the black basses. Pages 344–356. In: H. Clepper, editor. Black Bass: Biology and Management. Sport Fishing Institute, Washington, DC. Snow, J. E., and J. I. Maxwell. 1970. Oregon moist diet as a production ratio for largemouth bass. The Progressive FishCulturist 32: 101–102. Sparrow, R. and A. Barkoh. 2002. Intensive production of Smallmouth bass fry. The Progressive Fish-Culturist 64: 205–209. Stickney, R. R. 2000. Crappie culture. Pages 184–185. In: R. R. Stickney, editor. Encyclopedia of Aquaculture. John Wiley & Sons, Inc., NY. Stinefelt, B. M., J. C. Eya, K. J. Semmens, and K. P. Blemings. 2004. Effect of diet and strain on growth and performance in hybrid bluegills. North American Journal of Aquaculture 66: 312–318. Swingle, H. 1946. Experiments with combinations of largemouth black bass, bluegills, and minnows in ponds. Transactions of the American Fisheries Society 76: 46–62. Swingle, H. S. 1951. Experiments with varying rates of stocking bluegills, Lepomis macrochirus Rafinesque, and largemouth bass, Micropterus salmoides (Lacepede) in ponds. Transactions of the American Fisheries Society 80: 218–230. Swingle, H. S. and E. V. Smith. 1938. Fertilizers for increasing the natural food for fish in ponds. Transactions of the American Fisheries Society 68: 126–135.

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Tidwell, J., S. Coyle, and T. Woods. 2000. Species Profile: Largemouth Bass. Southern Regional Aquaculture Center Publication 722, Mississippi State University, Stoneville, MI. Tidwell, J., C. Webster, and J. Clark. 1992. Growth, feed conversion, and protein utilization of female green sunfish × male bluegill hybrids fed isocaloric diets with different protein levels. The Progressive Fish-Culturist 54: 234–239. Tidwell, J. H., C. D., Webster, and S. D., Coyle. 1996. Effects of dietary protein on second year growth and water quality for largemouth bass (Micropterus salmoides) raised in ponds. Aquaculture 145: 213–223. Tidwell, J. H., S. D. Coyle, L. A. Bright, A. VanArum, and D. Yasharian. 1994. Effect of water temperature on growth, survival, and biochemical composition of largemouth bass (Micropterus salmoides). Journal of the World Aquaculture Society 34: 175–183. Tidwell, J. H., C. D. Webster, S. D. Coyle, and G. Schulmeister. 1998. Effect of stocking density on growth and water quality for largemouth bass Micropterus salmoides growout in ponds. Journal of the World Aquaculture Society 29: 79–83. Toetz, D. W. 1966. The change from endogenous to exogenous sources of energy in bluegill sunfish larvae. Investigations of Indiana Lakes & Streams 7: 115–146. Tomelleri, J. and M. Eberle. 1990. Fishes of the Central United States. University Press of Kansas, Lawrence, KS. Twibell, R. G., K. A. Wilson, S. Sanders, and P. B. Brown. 2003. Evaluation of experimental and practical diets for bluegill Lepomis macrochirus and hybrid bluegill L. cyanellus × L. macrochirus. Journal of the World Aquaculture Society 34: 487–495. Vogele, L. E., R. L. Boyer, and W. R. Heard. 1971. A portable underwater suction device. The Progressive Fish-Culturist 33(1): 62–63. Wagner, G. N. and S. J. Cooke. 2005. Methodological approaches and opinions of researchers involved in the surgical implantation of telemetry transmitters in fish. Journal of Aquatic Animal Health 17: 160–169. Wang, N., R. S. Hayward, and D. B. Noltie. 1998. Effect of feeding frequency on food consumption, growth, size variation, and feeding pattern of age-0 hybrid sunfish. Aquaculture 165: 261–267. Wang, H. P., R. S. Hayward, and G. W. Whitledge. 2003. Prey-size preference, maximum handling size and consumption rates for redear sunfish Lepomis microlophus feeding on two gastropods common to aquaculture ponds. Journal of the World Aquaculture Society 34: 379–397. Webster, C. D., L. G. Tiu, and J. H. Tidwell. 1997. Growth and body composition of juvenile hybrid bluegill Lepomis cyanellus × L. macrochirus fed practical diets containing various percentages of protein. Journal of the World Aquaculture Society 28: 230–240. Webster, C. D., J. H. Tidwell, L. S. Goodgame, J. A. Clark, and D. H. Yancy. 1992. Effects of protein level on growth and body composition of hybrid sunfish (Lepomis cyanellus × L. macrochirus) reared in ponds. Transactions of the Kentucky Academy of Science 53: 97–100. Webster, C. D. and J. H. Tidwell. 2002. Centrarchids: hybrid bluegill (Lepomis cyanellus × Lepomis macrochirus). In C. D. Webster and C. Lim, editors. Nutrient Requirements and Feeding of Finfish for Aquaculture. CAB International, Wallingford, Oxon. White, B. L. 1988. Culture of Florida Largemouth Bass Micropterus salmoides floridanus. Texas A&M University Extension Publication A0303, College Station, TX. Wickstrom, G. A. and R. L. Applegate. 1989. Growth and food selection of intensive cultured largemouth bass fry. The Progressive Fish-Culturist 51: 79–82. Williamson, J. H. and G. J. Carmichael. 1990. An aquacultural evaluation of Florida, northern, and hybrid largemouth bass, Micropterus salmoides. Aquaculture 85: 247–257. Williamson, J. H., G. J. Carmichael, K. G. Graves, B. A. Simco, and J. R. Tomasso. 1993. Centrarchids. Pages 145–197. In: R. R. Stickney, editor. Culture of Non-salmonid Freshwater Fishes, 2nd edition. CRC Press, Boca Raton, FL. Willis, D. W. and S. A. Flickinger. 1981. Intensive culture of largemouth bass fry. Transactions of the American Fisheries Society 110: 650–655. Wills, P. S., J. M. Paret, and R. J. Sheehan. 1994. Pressure induced triploidy in hybrid Lepomis. Journal of the World Aquaculture Society 25: 507–511. Wrenn, W. B., B. J. Armitage, E. B. Rodgers, T. D. Forsythe, and K. L. Grannemann. 1979. Effects of Temperature on Bluegill and Walleye, and Periphyton, Macroinvertebrate, and Zooplankton Communities in Experimental Ecosystems. U.S. Environmental Protection Agency, Duluth, MN. EPA-600/3-79-092, 172 pp.

Chapter 11

Centrarchid fisheries S. Quinn and C. Paukert

11.1 Introduction The centrarchid family has become important as a fishery resource for several reasons: (i) more members of this group commonly exceed edible size (∼0.2 kg) than any other North American fish family; (ii) most species inhabit shallow littoral habitats that are readily accessible to anglers; (iii) most species are generally regarded as desirable for human consumption; (iv) several species have received wide public acclaim as sportfish. The adaptability of many centrarchids to diverse and altered habitats also has allowed them to thrive in aquatic ecosystems where other species have dwindled. Larger centrarchid species are opportunistic predators, a characteristic that has promoted fast growth and allowed habitat expansion, while simultaneously attracting the attention of recreational anglers. Today, 25 of 34 centrarchid species support recreational fisheries, with 19 of those supporting fisheries of at least regional importance in terms of angler preference (Table 11.1).

11.2 Historical fisheries Fishing for centrarchids in North America was first described in Florida by the French Ribault expedition, as Native Americans captured largemouth bass (Micropterus salmoides) or possibly Florida bass (M. floridanus), in reed enclosures (Robbins and MacCrimmon 1974). Spearing and angling also were practiced in the eighteenth century by Seminole Indians of northern Florida, including the use of artificial lures made of deer hair (Bartram 1943). The earliest descriptions of smallmouth bass (M. dolomieu) fisheries came later, though this lapse likely is due to the history of exploration in North America by Europeans, rather than the practices of local peoples. Explorers noted, however, that with the region’s abundant game animals, fish were not widely sought by natives. Where fishing was prevalent in the interior of North America, women and children typically were given those tasks (Hulbert and Schwarze 1910). In the Northwest, in contrast, fishing was very important in local cultures as well as for nutrition, though salmonids and marine species were targeted (Stewart 1977). Information on early fisheries for centrarchids is scarce, though artisanal fisheries for all species of edible size were apparently practiced where native ranges and human settlements coincided. In California, for example, Indians of the Sacramento-San Joaquin drainage fished for Sacramento perch (Archoplites interruptus), the only centrarchid native west of the Rocky Mountains to persist into modern times (McGinnis 1984).

11.2.1 Commercial fisheries Commercial fisheries have a long tradition throughout North America, although fishing literature and fisheries investigations in freshwater ecosystems have focused primarily on recreational fisheries. For this discussion, commercial fisheries may be defined as the capture of fish for purposes of sale, rather than for recreation or personal consumption. Centrarchid aquaculture, which also involves sale of fish, represents another branch of commercial fisheries and is discussed in Chapter 10 of this volume. Small-scale commercial fisheries for centrarchids are as old as the fishmongering business, though quantitative or qualitative analyses of such small-scale fisheries are scarce (Trautman 1981). 312

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Table 11.1 Names, distribution, and fishery status of centrarchids. Scientific name

Common name

Distribution

Recreational status

Commercial status

Acantharchus pomotis

Mud sunfish

Common, U.S. East Coast

None

None

Ambloplites ariommus

Shadow bass

Common, U.S. Gulf Coast

Minor regional importance

None

Ambloplites cavifrons

Roanoke bass

Limited, North Carolina, Minor regional Virginia importance

None

Ambloplites constellatus

Ozark bass

Limited, Arkansas, Missouri

Very minor

None

Ambloplites rupestris

Rock bass

Very common, eastern U.S. and southeastern Canada

Secondary importance

Historic; limited now

Archoplites interruptus

Sacramento perch

Limited, U.S. West Coast

Secondary importance

None

Centrarchus macropterus

Flier

Limited, southeastern U.S.

Minor regional importance

None

Enneacanthus chaetodon

Blackbanded sunfish

Limited, southeastern U.S.

None

None

Enneacanthus gloriosus

Bluespotted sunfish

Common, U.S. East Coast

None

None

Enneacanthus obesus

Banded sunfish

Limited, U.S. East Coast

None

None

Pomoxis annularis

White crappie

Very common, U.S., northern Mexico

Very important

Historic

Pomoxis nigromaculatus

Black crappie

Very common, U.S., southern Canada

Very important

Historic; limited now

Lepomis auritus

Redbreast sunfish

Common, East Coast of North America

Regionally important

Historic, limited now

Lepomis cyanellus

Green sunfish

Very common, U.S., northern Mexico

Secondary importance

Historic

Lepomis gibbosus

Pumpkinseed

Very common, northern U.S., southern Canada

Secondary importance

Historic; limited now

Lepomis gulosus

Warmouth

Common, eastern U.S.

Secondary importance

Historic

Lepomis humilis

Orangespotted sunfish

Common, central U.S.

Minor regional importance

None

Lepomis macrochirus

Bluegill

Very common, U.S., southern Canada, northern Mexico

Very important

Historic; limited now

Lepomis marginatus

Dollar sunfish

Limited, southeastern U.S.

None

None

Lepomis megalotis

Longear sunfish

Common, central U.S.

Minor regional importance

None

Lepomis microlophus

Redear sunfish

Very common, southeastern U.S.

Minor regional importance

Historic; limited now (continued)

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Table 11.1 (continued). Scientific name

Common name

Distribution

Recreational status

Commercial status

Lepomis miniatus

Redspotted sunfish

Limited, central U.S.

None

None

Lepomis peltastes

Northern longear sunfish

Common, central U.S.

Minor regional importance

None

Lepomis punctatus

Spotted sunfish

Common, southeastern U.S.

Secondary importance

Historic; limited now

Lepomis symmetricus

Bantam sunfish

Limited, lower Mississippi River drainage

None

None

Micropterus cataractae

Shoal bas

Limited, Florida, Georgia, Alabama

Regionally important

None

Micropterus coosae

Redeye bass

Limited, Alabama, Georgia, South and North Carolina, Tennessee, Kentucky

Regionally important

None

Micropterus dolomieu

Smallmouth bass

Very common, U.S., southern Canada; introduced internationally

Very important

Historic

Micropterus floridanus

Florida bass

Very common, southeastern U.S., introduced Asia, Africa

Very important

Historic in native range; limited worldwide

Micropterus notius

Suwannee bass

Limited, Florida, Georgia

Regionally important

None

Micropterus punctulatus

Spotted bass

Very common, central U.S.

Very important

Historic

Micropterus salmoides

Largemouth bass

Very common, U.S., southern Canada; introduced internationally

Very important

Historic in native range; limited worldwide

Micropterus treculi

Guadalupe bass

Limited, Texas

Regionally important

None

The earliest inland subsistence and small-scale commercial fisheries by white settlers typically targeted species that migrated through rivers, commonly walleye (Sander vitreus) and white bass (Morone chrysops; Trautman 1981). Before about 1850, commercial fishing gear consisted primarily of spears, seines, weirs, and trotlines. Around 1850, use of twine gillnets and pound nets began, resulting in increased catches. Trautman (1981) reported that commercial fishing in Ohio’s large inland reservoirs peaked prior to 1875. He reports, “thousands of barrels of largemouth black basses, bluegills, pumpkinseeds, and bullheads were shipped annually from these reservoirs. After 1875, a decrease in fish abundance became evident in these reservoirs, in the shallows of Lake Erie, and especially in the streams.” Overfishing and habitat degradation led to early legislation to protect fisheries. Commercial fishing in inland waters has been primarily governed by individual states and provinces, and sometimes local jurisdictions, with some oversight by federal governments. The Ohio Commission of Fisheries was created by legislative act in 1873, and charged with fish propagation, introducing nonnative species, and preventing overexploitation (Trautman 1981). Although restrictions on

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315

commercial fishing became increasingly stringent, in terms of permitted waters and targeted species, existing regulations often allowed anglers to sell their catch, a practice known as “market fishing.” Black bass were a common target during the early decades of the twentieth century (Trautman 1981). Ohio’s situation generally reflected that of the developing states in the eastern half of the United States. States and provinces gradually passed laws to protect fisheries from destruction by habitat alteration or overfishing. Many species, including centrarchids were proclaimed “gamefish,” with regulations to limit daily catches and possession limits, seasonal restrictions, and length limits. Passage of the Lacey Act (1900) and Federal Black Bass Act (1926) made enforcement of state laws easier, as it became illegal to transport across state lines fish and wildlife taken illegally. As early as 1889, Canadian fisheries managers had acknowledged the importance of protecting bass during the spawning period and therefore established a closed bass season in southern Ontario’s Lake Simcoe from April 15th to June 15th (MacCrimmon and Skobe 1970). In 1892, a 10-inch minimum-length limit and daily creel of 12 smallmouth bass were imposed to protect that increasingly popular fishery. Over the next half century, various seasonal closures for bass were tried until the current season (last Saturday in June until November 30th) was established throughout most of southern Ontario. During the mid-twentieth century, several states promoted commercial fishing to utilize nongame fish for food and to simultaneously reduce their populations, which was thought to increase growing conditions for gamefish, particularly centrarchids and percids (Priegel 1971; Fritz and Wight 1986). Regulations typically required release of “gamefish.” Thus the designation “gamefish” has been related to commercial harvest of freshwater species in nearly all North American jurisdictions, as anglers may take “nongame” fish with methods not restricted to rod and reel, and the catch sometimes can be sold. However, the specifics of laws in some states allowed “market fishing” to continue. Recent regulation changes still reflect some of the historical aspects of market fishing. As of March 1, 2005, the Kentucky Department of Fish and Wildlife Resources enacted a 20-fish daily creel limit for redear sunfish (Lepomis microlophus) to restrict overharvest by commercial fisheries (Benjy Kinman, Kentucky Department of Fish and Wildlife Resources, personal communication). Once redear harvest was regulated, they became “gamefish” and no longer subject to commercial harvest. In New York, species not governed by length limits may be caught by angling and sold, within the bounds of daily and possession limits. Recently, the New York Department of Environmental Conservation enacted length limits on crappie (Pomoxis spp.), effectively ending commercial fishing for these species. Although small-scale commercial fisheries for sunfish species (Lepomis spp.), as well as rock bass (Ambloplites rupestris) and for other panfish such as yellow perch (Perca flavescens) still exist. The largest commercial fishery for centrarchids in North America targeted crappie and sunfish on 382,000 ha Lake Okeechobee, Florida; using trawls, haul seines, traps, and trotlines (Schramm et al . 1985). The objective was to allow utilization of surplus fish, while reducing density and thus increasing growth rates. To prevent sale of fish from other waters, regulations required that all black crappie (Pomoxis nigromaculatus), bluegill (Lepomis macrochirus), and redear sunfish sold bear a metal tag purchased from the Florida Game and Fresh Water Fish Commission. Between 1976 and 1981, almost 3.8 million kg of black crappie were harvested, with average annual harvest of 836,638 kg, which was estimated at 56% of the harvestable biomass. Sunfish harvest averaged 571,333 kg, 24% of harvestable biomass (Schramm et al . 1985). Although the management objectives of increasing growth rates and harvesting underutilized resources were met, and relative weight (a measure of body condition; Anderson and Neumann 1996) of target species increased, commercial fishing was closed in 1981 due to (i) low water conditions that limited angling and commercial catches, (ii) a weak 1979 year-class of crappie, (iii) high exploitation rates, and (iv) public sentiment that commercial fishing was responsible for poor angling success (Miller et al . 1990). A similar commercial fishery for crappie and other centrarchids (not black bass) existed at Reelfoot Lake, Tennessee, from 1964 until 2002 (an earlier commercial fishery had been closed in 1955), with annual harvests ranging from 12,000 to 19,000 kg during the 1990s (Bill Reeves, Tennessee Wildlife Resources Agency, personal communication). Though no positive or negative effects on the sport fishery were detected, commercial fishing was terminated due to substantial exploitation of the largest size groups of crappie, cost for the agency to administer the program, and conflicts with recreational anglers. In Canada, commercial fishing for centrarchids followed a similar path. Scott and Crossman (1973) reported, “smallmouth bass in Canada were taken by the ton by hook and line and by nets until at least 1936.” An International Anglers Commission in 1894 recommended a closed season and the prohibition of the sale of black bass, saving these species for sport angling (Scott and Crossman 1973). Today, there is a limited commercial fishery on Ontario’s Long Point Bay of Lake Erie, operated under a quota system by First Nation peoples. Harvest of crappie, rock bass, and sunfish has ranged

316

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from 6500 to 30,400 kg from 1999 through 2004, with the majority being sunfish (John Johnson, Ontario Ministry of Natural Resources, unpublished data). At the eastern end of Lake Ontario, First Nation tribal members may harvest rock bass, black crappie, and sunfish under a quota system, with annual catches since 1999 ranging from about 60,000–80,000 kg of sunfish, 4500–8000 kg of crappie, and smaller amounts of rock bass (John Johnson, Ontario Ministry of Natural Resources, unpublished data). Outside North America, information on commercial centrarchid fisheries is scarce. Largemouth bass, smallmouth bass, spotted bass (M. punctulatus), and bluegill were introduced to southern Africa between 1928 and 1939, and have become naturalized (Skelton 1993). Hickley et al . (2002) reported that largemouth bass comprised 22% of the commercial gill net fishery at Lake Naivasha in Kenya. In Zimbabwe, where many largemouth bass fisheries exist, commercially licensed anglers may take and sell largemouth bass, though such harvest is minor (Anthony Williams, African Fisherman, personal communication). Largemouth bass were introduced to Japan in 1925 as a commercial fishery resource (Iguchi et al . 2004), but they have not become popular as food (Quinn 2003). In addition, recent legislation has targeted them for reduction as an invasive species. Bluegill were introduced to Japan in 1960, and have proved less popular as a sportfish (compared to other fish targeted by the locals), and also have recently been labeled unwanted invasives (Maezono et al . 2005).

11.2.2 Origins of recreational fisheries 11.2.2.1 North America The tradition of recreational angling, defined as fishing for pleasure and not for sale (Murphy and Willis 1996), stemmed from the British heritage that many of the early North American colonists shared, which fostered preferences for trout and salmon among freshwater species (Henshall 1881). The first centrarchids to attract substantial attention from recreational anglers were the black basses (Micropterus spp.). Due to the continuing popularity of salmonids, angling for black bass became popular earlier in central and southern states that have limited coldwater fisheries. By the mid-eighteenth century, anglers in the Gulf Coast states, particularly Florida, practiced techniques like “skittering” and “bobbing,” which involved long wooden poles and large homemade baits tethered on a short line, with no reel (Henshall 1881). Whereas skittering involved pulling an artificial lure across the surface to attract fish, bobbing had a more vertical presentation aspect. Angling for bass was advanced in the early 1800s by development of the “Kentucky reel,” a level-wind style, built with a drag system and clicker for spool control (Kimball and Kimball 1980). During the late nineteenth and early twentieth century, further advances were made in flyfishing and baitcasting (level-wind) rods and reels as well as fishing lines. For example, multiplying gears in reels improved speed capability, while the shape and material of the gears increased winching power. During this era, manufacture of specialized angling equipment grew rapidly, including bait containers, tackle boxes, hook disgorgers, as well as a wide variety of artificial lures (Luckey 1996). During the late nineteenth century, literature on bass fishing also began to develop (Henshall 1889). Evidently, black bass species attracted by far the greatest recreational interest among centrarchids through the early decades of the twentieth century. After World War II, development of open-face spinning reels and nylon monofilament lines offered easy fishing to the growing human population who found increasing leisure time. Rod blank materials advanced from bamboo and steel to fiberglass and graphite. Technological developments in metals and plastics made light-tackle fishing feasible, and the popularity of fishing for smaller centrarchid species (particularly sunfish and crappie) grew rapidly through the second half of the twentieth century, mirroring the fast growth of recreational fishing in the United States and Canada (Stroud 1970). As recreational fisheries for centrarchids grew, many experienced anglers found careers as fishing guides, bringing clients to fishing locations and demonstrating fishing techniques. The origins of modern competitive fishing (see Section 11.3.1) occurred in the mid-1950s with bass tournaments in Texas. Ranges of centrarchid species expanded dramatically beginning in the late nineteenth century, as a result of state and federal agency stockings and subsequent fish movements. Largemouth and smallmouth bass were first introduced to California in 1874, with stockings of largemouth bass in Washington and Oregon from 1890–1895 (Wydoski and Whitney 1979). Largemouth bass were stocked most widely because of their increasing popularity with recreational anglers, physiological hardiness that aided survival during primitive transport, and adaptability to diverse environments. Introduced populations tended to thrive and expand. Native to 28 states and 2 Canadian provinces, largemouth bass were stocked into waters of 26 states by 1892 and into 4 additional provinces by 1930 (Robbins and MacCrimmon 1974).

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Although less information on other centrarchid species is available, range expansions of species regarded as gamefish followed a similar pattern. For example, the first introductions of black crappie, white crappie (P. annularis), and bluegill into Washington occurred in the 1890s (Wydoski and Whitney 1979). From there, introductions were made to British Columbia.

11.2.2.2 International Largemouth bass were planted in 14 Central and South American countries and territories by 1959 and into the waters of 16 African countries from 1929 to 1966, along with European and Asian nations (see Plate 1). Smallmouth bass were introduced internationally but less widely distributed. Robbins and MacCrimmon (1974) provide dates and details on worldwide introductions of black bass species. Popular sport fisheries have developed, particularly in southern Africa, Japan, Spain, Italy, and France (Quinn 2003), though Japanese fisheries authorities have recently declared centrarchids nuisance species and attempted eradication, which has been successful with smallmouth bass in several lakes (Iguchi et al . 2004). Bluegills have become naturalized in parts of Africa and Asia. Although popular fisheries for largemouth bass exist in South Africa and Zimbabwe, all centrarchids are considered a conservation problem due to predation on or competition with native species (Skelton 1993; Cambray 2003).

11.3 Recreational fisheries for black bass Micropterus spp. Expansion of the range of black bass and growth of recreational fisheries in the United States has been linked to reservoir construction. In 1900, there were about 100 reservoirs over 200 ha (Jenkins 1970). Reservoir construction peaked in the 1960s and decreased greatly by the late 1980s, resulting in more than 1700 reservoirs over 200 ha today, with aggregate area exceeding 4.5 million ha (Miranda 1996). By 1975, and likely years before, largemouth bass had become the most widely distributed and popular gamefish in the United States (Anderson 1975). Even in states that offer abundant opportunities for coldwater fishing (e.g., New York), black bass had become the most targeted fish category by 1973 (Brown 1976). Federal agencies including the Soil Conservation Service and U.S. Department of Agriculture encouraged construction of farm ponds throughout the United States during the early twentieth century, increasing their number from about 20,000 in 1934 to well over 2,000,000 by 1965 (Swingle 1970). By 1978, Anderson et al . (1978) estimated that central North America, including Ontario and Manitoba, contained more than 800,000 ponds of less than 2.4 ha, covering more than 365,000 ha total, and that ponds comprised 15 to 30% of surface waters in 5 midwestern states. These small waters provided extensive new habitat for largemouth bass and bluegill, the most common stocking combination. In Ontario, the province with the largest black bass fisheries, popularity lagged through much of the twentieth century, but rose rapidly in the 1980s (MacMahon 1994). By 2000, black bass ranked fifth in catch numbers for all of Canada, with 22.5 million caught (Department of Fisheries and Oceans 2003). Six provinces reported black bass catch statistics, with the highest catch in Ontario, followed by Quebec, British Columbia, and Manitoba. No other centrarchids were reported, with catches presumably lumped as “other species” (Department of Fisheries and Oceans 2003). Important though localized smallmouth bass fisheries also have developed in Canada’s eastern provinces of Nova Scotia and New Brunswick. By 1985, there were16 million U.S. anglers age-16 and older who primarily fished for black bass, and these anglers accounted for 42% of all freshwater anglers (Grambsch 1989). Peak bass fishing popularity was in the eastern half of the United States. In the 1996 national survey, 81% of bass anglers were male, compared to 74% of all anglers, and high rates of participation were noted for all age groups (Pullis and Laughland 1999). Analyzed by age, peak participation in bass fishing was equal at 47% for young (16–17) and middle-age (45–54) age groups. Participation by age groups 18–24 and 25–34 was also high at 46% (Pullis and Laughland 1999). Participation in bass fishing increased with level of education, as well as income, up to the $30,000 to 34,000 income category (Pullis and Laughland 1999). Expanding interest in bass fishing led investigators to evaluate economic impacts. In 1949, the cost of catching one pound of largemouth bass at Ridge Lake, Illinois, was estimated at US $9.70 (Bennett and Durham 1951). In an analysis of 1996 data from the United States, Fish and Wildlife Service, Boyle et al . (1998) determined that black bass anglers were willing to pay US$2.96 to 4.85 per fish, depending on the United States region. In recent times, reliance on technologically advanced watercraft and a wide variety of artificial lures has further spurred the economic impacts of bass fishing (see Plate 2). For example, at Lake Fork, Texas, a popular largemouth bass fishery, visiting anglers spent US

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$27,487,000 in a year (Chen et al . 2003). It has been estimated that expenditures by bass anglers comprise 60–70% of total annual sportfishing expenditures in the United States. (Shupp 2002). Among the eight black bass species, largemouth bass, including the recently described Florida bass (M. floridanus; Kassler et al . 2002) are the most important recreationally and economically because of their broad distributions and popularity with anglers. The largemouth bass also is largest, with a record weight of 10.09 kg (International Game Fish Association 2005). Smallmouth bass are primarily targeted in several states and provinces, as well as watersheds within other jurisdictions. Record weight is 4.93 kg (International Game Fish Association 2002). Spotted bass (Micropterus punctatus), the third-most widely distributed black bass species, typically overlap the ranges of largemouth or smallmouth bass (occasionally both). This species sometimes is regarded as less desirable, in part due to typically slower growth and smaller size (Buynak et al . 1991a). In some systems containing Alabama spotted bass, however, growth parallels that of largemouth bass (Maceina et al . 1996), and important fisheries exist both in its native range and where transplanted into California reservoirs, where many record-size spotted bass have been caught (International Game Fish Association 2005). Kassler et al . (2002) revised black bass taxonomy, noting the yet undescribed specific status of the Alabama spotted bass. Record weight for this fish is 4.65 kg (International Game Fish Association 2005). The four rarer species [shoal bass (M. cataractae), Suwannee bass (M. notius), Guadalupe bass (M. treculi ), and Coosa (redeye) bass (M. coosae)] are limited in distribution and overlap with other more common species (Koppelman and Garrett 2002), reducing their importance as recreational species on a statewide basis. The esthetically pleasing riverine habitats favored by these four species make them specialty fisheries targeted by local experts. In the Flint River, Georgia, for example, shoal bass are the dominant species and are locally popular, with fish commonly exceeding 2 kg. Record weights are 3.99 kg for shoal bass, 1.75 kg for Suwannee bass, and 1.67 for Guadalupe bass (International Game Fish Association 2005). That agency does not hold a record for Coosa (redeye) bass due to earlier confusion between it and shoal bass. Record size for Coosa bass is 2.32 kg (National Fresh Water Fishing Hall of Fame 2005). To catch black bass, anglers typically cast artificial lures from boats, and the fishing tackle industry has profited by the diversity of wood, soft plastic, hard plastic, and metal lures of every size, color, and description that anglers use. “Bass boats” have become one of the more popular styles of recreational craft, and both fiberglass and aluminum models are popular, powered by outboard engines ranging from 5 to 300 horsepower, along with quiet, battery-powered electric positioning (trolling) motors (Plate 2). Electronic accessories, particularly sonar and global positioning systems (GPS), are widely used to select fishing spots. Trolling and various forms of live bait fishing also are popular in some regions. Details on gear and fishing techniques can be found in Oster (1983) and Lindner et al . (1990). The American Fisheries Society published a major symposium on black bass ecology, conservation, and management (Philipp and Ridgway 2002).

11.3.1 Competitive angling events Bass tournament fishing has expanded continually since its inception in Texas in the mid-1950s. Early growth of competitive bass fishing generally paralleled increased bass fishing participation as a whole, in terms of geographic distribution, number of participants, and growing avidity of bass anglers. Schramm et al . (1991a) tabulated 20,697 competitive fishing events during 1989 (19,719 in freshwater) in all North America jurisdictions and for all species groups. During 2000, Kerr and Kamke (2003) estimated that 29,500 competitive angling events took place in the United States and Canada, with 77.8% of those for black bass. In addition, many small-scale competitions have not been included in summaries as they usually do not require permits for operation. In Canada, competitive fishing also has increased, primarily in Ontario, and 40% of events target black bass (Kerr 1999). Tournaments have increased over the years and formats have evolved, based on scientific guidelines for fish handling and angler attitudes. In Texas, 2418 black bass tournaments were held from 1993 to 1997 (Wilde et al . 1998b). Although these tournaments ranged from just a few boats to over 2000, most events involve fewer than 20 boats. The number of boats per tournament and the number or tournaments per lake appear to have increased over the last 25 years (Wilde et al . 1998b), in addition to their geographic expansion. For example, bass tournaments have recently become established in Manitoba, Nova Scotia, and British Columbia. At the earliest tournaments, all bass were harvested, but an estimated 97% now require live release after weigh-ins (Wilde et al . 1998b). The first attempt to release tournament-caught bass was in 1972 (Tufts and Morlock 2004). High

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mortality at tournaments in the 1970s increased awareness of the need to protect bass (Holbrook 1975), and improvements were gradually made in boat livewell systems and tournament handling procedures. Competitive formats are varied and include: team tournaments (two cooperating partners); draw tournaments (two partners drawn at random and competing with each other as well as the rest of the field); pro-am tournaments (typically with a pro angler controlling the boat and keeping a separate catch from the amateur partner); road-runner tournaments (anglers can fish several lakes); jackpot tournaments (anglers contribute money to a pot and the winner takes all); tagged fish events where prizes are awarded for tagged fish that are caught; and big-bass derbies, where the largest individual bass caught on an hourly or daily basis merit prizes (Wilde et al . 1998b). Tournament field size may range from a dozen or so boats at club competitions to several hundred at professional level bass tournaments to several thousand at big-bass derbies. In several states, exemptions from length limits have been granted for bass tournaments that receive official permits from the management agency (Gilliland 1998; Jacobs et al . 2002). Bass anglers are a diverse group that includes both tournament and nontournament anglers. Although tournament anglers have been perceived as a rather homogeneous group in terms of angler motives and attitudes (e.g., Schramm et al . 1991a), recent research suggests these anglers may be as diverse as nontournament anglers (Wilde et al . 1998a). Wilde et al . (1998a) reported that tournament anglers emphasized motives that involve catching fish more than nontournament bass anglers, and were more interested in developing their skills and catching a large (trophy) fish (Wilde et al . 1998a). In that study, tournament and nontournament anglers were equally satisfied with the number of fish caught and other catch-related outcomes. Tournament anglers fished about twice as frequently as nontournament anglers and at least 33% were members of fishing clubs. Tournament anglers were 96.9% male and averaged slightly younger than nontournament anglers (37.9 versus 42.9 years of age; Wilde et al . 1998a). Tournament anglers are more likely to belong to fishing clubs and subscribe to fishing magazines than nontournament anglers (Wilde et al . 1998a). From early prize purses of several thousand $US, championship events at the highest levels of competition in 2006 provide $500,000 to the winner. Moreover, the close relationship among tournament organizations, competitive anglers, and the fishing tackle industry through advertising, financial sponsorships and other arrangements magnifies the importance of these events far beyond local economic impacts or participation. Product development and media coverage of recreational fishing are often linked to tournaments, as successful competitors may become spokespersons and develop fan bases, as with other professional sports. For example, Denny Brauer, a popular black bass tournament angler, was pictured on the cover of the Wheaties cereal box in 1998, further emphasizing that tournament angling has become a mainstream sport (see Plate 3). Television coverage of tournaments by national broadcasters has expanded the visibility of competitive bass fishing considerably as well. Though competitive fishing has aroused controversy (Schramm et al . 1991b; Shupp 2002; Kerr and Kamke 2003), economic benefits have been widespread (Schramm et al . 1991b; Grant 1999) and participation has increased. Many assessments of tournament-related mortality have been conducted (Wilde 1998). In addition, tournament anglers and organizers have become increasingly concerned about fish care and many tournaments have stricter regulations than imposed by resource management agencies (Wilde et al . 1998a). Among other centrarchids, only crappie have inspired significant interest from competitive angling groups, and events are smaller in scale, number, and economic impact.

11.4 Recreational fisheries for crappie Pomoxis spp. Reservoir construction also increased habitat for black and white crappie in the United States, and angling popularity increased in a manner somewhat parallel to black bass. Early introductions moved both species west of their range to California by 1917 (Goodson 1966). Popular for food as well as for recreation, crappie harvest often ranked first or second among sport species in southeastern fisheries by the 1970s (Jenkins and Morais 1971; Mitzner 1981). The 1991 U.S. national survey estimated 9.2 million crappie anglers and annual effort for the two species at 91 million angler days (U.S. Department of the Interior 1991). Ten years later, crappie angler numbers declined somewhat, though days of fishing increased to 95 million days (U.S. Department of the Interior 2002). State surveys suggest crappies rank among the top three most popular species groups in 17 states, though they rank first in no state (Quinn, unpublished data). Small impoundments represent locally important recreational fisheries for crappies (Gabelhouse 1984a), although fisheries also commonly exist in large reservoirs and natural lakes throughout the United States and southeastern Canada.

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During the era of reservoir building in the second half of twentieth century, increasing media attention on crappie fishing, including magazine coverage, television shows, as well as growth in tackle designed for crappie fishing, corresponded closely to rising angler interest in these species (Kehde 2000; see Plate 4). Angling techniques are diverse, ranging from shore-fishing with long cane poles to trolling offshore in boats equipped with numerous rod holders, capable of efficiently covering deep structure revealed by sonar, presenting multiple lures styles and colors at different depths. Various live baits and small artificial lures, particularly leadhead jigs with soft plastic or feather dressing are commonly used. Though both species support major fisheries across the United States, and black crappie are locally popular in waters of southern Canada and Mexico, differential behavior of the two species has led to differential exploitation where they coexist (Oster 2005). In Kentucky Lake, anglers exploited white crappie in traditional offshore areas, while the increasing population of black crappie was harvested at a much lower rate, as that species favored shallow cover during much of the spring and summer (Oster 2005). Miranda and Dorr (2000) reported changes in angling catchability with size in both species. Natural hybridization has occurred in several reservoirs (Dunham et al . 1994; Travnichek et al . 1997) with uncertain effects on fisheries. Stocking hybrid crappies has been conducted in reservoirs where black and white crappies are limited (Hooe et al . 1994), and introductions of the “blacknose crappie,” a color morph have also been made (Isermann et al . 2002). Three crappie management symposia have been held by the American Fisheries Society, with presentations on diverse aspects of crappie biology and management (Mitzner 1984; Hooe 1991; Boxrucker and Irwin 2002). Studies suggest that crappie anglers are typically harvest oriented (Quinn 1996; Dorr et al . 2002), basing fishing quality on catch rates of fish above a minimally acceptable size. But crappie specialist anglers motivated by catching large fish and willing to accept more stringent regulations have been described (Allen and Miranda 1996). Though that group was less numerous than generalist anglers or springtime anglers, the authors predicted an increase in their numbers, due to increased media exposure of crappie fishing. Economic studies of important crappie fisheries demonstrate substantial expenditures associated with this form of angling (Palm and Malvestuto 1983; Dorr et al . 2002). On Sardis Lake, Mississippi, for example, crappie anglers were willing to pay us to US $2.9 million annually in 1995 (Dorr et al . 2002). The all-tackle world record for white crappie is 2.35 kg and the record for black crappie is 2.05 kg (International Game Fish Association 2005), though several states maintain higher state records (National Fresh Water Fishing Hall of Fame 2005).

11.5 Recreational fisheries for sunfish Lepomis spp. For purposes of this discussion, 10 sunfish species may be included in the gamefish category: redear sunfish, bluegill, pumpkinseed (Lepomis gibbosus), green sunfish (Lepomis cyanellus), longear sunfish (Lepomis megalotis), northern redear sunfish (Lepomis pelastes), redbreast sunfish (Lepomis auritus), spotted sunfish (Lepomis punctatus), orangespotted sunfish (Lepomis humilis), and warmouth (Lepomis gulosus). In some areas, complexes of sunfish species (as many as eight species) comprise popular fisheries (Kornegay et al . 1994). As sunfish species are lumped under the grouping “panfish” by the U.S. Fish and Wildlife Service in their surveys as well as those conducted by states and provinces, numbers of anglers who specifically target individual centrarchid species are elusive. But as the most widely distributed and most commonly caught group in this category, it is likely that a large portion of the 7.9 million anglers who pursued “panfish” in 2001 (U.S. Department of the Interior 2002) spent time fishing for bluegill and other centrarchid sunfishes. Moreover, sunfish species are widely favored by young anglers under age-16 and thus not tabulated in that survey. In many statewide angler surveys, the sunfish group includes all Lepomis spp. (and sometimes other groups of centrarchids as well). In 12 states, sunfish rank among the top five preferred species groups (Quinn, unpublished data). Despite the abundance, diversity, and widespread appeal of Lepomid species to anglers, economic evaluations of sunfish fisheries are lacking, as are demographic descriptions of sunfish anglers. Many sunfish species hybridize naturally, both in natural and altered ecosystems (Dawley 1987; Konkle and Philipp 1992; Chapter 2), and several hybrid forms are stocked in small impoundments for management purposes (Henderson and Whiteside 1975; Guest 1984; Brunson and Robinette 1986). Reduced reproduction, fast growth, increased catchability, and large size of hybrid forms are characteristics that encourage their production and sale by commercial hatcheries, primarily for stocking in private impoundments (see Plate 5). Redear sunfish: The redear sunfish is the largest member of the genus, often exceeding 1 kg in prime habitats (world record 2.48 kg; International Game Fish Association 2005). Native to the southeastern states and the Mississippi and Rio Grande drainages, redear have been widely transplanted as far north as southern Michigan (Wilbur 1969), where they attain

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large size in some waters. The center of recreational angling popularity for redear sunfish remains in Florida, Georgia, and other southeastern states, where anglers target fish particularly during the spawning season when fish gather in large groups in shallow water. Their diet is comprised of invertebrates, particularly molluscs and aquatic insects (Wilbur 1969), and anglers typically use live baits including crickets and small worms fished on the bottom or suspended under a float, though they are also taken on small artificial lures. Bluegill: The bluegill is the second largest Lepomis species, commonly exceeding 0.5 kg and with a record of 2.15 kg (International Game Fish Association 2005). It is the most widespread and popular one in the United States, found in 49 states and Canadian provinces such as Ontario, where its range is expanding rapidly. Coppernose bluegill, a southeastern subspecies (L. m. purpurescens) have been stocked outside their native range due to purported advantages in growth rate (Prentice and Schlechte 2000). Although widely regarded as a fine fish to introduce youth to fishing because of their modest size, abundance, good flavor, and high catchability, specialized anglers also pursue this species. Experts have refined tackle and tactics to find and catch larger specimens during all seasons of the year, including fishing through the ice (see Plate 6). State and national angler award programs (Quinn 1987) typically offer awards for bluegill, whereas a few also include redear sunfish, redbreast sunfish, and pumpkinseeds. Bluegill harvest numbers often are high in state assessments, due to abundance, catchability, and popularity as food. For example, Muoneke (1992) reported that bluegill comprised 13.6% of all harvested species by number in the inland waters of Texas, and were exceeded in statewide harvest only by channel catfish and white crappie. Negative effects of fishing pressure on bluegill populations structure have been noted (Coble 1988; Olson and Cunningham 1989). Due to the population and spawning dynamics of bluegill, removal of larger specimens sometimes results in overabundance of small bluegills, decreased growth rates, and a condition known as “stunting” that can be difficult to reverse (Beard et al . 1997). Angling effort may then decline, which may not restore fishing quality (Beard and Kampa 1999). Green sunfish: Though widespread in distribution, and attaining large size for sunfish (0.97 kg: International Game Fish Association 2005), green sunfish (L. cyanellus) are not highly prized catches, and most are taken incidentally by anglers fishing for other sunfish species. Their lack of popularity may be related to the poor water quality where these fish are sometimes found. Green sunfish are tolerant of low dissolved oxygen, extreme turbidity, and are often found where no other centrarchids can live (Pflieger 1975). Hybridization with redear sunfish, pumpkinseeds, and bluegill is common. Hybrids of bluegill and green sunfish are produced in private hatcheries and sold for stocking in private ponds in the southeast. The record for this hybrid is 0.97 kg (International Game Fish Association 2005), though substantially larger specimens have been reported. In several regions, green sunfish are collected for use as bait for species such as flathead catfish (Pylodictis olivaris). Redbreast sunfish: Redbreast sunfish (L. auritus) are highly prized where they are abundant, particularly in coastal streams from Massachusetts to Florida (Shannon 1966; Bass and Hitt 1974). Their brilliant coloration, large average size (world record 0.79 kg: International Game Fish Association 2005), and willingness to strike small artificial lures as well as live baits contribute to their popularity. Longear Sunfish: Longear sunfish, including the two former subspecies now recognized as separate species, L. megalotis and L. peltastes, are widely distributed through central North America from southern Canada and the Great Lakes states though central Texas and into Mexico. The record size is relatively large (0.79 kg; International Game Fish Association 2005), but most populations do not contain large individuals. Longear sunfish have thrived in small, clear streams of the Midwest, which are increasingly scarce due to siltation. They have, however, adapted successfully to clear impoundments with rock and gravel substrates from the Ozarks to New Mexico (Boyer and Vogele 1971), where they are caught incidentally by anglers targeting crappie or bluegill. Pumpkinseed: The pumpkinseed (L. gibbosus) was originally found along the Atlantic Coast from the Maritime Provinces to Georgia and west through the Great Lakes and the Red River of the North and Mississippi River drainages. It has been introduced to many western states and British Columbia. They have a smaller maximum size (record weight 0.63 kg; International Game Fish Association 2005), but often reach 0.2 kg or typical “eating size,” and their flesh is highly esteemed (Becker 1983). Pumpkinseeds are also popular because of their brilliant coloration and their willingness to strike artificial lures, even larger ones fished for black bass. Anglers typically target pumpkinseeds with small spinners, jigs, and various live baits fished under a float, although a large part of their diet is molluscs.

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Warmouth: Warmouth (L. gulosus) are widely distributed and locally abundant in ponds, lakes, and streams along the Atlantic coast from Florida to Virginia, and west through Wisconsin and Texas as far south as the Rio Grande drainage. The warmouth achieves a large size (1.1 kg; International Game Fish Association 2005), and 17 states maintain angler records. With its expansive mouth, larger warmouth often feed on small fish and crayfish (Guillory 1978), and commonly strike small lures and live baits fished for other species. Where abundant, such as in the Suwannee River and Okefenokee Swamp in Georgia, warmouth are one of the important gamefishes among the panfish group (Germann et al . 1974). Larimore (1957) noted its high culinary value while noting its relatively low occurrence in creel surveys in mid-western waters. Orangespotted sunfish: Lepomis humilis is locally abundant in streams, lakes, and ponds from North Dakota east to Ohio and south through the Mississippi River drainage to central Texas. Four states maintain records for orangespotted sunfish, though the largest is the Tennessee record of 0.14 kg (National Fresh Water Fishing Hall of Fame 2005). This colorful species is typically caught only incidentally. Spotted sunfish: Spotted sunfish (L. punctatus) are native to the southeastern United States from eastern Texas through peninsular Florida and as far north as central Illinois, inhabiting ponds or slow-moving streams with vegetation or woody cover. Three states maintain records for spotted sunfish and the largest is the Florida state record, 0.38 kg (National Fresh Water Fishing Hall of Fame 2005). Spotted sunfish rarely reach edible size and are taken incidentally in small southeastern streams as far north as southern Missouri (Pflieger 1975). Three other sunfish species, the dollar sunfish (L. marginatus) redspotted sunfish, (L. miniatus), and the bantam sunfish (L. symmetricus) rarely reach catchable size and are unimportant as recreational fisheries resources, though they are colorful, fascinating in their life histories, and ecologically important.

11.6 Fisheries for Ambloplites spp. The rock bass (Amploplites rupestris) is a small to medium-size centrarchid [maximum size 1.36 kg (International Game Fish Association 2005), but rarely exceeding 0.5 kg] that is widely distributed across the eastern United States and southern Canada. Jordan (1905) noted, “This species is preeminently a boy’s fish, though it is by no means despised by anglers of mature years.” An opportunistic feeder and aggressive biter, many rock bass are caught incidentally by anglers using live bait and small artificial lures to target other species, particularly black bass, walleyes, and other sunfish. Rock bass are popular sportfish in Ozark streams, however, exceeded only by smallmouth bass (Pflieger 1975; Roell 1992). In these streams, length limits to protect populations are in place, apparently the only jurisdiction to do so, though other states and provinces include rock bass in aggregate “panfish” daily bag limits. With light tackle, rock bass are regarded as good for sport and food (Schneberger 1973). Aside from length limits in Ozark streams, only Virginia regulates rock bass with a length limit, an 8-inch minimum-length limit imposed in 1997 for rock bass and co-occurring Roanoke bass (A. cavifrons), which are considerably rarer, but easily confused by anglers. The three other congeners support small-scale local fisheries. The Roanoke bass, endemic to rivers of North Carolina and Virginia, has been described as “much sought after by anglers who know where and how to fish for it” (Smith 1969). It grows somewhat larger than rock bass, with records exceeding 1 kg in both states. Although Virginia protects Roanoke bass populations with an 8-inch length limit and 5-fish bag limit, North Carolina does not. Ozark bass (Ambloplites constellatus) are endemic to the White River drainage in northern Arkansas and southern Missouri, and possibly the upper Osage River (Koppelman et al . 2000). Records for the species are not kept by either state, and the species was undescribed until 1977 (Cashner and Suttkus 1977). It may be confused with rock bass, as ranges overlap. It is targeted by anglers in areas of abundance, particularly the Buffalo River and upper White River (Cashner 1980a). The all-tackle world record is 0.45 kg (International Game Fish Association 2005). Shadow bass (Ambloplites ariommus) have a wider distribution, occurring through the Gulf Coast drainages above and below the fall line, from the Apalachicola River to Lake Ponchartrain in Louisiana, and in tributaries of the lower Mississippi Valley as far north as southeastern Missouri. They thrive in clear unimpeded streams with sand or gravel substrates (Cashner 1980b). Shadow bass are popular gamefish in streams where they are abundant, and readily take artificial lures and live baits (Robison and Buchanan 1988). The world record is 0.82 kg (International Game Fish Association 2005).

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11.7 Recreational fisheries for other centrarchids Several other centrarchid species offer angling opportunities where they commonly occur. These typically omnivorous residents of slow-flowing streams and lakes are locally popular with anglers who typically use light spinning tackle or poles to catch the unusual indigenous species on live bait and small artificial lures. Flier (Centrarchus macropterus) inhabit swampy creeks along the Coastal Plain of the Atlantic and Gulf coasts, extending north in the Mississippi River watershed to southern Illinois. The all-tackle record is 0.56 kg, for a pair of fish from North Carolina and Georgia (International Game Fish Association 2005), and reports suggest small local fisheries (Jenkins and Burkhead 1994). Sacramento perch, the only centrarchid endemic to western states, is one of the larger centrarchids, with a record of 1.44 kg (International Game Fish Association 2005), though historical records suggest that they may have grown much larger (McGinnis 1984). Competition from introduced centrarchids has limited populations in the species’ native range, though localized recreational fisheries exist in reservoirs were populations remain abundant. Transplanted populations in four other western states have succeeded, particularly in alkaline waters where this species thrives (McGinnis 1984). In Utah and Nevada, state records exceed the world record (National Fresh Water Fishing Hall of Fame 2005). The mud sunfish (Acantharchus pomotis) is taken incidentally by anglers in its Atlantic Coast range, but apparently is not targeted, and no angling records exist. This species, along with the three smaller and more colorful members of the Enneacanthus genus, are sometimes collected by aquarists.

11.8 Regulations 11.8.1 Managing with regulations Angling regulations for centrarchids have been used to develop more favorable abundance or size structure, to alter the predator or prey densities, limit or provide equitable distribution of harvest, and for nonbiological reasons (principally regional tradition; Van Vooren 1991; Quinn 1996). The literature contains many evaluations (particularly for black bass) of their effects on abundance, size structure, and growth of fish populations and angler catches (Wilde 1997). Three forms of harvest regulations have typically been used: length or size limits, creel (daily bag and possession) limits, and seasonal restrictions (Redmond 1986), although other regulations such as gear restrictions are still used in some waters. In selecting regulations, managers have been increasingly aware of the need to consider not only biological and ecological considerations, but social ones as well, including angler attitudes, expectations, and satisfaction. Black bass are among the most highly regulated species group in North America, and all three regulation types have been widely applied since the late nineteenth century (Fox 1975; Redmond 1986; Quinn 2002). Length-limit regulations include minimum- and maximum-length limits and protected and harvest slot-length limits. Minimum length-limits have been most commonly applied to centrarchids, particularly largemouth bass (Wilde 1997), though slot and maximum length limits have been increasingly applied (Noble and Jones 1999). In the last two decades, managers have been making greater use of length limits to regulate crappie harvest (Quinn 1996; Boxrucker and Irwin 2002), though difficulties in assessment of length limits due to variable recruitment have been noted (Allen and Pine 2000). Also, varying angler opinions on crappie catch preferences (Petering et al . 1995; Bister et al . 2000) have complicated implementation of length limits for these species. In general, minimum-length limits for centrarchids may benefit populations characterized by: average to fast growth rates; low to moderate natural mortality; high exploitation rate; and low to moderate recruitment (Allen and Miranda 1995; Noble and Jones 1999). Protected slot-length limits are intended to restructure populations characterized by high recruitment, slow growth, and rather high natural mortality, by allowing harvest of abundant small fish, while protecting an adult spawning stock that has been reduced considerably from an unregulated condition. Harvest of larger specimens is allowed to increase harvest poundage and allow for the take of trophy fish, though bag reductions for the catch above the upper end of the slot are common (often one fish). Increasing numbers of “trophy” largemouth bass fisheries with steady recruitment have been managed with high slot limits (Parks and Seidensticker 1998; DiCenzo and Garren 2001), while several “trophy” smallmouth bass waters with low recruitment may be managed with high minimum-length limits (e.g., Mille Lacs Lake, Minnesota: 533 mm; Chequamegon Bay, Wisconsin: 559 mm). Reluctance to manage bluegill and

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other sunfish with length limit regulations has been widespread (Reed and Parsons 1999), due to the harvest orientation of bluegill anglers (Quinn 1996; Reed and Parsons 1999; Ott et al . 2001), and variable population dynamics that may stymie results (Beard et al . 1997; Paukert et al . 2002b). Recent evaluations have noted difficulties in accurately assessing effects of length limits (Allen and Pine 2000), and variable results have been reported in the literature (Wilde 1997). Creel limits have been imposed to limit greed and to distribute harvest (Radomski 2003) and have been widely used for centrarchids listed as gamefish. A recent trend has been for reductions in daily bag limits for crappie and sunfish, and sometimes rock bass (Quinn 1996). Though sometimes regarded as a buffer against overharvest and widely accepted by anglers (Radomski 2003), evaluations indicate creel limits are poor tools for this job because to be biologically effective they often must be set below what is acceptable to anglers (Cook et al . 2001). Instead, creel limits may serve to limit angler expectations or to potentially increase angler satisfaction by providing a target and the satisfaction of catching a “limit” (Noble and Jones 1999; Radomski et al . 2001). Although some creel limits are species-specific, aggregate creel limits (black bass, sunfish, crappies, or even “panfish”) are common (Noble and Jones 1999). Seasonal restrictions (closed seasons) prohibit angling (or harvesting) fish during periods of the year (Quinn 2002). Justifications for seasonal closures include: providing equitable distribution of harvest; promoting reproduction by protecting fish during the spawning season; preventing over harvest of large fish; protecting vulnerable fish in winter hibernacula (Quinn 2002); and for safety (Noble and Jones 1999). Seasonal closures for black bass are traditional in several regions of North America and have gained increased exposure as catch-and-release fishing has become more popular (Quinn 2002). Seasonal restrictions have not been applied to other centrarchid species, except where seasonal closures apply to all fisheries. Also, recent biological evaluations of angling for spawning fish have brought increased attention to this issue (e.g., Philipp et al . 1997; Cooke et al . 2002), along with increased interest among anglers (Schramm and Quinn 1999). Harvest regulations have been widely used to improve the size structure of black bass populations and to satisfy angler desires for more, and often, larger bass. The complexities of assessing regulation effects in the face of environmental variables, unknown biological factors, and angler behavior have been noted (Buynak et a1. 1991b; Quinn 1996). Variable annual recruitment of crappie has made assessments of regulations difficult, and led to questions about their value in managing those species (Allen and Pine 2000). Fishery managers often have to determine which centrarchid fishery options are preferred for particular water bodies. In some cases, water bodies can support high-quality largemouth bass populations including a high proportion of larger individuals, but only through management that tends to reduce the size structure of bluegill or crappie populations in those waters. In small impoundments where largemouth bass and “panfish” coexist, managers can choose among three management options: the “panfish” option, big bass option, or the balanced option (see Figure 11.1; Willis et al . 1993). The 100

Bluegill PSD

80 "Panfish option"

60

"Balanced option"

40 20

"Big bass option" 0 0

20

40 60 Largemouth bass PSD

80

100

Figure 11.1 Relationship between bluegill proportional stock density (PSD; the number of bluegill ≥80 mm that are also ≥150 mm) and largemouth bass PSD (number of fish ≥200 mm that are also ≥300 mm). Management options are three typical scenarios for management of largemouth bass and bluegill in small ponds or impoundments. Data are modified from Novinger and Legler (1978), Gabelhouse (1984a), Anderson (1985), and Willis et al . (1993).

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“panfish” option yields a higher proportion of quality-sized “panfish,” along with abundant small largemouth bass. The big bass option fosters a higher proportion of quality-sized largemouth bass and an abundance of small “panfish.” The balanced option results in largemouth bass and “panfish” populations of moderate size and abundance. These options can be defined by plotting proportional stock density (PSD) values of the “panfish” and bass. PSD is a proportional index that quantifies length-frequency data based on stock and quality-sized fish (Gabelhouse 1984b), and higher values indicate a population with a higher proportion or large (quality-sized) fish. Ranges of PSD have been used to define these options (e.g., Anderson 1978a; Novinger and Legler 1978; Gabelhouse 1984a; Anderson 1985; Willis et al . 1993) and have been generally accepted for various centrarchids and other species. Therefore, anglers and managers can prepare management plans to develop the preferred type of fishery for water bodies. Far fewer studies have examined angler satisfaction resulting from regulations than research on the biological consequences of regulatory actions. In an Ohio reservoir, angler support for a minimum-length limit for crappie was high (54%) before regulation, and even higher (74%) after its implementation corresponded with increased catch rates and mean fish size (Hale et al . 1999). In a statewide survey in Texas, largemouth bass angler satisfaction typically increased with largemouth bass catch rates, with similar patterns were noted among crappie anglers (Costello and Betsill 1996). In Ohio, anglers were more satisfied with efforts to increase average length of crappies caught than efforts to increase the numbers of fish caught (Petering et al . 1995). In contrast, a socioeconomic survey conducted prior to implementing crappie regulations in Mississippi suggested that changes in creel limits might reduce angler trips, while changes in minimum-length limits had less impact on participation (Dorr et al . 2002). Fishery managers have increasingly addressed the need to include human dimensions information in regulation planning and evaluation processes, in conjunction with biological data (Hudgins and Malvestuto 1996). Human dimensions surveys help assess the overall effects of regulations on the quality of fishing, though results can be confusing due to vagaries of angler behavior (Beard et al . 2003), as well as the often unpredictable response of fish populations in large ecosystems (Buynak et al . 1991a). In some instances, angler support for a regulation may be high, even though biological benefits are minimal (Bister et al . 2000). In Nebraska lakes, for example, anglers were willing to accept a 200 mm minimumlength limit to increase bluegill size structure, although low exploitation deemed the regulation unnecessary (Paukert et al . 2002b). Today, anglers are more knowledgeable about potential benefits of regulations and may be proactive by supporting or even promoting regulations (e.g., Dean 1996; Buynak et al . 1999; Paukert et al . 2002b). In several states, exemptions from local or statewide length limits have been granted for bass tournaments that receive official permits from the management agency (Gilliland 1998; Jacobs et al . 2002). Tournament anglers may consider the regulations too stringent to allow for fair competition where catches of bass must be weighed prior to release. Such exemptions for tournament anglers may foster opportunities for competitive fishing but could counteract benefits of regulations, especially if tournament pressure is heavy (Edwards et al . 2004).

11.8.2 Factors that affect angling quality Angler motivation surveys have indicated the importance of environmental quality or esthetics, social factors, and diverse other personal values in addition to catch-related motivations (Holland and Ditton 1992; Fedler and Ditton 1994). The moving target of fishing quality can create confusion among managers. For example, anglers primarily interested in catchand-release fisheries may not view harvest as an important factor in fishing quality (Ross and Loomis 2001), while catch of particular sizes of fish may be more important to other groups (Janssen and Bain 1994). Clearly, factors affecting fishing quality may depend on the targeted angler group, geographic location, species, and changing angler attitudes. Historically, the number of fish caught per unit time was considered an index of quality (Anderson 1975), but the size of the fish caught has become increasingly important. Bluegill anglers historically have been harvest oriented, but recently anglers have been more willing to consider restrictive regulations if they would improve size structure (Reed and Parsons 1999; Paukert et al . 2002b). Management for high-quality sunfish populations often involves promoting the abundance of small predators, particularly small adult largemouth bass (Anderson 1978b; Gabelhouse 1984b; Guy and Willis 1990). Therefore, anglers may have to sacrifice the quality of a fishery for one centrarchid (largemouth bass) to increase quality of another (bluegill; see Figure 11.1).

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Regulations that increase the size structure of a fish population (Section 11.8.1) presumably increase fishing quality, although assessments of angler satisfaction following management measures also can be performed. As Voiland and Duttweiler (1984) castigated fishery researchers for ignoring human dimensions, significant advancements have been made in this area (Ditton 1996). Investigations into diversity among centrarchid anglers have recently been conducted (Wilde and Ditton 1994; Allen and Miranda 1996). Still, studies on the effects that regulations have on angler satisfaction are limited, compared to investigations of biological effects. Environmental factors also affect angling quality, in ways that are less clearly understood. Obviously, adequate habitat is needed for optimal abundance and growth of fishes that in turn fosters high-quality angling. For many centrarchid gamefish, vegetation coverage can be important. Durocher et al . (1984) reported a positive relationship between vegetative coverage and largemouth bass standing crop, up to 20% aerial coverage, and Wiley et al . (1984) modeled optimal macrophyte density for largemouth bass production. Paukert and Willis (2002) found that bluegill selected for emergent vegetation, even when only 20% or less of the lake was covered with this vegetation. Growth rate of black crappie was reduced at hydrilla (Hydrilla verticillata) coverage over 50% (Maceina and Shireman 1982), and crappie recruitment and growth increased following macrophyte removal at Lake Conroe, Texas (Maceina et al . 1991). Although such studies have not linked angler satisfaction to habitat parameters, the inference that improved fisheries make anglers happy can be logically made. Water quality can also be important, and in sometimes unexpected ways. In Alabama, for example, older, eutrophic reservoirs were associated with higher angler catches of larger largemouth bass (Hendricks et al . 1995). Similarly, Maceina and Bayne (2001) found that as a reservoir became more oligotrophic (through declines in point and nonpoint source phosphorus loading), size of largemouth bass in angler catches declined while spotted bass catches increased. Introduced species, particularly invasive exotics, have substantially changed environmental parameters in countless fisheries. In addition to exotic macrophytes discussed in Section 11.9.2 of this chapter, zebra mussels (Dreissena polymorpha), round gobies (Neogobious melanostomus), and other exotic vertebrates and invertebrates have been inadvertently introduced into high-quality smallmouth bass fisheries in the Great Lakes ecosystem, and effects on fish populations have been studied (Steinhart et al . 2004). For a further assessment of exotic species introductions on centrarchid populations, see Chapter 12 of this volume. In addition to harvest regulations, other management strategies can improve angling quality. Water level manipulations, drawdowns for vegetation control, predator and prey stockings, removal of small fish, placement of artificial cover, lake rehabilitation, and habitat improvement have enhanced centrarchid fisheries. Recently, major efforts to improve degraded habitat in large Florida lakes have shown some benefits, though complete assessments are challenging (Allen et al . 2003). Ideally, fishery managers should identify the target audience and desired outcomes through human dimensions research before attempting to manipulate fish populations for human benefits. Anglers must also realize that quality fisheries for some centrarchids may not be feasible because of unsuitable habitat, conflict with other fishery goals, cost, or other considerations. For example, urban fisheries are typically harvest oriented and therefore fisheries managers attempting to create a trophy fishery may conflict with other groups that would prefer a put-and-take fishery. Quality centrarchid fisheries can occur and will continue to occur where suitable habitat, adequate forage, public support, and appropriate management coincide.

11.9 Future considerations in centrarchid management 11.9.1 Toward sustainable fisheries Sustainable centrarchid fisheries depend on the availability of suitable habitat, forage, water quality and quantity, and appropriate management of these species. Reservoir populations of centrarchids may be slowly changing as reservoirs age and few new reservoirs are built. As the quality of reservoir habitats declines for some species (e.g., smallmouth bass in silted or murkier waters), other centrarchids and non-centrarchids better suited to these systems may prosper. In addition, stream degradation and dewatering may lead to reduced fish populations in lotic systems. Natural lakes will continue to be affected by urbanization and shoreline development (Radomski and Goeman 2001), and fishery effects are inevitable. Although some habitat alterations may benefit some populations of some centrarchid species, others may simultaneously decline. In Alabama reservoirs, for example, reductions in phosphorus loading (caused by reductions in point and nonpoint pollution) reduced the angling catch of large largemouth bass, while increasing the spotted bass population (Maceina and Bayne 2001).

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Figure 11.2 A catch-and-release ethic has developed gradually among centrarchid anglers. All fish were harvested in early bass tournaments, but anglers and tournament promoters now try to release as many fish as possible in satisfactory conditions after the weigh-in. Immediate voluntary release rates of black bass typically exceed 90% while release rates for smaller centrarchid species were considerably lower, but have been increasing.

Management and regulations are essential to ensure sustainability of fisheries in the face of angler harvest and continued human expansion, which tends to alter or eliminate aquatic habitats. Various regulations are used to manage centrarchid fisheries, depending on species and fishery goals (see Section 11.8). For regulations to succeed, however, angler acceptance and compliance are necessary. If noncompliance with regulations is substantial, benefits may be nullified (Gigliotti and Taylor 1990). In addition to increasingly conservative regulations, catch-and-release angling has increased dramatically (Quinn 1996) and this trend has helped sustain high-quality black bass populations (see Figure 11.2). A shift toward less consumptive attitudes toward crappie and sunfish has also been noted as the concept of “selective harvest” (Quinn 1996) has been spreading among conservation-minded anglers. Selective harvest describes the decision process of whether to harvest or release caught fish, depending on their abundance, size, age, and the human need for nutrition. In competitive fishing, increasing monitoring and permitting is likely, primarily to alleviate social problems caused by crowding of boating accesses, and boating pressure on the water. Although biological effects of tournament fishing for black bass have been considered minor (Duttweiler 1985; Schramm et al . 1991b), managers and tournament sponsors will work toward new techniques for weigh-ins that will continue to reduce this form of mortality (Gilliland and Schramm 2002; Tufts and Morlock 2004). Sustainability of centrarchid fisheries largely depends on maintenance of suitable habitat and appropriate management of these species and their ecosystems. If suitable habitat is not maintained through innovative strategies, such as drawdowns for substrate removal (Allen et al . 2003), placement of artificial cover (Hunt et al . 2002) or artificial substrates (Jackson et al . 2000), and planting of native vegetation (Smart et al . 1996), the quality of fisheries will decline. Where suitable habitat is presently available, appropriate management (particularly harvest regulations, but also habitat maintenance) can sustain healthy fish populations for future generations.

11.9.2 Effects of reservoir ageing, reservoir hydrology, dam removal, and associated physical changes on centrarchid habitats and fisheries Reservoirs are artificial environments created by damming riverine environments to produce lentic habitats. Impoundments offer a variety of recreational opportunities, including the development of quality centrarchid fisheries for various species,

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depending on climate, geographic region, and reservoir features. For example, largemouth, smallmouth, and spotted bass have been found to segregate along longitudinal habitat gradients within impoundments (Buynak et al . 1989; Sammons and Bettoli 1999; Long and Fisher 2005), offering different recreational opportunities. In addition to diverse recreational opportunities that reservoirs offer, they have become controversial because dams can negatively affect habitat for native species and alter esthetics. Nonetheless, reservoirs offer many of the most important centrarchid fisheries in North America and worldwide and should continue to provide opportunities in the future. Reservoir dynamics: Currently, there are over 1700 reservoirs over 202 ha in the United States (Miranda 1996), with countless more small impoundments. Few new reservoirs are being built, however, and rapid aging of impoundments has limited their fishery potential. As these systems stabilize during trophic depression, littoral habitat complexity declines and the assemblage typically becomes dominated by species of less interest to recreational anglers (Kimmel and Groeger 1986; Ploskey 1986). Thus, a negative relation between reservoir age and sportfish abundance has been noted (Kimmel and Groeger 1986; Miranda and Durocher 1986; Ploskey 1986). Also, nutrient abatement has occurred in some reservoirs because of the reduction of point and nonpoint source pollution or construction of upstream impoundments that trap nutrients (Ney 1996; Maceina and Bayne 2001). Abatement procedures can reduce available nutrients and alter the fish community. For example, Lake Mead, a mainstem impoundment of the Colorado River, had a prolific largemouth bass fishery until Glen Canyon Dam was built upstream of Lake Mead. The resulting nutrient loads into Lake Mead decreased and the largemouth bass fishery declined (Ney 1996). Changing characteristics of reservoirs may continue to alter species composition and quality of centarchid fisheries, with shifts in species dominance (Maceina and Bayne 2001). Early in the aging process, centrarchid fisheries may benefit from eutrophication, but later declines are likely. For example, eutrophic status of Alabama reservoirs was positively correlated with weight of angler catches of black bass (Hendricks et al . 1995). Although a trophic upsurge may occur immediately after reservoir filling (Kimmel and Groeger 1986), declines in productivity after an upsurge may soon limit centrarchid fisheries. In addition, if nutrient abatement or increased sedimentation occurs, this will lead to reduced water quality and clarity, which may result in reduced vegetation (Smart et al . 1996). Aquatic vegetation is important habitat for many centrarchids (Savino and Stein 1982; Engel 1990; Harrington et al . 2001; Paukert et al . 2002a), and lack of vegetation may limit the quantity and quality of fisheries for some species. As reservoirs continue to age, further changes in the fish communities and habitats may be anticipated. The future of centrarchid fisheries in reservoirs will be affected by the degree of nutrient abatement or other maintenance measures (e.g., dredging, water level management, vegetation management), as they affect productivity. With few new reservoirs being constructed, however, reservoir aging may eventually lead to overall declines in centrarchid fisheries due to the prevalence of these artificial habitats. Casselman et al . (2002) postulated, however, that global warming will enhance production of coolwater species like smallmouth bass in northern latitudes. Yet such effects might be negative at the southern fringes of the species’ range. Reservoir hydrology: Reservoir hydrology is a key factor in centrarchid reproduction and recruitment (Ploskey 1986), and thus affects fisheries for these species. Interrelated effects on aquatic vegetation also occur. Water level changes in reservoirs and regulated rivers have been related to recruitment of many centrarchids (Raibly et al . 1997; Slipke et al . 1998; Sammons and Bettoli 2000; Koel and Sparks 2002; Sammons et al . 2002). In general, high water, particularly during spring spawning periods and ensuing months were related to stronger year classes of centrarchid species. Presumably, increased recruitment of fishes as a result of higher water benefits future fisheries. In addition, increased largemouth bass recruitment has also been linked to increased water levels during summer in an Oklahoma reservoir (Boxrucker et al . 2005). Toward this end, reservoir operators (e.g., power companies, U.S. Army Corps of Engineers; U.S. Bureau of Reclamation; U.S. Bureau of Land Management) may be able to alter their water level goals to help fisheries (e.g., Maceina 2003). Aquatic plant management: Vegetation management has been an important and controversial topic (Henderson 1996), with potentially powerful implications for fish populations, including centrarchid species (Maceina et al . 1991; Bettoli et al . 1993). Although positive correlations between aquatic plant density [including nonnative species Eurasian milfoil (Myriophyllum spicatum) and hydrilla] and centrarchid abundance have been reported (Durocher et al . 1984; Killgore et al . 1989; Smith and Orth 1990), increased growth rates of certain centrarchid species have occurred in response to vegetation reductions (Maceina et al . 1991; Olson et al . 1998). Variable results among species and year classes also have been reported (Unmuth et al . 1999). In general, largemouth bass anglers favor greater vegetative cover (Wilde et al . 1992), while other recreational users (e.g., boaters, water skiers, jet-skiers) and shoreline residents favor reductions. Engel (1990)

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and Killgore et al . (1993) provide reviews of relationships between aquatic plants and fish populations, with effects of vegetation control. Reservoir and lake management for multiple use, and with considerable public input, will become increasingly important (McMullan 1996; Ungate 1996). Dam removal: Although dams promote lentic habitats that may benefit some centrarchid populations, they have been implicated in declines of native fish biodiversity (Cross and Moss 1987; Li et al . 1987; Petersen and Paukert 2005). As a result, there has been increasing impetus to remove dams and restore riverine systems to pre-impoundment conditions. To date, most removed dams have been smaller structures that are beyond repair (Born et al . 1998). Removal of major dams is unlikely in the near future because of their socioeconomic benefits. Removal of smaller dams will likely have mixed effects on centrarchid fisheries. For example, abundance of lentic species like largemouth bass, crappie, and bluegill may decline after dam removal, but lotic species like smallmouth bass (Weathers and Bain 1992) and spotted bass (Horton et al . 2000), and the rarer riverine species (Koppelman and Garrett 2002) may benefit from removals. In Wisconsin, removal of a dam on the Milwaukee River increased smallmouth bass abundance, likely through increased reproduction and recruitment (Kanehl et al . 1997). On the other hand, removal of a dam in Florida benefited the largemouth bass population as well as improving water quality (Hill et al . 1994). Dam removal may be expected to have mixed effects on centrarchid fisheries, based on evolving habitat changes and species requirements. Removal of smaller watershed dams in disrepair may change centrarchid angling opportunities from lotic-dominated species to lentic-dominated species.

11.9.3 How will recreational fisheries be perceived and managed in the future? The future of centrarchid fisheries depends on the quality of habitats available as well as the future of recreational fisheries in general. Urbanization, reservoir aging, dam removal, and other alterations to habitat will continue to substantially alter centrarchid fisheries. Although habitat degradation may weaken some fisheries, other centrarchid populations may develop as habitats become more suitable for them, as noted in the dam removal discussion (Section 11.9.2 of this chapter). Although urbanization may degrade natural habitats, urban fisheries programs promote centrarchid fisheries in altered habitats and provide more opportunities for urban anglers, typically with species that are readily caught by youths. Many urban fishery programs are spearheaded and run by state and provincial government fish and wildlife agencies in cooperation with nongovernmental organizations (NGOs) in an attempt to attract more anglers to the sport and to promote local fishing opportunities (see Plate 8). Future fisheries participation will depend on opportunities made available to our increasingly urban society (Schramm and Edwards 1994). Increasing opposition to black bass and bluegill as unwanted exotic species in Africa and Japan was noted earlier (Section 11.2.1) and efforts to reduce their numbers have been undertaken. In North America as well, introduced smallmouth bass have been implicated in predation on threatened salmonids in the Pacific Northwest (Zimmerman 1999; Naughton et al . 2004) and in reducing species richness and lake trout abundance in south-central Ontario (Jackson 2002). In the central United States, largemouth bass have been implicated in the decline of federally endangered Topeka shiner (Notropis topeka; Schrank et al . 2001). Elimination of protective regulations for introduced centrarchids, habitat alteration, and fish removals may be undertaken where the public supports such measures. The number of licensed anglers in the United States has remained rather constant despite population growth (Murdock et al . 1992; Namminga and Erickson 1998), and has declined in Canada (Department of Fisheries and Oceans 2003). These trends may affect centrarchid fishery management programs in unpredictable ways. Changing human demographics from rural populations to increasingly urban and suburban populations with increased minority participation in fishing (Murdock et al . 1992) may affect the direction of management initiatives. Marketing fishing opportunities to the demographic mosaic of North America is challenging, but sociological experts believe it is an important component of ensuring the future of recreational fishing opportunities (Duda 1997; MacKee 1997). Many centrarchids are well suited for urban pond fisheries and may increase relative to fisheries for other species, but changes will be shaped by marketing efforts and future participation in recreational fishing (Plate 8). Although challenges to future management are many, constant improvements in techniques for data collection, management, and analysis have been achieved through research, with powerful assistance from increasing computer capabilities. Advances in scientific management will aid managers in sustaining centrarchid fisheries in future decades. Future management also will be aided by the evolving curricula of today’s colleges and graduate programs, which have focused to a greater degree on interactions of social and biological factors in fishery management (Newcomb et al . 2002).

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Guillory, V. 1978. Life history of warmouth in Lake Conway, Florida. Proceedings of the Annual Conference of the Southeastern Association of Fish and Wildlife Agencies 32: 490–501. Guy, C. S. and D. W. Willis. 1990. Structural relationships of largemouth bass and bluegill populations in South Dakota ponds. North American Journal of Fisheries Management 10: 338–343. Hale, R. S., M. E. Lundquist, R. L. Miller, and R. W Petering. 1999. Evaluation of a 254-mm minimum length limit on crappies in Delaware Reservoir, Ohio. North American Journal of Fisheries Management 19: 804–814. Harrington, J. C., C. P. Paukert, and D. W. Willis. 2001. Pumpkinseed population characteristics in Nebraska Sandhills lakes (Pisces: centrarchidae: Lepomis gibbosus). Transactions of the Kansas Academy of Sciences 27: 25–30. Henderson, J. E. 1996. Management of nonnative aquatic vegetation in large impoundments: balancing preferences and economic values of angling and nonangling groups. Pages 373–381 In L. E. Miranda and D. DeVries, editors. Multidimensional Approaches to Reservoir Fisheries Management. American Fisheries Society Symposium 16, Bethesda, MD. Henderson, E. B. and B. G. Whiteside. 1975. Population dynamics of the green sunfish × redear sunfish hybrid as compared with its reciprocal cross and parental species. Proceedings of the Annual Conference of the Southeastern Association of Game and Fish Commissioners 29: 273–278. Hendricks, A. S., M. J. Maceina, and W. C. Reeves. 1995. Abiotic and biotic factors related to black bass fishing quality in Alabama. Lake and Reservoir Management 11: 47–56. Henshall, J. A. 1881. Book of The Black Bass. Robert Clarke and Company, Cincinnati, OH. Henshall, J. A. 1989. More About The Black Bass. The Robert Clarke Company, Cincinnati, OH. Hickley, P., R. Bailey, D. M. Harper, R. Kundu, M. Muchuri, R. North, and A. Taylor. 2002. The status and future of the Lake Naivasha fishery Kenya. Hydrobiologia 488: 181–190. Hill, M. J., E. A. Long, and S. Hardin. 1994. Effects of dam removal on Dead Lake, Chipola River, Florida. Proceedings of the Southeastern Association of Fish and Wildlife Agencies 48: 512–523. Holbrook, J. A., II. 1975. Bass fishing tournaments. Pages 408–414 In R. H. Stroud and H. Clepper, editors. Black Bass Biology and Management. Sport Fishing Institute, Washington, DC. Holland, S. M. and R. B. Ditton. 1992. Fishing trip satisfaction: a typology of anglers. North American Journal of Fisheries Management 12: 28–33. Hooe, M. L. 1991. Crappie biology and management. North American Journal of Fisheries Management 11: 483–484. Hooe, M. L., D. H. Buck, and D. H. Wahl. 1994. Growth, survival, and recruitment of hybrid crappies stocked in small impoundments. North American Journal of Fisheries Management 14: 137–142. Horton, T. B., C. S. Guy, and J. S. Tilma. 2000. Vulnerability of spotted bass to angling in Kansas streams. Journal of Freshwater Ecology 15: 7–11. Hudgins, M. D. and S. P. Malvestuto. 1996. Minimum sociocultural and economic data requirements for optimum yield management of reservoir fisheries. Pages 223–235 In L. E. Miranda and D. R. DeVries, editors. Multidimensional approaches to reservoir fisheries management. American Fisheries Society Symposium 16, Bethesda, MD. Hulbert, A. and W. N. Schwarze. 1910. David Zeisberger’s History of the North American Indians. Ohio Archaeological and Historical Publications 19 pp. 1–189. Columbus, OH. Hunt, J., N. Bacheler, D. Wilson, E. Videann, and C. A. Annett. 2002. Enhancing largemouth bass spawning: behavioral and habitat considerations. Pages 277–290 In D. P. Philipp and M. S. Ridgway, editors. Black Bass: Ecology, Conservation, and Management. American Fisheries Society Symposium 31, Bethesda, MD. Iguchi, K., K. Matsuura, K. M. McNyset, A. T. Peterson, R. Scachetti-Pereira, K. A. Powers, D. A. Vieglais, E. O. Wiley, and T. Yodo. 2004. Predicting invasions of North American basses in Japan using native range data and a genetic algorithm. Transactions of the American Fisheries Society 33: 845–854. International Game Fish Association. 2005. 2005 World Record Game Fishes. International Game Fish Association, Dania Beach, FL. Isermann, D. A., P. W. Bettoli, S. M. Sammons, and T. N. Churchill. 2002. Initial poststocking mortality, oxytetracycline marking, and year-class contribution of black-nosed crappies stocked into Tennessee reservoirs. North American Journal of Fisheries Management 2: 1399–1408. Jackson, D. A. 2002. Ecological effects of Micropterus introductions: the dark side of black bass. Pages 221–232 In D. P. Philipp and M. S. Ridgway, editors. Black Bass: Ecology, Conservation, and Management. American Fisheries Society Symposium 31, Bethesda, MD.

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Plate 1 Introduced to the African continent beginning in 1928, largemouth bass have expanded their range and attained large size, particularly in Zimbabwe and South Africa. In 2004, Maxwell Mashandure caught the African record largemouth bass from Lake Manyame in Zimbabwe, weighing 8.28 kg. In some regions, however, exotic centrarchids are considered a conservation problem due to predation on or competition with native species. Photo credit: African Fisherman.

Plate 2 The ‘‘bass boat’’ has become a popular form of recreational fishing craft, corresponding to the growth of bass fishing. Although a large outboard motor enables anglers to fish distant areas, an electric trolling motor mounted on the bow allows precise boat control in shallow areas often occupied by centrarchids. Bass boats are equipped with livewells to maintain a catch of fish alive during tournaments.

Plate 3 Bass tournament champions like Denny Brauer of Missouri have become popular heroes who may be depicted in advertising promotions such as Wheaties cereal. Tournament competitors are sponsored financially by corporations that promote products via tournament exposure in the media and at outdoors events.

Plate 4 Reservoir construction in the second half of the twentieth century increased habitat for black and white crappie in the United States, and angling popularity of these species increased with it. Angling techniques for these species are diverse, ranging from shore-fishing with long cane poles to trolling offshore structure in boats equipped with numerous rod holders for presenting different baits at variable depths. Photo credit: Soc Clay.

Plate 5 Many sunfish species hybridize readily in both natural and altered ecosystems, and several hybrid forms are stocked in small impoundments and farm ponds for management purposes. This specimen is a natural cross between a green sunfish and a pumpkinseed, caught in Minnesota. Photo credit: Jeff Simpson.

Plate 6 In Canada and northern United States states, ice fishing for centrarchids is an important recreational activity, with the opportunities lasting at least 4 months in colder regions. Sunfish species and crappie are popular for ice fishing, as they form large aggregations and take small baits readily. Photo credit: In-Fisherman.

Plate 7 The largemouth bass has become the most popular target for recreational anglers across North America due to widespread stocking, its ability to thrive in diverse environments, large size, aggressive nature, and associated media attention. Modern management often strives to increase fishing quality by promoting production of large bass through regulations and habitat improvement measures. Photo credit: Steve Quinn.

Plate 8 Development of fishing opportunities for youth and encouragement to participate in the sport will be important in sustaining the recreational angling tradition in North America and ensuring high-quality centrarchid fisheries in the future. Photo credit: Doug Stange.

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Schramm, H. and S. Quinn. 1999. Should we fish for spawning bass? In-Fisherman 24(2): 54–68. Schramm, H. L., Jr., M. L. Armstrong, N. A. Funicelli, D. M. Green, D. P. Lee, R. E. Manns, Jr., B. D. Taubert, and S. J. Waters. 1991a. The status of competitive sport fishing in North America. Fisheries 16(3): 4–12. Schramm, H. L., Jr., M. L. Armstrong, A. J. Fedler, N. A. Funicelli, D. M. Green, J. L. Hahn, D. P. Lee, R. E. Manns, Jr., S. P. Quinn, and S. J. Waters. 1991b. Sociological, economic, and biological aspects of competitive fishing. Fisheries 16(3): 13–21. Schramm, H. L. and G. B. Edwards. 1994. The perspectives of urban fisheries management. Fisheries 19(10): 9–14. Schrank, S. J., C. S. Guy, M. R. Whiles, and B. L. Brock. 2001. Influence of instream and landscape level factors on the distribution of Topeka shiners Notropis topeka in Kansas streams. Copeia 2001: 413–421. Scott, W. B. and E. J. Crossman. 1973. Freshwater Fishes of Canada. Fisheries Research Board of Canada Bulletin 184, Ottawa, Ontario. Shannon, E. H. 1966. Geographical distribution and habitat requirements of the redbreast sunfish Lepomis auritus in North Carolina. Proceedings of the Annual Conference of the Southeastern Association of Game and Fish Commissioners 20: 319–323. Shupp, B. 2002. The B.A.S.S. perspective on bass tournaments: a 21st century opportunity for progressive resource managers. Pages 715–716 In D. P. Philipp and M. S. Ridgway, editors. Black Bass: Ecology, Conservation, and Management. American Fisheries Society Symposium 31, Bethesda, MD. Skelton, P. 1993. A Complete Guide to the Freshwater Fishes of Southern Africa. Southern Book Publishers, Halfway House, South Africa. Slipke, J. W., M. J. Maceina, D. R. DeVries, and F. J. Snow. 1998. Effects of shad density and reservoir hydrology on the abundance and growth of young-of-year crappie in Alabama reservoirs. Journal of Freshwater Ecology 13: 87–95. Smart, R. M., R. D. Doyle, J. D. Madson, and G. O. Dick. 1996. Establishing native submersed aquatic plant communities for fish habitat. Pages 347–356 In L. E. Miranda and D. R. DeVries, editors. Multidimensional Approaches to Reservoir Fisheries Management. American Fisheries Society Symposium 16, Bethesda, MD. Smith, S. M. and D. J. Orth. 1990. Distributions of largemouth bass in relation to submerged aquatic vegetation in Flat Top Lake, West Virginia. Proceedings of the Annual Conference of the Southeastern Association of Fish and Wildlife Agencies. 44: 36–44. Smith, W. B. 1969. A preliminary report on the biology of the Roanoke bass Ambloplites cavifrons Cope in North Carolina. Proceedings of the Southeastern Association of Game and Fish Commissioners 23: 491–500. Steinhart, G. B., M. E. Sandrene, S. Weaver, R. A. Stein, and E. A. Marschall. 2004. Increased parental care cost for nest-guarding fish in a lake with hyperabundant nest predators. Behavioural Ecology 16: 427–434. Stewart, H. 1977. Indian Fishing. University of Washington Press, Seattle, WA. Stroud, R. H. 1970. Future of fisheries management in North America. Pages 291–308 In N. G. Benson, editor. A Century of Fisheries in North America. American Fisheries Society Special Publication 7, Bethesda, MD. Swingle, H. S. 1970. History of warmwater pond culture in the United States. Pages 95–105 In N. G. Benson, editor. A Century of Fisheries in North America. American Fisheries Society Special Publication 7, Bethesda, MD. Trautman, M. B. 1981. The Fishes of Ohio. Ohio State University Press, Columbus, OH. Travnichek, V. H., M. J. Maceina, M. C. Wooten, and R. A. Dunham. 1997. Symmetrical hybridization between black crappie and white crappie in an Alabama reservoir based on analysis of the cytochrome-b gene. Transactions of the American Fisheries Society 126: 127–132. Tufts, B. L. and P. Morlock. 2004. The Shimano Water Weigh-in System; A “Fish-friendly” Guide. Shimano Canada Limited, Whitney, Ontario. Ungate, C. D. 1996. Resolving conflicts in reservoir operations: some lessons learned at the Tennessee Valley Authority. Pages 23–27 In L. E. Miranda and D. DeVries, editors. Multidimensional Approaches to Reservoir Management. American Fisheries Society Symposium 16, Bethesda, MD. Unmuth, J. M. L., M. J. Hansen, and T. D. Pellett. 1999. Effects of mechanical harvesting of Eurasian milfoil on largemouth bass and bluegill populations in Fish Lake, Wisconsin. North American Journal of Fisheries Management 19: 1089–1098. U.S. Deparment of the Interior. 1991. 1991 National Survey of Fishing, Hunting, and Wildlife-associated Recreation. U.S. Department of the Interior, Fish and Wildlife Service, Washington, DC.

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Chapter 12

Contemporary issues in centrarchid conservation and management S. J. Cooke, K. C. Hanson, and C. D. Suski

12.1 Introduction Centrarchid fishes are prominent members of the North American freshwater ichthyofauna. The 34 extant species include some of the most popular and heavily managed sport fish in the world, as well as some of the most obscure and understudied freshwater species in North America. Indeed, several species have only recently been defined, with little known about their natural history. Beyond the species level, there is also a growing recognition that there is significant intraspecific variation among populations. With tremendous inter- and intraspecific diversity, there is great interest in ensuring that these fish are managed and conserved in a manner that maintains genetic integrity of unique populations and ensures long-term persistence. Furthermore, many centrarchids have been introduced to other parts of the globe, providing unique management and conservation challenges. The purpose of this chapter is to provide a detailed overview of the conservation and management issues associated with centrarchid fishes. In particular, the goal is to summarize the various threats that necessitate the use of different conservation and management strategies, highlighting those strategies that have been effective at ameliorating threats. The general conservation status of centrarchids will also be summarized, including the identification of those that are imperiled. More globally, the role of centrarchids as introduced species will also be considered. A consistent message that will be promoted throughout this chapter is that knowledge of basic centrarchid biology can aid in the conservation and management of centrarchid fishes. At times, there is some overlap with other chapters (e.g., Chapter 11 on centrarchid fisheries), but the emphasis here is on integrating material on the basic biology of centrarchids presented earlier in this tome.

12.2 Threats to centrarchid fishes and strategies for minimizing threats Globally, freshwater fishes represent the most imperiled taxa, second only to the amphibians (Bruton 1995). Freshwater fishes face a number of assaults associated with anthropogenic activities. This synthesis not only focuses on broad-scale patterns that should be relevant to many centrarchid species, but also recognizes that there is a large diversity in the threats and sensitivities to threats across the 34 species.

12.2.1 Recreational fisheries Recreational angling has become a popular activity worldwide and is a major component of regional and national economies (Cowx 2002; Cooke and Cowx 2004). Multiple species of centrarchid fishes are commonly targeted by recreational anglers (see Chapter 11 for details). For example, largemouth bass, smallmouth bass, and Florida bass are some of the most popular sport fishes in North America (Pullis and Laughland 1999). In recent years, these species have also become the focus of an ever increasing number of competitive angling events (Schramm et al . 1991; Kerr and Kamke 340

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2003). Crappie (Pomoxis spp.) are also extremely sought-after sport fishes, primarily in reservoirs across the continental United States (Allen and Miranda 1998). Bluegill and other Lepomids are also commonly targeted by anglers. More information on the current and historical roles that centrarchid fishes have played in recreational fisheries can be found in Chapter 11. Recently, it has also been recognized that recreational angling may be involved in the decline of several different fisheries around the world (Cooke and Cowx 2004, 2006; Allen et al . 2005). When considering the potential threats posed to fish populations by anglers, it is important to consider both the harvest of fish as well as the fate of those fish that are angled and released. These are both discussed in detail later.

12.2.1.1 Harvest of centrarchids During the era where catch-and-keep angling was the primary focus of recreational fisheries, centrarchid fishes faced a number of threats. At the time, most research focused on the effects of removing individuals, especially of a certain size, from a population. In fact, angling mortality is typically considered the most important factor in structuring some centrarchid populations such as bluegill (Beard and Essington 2000). Because anglers primarily target larger fish, prized both for consumption and as “trophies”, certain size classes can be heavily exploited. As such, certain population-level effects have been noted. At an extreme level, heavily fished populations can be subject to population crashes (Wilde 1997). Overfishing could also lead to demographic changes in the population including a shift to smaller individuals reproducing earlier in life (Wilde 1997). Neither of these situations appealed to fisheries managers or anglers. As such, many restrictions have been enacted to protect populations and limit the effects of harvest. Typical harvest regulations include bag limits (reducing the number of fish that can be kept by an angler on a given day) and length limits (only allowing fish of a certain size to be kept; Noble and Jones 1999), although there are a number of other strategies that can be employed to manage and conserve centrarchid fisheries in light of recreational fisheries (discussed later). In all cases, there is an assumption that compliance is high, but in practice, enforcement effort and compliance tend to be low. Modeling exercises have revealed that even with low levels of failed compliance (i.e. 15% of total harvest is illegal), largemouth bass fisheries do not benefit from the presence of harvest regulations (Gigliotti and Taylor 1990). Most regulations (especially size limits and bag limits) are limited to largemouth bass, spotted bass, Florida bass, smallmouth bass, black crappie, white crappie, and bluegill. The effects of these management options are heavily dependent on outside factors such as environmental variables and unknown biological relationships, and their effects on the population can be unknown (Quinn 1996). In some instances, these regulations can be effectively used to manipulate abundance and size structure of a population, and to limit harvest in order to maintain sustainable fisheries (Quinn 1996; Wilde 1997).

12.2.1.2 Size limits A commonly used harvest regulation is the restriction of fish sizes that can be harvested. Typically, this restriction is designed to ensure that immature fish are either returned to the water to allow them to mature or that these subadults are not targeted by anglers (Wilde 1997; Noble and Jones 1999). Birkeland and Dayton (2005) identified that it is important to release larger fish. For size limitations to work, they must be based on sound information about the population size structure, size at sexual maturity, and natural mortality rates. For centrarchids, minimum size limits are quite common. When a minimum size limit was instituted in a Wisconsin lake, Newman and Hoff (2000) revealed that harvest rates of smallmouth bass above the minimum size limit increased dramatically. Modeling efforts in Florida revealed that minimum size limits should improve angler catch rates (fish harvested and released; Allen et al . 2002). In Nebraska, a 200-mm minimum length limit minimally increased size structure at current levels of exploitation across all bluegill populations surveyed; the populations with the lowest natural mortality and fastest growth provided the highest increase in size structure with the lowest reduction in yield and number harvested (Paukert et al . 2002). Minimum size limits have also been used for crappie (Colvin 1991) although in some cases they have been rescinded due to angler complaints (Boxrucker 2002). Slot limits (where there is a range of sizes that cannot be harvested) are also frequently employed for centrarchid fishes. In a study of largemouth bass in Delaware ponds, it was revealed that slot limits were ineffective at protecting largemouth bass populations because angler harvest rates of individuals shorter than the protected slot limits were too low to restructure the population (Martin 1995). Angler cooperation is crucial to interactive management techniques such as slot limits and given the strong catch-and-release ethic in many fisheries, many harvest regulations fail. Wilde (1997) reviewed

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length limit evaluations for largemouth bass throughout the United States and found that fishery responses (e.g., change in size structure, angler catch rates) often did not occur, likely because of short evaluation periods after implementation of the regulation. Such regulations are most likely to succeed when there is high angler compliance as well as detailed information on the fishery.

12.2.1.3 Creel/bag limits Creel (AKA bag) limits were designed to mitigate fisheries crashes by capping the number of fish that could be harvested per day (Radomski 2003). Where catch is removed for consumption, limits are frequently placed on total harvest in attempts to control overexploitation and conserve the spawning stock. Typically this is imposed through catch restrictions, that is, quotas in commercial fisheries and bag limits in recreational fisheries. These restrictions do not apply when the fish is returned to water alive after capture. Such restrictions allow for the sharing of the catch when stocks are low or under intense pressure for exploitation. Bag limits are commonly applied to migratory game and put-and-take fisheries to provide equity of catch. An alternative to the bag limit is catch-and-release where restrictions are placed on harvest and all excess fish must be released back to the water. In some cases, harvest limits have completely eliminated harvest of selected species. In some cases, stunting of bluegill populations (high densities of small, slow-growing fish) has been regarded as a symptom of there being too few predators, and in particular, largemouth bass. In fact, some authors (e.g., Anderson 1974) have suggested that largemouth bass overharvest may be the most serious problem limiting the sustained quality of fishing in cases where the waterbody has adequate habitat. Because overharvest of largemouth bass can lead to bluegill overpopulation and reduced fishing quality (e.g., Anderson 1976; Novinger and Legler 1978), restrictions on largemouth bass harvest are frequently used for management of bluegill. However, reduced bag limits rarely reduce harvest unless they are extremely restrictive (Redmond 1974; Shroyer et al . 2003). For example, in Minnesota, after harvest was prohibited for largemouth bass in two lakes, largemouth bass quality increased (i.e. number, sizes); however, bluegill populations were adversely affected (Shroyer et al . 2003).

12.2.1.4 Closed seasons The imposition of a closed season is designed to allow uninterrupted reproduction and the early development of the fish, including, for migratory fish, free passage to spawning grounds. In practice this action has been extended to protect stocks that are heavily exploited through restricted catch. This restriction has often come under heavy criticism because closed seasons are wrongly timed and do not protect fish when they are most vulnerable, such as during the reproductive period (Cowx 2002). Most often, seasonal angling restrictions prohibit the targeting of certain species, especially the black basses, during the reproductive period to ensure that individuals are successful in raising broods (Quinn 2002). Seasonal angling restrictions are widely practiced on the northern limits of the ranges of black basses (Quinn 2002). However, there are few if any closed seasons for other centrarchids in North America. Currently, there is much debate as to the effectiveness of these management practices (see later).

12.2.1.5 Gear restrictions Gear restrictions are used to reduce exploitation of populations by influencing the efficiency of fishing, and the size and species of fish caught. In commercial fisheries, gear type and dimensions, for example, mesh size and size of net regulation, are used to minimize capture of immature and unwanted fish. Much research is now focused on designing gears that select specific target species and sizes of fish, thus minimizing bycatch (see Cooke and Cowx 2004). In recreational fisheries, gear restrictions are usually linked to the type of angling method, for example, fly fishing or spinning, and the baits used, and more recently the use of barbless hooks or circle hooks. To date, there are few examples of gear restrictions for centrarchids outside of competitive angling events where live/organic baits are typically restricted.

12.2.1.6 Protected areas Closed areas are designed to protect stocks directly by denying access to exploitation, and are now well represented in the literature with increased emphasis on aquatic protected areas. These can range from sanctuary areas, where fishing is

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prohibited to protect vulnerable life stages of fish, to restrictions to fishing in areas where the fish are particularly vulnerable to exploitation. In marine systems, protected areas have typically been focused on restricting or eliminating commercial fisheries. However, there are now greater efforts to regulate both fisheries sectors (i.e. commercial and recreational) with the use of protected areas. Some jurisdictions have begun to design aquatic protected areas and closed seasons to protect centrarchid fish populations. Aquatic protected areas prohibit angling in portions of a waterbody to ensure that a portion of the population is allowed to live and reproduce undisturbed by angling and serve as a population source for the rest of the lake. A sanctuary for smallmouth bass on Lake Erie was regarded as effective as angler success [catch per unit effort (CPUE)] was higher during years in which it was instituted (Sztramko 1985). This difference may have resulted either from a preseason harvest of smallmouth bass, which reduced availability during the legal season, a reduction in recruitment, or both. More recently, Suski et al . (2002) described a voluntary sanctuary for largemouth bass and smallmouth bass that was instituted during the reproductive period. Reproductive success was significantly higher within the protected area. Opponents of the use of aquatic protected areas point to the fact that starvation during the first winter is the highest source of mortality on juvenile fishes, and that as such, any reductions in individual reproductive success due to angling during the reproductive period are not noticeable. Further research on the link between individual reproductive success and overall population recruitment is required to properly assess the effectiveness of aquatic protected areas.

12.2.1.7 Ecosystem management Although management of fisheries is moving away from command control systems of fisheries toward ecosystem-based management and community participation approaches, there are major challenges with such approaches in recreational fisheries. Specifically, these strategies are unlikely to function because of the individualistic behavior of the proponents (Pereira and Hansen 2003), although Cowx and Gerdeaux (2004) believe that a change in emphasis to incorporate stakeholders in the decision making is the best way forward. At present, there are few specific examples of where centrarchids have been incorporated into ecosystem management in North America.

12.2.1.8 Catch-and-release angling Centrarchid fishes that are angled are released at rates that are likely unparalleled. Although superficially, release of a captured fish may not seem to be a “threat to centrarchid fishes,” the popularity of recreational fishing has meant that in many cases, few fish are harvested so stress, injury, and mortality from catch-and-release do become the primary consequences of recreational fisheries. Not surprisingly, the centrarchid fishes are some of the best studied with respect to catch-and-release, comparable only to the salmonids (Cooke and Suski 2005; Arlinghaus et al . 2007). Whereas early research on catch-and-release in recreational fishing focused on direct mortality (Muoneke and Childress 1994), current studies have begun to investigate the role of sublethal stressors and their subsequent effect on fishes at the individual and population levels (Cooke et al . 2002). The negative impact of recreational angling has important implications for the conservation and sustainability of centrarchid fisheries and the negative consequences of this activity are presented later. Most often, immediate mortality as a result of angling occurs due to complications in the hooking of a fish resulting from hooking locations such as the gills, gullet, or eyes (Muoneke and Childress 1994). Hooking in these areas, especially the gills, can cause bleeding that leads to immediate death (Pelzman 1978). In addition, more deeply hooked fish require longer hook removal time leading to increased air exposure durations (Cooke et al . 2001b). Delayed mortality can occur during the first 24 hours after release or even later (Muoneke and Childress 1994). Muoneke and Childress (1994) reported that hooking mortality among centrarchid fishes was highly variable and under certain conditions could reach quite high levels (i.e. >90% mortality for some centrarchids—although this is typically during competitive angling events at high water temperatures). There are a number of strategies that can be employed to minimize hooking mortality of centrarchids. For example, barbless hooks have been shown to reduce tissue damage, bleeding, and air exposure duration (through more rapid hook removal) in rock bass (Cooke et al . 2001b). In addition, use of artificial baits rather than organic/live baits tends to result in shallower hooking and less injury and mortality, as has been observed for bluegill (Siewert and Cave 1990) and smallmouth bass (Clapp and Clark 1989). Interestingly, however, scented lures do not appear to cause greater injury or mortality than nonscented lures for smallmouth bass (Dunmall et al . 2001). Hook type also has the potential to influence hooking depth.

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For example, circle hooks have been shown to reduce deep hooking and instead facilitate jaw hooking in a number of fish species (Cooke and Suski 2004). However, there is little evidence that circle hooks make a meaningful difference for centrarchids including rock bass (Cooke et al . 2003a), largemouth bass (Cooke et al . 2003c), bluegill (Cooke et al . 2003e), or pumpkinseed (Cooke et al . 2003e). One of the primary reasons for inconsistent results with circle hooks in centrarchids is the wide range of mouth morphologies and body sizes that makes it difficult to select an appropriately sized circle hook (Cooke et al . 2005a). Research into the sublethal stressors that result from a catch-and-release angling event is also on the rise. Various components of a catch-and-release angling event have been determined to be quite stressful and harmful to the angled fish. An angling event for a fish of any species is essentially a period of intense aerobic and anaerobic exercise that can lead to a host of physiological changes such as depletion of energy stores, increases in lactate in muscle, and disturbances to acid/base balance and osmoregulation. As angling duration increases, the magnitude of these effects also increases. In largemouth bass, the severity of physiological disturbances such as increased levels of lactate, chloride, and plasma glucose has been shown to correlate positively with angling duration (Gustaveson et al . 1991). Similarly, Kieffer et al . (1995) found that physiological disturbance in white muscle (increased lactate and metabolic protons) as well as energy depletion were also more severe as angling duration increased. Smallmouth bass that were angled to exhaustion were also found to require longer periods of time to recover from the cardiac disturbance caused by angling (Schreer et al . 2001). As such, efforts to minimize angling duration (such as use of appropriate equipment) are helpful in minimizing anaerobic physiological disturbance. Air exposure has also been proven to cause negative physiological disturbances for a variety of fish species, and the results of these studies are applicable to centrarchid fishes. While exposed to air, gill filaments can adhere to each other as a result of the collapse of gill lamellae (Boutilier 1990). During this time, the fish are essentially deprived of oxygen and subjected to induced anoxia that can reduce the amount of oxygen delivered to tissues (Ferguson and Tufts 1992). Air exposure has also been shown to increase the severity of various physiological disturbances associated with angling (Ferguson and Tufts 1992). Air exposure also induces negative cardiovascular disturbances in both rock bass and smallmouth bass, with individuals exposed to air for longer durations requiring longer to return to basal levels (Cooke et al . 2001b; Cooke et al . 2002). In addition, if fish are held in nets during air exposure, scale loss can occur, which has been identified as a precursor to mortality in bluegill (Barthel et al . 2003). Simply minimizing air exposure duration, or ideally eliminating it, is the best way to minimize the negative consequences of air exposure. Fish should be held by wet hand rather than in nets if possible. Mortality among angled individuals has also been linked to water temperature during the angling event. Physiological disturbance and associated mortality have been shown to occur more often when fish are angled at extremely high temperatures. Fish subjected to exhaustive exercise show increased levels of physiological disturbance (lactate and metabolic protons in the blood) at higher water temperatures. High water temperatures have been found to exacerbate the physiological disturbances associated with angling duration (Meka and McCormick 2005). In smallmouth bass and largemouth bass, the recovery from the cardiac disturbance associated with angling also varies with water temperatures (Schreer et al . 2001; Cooke et al . 2003d). Also, mortality of angled largemouth bass increased with water temperatures, particularly beyond a threshold in the high 20◦ Cs (Wilde 1998). Anglers should avoid fishing at high water temperatures (i.e. >30◦ C) or if that is not possible, minimize other stressors such as air exposure and angling duration. One of the only studies evaluating the interaction between multiple stressors revealed that mortality rates of bluegill were highest when warm water temperatures (>26◦ C) were coupled with prolonged air exposure (>120 s; Gingerich et al . 2007). Mortality was negligible when air exposure was eliminated even though water temperatures were high. Centrarchid fishes are particularly vulnerable to angling during their reproductive period. Briefly, during the reproductive period male centrarchids construct nests, court females, and provide vigorous defense to the developing brood for some amount of time ranging from a few days to a month or longer (Cooke et al . 2006). Males angled prior to the reproductive period were found to produce fewer and smaller offspring than nonangled males (Ostrand et al . 2004). During the reproductive period, when the male is removed from the nest by anglers, predators can devour the brood, thereby directly reducing the fitness of the individual (Neves 1975; Philipp et al . 1997; Steinhart et al . 2004a; Hanson et al . 2007). Research has demonstrated that brood loss to predation is responsible for nest abandonment in angled centrarchids, rather than physiological disturbances associated with the catch-and-release angling event (Suski et al . 2003b). As the time the male is kept away from the nest increases, the percentage of the brood consumed by predators also increases, increasing the likelihood of abandonment by the male (Kieffer et al . 1995; Philipp et al . 1997). More importantly, the individual males

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that are most vulnerable to angling are often largest and most aggressive fish that have nests with the highest numbers of eggs (Suski and Philipp 2004). Because males with the largest broods (and therefore the largest potential to contribute to year class formation) are the most likely to be caught by anglers, negative population-level effects may occur if nesting centrarchids are subjected to angling pressure during the nest-guarding period (Suski and Philipp 2004). Ridgway and Shuter (1996) predicted that as the number of angled male smallmouth bass increased across the reproductive period, the abundance of age-0 fish would decrease due to brood predation and nest abandonment. The negative effects of a catch-and-release event linger with angled male even after he returns to the nest and resumes nest-guarding behavior. Previously angled largemouth bass have reduced locomotory potential when compared to nonangled individuals while guarding nests (Cooke et al . 2000). This disturbance coupled with brood loss due to predation during the angling event could increase nest abandonment and loss of fitness (Cooke et al . 2002). Also, during the parental care period, nestguarding male bass are not free to forage normally and are engaged in a set of energetically costly behaviors (Hinch and Collins 1991; Cooke et al . 2006). Physiological disturbance during this time period of high stress, low food consumption, and high energetic demands may be particularly debilitating to the ability of the male to successfully raise a brood (Cooke et al . 2002). Based on this information, it appears prudent that angling should be restricted during this period. Interestingly, there are very few jurisdictions where angling during bass reproductive period is actually prohibited (e.g., Ontario; Quinn 1989). The topic of restrictive angling regulations during centrarchid spawning is a contentious topic in the angling and fisheries management communities with several weak arguments supporting the more liberal perspective: (i) Work to date has focused on the northern populations where the growing season is much shorter. As such, the findings from the “north” do not apply elsewhere. Although it is quite likely that there are latitudinal differences in reproductive biology and growing season, there is still no evidence to support the idea that angling during the reproductive period is either beneficial or benign. (ii) If catch-and-release angling for nesting bass is harmful, then why is there not evidence of massive collapse in intensive fisheries? This argument is difficult to address given the challenge of monitoring fish populations, particularly adult centrarchids. However, in many jurisdictions where angling for nesting fish is permitted, there are also supplemental stocking programs that could mask negative effects. What is clear is that there is a need for additional research to evaluate the link between reproductive success and recruitment, as well as comparative research in warmer clines (than Ontario) to test the hypothesis that angling during the reproductive period is not an issue for black bass in the south. Because of the contentiousness of this issue, only with additional data in hand from more regions will managers be able to make informed decisions based on scientific fact.

12.2.1.9 Competitive angling events An area of specific concern for centrarchid conservation is the growing popularity and prevalence of angling tournaments targeting black basses, specifically largemouth and smallmouth bass (Shupp 1979; Schramm 1991). During tournaments, angled fish face multiple situations that can result in physiological disturbances, and that may ultimately lead to mortality (Suski et al . 2003a; Siepker et al . 2007). That said, competitive angling events provide unique opportunities to assess black bass fisheries through tournament monitoring programs, and recent estimates of mortality rates confirm that, at many tournaments, most fish are returned to the water alive following the completion of the angling day (Wilde 1998). In some cases, tournament-collected data provide the only information on difficult-to-sample water bodies such as medium-sized rivers (e.g., Cooke et al . 1998). During competitive angling events, multiple fish are often confined to livewells for extended periods of time. While retained in a livewell, fish can quickly face extremely poor water quality as ammonia and dissolved carbon dioxide levels rise and dissolved oxygen decreases (Hartley and Moring 1993; Kwak and Henry 1995), resulting in a state of hypoxia and a host of physiological disturbances associated with air exposure (Furimsky et al . 2003). These conditions are exacerbated by high densities of fish confined within the livewell (Cooke et al . 2002). Also, when confined at high densities in a livewell, fish show increased physiological and cardiac disturbances (Cooke et al . 2002). Another source of mortality during livewell confinement may be disturbances associated with wave conditions (Kwak and Henry 1995). Recent video analysis of largemouth bass behavior during livewell confinement found that during low level disturbances, individuals remained active (Suski et al . 2005). During high intensity disturbance, largemouth bass tended to face the direction of the disturbance while staying near the bottom of the livewell, allowing them to avoid repeatedly hitting

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the sides of the livewell (Suski et al . 2005). Anglers should ensure that livewells are properly circulated so as keep water quality favorable (Gilliland 2002), keep densities of fish in livewells as low as possible (Cooke et al . 2002), and operate their boat in a manner that minimizes disturbance associated with wave action (Suski et al . 2005). The addition of livewell conditioners has also been suggested as a way to help fish recover from livewell confinement. Currently, there is conflicting evidence as to whether livewell conditioners enhance recovery, and more research needs to be conducted on this topic to conclusively prove the benefit or harm of livewell conditioners (Gilliland 2002; Cooke et al . 2002). Recent research revealed that hyperoxygenation or decreasing livewell water temperatures did not aid in recovery of bass during livewell retention and actually increased physiological disturbance (Suski et al . 2006). Livewells are always preferable to stringers or fish baskets for temporarily retaining centrarchids (Cooke and Hogle 2000). During an angling tournament, fish are subjected to repeated air exposure. While angling, fish are often air exposed as anglers repeatedly place and remove them from livewells while culling individuals from the final catch (Cooke et al . 2002). At the end of a tournament, fish are subjected to weigh-in processes before release. Often, these processes include extended periods of confinement in nonaerated water in holding areas followed by air exposure during the weighing (Suski et al . 2004). During this time period, bass showed significant metabolic disturbances related to air exposure including increases in tissue lactate, cardiac disturbances, and decreases in tissue energy stores (Suski et al . 2004). The cumulative effect of these stressors may lead to later mortality by impairing the ability of released individuals to survive (Cooke et al . 2002). To minimize the physiological disturbances of weigh-in, it has been suggested that tournaments minimize air exposure throughout, but especially during weighing by keeping fish in well-aerated water as often as possible (Furimsky et al . 2003; Suski et al . 2004). Recent innovations have included the development of a water weigh-in system that almost eliminates air exposure (Suski et al . 2004). In addition to the disturbances that bass can experience during an angling tournament, research has shown that events following the release of fish can have potential for population-level impacts. Specifically, high concentrations of fish are often released in a small area at the conclusion of an angling tournament resulting in a “stockpiling” of fish that can persist for short periods of time. Ridgway (2002), for example, reported that over 2 weeks had passed before translocated largemouth bass moved 400 m from a common release site, whereas Wilde and Paulson (2003) showed that 63% of tournament-caught largemouth bass remained within 0.5 km of their release site following a 43-day monitoring period. Ridgway and Shuter (1996) showed that displaced smallmouth bass remained near their release site from <1 day to 30 days (mean = 7.79 days), whereas Bunt et al . (2002) reported that smallmouth bass in Ontario remained within 1 km of their release site for a mean duration of 54 days (range = 9–300 days, n = 18 fish). A review by Wilde (2003) found that 51% of largemouth bass and 26% of smallmouth bass released following angling tournaments remained within 1.6 km of the release site. Gravel and Cooke (2008) suggested that dispersal of smallmouth bass from a release site may be retarded if fish have experienced barotrauma during an angling tournament, but this hypothesis has not been tested with tournament-caught largemouth bass. In addition to concerns of stockpiling, several studies have reported that tournament-caught fish often do not return to their pre-tournament home ranges, which may negatively impact feeding or reproduction. In a recent review, Wilde (2003) reported that only 14% of largemouth bass and 32% of smallmouth bass caught during angling tournaments returned to their capture sites. Wilde (2003) also reported that there was no relationship between the distance traveled by released bass and the duration of time for which they were followed after release, and that dispersal rates did not differ across the different waterbodies studied. The likelihood of bass returning to their home range might be influenced by the distance that fish are released from their home range. For example, in controlled displacement experiments, Ridgway (2002) showed that 37% of smallmouth bass that were displaced between 1.5 and 16.5 km from their home ranges returned to their capture site, but 100% of largemouth bass released at less than 8 km from their home range returned to their release site. Further research in this area is warranted to quantify the population-level impacts of dispersal and altered home ranges.

12.2.2 Commercial fisheries Commercial fisheries are active in large lakes and rivers throughout the native range of most centrarchid fishes, especially in the Mississippi River drainage and the Laurentian Great Lakes. Traditionally, small-scale commercial fisheries were operated targeting centrarchid fishes (Trautman 1981). In the early twentieth century, multiple jurisdictions throughout

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North America designated most centrarchid species as “gamefish” and enacted legislation to prohibit their commercial harvest and transportation (Chapter 11). Other centrarchid species, such as sunfish (Lepomis spp.), crappie (Proxomis spp.), and rock bass (Ambloplites rupestris), although considered “gamefish,” have been subjected to commercial harvest in limited numbers in various jurisdictions (Chapter 11). Between the years 1976 and 1981, the largest commercial fishery targeting centrarchid species occurred in Lake Okeechobee, Florida, in an attempt to improve the crappie (Pomoxis nigromaculatus) fishery by reducing population densities to improve individual growth (Schramm et al . 1985). The fishery targeted black crappie, bluegill (Lepomis macrochirus), and redear sunfish (Lepomis microlophus) and was considered a success for management reasons, but closed due to the possibility of overexploitation and public sentiment against commercial harvest of fishes sought after for recreational purposes (Schramm et al . 1985; Miller et al . 1990). Because of the immense popularity of the recreational centrarchid fishery and associated economic benefits, the value of centrarchids as sportfish outweighs their value to the commercial fishery. As mentioned earlier, the commercial harvest of other economically important fish species occurs throughout the native range of centrarchid fishes. Within the Mississippi River drainage, multiple species of pelagic filter feeders are harvested mainly by netting (Sheehan and Rasmussen 1999). This practice has raised the concern that the bycatch in these areas may contain game fish species such as centrarchids. Due to the fact that the value of many sport fish species to local economies in recreational fisheries is greater than commercial value, there are fears that commercial fishing may hurt recreational angling opportunities in the area (Noble and Jones 1999). As such, many gear and harvest regulations have been put in place to lessen the frequency of game fish as bycatch in inland fisheries (Fritz and Wright 1986). For instance, certain harvest techniques, such as trap netting, which focus on species in the littoral zone are often restricted during the spring months when centrarchid fishes frequent these areas to spawn. Other restrictions include regulations on mesh size of commercial nets, types of nets that can be used, and strict quotas on acceptable bycatch (Noble and Jones 1999). As a result of these restrictions, the incidental catch of centrarchid fishes seems to be low (Noble and Jones 1999).

12.3 Introduction of exotics Across their endemic range, centrarchid fishes have been impacted heavily by the introduction of exotic species. Sometimes these threats are in the form of fishes that consume important life stages of centrarchids or compete for food and space (Moyle 1986). In other instances, the threats come in the form of exotic plants or invertebrates that alter the habitat and water chemistry or productivity of the environment, affecting the ecology of the endemic centrarchids. The threats associated with introduction of exotic organisms are rarely restricted to the centrarchid fishes and in fact have contributed to the imperilment and demise of many freshwater fishes in North America (Richter et al . 1997; Ricciardi and Rasmussen 1998). Here, we present only a brief overview of some of the more devastating and well-known interactions between centrarchid fishes and exotic organisms that cover a range of exotic taxa and impacts. Interestingly, many of the more prominent and devastating effects are concentrated in the Laurentian Great Lakes (Mills et al . 1993), but are increasingly spreading throughout the Mississippi and other drainages. The round goby (Neogobius melanostomus) represents one of the most recent (June of 1990; Jude et al . 1992) and potentially devastating invaders to the Laurentian Great Lakes and has been already implicated in a number of threats to smallmouth bass and other centrarchids. The goby is a bottom-dwelling fish endemic to Europe (the Black, Caspian, Marmara, Azov, and Aral seas) that has been observed at densities exceeding 100/m2 in Lake Erie (Charlebois et al . 1997). In North America, they are well regarded for their direct effect on the reproductive output of endemic fishes. Although for centrarchid fishes they have not led to the recruitment failures seen in the mottled scuplin (Janssen and Jude 2001), there is a growing body of literature indicating that the goby can directly reduce offspring numbers in nests through predation, but usually only when the impact of weather conditions such as storms make care difficult for centrarchid fishes, especially from recreational angling (Steinhart et al . 2004a). Experimental removal of smallmouth bass from their nest by recreational angling led to round goby consuming all offspring within 15 minutes (Steinhart et al . 2004a). Even when the nest-guarding male was released after capture, as many at 2000 offspring were consumed by round goby during the time that the parent was absent. There is also an increased cost associated with having to defend nests from hyperabundant nest predators such as round goby. Steinhart et al . (2004b) compared nest-guarding behavior and energy expenditures in Lake Erie with a hyperabundant

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population of round goby versus a system with fewer predators overall and no gobies. Nest defense characterized by chasing predators was nine times higher in the presence of gobies resulting in a decline in the mass and energy density of nest-guarding males. In fact, the standard metabolic rate of smallmouth bass was raised by 210% in the presence of gobies but only 28% in the other system. In addition, the added cost of defending the nest may impair the ability of parental male centrarchid fishes to engage in reproduction in subsequent years, hence affecting lifetime fitness as well as growth and survival. Although gobies prey upon the eggs and offspring of smallmouth bass and other centrarchids, some centrarchids also prey upon gobies. Because gobies have the potential to mobilize contaminants from the bethos to higher trophic levels (Morrison et al . 2000), this may also contribute to future contaminant problems with piscivores such as smallmouth bass. Another example of a Great Lakes exotic that is a threat to centrarchid fishes is the zebra mussel (Dreissena polymorpha). Since its introduction into the Great Lakes around 1988, the distribution of the zebra mussel has expanded to include many inland water ways throughout Midwestern North America prompting concern for endemic organisms. Zebra mussels have become the primary filter feeder in many aquatic systems driving changes in zooplankton community structure and abundance (Beeton and Hageman 2001). Despite these changes, the effects of zebra mussels on centrarchids and other fishes has been equivocal (e.g., Trometer and Busch 1999). In some experiments, adult bluegill growth has not been affected by the presence of zebra mussels (e.g., Richardson and Bartsch 1997) but in some cases growth has improved for adult pumpkinseed (Mercer et al . 1999) and largemouth bass (Strayer et al . 2004). However, growth impairments on centrarchids have been noted during early life stages. Raikow (2004) reported that during their first 2 weeks of life, larval bluegill reared in the presence of zebra mussels grew 24% more slowly than fish reared without zebra mussels. The author concluded that the differential growth rates were due to competition between mussels and bluegill for food in the form of microzooplankton. Furthermore, the author surmised that there was also indirect competition by starving the zooplankton as zebra mussels consumed the phytoplankton. Thus, obligate planktivores, such as the early life stages of most centrarchid fishes, might suffer from the presence of zebra mussels (Raikow 2004). In another study, predation by bluegill on amphipods was significantly lowered by mussel presence due to a reduction of predation risk for amphipods from increased habitat complexity provided by zebra mussels on the substrate (Gonzalez and Downing 1999). Invasive exotic aquatic vegetation also represents a major threat to centrarchid fishes. In particular, canopy-forming macrophytes such as Eurasian watermilfoil (Myriophyllum spicatum) and hydrilla (Hydrilla verticillata) have had significant impacts on centrarchid ecology. Both species of plants are now established throughout North America in lentic environments. The primary effect of these two exotic plants is that they displace the more structurally complex macrophytes that are endemic to the waterbody. A series of experiments by Valley and Bremigan (2002) revealed that dense canopy monocultures typical with exotic macrophytes increased search times and reduced attack and consumption rates of largemouth bass on bluegill. However, the effects of macrophyte density and degree of canopy monoculture on largemouth bass foraging success were similar in magnitude. Therefore, among systems, largemouth bass foraging will depend upon the degree to which macrophyte density and architecture influence structural complexity. In the winter, the decomposition of these exotic macrophytes under the ice can contribute to hypoxia and winterkill (Smith and Barko 1990). In addition to the few detailed examples presented earlier, several other impacts have been documented. For example, a number of exotic parasite introductions have also afflicted centrarchid fishes. The parasitic copepod Neoergasilus japonicus, native to eastern Asia, has been documented on largemouth bass, pumpkinseed sunfish, bluegill, green sunfish, rock bass, and smallmouth bass in the Great Lakes (Hudson and Bowen 2002). In recent years there has also been interest in examining the influence of tilapine fishes on endemic centrarchids in the southern United States (e.g., Ippolito 1985; Shafland 1995; Peterson et al . 2002) with disparate results. Others have documented the consequences of introduced planktivores (i.e. inland silversides and threadfin shad) on white crappie (Crowl and Boxrucker 1988). There are also an untold number of other impacts on centrarchid fishes associated with exotic organisms. This is likely particularly true for some of the nongame species that are not as well studied as the centrarchids with higher economic value. There are no specific strategies for centrarchid fishes with respect to exotics. Organisms are introduced both accidentally and intentionally and as described earlier, can have major negative consequences on centrarchids (and other fishes). General strategies for minimizing the introduction and spread of exotics include public education and regulations (on the transport of live animals, ballast water spilling, etc.). Increased research on centrarchid interactions with exotics may help to predict and control impacts of exotics (Ricciardi and Rasmussen 1998).

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12.4 Environmental alteration and degradation As the aquatic environment is faced with an increasing burden of pollutants, fish populations face an ever increasing number of threats from toxins, thermal effluents, changes in turbidity, and eutrophication.

12.4.1 Pollution 12.4.1.1 Toxins and heavy metals Centrarchid fishes are commonly used as models in toxicity tests. Currently, in Canada, pesticides require testing with both bluegill (warmwater fish) and rainbow trout (coldwater fish) prior to approval for use. Bluegill are a standard test organism in North America for toxicological research and regulatory studies, partially due to their distribution in many warmwater systems, as well as the fact that they are thus readily available do well in captivity. They habituate quickly to laboratory conditions enabling complex studies of variables such as feeding behavior and ventilation rates. Acute toxicity of bluegill has been determined for a number of substances including toxaphene (Johnson and Julin 1980); however, rarely are these studies published in the primary literature. Bluegills have also been used to study the rate of bioaccumulation of heavy metals such as mercury (Peterson et al . 1996). Also, in the 1970s, bluegill were used extensively as a part of automatic biological monitoring facilities to assess the toxicity of industrial effluents to aquatic organisms (e.g., Gruber and Cairns 1981). Bluegill ventilatory rates were monitored using individual holding cells fitted with electrodes. Chlorine is also toxic to centrarchids (Cooke and Schreer 2001). For example, Cooke et al . (2004) observed that 50% of smallmouth bass that they were monitoring in a thermal effluent canal left during a biofouling chlorination pulse and did not return. Heavy metals, the by-product of many industrial and mining processes, often pollute inland waterbodies inhabited by centrarchid fishes, posing a threat both to fish inhabiting the area and to humans who consume those fish. Heavy metals often enter aquatic systems through runoff from agricultural or industrial areas, and are subsequently present in sediments for long periods of time, posing a threat to fishes through bioaccumulation (Saiki et al . 1992; Campbell 1994; Park and Curtis 1997). Exposure to heavy metals such as cadmium, arsenic, selenium, and mercury has been shown to reduce growth rates in bluegill, as well as possibly hindering foraging efficiency (Cope et al . 1994; Lefcort et al . 2002). Heavy metals can also disturb brain function and liver function in bluegill (Choich et al . 2004; Oliveira et al . 2004). Bluegill exposed to copper show decreases in ATP and ADP as well as a loss in tissue water (Heath 1984). Largemouth bass subjected to high levels of mercury in the wild have been shown to suffer reproductive problems such as development of intersex individuals and poor gonadal condition (Schmitt et al . 2005). Physiological disturbances occur within the blood and intestinal tissue of bluegill when exposed to high levels of methylmercury (Hossain and Dutta 1983; Dutta et al . 1983). The levels of mercury and methylmercury within the tissues of centrarchid fishes can often be above the safe guideline for human consumption set by the US Food and Drug Administration. Often, the levels of mercury and methylmercury are quite low in smaller sunfishes such as bluegill, pumpkinseed, and redear sunfish that inhabit lower trophic levels (Mills et al . 1994; Dupre et al . 1999; Mueller and Serdar 2002). Unfortunately, larger, piscivorous centrarchid species, such as largemouth and smallmouth bass, are subject to biomagnification of heavy metals and often have high levels of contaminants in their tissues (Park and Curtis 1997; Neumann and Ward 1999; Scheuhammer and Graham 1999; Burger et al . 2001; Burger et al . 2002; Mueller and Serdar 2002). Also, levels of heavy metals increase with size of fish and age (Scheuhammer and Graham 1999; Burger et al . 2001, 2002; Castro et al . 2002). Consumption of fishes with high levels of contaminants, especially heavy metals, can be extremely dangerous for humans, especially pregnant or nursing mothers (Jarup 2003). Heavy metal poisoning can cause serious neurological damage in developing fetuses, damage the internal organs of adults, and elevate the risk of cancer in humans (Watanabe et al . 2003; Jarup 2003; Saiki et al . 2005). Consumption of contaminated fish can also lead to reproductive problems for piscivorous aquatic birds such as loons and herons (Scheuhammer and Graham 1999). To prevent exposure of centrarchid fishes to toxic contaminants, multiple steps can be taken. Industrial and agricultural runoff should be properly filtered to remove contaminants prior to reaching waterbodies. To reduce the bioavailability of toxins in contaminated areas, clean sediment can be used to seal contaminants away from the water column, thus

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preventing their bioaccumulation in fishes and other biota (Haines et al . 2003). These strategies are generic to freshwater fishes and not specific to centrarchids.

12.4.1.2 Thermal pollution Thermal pollution poses unique threats to fish due to the fact that their activity and metabolic rates fluctuate with water temperature (Fry 1971). In fact, ambient water temperature has been called the abiotic “master” factor controlling fish activity, metabolism, and behavior (Brett 1971). Thermal pollution most often arises due to the need for cooling water in many modern industrial practices and can increase absolute water temperatures as well as cause extreme temperature fluctuations (Coutant 1970). The thermal conditions that result can often be harmful to fish (Coutant 1970, 1977), but may also be beneficial under certain circumstances. As such, anthropogenic thermal pollution can induce marked changes in behavior among affected centrarchid fishes. Thermal discharge canals can provide thermal refugia to fish during the winter months when ambient water temperatures drop in northern latitudes. It was also noted by Cooke et al . (2003b) that fish showed elevated parental care activity rates that may have been influenced by the elevated water temperatures. Studies in the same system revealed that smallmouth bass resided in the thermal effluent channel overwinter, and departed the canal when water temperatures in the lake rose in spring time (McKinley et al . 2000; Cooke et al . 2004). During the winter period, fish conducted extensive local movements and foraged on prey that had passed through the discharge system (Cooke et al . 2004). It was hypothesized that bass resided in this area because of the combination of ample forage and higher water temperatures that allowed fish to not go into a state of torpor during the winter (Ross and Winter 1981; Cooke et al . 2004). Thermal pollution can also accelerate behaviors that are triggered by water temperature. Cooke et al . (2003b) observed that smallmouth bass affected by thermal discharge from a coal power plant on Lake Erie initiated spawning approximately a month sooner than unaffected fish. During the nest-guarding phase, several upwelling events cooled water temperatures below 15◦ C (commonly cited as the minimum temperature at which smallmouth bass will spawn), but male bass remained on their nests until broods were reared successfully (Cooke et al . 2003b). Lastly, in areas with high ambient water temperatures, thermal discharge canals can increase water temperatures to the lethal range of centrarchid fishes. It is not uncommon for thermal discharges to raise local water temperatures by 5 to 14◦ C. If this were to be coupled with high ambient water temperatures during summer months, the lethal thermal maximum for certain centrarchids could easily be reached (Fields et al . 1987; Currie et al . 1998). As such, it would be expected that centrarchid fishes would avoid areas affected by the effluent during these times. Cooke et al . (2004) noted that temperatures in a cooling canal reached the upper tolerance limit for smallmouth bass during summer months. To protect centrarchids and other fishes from fluctuating thermal conditions, management agencies have imposed guidelines that regulate the maximal change as well as rate of change in water temperature relative to ambient conditions.

12.4.1.3 Sedimentation/turbidity Although not directly lethal to adult fish, increased siltation and changes in turbidity can also be a concern for centrarchid fishes. Most research into this subject has focused on the effects of increased silt load on the ecology of fishes. In general, it has been shown that increased turbidity and silt loads interfere with the abilities of fishes to forage. Increased silt loads decrease the distance at which a prey item may be visible, thus impairing the abilities of large, visually orientated predators, such as centrarchids, to locate and subdue prey (Utne-Palm 2002). The reactive distance (defined as the distance at which a predator visually detects prey) and foraging success of smallmouth bass decreases with increasing turbidity (Sweka and Hartman 2003). Miner and Stein (1996) measured the reaction distances of prey (bluegill) and predator (largemouth bass) in increasingly turbid environments. It was found that the reaction distance of the predator decreased more quickly in turbid environments than that of the prey, thereby affording the prey a higher probability of survival in more turbid water (Miner and Stein 1996). Johnson and Hines (1999) determined that as silt loads increased, juvenile razorback sucker (Xyrauchen texanus) were better able to avoid predation by green sunfish (Lepomis cyanellus). Other studies, many on other families of fishes, question the role turbidity plays in foraging success in the wild. Reid et al . (1999) found that as turbidity increased, no significant differences could be found in capture success by adult largemouth bass. When the stomach contents of fish collected from turbid and clear environments were analyzed, it was

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determined that consumed prey items are more regulated by prey availability than by water conditions (Reid et al . 1999). Due to the abilities of fishes to successfully forage in naturally occurring low light levels, and indeed in the absence of light, it has been proposed that other, nonvisual mechanisms, such as the lateral line system, may be equally important in foraging success (Rowe et al . 2003). Also, other factors—such as increased predation activity, reduced visual acuity of prey, altered contrast of prey, and reduced anti predator behaviors—may mitigate the perceived advantage of prey in turbid water conditions (Granqvist and Mattila 2004). Increased siltation in lakes and rivers can have potentially damaging impacts on the spawning success of centrarchid fishes. When spawning, male centrarchids construct nests in the littoral zones of lakes. These nests are often constructed in specific substrate selected by the males for the purpose of egg adhesion and water quality (Heidinger 1975). Some species, such as smallmouth bass, spotted bass, and rock bass, prefer hard, rocky substrate with minimal amount of fine sediment (Coble 1975; Vogele 1975; Gross and Nowell 1980). Increased sedimentation may have negative impacts on species such as these by limiting access to proper spawning areas. Whereas other species, such as largemouth bass and bluegill, may choose to construct nests on finer sediment (Kramer and Smith 1962), suspended sediment in the water column can be detrimental to nest success. All male centrarchids, to a greater or lesser extent, provide parental care to their brood including fanning the nest to prevent sediment deposition that would result in the smothering of eggs or larvae and subsequent nest failure. Nests in areas in which large quantities of suspended sediment are present would have a greater chance of being smothered as sediments were deposited, and would, therefore, not be suitable nesting habitat. Increases in suspended sediments in the water column can also have negative sublethal effects on adult centrarchids. Suspended sediment can coat the gills of adult fish, thereby limiting their ability to conduct gas exchange and waste removal across the gill membrane (Ellis 1944; Waters 1995; Bunt et al . 2004). Bunt et al . (2004) found that rock bass showed increased cardiovascular disturbance when subjected to water with increased silt loads. Interestingly, individuals of riverine origin rapidly acclimated to silt concentrations, whereas individuals from lacustrine environments did not, pointing to the possibility of local adaptation to turbid water conditions (Bunt et al . 2004). Exposure to suspended sediments can also increase exposure to toxic metals as well as limit growth in centrarchid fishes (Cope et al . 1994). While the effects of suspended sediment may not be lethal to adult fish, various sublethal stressors that occur can decrease the overall condition of the individual. All freshwater fish benefit from land-use strategies that minimize silt runoff, which is the primary contributor to turbidity.

12.4.2 Eutrophication Anthropogenic eutrophication of water bodies is occurring throughout the range of centrarchid fishes, often with negative impacts on fish communities. As a water body becomes more eutrophic, vegetative and algal biomass may increase drastically. This may then influence water quality in multiple ways that are detrimental to the survival of fishes. Increased aquatic vegetation can lead to drastic changes in dissolved oxygen in the water. During warm months and at night, aquatic vegetation can reduce dissolved oxygen to levels resulting in hypoxic conditions that are detrimental to centrarchid fishes (Sculthorpe 1985; Frodge et al . 1990). Hypoxia can lead to physiological disturbance, if not direct mortality (Furimsky et al . 2003). Typically, “summer kills” occur in eutrophic lakes when massive blooms of algae reduce dissolved oxygen to lethal levels in a water body resulting in large-scale fish mortality. Additionally, during winter months when ice cover prevents photosynthesis, aquatic vegetation typically dies and then decomposes on the bottom of the lake. “Winter kills” may occur if dissolved oxygen reaches the lethal minimum of centrarchid fishes as a result of hypoxia due to vegetation decomposition (Smith and Barko 1990). Also due to respiration, plants can cause swings in water chemistry such as large changes in pH and carbon dioxide (Sand-Jensen 1989). If environmental pH drops too low, fish can suffer from blood acidosis, which reduces the blood’s ability to transport oxygen (Perry and McDonald 1993; Randall and Lin 1993). Centrarchid fishes may fare poorly in highly eutrophic water bodies, and may need to avoid thickly vegetated areas or modify behavior due to poor water quality conditions created by aquatic vegetation (Miranda and Hodges 2000; Miranda et al . 2000). It has also been found that as water bodies become increasingly eutrophic, the CPUE of sportfish, including multiple centrarchid species, declines (Egertson and Downing 2004). Also, in areas of highly dense macrophytes, piscivorous centrarchids suffer from reduced foraging efficiency, which may also result in reduced growth (Crowder and Cooper 1979; Savino and Stein 1982; Valley and Bremigan 2002).

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12.4.3 Physical habitat alteration One of the greatest threats to global biodiversity is habitat destruction or alteration. Humans have greatly altered many riverine and lacustrine habitats through a wide variety of activities. As a result of this habitat alteration, freshwater fish populations are threatened, sometimes to the point of extinction (Miller et al . 1989; Chu et al . 2005). Riverine environments are often altered to suit the needs of agriculture (both as water supply and drainage), electrical generation, and navigation. As such, many rivers and streams throughout the range of centrarchid fishes have been altered significantly. Large river systems in North America have been channelized and prevented from flooding. Consequently, fish often find themselves subjected to unnatural hydrological regimes as well as unable to move to favorable habitat in floodplains. Junk et al . (1989) found that fish production is increased in rivers that retain access to floodplain habitats. Within floodplain habitats, centrarchid fishes find greater food availability, which can lead to increased growth and fecundity (Springate et al . 1985; Crim and Glebe 1990; Neckles et al . 1990; Lemke et al . 2003). Greater numbers of juvenile centrarchid fishes are often found in backwater areas of floodplains rather than in the river itself (Slipke et al . 2005). Channelized streams suffer from severely degraded habitat that leads to loss of biodiversity. Centrarchid fishes residing in channelized streams may not have access to suitable spawning or foraging habitats. Populations in degraded areas oftentimes suffer from low numbers, and individuals within the population may be small as a result of poor quality forage. Lacustrine environments are often subjected to shoreline development in the form of residential development. Along with the building of homes along water bodies, roads, water intakes and effluent outflows, and boat access are constructed. Increased access to waterbodies can increase mortality due to angling and could imperil local fish populations (Pauly et al . 2001; Chu et al . 2003). It was found that the stresses associated with urban development and agriculture are among the key threats to fish biodiversity in Canada (Chu et al . 2003). The construction of roads and homes physically altered aquatic habitat, and modification of shoreline vegetation can also lead to increases in sedimentation as well as reduction in structure in littoral zones (Christensen et al . 1996; Jennings et al . 1996). Without suitable structural complexity in the littoral zone, many species of centrarchids may suffer reduced efficiency of foraging and reduced growth (Aggus and Elliot 1975; Prince et al . 1975). Due to the fact that centrarchid fishes associate with specific habitats in the littoral zone, changes in species abundance may also occur with the alteration of habitat (Hinch et al . 1991). Centrarchid species are also particularly at risk due to their need for very specific spawning habitats in the littoral zone, which could be altered by shoreline development (Kramer and Smith 1962; Neves 1975; Bozek et al . 2002). Ultimately, these changes could alter fish assemblages in affected areas (Jennings et al . 1996, 1999). Water quality can be degraded by waste water discharge, storm runoff, and agricultural runoff containing pesticides and fertilizers (Chu et al . 2003). This can in turn lead to increased nutrient loading and increases in eutrophication (Carpenter et al . 1998; Garrison and Wakeman 2000; Moore et al . 2003). Eutrophication leads to increases in aquatic vegetation, which can then decrease local water quality, forcing centrarchid fishes to avoid these areas (Miranda and Hodges 2000; Miranda et al . 2000). Also, in areas of dense aquatic vegetation, piscivorous centrarchid fishes have increased difficulty foraging, and may exhibit lowered growth rates (Crowder and Cooper 1979; Savino and Stein 1982; Valley and Bremigan 2002). Unfortunately, with the human population and its need for freshwater ever growing, many waterbodies will be subjected to habitat alteration and degradation for many years to come. Management of shoreline areas should seek to minimize the impacts of shoreline development as well as maintaining water quality and avoiding eutrophication. If possible, areas of degraded habitat can be restored. In recent years, strong efforts to restore streams have been undertaken on local to regional scales. Common practices include the removal of trash and excess sediment, reduction of pollution inputs, restoration of riparian habitat, and construction of complex habitat within the waterway itself (Prince et al . 1975; Roni et al . 2002). Similar habitat management practices have been applied to lakes. Reservoir managers have begun to introduce native aquatic vegetation to reservoirs to increase the amount of suitable habitat (Smart et al . 1996). It has also been long noted that the construction of artificial reefs provides valuable habitat for both adult and juvenile centrarchids throughout their lifetimes (Prince et al . 1975). In Florida, fisheries managers have utilized habitat restoration techniques such as reducing the densities of macrophytes due to eutrophication and removal sediment to increase the abundance of multiple centrarchid species (Moyer et al . 1995; Allen and Tugend 2002). Unfortunately, the effectiveness of these techniques was short-lived in at least one instance (Moyer et al . 1995).

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12.4.4 Altered flow regimes and barriers To supply society’s ever-growing demand for water and electricity, rivers throughout North America have been dammed to provide water supplies in the form of reservoirs and hydro electrical power. The construction of a dam drastically alters the habitat and flow dynamics in the nearby area in manners that often threaten riverine fish species. Most often research on the effects of dams is conducted on migratory fishes (mainly salmonids), though examples from research conducted on noncentrarchid fishes can be used to highlight some of the threats associated with the unstable hydrology around dams. Adult individuals can often become entrained in areas affected by water withdrawal systems (Webb 1998; Johnson et al . 2004). These water withdrawal systems may ultimately lead to mortality as fish are passed through turbines or other machinery. Dams are also an impediment to migratory movements of fishes. Though not often thought of as migratory fishes, some species of centrarchids may move great distances in riverine environments to find suitable habitat for spawning or overwintering (Bunt et al . 2001). Dams can be a physical barrier that prohibits such movements, forcing fish to utilize suboptimal habitats (Bunt et al . 2001). The reservoirs created via damming drastically alter the habitat of a riverine system. Impoundments more closely resemble small, eutrophic lakes than reaches of a river, and may often suffer from increased sedimentation and decreased water quality (Ney 1996). These reservoirs are generally not suitable habitat for riverine species, though many species of lacustrine centrarchids find impoundments quite habitable (Buynak et al . 1989; Martinez et al . 1994; Sammons and Bettoli 1999; Long and Fisher 2005; Quist et al . 2005). As such, the biodiversity of a dammed site may decline as native riverine species become locally extirpated (Cross and Moss 1987; Petersen and Paukert 2005). To mitigate the ecological harm associated with dams, fishways, or channels that allow fish movement around a dam, are often included in dam construction to allow for unimpeded fish movements. Fishways have been found to allow multiple centrarchid fishes to successfully navigate around dams (Bunt et al . 1999, 2001). Fishway passage efficiency can be optimized by controlling the velocity of water through the passageway to allow for ease of movement of migrating species (Bunt et al . 1999). To enhance fishway attraction, entrances to the fishway can be modified, and the fishway entrance can be placed near the dam in areas where the fish are attracted by water discharge (Bunt 2001). These modifications have been noted to increase the attraction of fishways to pumpkinseeds (Bunt 2001). In recent years, the topic of dam removal has become heavily debated as a management tool for stream restoration (Hart and Poff 2002). Multiple jurisdictions have initiated dam removal projects targeting structures that are aging and no longer in practical use (Born et al . 1998; Stanley and Doyle 2003). In general, the removal of a dam restores a stream to its original hydrologic regime, which allows for increased habitat for native riverine species (Weathers and Bain 1992; Bednarek 2001; Koppelman and Garrett 2002). Riparian vegetation and macroinvertebrate communities often return to pre-dam conditions. After a dam is removed, sediment that was previously trapped in impoundments is typically mobilized resulting in changes to a harder, coarser substrate in the affected reaches of the river (Bednarek 2001; Wildman and MacBroom 2005). The increased mobility of sediment can also lead to nutrient leaching, and possible eutrophication, downstream of dam removal sites (Ahearn and Dahlgren 2005). Dam removal can be a very powerful tool for stream restoration, but also poses unique threats to the riverine environment, and as such, should be thoroughly researched and considered before being put into practice (Stanley and Doyle 2003). Closely related to the construction of dams throughout North America, many jurisdictions have begun to regulate flow levels in lakes and rivers to maintain minimum water levels and avoid undue ecological harm (Travnichek et al . 1995; Bowen et al . 1998). Particularly in lentic environments, abrupt changes in flow levels have been noted to have multiple deleterious effects on centrarchid species, mainly in year class strength and formation. In lentic environments, juvenile fish are extremely susceptible to displacement as a result of increased flows due to flooding during the reproductive period (Harvey 1987). Other studies have found that flooding during the reproductive period can negatively impact recruitment of smallmouth bass by the combined effects of decreased dissolved oxygen, increased turbidity, and juvenile displacement and subsequent mortality (Larimore 1975; Filipek et al . 1991; Mason et al . 1991; Sallee et al . 1991; Swenson et al . 2002). Post spawning, increased flow can also decrease the growth rate of juvenile fish. Conversely, some centrarchid species, such as the Lepomis spp., may be positively affected by flood events prior to the reproductive period. In general, fish production in many large riverine environments is positively correlated with access to floodplain habitats during flooding events (Junk et al . 1989). Flooding prior to the reproductive period connects many riverine environments with floodplain habitats, and can thereby increase food availability and, subsequently fecundity, in Lepomis spp. (Springate et al . 1985; Crim and Glebe 1990; Neckles et al . 1990).

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Low water levels can also have negative impacts on lotic dwelling centrarchid species. Low water levels can reduce the amount of suitable habitat that adult individuals can inhabit as well as hamper movements and ability to forage (Lohr and Fausch 1997). Drought can also be quite detrimental to recruitment of centrarchid fishes. Multiple studies have found that high spring water levels are positively correlated with year class strength in largemouth bass (Meals and Miranda 1991; Bonvechio and Allen 2005). If water levels decrease during the reproductive period, spawning will often stop until water levels begin to rise again (Ozen and Noble 2002). Many previous studies have surmised that the benefits of high spring water levels include increases in the amount of suitable nesting habitat and food availability, as well as potential decreases in predation levels (Keith 1975; Aggus and Elliot 1975; Shirley and Andrews 1977; Aggus 1979; Timmons et al . 1980; Miranda et al . 1984; Ploskey 1986; Meals and Miranda 1991). Also, generally, high water levels during the spawning season are positively correlated with strong year classes among centrarchid species residing in reservoirs (Raibley et al . 1997; Sammons et al . 1999, 2002; Sammons and Bettoli 2000). Keaton et al . (2005) found that population levels of centrarchid fishes doubled in years following severe drought in South Carolina streams, presumably due to increased water levels and habitat availability. Lastly, extremely low water levels can induce mortality of adult individuals directly (Lohr and Fausch 1997). Low water levels can also have positive effects on centrarchid fishes. Food items may become concentrated in small spatial areas, thereby increasing the effectiveness of foraging (Jenkins 1970; Aggus 1979). As a result, adult individuals may exhibit increased growth rates, increased condition at the time of spawning, and increased fecundity (Aggus 1979; Liston and Chubb 1985; Crim and Glebe 1990). Clearly, the topic of managing water levels to promote recruitment among centrarchid fishes is quite complicated at best. If possible, a flooding event prior to spawning may increase overall condition and ability to spawn of adult individuals, possibly leading to increases in subsequent year class strength. Extreme flood pulses should be avoided during the reproductive period to negate the deleterious effects of high flow rates on juvenile and fry centrarchid fishes. In the southerly latitudes, increasing water levels in reservoirs or lakes could be used to stimulate centrarchid spawning (Ozen and Noble 2002). When managing to control the spread of centrarchid fishes, flood pulses during the reproductive period or extremely high flows could be used to control centrarchid population levels and allow for increases in native fish populations (Bernardo et al . 2003).

12.4.5 Climate change As global climate change occurs due to concentrations of trace gases, primarily CO2 , in the atmosphere, global air temperatures should increase in temperate latitudes (Hansen et al . 1981). It is also predicted that water temperatures throughout these latitudes will increase (Stefan et al . 1998). Increases in environmental temperature can have a multitude of effects on fish as water temperature is the acknowledged “master factor” regulating fish metabolism, physiology and, often times, behavior (Brett 1971). As such, multiple effects of climate change on centrarchid fishes have been predicted. There is a well-established, positive correlation between summer air temperature and year class strength that has been repeatedly noted for smallmouth bass (Doan 1940; Watt 1959). As such, studies have predicted that increases in global temperature would increase year class strength of smallmouth bass (Casselman et al . 2002). Indeed, Suski and Ridgway (2007) showed that climatic factors responsible for increases in global temperature correlate positively with nesting success for smallmouth bass, suggesting that future climate change could result in increased smallmouth bass year class formation across the northern tier of the species. Growth rates of centrarchid fishes are predicted to increase as global warming occurs (Shuter 1990; McCauley and Kilgour 1990; King et al . 1999). This increase in growth rates would be most dramatic in northern latitudes, as global warming would shorten the duration of winter, thereby lessening the effects of annual winter starvation on populations (Shuter 1990; Shuter and Post 1990; King et al . 1999). Water temperatures have been cited as regulating the distribution of warmwater fishes such as centrarchids. As air temperatures increase with climate change, the thermal habitat of most northern waterbodies would become suitable for warmwater fish habitation (Magnusson et al . 1990; DeStasio et al . 1996). There is also the possibility that populations of centrarchid fishes would be able to expand their distributions farther north. It has been theorized that the northern limit of centrarchid distributions are regulated by the fact that during winter months, foraging is restricted and starvation occurs (Shuter and Post 1990). As climate change warms North America, the duration of winter would decrease and starvation would not occur as often in northern waterbodies (Shuter and Post 1990). This would then allow centrarchid

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populations to expand northward (MacCauley and Kilgour 1990; Shuter and Post 1990; Minns and Moore 1992). As centrarchid distributions shifted farther north, local fish communities could suffer from shifts in community structure associated with the introduction of centrarchid fishes (Jackson 2002). An in-depth discussion of the effects of introduced centrarchids is presented later in this chapter.

12.5 Stocking—mixing of populations and outbreeding For more information on the introduction of centrarchids into new areas, please see the section on introduced centrarchids in this chapter. Because multiple centrarchid species, primarily the black basses, are highly prized as gamefish, many governmental agencies have either historically conducted or currently conduct stocking initiatives (Noble 2002; Isermann et al . 2002). Where centrachid populations have already become established, stocking has occurred to enhance local population numbers or sizes in order to enhance recreational fisheries (Philipp et al . 2002). To this end, individuals selected for quick growth and larger size have been stocked into populations throughout North America (Philipp et al . 2002). These stocking efforts generally end up mixing genetically distinct stocks from throughout North America (Philipp et al . 2002). In fact, in the upper Midwest of the United States, evidence has emerged that points to the existence of close to 60 separate stocks of largemouth bass, each genetically distinct from the others (Fields et al . 1997). In an extreme case, stocking has led to the translocation of Florida largemouth bass into areas inhabited by populations of northern largemouth bass throughout North America (Philipp and Claussen 1994). Previously, the two species were mistaken as being a single species due to morphological similarity and the fact that they readily hybridize (Kassler et al . 2002). Since the classification of Florida largemouth bass as a separate species (Kassler et al . 2002), stocking of this species can be considered an introduction of an exotic species (Philipp et al . 2002). Stocking in this manner, whether it concerns different stocks within a species or the hybridization of distinct species, can lead to a host of negative effects that may prove to be counter productive to enhancing local fisheries. The main concern that arises from mixing populations via stocking is that the fitness of the resulting population will be reduced through outbreeding depression (Philipp et al . 2002). Philipp et al . (2002) showed two negative consequences of outbreeding depression in a “common garden” experiment involving northern largemouth bass and Florida largemouth bass. When individuals from other geographic locales were introduced to Illinois ponds, the nonnative stocks showed reduced survival, growth, and reproductive success (Philipp et al . 2002). Also, when the stocks were allowed to mix, hybrid populations showed reduced reproductive fitness (Philipp et al . 2002). These losses in fitness are generally deemed to be related to loss of adaptation to local conditions that occurs through the mixing of two nonrelated genomes (Philipp et al . 1985; Fields et al . 1987). Functionally, coadapted gene complexes tailored to the local environment are disrupted in hybrid individuals, thereby leading to the reduced fitness known as outbreeding depression (Templeton 1986; Philipp et al . 2002). Goldberg et al . (2005) also noted that hybrid largemouth bass resulting from outbreeding are more susceptible to the largemouth bass virus (LMBV) and exhibited higher levels of mortality than did wild type bass (see the section on parasites and diseases in this chapter). These effects were attributed to the disruption of coadapted gene complexes in the immune system (Goldberg et al . 2005). Clearly, outbreeding depression as a result of stocking is quite counterproductive to the objective of improving fisheries, and other options need to be considered. The most simplistic solution to avoid the negative effects of outbreeding depression is to stop stocking programs that introduce stocks from geographically disparate areas. Philipp et al . (2002) echoed earlier calls by Childers (1975) to discontinue the practice of mixing stocks from geographically distinct areas as well as enacting measures to protect selected populations of fish from being genetically “mixed” with disparate populations. If stocking programs are to be continued, they should be practiced responsibly. Stocks should only be mixed within the same or adjacent conservation management units (Cooke et al . 2001a). Perhaps the focus of management efforts should shift to a view based upon the conservation genetics perspective of conserving the genetic diversity both within and among populations (Philipp et al . 2002).

12.6 Parasites and diseases Centrarchid fishes are host to a variety of parasites and diseases that infect many tissues in the body. Disease and parasitic infections have been characterized for the epidermis (Francis-Floyd et al . 1993; Hawke et al . 2003; Do Huh

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et al . 2005), mouth (Noga et al . 1990), eyes (Marcogliese and Compagna 1999), gills (Muzzall et al . 1995), and various internal organs in the body cavity (Leino 1996; Muzzall and Peebles 1998; Aloo 1999; Petrie-Hanson 2001; Pasnik et al . 2005). These infections may have many deleterious effects including physical harm such as lesions (Noga et al . 1990; Hawke et al . 2003), increased mucus production (Do Huh et al . 2005), wounded organs (Aloo 1999), and, possibly, death (Petrie-Hanson 2001). Infected individuals that survive may also be subjected to retarded growth, altered behavior (Plumb et al . 1996; Woodland et al . 2002), increased stress, and increased susceptibility to other diseases (Noga et al . 1990). Generally, parasite and disease infection and prevalence fluctuates with factors such as season, host behavior, and host habitat selection (Olson and Nickol 1996; Wilson et al . 1996; Landry and Kelso 1999; Banks and Ashley 2000; Fellis and Esch 2004). The latest and most publicized threat to centrarchid fisheries is the emergence of LMBV. In 1995, a fish kill of ∼1000 adult largemouth bass occurred in Santee Cooper Reservoir, South Carolina, and was eventually attributed to a new pathogen, LMBV (Plumb et al . 1996). Since the initial discovery, LMBV has been documented in 17 states of the United States, and is primarily responsible for fish kills in the southeastern United States (Goldberg 2002). It is thought that the virus is spread both from direct transmission between individuals and through the ingestion of infected prey items (Plumb and Zilberg 1999; Goldberg 2002; Woodland et al . 2002; Grant et al . 2005; Inendino et al . 2005) . Fish kills connected to LMBV primarily occur during summer months, and may be caused by high water temperatures, low dissolved oxygen levels, decreased water quality, and increased stress due to angling (Grizzle and Brunner 2003; Inendino et al . 2005). Although the virus has been thought to cause fish kills in largemouth bass, it has been detected among healthy populations of largemouth bass as well as other centrarchid species (Goldberg 2002). Due to the fact that the disease seems to be widespread and lingering within wild populations, LMBV has become a topic of much research and heated debate on its possible impact on warmwater fisheries (Goldberg 2002). The debate on the threat of LMBV focuses on the variability of the population-level effects of the disease. Currently, many infected populations survive without suffering from fish kills or any visible effects (Goldberg 2002; Grizzle and Brunner 2003). Also, in populations where fish kills have occurred, population numbers have rebounded and no subsequent fish kills have been reported (Goldberg 2002). Combined with the current lack of knowledge on the mechanisms that lead to LMBV-derived mortality, the threat that the disease poses is currently unknown. Due to the fact that centrarchids are popular and valuable gamefish, interest into the emergence and effects of diseases has increased. A growing body of literature indicates that anthropogenic disturbances have caused the perceived increase in the emergence and spread of wildlife diseases (Dobson and Foufopoulos 2001; Daszak et al . 2001). Humans aid in the spread of wildlife disease through the introduction of nonnative species (complete with their nonnative parasites and diseases) to new areas as well as mixing infected individuals or populations of endemic species with healthy individuals or populations (Grant et al . 2005). Also, anthropogenic disturbances coupled with infection by either parasites or disease can lead to increased mortality among populations. Outbred largemouth bass populations, which could arise in the wild as a product of stocking, have been shown to be more susceptible to infection by LMBV (Goldberg et al . 2005). These signs indicate the possibility that anthropogenic disturbance is a significant factor affecting the emergence and spread of wildlife disease. If this is indeed the case, conservation groups and fisheries managers should expect to face a growing number of parasitic and disease threats to warmwater fisheries in the coming years.

12.7 Exotic centrarchids as threats to conservation Outside of their endemic range, centrarchid fishes have been successfully introduced to many water bodies worldwide, establishing viably reproducing populations (Chapter 11). In particular, largemouth bass have been introduced to at least 50 countries worldwide (Robbins and MacCrimmon 1974), and, as of 1999, have been named one of the one hundred worst invasive species in the world (ISSG 1999). While these introductions may have many perceived beneficial side effects, mostly revolving around increased recreational angling opportunities, endemic fishes and ecosystems often suffer deleterious effects due to predation and competition with centrarchids (Cambray 2003). Presented here is a brief overview of the effects of centrarchid fishes as exotic species in multiple geographic locales worldwide. Large, piscivorous centrarchid fishes, mainly the Micropterus spp., pose a threat to endemic fish populations through direct predation that can change food webs in lakes and rivers (Zaret and Paine 1973; Whittier and Kincaid 1999). Within their native ranges, the direct effects of black bass predation have been observed repeatedly (Tonn and Magnusson 1982;

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Power et al . 1985; Harvey et al . 1988; Jackson et al . 2001; Jackson 2002). In North America, predation by largemouth bass and smallmouth bass on ocean-migrating salmonid smolts may lower population numbers as well as later numbers of adults returning to spawn (Tabor et al . 1993; Fayram and Sibley 2000; Bonar et al . 2005). In the lower reaches of the Fraser River in British Columbia where centrarchid introductions appear to be very recent, populations of largemouth bass are expanding rapidly and represent one of the biggest threats to salmon restoration and conservation (Scott Hinch, University of British Columbia, Unpublished Data). Introduced centrarchid fishes are, therefore, seen as a major threat to already threatened and endangered salmonid stocks. Local extirpation of pupfish species in Mexico [e.g., San Cristobal pupfish (Profundulus hildebrandi ); Velazquez-Velazquez and Schmitter’Soto 2004] have been linked to predation by introduced largemouth bass. Introduced centrarchids have also been noted as a primary threat to endangered native fishes in Portugal (Collares Pereira et al . 2000). Introduced largemouth bass have been shown to predate heavily upon native fish species in Japan (Nakai 1999). In a study of the impacts of a single smallmouth bass population in South Africa, researchers determined that native cichlids comprised 80% of the diet of the bass (Vlok and Engelbrecht 2003), and recent local extinctions of small cyprinid minnows (Barbus spp.) are directly linked to predation by largemouth bass (Cambray and Stuart 1985). Additionally, smaller centrarchid species may prey upon the eggs and spawn of native fish species, although direct evidence is often difficult to obtain due to the fact that eggs are easily and quickly digested (Bain and Helfrich 1983). In a recent icthyofauna survey in South Korea, largemouth bass were found to inhabit 93% of sites surveyed (Jang et al . 2002). Analysis of the stomach contents of largemouth bass caught in the Nakdong River system, South Korea, revealed that 60% of the diet of bass was composed of native cyprinids (Cho 2003). Clearly, direct predation by large, piscivorous centrarchids poses a severe threat to endemic species. Centrarchid fishes often directly compete with native fishes for prey items. Diet overlaps between large centrarchids and native top predators have been noted in multiple countries. The diets of largemouth bass and native pike (Esox lucius) have been noted in Italy (Lorenzoni et al . 2002). As the range of smallmouth bass has expanded farther north in Canada, direct predation on minnow species by bass have forced native lake trout to shift to a lower quality diet based on invertebrates (Vander Zanden et al . 2004). Smaller centrarchids have also been noted to compete with endemic fishes for food resources. In Belgium, pumpkinseed (L. gibbosus) compete with both gudgeon (Gobio gobio) and roach (Rutilus rutilus; Declerck et al . 2002). Competition between invasive bluegill (L. macrochirus) and native Sacramento perch (Archoplites interruptus) result in reduced growth for Sacramento perch when food is limited, mainly as a result of aggressive dominance by bluegill (Marchetti 1999). Ultimately, large-scale changes in fish communities as a result of the predation and diet overlap situations, mentioned earlier, in the wake of centrarchid introduction have been noted worldwide. Primarily, as centrarchid fishes are introduced into an area, species composition changes occur, often with a reduction in diversity (Chapleau et al . 1997; Whittier et al . 1997). In general, the introduction of large, piscivorous centrarchid species such as black bass lead to a decrease in the abundance of small Cyprinid species (Jackson 2002). In multiple river systems in western Europe, such as the Tagus river in Spain (Elvira et al . 1998; Elvira and Almodovar 2001), and the Guadiana (Bernardo et al . 2003) and the Raia rivers in Portugal (Godinho and Ferreira 2000), introduced centrarchid fishes, especially largemouth bass and pumpkinseed, have become some the most common fish species present in these rivers. In the worst of circumstances, native fish populations often decline or become locally extirpated (Ross 1991; Moyle and Light 1996; Fausch 1998). If native fishes do not die out, populations may shift habitat preferences (Brabrand and Faafeng 1993). The introduction of centrarchid fishes has also been linked to the decline or extirpation of multiple endemic fish species in various states throughout the United States (Robertson and Winemiller 1998; Eby et al . 2003; Schade and Bonar 2005). In light of these findings, extreme caution must be exercised when introducing centrarchid fishes to new areas to maintain local diversity and prevent the extirpation of endemic species. Although it is sometimes possible to reverse an undesirable introduction of centrarchids (Iguchi et al . 2004), most times the introduction is irreversible. In North America, the “stocking” mentality has seen centrarchids, particularly smallmouth bass, largemouth bass, and Florida bass, stocked in almost all waters within a region. Even in cases where these species are endemic, there is a need to maintain a diversity of fish communities, not only those where large centrarchids dominate. In some parts of North America, centrarchids have been introduced into historically fishless ponds, and had devastating consequences for imperiled amphibians. At times there is conflict between fisheries management and conservation where management is focused on generating more and better angling opportunities whereas conservation is focused on maintaining biodiversity. Indeed, at times fisheries managers and well-intentioned anglers focused on expanding bass populations are actually themselves not operating under the guise of conservation, and instead are actually a threat to aquatic biodiversity.

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12.8 Global conservation status of centrarchids Globally, few centrarchid fishes are currently listed by the International Union for the Conservation of Nature (IUCN) Red List as being globally threatened. The exceptions include the Roanoke bass (Ambloplites cavifrons), Suwannee bass (Micropterus notius), and Guadalupe bass (Micropterus treculi ) (Gimenez 1996). It is important to note that a number of centrarchids are considered threatened in the context of regional (e.g., state, provincial) or national (e.g., US Endangered Species Act, Canadian Species at Risk Act) threat assessments as summarized in Chapter 13. Here, we briefly summarize the three species that are currently on the IUCN Red List and thus presumably the species that are most imperiled. It is important to note that for many of the centrarchid species, there is simply insufficient knowledge of their distribution, natural history, and population biology to make informed decisions regarding their status so it is possible that more centrarchids are threatened than what would appear in various threat assessment documents.

12.8.1 Roanoke bass The Roanoke bass has been classified by the IUCN (based on ver. 2.3; 1994) as Vulnerable (VU D2). A taxon is considered vulnerable when it is facing a high risk of extinction in the wild in the medium-term future. Specifically, Roanoke bass were classified because their population was regarded as exhibiting an acute restriction in their area of occupancy (typically less than 100 km2 ) or in the number of locations (typically less than five). Such a taxon would thus be prone to the effects of human activities (or stochastic events whose impact is increased by human activities) within a very short period of time in an unforeseeable future, and is thus capable of becoming Critically Endangered or even Extinct in a very short period. Indeed, the Roanoke bass has been extirpated from portions of its former range and many populations appear to be persisting in marginal habitats (Petrimoulx 1983; Jenkins and Burkhead 1994). Specific threats facing populations of Roanoke bass include interactions with introduced rock bass, habitat degradation, and impoundments (Cashner and Jenkins 1982; Jenkins and Burkhead 1994; See Chapter 13 for additional details).

12.8.2 Suwannee bass The Suwannee bass has been classified by the IUCN (based on ver. 2.3; 1994) as Lower Risk (LR-nt). A taxon is LR when it has been evaluated and does not satisfy the criteria for any of the categories—Critically Endangered, Endangered, or Vulnerable. Suwannee bass were considered to be “Near Threatened” indicating that they do not qualify for Conservation Dependent, but are close to qualifying for Vulnerable. The Suwannee bass has a restricted range (Warren et al . 2000; Koppelman and Garrett 2002) although populations do not seem to be in decline. In fact, there is some evidence that the present range includes more river systems than were known historically (see Chapter 13 for details).

12.8.3 Guadalupe bass The Guadalupe bass has been classified by the IUCN (based on ver. 2.3; 1994) as Data Deficient (DD). This classification is used when there is inadequate information to make a direct, or indirect, assessment of its risk of extinction based on its distribution and/or population status. A taxon in this category may be well studied, and its biology well known, but appropriate data on abundance and/or distribution is lacking. Data Deficient is therefore not a category of threat or LR. Listing of taxa in this category indicates that more information is required and acknowledges the possibility that future research will show that threatened classification is appropriate. There is evidence that the species has declined dramatically in recent history because of decreased stream flow, reservoir construction, habitat degradation, and extensive, introgressive hybridization with nonnative smallmouth bass (summarized in Koppelman and Garrett 2002; see Chapter 13).

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12.9 Conclusion The purpose of this chapter was to provide a detailed overview of the conservation and management issues associated with centrarchid fishes. A consistent message that we promoted throughout the chapter was that knowledge of basic centrarchid biology can aid in the conservation and management of centrarchid fishes. By summarizing the various threats that are faced by centrarchid fishes (e.g., pollution, exploitation, introduced species), it became apparent that this group is not unlike many other freshwater fish in North America. In some respects, centrarchids experience more extensive threats due to their popularity within the angling community (e.g., relative to other nongame fishes such as catostomids; Cooke et al . 2005b). However, what may be viewed as a threat is also one of the most powerful forces for ensuring that aquatic resources are protected—the angling community. One of the most important tasks will be to educate anglers on the importance of all centrarchids (and indeed all freshwater fish), not simply those that are targeted by anglers. By no means are we advocating the development of recreational fisheries for some of the rarer centrarchid species. Instead, we are advocating for a greater recognition of all centrarchids and freshwater fish diversity more generally. Such an approach is consistent with the notion of ecosystem-based management. However, as noted earlier, rarely are centrarchids managed in the context of an ecosystem. Instead, species that are actively managed tend to be those that are of recreational value and the management strategies tend to be focused on single species (e.g., largemouth bass) or congeners (lepomids, black bass, crappies). Centrarchids contribute important ecological services including serving as hosts for the glochidia of unionid mussels, provide important food for piscivorous fishes and birds, and restructure substrate through their spawning activities (see Holmlund and Hammer 1999). Perhaps educating the public about the valuable role of centrarchids within freshwater communities will help to conserve them as well as the entire ecosystems. We hope that this book and this chapter will contribute to that vision. More globally, we also considered the role of centrarchids as introduced species. Despite being a book focused on a specific family of fishes, we want to be clear that in no way do we advocate the introduction of centrarchids outside of their endemic range. Perhaps greater knowledge (such as provided in a synthesis such as this book) will enable managers and conservation scientists to better understand the potential consequences of the introduction of centrarchids and equip them with knowledge to develop appropriate mitigation/biocontrol strategies. We also caution the movement and stocking of fish within their endemic range without consideration of local adaptation (and the potential for outbreeding depression).

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Waters, T. F. 1995. Sediment in Streams: Sources, Biological Effects and Control. American Fisheries Society, Monograph 7. Bethesda, MD. Watt, K. E. F. 1959. Studies on population productivity. II. Factors governing productivity in a population of smallmouth bass. Ecological Monographs 29: 367–392. Weathers, K. C. and M. B. Bain. 1992. Smallmouth bass in the Shoals Reach of the Tennessee River: population characteristics and sport fishery. North American Journal of Fisheries Management 12: 528–537. Webb, P. W. 1998. Entrainment by river chub nocomis micropogon and smallmouth bass Micropterus dolomieu on cylinders. Journal of Experimental Biology. 201: 2403–2412. Whittier, T. R. and T. M. Kincaid. 1999. Introduced fish in Northeastern USA lakes: regional extent, dominance, and effect in native species richness. Transactions of the American Fisheries Society 128: 769–783. Whittier, T. R., D. B. Halliwell, and S. G. Paulsen. 1997. Cyprinid distributions in Northeast U.S.A. lakes: evidence of regional-scale minnow biodiversity losses. Canadian Journal of Fisheries and Aquatic Sciences 54: 1593–1607. Wilde, G. R. 1997. Largemouth bass fishery responses to length limits. Fisheries 22(6): 14–23. Wilde G. R. 1998. Tournament-associated mortality in black bass. Fisheries 23(10): 12–22. Wilde, G. R. 2003. Dispersal of tournament-caught black bass. Fisheries 28(7): 10–17. Wilde, G. R. and L. J. Paulson. 2003. Movement and dispersal of tournament-caught largemouth bass in Lake Mean, Arizona-Nevada. Journal of Freshwater Ecology 18: 339–342. Wildman, L. A. S. and J. G. MacBroom. 2005. The evolution of gravel bed channels after dam removal: case study of the Anaconda and Union City Dam removals. Geomorphology 71: 245–262. Wilson, D. S., P. M. Muzzall, and T. J. Ehlinger. 1996. Parasites, morphology, and habitat use in a bluegill sunfish (Lepomis macrochirus) population. Copeia 2: 348–354. Woodland, J. E., C. J. Brunner, A. D. Noyes, and J. M. Grizzle. 2002. Experimental oral transmission of largemouth bass virus. Journal of Fish Diseases 25: 669–672. Zaret, T. M. and R. T. Paine. 1973. Species introduction in a tropical lake. Science 182: 449–455.

Chapter 13

Centrarchid identification and natural history M. L. Warren, Jr.

13.1 Introduction The family Centrarchidae (Order: Perciformes) is one of the most diverse, widespread, and conspicuous fish families native to freshwater habitats of North America. Among endemic fish families of North America, only the North American catfish family (Ictaluridae) has more species. The family name, Centrarchidae, refers to the anal fin spines of species in the family, and the common name, sunfishes, to the bright breeding colors displayed by males of some species in the family. Because of their diversity, wide distribution, and economic value, some of the earliest taxonomic descriptions and natural history observations on North American freshwater fishes focused on the centrarchids (e.g., Linnaeus 1758; Lac´ep`ede 1801; Rafinesque 1820; Abbott 1870). The family contains 34 extant species classified in eight genera, but morphological and genetic evidence suggests that additional, but currently unrecognized, diversity exists within most of the genera. The most diverse genus, Lepomis, the bream (or panfish) of anglers, is comprised of 13 extant species, but at least 8 of these show evidence of polytypy (e.g., Bermingham and Avise 1986; Fox 1997; Harris 2005). The genus Micropterus, referred to collectively as black basses (Philipp and Ridgway 2002), contains eight extant species, but again, at least three species are polytypic (e.g., Stark and Echelle 1998; Kassler 2002; Miller 2005). The genera Ambloplites (rock basses), Enneacanthus (banded sunfishes), and Pomoxis (crappies) contain four, three, and two extant species, respectively, and at least one species each of Ambloplites and Enneacanthus is polytypic (Koppelman 2000; T. Darden, South Carolina Department of Natural Resources, personal communication). The genera Acantharchus, Archoplites, and Centrarchus are monotypic, but populations of both Acantharchus pomotis and Archoplites interruptus show geographical patterns of morphological divergence (Cashner et al . 1989; Moyle 2002). The natural range of extant centrarchids is confined primarily to warm, freshwater habitats in North America east of the western continental divide except for the Sacramento perch (A. interruptus), whose native range is west of the divide in the Central Valley of California (San Joaquin-Sacramento, Pajaro, Salinas river drainages, Moyle 2002). The northern natural continental limit of the family is occupied by members of Lepomis, Ambloplites, Pomoxis, and Micropterus in the St. Lawrence River, northern Great Lakes, and southwestern Hudson Bay drainages in eastern Canada (Scott and Crossman 1973). The Rio Conchos (Rio Grande drainage) (Lepomis) and Rio Soto la Marina (Micropterus, Miller and Smith 1986; Miller 2005) of northern Mexico delimit the southern continental limits of the native range of extant centrarchids. The Mississippi River Basin and, to a lesser extent, the Gulf and Atlantic Slope drainages harbor the most diverse assemblages of native centrarchids (Warren et al . 2000). The native ranges of Pomoxis and Lepomis largely coincide with that of Micropterus, but both extend farther northwest into the northern plains drainages, and the native range of Lepomis extends farther northeast into southern New Brunswick (Scott and Crossman 1973). Members of Acantharchus and Enneacanthus are confined to drainages of the Atlantic Coastal Plain, peninsular Florida, and eastern Gulf Coastal Plain (Page and Burr 1991). The native range of Centrarchus overlaps Acantharchus and Enneacanthus but extends into drainages of the western Gulf Coastal Plain of eastern Texas and north to southern Illinois and Indiana in the lower Mississippi River Basin. Centrarchids, particularly the genera Ambloplites, Lepomis, Micropterus, and Pomoxis are among the most widely introduced groups of fishes in the world. Nonnative populations are established across much of temperate North America and intercontinentally (e.g., South America, Europe, Africa, Asia, Oceania) and are often associated with adverse ecological consequences for the native fauna (e.g., Robbins and MacCrimmon 1974; De Moor and Bruton 1988; FAO 1998; Fuller et al . 1999; Rahel 2000; Jackson 2002; Jang et al . 2002; Moyle 2002). 375

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The most distinctive characteristic of centrarchids is their reproductive behavior. Males in the family construct and defend a well-defined, depressional, oval- to circular-shaped nest. Downward-directed thrusts of the caudal fin are a primary and conspicuous nest-building activity in most centrarchids (caudal sweeping, Miller 1963), but a variety of other actions may also be used as the male clears the nesting area (e.g., sweeping of the pectoral fins, pushing stones, or transporting debris by mouth) (Dickson 1949; Hunter 1963; Miller 1963; Gross and Nowell 1980; Noltie and Keenleyside 1987b). Centrarchids may nest solitarily or colonially. Solitary nesters (nests >1 m apart) tend to nest near simple cover (e.g., bases of logs, rocks, or macrophytes) and defend a territory exceeding the nest perimeter (>2.5 m, Colgan and Ealey 1973; Avila 1976; Winemiller and Taylor 1982; Colgan and Brown 1988; Ridgway 1988; Jennings and Philipp 1992b; Scott 1996). Colonies of nests, consisting of several to hundreds of abutting nests, tend to occur in shallow open water, and in dense colonies nest defense is constrained primarily to the nest perimeter (Hunter 1963; Colgan et al . 1981; Gross and MacMillan 1981; Gross 1982). Spawning can occur immediately after nest construction or be delayed for several days, during which the male defends the nest and surrounding territory and waits for spawning-ready females (Carr 1946; Kramer and Smith 1962; Boyer and Vogele 1971; Miller and Kramer 1971; Avila 1976; Vogele 1975a; Colgan and Gross 1977; Gross and Nowell 1980; Cooke et al . 2001b). Male aggression intensifies during the courtship and spawning period. Males over nests display to nearby or approaching males and females using combinations of many behaviors (e.g., caudal sweeping, nest hovering, fin spreading, mouth gapes, jaw snaps, lateral displays, substrate biting, and opercular spreads). Male to male aggressive interactions, including combat, are not uncommon, particularly among colonial-nesting species. Males most frequently rush toward an interloper with a quick retreat to the nest (thrust, Miller 1963), but if the intruder does not retreat, males laterally display, spread opercles, or actually ram, push, bite, or jaw grasp the other male. Much of male aggression is directed at or near the head and opercular area, but frayed fins and body abrasions of males attest to the vigorousness of male aggression in defense of the nesting territory (Hunter 1963; Keenleyside 1967, 1971; Colgan and Gross 1977; Gross and Nowell 1980). Male courtship of females may be preceded by attempts to repulse females near the nest, behaviors that coax or guide the female to the nest, or both. Repeated repulsion of approaching females by males is documented in Archoplites (Mathews 1965), Ambloplites (Gross and Nowell 1980; Petrimoulx 1984; Noltie and Keenleyside 1987b), Lepomis (e.g., Hunter 1963; Huck and Gunning 1967; Keenleyside 1967; Ballantyne and Colgan 1978a,b,c), and Pomoxis (Siefert 1968). If ready to spawn, a female, assuming a subordinate demeanor, continues to slowly approach the nest despite repeated attacks by the male. Male-leading or -guiding courtship behaviors are known in Lepomis, Micropterus, and Centrarchus, although Lepomis females often enter nests with little or no overt courtship (Carr 1942; Dickson 1949; Hunter 1963; Keenleyside 1967; Chew 1974; Coble 1975; Vogele 1975a; Avila 1976; Gross 1982; Ridgway et al . 1989; Lukas and Orth 1993; Cooke et al . 2001b). Repulsing or guiding male behaviors directed at females may be species or context specific, are difficult to separate cleanly into courtship or aggression, and often co-occur (Keenleyside 1967; Ballantyne and Colgan 1978a,b,c). Once a pair is situated over the nest, they orient broadside and head to head and swim in slow, tight circles over the nest. The pair settles to the substrate, and egg deposition occurs as the female tilts away from the male and presses her vent near the substrate; the male presses his vent to the female’s while remaining upright or rolling toward the female. Egg and sperm release is accompanied by shuddering in both sexes; the demersal, adhesive eggs adhere to the nest substrate and to one another in clumps. Typically the pair rests, then repeats the sequence multiple times, until the male chases the female out of the nest. Rests between spawning bouts tend to shorten as the spawning event continues. These sequences may be in quick succession if the pair is not interrupted by intruders, but completion of spawning with a single female may occur over extended periods (15 minutes to 3.5 hours), even without interruption (Siefert 1968; Neves 1975; Vogele 1975a; Gross 1982, 1991; Isaac et al . 1998; Cooke et al . 2001b). After spawning, males aggressively guard the eggs and larvae, but the length of male parental care after the eggs hatch differs among genera and species within genera. Today, centrarchids are the primary focus of the recreational fishing industry in the United States and much of southeastern Canada. The relatively large size of many centrarchids, vulnerability to natural baits or artificial lures, and the excellent taste of the flesh combine to create a popular sport fishery worth billions of dollars a year. The black basses (Micropterus), particularly the Florida bass and largemouth bass, the bream or panfishes (Lepomis), especially the bluegill, and the crappies (Pomoxis) are sought by anglers more than any fresh or saltwater sport fishes in the United States. Angler numbers and days spent fishing for centrarchids dwarf those reported for salmonids, walleye, or saltwater fishes (USFWS 2002). A prodigious body of information is available on centrarchid natural history. Most research, however, has focused on a relatively few but important sport fish species, and there is no single-source recent summary of natural history information for all species in family. The objective here is to provide synopses of the characteristics and the natural history of the

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8 genera and 34 species of centrarchid fishes and to provide a dichotomous key to the family. A secondary objective of this chapter is to highlight species for which information on their natural history is lacking, fragmentary or anecdotal.

13.2 Generic and species accounts The bulk of the chapter consists of a separate account for each genus and each species within a genus, with the exception of monotypic genera. Only species accounts are given for monotypic genera. Within the characteristics sections of generic and species accounts, the definition of counts, standard length (SL), total length (TL), and other measurements follow standard ichthyological methods (see Page and Burr 1991; Jenkins and Burkhead 1994; Boschung and Mayden 2004) or are given in the citations associated with that section. Counts are presented as a total range, that is, 19 to 25; a modal (usual) count followed by a range, that is, usually 22, 19 to 25; or the most frequently encountered range of counts (ca. ≥90%) and the extremes, that is, (19)21 to 23(25). Only published sources were used to designate a confirmed freshwater mussel host (e.g., mussel larvae successfully infected and transformed on a centrarchid host). A putative host is similarly defined, except that the data are from unpublished sources and need verification. Published or unpublished accounts of mussel larvae infection on a centrarchid species without observation of transformation to the juvenile stage are not included.

13.3 Acantharchus pomotis (Baird) 13.3.0.1 Mud sunfish Characteristics: Moderately oblong and robust body, depth <0.4 of SL. Large, terminal mouth, lower jaw projecting slightly, supramaxilla large (≤2 times into length of maxilla), upper jaw extending beyond middle of eye. Eye large, diameter greater than snout length. Three to four parallel, brown to olive-black stripes across face (above eye, through eye, along upper jaw) and four to five dark brown stripes along side, often broken into mottling. Opercle with two flat extensions; opercular tab short and deep, spot prominent, dark brown to black, with orange (in large individuals) or light ventral and dorsal edges. Rounded caudal fin. Long dorsal fin, 10 to 12 spines, 9 to 13 rays, 20 to 24 total; and moderate length anal fin, 4 to 6 spines, 9 to 11 rays, 14 to 16 total. Dorsal fin continuous with shallow gap between spines and rays. Dorsal fin base about 1.7 to 1.9 times longer than anal fin base. Stout, moderate length gill rakers (5–7). Cycloid scales on head and body. Lateral line scales, 32 to 45; cheek scale rows, (5)6 to 8(9); breast scale rows, (10)12 to 14(16); branchiostegal rays, 7; pectoral rays, 14 to 15; vertebrae, 29 or 30. Teeth on endopterygoid, ectopterygoid, palatine (villiform), and glossohyal (tongue, one elongate patch) bones; vertebrae, 30 (13 + 17) (Bailey 1938; Cashner 1974; Cashner et al . 1989; Page and Burr 1991; Mabee 1993). Size and age: Typically 25 to 91 mm TL at age 1. Large individuals measure 150 mm TL and reach age 4+ to 8+ (maximum 206 mm TL, 190 g) (Breder and Redmond 1929; Mansueti and Elser 1953; Cashner et al . 1989; Page and Burr 1991; Pardue 1993; Jenkins and Burkhead 1994). North Carolina populations grew more rapidly in length and were shorter lived (4 vs 7–8 years) than populations in Maryland and New York (Mansueti and Elser 1953; Pardue 1993). Coloration: Dorsum and background of sides light olive or greenish gold to dark green or brown; olive to chocolate brown longitudinal stripes or mottling on sides. Ventral head and breast yellowish tan, mottled posteriorly on belly to flanks. Median fins olivaceous to dark brown, may be mottled in small individuals. Tips of anal spines and rays often darkened to produce marginal band. Caudal with broad, dark band at base; median rays may be darkened from base to tip, creating a striped effect. Dull red or brown iris. Little sexual dimorphism evident and no perceptible color changes occur in the breeding season, but chocolate brown mottling and ear tab tend to be darker in males than in females. Young may have up to 15 thin stripes along sides punctuated by dark pigment producing a somewhat spotted lateral pattern (Cashner et al . 1989; Page and Burr 1991; Pardue 1993; Jenkins and Burkhead 1994; Marcy et al . 2005). Native range: The mud sunfish occurs primarily on the Atlantic Coastal Plain and in lower Piedmont drainages from Hudson River, New York, to St. Johns River, Florida, and also occupies the extreme eastern Gulf Coastal Plain drainages from the Suwannee to St. Marks rivers in northern Florida and Georgia (Page and Burr 1991).

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Habitat: The mud sunfish is a decidedly lowland species, inhabiting sluggish waters of swamps, vegetated lakes, ponds, sloughs, and backwaters and pools of creeks and small to medium rivers. The species occurs across a broad range of pH (about 4–9) and in a study of New Jersey lakes was significantly more frequent in acidic waters (Graham 1993). The species is most often associated with plants, detritus, undercut banks, instream wood, and other cover (Page and Burr 1991; Pardue 1993; Jenkins and Burkhead 1994). In a North Carolina swamp, 70% of individuals recaptured (31 total) were within 0.2 km, and 30% moved 2.7 to 4.9 km from where they were marked. Increased movements occur from January to May, presumably in association with spawning activity, lower water temperatures, and higher water levels (Pardue 1993). Mud sunfish frequently invade intermittent tributaries and wetlands that dry infrequently (Snodgrass et al . 1996; Marcy et al . 2005). Food: The mud sunfish is reputed to be active at night, maintaining close affinity with and resting head down in vegetative cover during daylight (e.g., Abbott 1870; Breder and Redmond 1929; Mansueti and Elser 1953; Laerm and Freeman 1986), but quantitative studies of diel activity or feeding are lacking. Decapods, amphipods, odonates, and coleopterans form the primary diet of juveniles and adults, but small fish begin to be included in the diet at least seasonally when individuals reach >105 mm TL (Pardue 1993). Reproduction: Maturity is reached at age 1+ and a minimum size of 66 to 140 mm TL. Spent females, egg sizes, and gonad to body weight ratios suggest that the mud sunfish begins and completes spawning at temperatures as low as 7 to 10◦ C (Pardue 1993), which is lower than minima reported for other centrarchids. The spawning period apparently extends from December to May in North Carolina and into June in New Jersey at water temperatures of 7 to 20◦ C (Breder 1936; Pardue 1993). The ovaries enlarge in the early fall and continue developing over winter (Pardue 1993), which is likely an adaptation for early spawning. Reproductive behaviors are essentially unknown. Males have been observed or captured over small depressional nests near the shoreline of lakes or near the banks of headwater streams in water 15 to 30 cm deep (Fowler 1923; Marcy et al . 2005). Mud sunfish produce audible grunting noises (Gerald 1971), but linkage with reproduction is undocumented. Mature ovarian eggs range from 0.7 to 1.1 mm diameter (Pardue 1993). At a median size of 128 mm TL, a female can produce 2304 mature eggs (range: 1515 at 114 mm TL to 3812 at 144 mm TL; data from Pardue 1993), which is one of the lowest batch fecundities among centrarchids (see also Ambloplites and Enneacanthus). Female allocation of energy to reproduction is also low relative to most centrarchids with peak female gonad to somatic weight values of 3% (Pardue 1993). Mature ovarian egg size is similar to that in Lepomis and may indicate a similar duration of male care provided to the embryos and larvae (Gross and Sargent 1985), but the combination of low batch fecundity and low female energy allocated to reproduction differs from reproductive patterns observed in all other centrarchids. Nest associates: None known. Freshwater mussel host: None known. Conservation status: The mud sunfish is widely distributed but not common anywhere. The species appears to be secure where its lowland habitats are undisturbed, particularly in the central portions of its Atlantic Coastal Plain range (North and South Carolina). Populations to the north and south are considered possibly extirpated (New York), imperiled (Delaware and Maryland), or vulnerable (Virginia, Georgia, and Florida) (NatureServe 2006). Similar species: All other centrarchids have ctenoid scales (cycloid in Acantharchus), and except for Enneacanthus, deeply to shallowly emarginate caudal fins (rounded in Acantharchus and Enneacanthus). Enneacanthus possess three anal fin spines (4–6 in Acantharchus). Systematic notes: The phylogenetic relationships of the monotypic genus Acantharchus to other centrarchid genera is the least resolved within the family. Phylogenetic analyses place the species as sister to all other centrarchids or as resolved within a clade of all centrarchid genera but Lepomis and Micropterus (Roe et al . 2002; Near et al . 2004, 2005). The species shows evidence of polytypy. A subspecies described from the Okefenokee Swamp region (Suwannee River drainage, Georgia) as A. pomotis mizelli (Fowler 1945) was based on little comparative data. In an extensive study of geographic variation, several meristic characters of populations in eastern Gulf of Mexico drainages diverged significantly from those of populations in Atlantic Slope drainages. Multivariate analyses of morphological characters suggested that a contact zone between northern Atlantic Slope populations and Gulf Slope populations exists in Atlantic Slope drainages

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of Georgia and Florida (Cashner et al . 1989). Resolution of the evolutionary distinctiveness of the two geographic groups awaits molecular phylogeographic analysis. Importance to humans: The mud sunfish is one of the least known of all centrarchids, even to avid sport fishers, fisheries biologists, and most ichthyologists. The species is apparently rarely taken by hook and line and can go uncaught and unnoticed by anglers even when it occurs in heavily fished ponds (Mansueti and Elser 1953). Unfortunately, so little is known about the species that its ecological function and value in lowland stream and wetland ecosystems cannot be evaluated, but its adaptability to such habitats and distribution across a broad latitudinal band suggest a long evolutionary history in those environments and a potentially important functional role. The basal phylogenetic relationship of Acantharchus within the centrarchids may provide an important key for unraveling the relationship of the centrarchids to other percoid fishes, a relationship that is currently unknown. Likewise, study of its reproductive biology and behavior could illuminate the evolutionary history of complex reproductive strategies and associated behaviors observed in other centrarchids.

13.4 Ambloplites Rafinesque The monophyletic genus Ambloplites, often referred to collectively as rock basses, is endemic to eastern North America and contains four species consisting of two sister group pairs: Ambloplites ariommus (shadow bass) and Ambloplites rupestris (rock bass) form one sister pair and Ambloplites cavifrons (Roanoke bass) and Ambloplites constellatus (Ozark bass), the other. Ambloplites is sister to the monotypic genus Archoplites, represented by the Sacramento perch, and these two genera are sister to the genus Pomoxis (Near et al . 2004, 2005). The genus is distributed broadly across eastern North America, mostly east of the Great Plains, from southern Canada to the Gulf Coastal Plain, but the natural ranges of all four species are allopatric within this region. The Roanoke bass–Ozark bass sister pair occupies some of the smallest ranges of any North American sport fish. The Roanoke bass is endemic to Atlantic Coast drainages of Virginia and North Carolina and the Ozark bass mostly to the White River of Arkansas and Missouri. The range of the shadow bass is essentially disjunct; part of the range includes drainages of the eastern Gulf Slope and lower Mississippi River and the remainder includes drainages of the Ouachita Mountains, Arkansas River Valley, and Ozark Plateau. The rock bass, the most broadly distributed member of the genus, has been introduced and is widely established outside its native range in both eastern and western North America (Cashner and Suttkus 1977; Fuller et al . 1999). Intentional (or suspected) introductions of rock bass and other species of Ambloplites into the ranges of congeners has obscured natural ranges, has produced introgressed populations, and threatens the genetic integrity of species within the genus, particularly the range-restricted endemics (Cashner and Suttkus 1977; Cashner and Jenkins 1982; Jenkins and Burkhead 1994; Koppelman et al . 2000). Ambloplites appear to differ from most other centrarchids, except their sister genus Pomoxis, in several aspects of reproductive behavior, but detailed, multiple observations are available only for rock bass. Male Ambloplites apparently do not use caudal sweeping to clear nesting areas as is common in most other centrarchid males (Miller 1963). Ambloplites males use a combination of behaviors to construct the nest, including undulations of the anal fin, sweeping of the pectoral fins, and pushing material forward with outstretched pectoral fins (bulldozing, Gross and Nowell 1980; Petrimoulx 1984; Noltie and Keenleyside 1987b). Males orient slightly head downward and use alternating strokes of the pectoral fins for fanning the eggs, similar to Pomoxis, rather than the horizontally oriented and primarily caudal- fin fanning as described for Lepomis or Micropterus (Carr 1942; Miller 1963; Gross and Nowell 1980; Noltie and Keenleyside 1987b). Males show no overt courtship of females, and mate choice appears to be restricted to male acceptance of females (Gross and Nowell 1980; Petrimoulx 1984). Males aggressively and persistently repel and even attack females approaching the nest, spawning only with the most persistent, submissive females, behaviors in contrast to the active leading or guiding behaviors of nest-defending males toward females in other genera (e.g., Lepomis and Micropterus). The relative position of the male to the female during spawning also appears to differ in, and perhaps among, Ambloplites. The male of the Roanoke and Ozark bass occupies a central nest position during pairings with females rather than a position outside the female (toward the nest rim); the rock bass male takes an outside nest position in spawning if circling occurs, but occupies a central position when no nest circling occurs (Gross and Nowell 1980; Petrimoulx 1984; Noltie and Keenleyside 1987b; Walters et al . 2000). Members of Ambloplites are popular sport and food fishes and are commonly taken by anglers. In Missouri, three species, the shadow bass, rock bass, and Ozark bass, comprise 10% of the catch and harvest of fishes in streams (Koppelman

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et al . 2000). Many individuals are caught incidentally with the same lures and tackle used by anglers seeking smallmouth, spotted, and redeye basses, which frequently co-occur with species of Ambloplites. Anglers specifically seeking rock basses use small lures and spinners, lures imitating minnows, or live bait, particularly dobsonfly larvae (hellgrammites) and small crayfishes (Nielsen and Orth 1988; Ross 2001). Anglers often refer to these fishes as “redeyes” because of the conspicuous red pigment in their iris or “goggle eyes” because of their relatively large and conspicuous eyes (Etnier and Starnes 1993; Koppelman et al . 2000). Generic characteristics: Moderately compressed, elongate body, depth <0.5 of SL; compressed when young, becoming thicker as adults. Large oblique mouth, lower jaw slightly projecting, supramaxilla large (≤2 times maxilla length), upper jaw extending under eye pupil. Black or dusky oblique teardrop; prominent, large eye (≥0.25 of head length) with red iris. No bright red, orange, blue, or green colors. Young camouflaged with large, irregularly shaped, dark blotches alternating with lighter areas on body. Young and adults capable of rapid chameleon-like changes in pigmentation, providing effective camouflage under varying light and background conditions (Viosca 1936; Petrimoulx 1984; Noltie and Keenleyside 1987b). Opercle with two flat projections; dusky to dark opercular spot with light edge. Preopercle posterior margin variable in degree and kind of serrations. Dorsal, caudal, and anal fins with dusky spots and brown wavy lines. Long dorsal fin, usually 11 or 12 spines, 10 to 12 rays, 22 or 23 total; and moderate anal fin, usually 6 spines, 10 or 11 rays, 16 or 17 total. Dorsal fin base about 1.7 to 2.0 times longer than anal fin base. Dorsal fin continuous with a shallow gap between spines and rays. Short, rounded pectoral fin. Emarginate caudal fin. Moderately long gill rakers, 12 to 16. Ctenoid scales. Branchiostegal rays, usually 6; pectoral rays, 14 or 15; vertebrae, 31 (13 + 18). Complete lateral line. Teeth on endopterygoid, ectopterygoid, palatine (villiform), and glossohyal (tongue, one or two circular patches) bones (Bailey 1938; Cashner 1974; Page and Burr 1991; Mabee 1993; Boschung and Mayden 2004). Similar species: The warmouth has somewhat similar overall body shape and body mottling but has only three anal spines and dark lines radiating from the eyes (Page and Burr 1991).

13.4.1 Ambloplites ariommus Viosca 13.4.1.1 Shadow bass Characteristics: See generic account for general characteristics. Relatively small, compressed, and deepest-bodied member of genus; body depth usually >0.42 of SL. Eye large, diameter typically >0.30 of head length. The pattern of dark blotches alternating with lighter areas on body in young is retained in adults, so that adults and young resemble the appearance of young A. rupestris. Preopercle sharply serrate to weakly crenate to entire at the angle. Dorsal fin elements, (20)22 to 23(24); anal fin elements, (15)16 or 17(18). Cheeks fully scaled with large, exposed scales. Cheek scale rows, (5)6 or 7(8); lateral line scales, (34)38 to 43(45); scale rows above lateral line, (5)6 or 7(8); scale rows below lateral line, (11)13 to 15(16); diagonal scale rows, (18)22 or 23(24); and breast scale rows, (13)16 to 18(20). One circular patch of teeth on tongue (Cashner 1974; Cashner and Suttkus 1977; Page and Burr 1991). Size and age: Typically reach 40 to 120 mm TL at age 1. Large individuals measure 160 to 203 mm TL, rarely exceed 340 g, and reach age 6+ to 9+ (maximum 220 mm TL); Missouri and Arkansas populations can apparently reach larger sizes (at least 254 mm TL) than other populations (Viosca 1936; Robison and Buchanan 1984; Page and Burr 1991; Pflieger 1997; C. S. Schieble, University of New Orleans, personal communication). World angling record, 820 g, Arkansas (IGFA 2006). Females may outlive males, and males slightly exceed females in average maximum size and weight, but growth curves for the sexes are similar (C. S. Schieble, University of New Orleans, personal communication). Coloration: Light green to brown on sides with irregular marbling of brown or gray dark blotches alternating with lighter areas, blotches often joined dorsally to form saddles. Scales on sides bear a dark, triangular spot at the base (apex forward), producing a pattern of longitudinal lines that run through but are often obscured by the light and dark pigmented areas. Lower sides and belly transitioning to straw color (Viosca 1936; Cashner 1974; Page and Burr 1991). Large breeding males have a distinct darkening of the membranes in the pelvic and anal fins from the fin tips to the base and distinct black, threadlike filaments on their pelvic fins. These filaments are yellow to white in females (C. S. Schieble, University of New Orleans, personal communication).

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Native range: The range of the shadow bass is disjunct. The species occupies Gulf Slope drainages from the Apalachicola River west to the lower Mississippi River, including the Mobile Basin, and also occurs in the Red, Ouachita, Arkansas, St. Francis, and Black rivers (Page and Burr 1991). Habitat: The shadow bass inhabits gravel, sand, and mud-bottomed creeks and small to medium rivers with low levels of turbidity and sedimentation. The species is almost always associated with pools and cover of boulders, logs, log complexes, or rootwads; water willow or other aquatic vegetation in shallow water often harbors young-of-the-year (Probst et al . 1984; McClendon and Rabeni 1987; Page and Burr 1991; Pflieger 1997, reported as rock bass; C. S. Schieble, University of New Orleans, personal communication). In a large-scale tagging study (Funk 1957), shadow bass (reported as rock bass) were regarded as sedentary, but 48% and 31% of recaptured individuals moved at least 1.6 km from the original point of tagging in the Black and Current rivers, Missouri, respectively. Measures of biomass and fish size indicated that adult shadow bass emigrated from the Current River to a large near-constant temperature spring (13.5◦ C) during cold winter months when river temperatures dropped below the spring temperatures. Individuals reentered the river during warm periods when river temperatures exceeded spring temperatures. During high use of the spring in cold periods, shadow bass in the spring had significantly higher relative stomach fullness and larger eggs than conspecifics in the river, suggesting that an energy subsidy was conferred on fishes that used the spring seasonally (Peterson and Rabeni 1996, reported as rock bass). Food: The shadow bass is primarily a benthic feeder. An extensive diet study in Missouri indicated that crayfish were by far the most important prey item in shadow bass >100 mm TL. Young-of-the-year initially relied on invertebrates, particularly chironomids and mayflies as prey, but began consuming crayfish at about 25 mm TL and increased consumption with growth. About 70% of usable energy of adult shadow bass was derived from consumption of crayfish. Shadow bass consumed crayfish species in proportion to their abundance in the river, were size selective for crayfish 30 to 44 mm in length, and showed no seasonal shifts in diet. Fish, primarily stonerollers, and other invertebrates, particularly mayflies and stoneflies, were additional, but less important, adult diet items (Probst et al . 1984; Rabeni 1992, reported as rock bass). A limited analysis of shadow bass diets in a small, sand-bottomed Gulf Coastal Plain stream in Louisiana indicated high consumption of benthic fish prey (e.g., darters, madtom catfish, shiners) and insects (e.g., dragonflies, stoneflies, caddisflies) but limited predation on crayfish (Viosca 1936). Diel activity and feeding studies are unavailable, but the absence of shadow bass at night from their daytime haunts suggests a nocturnal component in activity and perhaps foraging (or at least a nocturnal shift in habitat use) (Probst et al . 1984). Reproduction: Maturity is reached at age 1+ and a minimum size of 87 mm TL in females and 108 mm TL in males (C. S. Schieble, University of New Orleans, personal communication). Nest building has not been described, but an extensive examination of reproductive biology is available for southern populations in Lake Pontchartrain, Pearl River, and Mississippi River tributaries (C. S. Schieble, University of New Orleans, personal communication). Based on ovarian condition and ovary to body weight ratios, southern populations have a protracted spawning period extending from January or February to May or June, corresponding to water temperatures ranging from 15 to 26◦ C. Peak ovarian condition occurs at about 23◦ C. Mature ovarian eggs average 0.98 mm diameter (range, 0.56–1.7 mm), suggesting a somewhat smaller average mature ova size than in rock bass, but maximum sizes are comparable (Gross and Nowell 1980). Two size classes of vitellogenic ova are reported in mature females, and these are present from January through May, suggesting production of multiple batches of eggs. At a mean size of about 120 mm SL, a female can potentially produce 1311 mature eggs (range: 161 eggs at 85 mm SL to 4113 eggs at 156 mm SL) in a single spawning event. Peak female ovary to body weight ratios average 4.1% in February and March and 2.7% in March through May. Female ovary to body weight ratios, mean total ova, and mean ova diameters decrease substantially in June and subsequent months (C. S. Schieble, University of New Orleans, personal communication). Nest associates: None known. Freshwater mussel host: None documented, but see account on A. constellatus. Conservation status: The shadow bass appears to be secure throughout its range (Warren et al . 2000), but is considered vulnerable in Louisiana (NatureServe 2006) where it is confined to the southeastern portion of the state. Increased sedimentation and turbidity in formerly clear, relatively fast-flowing Gulf Coastal Plain and Mississippi Alluvial Valley streams could and likely have reduced available habitat for this species (Pflieger 1997; C. S. Schieble, University of New Orleans, personal communication).

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Similar species: Color pattern of sides of adult Ozark bass and rock bass (>100 mm TL) are irregularly arranged freckles or rows of blackish spots, lacking the usually conspicuous, alternating light and dark blotches of adult shadow bass. Juveniles of all three species are similarly patterned (Pflieger 1997). Systematic notes: Patterns of differentiation in the Ozark populations of A. ariommus and its sister species, A. rupestris, can render identification difficult, irrespective of whether morphological criteria or allozyme-derived genetic data are used. Some suggest that the patterns of differentiation indicate a north-to-south cline between A. rupestris and Ozarkian A. ariommus populations that are indicative of conspecificity, but the observed patterns are confounded by known or suspected introductions of both species into various drainages in the region. For example, populations of Ambloplites in the Gasconade River and Charette Creek (both Missouri River drainage) display allozyme-derived genetic distances intermediate between A. rupestris and A. ariommus, which are likely attributable to past introductions (Koppelman et al . 2000). Even in naturally occurring populations, intermediacy is not positive proof of conspecificity of A. rupestris and A. ariommus because long-term evolutionary retention of ancestral polymorphisms after divergence of sister species is common in centrarchids (Near et al . 2005). Further, morphological differences between the two species in the Ozarks are supported (e.g., cheek and breast scales, adult color patterns) (Koppelman et al . 2000). At this time, field identification of A. ariommus in the Ozarks appears to be best accomplished on the basis of adult body coloration, body depth to length ratio, aspects of squamation, and geography (Pflieger 1997; Koppelman et al . 2000). Notwithstanding the Ozarkian populations, extensive morphological comparisons and limited population sampling of allozymes indicate that A. ariommus is polytypic. Populations in drainages of the Florida Panhandle and perhaps the Mobile Basin may be distinct (Cashner 1974; Koppelman et al . 2000), but resolution of the nature of the differentiation awaits a rangewide phylogeographic analysis of the species. Importance to humans: The shadow bass has many desirable qualities as a sport fish although the relatively small maximum size limits angler interest in some parts of its range. The species readily takes a lure or natural baits and is a popular catch for anglers using ultralight gear or fly rods in streams and rivers of the Coastal Plain of Mississippi and the Ozark and Ouachita Mountains of Missouri and Arkansas (Robison and Buchanan 1984; Probst et al . 1984; Ross 2001). Creel surveys in the Pascagoula and Pearl rivers of Mississippi indicated that shadow bass constituted 1% and 0.6% of the total catch by weight, respectively (Ross 2001). The flavor and texture of the flesh of the shadow bass is similar to other centrarchids such as spotted bass and bluegill (Viosca 1936).

13.4.2 Ambloplites cavifrons Cope 13.4.2.1 Roanoke bass Characteristics: See generic account for general characteristics. Relatively large, elongate body; body depth >0.41 of SL. Eye large, diameter about 0.25 of head length. Body pattern similar to that of A. rupestris but with freckled pattern (scattered, dark brown spots) on side of body and head. Adults with unique color pattern of numerous iridescent gold to white spots on upper body and head. Preopercle strongly serrate at the angle. Dorsal fin elements, (22)23(24); anal fin elements, (16)17(18). Cheeks naked or incompletely scaled with small, deeply imbedded scales. Lateral line scales, (39)42 to 46(49); scale rows above lateral line, (8)9 or 10(12); scale rows below lateral line, (13)14 or 15(16); diagonal scale rows, 23 to 26(27); and breast scale rows, (26)30 to 34(36). One or two oval patches of teeth on tongue (Bailey 1938; Cashner 1974; Cashner and Jenkins 1982; Page and Burr 1991; Mabee 1993). Size and age: Typically reach 42 to 89 mm TL at age 1. Large individuals measure 250 to 296 mm TL, weigh 770 g, and reach age 4+ to 9+ (355 mm TL) (Smith 1971; Carlander 1977; Petrimoulx 1983; Jenkins and Burkhead 1994). World angling record, 620 g, Virginia (IGFA 2006). State records in Virginia and North Carolina are 1.12 and 1.13 kg, respectively. The Roanoke bass is the largest species in the genus with many plausible historical accounts of individuals weighing >1.0 kg (Jenkins and Burkhead 1994). Coloration: Numerous iridescent gold to white spots on upper side of body and head. Ground colors variable, ranging from olive to tan to black to cream or blends of lighter and darker shades. Lateral pattern may consist of parallel rows of black spots, formed by scales darkened at bases, producing a lined pattern or indistinct dark and light blotches. Sides transition to white to bronze on breast and belly. All fins with some degree of yellow pigment, but median fins tend to be

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more olive and may be mottled or barred. Membranes of anal fin of breeding males dusky to dark but lack dark marginal band (Cashner 1974; Cashner and Jenkins 1982; Page and Burr 1991). Sexual dimorphism in color is minimal, but during nest guarding and spawning, the male darkens intensively and the pale spots become more evident (Petrimoulx 1984). Native range: The Roanoke bass is endemic to the Neuse, Tar, Roanoke, and Chowan river drainages, North Carolina, and Virginia (Page and Burr 1991). Habitat: The Roanoke bass occurs across a broad range of stream types in the upper Coastal Plain, Piedmont, Blue Ridge, and Ridge and Valley. The species is most common in flowing, rocky, and sandy creeks and small to medium rivers above the Fall Line, where it is often associated with deep runs. Roanoke bass appear to frequent faster currents than congeners (Smith 1971; Petrimoulx 1983; Jenkins and Burkhead 1994). Food: The Roanoke bass is primarily a benthic feeder. Crayfish are the most important prey item for adults (>150 mm TL), augmented by small fish (e.g., darters, catfish, shiners) and various aquatic insects, particularly mayflies and caddisflies (Smith 1969, 1971; McBride et al . 1982; Petrimoulx 1983). Fish are less important in the diet in spring than in summer or fall, but overall, 75% of the food volume of adults consists of crayfishes, and the remaining 25% is primarily fishes (Petrimoulx 1983). Young fish (<100 mm TL) transition at 100 to 150 mm TL from a diet of mayflies, amphipods, and other small invertebrates to one predominated by crayfish, mayflies, and small fish. A high frequency of river weed (Podostemum sp.) and associated invertebrates in stomachs of Roanoke bass suggests that foraging occurs in areas of considerable current (McBride et al . 1982; Jenkins and Burkhead 1994). Reproduction: Matures at age 2+ if a minimum size of 150 mm TL and 75 to 100 g body weight is reached (Smith 1971; Petrimoulx 1983). Based on ovarian condition and spawning observations, Roanoke bass spawn in May and June (perhaps as late as early July) at water temperatures of 20 to <25◦ C; postreproductive females first appear in samples in late July (Smith 1969, 1971; Petrimoulx 1983, 1984). Males (280–330 mm TL) initiated and completed nest building in 1 day as water temperatures approached 20◦ C in a hatchery pond in Virginia (Petrimoulx 1984). Substrate preparation was minimal, except that the guardian male removed snails and pebbles from the center of the nest by mouth and expelled them outside the nest; fanning, nest sweeping, or plant uprooting was never observed. The firm substrate of the pond may have limited the need for extensive nest preparation. Nests are solitary (≥1.3 m apart), 305 to 330 mm in diameter, 25 to 75 mm deep, at water depths of 30 to 60 cm, and excavated in gravel (<2.5 cm diameter) substrates if available (Smith 1969; Petrimoulx 1983). The male aggressively drives females away from the nest, but after about 45 minutes, when the female refuses to be driven off, the pair circles the nest, and spawning ensues with the male (in a central position) and female (outside position) in a broadside, face-to-face position. Spawning with each female lasts about 2.5 hours. In the observation pond, males spawned with two females simultaneously, but this may reflect low numbers of guardian males in the observation pond (Petrimoulx 1984). Mature ovarian eggs range from 1.3 to 2.0 mm in diameter (Smith 1969) and are among the largest reported for centrarchids. Two size classes of maturing ova are reported in females (vitellogenic and mature), suggesting two potential batches of eggs (Smith 1969; Petrimoulx 1983). In a North Carolina pond, the occurrence of two size classes of young-of-the-year also suggested at least two spawnings (Smith 1969), but renesting was not observed in the Virginia pond (Petrimoulx 1984). The relationship between total number of maturing ova (Y) and TL (X) is described by the linear function Y = −3937.1 + 36.7 TL (n = 16, R2 = 0.70, equation from Petrimoulx 1983). At a median size of about 193 mm TL, a female can potentially produce 3256 vitellogenic and mature eggs (range: 2440 eggs at 136 mm TL to 6476 eggs at 250 mm TL). At about 20◦ C, eggs hatch in 2 to 3 days, larvae reach swim-up 2 to 3 days later, and larvae disperse from the nest over a 3- to 4-day period. The male guards the nest until larvae reach the swim-up stage, gradually reducing holding time over the nest as larvae disperse (Petrimoulx 1984). Young Roanoke bass are apparently extremely wary and seek cover in thick vegetation (Smith 1969, 1971; Petrimoulx 1984). Nest associates: None known. Freshwater mussel host: None known. Conservation status: The Roanoke bass is considered vulnerable throughout its range (Warren et al . 2000; NatureServe 2006). In Virginia, the species is generally rare, and most extant populations are small. In North Carolina, the species is sparsely distributed but locally common (Smith 1969; Jenkins and Burkhead 1994). The Roanoke bass has been extirpated from portions of its former range (e.g., upper Roanoke River), and many populations appear to be persisting in marginal

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habitats where recruitment is poor (Petrimoulx 1983; Jenkins and Burkhead 1994). Losses and declines of populations are attributed to interactions with introduced rock bass, habitat degradation, and impoundments (Cashner and Jenkins 1982; Jenkins and Burkhead 1994). Establishment of additional populations by stocking in heavily silted streams had no apparent success in Virginia or North Carolina, but carefully planned stocking in suitable, high-quality habitats lacking potential nonnative competitors (e.g., rock bass, spotted bass) might produce additional populations (McBride et al . 1982; Jenkins and Burkhead 1994). Similar species: The rock bass has cheeks that are conspicuously scaled with relatively large scales that are only slightly to moderately embedded; the body lacks distinct, round pale spots; and the anal fin is marked by a dusky or black edge that contrasts with the rest of the fin. In the Roanoke bass the cheek is unscaled or partially scaled with tiny deeply embedded scales; the body is marked with distinct, round pale spots; and a dark margin on the anal fin is usually absent, rarely slightly developed, but never distinctly contrasting with the rest of the fin (Cashner and Jenkins 1982; Jenkins and Burkhead 1994). Systematic notes: Ambloplites cavifrons forms a sister pair with A. constellatus (Near et al . 2004, 2005). Until the late twentieth century A. cavifrons was often considered a subspecies of A. rupestris and was not differentiated from that widespread species by fisheries agencies. Cashner and Jenkins (1982) provided a clear morphological diagnosis of A. cavifrons, delimited the restricted range, reviewed the confused taxonomic history and resulting repeated stockings of A. rupestris in rivers and streams with native A. cavifrons, and provided morphological evidence of extremely limited hybridization of nonnative A. rupestris with native A. cavifrons. Mitochondrial and nuclear DNA analyses provide further evidence of the distinctiveness of A. cavifrons from congeners and its relatively distant evolutionary relationship to A. rupestris (Roe et al . 2002; Near et al . 2004, 2005). Importance to humans: Although long unrecognized as distinct among Ambloplites, the Roanoke bass possesses qualities of a first-class sport fish. The species is the largest member of the genus, is regionally unique, and is highly palatable (Jenkins and Burkhead 1994). A review of anglers’ catches (1964–1977, 1983) revealed that the majority of the Virginia citations for trophy Ambloplites (species not distinguished, 0.45 kg, 304 mm TL) were almost certainly Roanoke bass (Jenkins and Burkhead 1994). The sport fishery for the Roanoke bass is specialized, but the species is ardently sought by the few anglers in Virginia and North Carolina knowing where and how to fish for it (Smith 1969; Jenkins and Burkhead 1994). Increased emphasis on developing the sports fishery for this unique, range-restricted fish would diffuse knowledge of the species among anglers and, in turn, enhance its chances for long-term viability.

13.4.3 Ambloplites constellatus Cashner and Suttkus 13.4.3.1 Ozark bass Characteristics: See generic account for general characteristics. Relatively large, elongate body, depth usually <0.42 of SL. Eye large, diameter ≤0.27 of head length. Body pattern similar to that of A. rupestris but with freckling (scattered dark brown spots) on side of body and head. Preopercle strongly serrate to weakly crenate at the angle. Dorsal fin elements, (22)23(24); anal fin elements, (15)17(18). Cheeks fully scaled with large, exposed scales. Cheek scale rows, (6)9(11); lateral line scales, (38)43 or 44(48); scale rows above lateral line, (6)8 or 9(10); scale rows below lateral line, (11)12 or 13(14); diagonal scale rows, (21)22 to 24; and breast scale rows, (20)22. One circular patch of teeth on tongue (Cashner 1974; Cashner and Suttkus 1977; Page and Burr 1991). Size and age: Typically reaches 41 mm TL at age 1. Large individuals measure 180 to 213 mm TL and reach age 6+ to 11+ (maximum 259 mm TL) (Cashner and Suttkus 1977; Page and Burr 1991; Pflieger 1997). World angling record, 450 g, Arkansas (IGFA 2006). State record in Arkansas, 681 g (AGFC 2007). Coloration: General coloration similar to that of shadow bass and rock bass, but ground color of olive to tan above and below the lateral line is more uniform on the body and among individuals. Sides of body, cheek, opercle, and preopercle are dominated by a freckled pattern of irregularly arranged dark spots. In a lateral scale row, one to three scales are darkened at the anterior base and followed by a series of scales lacking the dark spots, producing the freckled pattern. On the body, the freckled pattern is most evident below the lateral line. Above the lateral line, four or five saddle-like blotches

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may be visible, but these are never dark enough to obscure the freckling or spotted pattern on the scales (Cashner and Suttkus 1977; Page and Burr 1991). Fins usually olive green, and no black marginal band develops on the anal fin. Sexual dimorphism in color is minimal, but males become nearly black and females grey during courtship and spawning (Walters et al . 2000). Native range: The Ozark bass is endemic to the upper White River of Missouri and Arkansas. The species drops almost completely out of the White River fauna at the physiographic border between the Ozark Plateau and the Mississippi Alluvial Valley. Isolated populations in the upper Osage River may be the result of introduction (Pflieger 1997; Koppelman et al . 2000). Habitat: The Ozark bass is abundant in clear, rocky pools of upland creeks and small to medium rivers in the White River drainage of the Ozark Plateau. The species also occurs in reservoirs. Ozark bass are often associated with cover of banks, boulders, or logs usually located away from the swiftest main channel currents (Cashner and Suttkus 1977; Robison and Buchanan 1984; Pflieger 1997). Food: The food of the Ozark bass has not been detailed, but the diet is likely similar to that of the rock bass and shadow bass. Reproduction: Knowledge of the reproductive biology of the Ozark bass is limited to a published account detailing aspects of nest sites and nesting chronology over two spawning seasons and describing behaviors of a single spawning pair in the Buffalo River, Arkansas (Walters et al . 2000). Asynchronous egg deposition and male nest guarding occurred over 4- to 5-week periods from mid-May to mid-June at water temperatures of 17 to 23.5◦ C. Nests were located in gravel and cobble substrates at depths of 0.5 to 2.9 m, and guarded by males ranging in size from 150 to 230 mm TL. Most nests (>74%) were <1 m from cover and were usually downstream of cover (e.g., boulders, logs). The majority of small nest-guarding males (<200 mm TL) were observed more than 2 weeks after initiation of spawning, but significant correlations of size of nest-guarding males and time since the beginning of spawning were not detected. During courtship, the male rarely directed or pushed the female into the nest; both sexes waved their soft dorsal, caudal, and pectoral fins almost constantly while keeping the spiny dorsal fin flat. Before each egg deposition, the male and female pair circled the nest several times, the female sometimes over the male and the male occasionally nipping the female near the caudal peduncle. Spawning ensued, with the pair dropping to the nest with the male (usually in a central position) and female (usually outside position) in a broadside, face-to-face position over the nest. Eighty-eight spawning bouts occurred in 2 hours, the pair drifting up from the nest between bouts. The female remained in or near the nest during this time. No postspawning aggression of the male toward the female was observed. A pair of Ozark bass were spawning at the same nest an hour later, but it is unknown if it was the same or another female. High water events were associated with renesting (nests with embryos), but new nests with embryos were found throughout the spawning season. At a mean temperature of 21◦ C, eggs hatched in ≥5 days, and larvae remained in the nest for 5 to 7 days. Dispersing young were grey. During the nesting period, no Ozark bass fry were observed outside areas guarded by males. No young-of-the-year were observed in daytime snorkeling transects, and few were caught in daytime seine hauls. In contrast, young-of-the-year were caught in larger numbers in nighttime seine samples, suggesting nocturnal activity in Ozark bass young (Walters et al . 2000). Nest associates: None known. Freshwater mussel host: None documented, but Ozark bass populations co-occur with populations of Villosa iris. Gravid females of V . iris possess highly modified mantle lures that, at least in Ozarkian populations, mimic the appearance and movement of small crayfishes (Barnhart 2006). The prominence of crayfish in the diet of some Ambloplites and the host relationship of A. rupestris (and other large centrarchids) with Villosa spp., suggest a potentially fascinating, but as yet unstudied, host–fish relationship. Conservation status: The Ozark bass is considered currently stable throughout its range (Warren et al . 2000; NatureServe 2006). Similar species: Other species of Ambloplites lack the distinctive freckled pattern of Ozark bass (Cashner and Suttkus 1977; Page and Burr 1991). In addition, the body depths in adult shadow bass and rock bass (>150 mm SL) are typically >0.41 of the SL and <0.41 of SL in Ozark bass (Koppelman et al . 2000).

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Systematic notes: Morphological and genetic evidence support long-term divergence and distinctiveness of A. constellatus from its sister species A. cavifrons and congeners (Cashner and Suttkus 1977; Koppelman et al . 2000; Near et al . 2004, 2005; Bolnick and Near 2005). Nevertheless, A. constellatus was not diagnosed and clearly differentiated from congeners until late in the twentieth century (Cashner and Suttkus 1977; Koppelman et al . 2000) and consequently was not recognized as distinct until relatively recently by fisheries managers. Early efforts to establish “rock bass” in Missouri and Arkansas streams involved brood stock taken from the upper White River, the range of A. constellatus (Cashner and Suttkus 1977; Robison and Buchanan 1984; Koppelman et al . 2000). These hatchery-based efforts were particularly intense in the 1930s and 1940s in Missouri (Pflieger 1997). Populations of Ambloplites in the Pomme de Terre and Sac rivers (upper Osage River, Missouri River drainage) are essentially identical to White River (Mississippi River drainage) populations of A. constellatus as evidenced by diagnostic allozyme loci, genetic distance, and phenotype (Cashner and Suttkus 1977; Pflieger 1997; Koppelman et al . 2000). In contrast, similar data suggest that the population in the Niangua River (middle Osage River) consists of non-F1 hybrids between A. constellatus and A. rupestris. No historical records are available before 1960 of the A. constellatus occurring anywhere in the Osage River. Similarly, no records of A. rupestris in the Niangua River drainage are known before 1940, and first documented records for the lower Osage River are from 1964 (Pflieger 1997). The populations of these species now established in the Osage drainage are likely the result of introduction of both species (Pflieger 1997), which may have produced the spatially limited hybridization as evidenced in the Niangua River (Koppelman et al . 2000). Impoundments in the upper Osage River appear to have limited dispersal of A. constellatus in the system, producing the essentially isolated populations in the Sac and Pomme de Terre rivers. Importance to humans: The Ozark bass is an abundant, popular, and sought-after sport fish in the upper White River of Missouri and Arkansas (Pflieger 1997; Koppelman et al . 2000).

13.4.4 Ambloplites rupestris (Rafinesque) 13.4.4.1 Rock bass Characteristics: See generic account for general characteristics. Relatively large, robust, elongate body, depth variable, usually >0.41 of SL. Eye large, diameter ≤0.30 of head length. Adults with rows of brown-black spots along side, forming horizontal lines. Preopercle strongly serrate to weakly crenate, but always a few teeth at angle. Dorsal fin elements, (20)22(24); anal fin elements, (15)16(17). Cheeks fully scaled with large, exposed scales. Cheek scale rows, (5)8 or 9(10); lateral line scales, (35)38 to 42(47); scale rows above lateral line, (6)7 or 8(10); scale rows below lateral line, 12 to 14(16); diagonal scale rows, (19)20 to 24(25); and breast scale rows, (18)21 to 24(27). One circular patch of teeth on tongue (Bailey 1938; Keast and Webb 1966; Cashner 1974; Cashner and Suttkus 1977; Cashner and Jenkins 1982; Page and Burr 1991). Size and age: Typically 42 to 102 mm TL at age 1. Large individuals measure 180 to 290 mm TL, weigh 200 to 454 g, and reach age 10+ to 14+ (maximum 430 mm TL) (Carlander 1977; Page and Burr 1991). World angling record, 1.36 kg, Pennsylvania and Ontario (IGFA 2006). Growth shows a latitudinal component in stream-dwelling rock bass such that northern populations grow more slowly than midlatitude populations. Among northern populations, maximum size and age of stream-dwelling rock bass are less than those of lake-dwelling rock bass, likely reflecting higher mortality in variable stream environments (Noltie 1988). In addition, subtle but significant differences occur in body form and relative fin sizes between northern lake and stream populations (Brinsmead and Fox 2002). Male rock bass can weigh more and reach longer lengths at age than females, but females can live longer (Ricker 1947; Carlander 1977; Noltie 1988). Coloration: Ground color of olive to tan above and on sides, fading to lighter, white to bronze, on breast and belly; brassy yellow flecks on sides; however, general coloration and shading highly variable among individuals and populations. If not obscured by darkened ground color, sides of body are dominated by a spotted pattern of regularly arranged dark spots, forming dark, uninterrupted horizontal lines. In a lateral scale row, scales are darkened by a spot at the anterior base, producing the horizontal striping effect. Light areas on the scales above and below the spot often give the appearance of light horizontal lines and together produce a pattern of alternating light and dark lines. The lined pattern is most evident below the lateral line. Four or five dorsal saddles may be visible, extending down to or just below the lateral line. Anal fin has a distinct, black marginal band that extends across the spiny portion to the fifth or sixth soft ray (Cashner 1974;

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Page and Burr 1991). Breeding males darken dramatically during the spawning period and develop black pigmentation along the spine and first ray of the pelvic fin or darken the entire fin (Cashner 1974; Gross and Nowell 1980; Noltie and Keenleyside 1987b). The pelvic fin margins of breeding female rock bass are yellowish white (Noltie 1985). External appearance of the genitalia (presence of the genital papillae in females) can be used as a reliable means of separating sexes during the breeding season (Noltie 1985). Native range: The rock bass has the largest native range in the genus occurring in the St. Lawrence River-Great Lakes, Hudson Bay (Red River), and Mississippi River Basins. Rock bass have been widely introduced and are established in Atlantic Slope drainages as far south as the Roanoke River, Virginia, and in the Missouri and Arkansas River drainages. The species is also established in several western states (Page and Burr 1991; Fuller et al . 1999). Habitat: The rock bass frequents cover in pools of creeks to small and medium rivers and the rocky and vegetated margins of lakes, being most common in silt-free rocky streams. Individuals in lakes frequent cover during the day (e.g., aquatic vegetation, rocky shelves, boulders) but disperse from these areas at night to feed (Keast 1977). Rock bass movements of >161 km (Funk 1957; Storr et al . 1983) are documented and populations may or may not show restricted summer home ranges. In Lake Erie, recaptured, tagged rock bass were taken from ≤3 km of their original location (MacLean and Teleki 1977). In Lake Ontario, postspawning rock bass showed less dispersion along the shoreline than prespawning individuals, but the degree of dispersal in both periods (about 2 weeks on average) was large (average 3.5 km versus 11.2 km, respectively; Storr et al . 1983). Overall average movement from April to June in tributaries to Lake Ontario was 500 m/d and maximal hourly movement was 200 m/h (Gerber and Haynes 1988). Summer home range in an Indiana stream was estimated at about 66 linear meters (Gerking 1950), and seasonal, multiyear samples in Tennessee streams revealed that 90% of recaptured rock bass remained in the same 500-m segment, and more than 50% were within the same 100-m segment (Gatz and Adams 1994). Some populations of rock bass migrate to wintering areas. In Lake Ontario, catches of tagged rock bass and dispersion models suggested movement from shoreline habitats to overwintering areas in deeper water (Storr et al . 1983), and littoral zone samples in Wisconsin lakes also indicated offshore movement in fall (Hatzenbeler et al . 2000). In small Virginia streams, fish in headwaters emigrated downstream in the fall, and in winter, fish used the deepest pools available (Pajak and Neves 1987). The presence of rock bass in a small North Carolina stream almost exclusively from autumn to spring over 10 years of sampling indicates that some populations migrate upstream to overwintering areas in fall and return downstream the following winter or spring (Grossman et al . 1995). Rock bass are sensitive to acidification, but sensitivity varies among life stages. Faunal analyses of northern lakes, in situ tests in lakes, and laboratory tests indicate that rock bass are negatively affected at pH 4.5 to 5.5 (Rahel and Magnuson 1983; Magnuson et al . 1984; McCormick et al . 1989; Eaton et al . 1992). Rock bass embryos, but not larvae, survived in an experimentally acidified lake at pH 5.1, recruitment was greatly reduced at pH 5.6, and high adult mortality occurred at pH 4.7. In the laboratory, survival of embryos and larvae (to 7-day post hatching) decreased by 40 to 50% at pH 5.0 and was near zero at pH 4.5. Larval survival also showed a dose-correlated decrease with decreasing pH (7.0 to 5.0) and increased Al (<0.6 to 56 µg/l) (Eaton et al . 1992). In a related laboratory study, juvenile rock bass (5.3 g) osmoregulated and survived up to 30 days at pH ≥4.5 but lost osmoregulatory control at pH 4.0 and died in ≤29 days (McCormick et al . 1989). Food: The rock bass is primarily a benthic feeder. Large invertebrates, such as crayfish, dragonfly nymphs, mayfly larvae, and caddisfly larvae are the primary diet items of adults (Keast and Welsh 1968; Keast 1977, 1985c; Johnson and Dropkin 1993; Roell and Orth 1993). In the New River, Virginia, where crayfish constitute more than 50% of the wet weight diet of individuals >100 mm TL, rock bass consume an estimated 31% of the annual production of crayfish of age 1 or 2 in the river (Roell and Orth 1993). Predation by rock bass is implicated in shifts in longitudinal distribution and species composition of juvenile crayfishes in headwaters of the New River, North Carolina (Fortino and Creed 2007). Small fish are taken during the second summer of life but contribute substantially to the diet only in larger adults (Keast 1977, 1985c; Elrod et al . 1981). Young-of-the-year feed heavily on cladocerans, isopods, amphipods, and chironomids; various aquatic insect larvae also contribute to the diet in the first summer (Keast 1977, 1980; George and Hadley 1979). The eyes of the rock bass are well equipped to allow successful capture of invertebrates in dimly lit bottom habitats. Lens quality increases until age 5, the distance of contraction and relaxation is high (≤28 diopters), and the ability to retain focus on approaching a target (93 diopters/s) is almost an order of magnitude greater than that reported for humans (Sivak 1973, 1990; Sivak and

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Howland 1973). The relatively large retina contains a temporal dorsal area of highest double cone densities that correlates with ability to detect prey below the horizontal plane (Williamson and Keast 1988). In the spring, diel studies indicate about equal feeding from mid-morning until noon and again from late afternoon to midnight (Keast and Welsh 1968) and in the fall, low levels of feeding during daylight hours with peak feeding between 2000 and 0400 hours (Johnson and Dropkin 1993). Diel movement of radio-tagged individuals in summer in Lake Ontario suggested higher diurnal than nocturnal activity. Activity was highest from 0900 to 2000 hours, decreasing substantially by 2200 hours; no diel patterns in activity were discerned in fish in tributaries to the lake (Gerber and Haynes 1988). Underwater observation in two lakes revealed an intensification of activity and feeding 30 minutes to 2 hours before darkness. During that time, large rock bass that aggregated in daytime resting areas near cover (1–8 m depth) moved as individuals or small groups into shallow water (Emery 1973; Helfman 1981). After darkness, individuals continued to be active in one lake, but in the other, individuals settled into and rested on rocks, logs, or plants. Underwater observations in a river indicated that rock bass are more active at night, tending to move from daytime cover to presumably feed in riffle and run habitats (Lobb and Orth 1991). Rock bass show active shoaling preferences for conspecifics and benefit from social enhancement of foraging (Brown and Colgan 1986; Templeton 1987; Brown and Laland 2003). Reproduction: Age at maturity is highly variable ranging from age 2+ to 7+ or even 9+ (about 125–150 mm TL) (Gross and Nowell 1980; Noltie 1988). Rock bass along the northern shore of Lake Erie make a 35- to 40-km spring migration to spawning grounds in an inner bay (MacLean and Teleki 1977), and other northern populations regularly ascend streams for spawning, moving up to 11 km/d (average 2.9 km/d), after overwintering in deeper waters (Noltie and Keenleyside 1987a; Gerber and Haynes 1988). Nest-site fidelity is high in some populations. Over 85% of recaptured rock bass in a northern lake nested within 50 m of their nest site in the previous year (Sabat 1994a), but in a Lake Ontario study, only 3 of 25 rock bass tagged during a spawning season and recaptured during subsequent spawning seasons were taken at the same site. The others were recaptured 28 to 185 km from the original tagging site (Storr et al . 1983). Males initiate nest building in late spring or early summer at temperatures as low as 14.0◦ C, and spawning temperatures range from about 18 to 23◦ C. Nests are circular in lakes (average 27 cm diameter) and elliptical in streams (37 cm wide, 43 cm long), about 5 to 7 cm deep, at water depths of 50 to 70 cm, and are typically excavated over coarse substrates (0.9–2.4 cm diameter). The spawning period can last from 6 to 8 weeks, but most reproductive activity occurs over a 3- to 4-week period; spawning tends to be synchronous in lakes and asynchronous in streams (Gross and Nowell 1980; Noltie and Keenleyside 1987a; Sabat 1994a). Large, older male rock bass (>100 g) nest and spawn 2 to 4 weeks earlier than smaller, younger males, and male size and number of eggs acquired are correlated positively, presumably reflecting female choice of mates (Noltie and Keenleyside 1987a; Sabat 1994b). In streams, nests are spaced widely (average 7.7 m apart) and near cover, but in lakes, nests are more closely spaced (average 1.6 m apart) with no apparent relation to cover (Gross and Nowell 1980; Noltie and Keenleyside 1987a). Circling of the nest by the male and female before spawning may occur for several minutes, or spawning may proceed without circling (Gross and Nowell 1980; Noltie and Keenleyside 1987b). A complete spawning bout can last 3.5 hours (average 2 h) and on average involves 120 separate egg releases (about 3–5 eggs per release); after each release, the female is often aggressively driven from the nest by the male for periods of 15 seconds to several minutes before returning for another bout (Gross and Nowell 1980). In synchronously spawning lake populations, females may spawn with more than one male, and males may spawn serially with alternating females (Gross and Nowell 1980), but in asynchronously nesting stream populations, males and females appear to be nearly monogamous (Noltie and Keenleyside 1987a,b). Mature ovarian eggs range from about 1.2 to 2.1 mm in diameter. Two size classes of ova are reported in females (modes, 1.65 mm and 0.44 mm) (Gross and Nowell 1980). Temporal changes in frequencies of egg diameter classes in lake-dwelling rock bass are coincident with spawning of two batches separated by a 16-day interval (Gross and Nowell 1980), and up to three discrete egg-laying bouts may occur over a 6- to 8-week period (Sabat 1994a,b). Information on numbers of mature ova in spawning-ready females is unavailable, but total fecundity is related positively to length (Carlander 1977). Based on observations of ovipositing females and numbers of larvae in nests, females appear to deposit about 400 to 500 eggs in a spawning bout (Gross and Nowell 1980). At a mean temperature of 22.5◦ C (range 16–22◦ C), eggs hatch in 5 days, and larvae disperse from nests 9 days later. Large older males may renest one or more times over the breeding season (Gross and Nowell 1980; Noltie and Keenleyside 1986; Sabat 1994b). Flooding, predation, and fouling of nests by algae are major causes of brood failure in stream-dwelling populations, resulting in frequent renesting attempts by males (Noltie and Keenleyside 1986). Parental males fan the eggs and defend the embryos and larvae (344 to 1758/nest) for an average of 14 days, abandoning the nest as the fry

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disperse (Carbine 1939; Gross and Nowell 1980; Noltie and Keenleyside 1986). Body weight of males can decline by 5 to 24% during the parental care period (Noltie and Keenleyside 1986; Sabat 1994a). Increased weight loss of parental male rock bass reduced probability of recapture in subsequent years (Sabat 1994a), suggesting a link between weight loss due to nesting and subsequent survivability of males. Free-swimming rock bass fry show no swarming behavior, begin agonistic behaviors sooner and at a smaller size (36 days post swim-up, 21 mm TL) than either Lepomis or Micropterus, and begin predator avoidance responses at 1 week of age (Brown 1984; Brown and Colgan 1985a). Freshwater mussel host: Confirmed host to Actinonaias ligamentina (Lefevre and Curtis 1910), Arcidens confragosus (Surber 1913), Pyganodon grandis, Utterbackia imbecillis (Tucker 1928; Trdan and Hoeh 1982), Strophitus undulatus (Van Snik Gray et al . 2002), V. iris (Zale and Neves 1982, as Villosa nebulosa; O’Connell and Neves 1999), and Villosa taeniata (Gordon et al . 1994). Putative host to Amblema plicata, Epioblasma obliquata, Lampsilis reeveiana, Lasmigona holstonia, Ligumia recta, Pyganodon cataracta, and Villosa constricta (unpublished sources in OSUDM 2006). Conservation status: The rock bass is currently considered stable throughout its range (Warren et al . 2000; NatureServe 2006). Introduction of rock bass into northern lakes where it is not native is implicated in declines in littoral zone fishes with potentially severe consequences for native lake trout populations dependent on those fishes for forage (Vander Zanden et al . 1999). Similar species: Other species of Ambloplites, except the Roanoke bass, lack the distinctive rows of spots of rock bass; the Roanoke bass has unscaled or partly scaled cheeks and iridescent gold to white spots on the upper side and head (Cashner and Jenkins 1982; Page and Burr 1991). Systematic notes: See accounts on A. ariommus, A. constellatus, and A. cavifrons. Importance to humans: Although underappreciated by many anglers, the rock bass is a feisty sport fish with firm, excellent-tasting flesh. As recently as the 1970s, rock bass contributed substantially to the commercial fishery and sport fishery catch in several Great Lakes (Scott and Crossman 1973; MacLean and Teleki 1977).

13.5 Archoplites interruptus (Girard) 13.5.0.1 Sacramento perch Characteristics: Moderately compressed, deep but somewhat elongate body, depth about 0.4 of SL. Large, oblique mouth, lower jaw projecting, supramaxilla large (≤2 times maxilla length), upper jaw extending under pupil of the eye. Opercle varies from two flat extensions to broadly rounded; dusky to dark opercular spot. Preopercle posterior margin sharply serrate. Long dorsal fin, 12 to 14 spines, 10 to 11 rays, 22 to 25 total; and moderate anal fin, 6 to 8 spines, 10 to 11 rays, 16 to 18 total. Dorsal fin base about twice as long as anal fin base. Dorsal fin continuous with shallow gap between spines and rays. Emarginate caudal fin. Rounded pectoral fins. Long, slender gill rakers, 25 to 30. Strongly ctenoid scales. Lateral line scales, 38 to 48; cheek scale rows, 6 to 9; branchiostegal rays, 7; pectoral rays, (13)14(15); vertebrae, 31(13 + 18). Teeth on entopterygoid, ectopterygoid, palatine (villiform), and glossohyal (tongue, two elongate patches) bones (Bailey 1938; Page and Burr 1991; Mabee 1993; Moyle 2002; C. M. Woodley, University of California-Davis, personal communication). Size and age: Typically 60 to 130 mm TL at the end of year one, depending largely on food availability and water temperature (C. M. Woodley, University of California-Davis, personal communication). Large individuals measure 370 to 400 mm TL, weigh 1.2 kg, and age 9+ (maximum, 610–730 mm TL and 3.6 kg) (Page and Burr 1991; Moyle 2002). World angling record, 1.44 kg, California (IGFA 2006). Females grow faster, reach larger sizes, and live longer than males (Mathews 1962; Aceituno and Vanicek 1976; Moyle 2002). Coloration: Olive brown above with 6 to 7 irregular dark bars on the upper side extending ventrally to the lateral line. Depending on habitat, varies from silver-green to purple sheen on mottled black and white side to silvery with dark barring; white ventrally. Breeding colors are variable. Males can be darker than females with purple opercula and a distinctive silvery spotting showing through the darker sides and can have a conspicuous darkened patch on top of their

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head; breeding females tend to be more uniform in color (Page and Burr 1991; Moyle 2002; C. M. Woodley, University of California-Davis, personal communication). Native range: The Sacramento perch is the only centrarchid with a native range west of the Rocky Mountains, where it was common and often abundant historically throughout the Central Valley of California (San Joaquin-Sacramento rivers), the Pajaro and Salinas rivers, and Clear Lake at elevations below 100 m. Currently, the only population that represents continuous occupation within the native range persists in Alameda Creek (Moyle 2002), but that population is considered unstable, the last record being of a single individual taken in 1999 in Calveras Reservoir (P. Crain and C. M. Woodley, University of California-Davis, personal communication). The species was introduced extensively outside its native range in the western United States between the 1870s and 1960s as a potential sportfish (McCarraher and Gregory 1970; Fuller et al . 1999) but now occurs outside the native range only in lakes, reservoirs, and associated streams in California, Nevada, Utah, and Oregon. Few of these populations are considered stable (Moyle 2002; Schwartz and May 2004; P. Crain, R. Schwartz, and C. M. Woodley, University of California-Davis, personal communications). Habitat: The Sacramento perch was formerly common in sloughs, slow-moving rivers, and lakes. The species often is associated with vegetation beds, which may be an essential habitat for young-of-the-year. Now, the species most commonly occurs in reservoirs and farm ponds. Because the original habitat was subject to extreme drought and flooding, Sacramento perch are notably tolerant of high turbidity, temperatures, alkalinity, chloride–sulfate salinity, and dissolved solids (Moyle 2002). Temperatures ≤30◦ C are readily tolerated (Moyle 2002). Recent work indicates the species is a cool-water centrarchid, with the preferred temperature ranging from 16 to 19◦ C; similarly, physiological optima appear to lie between 18 and 23◦ C (C. M. Woodley, University of California-Davis, personal communication). The species survived ≥12 months at pH >9 and maximal alkalinities >2000 mg/l in alklai lakes of Nebraska. Other centrarchids introduced in these habitats survived from a few hours to less than a month (McCarraher and Gregory 1970; McCarraher 1971). The species can reproduce in ponds with maximal pH and dissolved solids of 8.8 and 19,248 mg/l, respectively (Imler et al . 1975), and chloride–sulfate alkalinities of 17 ppt (McCarraher and Gregory 1970). Food: The Sacramento perch is a sluggish, slow-stalking, highly opportunistic suction-feeding carnivore (Vinyard 1982; Moyle 2002). It feeds primarily by “inhaling” organisms off the bottom or aquatic plants and by capturing zooplankton, fish, or emerging insects in midwater (Moyle et al . 1974). The species has numerous, long gill rakers that likely play an important functional role in the extended (<90 mm TL) feeding on zooplankton and other microcrustaceans. Although slight peaks in foraging occur at dawn and dusk, Sacramento perch show no obvious diel feeding periodicity, feeding at all times of the day and night (Moyle et al . 1974; Moyle 2002). Large individuals (>90 mm TL) in an introduced population (Pyramid Lake, Nevada) switched almost exclusively to piscivory, but in many populations, microcrustaceans and aquatic insect larvae and pupae continue as important components of the adult diet (Moyle et al . 1974; Imler et al . 1975; Aceituno and Vanicek 1976). Reproduction: Maturity is reached at age 2 to 3+ at a minimum size of about 120 mm fork length (FL). Spawning occurs at water temperatures of 18 to 29◦ C and can extend from March through early August with peaks in late May to early June (Murphy 1948; Mathews 1962; McCarraher and Gregory 1970; Aceituno and Vanicek 1976; Moyle 2002). Published accounts of reproductive behaviors are few, somewhat inconsistent, and based on limited observations. Although some observations suggested definite male territory defense (about 40 cm diameter) without preparation of the substrate, more recent extensive observations indicate male digging of nests with the caudal fin and subsequent defense of obvious cleared, depressions (C. M. Woodley, University of California-Davis, personal communication). Territories and nests are often associated with vegetation or filamentous algae beds in shallow water (20–50 cm deep) and over substrates of mud, clay, or rocks; rock piles or other cover may also attract spawning individuals (Murphy 1948; Mathews 1962, 1965; Aceituno and Vanicek 1976; Moyle 2002; C. M. Woodley, University of California-Davis, personal communication). Nest preparation may span several days (Moyle 2002). Some observed nests were arranged linearly along shorelines, but others were suggestive of colonies (Murphy 1948; Aceituno and Vanicek 1976; Moyle 2002). Tail quivering occurs in territorial males, a behavior which appears distinct from the nest sweeping behavior of other centrarchids (caudal sweeping, Miller 1963; Mathews 1965). The male remains stationary over the nest with the head down and pectoral fins out and rapidly oscillates the tail back and forth in small arcs, at 3 to 5 oscillations per second, ending with the head up and nearly perpendicular to the nest. After several seconds the male rests, then repeats the behavior, which intensifies during courtship and spawning. Territorial males repeatedly repulse approaching females (Mathews 1965). After repeated attempts to repulse

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the female (≤1 hour), the male swims stiffly to the ready female and nips at the vent (Moyle 2002). Pairs of Sacramento perch spend up to 30 minutes on the nest before spawning, during which time the male nips or nudges the female and both substrate bite, undulate, and contort their bodies, and jaw gape. Females may mate with more than one nesting male (Moyle 2002). In a natural setting, a male and female in the nest oriented broadside during spawning, but in opposite directions, unlike the head-to-head spawning position typical of other centrarchids. They made tight circles during gamete release as is typical of many centrarchids, but both the male and female tilted away from one another at the moment of release, another apparent departure from typical centrarchid gamete release (Mathews 1965; see also Bolnick and Miller 2006). Eggs are demersal, slightly adhesive, and upon deposition, adhere to surrounding vegetation or substrate in the bottom of the nest. Sacramento perch have among the smallest mature eggs among centrarchids (0.67 mm diameter) (Mathews 1962) and one of the highest batch fecundities among centrarchids (see Centrarchus macropterus and Pomoxis). Descriptive accounts indicate a unimodal distribution of mature or ripening ova sizes in mature females (Mathews 1962), suggesting release of a single batch of eggs. The relationship between number of mature eggs (Y) and TL (X) is described by the power function Y = 0.0279X2.6148 (n = 32, R2 = 0.89, data from Mathews 1962, FL converted to TL, see Aceituno and Vanicek 1976). At a mean size of 200 mm TL, a female can produce 29,003 mature eggs (range: 9820 eggs at 117 mm TL to 121,570 eggs at 330 mm TL, Mathews 1962). Hatching occurs in 51 hours and larval swim-up between 4 and 6 days at 22◦ C (Mathews 1962). From a single nest observation, male parental care is oft-cited as lasting only 3.5 days at water temperatures between 22 and 24◦ C, which is a short period of parental care relative to other centrarchids (Mathews 1965). More extensive observations at cooler water temperatures indicate that males stay at the nest for 5 to 7 days, apparently abandoning the nest only after larvae swim-up and move out of the nest area (Mathews 1962, 1965; C. M. Woodley, University of California-Davis, personal communication). Nest associates: None known. Freshwater mussel host: None known. Conservation status: Although tolerant of a range of physicochemical conditions, the distribution and abundance of native populations of the Sacramento perch has declined gradually since the nineteenth century. Declines are attributed to habitat alteration, embryo predation, and interspecific competition, particularly from nonnative centrarchids, such as bluegill and black crappie (Murphy 1948; Aceituno and Nicola 1976; Vanicek 1980; Marchetti 1999; Moyle 2002). In experiments with limited food resources, growth was depressed and habitat use shifted in the Sacramento perch in the presence of the more aggressive, dominating bluegill (Marchetti 1999). Native populations in the Pajaro and Salinas rivers and Clear Lake (Lake County) are extirpated (Gobalet 1990; Moyle 2002; Schwartz and May 2004). Within their native range the species persists primarily in ponds, reservoirs, and recreational lakes into which they were introduced, often upstream of native habitat (Moyle 2002). The species is considered of special concern in California rather than endangered because a few introduced populations appear secure (e.g., Garrison Reservior, Utah; Crowley Reservoir, California). However, even in many introduction sites in California and elsewhere, the species is uncommon, extremely rare, or extirpated (Moyle 2002; P. Crain and C. M. Woodley, University of California-Davis, personal communications; see section on native range). Similar species: The anal fin base of the white crappie and black crappie is about as long as the dorsal fin base, and the dorsal fin in these species has six to eight spines. Systematic notes: Archoplites interruptus is sister to the genus Ambloplites, and the Archoplites–Ambloplites pair are sister to Pomoxis (Roe et al . 2002; Near et al . 2004, 2005). Fossil representatives of the genus Archoplites are widespread west of the continental divide in Miocene to Early Pleistocene deposits (e.g., Idaho, Washington, Oregon, Utah, Nevada, and California) (Miller and Smith 1967; Smith and Miller 1985; Minckley et al . 1986; McPhail and Lindsey 1986; Near et al . 2005). Two other species, both extinct, are congeners: A. clarki Smith and Miller, from Miocene lacustrine deposits in northern Idaho (Smith and Miller 1985) and A. taylori Miller and Smith, from Late Pliocene to Early Pleistocene lacustrine deposits in southwestern Idaho (Miller and Smith 1967; Smith and Patterson 1994). Meristic variation among populations of A. interruptus is low, but some differences in color pattern exist (Hopkirk 1973; Moyle 2002). The population in Clear Lake probably is genetically distinct because of long isolation from other populations (Moyle 2002). Importance to humans: Historically, the Sacramento perch was one of the most common fishes caught by native peoples of California. In the late nineteenth century, 18,144 to 195,954 kg (40,000 to 432,000 lb) were sold annually in San Francisco (Gobalet and Jones 1995; Moyle 2002).

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13.6 Centrarchus macropterus (Lac´ep`ede) 13.6.0.2 Flier Characteristics: Deep, extremely compressed body, depth about half of SL. Small, supraterminal, oblique mouth, lower jaw projecting, supramaxilla moderate (2.1 to ≤3 times into length of maxilla), upper jaw not reaching past middle of eye. Eye large, diameter equal or greater than snout length. Large black teardrop. Interrupted rows of dark spots along the side. Juveniles (≤65 mm SL) with red-orange halo encircling black spot on posterior of soft dorsal fin. Opercle lacks flat extensions; opercular spot black. Preopercle posterior margin finely serrate. Long dorsal fin, 11 to 14 spines, 12 to 15 rays, 25 to 27 total; and long anal fin, 7 to 9 spines, 13 to 17 rays, 22 to 24 total. Dorsal fin base about 1.1 to 1.3 times longer than anal fin base. Spiny and soft dorsal fins continuous and smoothly rounded. Emarginate caudal fin. Long, pointed pectoral fin. Long, slender gill rakers, 30 to 40. Ctenoid scales. Lateral line scales 36 to 44; cheek scale rows, 4 to 7; branchiostegal rays, 7; pectoral rays, (12)13(14); vertebrae, 31(13 + 18). Teeth on entopterygoid, ectopterygoid, palatine (villiform), and glossohyal (tongue, two patches) bones (Bailey 1938; Page and Burr 1991; Mabee 1993; Jenkins and Burkhead 1994; Boschung and Mayden 2004). Size and age: Typically reach 55 to 72 mm TL at age 1. Large individuals measure 210 mm TL, weigh 156 to 197 g, and reach age 7+ to 8+ (maximum 250–356 mm TL) (Conley 1966; Geaghan 1978; Etnier and Starnes 1993; Jenkins and Burkhead 1994; Pflieger 1997). World angling record, 560 g, Georgia and North Carolina (IGFA 2006). Females can reach larger sizes and live longer than males (Conley 1966; Geaghan and Huish 1981). Coloration: Olive green to olive brown above; sides brassy yellow or silver with green and bronze flecks; rows of brown spots on sides forming horizontal lines. Brown-black spots on medial fins often form wavy bands or bars. Iris with vertical black bar continuing as tear drop. Young with four to five broad dark bars on side (Page and Burr 1991; Jenkins and Burkhead 1994; Pflieger 1997; Boschung and Mayden 2004). Native range: The flier occurs primarily on the Coastal Plain from the Potomac River drainage, Maryland, to central Florida, and west to the Trinity River, Texas. The species penetrates the Mississippi Embayment to southern Illinois and southern Indiana, where it occurs above the Fall Line (Page and Burr 1991). Habitat: The flier is a decidedly lowland species, inhabiting swamps, vegetated lakes, ponds, sloughs, and backwaters and pools of small creeks and small rivers. The species is usually associated with densely vegetated, clear waters (Page and Burr 1991; Jenkins and Burkhead 1994; Pflieger 1997; Boschung and Mayden 2004). Relative abundances were highest in hypoxic habitats in the Atchafalaya River Basin, Louisiana, where most fishes occurred in low relative abundances (Rutherford et al . 2001). The species also occurs in acid waters (pH 3.7 to 4.8), although growth appears to be diminished at low pH (Geaghan 1978); it is the most common sunfish in the acidic Okefenokee Swamp (Laerm and Freeman 1986). Movements of 12.7 km are documented, but ≥75% of individuals recaptured within 90 days of marking were found <200 m from their release site (Whitehurst 1981), suggesting fidelity to limited activity areas over extended periods. Increased movements occur in spring, presumably in association with spawning (Holder 1970; Whitehurst 1981). Food: The flier is a primarily nocturnal feeder with feeding practically ceasing during daylight hours (Conley 1966). The diet varies considerably with size, but zooplanktivory is continued to relatively large sizes and is likely associated with the possession of numerous, long gill rakers. Young (<22 mm TL) feed exclusively on copepods. Small crustaceans (primarily copepods and cladocerans), augmented with aquatic insects, form the bulk of the diet of individuals <175 mm TL. At larger sizes, insects are of primary importance, but small fish (mainly young bluegills) and crustaceans are also taken (Chable 1947; Conley 1966; Geaghan 1978; Jenkins and Burkhead 1994; Pflieger 1997). Reproduction: Maturity is reached at age 1+ and a minimum size of about 70 to 75 mm TL. Fliers are among the earliest, lowest temperature spawners in the family. The ovaries enlarge and continue developing in the fall and over winter (Conley 1966), which is likely an adaptation for early spawning. Nest building is initiated at 14◦ C and the brief 10- to 14-day spawning period begins at water temperatures of 17◦ C in March and April (Dickson 1949; Conley 1966; Pflieger 1997). Only a single anecdotal account of reproductive behaviors is available (Dickson 1949). The male establishes and defends a territory and prepares a typical, saucer-shaped depressional nest using his mouth and fins. Nesting occurs in shallow water (0.3–1.2 m depth) and is apparently colonial (2–15 closely spaced nests, similar to bluegill). Males remain relatively

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motionless over the nest and are quick to flee on approach and exceedingly slow to return to the nest (Dickson 1949). The male leads the female to the nest. On entering the nest, the female remains motionless in the nest as the male circles several times; biting is mutual during spawning. Females may mate with more than one nesting male (Dickson 1949). Eggs are demersal, adhesive, and golden yellow. Mature ovarian eggs are the smallest of all centrarchids (0.300–0.434 mm diameter) (Dickson 1949; Conley 1966), and size-adjusted batch fecundities are high for a centrarchid (see Archoplites and Pomoxis). Only one size class of maturing ova is reported in mature females, and postspawning females did not retain mature or maturing eggs (Conley 1966), suggesting production of a single batch of eggs. The relationship between number of mature eggs (Y) and TL (X) is described by the power function Y = 0.0230X2.7525 (n = 63, R2 = 0.79, data from Dickson 1949, Alabama; Conley 1966, Missouri). At a mean size of 114 mm TL, a female can produce 10,552 mature eggs (range: 4412 eggs at 70 mm TL to 48,254 eggs at 205 mm TL). Peak spawning female ovary to body weight ratios are among the highest of any centrarchid (see Enneacanthus and Lepomis), reaching 12.5% in early spring (Conley 1966). The tiny eggs suggest that the flier lies close to Pomoxis or Archoplites on the male parental care continuum (Gross and Sargent 1985). Hatching occurs in 7 to 8 days at about 19◦ C. One (or few) anecdotal observation suggested that the male leaves the nest and eggs before hatching (Dickson 1949), which, if true, is a notable departure from centrarchid male reproductive behavior. Detailed study of parental care and other aspects of the reproductive biology of the flier could provide insight into evolution of these traits in other Centrarchinae. Nest associates: None known. Freshwater mussel host: None known. Conservation status: The flier appears to be secure where its lowland habitats are undisturbed (Warren et al . 2000) but its conservation is of concern at the periphery of its range (vulnerable, Illinois, Missouri, and Oklahoma; critically imperiled, Maryland) (NatureServe 2006). Similar species: The white crappie and black crappie lack the dark teardrop and rows of spots on the sides and have 6 to 8 dorsal fin spines. Systematic notes: Centrarchus is a monotypic genus that is basal to a clade comprised of the genera Enneacanthus, Pomoxis, Archoplites, and Ambloplites (Roe et al . 2002; Near et al . 2004, 2005). Comparative studies of variation across the range of C. macropterus are lacking. Importance to humans: The flier is too small and localized in distribution to contribute to most sport fisheries. The species is a popular sport fish in the Okefenokee Swamp, where it makes up a considerable portion of the sunfish creel (Laerm and Freeman 1986). The flier rapidly seizes live or artificial bait and often leaps out of the water (hence, the name flier). The flesh is likened to that of bluegill (Dickson 1949).

13.7 Enneacanthus Gill The genus Enneacanthus consists of a clade of three diminutive species in which Enneacanthus chaetodon, the blackbanded sunfish, is sister to Enneacanthus gloriosus, the bluespotted sunfish, and Enneacanthus obesus, the banded sunfish. Enneacanthus is sister to a clade comprised of the genera Pomoxis, Archoplites, and Ambloplites (Near et al . 2004, 2005). The genus is distributed in the lower Piedmont and Coastal Plain drainages of the Atlantic Slope and eastern Gulf of Mexico from New Hampshire to Mississippi. With the exception of the bantam sunfish, Lepomis symmetricus, species of Enneacanthus are the smallest centrarchids (Page and Burr 1991). All three species are adapted to lowland habitats with abundant aquatic vegetation in which individuals aggregate. Their rounded caudal fins and deep, compressed bodies likely help these fishes navigate in thick aquatic vegetation. The genus Enneacanthus also shows extreme tolerance and adaptations to low pH in wetland habitats. Each species in the genus occurs in acid, dystrophic waters (e.g., bogs, swamps), but a gradient in tolerance exists from the most (banded sunfish) to the least tolerant (blackbanded sunfish) (Gonzalez and Dunson 1989a,b,c, 1991). Differential pH tolerance within the genus apparently exerts a strong effect on local distribution in areas of overlap (Graham and Hastings 1984; Gonzalez and Dunson 1991; Graham 1993), and in banded sunfish, it is rooted in highly specialized physiological adaptations (Gonzalez and Dunson 1989a,b,c, 1991).

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Characteristics: Deep, compressed body, depth >0.4 of SL. Mouth small, jaws equal, supramaxilla small (>3 times into length of maxilla), upper jaw not extending beyond front of eye. Eye large, diameter greater than snout length. Black teardrop. Opercle with two flat extensions. Rounded, truncate, or slightly emarginate caudal fin. Dorsal fins continuous. Long dorsal fin, (7)9 to 10(11) spines, 10 to 12 rays, usually 21 total, and short anal fin, 3 spines, 9 to 13 rays, 13 to 16 total. Preopercle margin entire. Long gill rakers, 11 to 14. Ctenoid scales. Vertebrae, 28 (12 + 16). Branchiostegal rays, 6. Teeth present or absent on palatine. No teeth on entopterygoid, ectopterygoid, or glossohyal (tongue) bones (Bailey 1938; Page and Burr 1991; Mabee 1993; Jenkins and Burkhead 1994). Similar species: See generic account for Lepomis and Micropterus.

13.7.1 Enneacanthus chaetodon (Baird) 13.7.1.1 Blackbanded sunfish Characteristics: See generic account for general characteristics. Deep, compressed body, depth ≥0.55 of SL. Mouth small, terminal. Eye large, diameter >1.2 of snout length. Six bold, black bars on sides, the first passes through the eye, the third extends dorsally through anterior spiny dorsal fin and ventrally through medial portion of pelvic fin, and the sixth through the caudal peduncle (often faint). Opercular spot dark with pale medial crescent. Rounded or slightly truncate caudal fin in young and juvenile, becoming truncate or slightly emarginate in adults. Long dorsal fin, (8)10(11) spines, 11 to 12 rays, usually 21 total, and short anal fin, 3 spines, (11)12 to 13(14) rays, 14 to 16 total. Dorsal fin continuous with deep notch between spines and rays. Dorsal fin base about 1.5 times longer than anal fin base. Dorsal and caudal fins not enlarged in breeding male. Pectoral fin narrow, somewhat pointed. Lateral line complete. Lateral scales, (23)25 to 29(32); cheek scale rows, (2)3(4); caudal peduncle scale rows, (16)18 to 21(22); pectoral rays, (9)11(13). Teeth present or absent on palatine bone (Bailey 1938; Page and Burr 1991; Mabee 1993; Jenkins and Burkhead 1994). Size and age: Typically reach 13 to 40 mm TL at age 1. Large individuals measure 40 to 60 mm TL (maximum 80 mm TL) and reach age 4+ (Schwartz 1961; Page and Burr 1991; Jenkins and Burkhead 1994). Length–weight relationships between males and females are similar in some populations (Schwartz 1961), but in a Delaware population females lived longer (age 3+) and reached larger maximum sizes (70 mm SL) than males (age 1+, <49 mm SL) (Wujtewicz 1982). Coloration: Prominent black vertical bars on sides (see Characteristics). Dusky yellow-gray to brown or black above, light below with tiny yellow flecks on sides. Leading edges of pelvic fins red, orange, or pink; third membrane of spiny dorsal fin similarly colored. Dorsal, anal, and caudal fins with black mottling. Iris reddish orange (Page and Burr 1991; Jenkins and Burkhead 1994; Marcy et al . 2005). Native range: The blackbanded sunfish is sporadically distributed below the Fall Line in Atlantic and Gulf Slope drainages from New Jersey to central Florida and west to the Flint River, Georgia. Large distributional gaps occur across the range (e.g., entire western Chesapeake basin), and populations in Georgia and Florida are isolated and widely scattered (Gilbert 1992b; Jenkins and Burkhead 1994). Four areas of concentration are evident. Three of these, the pine barrens of New Jersey, the sandhills in southeastern North Carolina, and the central highlands of Florida, are characterized by well-drained sandy soils with vegetation of pine and scrubby oak species and dystrophic, acidic waters. The fourth area is the acidic Okefenokee Swamp in Georgia (Gilbert 1992b). The broad gaps in the E. chaetodon distributional pattern may have arisen from prehistoric changes in sea levels, subtle ecological habitat differences, and competition with other fishes (Jenkins et al . 1975; T. Darden, South Carolina Department of Natural Resources, personal communication). Habitat: The blackbanded sunfish inhabits vegetated lakes, ponds, and quiet sand- and mud-bottomed pools and backwaters of creeks and small to medium rivers (Page and Burr 1991). Distributional studies in New Jersey indicate that the species occurs most often in acidic lakes (pH range, 7.0 to 4.1) (Graham and Hastings 1984; Graham 1993) and is most frequent in streams with a pH between 5.0 and 4.5 (Zampella and Bunnell 1998). In spring samples of small, sandy North Carolina streams, the species occurred most often in active beaver ponds apparently avoiding unimpounded stream channels and abandoned beaver ponds (Snodgrass and Meffe 1998). Although certainly tolerant of acidic conditions, laboratory studies suggest it is less tolerant of low pH than congeners. At pH 4.0 and 3.5, the blackbanded sunfish experienced the greatest disturbance of net Na flux, an indicator of pH stress, among the three species of Enneacanthus. All individuals of the

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blackbanded sunfish survived and recovered from a 12-hour exposure at pH 4.0, but 60% of test animals died in <12 hours at pH 3.5 (Gonzalez and Dunson 1989a). Food: The blackbanded sunfish apparently takes small invertebrates from the surface of vegetation, the water column, and the bottom (Reid 1950a; Schwartz 1961; Wujtewicz 1982). Aquatic insects (chironomid, caddisfly, and dragonfly larvae), amphipods, filamentous algae, and plant leaves dominate the diet; the algal and plant material are perhaps incidentally taken with invertebrates. The species apparently feeds throughout the day and perhaps even nocturnally (Schwartz 1961; Wujtewicz 1982). Reproduction: Knowledge of the reproductive behavior and biology of the blackbanded sunfish is sketchy, limited largely to aquarium observations by hobbyists, and almost entirely based on anecdotal accounts and unpublished reports (summaries by Hardy 1978; Jenkins and Burkhead 1994). Females mature at 33 mm SL and age 1+, or perhaps age 0+; males presumably mature at age 1+ (Wujtewicz 1982). Breeding activity is associated with water temperatures of about 20 to 28◦ C (Breder and Rosen 1966; Wujtewicz 1982; Sternburg 1986), and spawning occurs as early as March in North Carolina (Smith 1907) and early May to late June in Delaware (Wujtewicz 1982). Adults in North Carolina streams migrate seasonally into beaver ponds to spawn, habitats which are also important for young-of-the-year (Snodgrass and Meffe 1999). The male may excavate and defend a small depressional nest (ca. 10 cm in diameter) in sand or gravel or push out hollows in filamentous algae beds or macrophytes in water about 30 cm deep (Breder 1936; Breder and Rosen 1966; Sternburg 1986). Movement of bottom materials during nest excavation has been attributed to using the mouth, body, tail, or just “finning” (Breder and Rosen 1966; Sternburg 1986; Jenkins and Burkhead 1994). Males lead the female to the nest by darting toward her, quivering, spreading the fins, and then swimming back to the nest (Breder 1936; Sternburg 1986). The pair releases gametes in the typical head-to-head, vent-to-vent centrarchid spawning position (Breder 1936; Sternburg 1986). Gamete release is repeated numerous times over about 1.5 hours with pauses of 10 to 30 seconds between bouts (Breder and Rosen 1966; Sternburg 1986). In an aquarium, two females spawned simultaneously with a single male (Sternburg 1986). Spawning in the species is apparently protracted. In aquaria, spawning occurs repeatedly over several weeks (Sternburg 1986; Rollo 1994), and in Delaware, females were gravid from early May through June (Wujtewicz 1982). Ripe eggs were 0.9 mm in diameter (Wujtewicz 1982). Eggs were small or absent in females in July in Maryland and averaged 0.3 mm in diameter in November (Schwartz 1961). Females contain 233 to 920 mature ova (33 to 52 mm SL, respectively) (Wujtewicz 1982), but all of these may not be deposited in a single spawning (Quinn 1988). Fertilized eggs are adhesive and sand colored (Hardy 1978). The male guards the eggs, which hatch in about 2 days (Breder 1936), and continues guarding the larvae until they are free swimming (about 4–5 days after hatching) (Sternburg 1986; Rollo 1994). A guardian male in an aquarium was observed picking up stray larvae in his mouth and “spitting” them back into the nest (Rollo 1994), a behavior at least unusual if not unique among centrarchids (Miller 1963). An anecdotal report of biparental care of eggs and fry also deserves further investigation (Quinn 1988). Nest associates: None known. Freshwater mussel host: None known. Conservation status: The blackbanded sunfish is considered vulnerable to critically imperiled across most of its range (Warren et al . 2000; NatureServe 2006). The species is presumed extirpated in Pennsylvania, and only populations in New Jersey are considered secure (NatureServe 2006). The fragmented range and tendency for populations to be isolated, even though often locally common (e.g., Gilbert 1992b; Marcy et al . 2005), increase extirpation risk. Continuing urban, agricultural, and coastal development that involves drainage of small wetlands and ponds exacerbate the extinction risk imposed by fragmentation and isolation. Collection of specimens for aquaria may also adversely impact some low-density populations (Burkhead and Jenkins 1991). Similar species: The banded sunfish and bluespotted sunfish lack the black pigment at the front of the dorsal fin. Small individuals of all three species are similar, but the blackbanded sunfish develops the distinctive adult markings early (about 10 mm TL) (Sternburg 1986). Systematic notes: A southern subspecies, E.c. elizabethae, was described from limited samples from the Okefenokee Swamp and central Florida, based on differences in dorsal fin spine counts, caudal peduncle scale counts, and subtle

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aspects of pigmentation (Bailey 1941). Subsequent work suggested a north–south cline (Sweeney 1972), but larger sample sizes confirm reduced average counts in Florida and southern Georgia specimens (Gilbert 1992b). Importance to humans: The handsome blackbanded sunfish has long been of interest to aquarists in southeast Asia, where it is cultured in large numbers and shipped back to enthusiasts in North America (Sternburg 1986; Quinn 1988; Schleser 1998) and in Germany, where it has been kept since 1897 (Jenkins and Burkhead 1994). The species is currently traded and sold on Internet websites by individuals and pet stores. Feeding, water conditioning, and breeding of the species are featured frequently in magazines and on websites of organizations promoting use of native fish in aquariums (e.g., North American Native Fish Association, The Native Fish Conservancy).

13.7.2 Enneacanthus gloriosus (Holbrook) 13.7.2.1 Bluespotted sunfish Characteristics: See generic account for general characteristics. Deep, compressed body, depth 0.4 to 0.6 of SL. Mouth small, terminal, or supraterminal. Rows of blue or silver spots along sides of large young and adults; bars on sides indistinct in adults. Opercular spot dark, sometimes with pale medial crescent, usually <0.5 of eye diameter in specimens >25 mm SL. Rounded caudal fin. Long dorsal fin, (7)9(11) spines, (10)11(13) rays, usually 21 total, and short anal fin, 3 spines, (9)10(11) rays, 13 to 14 total. Dorsal fin continuous. Dorsal fin base about 1.5 to 1.7 times longer than anal fin base. Breeding male with enlarged second dorsal and anal fins; female lacks enlarged fins. Pectoral fin rounded. Lateral line may be lacking on several posterior scales. Lateral scales, (25)30 to 32(35); cheek scale rows, (3)4(5); caudal peduncle scale rows, (14)16 to 18(20); pectoral rays, (9)11 to 12(13). Teeth (cardiform) present on palatine bone (Bailey 1938; Sweeney 1972; Peterson and Ross 1987; Page and Burr 1991; Mabee 1993; Jenkins and Burkhead 1994). Size and age: Typically reach 19 to 34 mm TL at age 1. Large individuals measure 52 to 63 mm TL (maximum 99 mm TL) and at least in northern populations reach age 5+ (Breder and Redmond 1929; Fox 1969; Werner 1972; Snyder and Peterson 1999b). In southern populations, individuals rarely live to age 4+ (Fox 1969; Snyder and Peterson 1999b). Maximal size in Gulf Coast populations is less than that in Atlantic Coast populations, a likely consequence of earlier maturity in the former (Peterson and VanderKooy 1997; Snyder and Peterson 1999b). Length to dry weight relationships did not differ for males and females in Mississippi populations (Snyder and Peterson 1999b), and older males were slightly heavier than same-age females in Florida (Fox 1969). Coloration: Olive brown to olive or very dark midnight blue on body and head. Rows of round to oval, blue, green, silver, or gold spots along the sides of large young and adults (lacking in Mississippi populations), and extending onto head. Opercular spot black to pearly blue, often with medial blue-green crescentic mark. Spots on head and sides most developed on breeding males, which have a nearly black background with bright iridescent spots. Young and nonreproductive adults may have indistinct bars on sides. Soft dorsal, anal, and caudal fins may be pink or reddish; pale whitish spots in median fins. Iris dull red or gold (Page and Burr 1991; Jenkins and Burkhead 1994; Ross 2001; Marcy et al . 2005). Native range: The bluespotted sunfish, the most wide-ranging Enneacanthus, occurs in the Coastal Plain and Piedmont of Atlantic and Gulf Slope drainages from southern New York south to southern Florida and westward to the Biloxi Bay drainages of southeastern Mississippi (Page and Burr 1991; Jenkins and Burkhead 1994; Ross 2001). An introduced population is established in the Black River drainage, Mississippi (Peterson and Ross 1987), and populations in the Lake Ontario drainage, New York, and Susquehanna River drainage, Pennsylvania, are of unknown provenance (Smith 1985; Fuller et al . 1999). Habitat: The bluespotted sunfish inhabits vegetated lakes, ponds, and sluggish sand- and mud-bottomed pools and backwaters of creeks and small to large rivers (Fox 1969; Page and Burr 1991; Peterson and VanderKooy 1997; Snodgrass and Meffe 1998). In spring samples in North Carolina, the species occurred most often in beaver ponds rather than in unimpounded stream channels (Snodgrass and Meffe 1998). In coastal Mississippi drainages, the species almost exclusively used side ponds of oxbows, avoiding main channel habitats. In the side ponds, highest relative abundance was associated with decreased pH, decreased conductivity, and increased coverage of submergent and emergent vegetation; presence and absence of the species in the ponds was associated significantly with a mean pH of 5.6 and 6.5, respectively (Peterson

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and VanderKooy 1997). In New Jersey, the species was distributed independently of a color-pH gradient occurring across a pH range of about 9.0 to 4.0 (median 7.0) in lakes (Graham and Hastings 1984; Graham 1993), and in pineland streams the species occurred at a median pH between 5.0 and 4.5 (Zampella and Bunnell 1998). Growth is not affected negatively until pH declines below 4.5, but individuals survived up to 12 weeks at pH 4.0 (Gonzalez and Dunson 1989c). Food: The bluespotted sunfish is an opportunistic diurnal forager on benthic, vegetational, and planktonic prey; adult diets are dominated by prey associated with submerged aquatic vegetation and associated sediments (Breder and Redmond 1929; Fox 1969; Graham 1989; Snyder and Peterson 1999a). Dominant adult food items are chironomid larvae (and other aquatic insects), gastropods, and small crustaceans (ostracods, copepods, cladocerans, amphipods). The young transition from a diet predominated by cladocerans, copepods, and chironomid larvae to the broader adult diet (Fox 1969; Graham 1989; Snyder and Peterson 1999a). In late summer, young-of-the-year stomachs were nearly empty at dawn, but stomach fullness and digestion of prey indicated that individuals began feeding at dawn and fed continuously until darkness (Graham 1986). Reproduction: Maturity is reached in northern populations at age 2+ at a minimum size of about 53 mm TL (40 mm SL, Breder and Redmond 1929). Southern populations mature at age 1+ and show 50% maturity at 23 to 25 mm TL (Fox 1969; Snyder and Peterson 1999b), apparently the smallest size at maturity of any centrarchid. Spawning is protracted, and depending on latitude gravid females and small young occur from early spring through fall (Breder and Redmond 1929; Fox 1969; Wang and Kernehan 1979; Jenkins and Burkhead 1994; Snyder and Peterson 1999b; Doyle 2003). Female and male gonad to body weight ratios show initial increases as water temperatures rise above 15◦ C and remain high throughout much of the summer, but decline if temperatures remain above 27◦ C (Snyder and Peterson 1999b). Observations of nests are few and guardian male behaviors unknown, but the size, substrate, and placement of the nests are apparently similar to E. chaetodon (summary in Breder and Rosen 1966). Mature ova percentages increase throughout the summer, indicating continued recruitment from smaller ova classes. In Mississippi populations, there was no size–fecundity relationship (Snyder and Peterson 1999b), and the number of mature ova per female averaged 117. In Florida populations, the number of mature eggs increased from 67 to 80 in age 1+ females to an average of 400 and 500 mature eggs in age 2+ and 3+ females, respectively (Fox 1969). Mature eggs averaged 0.9 mm in diameter in freshly stripped eggs (Breder and Redmond 1929) and 0.68 mm in preserved females (Snyder and Peterson 1999b). Eggs are adhesive and demersal (Breder and Redmond 1929). Hatching occurs in 57 hours at 23◦ C, and length at hatching is 2.3 mm TL (Breder and Redmond 1929). Nest associates: None known. Freshwater mussel host: None known. Conservation status: The bluespotted sunfish is considered currently stable over its range, but populations at the periphery of the range (Mississippi, Alabama, New York, and Maryland) are listed as vulnerable (Warren et al . 2000; NatureServe 2006). Similar species: Pigmentation patterns of young bluespotted sunfish are virtually indistinguishable from banded sunfish, and even adults of the two species can be difficult to distinguish. In breeding male bluespotted sunfish the pale markings are nearly always present, are broadly oval, and are greenish yellow or gold in color; the body is often very dark, olive blue; and the dark lateral bars are absent or indistinct. In breeding male banded sunfish bright markings are sometimes present as gold-green crescentic flecks, the species never appears blue, and the lateral bars are dark and evident (Jenkins and Burkhead 1994). Average counts of caudal peduncle scale rows also appear to reliably separate the species, but traditionally used characteristics, such as completeness of the lateral line and relative size of the opercular spot, are not reliable across much of the range (Peterson and Ross 1987; Jenkins and Burkhead 1994). Systematic notes: Evolutionary relationships among E. gloriosus populations and between E. gloriosus and E. obesus appear to be complex and not yet fully resolved. Phylogeographic analyses of mitochondrial DNA indicate that E. gloriosus and E. obesus are not monophyletic taxa and suggest either incomplete lineage sorting or a polyphyletic E. obesus (T. Darden, South Carolina Department of Natural Resources, personal communication). Introgression was detected using nuclear-encoded allozyme data in sympatric populations of the sister species pair E. gloriosus and E. obesus in New Jersey (Graham and Felley 1985). In areas of allopatry, hybridization was not detected, but appreciable introgression was present in co-occurring populations. Developmental instability was correlated positively with the degree of introgression

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(heterozygosity), indicating that hybridization may result in reduced fitness for the hybrid individuals (Graham and Felley 1985). Morphological variation in the two species in Virginia also shows considerable and curious overlap (Jenkins and Burkhead 1994). Phylogeographic analyses appear to support an Okefenokee Swamp–based center of dispersal for E. gloriosus and relatively long-term isolation and differentiation of Florida populations from other Atlantic Slope populations (T. Darden, South Carolina Department of Natural Resources, personal communication). In addition, populations in Mississippi are morphologically divergent from other E. gloriosus populations (Peterson and Ross 1987). Importance to humans: The bluespotted sunfish, like its congener the blackbanded sunfish, has attracted the attention of aquarists. A perusal of Internet sites indicates that the species is regarded as an adaptable aquarium fish, although feeding and water conditioning can be challenging. The species is actively sold and traded by enthusiasts and retailers.

13.7.3 Enneacanthus obesus (Girard) 13.7.3.1 Banded sunfish Characteristics: See generic account for general characteristics. Deep, compressed, somewhat thick body, depth 0.4 to 0.5 of SL. Mouth small, supraterminal, oblique. Rows of purple-gold crescentic flecks on sides; five to eight dark bars on sides. Opercular spot dark, usually >0.5 of eye diameter in specimens >25 mm SL. Rounded caudal fin. Long dorsal fin, (7)9(11) spines, (10)11(13) rays, usually 21 total, and short anal fin, 3 spines, (10)10 to 11(12), 13 to 14 total. Dorsal fin continuous. Dorsal fin base about 1.5 to 1.7 times longer than anal fin base. Breeding male with enlarged second dorsal and anal fins and longest pelvic rays distally filamentous; female lacks enlarged fins and filamentous extensions. Pectoral fin rounded. Lateral line usually interrupted or incomplete. Lateral scales, (27)30 to 32(35); cheek scale rows, (3)4(5); caudal peduncle scale rows, (17)19 to 22(24); pectoral rays, (10)11 to 12(13). Teeth (cardiform) present on palatine bone (Bailey 1938; Peterson and Ross 1987; Page and Burr 1991; Mabee 1993; Jenkins and Burkhead 1994). Size and age: Reached 20 to 30 mm TL at age 1 in a Connecticut reservoir (Cohen 1977); age 0+ fish were 34 to 35 mm SL in October and 51 mm SL the following April in the Okefenokee Swamp (Freeman and Freeman 1985). Large individuals measure 55 mm TL (maximum 95 mm TL) and reach age 6+ (Cohen 1977; Page and Burr 1991). Males tend to live longer and grow slightly faster than females (Cohen 1977). Coloration: Dusky olive above, light below, with olive-black or five to eight black bars on the sides that may vary in distinctiveness. Rows of purple-gold crescentic flecks along side. Opercular spot black, bordered with iridescent goldgreen margin. Median fins dark with rows of blue to white spots. Breeding male, and to a lesser degree, breeding female with gold-green or blue flecks on head, body, and median fins, fin spines glowing white. Iris orange-red (Page and Burr 1991; Jenkins and Burkhead 1994). Aspects of subtle differences in coloration between E. obesus and E. gloriosus are summarized by Jenkins and Burkhead (1994). Native range: The banded sunfish occurs primarily on the Coastal Plain of Atlantic and Gulf Slope drainages from southern New Hampshire south of central Florida and west of the Perdido River drainage of Alabama (Page and Burr 1991; Boschung and Mayden 2004). Across the range, the species can be rare to relatively common (Smith 1985; Laerm and Freeman 1986; Jenkins and Burkhead 1994; Boschung and Mayden 2004; Marcy et al . 2005). An introduced population is established in the Black River drainage of Mississippi (Peterson and Ross 1987). Habitat: The banded sunfish inhabits heavily vegetated lakes, ponds, and sluggish sand- or mud-bottomed pools and backwaters of creeks and small to large rivers (Page and Burr 1991). The species is perhaps one of the most acid-tolerant fishes known (Gonzalez and Dunson 1987) and occurs in waters with pH 3.7 (e.g., New Jersey, Graham and Hastings 1984; Graham 1989; Georgia, Freeman and Freeman 1985). In multivariate studies in New Jersey, the banded sunfish was associated more strongly with acidic (pH 6.6–4.1), dystrophic habitats than either congener in lakes (Graham and Hastings 1984; Graham 1993) and in streams occurred most frequently between pH 5.0 and 4.5 (Zampella and Bunnell 1998). Individuals survived 2-week laboratory exposures to pH 3.5, and 60% of test individuals survived 3-week exposures to pH 3.3 after a gradual lowering from 3.5 over a 1-week period (Gonzalez and Dunson 1987). Growth was unaffected down to a pH of 3.75 (Gonzalez and Dunson 1989c). These findings suggest that the banded sunfish may have distinct

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competitive advantages over congeners and other sunfishes in low pH habitats (Gonzalez and Dunson 1991). Its tolerance of low pH is the result of complex adaptations for compensating for losses in body Na that would kill other fishes and involves the ability to limit branchial electrolyte permeability during acidic exposure (Gonzalez and Dunson 1987, 1989a,b,c). The gills of banded sunfish have a high affinity for Ca that reduces leaching by H+ and prevents high Na losses down to pH 3.5. In addition to limiting Na efflux, the species apparently can shift internal Na from osmotically inactive sources (e.g., bone) to plasma, which maintains Na concentrations of extracellular fluid. Although chronic acid exposure causes a large drop in body Na concentration (up to 52%, lethal to most fishes), these adaptations allow the banded sunfish to survive (Gonzalez and Dunson 1987, 1989a,b,c, 1991). Food: The banded sunfish, like its sister species the bluespotted sunfish, is an opportunistic forager on benthic, vegetational, and planktonic prey; adult diets are dominated by prey associated with submerged aquatic vegetation (Chable 1947; Cohen 1977; Graham 1989). Although diets overlap substantially between the two species, the banded sunfish gleans more vegetational prey and eats less benthic and planktonic prey than the bluespotted sunfish where the two co-occur (Graham 1989). Dominant adult food items are chironomid larvae (and other aquatic insects) and small crustaceans (cladocerans, copepods, amphipods). The young transition from a diet predominated by cladocerans, copepods, and chironomid larvae to the broader adult diet (Graham 1989). In late summer, young-of-the-year stomachs were nearly empty at dawn, but stomach fullness and digestion of prey indicated that individuals began feeding at dawn, paused between late morning and midday, and then fed continuously until dark (Graham 1986). Reproduction: Maturity is reached at age 2+ in females at a size of about 35 to 40 mm TL, but some smaller, age 1+ females are capable of spawning (Cohen 1977). Information on minimum size and age of maturity of males is lacking, but males are reproductively active by at least 59 mm TL (Harrington 1956). Gonadal development and associated nesting and spawning behaviors are controlled by increasing photoperiod and temperature (Harrington 1956). When males and females collected from ponds in fall were exposed in the laboratory to 15 hours of daylight and 21.7◦ C water temperature, ovary volume, ova size, testis volume, and male breeding colors developed rapidly (about 38 days), and nest building and spawning occurred. In contrast, in a parallel set of experiments at 21.7◦ C conducted under a fall photoperiod (9.2–11.6 hours daylight), individuals did not show gonadal enlargement or other reproduction-associated changes. In natural environments, spawning can be protracted. Gravid females and nuptial males occur from April to July in Virginia (Jenkins and Burkhead 1994), and capture of small young in Delaware suggests a late spring-through-summer breeding season (Wang and Kernehan 1979). In contrast, young-of-the-year only appeared in early June collections in a year-long sampling effort in the Okefenokee Swamp, Georgia (Freeman and Freeman 1985). Peak spawning and egg development occurred in June and July in a Connecticut reservoir at surface water temperatures of 23 to 27◦ C. Most details of reproductive biology, spawning behavior, and aspects of parental care are undocumented. In aquaria, breeding males establish territories, engage in threat postures and chasing, excavate depressional nests with their mouths, and vigorously defend the nest, eggs, and free-swimming larvae (Harrington 1956; Breder and Rosen 1966; Cohen 1977; Rollo 1994). One large male (52 mm SL) bred on 10 different days (of 26 days observed) and participated in 107 spawning acts under laboratory conditions (Harrington 1956). The interval between spawning acts was from 0 to 4 days. Mean fecundity, presumably based on total ova, increases with age (and size) ranging from 802 eggs at age 1 to 1400 eggs at age 6 (Cohen 1977). Mature ova are 0.6 mm in diameter. Fertilized eggs are adhesive and colorless, eggs hatch in about 3 days at 21.7◦ C, and larvae become free swimming about 5 days after hatching (Harrington 1956; Rollo 1994). Nest associates: None known. Freshwater mussel host: None known. Conservation status: Although not in danger of imminent extinction because of occupation of broad latitudinal range across many independent drainage systems, the banded sunfish is considered vulnerable to critically imperiled in many states within its range (New Hampshire, Rhode Island, Connecticut, Virginia, Alabama, Pennsylvania, New York) (Warren et al . 2000; NatureServe 2006). Similar species: See account on bluespotted sunfish. Systematic notes: See account on E. gloriosus.

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Importance to humans: Like congeners, the banded sunfish is popular among enthusiasts interested in keeping and rearing native fishes (Rollo 1994; Schleser 1998). Although perhaps underappreciated, the ability of the species to tolerate waters of relatively high acidity should increase scientific interest in the species.

13.8 Lepomis Rafinesque The genus Lepomis is a monophyletic clade of 13 species and is sister to the genus Micropterus (Near et al . 2004, 2005). The natural range encompasses most of eastern North America east of the Rocky Mountains, reaching northward to the Great Lakes, St. Lawrence River, and Hudson Bay drainages of Canada and eastward and southward in the Mississippi River Basin, Atlantic Slope, and Gulf of Mexico drainages west to the Rio Grande. Breeding males of some Lepomis are among the most colorful of all North American native fishes, and the reproductive habits of several species are among the best-studied and most fascinating within the fish fauna. The literature is extensive and only a brief overview is presented here and in the individual accounts. Lepomis share many features common to centrarchid reproduction. Males establish territories, excavate nests, fan, and guard eggs and defend newly hatched larvae until the swim-up stage. In addition, many Lepomis develop brilliant breeding colors and possess highly complex reproductive behaviors that can involve motor, visual, and auditory signals, and several species have evolved alternative mating strategies. Territorial breeding males excavate the typical circular depressional nest of other centrarchids, but many distinctive behaviors and combinations of behaviors are documented, often being associated with nest defense, courtship, or both. The male is faced with defending a nesting territory using agonistic behaviors and successfully mating with a female using courtship behaviors, motivations that necessarily shift from moment to moment, particularly in colonial nesters, and often appear in conflict (Keenleyside 1967; Steele and Keenleyside 1971; Ballantyne and Colgan 1978a,b,c). Males over nests display to nearby or approaching males and females using combinations of nest hovering, dashes to the surface and back to the nest, nest sweeping with the caudal fin, fin spreading, mouth gapes, jaw snaps, lateral displays (males side-by-side with fins erect), breast displays, substrate biting, and opercular spreads. Males most frequently rush toward an interloper with a quick retreat to the nest (thrust, Miller 1963), but if the intruder does not retreat, males display or actually ram, push, bite, or jaw grasp the other male. Males may also engage in rim circling, in which males repeatedly and rapidly circle their nest (e.g., over 100 circles in 30 minutes) with fins displayed (Miller 1963; Hunter 1963; Huck and Gunning 1967; Boyer and Vogele 1971; Avila 1976; Colgan et al . 1979; Lukas and Orth 1993). The act likely makes the male more conspicuous to females (Miller 1963; Avila 1976) but also serves as a territorial advertisement to other males (Colgan et al . 1979). In courtship, as a spawning-ready Lepomis female approaches a male’s nest, the male performs courtship circles by darting from the nest with fins spread, encircling the female and leading her toward the nest (Keenleyside 1967; Boyer and Vogele 1971; Avila 1976; Ballantyne and Colgan 1978a,b,c; Gross 1982). The male may courtship circle many times in rapid succession until the female follows him to the nest or leaves (Miller 1963; Keenleyside 1967). Augmenting the motor behaviors and breeding colors developed on the body and head, males of some species also have exaggerated opercular flaps. The ear flaps (or ear tabs) are species specific in orientation, size, and color patterns and serve as sex ornaments (secondary sexual characteristics) that play a complex role in mate choice, species recognition, and aggression between rival males (Keenleyside 1971; Colgan and Gross 1977; Stacey and Chiszar 1977). Opercle flaring directed at females is frequent in courting males (Keenleyside 1967), and the flap apparently signals to the female the species, condition, and quality of the male (Childers 1967; Goddard and Mathis 2000). Females prefer males with larger opercular flaps (e.g., Lepomis megalotis), and larger flaps increase the probability of a male in attaining and holding central nesting sites in a colony, where females spawn preferentially relative to peripheral nests (e.g., Lepomis macrochirus) (Gross and MacMillan 1981; Cˆot´e and Gross 1993; Goddard and Mathis 1997; Ehlinger 1999). Aggressiveness and dominance also are closely linked to the opercular flap. Males of at least some Lepomis appear to assess the resource-holding power of rivals by their opercular flap size (Goddard and Mathis 2000). Out of age, size, and seven morphological features in male bluegill, opercular flap size was the only feature that corresponded significantly with male rank in a breeding territory dominance hierarchy in experimental tanks (Ehlinger 1999). Some territorial, breeding male Lepomis further augment motor and visual reproductive signals with sound. On sighting a female near his nest, a nesting male rushes toward her and back toward his nest while producing a series of gruntlike

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sounds (bluegill, green sunfish, longear sunfish, and redspotted sunfish) or popping sounds (pumpkinseed and redear sunfish) (Gerald 1971; Ballantyne and Colgan 1978a,b,c). The sounds are also produced as males attack other males intruding into their nesting territory or in noncourtship agonistic contexts (Ballantyne and Colgan 1978a,b,c). Sound production is attributed to manipulation of the pharyngeal jaw pads, but in agonistic or courtship contexts is not associated with feeding (Ballantyne and Colgan 1978a,b,c). Sound characteristics suggest species specificity (Gerald 1971), and conspecific and heterospecific sounds elicit auditory brainstem responses in Lepomis (Wysocki and Ladich 2003), but individual variation in sound characteristics is high (Ballantyne and Colgan 1978a,b,c). Females are more responsive to conspecific than heterospecific sounds, but males respond to both (Gerald 1971; Ballantyne and Colgan 1978a,b,c). Sound production may facilitate location of nesting males by females in conditions of low visibility (Gerald 1971; Steele and Keenleyside 1971), but the behavior also appears to be part of a ritualized sequence of behaviors (e.g., jaw snaps and courtship circles), signaling that the male is both highly aggressively and sexually aroused (Ballantyne and Colgan 1978a). Alternative male reproductive strategies are highly evolved in Lepomis (Gross 1982; Jennings and Philipp 1992a; Philipp and Gross 1994; Avise et al . 2002). In a nest takeover strategy, large guardian males permanently displace small guardian males, or in nesting colonies, neighboring guardian males may intrude temporarily in another male’s nest to steal fertilizations with a female (Keenleyside 1972; Avila 1976; Dominey 1981; Gross 1982; Dupuis and Keenleyside 1988; Jennings and Philipp 1992b,c; DeWoody et al . 1998). Nesting male Lepomis habituate to the appearance of males on neighboring nests and become less aggressive toward them (Colgan et al . 1979), so unmated neighbors can more easily intrude and steal fertilizations (Keenleyside 1972; Jennings and Philipp 1992b). These strategies, however, appear to occur in relatively low frequencies (<5% of nests, DeWoody and Avise 2001; Neff 2001). A more common parasitic reproductive strategy is used by cuckolder males of Lepomis, which do not invest in parental care, but do attempt to steal fertilizations from guardian males. Small sneaker males steal fertilizations from guardian males by hovering near the nest margin and darting in and out to release sperm beneath the spawning female and guardian male (Dominey 1980; Gross 1982, 1984, 1991). When sneaker males are about as large as reproducing females, they can switch to the satellite tactic (Gross 1982). Satellite males mimic females in behavior and coloration and, if the guardian male is deceived, which occurs frequently, they can hold a position in the nest between the spawning female and guardian male and steal fertilizations (Dominey 1980; Gross 1982; Fu et al . 2001). Sneaker and satellite morphs are documented only in bluegill (Dominey 1980; Gross 1982). Sneaker male morphs occur in populations of longear sunfish (Jennings and Philipp 1992b,c), northern longear sunfish (Keenleyside 1972; Jennings and Philipp 1992c), pumpkinseed (Gross 1979, 1982), and spotted sunfish (DeWoody et al . 2000a). Cuckolder male morphs were sought but not detected in North Carolina populations of dollar sunfish, bluegill, and redbreast sunfish (Belk 1995; DeWoody et al . 1998; Mackiewicz et al . 2002). Even so, observations of the intrusion of ostensibly “small females” between spawning pairs of Lepomis suggest that the parasitic strategy may occur in other populations or species (e.g., Hunter 1963; Boyer and Vogele 1971; Lukas and Orth 1993). The life history of parasitic males differs dramatically from that of guardian males. Parasitic males do not develop breeding colors and are smaller, grow slower, mature earlier, allocate more body mass to testis weight, differ in sizeadjusted body shape, and are shorter lived than guardian males (Gross 1982; Jennings and Philipp 1992c; Drake et al . 1997; Ehlinger 1997; Ehlinger et al . 1997; Stoltz et al . 2005). Demographic analyses of bluegill populations indicate that parasitic phenotypes do not become guardian males (Dominey 1980; Gross 1982; Drake et al . 1997) and that alternative male phenotypes are determined early in the life history (Ehlinger et al . 1997). In other Lepomis with alternative strategies, demographic data also are suggestive, although not conclusively, of an early and permanent divergence in life history between guardian and sneaker male phenotypes (Jennings and Philipp 1992c). Generic characteristics: Deep, compressed body (somewhat elongate in Lepomis cyanellus and Lepomis gulosus). Opercle rounded or produced into flexible ear flap. Emarginate caudal fin. Dorsal fin shallowly emarginate, spiny portion continuous with soft-rayed portion. Long dorsal fin, usually 10 spines, 10 to 12 rays, usually 20 to 21 total; and short anal fin, 3 spines, 9 to 11 rays, 12 to 14 total. Dorsal fin base about two times longer than anal fin base. Preopercle margin usually entire (weakly crenate in L. gulosus). Ctenoid scales. Vertebrae, 29 to 31(12 or 13 + 17 or 18). Branchiostegal rays, 6 (Bailey 1938; Page and Burr 1991; Mabee 1993; Boschung and Mayden 2004). Similar species: Presence of three anal fin spines separates Lepomis from all other centrarchids except Enneacanthus and Micropterus. Lepomis have shallowly emarginate caudal fins (versus rounded in Enneacanthus) and deep, laterally compressed bodies with <55 lateral scales (versus elongate body and ≥55 lateral line scales in Micropterus).

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13.8.1 Lepomis auritus (Linnaeus) 13.8.1.1 Redbreast sunfish Characteristics: See generic account for general characteristics. Body deep, compressed, depth 0.38 to 0.48 of SL. Mouth moderate, terminal, oblique, supramaxilla small (>3 times and ≤4 times into length of maxilla), upper jaw extending to (or almost to) anterior margin of eye. Wavy blue lines apparent on preorbital area, cheek, and usually opercle. Opercular flap long, narrow, flexible, oriented horizontally or pointing upward, black to posterior margin, usually bordered above and below with blue line. Soft dorsal fin acute. Pectoral fin short and rounded, tip usually not reaching past eye when bent forward. Short thick gill rakers, 9 to 12, longest about twice the greatest width in adults. Lateral line complete. Lateral scales, (39)41 to 50(54); rows above lateral line, 7 to 9; rows below lateral line, 14 to 16(17); caudal peduncle scale rows, (21)22 to 23(25); cheek scale rows, 6 to 9; pectoral rays, (13)14(16). Pharyngeal arches narrow with short, pointed teeth. Teeth on palatine bone. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Scott and Crossman 1973; Barlow 1980; Etnier and Starnes 1993; Mabee 1993; Boschung and Mayden 2004). Size and age: Size at age 1 is highly variable among habitat types and latitudes, ranging from 32 to 102 mm TL (median 59 mm). Large individuals measure 200 to 250 mm TL, weigh 150 to 300 g, and attain age 5+ to 7+ (maximum 305 mm TL, age 8+) (Bass and Hitt 1974; Sandow et al . 1975; Carlander 1977; Page and Burr 1991; Marcy et al . 2005). World angling record, 0.79 kg, Florida (IGFA 2006). Florida angling record, 0.94 kg (FFWCC 2006). Growth differences between males and females are minimal to nonexistent (Sandow et al . 1975; Carlander 1977). Coloration: Narrow, elongate black ear flap, dark to posterior margin, bordered above and below with blue lines. Wavy, often narrow, blue lines radiate from mouth across sides of snout onto cheek and opercle, broken and often less distinct on opercle. Dark olive above and on sides with yellow flecks and rows of red-brown to orange spots on upper sides, orange spots scattered on lower side. White to orange below. Clear to dusky yellow to orange fins. Breeding male with bright orange breast and belly, orange fins, light powder blue sides with orange spots (Page and Burr 1991; Jenkins and Burkhead 1994; Marcy et al . 2005). Native range: The redbreast sunfish is native to the Atlantic and Gulf Slopes from New Brunswick to central Florida and west to the Apalachicola and possibly the Choctawhatchee River drainages of Georgia and Florida. The native or introduced status in the Tallapoosa and upper Coosa rivers of Alabama and Georgia, where the species is widespread and common, is uncertain (Boschung and Mayden 2004). The species has been widely introduced and is established well outside its native range (e.g., Rio Grande to southeastern Ohio River basin) and in some areas (e.g., upper Tennessee River drainage) may be displacing native Lepomis (Page and Burr 1991; Etnier and Starnes 1993; Fuller et al . 1999; Miller 2005). Habitat: The redbreast sunfish inhabits rocky, sandy, or mud-bottomed pools of creeks and small to medium rivers and can also occur in lakes, ponds, or reservoirs (Page and Burr 1991). The species is usually associated with cover (e.g., instream wood, stumps, or undercut banks), and in streams, abundance increases with decreasing water velocity and increasing depth and cover (Meffe and Sheldon 1988). Redbreast sunfish are relatively sedentary (home activity area usually <100 m stream length), but long-distance movements (1–17 km) occur (Hall 1972; Gatz and Adams 1994; Freeman 1995). Peak movements occur in the spring before spawning (Hall 1972; Hudson and Hester 1975; Gatz and Adams 1994). Food: The redbreast sunfish is an opportunistic invertivore that may feed most heavily during the day or at night (Cooner and Bayne 1982; Bowles and Short 1988; Johnson and Dropkin 1993). Aquatic insects, particularly mayfly, dragonfly, caddisfly, and dipteran larvae, make up the bulk of the diet. Gastropods, aquatic beetles, terrestrial and emerging aquatic insects, crustaceans, and a wide variety of other invertebrate taxa also are consumed frequently, but fish, although eaten, are not important dietary items. As young redbreast sunfish grow, the diet increasingly includes larger aquatic invertebrates and more aerial and terrestrial insects (Sandow et al . 1975; Cooner and Bayne 1982; Sheldon and Meffe 1993; Murphy et al . 2005). High volumes of vegetation and organic debris in stomachs suggest concentrated foraging among plants and on the bottom (Davis 1972; Bass and Hitt 1974; Sandow et al . 1975; Cooner and Bayne 1982). In the summer, diversity of food items in the diet was highest in daylight hours, but feeding occurred throughout a 24-hour period (Cooner and Bayne 1982), and in the fall, feeding peaked between 2000 and 0400 hours (Johnson and Dropkin 1993). In late winter, indirect evidence indicates elective feeding on nocturnally drifting amphipods (Bowles and Short 1988).

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Reproduction: Maturity is reached at ages 1+ to 2+ at a minimum size of about 90 to 114 mm TL (Davis 1972; Bass and Hitt 1974; Sandow et al . 1975; Lukas and Orth 1993). Nest building and spawning begin as water temperature increases from about 17 to 20◦ C and continues to 31◦ C. Spawning is protracted (April–early June to August or even October), depending in part on latitude (Bass and Hitt 1974; Lukas and Orth 1993). Nesting activity decreases over the summer and is related strongly to the number of degree days accumulated after water temperatures reach 20◦ C, although declines may also be related to renesting by unsuccessful males or declining numbers of spawning-ready females (Sandow et al . 1975; Lukas and Orth 1993). Males excavate depressional nests by carrying stones in their mouth and by caudal sweeping. Nests are 47 to 94 cm in diameter, 4 to 15 cm deep, and at water depths of 36 to 200 cm. Nests are usually placed in low-velocity habitats over coarse sand, gravel, or sand–gravel substrates and near cover of logs, stumps, boulders, plants, or bedrock ledges (Breder 1936; Miller 1963; Davis 1972; Sandow et al . 1975; Thorp et al . 1989; Helfrich et al . 1991; Lukas and Orth 1993; Marcy et al . 2005). Active nests may be widely spaced (4.5–9.1 m apart) or occur in loose aggregations of >80 nests (about 1.9 m apart) (Lukas and Orth 1993; Fletcher 1993). Nesting and spawning occurs in tidal waters supporting marine faunal elements, beaver ponds, backwaters, coves, and main flowing channels (Davis 1972; Bass and Hitt 1974; Sandow et al . 1975; Thorp et al . 1989; Helfrich et al . 1991; Lukas and Orth 1993; Snodgrass and Meffe 1999; Marcy et al . 2005). Nesting males (114–174 mm TL) may actively court females or females may enter nests with no courtship, ultimately spawning with two to six or more nest-guarding males (Lukas and Orth 1993; DeWoody et al . 1998). Reported spawning behaviors appear typical of most Lepomis (e.g., nest circling, repeated dips), but males use caudal sweeping to mix fertilized eggs into the nest substrate (Miller 1963; Lukas and Orth 1993). Genetic paternity analyses in a North Carolina population indicated that nest-guarding males sired most (>96%) of the young in their nests. Nest takeovers were rare, but 44% of assayed nests contained low percentages of offspring from nonguardian males, even though no sneaker male morphs were detected (DeWoody et al . 1998; DeWoody and Avise 2001). Intrusion by an ostensible female between a spawning pair (Lukas and Orth 1993) also suggests the possibility of sneaker males in some populations. Mature ovarian eggs range from 0.90 to 1.64 mm (mean 1.20 mm) (Sandow et al . 1975). The relationship between total number of mature ova (Y) and total length (X) is described by the linear function log Y = −3.8786 + 3.1628 log X (n = 79, R2 = 0.71, equation from Sandow et al . 1975). At a median size of 153 mm TL, a female can potentially produce 1074 mature eggs in a single batch (range: 435 at 115 mm TL to 6104 eggs at 265 mm TL). The adhesive, yellow to amber, fertilized eggs hatch in 3 days at 20 to 24◦ C. Newly hatched larvae are 4.6 to 5.1 mm TL, and most larvae are free swimming at 7.6 to 8.2 mm TL (Hardy 1978; Buynak and Mohr 1978; Yeager 1981). The guardian male vigorously defends the nest, eggs, and larvae from nest predators, may reduce foraging activity, and may cannibalize offspring in his own nest (Thorp et al . 1989; Lukas and Orth 1993; DeWoody et al . 2001). Nest associates: Dusky shiner, Notropis cummingsae (Fletcher 1993); swallowtail shiner, Notropis procne (Buynak and Mohr 1978); golden shiner, Notemigonus crysoleucas (Shao 1997). Freshwater mussel host: Putative host to Lampsilis teres, L. recta, and V. constricta (unpublished sources in OSUDM 2006). Conservation status: The redbreast sunfish is widespread and often abundant within its native range. It is considered vulnerable in Rhode Island, Massachusetts, and New York (Smith 1985; NatureServe 2006). In Massachusetts, it appears to have declined since the mid-1800s owing to changes in water quality or behavioral interactions with introduced species, especially the bluegill (Hartel et al . 2002). Similar species: Adult longear, northern longear, and dollar sunfishes have a shorter ear flap that is bordered by a white or orange edge, possess blue marbling or spots on the side of the adult, and lack distinct rows of red-brown spots on the upper side (Page and Burr 1991). Systematic notes: Lepomis auritus is sister to a clade inclusive of L. marginatus, L. megalotis, and L. peltastes (Near et al . 2004, 2005). Comparative studies of variation across the range of L. auritus are lacking. Importance to humans: The redbreast sunfish is a popular, sought-after sport fish in streams and rivers across most of the Atlantic Slope and eastern Gulf Coast (e.g., Suwannee River). On light tackle, redbreast sunfish offer excellent sport, being somewhat more aggressive, more surface oriented, and more active in cool waters than bluegill. The quality of the flesh is excellent and rated higher than that of Micropterus by some (Etnier and Starnes 1993; Jenkins and Burkhead 1994).

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13.8.2 Lepomis cyanellus Rafinesque 13.8.2.1 Green sunfish Characteristics: See generic account for general characteristics. Body deep, compressed, but elongate and thick relative to other Lepomis, depth 0.37 to 0.45 of SL. Mouth large, terminal, slightly oblique, supramaxilla small (>3 and ≤4 times length of maxilla), upper jaw extends well beyond anterior edge of eye, and in large individuals may extend to posterior edge of eye or beyond. Adult with dark spot at posterior base of soft dorsal and sometimes anal fin. Green to blue wavy lines on sides of snout, cheek, and opercle. Opercular flap stiff, short, black in center, edged in pale or yellow tinge that extends forward to form light borders above and below. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Long slender gill rakers, 11 to 14, longest about six times greatest width, thicker in large adults. Lateral line complete. Scales small. Lateral scales, (41)45 to 50(53); rows above lateral line, 8 to 10; rows below lateral line, 16 to 19; cheek scale rows, 6 to 9; caudal peduncle scale rows, 23 to 25; pectoral rays, 13 to 15. Pharyngeal arches narrow, strong, with small, thin, sharply pointed to conically blunt teeth. Teeth on palatine bone. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue, rarely a few teeth present) bones (Bailey 1938; Childers 1967; Trautman 1981; Becker 1983; Page and Burr 1991; Etnier and Starnes 1993; Mabee 1993). Size and age: Size at age 1 is highly variable among habitats and across latitudes, ranging from 30 to 165 mm TL (median 51 mm). Large individuals measure 150 to 225 mm TL, weigh 85 to 200 g, and attain age 5+ to 6+ (maximum 310 mm TL, age 10+) (Carlander 1977; Page and Burr 1991; Pflieger 1997; Quist and Guy 2001). World angling record, 0.96 kg, Missouri (IGFA 2006). Growth in mid-western prairie streams, where the species is common, is associated positively with abundance of instream wood, likely reflecting cover or food resources associated with wood (Quist and Guy 2001). Males may grow faster and perhaps live longer than females, but differences can be slight, becoming most apparent in individuals >100 mm TL (Hubbs and Cooper 1935; Carlander 1977). Coloration: Black, relatively short, ear flap with conspicuous light border. Wavy, often narrow, blue lines radiate from mouth across sides of snout onto cheek and opercle (often broken on opercle). Yellow, orange, or whitish margins on second dorsal fin, caudal fin lobes, anal fin, and pelvic fins, more prominent in breeding males. Blue-green above and on sides; iridescent, narrow, pale blue stripes on body scales interspersed with yellow metallic flecking; the blue stripes often broken into irregular mottling or spotting, especially posteriorly; sometimes with dusky bars on side. White to yellow belly (Hunter 1963; Page and Burr 1991; Etnier and Starnes 1993; Jenkins and Burkhead 1994). Native range: The green sunfish is native to the east-central United States, west of the Appalachians from the Great Lakes, Hudson Bay, and Mississippi River Basins from New York and Ontario to Minnesota and South Dakota and south to the Gulf Slope drainages from the Escambia River, Florida, and Mobile Basin, Georgia and Alabama, west to the lower Rio Grande basin, Texas, and northern Mexico (Page and Burr 1991; Miller 2005). The species has been widely introduced and is established over much of the United States including Atlantic and Pacific Slope drainages and Hawaii (Page and Burr 1991; Fuller et al . 1999). Introduced populations of green sunfish in Atlantic Slope and in western US waters are implicated in suppression and decline of native game and nongame fishes as well as frogs and salamanders (Lemly 1985; Fuller et al . 1999; Dudley and Matter 2000; Moyle 2002). Habitat: The green sunfish is a highly successful, aggressive, competitive species occurring in a variety of habitats including clear to turbid headwaters, sluggish pools of large streams, isolated, dry season–stream pools, and shallow shorelines of lakes, ponds, and reservoirs (Werner and Hall 1977; Werner et al . 1977; Capone and Kushlan 1991; Page and Burr 1991; Etnier and Starnes 1993; Taylor and Warren 2001; Smiley et al . 2005). In pond experiments, the presence of green sunfish induced dramatic shifts in foraging habitat and prey types in co-occurring congeners (Werner and Hall 1977, 1979). Green sunfish also invoke strong antipredator behaviors in aquatic insects and amphibians (e.g., Sih et al . 1992; Krupa and Sih 1998). The species is among the most tolerant of Lepomis to adverse conditions of high turbidity (<3500 FTU), low dissolved oxygen (DO) (<1 ppm), high temperatures (average critical thermal maxima 37.9◦ C, acclimated at 26◦ C), and high alkalinity (>2000 ppm, pH = 9.5) (McCarraher 1971; Horkel and Pearson 1976; Matthews 1987; Smale and Rabeni 1995a,b; Beitinger et al . 2000). Marked individuals in streams may show little movement, being recaptured in home pools over multiple seasons or longer (Gerking 1950, 1953; Smithson and Johnston 1999). Homing ability after short-distance displacement, exploratory pool-to-pool movements (>400 m), and long-distance movements (>16 km) are

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documented (Funk 1957; Hasler and Wisby 1958; Kudrna 1965; Smithson and Johnston 1999). The green sunfish is also an adept disperser and “pioneer” species, rapidly colonizing streams recovering from seasonal drying or drought, moving into and out of seasonally inundated floodplain habitats, and often invading ponds or small lakes (Ross and Baker 1983; Matthews 1987; Kwak 1988; Capone and Kushlan 1991; Etnier and Starnes 1993; Taylor and Warren 2001; Moyle 2002; Adams and Warren 2005). Food: The adult green sunfish is a solitary ambush predator whose large mouth allows it to feed on larger food items at a given body size than most congeners (Sadzikowski and Wallace 1976; Werner and Hall 1977). The size-adjusted gape area of the species is the second largest within the genus (see L. gulosus; Collar et al . 2005a,b). The adult diet consists primarily of aquatic insects, particularly large odonate, mayfly, and beetle larvae; fish; crayfish; and terrestrial invertebrates, but a variety of other taxa are consumed (e.g., snails, and unusually, a bat) (Minckley 1963; Applegate et al . 1967; Etnier 1971; Sadzikowski and Wallace 1976; Werner 1977; Carlander 1977; Lemly 1985). Young green sunfish transition from an initial diet of microcrustaceans to larger invertebrates and at 50 to 99 mm TL increase consumption of crayfishes and fishes (Applegate et al . 1967; Mittelbach and Persson 1998). High volumes of plant material in stomachs are indicative of considerable foraging for invertebrates, such as odonate larvae, associated with vegetation (Etnier 1971; Sadzikowski and Wallace 1976). In laboratory studies, activity levels are largely diurnal, peaking at dusk and dawn, but the presence in stomachs of prey only available after dark indicates a nocturnal or at least crepuscular component to feeding (Etnier 1971; Beitinger et al . 1975; Langley et al . 1993). Green sunfish produce a chemical alarm substance that induces antipredatory behaviors in conspecifics, regardless of size. In contrast, chemical alarm cues from sympatric heterospecific fishes induce antipredator responses in juvenile green sunfish and foraging responses in adults (Golub and Brown 2003). Reproduction: Maturity is reached at age 1+ to 3+ at a minimum size of about 45 to 76 mm TL (Carlander 1977). The combined effects of increased photoperiod (15 hours) and rising temperature in spring control prespawning gonadal development (Kaya and Hasler 1972; Smith 1975). Under controlled photoperiods, temperature, and food availability, 6-month old individuals (60–100 mm TL) can be induced to spawn (Smith 1975). Spawning is protracted (mid-May to early August), with the initiation of spawning depending in part on latitude (Hunter 1963; Kaya and Hasler 1972; Carlander 1977; Pflieger 1997). Nest building and spawning begin as water temperatures increase to 20◦ C, and peak spawning occurs between about 20 and 28◦ C (Hunter 1963). Nesting activity decreases and gonadal regression occurs as water temperatures remain over 28◦ C for extended periods (Hunter 1963; Kaya 1973). Males excavate nests by caudal sweeping. Nests are about 31 cm in diameter and usually placed over gravel in open, shallow areas (4–35 cm water depth, rarely 100 cm). Within a population, small males nest later in the season and in shallower water than large males (Hunter 1963), and at similar latitudes, individuals from stunted populations become ripe 2 to 4 weeks later than nonstunted populations (Childers 1967). Nests may be widely spaced (up to 30 m apart) when population densities are low but can also be placed rim-to-rim in crowded colonies (Hunter 1963; Childers 1967; Pflieger 1997). Colony formation closely parallels that of other colonial-nesting Lepomis (e.g., Bietz 1981; Neff et al . 2004), but whether colonial nesting occurs in the absence of habitat limitation is not completely clear (Hunter 1963; Childers 1967; Pflieger 1997). Spawning events are synchronous in colonies, occurring at intervals of 8 to 9 days over the spawning season; males may nest five or more times in succession during this period, and females presumably participate in multiple spawning events (three to six) over the season (Hunter 1963). Nest-guarding males produce gruntlike sounds as part of courtship (Gerald 1971); other reported courtship, spawning, and nest defense behaviors appear typical for the genus (Hunter 1963; Childers 1967). During nest building and spawning, males are territorial, aggressive, and even combative toward other males, females, and nest predators; only the most persistent spawning-ready females are allowed into the nest. Activity of spawning males is intensified. For example, in a 10-minute period a guardian male completed five spawning acts, made ten defensive forays outside the nest, threatened his neighbor once, and rim-circled 39 times (Hunter 1963). During a given spawning event, females attempt to mate (and likely do mate) with multiple males, but appear most attracted to males that are already spawning. Occasional intrusions by an ostensible female between a spawning pair (Hunter 1963) suggest the presence of sneaker males in at least some populations, but alternative mating systems in green sunfish are unconfirmed. Mature ovarian eggs are 0.8 to 1.0 mm in diameter, and fertilized eggs are 1.0 to 1.4 mm in diameter (mean 1.23 mm) (Meyer 1970; Kaya and Hasler 1972; Taubert 1977). Depending on their size, females may carry 2000 to 10,000 eggs (Beckman 1952 in Moyle 2002), but little else is apparently known about fecundity. The adhesive, fertilized eggs hatch in 2.1 days at 23.8◦ C (1.3 days at 27.1◦ C) (Childers 1967). Newly hatched larvae are 3.6 to 3.7 mm TL, and, depending on temperature, larvae are free swimming for about 3 to 6 days after fertilization at 4.6 to 6.3 mm TL (Childers 1967; Meyer 1970; Taubert

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1977). Successful males guard and vigorously defend the nest, eggs, and larvae for 5 to 7 days, but earlier abandonment of nests is common (Hunter 1963). Nest associates: Red shiner, Cyprinella lutrensis (Pflieger 1997); redfin shiner, Lythrurus umbratilis (Hunter and Wisby 1961; Hunter and Hasler 1965; Snelson and Pflieger 1975; Trautman 1981; Johnston 1994a,b; Pflieger 1997); golden shiner, N. crysoleucas (suspected, Pflieger 1997); Topeka shiner, Notropis topeka (Pflieger 1997). Freshwater mussel host: Confirmed host to A. ligamentina, Anodonta suborbiculata, Elliptio complanata, Glebula rotundata, Lampsilis altilis, Lampsilis bracteata, Lampsilis cardium, Lampsilis higginsii , Lampsilis hydiana, L. reeveiana, Lasmigona complanata, Ligumia subrostrata, L. recta, Megalonaias nervosa, P. grandis, V. iris, Villosa vibex , and U. imbecillis (Young 1911; Lefevre and Curtis 1912; Tucker 1927, 1928; Stern and Felder 1978; Trdan and Hoeh 1982; Parker et al . 1984; Waller and Holland-Bartels 1988; Howells 1997; Barnhart and Roberts 1997; Haag et al . 1999; O’Dee and Watters 2000). Putative host to A. plicata, Lampsilis radiata, Lasmigona compressa, S. undulatus, Toxolasma lividus, and Toxolasma parvus, (unpublished sources in OSUDM 2006). Conservation status: Although abundant in few natural habitats (e.g., Pflieger 1997; Quist and Guy 2001), the green sunfish is widespread and stable within its native range. Similar species: Other Lepomis lack yellow-orange edges on the fins and the black spot at posterior base of the dorsal fin (except the bluegill) and have a smaller mouth (except the warmouth). The bluegill has long, pointed pectoral fins, and the warmouth has dark red-brown lines radiating posteriorly from the eye, mottling on the side, and a small patch of teeth on the tongue (Page and Burr 1991). Systematic notes: Lepomis cyanellus forms a sister pair with L. symmetricus, and the pair represents the second largest and the smallest Lepomis, respectively (Near et al . 2004, 2005). Comparative studies of variation across the range of L. cyanellus are lacking. Importance to humans: The green sunfish rarely reaches a size of interest to anglers other than children. Because of its propensity to invade, overpopulate, stunt, and compete with other fishes in ponds or small lakes, green sunfish are considered a pest by those attempting to maintain quality bluegill-bass sport fisheries. The species is commonly used by anglers as live bait on trotlines, set hooks, and jugs for catfishes. Hybrids between a female green sunfish and a male bluegill (known as “hybrid bream”) are cultured and stocked in ponds to create put-and-take fisheries. The hybrids are aggressive, fast growing, and easy to catch, and if properly managed, produce excellent results (Ross 2001).

13.8.3 Lepomis gibbosus (Linnaeus) 13.8.3.1 Pumpkinseed Characteristics: See generic account for general characteristics. Body, deep, compressed, often almost disk-like, depth about 0.40 to 0.53 of SL. Mouth moderate, terminal, slightly oblique, supramaxilla absent, upper jaw extends almost to, or to, anterior edge of eye. Wavy blue lines on cheek and opercle of adult. Bold dark brown wavy lines or orange spots on soft dorsal, anal, and caudal fins. Opercular flap stiff, short, with black center bordered in white or yellow with a prominent red (males) to yellowish (females) semicircular spot at posterior edge (often pale or yellowish in young). Pectoral fin long, sharply pointed, usually reaching far past eye when laid forward across cheek. Short, thick gill rakers, about 12; scarcely longer than wide. Lateral line complete. Lateral scales, (35)37 to 44(47); rows above lateral line, 6 to 8; rows below lateral line, 12 to 15; cheek scale rows, 3 to 6; caudal peduncle scale rows, 17 to 21; pectoral rays, 11 to 14. Pharyngeal arches extremely broad, heavy with large rounded, molariform teeth. Teeth present or absent on palatine bone. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Scott and Crossman 1973; Trautman 1981; Becker 1983; Page and Burr 1991; Mabee 1993; Jenkins and Burkhead 1994). Size and age: Size at age 1 is highly variable among habitats and across latitudes, ranging from 15 to 99 mm TL (median 40 mm). Large individuals measure 150 to 225 mm TL, weigh about 150 to 200 g, and attain age 6 to 9+ (maximum 400 mm TL, age 10+) (Carlander 1977; Page and Burr 1991; Fox 1994). World angling record, 0.63 kg, New Mexico (IGFA

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2006). Pumpkinseed populations sympatric with bluegill show increased early growth rates, despite reduced resources, relative to populations allopatric with bluegill, providing evidence for counter-gradient evolutionary selection for rapid growth (Arendt and Wilson 1997, 1999). Older males tend to be larger than same-age females, and subtle differences in body form occur between male and female pumpkinseed (Deacon and Keast 1987; Brinsmead and Fox 2002). Coloration: Ear flap black with light border, marked with bright red or yellow-orange spot on posterior edge. Wavy, usually wide, blue lines radiate from mouth across sides of snout onto cheek and opercle of adult. Many bold dark brown wavy lines or orange spots on second dorsal, caudal, and anal fins. Olive above and on sides with many gold and yellow flecks. Adults blue-green, spotted with orange; dusky chainlike bars mark sides of young and adult female; white to red-orange below (Page and Burr 1991). Native range: The pumpkinseed is native to Atlantic Slope drainages from New Brunswick south to the Edisto River, South Carolina, and to the Great Lakes, Hudson Bay, and upper Mississippi River Basins from Quebec and New York west to southeast Manitoba and North Dakota and south to northern Kentucky and Missouri. The species has been widely introduced and is established over much of the United States and southern Canada, including some Pacific Slope drainages (Scott and Crossman 1973; Page and Burr 1991; Fuller et al . 1999; Moyle 2002). Habitat: The pumpkinseed inhabits vegetated lakes and ponds and quiet vegetated pools of creeks and small rivers (Page and Burr 1991). Lake- and stream-dwelling populations differ in subtle aspects of body morphology (e.g., pectoral fin length), differences attributed to adaptation to lentic versus lotic environments (Brinsmead and Fox 2002). Juvenile and adult pumpkinseed tend toward lengthy occupancy of home activity areas (about 11 m2 to 1.12 hectares, respectively) and can home to those areas when displaced (Shoemaker 1952; Hasler et al . 1958; Kudrna 1965; Reed 1971; Fish and Savitz 1983; Wilson et al . 1993; Coleman and Wilson 1996; McCairns and Fox 2004). Food: The pumpkinseed is a highly specialized molluscivore, feeding primarily on snails by crushing them between heavy pharyngeal jaw bones that are equipped with molariform teeth, enlarged muscles, and specialized neuromuscular adaptations (Lauder 1983a,b, 1986; Hambright and Hall 1992; Wainwright and Lauder 1992; Huckins 1997). Adults also feed heavily on dipteran, mayfly, and caddisfly larvae and beetles, and also ingest cladocerans, amphipods, isopods, ostracods, larval odonates, and terrestrial invertebrates (Seaburg and Moyle 1964; Sadzikowski and Wallace 1976; Keast 1978; Laughlin and Werner 1980; Deacon and Keast 1987; Huckins 1997; Jastrebski and Robinson 2004). Young age-0 fish (>18 mm TL) consume a diet predominated in biomass by zooplankton and chironomids (Hanson and Qadri 1984), and at least in pond experiments, their combined predatory effects can change zooplankton composition (Hambright and Hall 1992). As they grow from 35 to 100 mm TL, the young transition gradually from a diet of soft-bodied littoral invertebrates to high numbers of snails (Keast 1978; Mittelbach 1984a; Keast and Fox 1990; Osenberg et al . 1992; Huckins 1997). Full development of the pharyngeal snail-crushing apparatus of pumpkinseeds depends on repeated, consistent consumption of snails (Bailey 1938). Pharyngeal bones and musculature associated with snail crushing are substantially reduced in individuals in snail-poor lakes relative to individuals from snail-rich lakes (Wainwright et al . 1991; Mittelbach et al . 1992; Osenberg et al . 2004). In the summer, peaks in feeding occur in late afternoon and at dawn with reduced but notable feeding after midnight (Keast and Welsh 1968). In the fall, daylight feeding is low and feeding peaks occur between 2000 and 0400 hours (Johnson and Dropkin 1993). In summer, age-0 pumpkinseed feed from shortly after sunrise until sunset (Hanson and Qadri 1984). Periodic infrared videography of foraging pumpkinseed over 8 months revealed frequent nocturnal foraging, mediated by a switch from benthic picking during daylight to zooplanktivory at night (Collins and Hinch 1993). In support of these field observations, laboratory experiments indicate volumes searched and feeding rates on zooplankton decrease at light intensities ≤10 lux (Hartleb and Haney 1998). Pumpkinseeds produce a chemical alarm substance that induces antipredatory behaviors in conspecific juveniles (<45 mm SL), but depending on the concentration, elicits either antipredatory or foraging responses in conspecific adults (>95 mm SL) (Marcus and Brown 2003; Golub et al . 2005). Response of juveniles to alarm cues was diminished under weakly acidic conditions (pH 6.0) (LeDuc et al . 2003). Pumpkinseed also respond to chemical alarm cues of largemouth bass (and ostariophysan alarm chemicals), but the response is mediated by size and habitat complexity. Under conditions of low to intermediate habitat complexity, large pumpkinseed (>80 mm SL) exhibit foraging responses and small pumpkinseed antipredator responses to bass chemical alarm cues. In highly complex habitat, both large and small pumpkinseed show antipredator responses to bass chemical alarm cues (Golub et al . 2005).

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Lake-dwelling pumpkinseeds show subtle intra- or interpopulation differences in body form (e.g., body depth, fin length, gill raker spacing) that are strongly associated with specializations for pelagic or littoral feeding (Robinson et al . 1996; Robinson and Schluter 2000; Brinsmead and Fox 2002; Gillespie and Fox 2003; Jastrebski and Robinson 2004; McCairns and Fox 2004). Intermediate forms occur in both habitats but show reduced fitness in growth and body condition (Robinson et al . 1996). Evidence from parasite analyses and strong site fidelity in pelagic and littoral zone pumpkinseed morphs suggest that trophic divergence and habitat segregation come into play early in the life history and could potentially affect gene flow (Robinson et al . 2000; Jastrebski and Robinson 2004; McCairns and Fox 2004). Intrapopulation morphological divergence between trophic morphs occurs across a relatively broad geographic region (Robinson et al . 2000; Gillespie and Fox 2003; Jastrebski and Robinson 2004). Divergence is expressed in the absence of open-water competitors (i.e. bluegill or other Lepomis) (Robinson et al . 1993), but may also be mediated by complex interactions of a number of ecological factors (Robinson et al . 2000). Reproduction: Maturity is reached at age 1+ to 4+ at 65 to 130 mm TL. Within a population, females may mature earlier and at smaller sizes than males (Carlander 1977; Fox and Keast 1991; Fox 1994; Danylchuk and Fox 1994; Fox et al . 1997). Age and size at maturity, onset and duration of spawning, size of eggs, and energy allocated for reproduction are plastic, varying in different, but proximate habitats (e.g., beaver ponds and nearby lakes, adjacent lakes) or regionally. Trade-offs among somatic growth and reproductive timing and allocation are linked to energy limitations, resource uncertainty in highly variable environments, and presence of other Lepomis (Deacon and Keast 1987; Fox and Keast 1991; Danylchuk and Fox 1994; Fox 1994; Fox et al . 1997). Spawning is protracted (early May to August), the initiation of spawning depending in part on latitude and population size structure (Burns 1976; Carlander 1977; Danylchuk and Fox 1994; Fox and Crivelli 1998). Gonadal development in both sexes accelerates as water temperatures warm to 12.0◦ C and photoperiod lengthens to 13.5 hours (Burns 1976). A combination of long photoperiod (16 hours) and warm temperature (25◦ C) induces nest-building behaviors in males (Smith 1970). Nest building and spawning begin as water temperatures increase to 17◦ C, and peak spawning occurs between about 20 and 22◦ C, but continues to at least 26◦ C (Miller 1963; Fox and Crivelli 1998; Cooke et al . 2006). Onset of spawning is later and the spawning season is longer in stunted than in nonstunted populations (Danylchuk and Fox 1994). Males excavate nests by caudal sweeping and uprooting and carrying away plants; conspecific or other centrarchid nests are often appropriated or reused (Ingram and Odum 1941; Miller 1963). Nests are 30 to 80 cm in diameter, at water depths of 18 to 50 cm (rarely >1 m), and often near simple cover (e.g., log, stump, boulder). Sand or small rocky substrates are chosen most often for nest sites, but a variety of substrates are used (Breder 1936; Ingram and Odum 1941; Colgan and Ealey 1973; Popiel et al . 1996). Nests are usually solitary (>1 m apart), but groups of two or three nests may be rim to rim (Ingram and Odum 1941; Miller 1963; Clark and Keenleyside 1967; Colgan and Ealey 1973). Nest-guarding males produce popping sounds as part of courtship of females and aggression toward conspecific males and other Lepomis (Gerald 1971; Ballantyne and Colgan 1978a,b,c). Other reported courtship, spawning, and nest defense behaviors appear typical for the genus (e.g., aggressive displays, courtship circles, rim circling) (Miller 1963; Steele and Keenleyside 1971; Colgan and Gross 1977; Colgan et al . 1981; Becker 1983; Clarke et al . 1984). Sneaker males are documented for pumpkinseed (Gross 1979), but in one surveyed population, guardian males sired about 85% of the larvae in their nests (range, 43–100%) (Rios-Cardenas and Webster 2005). Mature ovarian eggs average 1.11 mm diameter (Gross and Sargent 1985), but 0.6 to 1.0 mm and 0.8 to 1.2 mm diameters are ranges reported for fertilized or fertilized and water-hardened eggs, respectively (Hardy 1978; Cooke et al . 2006). Female batch fecundity increases with weight, but varies significantly among populations (Deacon and Keast 1987). The relationship between batch fecundity (Y) and total weight (X) is described by the linear function, log10 Y = −0.0592 + 1.9461 log10 X (n = 37, R 2 = 0.20, one of four equations from Deacon and Keast 1987). At 48 g (128 mm TL), a female can potentially produce 5455 mature eggs in a single batch (range: 2451 at 20 g and 98 mm TL to 10,633 eggs at 126 g and 184 mm SL, respectively). The white to transparent, adhesive, fertilized eggs hatch in about 3 days at 18 to 22◦ C, larvae at hatching are 2.6 to 3.1 mm TL, and larvae reach swim-up at about 5.2 mm TL, some 4 days after hatching (Miller 1963; Colgan and Gross 1977; Hardy 1978). The cycle for the successful guardian male typically takes 10 days (range 6–15 days) with 2 days for territory establishment and nest construction, three for spawning and egg guarding, four for larval guarding, and one for fry dispersal and nest abandonment. Territoriality and aggressiveness in guardian males is highest during egg guarding and early larval stages, diminishing as larvae grow (Colgan and Gross 1977; Colgan and Brown 1988; Cooke et al . 2006). Males may lose on average 6.3% of their body weight from spawning to fry dispersal (Rios-Cardenas and Webster 2005). Females can participate in one to six spawning periods (average two to three) over a 7- to 8-week period, during which an estimated

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12 to 40% of prespawning body mass is allocated to reproduction (Fox and Crivelli 1998). In lakes, fry apparently initially disperse offshore but return to littoral habitats in late summer (Keast 1978; Brown and Colgan 1984, 1985a; Mittelbach 1984a; Rettig 1998). Nest associates: Golden shiner, N. crysoleucas (Shao 1997). Freshwater mussel host: Confirmed host to Alasmidonta varicosa, P. grandis, and U. imbecillis (Trdan and Hoeh 1982; Fichtel and Smith 1995). Putative host to Alasmidonta undulata, A. plicata, E. complanata, L. radiata, Lampsilis siliquoidea, L. reeviana, Lasmigona costata, L. recta, P. cataracta, and S. undulatus (unpublished sources in OSUDM 2006). Conservation status: The pumpkinseed is secure across most of its native range but is considered critically imperiled in Manitoba and vulnerable in Illinois (NatureServe 2006), which include the northwestern and southern peripheries of its native distribution, respectively (Page and Burr 1991). Similar species: All other Lepomis have shorter, rounded pectoral fins, except the redear sunfish and bluegill. The redear sunfish and bluegill lack bold spots on the second dorsal fin and wavy blue lines on the gill cover (Page and Burr 1991). Systematic notes: Lepomis gibbosus is basal to a clade consisting of L. microlophus, and the sister pair L. punctatus– L. miniatus (Near et al . 2004, 2005). Based on shared behavioral and morphological specializations for snail crushing, L. gibbosus was proposed previously as sister to L. microlophus (Bailey 1938; Mabee 1993). Frequencies of nuclearencoded allozyme loci across populations in four east-central Ontario watersheds revealed low genetic variability, but populations were significantly substructured genetically. The patterns in genetic variation are congruent with hypothesized post-Pleistocene recolonization routes (Fox et al . 1997). Comparative studies of variation across the entire range of L. gibbosus are lacking, but anal and dorsal ray counts and differences in size and age at maturity show east to west differences (Scott and Crossman 1973; Fox et al . 1997). Importance to humans: Although not often reaching a size of interest to many anglers, the pumpkinseed can contribute substantially to the sport fishery catch in northern lakes (e.g., Minnesota, Eddy and Underhill 1974; Wisconsin, Becker 1983), at least historically contributed to the Great Lakes commercial fishery catch (Scott and Crossman 1973), and is an easy and delightful catch for young anglers. The flesh is white, flaky, sweet, and delicious, comparable to that of the bluegill. The species can be taken in late afternoons with light tackle on live bait, small dry flies, poppers, or wet fly trout patterns (Scott and Crossman 1973; Eddy and Underhill 1974; Becker 1983). The pumpkinseed is important ecologically, forming part of the food for many predatory fishes including important game fishes (e.g., black basses, walleye, yellow perch, and muskellunge) (Scott and Crossman 1973). Among northern North American freshwater fishes, the pumpkinseed is among the most striking in beauty and color (Jordan and Evermann 1923; Becker 1983). Because of their color and ease of keeping and breeding, the species is a prized aquarium fish in Europe (Goldstein 2000).

13.8.4 Lepomis gulosus (Cuvier) 13.8.4.1 Warmouth Characteristics: See generic account for general characteristics. Body relatively thick, robust, somewhat elongate, depth 0.4 to 0.5 of SL. Large, terminal oblique mouth, lower jaw projecting slightly, supramaxilla moderately large (>2 to ≤3 times length of maxilla), upper jaw extending well beyond anterior edge of eye to center of eye or beyond in adults. Dark red-brown lines (3–5) radiating posteriorly from snout and red eye. Opercular flap short, stiff, black with paler and often red-tinged border. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Long, thin gill rakers, 9 to 13, longest about four (adults) to six (young) times the greatest width. Lateral line complete. Lateral scales, 36 to 48; rows above lateral line, 6 to 9; rows below lateral line, 12 to 15; cheek scale rows, 5 to 7; caudal peduncle scale rows, 19 to 23; pectoral rays, 12 to 14. Pharyngeal arches narrow with bluntly conical teeth. Teeth on endopterygoid, ectopterygoid, palatine (villiform), and glossohyal (tongue, one patch) bones (Bailey 1938; Birdsong and Yerger 1967; Trautman 1981; Becker 1983; Etnier and Starnes 1993; Mabee 1993; Jenkins and Burkhead 1994; Boschung and Mayden 2004).

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Size and age: Size at age 1 is highly variable among habitats and across latitudes, ranging from 25 to 155 mm TL (median 55.5 mm TL). Large individuals measure 150 to 200 mm TL, weigh about 200 g, and attain age 5 to 7+ (maximum 310 mm TL, age 8+) (Carlander 1977; Page and Burr 1991). World angling record, 1.1 kg, Florida (IGFA 2006). Coloration: Ear flap short, black with yellow edges and posterior red spot (adult). Dark red-brown lines radiating from back of red eye. Olive brown above; dark brown mottling on back and upper side; often 6 to 11 chainlike dark brown bars on sides; cream to light yellow below; dark brown spots (absent on young) and wavy bands on fins. Breeding male boldly patterned on body and fins with a bright red-orange spot at base of second dorsal fin and black pelvic fins (Page and Burr 1991). Young and juveniles usually with a distinctive purplish sheen. Native range: The warmouth is native to the Great Lakes and Mississippi River Basin from western Pennsylvania to Minnesota and south to the Gulf of Mexico and the Atlantic and Gulf drainages from the Rappahannock River, Virginia, to, but apparently not including, the Rio Grande, Texas, New Mexico, and Mexico (Page and Burr 1991; Miller 2005). The species is an apparent recent (ca. 1966) natural immigrant in the waters of southern Ontario, where it is naturalized (Crossman et al . 1996). The warmouth has been introduced widely and is established over much of the United States, including some Pacific Slope drainages (Fuller et al . 1999; Moyle 2002). Habitat: The warmouth inhabits vegetated lakes, ponds, swamps, reservoirs, and quiet waters of slow-flowing streams, being most common, and often abundant, in lowland areas and rare in uplands (Larimore 1957; Holder 1970; Guillory 1978; Page and Burr 1991; Snodgrass and Meffe 1998). Individuals are most often solitary and usually associated with areas of dense vegetation, root wads, stumps, overhanging banks, or rock cavities over silt or mud substrates (Larimore 1957; Loftus and Kushlan 1987). Smaller warmouth (<127 mm TL) tend to remain in dense vegetation in shallow water, but larger individuals occur more often in deeper waters (Larimore 1957). Warmouth appear well adapted to the rigors of coastal plain wetland habitats of the southern United States. The species is tolerant of low DO levels and high turbidity, is adept at locating deep water refuge (e.g., alligator ponds) in response to seasonal drying of wetlands, and tolerates moderately brackish waters (<12.5 ppt) (Larimore 1957; Kushlan 1974; Loftus and Kushlan 1987; Killgore and Hoover 2001; Rutherford et al . 2001; Boschung and Mayden 2004). The physiological bases for or limits of these tolerances are unstudied. In a North Carolina swamp system, average movement for 20% of recaptured individuals was 5.0 km over 21 days. Notably, another 31% of recaptures moved 0.6 to 1.8 km (35–75 days at large), and 65% of marked individuals were never recaptured (Whitehurst 1981). Trap catches in the Okefenokee Swamp and Suwannee River suggested highest activity at night and peak movements in spring just before spawning (Holder 1970). Food: The warmouth is a solitary, opportunistic predator whose large mouth allows it to feed on larger food items at a given body size than congeners. The size-adjusted gape area of the species is the largest among Lepomis (Collar et al . 2005a,b). The adult (>125 mm TL) diet consists primarily of small fish (e.g., sunfishes, darters, pickerels, killifish, mosquitofish), crayfish, and odonate larvae, but a variety of other taxa are consumed (e.g., freshwater shrimp, isopods, mayflies, caddisflies) (McCormick 1940; Chable 1947; Larimore 1957; Germann et al . 1974; Guillory 1978). The largest adults (>200 mm TL) often feed almost exclusively on crayfishes (Guillory 1978). Young warmouth transition from an initial diet of microcrustaceans to invertebrates (e.g., midge and caddisfly larvae) and at about 75 mm TL begin increasing use of the larger prey dominating the adult diet (Larimore 1957; Germann et al . 1974; Desselle et al . 1978; Guillory 1978). Dawn and dusk samples in the summer suggest that most feeding occurs at or before dawn with little feeding in the afternoon (Larimore 1957). Reproduction: Maturity is reached at ages 1+ to 2+ at 57 to 152 mm TL (Larimore 1957; Germann et al . 1974; Guillory 1978). Spawning is initiated as water temperatures approach 21◦ C (as low as 15◦ C) and is protracted (April or May to July or August) with female ovary to body weight ratios peaking in late May to early June as water temperatures reach 27 to 29◦ C (Larimore 1957; Germann et al . 1974; Guillory 1978). Males excavate nests in a few hours by caudal sweeping, and depending on the time spent by the male, the nest may be a rather shapeless oval depression (about 10 cm × 20 cm) with only loose silt swept away or a deep, symmetrical circular depression (45 cm diameter, 13 cm deep). Nests are constructed at water depths of 15 to 152 cm (most <76 cm) and are often near simple cover (e.g., tree base, log, stump, boulder,) or on logs, roots, or mats of submerged plants. If available, small rocky substrates in silt-laden areas are chosen most often for nest sites and sand avoided, but in southern wetlands, nest bottoms often consist of tree leaves and needles swept free of silt. Bottom type appears less important than nearby cover for nest placement (Larimore 1957; Birdsong and Yerger 1967; Fletcher and Burr 1992). Nests are usually solitary (>4 m apart), but if habitat is limiting nests may be closely

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spaced (Carr 1940; Larimore 1957; Childers 1967). Courtship and spawning behaviors (based primarily on aquarium observations) appear typical for the genus (e.g., male aggressive displays, jaw gapes, opercular flares), but warmouth apparently do not rim circle; other than egg fanning by the male, no detailed observations are available on nest care or nest defense behaviors. During active courtship of a female, the body of a male becomes bright yellow and the eyes blood red in color, the change in colors requiring only 5 to 10 seconds. Only when the female is ready to lay eggs will she allow the male to guide her to the nest. In aquaria, a nest-guarding male will ultimately kill an unresponsive female (Larimore 1957). During paired circling of the nest (female near the center, male outside), the female jaw gapes a few times, violently jerks her body, and releases about 20 eggs while simultaneously thumping the male on the side in an apparent signal for him to release sperm. These behaviors are repeated sequentially for about 1 hour with brief pauses in between bouts, at which time males may use caudal sweeping to mix eggs into the substrate (Larimore 1957). Mature ovarian eggs (waterhardened) average 1.01 mm in diameter (Merriner 1971a). Mature females contain two or more egg class sizes throughout the spawning season (Larimore 1957; Germann et al . 1974). Batch fecundity increases with female size. The relationship between batch fecundity (Y) and total length (X) is described by the linear function, log10 Y = −1.6108 + 2.4859 log10 X (data from mean number of mature eggs of nine length classes, R2 = 0.85, Germann et al . 1974). At 195 mm TL, a female can potentially produce 12,078 mature eggs in a single batch (range: 6825 eggs at 155 mm TL to 20,238 eggs at 240 mm SL, respectively). Another estimate of batch fecundity is much lower (i.e. log10 Y = 0.1619 + 1.418 log10 X, where X is SL, Guillory 1978). The fertilized eggs are pale, amber-colored, and adhesive, hatching in about 1.5 days at 25.0 to 26.4◦ C (71.1 hours at 22.6◦ C, 33.9 hours at 26.9◦ C, and 32.5 hours at 27.3◦ C). Larvae at hatching are 2.3 to 2.9 mm TL and reach swim-up at about 4.7 to 7.6 mm TL, some 3 to 5 days after hatching (Larimore 1957; Childers 1967). After leaving the nest, young apparently do not form schools, but hide themselves in dense vegetation or other cover. Likewise, juvenile warmouth do not aggregate in large groups (Larimore 1957). Nest associates: Bluehead shiner, Pteronotropis hubbsi (Fletcher and Burr 1992). Freshwater mussel host: Confirmed host to A. suborbiculata, L. subrostrata, Toxolasma texasensis, and U. imbecillis (Stern and Felder 1978; Barnhart and Roberts 1997). Putative host to T. parvus (unpublished sources in OSUDM 2006). Conservation status: The warmouth is currently stable over most of its range (Warren et al . 2000; NatureServe 2006). Peripheral populations in Pennsylvania and West Virginia are considered imperiled, and recently naturalized populations in Ontario are listed as critically imperiled (NatureServe 2006), although the necessity for the latter status has been questioned (Crossman et al . 1996). Similar species: The green sunfish lacks dark lines radiating posteriorly from eye, lacks teeth on the tongue, and has a dark spot at the posterior base of the second dorsal fin (Page and Burr 1991). Systematic notes: Lepomis gulosus is basal to the sister pair L. symmetricus and L. cyanellus (Near et al . 2004, 2005). Mitochondrial DNA analyses revealed distinct eastern and western populations of L. gulosus, occurring along the Atlantic Slope through Florida to eastern tributaries of Mobile Basin and from the Tombigbee River westward, respectively (Bermingham and Avise 1986). L. gulosus has a checkered taxonomic and nomenclatural history (summary in Berra 2001), but comparative studies of variation across the range of the species are lacking. Importance to humans: Over much of its range, the warmouth is taken most often by bream or crappie anglers but usually not in abundance. Even so, warmouth can comprise a large part of the sport fish catch in habitats like the Okefenokee Swamp, Georgia, or Reelfoot Lake, Tennessee (Larimore 1957; Germann et al . 1974). Warmouth are quick to take an artificial lure or live bait. The species is an excellent table fish, the flavor and texture of the flesh being judged as intermediate between the bluegill and the largemouth bass (Larimore 1957).

13.8.5 Lepomis humilis (Girard) 13.8.5.1 Orangespotted sunfish Characteristics: See generic account for general characteristics. Body moderately deep, compressed, slab-sided, depth 0.38 to 0.45 of SL. Mouth moderately large, oblique, supramaxilla absent, upper jaw extends to, or just beyond, anterior edge of eye. Orange or red-brown wavy lines on cheek and opercle in adults. Opercular flap moderate to long (in adults),

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very flexible, usually angled upward with black center and wide, white to pale green, conspicuous border (flushed with orange in breeding males). Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Moderately thin gill rakers, 10 to 15, longest about five times greatest width. Enlarged, elongate sensory pits on preopercle and head between eyes, pits larger than any other Lepomis, width of each pit about equal to distance between pits. Lateral line complete or incomplete. Lateral scales, 32 to 42; cheek scale rows, 5; pectoral rays, 13 to 15. Pharyngeal arches narrow with sharply pointed teeth. Teeth on palatine bone. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Bailey 1938; Trautman 1981; Becker 1983; Mabee 1993; Ross 2001; Boschung and Mayden 2004). Size and age: Size at age 1 is highly variable among habitats and across latitudes, ranging from 23 to 86 mm TL (median 45 mm TL). Large individuals measure 75 to 125 mm TL, weigh <60 g, and attain age 3+ (maximum 177 mm TL, about 150 g, age 4+) (Barney and Anson 1923; Carlander 1977; Page and Burr 1991; TWRA 2006). Coloration: Black ear flap, usually angled upward, with conspicuous wide white, pale green, pale lavender, pinkish, or light crimson border. Olive above with bright orange (large male) or red-brown (female) spots on silver-green side. Orange (male) or red-brown (female) wavy lines on cheek and opercle. White to orange below; fins unspotted. Young with chainlike vertical bars and no spots on side. Breeding male brilliantly colored with red-orange spots on side; reddish orange eye, belly, anal fin, and dorsal fin edge; pelvic fins white to orange with black edge (Noltie 1990; Page and Burr 1991; Etnier and Starnes 1993). Native range: The orange-spotted sunfish is native to southwestern Lake Erie and Lake Michigan, the extreme headwaters of the Red River of the North (Hudson Bay drainage), and the Mississippi River Basin from Ohio to southern North Dakota and south to Louisiana and in Gulf Slope drainages from the Mobile Basin, Alabama, to the Colorado River, Texas (Page and Burr 1991). In historical times, the species expanded its range into southeastern Michigan and adjacent Ontario, northward in Wisconsin, and eastward across Indiana and Ohio, as agricultural activities converted formerly clear prairie-type streams into turbid plains-type streams (Trautman 1981; Holm and Coker 1981; Becker 1983; Noltie 1990; Bailey et al . 2004). The species has been introduced sporadically on the periphery of its native range, usually unintentionally as stock contaminant with other centrarchids (Fuller et al . 1999). Habitat: The orangespotted sunfish inhabits quiet pools of creeks and small to large, often turbid, rivers, as well as overflow swamps and backwaters of sluggish streams, natural lakes, and reservoirs (Noltie 1990; Page and Burr 1991; Etnier and Starnes 1993; Miranda and Lucas 2004). The species is rarely abundant but is most common in low-gradient habitats. The orangespotted sunfish is among the most tolerant of Lepomis to adverse conditions of low DO (<1 ppm) and high temperatures (average critical thermal maxima 36.4◦ C, acclimated at 26◦ C) (Matthews 1987; Smale and Rabeni 1995a; Beitinger et al . 2000). Food: The orangespotted sunfish is an opportunistic invertivore, feeding extensively on midge larvae, caddisfly larvae, hemipterans, and microcrustaceans, rarely consuming small fish (Barney and Anson 1923; Clark 1943; Noltie 1990). These primary diet items, along with aerial insects in stomachs, indicate both bottom and surface feeding (Clark 1943; Etnier and Starnes 1993). When exposed to different diets, orangespotted sunfish show subtle but measurable changes in morphology, primarily in head shape, suggesting diet as a strong determinant of trophic morphology (Hegrenes 2001). Reproduction: Maturity is reached at ages 1+ to 2+ at 30 to 50 mm TL (Barney and Anson 1923; Noltie 1990). Spawning is initiated as water temperatures approach 18◦ C and is protracted (April or May–late August) beginning 6 weeks earlier at southern (e.g., Louisiana) than at northern (e.g., Iowa) latitudes. Spawning is reported across a range of water temperatures from 24 to 32◦ C (Barney and Anson 1923; Cross 1967; Becker 1983; Noltie 1990). Ripe males and females are taken throughout the summer months. Scale growth increments suggest that fish hatched early in the spawning season obtain sexual maturation in August of the second year of life (age 1+) and those hatched latter delay maturation to early summer of the third year of life (age 2+) (Barney and Anson 1923). Males build nests at water depths of 30 to 61 cm, using caudal sweeping, pushing with the head, and fin undulations to remove overlying silt and mud, to ultimately form semicircular depressions about 15 to 18 cm in diameter and 30 to 40 mm deep with firm, exposed bottoms. Nests are colonial (<1.0 m apart) with males defending a territory of 30 to 60 cm (Barney and Anson 1923; Miller 1963; Cross 1967). Males actively court females by repeatedly rushing out to them and rapidly returning to the nest, while producing a series of gruntlike sounds (Gerald 1971). Other courtship, spawning, and nest-guarding behaviors appear typical for the genus (e.g., male

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aggressive displays, rim circling, egg fanning), but few detailed observations are available (Barney and Anson 1923; Miller 1963). Fecundity increases with female size, but it is unclear if available egg counts were based on total or mature ova in females (Barney and Anson 1923; Becker 1983). The relationship between fecundity (Y) and total length (X) is described by the linear function, log10 Y = −2.2596 + 2.9785 log10 X (data from Barney and Anson 1923, n = 28, R2 = 0.80, four likely partially spent females deleted). At 68 mm TL, a female can potentially produce 1580 eggs in a single batch (range: 138 eggs at 30 mm TL to 5776 eggs at 105 mm TL). The nearly transparent, amber to colorless, fertilized eggs are about 0.5 to 1.0 mm in diameter and hatch in about 5 days at 18.0 to 21.0◦ C (Barney and Anson 1923; Cross 1967; Becker 1983). Yolk-sac larvae and larvae (ages unstated) are 5.3 and 7.0 mm TL, respectively (Tin 1982). A reported hatching size of 10 mm TL (Barney and Anson 1923) seems much too large and needs verification. Nest associates: Red shiner, C. lutrensis (Pflieger 1997) and redfin shiner, L. umbratilis (Snelson and Pflieger 1975; Trautman 1981). Freshwater mussel host: Confirmed host to A. ligamentina, E. complanata, L. complanata, L. recta, and P. grandis (Young 1911; Arey 1932). Putative host to L. compressa and T. parvus (unpublished sources in OSUDM 2006). Conservation status: The orangespotted sunfish is secure throughout much of its native range (e.g., Warren et al . 2000), but peripheral populations in Michigan, West Virginia, and southwestern Ontario are considered imperiled (NatureServe 2006). Similar species: Other Lepomis with orange spots on the side have dark (blue or olive brown) sides and lack the wide white edge on the ear flap, the elongated sensory pores on the preopercle, and the enlarged sensory pores on top of the head (Page and Burr 1991). Systematic notes: Lepomis humilis forms a sister pair with L. macrochirus (Near et al . 2004, 2005). This sister pair represents the second smallest and the largest species, respectively, in the genus and interestingly, display near complete overlap in their geographic ranges (Page and Burr 1991; Near et al . 2004). Comparative studies of variation across the range of L. humilis are lacking. Importance to humans: The orangespotted sunfish does not reach a size of interest to most anglers. The species is reportedly a good bioassay animal and aquarium fish (Becker 1983; Schleser 1998), and ecologically, is suggested as a natural biological control for mosquitoes (Barney and Anson 1923).

13.8.6 Lepomis macrochirus Rafinesque 13.8.6.1 Bluegill Characteristics: See generic account for general characteristics. Deep, compressed body, depth 0.43 to 0.56 of SL. Mouth small, strongly oblique, supramaxilla absent, upper jaw rarely reaches anterior edge of eye. Large black spot at posterior of soft dorsal fin. Opercular flap moderate to long, flexible, black at margins, lacks distinct pale or light edges. Pectoral fin long and pointed, tip usually reaches past eye when laid forward across cheek. Long, slender gill rakers, 13 to 16, longest about four to five times the greatest width. Lateral line complete. Lateral scales, (38)41 to 46(50); rows above lateral line 7 to 9; rows below lateral line, 14 to 17; cheek scale rows, 4 to 7; caudal peduncle scale rows, 18 to 21; pectoral rays, 12 to 15. Pharyngeal arches moderately wide with thin, sharply pointed teeth. Teeth present or absent on palatine. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Bailey 1938; Keast and Webb 1966; Trautman 1981; Becker 1983; Mabee 1993; Jenkins and Burkhead 1994; Boschung and Mayden 2004). Size and age: Size at age 1 is highly variable among habitats and across latitudes, ranging from 18 to 122 mm TL (median 51 mm TL) (Carlander 1977). Interestingly, mean size by fall of age-0 bluegill in lakes is the same across a broad range of latitudes (ca. 55 mm TL), suggesting that northern bluegill grow as rapidly in the first summer as southern bluegill (Garvey et al . 2003). Local factors, such as abundance of specific prey types (cladocerans versus invertebrates), proportion of littoral habitat, and exploitation can differentially affect growth in small (ca. 50 mm TL) and large bluegills (Shoup et al . 2007). Large individuals can exceed 200 mm TL, 200 g, and attain age 6+ to 7+, although individuals in northern populations tend

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to live longer than their faster growing southern counterparts (maximum about 410 mm TL, 567 g, and age 11+) (Carlander 1977; Page and Burr 1991). World angling record, 2.15 kg, Alabama (IGFA 2006). Parental males grow faster than females and show subtle, but detectable differences in body shape (deeper bodied, longer paired fins) (Ehlinger 1991). Cuckolder, nest-parasitic males grow slower and mature earlier than parental males (Dominey 1980; Gross 1982; Drake et al . 1997; Ehlinger 1997; Ehlinger et al . 1997). Coloration: Ear flap, short to moderately long, black to margin. Large black spot at rear of second dorsal fin. Dark bars (chainlike in young and absent in turbid water) or plain sides on body. Adult with blue sheen overall and two blue streaks from chin to edge of gill cover. Olive back and side with yellow and green flecks; paler on belly to brassy yellow on breast; clear to dusky fins. Breeding male with blue, blue-olive, or blue-green head and back; red-orange breast; black pelvic fins (Page and Burr 1991; Jenkins and Burkhead 1994). Native range: The bluegill is native to the St. Lawrence-Great Lakes system and Mississippi River Basin from Quebec and New York to Minnesota and south to the Gulf of Mexico and in Atlantic and Gulf Slope drainages from the Cape Fear River, Virginia, to the Rio Grande River, Texas and Mexico (Page and Burr 1991; Miller 2005). The species has been widely introduced and is now established and often exceedingly abundant in suitably warm waters of most of North America (Fuller et al . 1999; Moyle 2002; Miller 2005) and other continents (e.g., South Africa, Korea, Japan), where because of stunting and competition with native fishes, the species is often considered a pest (De Moor and Bruton 1988; Jang et al . 2002; Kawamura et al . 2006). Nonnative bluegills are implicated in the decline of the native Sacramento perch in California and other native fishes in the western United States (Marchetti 1999; Moyle 2002). Habitat: The bluegill inhabits all types of warmwater lacustrine habitats (e.g., oligohaline estuaries, swamps, lakes, ponds, reservoirs, canals) as well as pools of creeks and small to large rivers. In lacustrine environments, whether natural or man made, the bluegill is often the most abundant centrarchid (Desselle et al . 1978; Becker 1983; Page and Burr 1991; Peterson and Ross 1991; Jenkins and Burkhead 1994). The species is among the most tolerant Lepomis to adverse conditions of low DO (<1.0 ppm) and high temperatures (average critical thermal maxima 40.4–41.4◦ C, acclimated at 35◦ C) (Moss and Scott 1961; Matthews 1987; Smale and Rabeni 1995a,b; Beitinger et al . 2000; Miranda et al . 2000; Killgore and Hoover 2001). However, RNA–DNA ratios indicate bluegill from hypoxic habitats (1.22–3.04 mg/l DO, always <2 mg/l at night) show reduced growth relative to individuals from normoxic habitats (>3.2 mg/l at night) (Aday et al . 2000). Bluegill can survive winter conditions of <1◦ C and <2 mg/l DO (Magnuson and Karlen 1970; Petrosky and Magnuson 1973; Knights et al . 1995), but winter anoxia, often associated with iceover of shallow lakes, limits their distribution in northern lakes (Tonn and Magnuson 1982; Rahel 1984). Bluegill indigenous to fresh or brackish waters showed no preference in salinity over a range of 0 to 10 ppt (Peterson et al . 1993). Coastal juvenile bluegill showed no influence on growth or osmoregulatory characteristics (e.g., hematocrit activity) at 10 ppt salinities and fed diets containing up to 4% NaCl (Musselman et al . 1995). Home activity area of bluegills in streams generally extends about 50 to 500 linear meters, and marked individuals are often recaptured in the same stream section throughout the summer or even over multiple seasons or years (Gunning and Shoop 1963; Whitehurst 1981; Gatz and Adams 1994). Although observed in few individuals, bluegills ranged as far as 17 linear km in Tennessee streams. About 20% of successive recaptures were ≥250 m apart over 4 years (Gatz and Adams 1994), and in a North Carolina swamp stream bluegills moved 3.4 km in 33 days (Whitehurst 1981). Home range of radio-tagged bluegill (>160 mm TL) over summer and early fall in an Illinois lake ranged from 0.15 to 0.72 ha (occupied from 12–34 days) with core use areas of 0.11 to 0.60 ha (Fish and Savitz 1983). Large, radio-tagged bluegill (>200 mm TL) tracked from April to September in a shallow Great Plains lake showed no difference in diel activity patterns or habitat use and showed low site fidelity, except during spawning (Paukert and Willis 2002; Paukert et al . 2004). Home areas ranged from 0.13 to 172 ha (core areas of 0.01 to 27.2 ha); individuals moved up to 1.1 km/h, but most rates of movement ranged from 30 to 100 m/h. Bluegills (40 to 125 mm TL) shifted from using the mid-depth zone (1.5–6.0 m) in summer to wintering in the shallow (<1.5 m) vegetated littoral zones of a Florida lake (Butler 1989), may move onshore after sunset and offshore after sunrise (Baumann and Kitchell 1974; Helfman 1981), and may emigrate in fall to avoid extreme winter conditions (Knights et al . 1995; Parsons and Reed 2005). Food: The bluegill is a generalist, travel-and-pause predator that can routinely exploit zooplankton in pelagic habitats and larger vegetation-dwelling invertebrates in littoral habitats (Werner et al . 1981, 1983; Ehlinger and Wilson 1988; Schramm

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and Jirka 1989; Dewey et al . 1997). The adult diet consists of an array of invertebrates including amphipods, cladocerans, larval dipterans, mayflies, and odonates, and terrestrial insects (e.g., McCormick 1940; Chable 1947; Seaburg and Moyle 1964; Applegate et al . 1967; Etnier 1971; Sadzikowski and Wallace 1976; Werner 1977; Schramm and Jirka 1989; Dewey et al . 1997; VanderKooy et al . 2000). Notably, bluegill shift from pelagic zooplanktivory to littoral invertivory at small sizes (12–15 mm SL), and then can shift back to zooplanktivory after a period of growth (>80 mm SL) (Werner 1969; Werner and Hall 1988; Rettig 1998). Surprisingly for a primarily diurnal feeder, laboratory-measured activity in bluegill decreased shortly after dawn, peaked about 1.5 hours after darkness, and remained above daylight levels throughout most of the night (Langley et al . 1993; see also Reynolds and Casterlin 1976a; Shoup et al . 2003). Diet studies indicate that nighttime feeding can be minimal with peak feeding often occurring after sunrise and at dusk (Sarker 1977; Keast and Fox 1992), but foraging in summer can be nearly continuous over a 24-hour period (Seaburg and Moyle 1964; Keast and Welsh 1968; Sarker 1977; Dewey et al . 1997). Peak feeding times are size mediated, occurring latter in the day for smaller (<95 mm) than larger individuals (105–135 mm TL) (Baumann and Kitchell 1974). The bluegill is an effective, adaptive predator. The species uses a highly stereotyped travel-and-pause foraging tactic, which is combined with a generalist but plastic morphology and an elaborate behavioral flexibility. These traits allow bluegills to switch foraging habitats, quickly learn new foraging behaviors (e.g., increased pause duration, faster pursuit), and successfully exploit new prey in response to changes in prey abundance, intraspecific and interspecific competition, or predation risk (e.g., Werner and Hall 1974, 1977, 1979, 1988; Mittelbach 1981, 1984b; Gotceitas and Colgan 1987, 1988; Ehlinger 1989, 1990; Colgan et al . 1981; Gotceitas 1990a,b; Wildhaber and Crowder 1991; Dugatkin and Wilson 1992; Mittelbach and Osenberg 1993; Rettig and Mittelbach 2002; Shoup et al . 2003). Intense, often selective, predation by bluegills can directly affect the size, abundance, and composition of zooplankton, which indirectly alters the density and composition of phytoplankton communities (Vanni 1986; Hambright et al . 1986; Mittelbach and Osenberg 1993). Similarly, bluegill predation on macroinvertebrates includes reductions in the biomass, abundance, and size of invertebrates and is often influenced by complex interspecific interactions with other centrarchids and size-mediated interactions with conspecifics (Crowder and Cooper 1982; Morin 1984a,b; Mittelbach 1988; McPeek 1990; McPeek et al . 2001; Rettig and Mittelbach 2002). The presence of the bluegill also can have dramatic effects on predator avoidance and other behaviors of amphibians (Jackson and Semlitsch 1993; Werner and McPeek 1994). In a mutualistic feeding role, bluegills serve as facultative cleaners by picking off ectoparasites, loose scales, and necrotic tissue from a host (i.e. other bluegill, Micropterus spp., striped mullet, Mugil cephalus, manatees, and perhaps large ictalurids) (Spall 1970; Sulak 1975; Powell 1984; Loftus and Kushlan 1987; Moyle 2002). Multiple observations tend to occur in the same locations, suggesting that bluegill establish permanent cleaning stations as documented in marine fishes. In the Everglades, groups of bluegills follow alligators through the water and trail closely behind lake chubsuckers (Erimyzon sucetta) as they forage along the bottom, presumably feeding on prey disturbed by these animals (Loftus and Kushlan 1987). Bluegills also join similar-sized Florida bass and together they group hunt for small fishes in clumps of vegetation (Annett 1998). The bluegill is well equipped visually to detect small or mobile prey (Hairston et al . 1982; Williamson and Keast 1988). In ample light (>10−6 W/cm2 ), bluegill can detect prey items 0.3 to 0.7% brighter than the visual background (Hawryshyn et al . 1988) with greatest detection ability in a forward-projecting pie-shaped wedge in the horizontal plane of the fish (Walton et al . 1994). Visual acuity increases by about 50% as bluegill increase in size from 35 to 60 mm SL (Hairston et al . 1982), but the rate of increase in acuity diminishes in fish >60 mm SL (Breck and Gitter 1983; Li et al . 1985; Walton et al . 1992, 1994, 1997). Increased acuity with growth confers visual access to increasing volumes of search space, and the ability to see increasing numbers of prey (Vinyard and O’Brien 1976; Gardner 1981; Hairston et al . 1982; Breck and Gitter 1983; Walton et al . 1994). For example, estimated visual and search volumes of bluegill viewing a 2-mm zooplankter increase by nearly three orders of magnitude from about 0.1 l at 8 mm SL to 90 l at 50 mm SL (Walton et al . 1994); the estimated visual volume more than doubles from 200 to >400 l for a 3-mm zooplankton target as fish size increases from 60 to 160 mm TL (Breck and Gitter 1983). Decreased light or increased turbidity dramatically influences feeding (and predator detection) in bluegills. Below illuminance of 10 lux, reactive distance to small zooplankton prey (1–3 mm) decreases at successively lower light levels, such that regardless of prey size, reactive distances at low light (0.7 lux) are reduced to 3 to 4 cm (Vinyard and O’Brien 1976). Similarly, reactive distances to a larger visual target (largemouth bass, 290 mm TL) decrease from about 175 cm at 3340 lux to <50 cm at 1.5 lux (Howick and O’Brien 1983). In ample light and clear water, bluegills (and perhaps other Lepomis) can recognize an object as prey (or predator) at greater distances than do largemouth bass (Howick and

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O’Brien 1983; Miner and Stein 1996). As light decreases to twilight levels, bluegills >40 mm TL lose their reactive distance advantage over largemouth bass such that only smaller bluegills can locate largemouth bass first under low light intensities (Howick and O’Brien 1983). Under constant light, detection ability of bluegills decreases as a log or exponential function of increasing turbidity for small zooplankton prey and large predators, respectively, but interactions of light and turbidity with feeding success are complex (Vinyard and O’Brien 1976; Gardner 1981; Miner and Stein 1993). Bluegills show subtle differences in intrapopulation body morphology. In lakes, differences in body morphology are associated with foraging and predator avoidance in littoral or open-water habitats. Bluegills from littoral habitats have deeper bodies, longer paired fins, and more posteriorly attached pectoral fins than those in open water (Ehlinger and Wilson 1988; Chipps et al . 2004). The open-water form also has a modified foraging behavior (decreased pause duration) (Ehlinger 1990). Relative to the littoral form, the open-water form shows increased predator avoidance behaviors (i.e. schooling defense), but in cover, predators take three times longer to capture the littoral form than the open-water form (Chipps et al . 2004). The feeding behavior and ecology of the bluegill are among the most extensively documented of any North American freshwater fish. Only a cursory review of this important body of literature is possible here. The interested reader is encouraged to consult papers cited herein and others, including, for example, Werner (1974), O’Brien et al . (1976), Werner et al . (1977), Bulow et al . (1978, 1981), Keast (1978, 1985a,b,c), Vinyard (1980), Savino and Stein (1982, 1989a,b), Mittelbach (1983), Brown and Colgan (1986), Butler (1988), Johnson et al . (1988), Osenberg et al . (1988, 1992), DeVries et al . (1989), DeVries (1990), Gotceitas and Colgan (1990), Savino et al . (1992), Schaefer et al . (1999), Harrel and Dibble (2001), Wildhaber (2001), Yonekura et al . (2002), McCauley (2005), and Spotte (2007). Reproduction: Maturity varies with sex, male alternative life history strategy, intraspecific competition, and latitude and can be reached at age 0+ (first summer of life) to age 6+ at a minimum size of about 73 to 172 mm TL and 15 to 82 g (Morgan 1951a,b; Carlander 1977; Gross 1982; Ehlinger et al . 1997). Time of maturation between the sexes can vary greatly even among lakes at similar latitudes, and cuckolder males within populations mature at an earlier age and size than parental males (Gross 1982; Ehlinger 1991; Drake et al . 1997). In ponds, small male bluegill are inhibited from maturing in the presence of large males, regardless of food availability, and laboratory evidence suggests that large parental males produce a pheromone that inhibits maturation in small males (Aday et al . 2003, 2006). Increased photoperiod (12–16 hours) and rising temperature in the spring controls prespawning gonadal development (Banner and Hyatt 1975; Mischke and Morris 1997). Spawning is protracted (mid-May–mid-August) (Morgan 1951a,b; Avila 1976; Gross 1982), particularly in southern Florida where reproduction extends from late February or early March through September with pauses in activity for up to 3 weeks (Clugston 1966). Nest building and spawning begin as water temperatures increase to 20◦ C, and spawning continues up to about 31◦ C (Morgan 1951a,b; Banner and Hyatt 1975); males in stunted populations initiate nest building several weeks later than males in nonstunted populations (Jennings et al . 1997; Aday et al . 2002). Males excavate saucer-shaped depressional nests by caudal sweeping (Morgan 1951a,b; Miller 1963; Avila 1976; Gross 1982), which alters substrate composition by removing small particles (<2 mm) to expose hard substrates or larger coarse gravel and pebble substrates (>8 mm diameter). Coarse nest substrates are associated with increased survival of fry (Bain and Helfrich 1983). Nests are placed in open, shallow areas (10–190 cm water depth, rarely >3.0 m), usually away from cover (Carbine 1939; Morgan 1951b; Clugston 1966; Avila 1976; Ehlinger 1999). Median depths of nest placement suggest that males may be able to sense ultraviolet radiation, and place nests deeper in high underwater ultraviolet radiation environments, which can damage developing embryos (Guti´errez-Rodriguez and Williamson 1999). Bluegills nest in crowded colonies that can contain hundreds of abutting nests, and these colonies often contain other nesting Lepomis spp. (Childers 1967; Avila 1976; Gross 1982; Cargnelli and Gross 1996). In colonies, spawning events (five to eight per spawning season) are synchronous, occurring at intervals of 10 to 14 days; males may nest one or more times in a season (Neff and Gross 2001), and females presumably participate in multiple spawning events. Colony formation is a definite social aggregation because it occurs in the absence of habitat limitation (Gross and MacMillan 1981). Colonial nesting affords decreased predation on offspring through cumulative nest defense (e.g., predator mobbing, Dominey 1981, 1983; Gross and MacMillan 1981) and decreased fungal infection of eggs (Cˆot´e and Gross 1993), both of primary benefit to parental males located centrally rather than peripherally in a colony (Neff et al . 2004). Nevertheless, a consistent but small proportion of bluegill males within a population nest solitarily (Avila 1976; Ehlinger 1999; Neff et al . 2004). These males are in better condition than colonial males but possess smaller ear tabs than centrally located males. Solitary nesters experience decreased cuckoldry relative to colonial males and show a nesting success equivalent to centrally located

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males, but higher success than peripherally located males (Gross 1991; Neff et al . 2004), suggesting that females do not discriminate between solitary and central males. Guardian males produce gruntlike sounds as part of courtship of females and aggression toward conspecific and other Lepomis males (Gerald 1971; Ballantyne and Colgan 1978a,b,c). Other male courtship, spawning, and nest defense behaviors are well documented and typical for the genus (e.g., aggressive displays, courtship circles, rim circling, paired nest circling, egg fanning) (e.g., Morgan 1951b; Miller 1963; Avila 1976; Colgan et al . 1979; Gross 1982; Clarke et al . 1984; Coleman et al . 1985; Coleman and Fischer 1991; Stoltz and Neff 2006). On the female entering a nest, a 15- to 90-minute spawning bout ensues in which the female releases small groups of eggs in a series of dips into the nest; females may dip hundreds of times during a bout (Avila 1976; Gross 1991; Fu et al . 2001). Males control the rate of dips by biting the female (Gross 1991). Males mate sequentially with several females (rarely with two females simultaneously) during synchronous spawning events (usually <1 day), resulting in accumulations of 4600 to 61,000 eggs/nest (Carbine 1939; Avila 1976; Gross 1982, 1991; Cargnelli and Gross 1996). Although discouraged by the male, spawning females frequently succeed in eating a portion of their predecessor’s eggs (Gross and MacMillan 1981). Mature ovarian eggs average from 1.09 to 1.30 mm diameter and fertilized, water-hardened eggs 1.2 to 1.4 mm in diameter (Morgan 1951b; Meyer 1970; Merriner 1971a; Hardy 1978; Gross and Sargent 1985; Cooke et al . 2006). Fecundity increases with female size. The relationship between potential batch fecundity (Y) and total length (X) is described by the linear function, log10 Y = −3.39794 + 3.4512 log10 X (mean numbers of 18 length class means for 91 females, R2 = 0.83, data from Morgan 1951b). At 165 mm TL, a female can potentially produce 17,990 mature eggs in a single batch (range: 5021 eggs at 114 mm TL to 45,575 eggs at 216 mm TL, respectively). The adhesive, fertilized eggs hatch in 2.1 days at 23.8◦ C (1.3 days at 27.1◦ C) (Childers 1967). Newly hatched larvae are 2.2 to 3.7 mm TL, and depending on temperature, larvae are free swimming about 3 to 4 days after hatching at a size of 4.30 to 5.70 mm TL (Childers 1967; Meyer 1970; Anjard 1974; Taubert 1977). Fry size at dispersal is correlated negatively with spawn date and hence, varies within a single population and spawning season (e.g., 4.3–6.7 mm) (Cargnelli and Gross 1996). Males guard and vigorously defend the nest, eggs, and larvae for about 7 days, but earlier abandonment of nests is common (see subsequent, Neff and Gross 2001; Neff 2003ab). Relatively large decreases in body weight (about 11%) and declines in lipid energy reserves occur in guardian males during the parental care period when feeding is reduced or curtailed (Avila 1976; Coleman et al . 1985; Coleman and Fischer 1991). During nest guarding, males with large broods sustain egg fanning for longer periods and more intensively defend the fry than males with small broods (Coleman et al . 1985; Coleman and Fischer 1991). Alternative mating strategies are highly developed in male bluegills. Both sneaker and satellite male morphs are only known in a single well-studied population of bluegill in Lake Opinicon, Ontario (Gross 1982), and presumable satellite equivalents (female mimics) were described from a New York lake (Dominey 1980). However, sneaker male morphs occur widely in populations of bluegill (Ehlinger 1997; Drake et al . 1997). Parasitic males can outnumber parental males 6:1, are excellent sperm competitors (80% fertilization rate), and are preferred by females, which release up to three times more eggs with the cuckolder than if alone with the guardian male (Fu et al . 2001; Neff 2001; Burness et al . 2004). Cuckolders reduce guardian male paternity in colonies by as much as 40% (average 23.1%), but their proportion of successfully fertilized eggs, relative to guardian males, decreases in colonies as their frequency reaches and exceeds numbers optimizing their fertilization success (Gross 1991; Philipp and Gross 1994). In an evolutionary response to intense cuckolding, guardian male bluegill apparently assess perceived paternity during the egg guarding stage through visual cues (presence of sneakers), and if perceived sneaker paternity is high, the guardian male decreases egg care or even abandons and cannibalizes eggs shortly after spawning (Neff and Gross 2001; Neff 2003a,b). Later in the broodguarding phase, the guardian male apparently assesses actual paternity (combined sneaker and satellite male fertilizations) through olfactory cues released by hatchlings and again adjusts his level of parental care, often resulting in a second wave of filial cannibalism and brood abandonment if actual cuckolding is high (Neff and Gross 2001; Neff and Sherman 2003, 2005; Neff 2003a,b). Given that guardian males can distinguish their fry from unrelated offspring (Neff and Sherman 2003), they may be able to selectively forage on unrelated fry while continuing to provide care to their fry (Neff 2003b). Nest associates: Golden shiner, N. crysoleucas (DeMont 1982). Freshwater mussel host: Confirmed host to Amblema neislerii , A. plicata, Elliptio buckleyi , Elliptio fisheriana, Elliptio icterina, Fusconaia masoni , G. rotundata, L. bracteata, L. cardium, L. higginsii, L. siliquoidea, Lampsilis straminea claibornensis, M. nervosa, P. grandis, S. undulatus, U. imbecillis, Villosa lienosa, and Villosa villosa (Howard 1914, 1922; Coker

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et al . 1921; Penn 1939; Trdan and Hoeh 1982; Parker et al . 1984; Waller and Holland-Bartels 1988; Hove et al . 1997; Howells 1997; Keller and Ruessler 1997; O’Dee and Watters 2000; O’Brien and Williams 2002; Rogers and Dimock 2003). Putative host to Anodontoides ferussacianus, E. complanata, E. hopetonensis, L. reeveiana, Lampsilis satura, L. teres, L. compressa, L. costata, L. recta, Pleurobema sintoxia, and T. parvus (unpublished sources in OSUDM 2006). Conservation status: The bluegill is secure throughout its range (Warren et al . 2000; NatureServe 2006). The morphological and genetic variation across the entire native range of this fish is poorly known, despite its considerable importance in fisheries management and compelling evidence of geographic differentiation (e.g., Avise and Smith 1974, 1977; Felley and Smith 1978; Felley 1980). Further, the species is still widely stocked with little or no concern for brood stock origin or effects on genetic integrity of native bluegill stocks or other native fishes. Similar species: The redear sunfish lacks a large, dark spot in the second dorsal fin and has a red edge on the ear flap and short gill rakers (Page and Burr 1991). Systematic notes: Lepomis macrochirus forms a sister pair with L. humilis (Near et al . 2004, 2005). The bluegill is polytypic. Three subspecies are generally recognized, but the geographic ranges and diagnostics of all forms are not well defined (Hubbs and Allen 1943; Hubbs and Lagler 1958; Avise and Smith 1974, 1977; Felley 1980; Page and Burr 1991). Populations on the Florida peninsula, colloquially known as coppernose bluegill (Ross 2001), differ morphologically (broader lateral bars and red fins) and genetically from the nominate subspecies L. m. macrochirus. Intergradation between the two occurs from the Ochlockonee River (eastern Gulf Coast drainage) north along the Atlantic Slope drainages to South Carolina (Avise and Smith 1974, 1977; Felley 1980). The name applied to the Florida form is L. m. mystacalis. The name L. m. purpurescens, although traditionally applied to the Florida form (Hubbs and Allen 1943), is associated with a type locality in North Carolina and is a synonym of L. m. macrochirus (Gilbert 1998). The name L. m. speciosus is applied to populations in Texas and Mexico (Hubbs and Lagler 1958; Page and Burr 1991). Lepomis m. macrochirus occupies the remainder of the native range. A color variant, known locally as the “handpaint brim,” occurs in the Apalachicola River valley in Florida (Felley and Smith 1978). Importance to humans: Because of their fearlessness, inquisitiveness, color, and activity, bluegill are seen, recognized, and enjoyed by more of the fishing and nonfishing public than probably any other species of freshwater fish (Scott and Crossman 1973). To many, nearly any Lepomis encountered is dubbed a “bluegill.” The bluegill probably accounts for more individual catches than any other gamefish in North America (Etnier and Starnes 1993), and for decades, the largemouth bass and bluegill have formed the core predator–prey species combination in sport fisheries management of warmwater ponds, lakes, and reservoirs (Bennett 1948; Swingle 1949). Historically, the species formed part of the commercial “sunfish” catch in natural lakes such as the Great Lakes and Reelfoot Lake, Tennessee (Schoffman 1945; Scott and Crossman 1973). The bluegill is a scrappy fighter that readily takes an array of small artificial flies, spinners, or natural baits (e.g., crickets, earthworms, or even dough balls). They attack the bait in groups, bite hard, and fight hard, creating a challenging catch for the experienced flyfisher, the cane pole enthusiast, or as a child’s first catch. The species is an excellent-tasting table fish, the flesh being white and slightly sweet (Scott and Crossman 1973; Etnier and Starnes 1993; Ross 2001).

13.8.7 Lepomis marginatus (Holbrook) 13.8.7.1 Dollar sunfish Characteristics: See generic account for general characteristics. Deep, compressed body, depth 0.5 of SL. Mouth small, terminal, oblique, supramaxilla small (>3 times and ≤4 times length of maxilla), upper jaw not extending posteriorly past anterior edge of eye. Wavy blue lines on cheek and opercle of adult. Opercular flap long, flexible, usually slanted upward, black in center, but often flecked with silver-green blotches, edged with white or pale green, lower and upper borders of equal width. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Short, thick, knoblike gill rakers, 9 to 10, longest about equal (adults) to two (young) times greatest width. Lateral line complete. Lateral scales, (34)37 to 40(44); rows above lateral line, 5 to 6; rows below lateral line, (12)13 to 14(15); cheek scale rows, 3 to

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4(6); caudal peduncle scale rows, (18)19(21); pectoral rays, (11)12 to 13. Pharyngeal arches narrow with sharply pointed teeth. No teeth on endopterygoid, ectopterygoid, palatine, or glossohyal (tongue) bones (Bailey 1938; Barlow 1980; Etnier and Starnes 1993; Mabee 1993). Size and age: Average 57 mm TL at age 1. Large individuals measure 95 mm TL and attain age 4+ or more (maximum 127 mm TL, age 6+) (Lee and Burr 1985; Page and Burr 1991; Winkelman 1993; Etnier and Starnes 1993). Mean male length is greater than that of same-age females (Winkelman 1993). Coloration: Similar to longear and northern longear sunfish but lateral line is colored brick red. Breeding male bright red, marbled and spotted with blue-green, and often with large silver-green flecks accenting dark center of ear flap (Page and Burr 1991). Native range: The dollar sunfish occurs in Atlantic and Gulf Slope drainages (mostly below the Fall Line) from the Tar River, North Carolina, to the Brazos River, Texas, and the Mississippi Embayment from western Kentucky and eastern Arkansas, south to the Gulf of Mexico (Page and Burr 1991). The species is most common in the southeastern United States, becoming increasingly uncommon in the western part of its range (Robison and Buchanan 1984; Loftus and Kushlan 1987; Page and Burr 1991; Wolfe and Prophet 1993; Snodgrass et al . 1996; Pflieger 1997; Marcy et al . 2005). Habitat: The dollar sunfish inhabits sand- and mud-bottomed wetlands, oxbows, or other swamplike habitats as well as the brushy pools of lowland creeks and small to medium rivers (Page and Burr 1991). The species is most often associated with small, low-gradient headwater streams, side channels of streams, beaver ponds, and periodically isolated floodplain wetlands (Meffe and Sheldon 1988; Etnier and Starnes 1993; Paller 1994; Snodgrass et al . 1996; Snodgrass and Meffe 1998). The dollar sunfish is one of the most abundant, but smallest, species of Lepomis in the Florida Everglades, where it is almost always associated with dense vegetation and reaches peak numbers in sawgrass marshes and marsh prairies (Loftus and Kushlan 1987). Removal of aquatic vegetation by grass carp (Ctenopharyngodon idella) in a eutrophic Texas reservoir resulted in almost complete elimination of the dollar sunfish (Bettoli et al . 1993). Food: The dollar sunfish is an opportunistic invertivore. The primary dietary items are midge larvae, microcrustaceans, terrestrial insects, snails, and oligochaetes (Chable 1947; McLane 1955; Lee and Burr 1985; Sheldon and Meffe 1993). Large amounts of detritus, filamentous algae, and terrestrial insects in stomachs indicate bottom-to-surface feeding (Etnier and Starnes 1993). Dollar sunfish leave stream channels to presumably forage on floodplains inundated during short-term spring flood events (Ross and Baker 1983). Reproduction: Maturity is reached at age 1+ at a minimum size of about 60 mm SL (Lee and Burr 1985). Spawning is protracted, occurring from April to September in Florida (McLane 1955) and May to July or August in North and South Carolina (Lee and Burr 1985; Winkelman 1996; Marcy et al . 2005). In the Carolinas, peak spawning occurs from mid-May to late June or July (Lee and Burr 1985; Winkelman 1996). Males use caudal sweeping to remove silt and organic debris from a variety of substrates to form small, shallow depressions (30 cm diameter), usually <2 m from shore at depths of 10 to 50 cm (Winkelman 1996). Nests may be solitary (>1 m apart) or in dense colonies of 20 or more closely spaced nests (Lee and Burr 1985; Mackiewicz et al . 2002; Marcy et al . 2005). The agonistic courtship and other reproductive behaviors of guardian males are apparently typical of other Lepomis, but observations are not extensive or detailed (Lee and Burr 1985; Winkelman 1996). Genetic analyses indicate that males spawn on average with 2.5 females (range 1–7) in a given spawning event and that about 95% of offspring in nests are sired by the guardian male. One nest takeover and one instance of cuckoldry by a neighboring nesting male were detected in 23 nests examined, but no evidence of nest parasitism by nonparental males was detected by paternity analysis or gonadal examination (Mackiewicz et al . 2002). The entire cycle of egg and larval guarding is about 6 days (Winkelman 1996). Colonial spawning in a North Carolina pond was asynchronous, continuing long after eggs were present in the nest and resulting in some males simultaneously guarding eggs and two previous broods. Nests produced about 150 to 200 larvae, and larvae reached 10 mm TL after 1 month (Lee and Burr 1985). Depending on reproductive stage of the nest, guardian males differentially adjusted retreat times from the nest in response to avian predator models (aerial and wading). Males returned to the nest sooner when offspring were present than when nests were empty, indicating awareness of a threat to their survival but a willingness to accept greater risk to protect their current brood (Winkelman 1996). Nest associates: Bluenose shiner, Pteronotropis welaka (Johnston and Knight 1999).

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Freshwater mussel host: None known (but see Stern and Felder 1978). Conservation status: The dollar sunfish is considered secure throughout most of its range, but is regarded within several states, particularly those on the periphery of the range, as vulnerable (Arkansas, Oklahoma, North Carolina) or critically imperiled (Kentucky) (NatureServe 2006). The species was likely much more widespread and abundant historically than it is now in those lowland areas subjected to stream channelization, wetland drainage, and intensive agricultural use (e.g., eastern Arkansas, western Kentucky, western Tennessee) (Robison and Buchanan 1984; Burr and Warren 1986; Etnier and Starnes 1993). Similar species: Within the range of the dollar sunfish, any longear-like sunfish occurring in nonflowing, low-gradient, or swamplike habitats is likely a dollar sunfish, although longear sunfish and dollar sunfish are taken together, especially in streams draining the eastern Mississippi Embayment (Burr and Warren 1986; Page and Burr 1991; Etnier and Starnes 1993). The longear sunfish usually has 13 to 14 pectoral rays and 5 to 7 cheek scale rows. The northern longear sunfish does not co-occur with the dollar sunfish and has a red spot on the ear flap. The redbreast sunfish lacks blue spots on the sides and has rows of red-brown spots on the upper sides, a longer narrower ear flap that is black to the edge, and usually 14 pectoral rays (Barlow 1980; Page and Burr 1991). Systematic notes: Lepomis marginatus is included in a clade with L. peltastes and L. megalotis (Near et al . 2004, 2005), but relationships among these species are unresolved. Interestingly, nuclear-encoded allozyme frequency data from a limited number of populations indicated that L. marginatus is genetically more similar to L. megalotis breviceps and L. m. aquilensis than to L. m. megalotis or L. peltastes (Jennings and Philipp 1992a). In contrast, phenetic analysis of 47 morphological and meristic characters indicated that L. marginatus (Louisiana and North Carolina samples) is most similar to its allopatric relative L. peltastes (Barlow 1980). Comparative studies across the range of L. marginatus are lacking, but polytypy is indicated from phenetic analyses of morphological characters (Barlow 1980), differences in opercular tab pigmentation (Page and Burr 1991; Etnier and Starnes 1993), and differences in breeding color patterns described by hobbyists (Wolff 2005). Importance to humans: Although not reaching a size of interest to panfish anglers, the dollar sunfish, where it occurs commonly, is an ecological indicator of relatively undisturbed lowland and wetland ecosystems.

13.8.8 Lepomis megalotis (Rafinesque) 13.8.8.1 Longear sunfish Characteristics: See generic account for general characteristics. Deep, compressed body, depth 0.43 to 0.45 of SL. Mouth moderately large, terminal oblique, supramaxilla small (>3 times and ≤4 times length of maxilla), upper jaw reaches posteriorly from beyond anterior of eye to just about center of eye. Wavy blue lines on cheek and opercle of adult. Opercular flap long, flexible (flared at end in large individuals), usually oriented horizontally (adult) or slanting upward (young), black in center with white edges, lower and upper edges of equal width, bordered above and below by blue line. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Short, thick, knoblike gill rakers, 12 to 14, longest about equal (adults) to twice (young) greatest width. Lateral line complete. Lateral scales, (31)36 to 48(50); rows above lateral line, (5)6 to 8(9); rows below lateral line, (11)14 to 15(19); cheek scale rows, (4)5 to 6(8); caudal peduncle scale rows, (16)18 to 23(25); pectoral rays, (11)13 to 14(15). Pharyngeal arches narrow with sharply pointed teeth. No teeth on endopterygoid, ectopterygoid, palatine, or glossohyal (tongue) bones (Bailey 1938; Barlow 1980; Trautman 1981; Mabee 1993; Boschung and Mayden 2004). Size and age: Size at age 1 is highly variable among habitats and across latitudes, ranging from 21 to 114 mm TL (median 47 mm TL). Individuals rarely exceed 155 mm TL or 100 g, and few live beyond age 6+ (maximum about 240 mm TL, 227 g, and age 9+) (Bacon 1968; Carlander 1977; Page and Burr 1991; Etnier and Starnes 1993; Jennings and Philipp 1992c). World angling record, 0.79 kg, New Mexico (IGFA 2006). Parental males grow faster than females (Carlander 1977; Jennings and Philipp 1992c). Coloration: Ear flap long, black in adult, edged in white, bordered above and below by blue lines. Numerous, wavy blue lines on sides of snout, cheek, and opercle. Young with olive back and side speckled with yellow flecks, often with

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chainlike bars on sides, white below. Adult dark red above, bright orange below, marbled and spotted with blue; clear to orange and blue, unspotted fins. Breeding males are among the most brilliantly colored North American fishes, with contrasting bright reddish orange and blue body, red eye, orange to red median fins, and blue-black pelvic fins (Page and Burr 1991). Nape with reddish stripe in upper Arkansas and Missouri River populations, and at least some populations in the upper White River, Missouri, lack the light border on the ear flap (Pflieger 1971; Barlow 1980; Goddard and Mathis 1997). Native range: The longear sunfish is native to the Mississippi River Basin west of the Appalachian Mountains from Indiana west to eastern Illinois and south to the Gulf of Mexico and to Gulf Slope drainages from the Choctawhatchee River, Florida, west to the Rio Grande, Texas, southern New Mexico, and northeastern Mexico (Page and Burr 1991; Miller 2005). The species is generally common, and often the most abundant Lepomis in upland or clear streams throughout its range. The species has expanded its range in recent decades north and westward in the Missouri River, Missouri, as a likely result of clear water conditions imposed on that system by upstream reservoirs (Pflieger 1997). The longear sunfish has been introduced sparingly outside its native range and is established in the upper Ohio River basin (New and Kanawha, above the Falls, rivers), the Atlantic Slope (Potomac River drainage and Maryland Coastal Plain), upper Rio Grande (New Mexico), and perhaps, the Pacific Slope of Mexico (Rio Yaqui) (Fuller et al . 1999; Miller 2005). Habitat: The longear sunfish inhabits rocky and sandy pools of headwaters, creeks, and small to medium rivers (Page and Burr 1991) and can thrive along shorelines of reservoirs (Bacon 1968; Gelwick and Matthews 1990; Bettoli et al . 1993; Etnier and Starnes 1993; Pflieger 1997). In some rivers, the longear sunfish can be the most abundant centrarchid (Gunning and Suttkus 1990). The species is tolerant of low DO (e.g., 100% survival at <1 ppm for 3 days) and high water temperatures (critical thermal maxima >34◦ C) (Matthews 1987; Smale and Rabeni 1995a,b; Beitinger et al . 2000). In streams, many individuals use restricted home activity areas (<100 m) over several seasons (or years) and displaced individuals can home over short distances apparently using olfactory cues (Gerking 1953; Gunning 1959, 1965; Gunning and Shoop 1963; Huck and Gunning 1967; Fentress et al . 2006). Even so, short (>200 m) interhabitat and long-distance (<15 km) exploratory movements are not uncommon, the species can quickly repopulate drought affected streams or defaunated stream reaches, and large individuals in streams appear to desert home activity areas in fall, presumably to migrate to wintering areas (Funk 1957; Boyer 1969; Berra and Gunning 1972; Matthews 1987; Lonzarich et al . 1998, 2000; Warren and Pardew 1998; Smithson and Johnston 1999; Fentress et al . 2006). A spring branch along Jacks Fork River, Missouri, serves as a winter thermal refuge for large numbers of longear sunfish. Lowest use of the spring branch occurs from April to October when adjacent river temperatures exceed those of the spring branch (13.5◦ C) and highest use occurs during cold periods when the spring waters exceed river temperatures. During cold, but not warm, periods, biomass and size of individuals in the spring branch are larger than those of individuals remaining in the river. Mark-recapture results suggest the existence of two populations of longear sunfish, one consisting of permanent spring branch residents and another that migrates to the spring branch during cold periods and back to the river during warm periods (Peterson and Rabeni 1996). Food: The longear sunfish is an opportunistic invertivore. Adults are principally benthic predators on larval midges, mayflies, and caddisflies but also consume a variety of other aquatic insects and terrestrial invertebrates as well as small fish, fish eggs (e.g., Micropterus and Pomoxis), isopods, amphipods, crayfishes, and gastropods (Minckley 1963; Applegate et al . 1967; Boyer 1969; Cooner and Bayne 1982; Angermeier 1985; Shoup and Hill 1997). Young longear sunfish (<50 TL) transition from an initial diet predominated by microcrustaceans and some aquatic insect larvae to increasing use of aquatic and terrestrial insects (50–100 mm TL). Surface insects can contribute substantially to the diet of the largest longear sunfish (>100 TL) (Applegate et al . 1967; Cooner and Bayne 1982; Angermeier 1985), and the species is highly efficient at capturing zooplankton or floating prey in flowing water (up to 18 cm/s; Schaefer et al . 1999). Feeding rates are initially high in spring, are relatively stable over much of the summer, and decline in October, a pattern attributed to decreasing availability of aquatic insect prey (Angermeier 1985; Kwak et al . 1992). Over a series of diel studies (May to October), feeding peaks occurred near dusk and dawn but some feeding occurred continuously over 24-hour periods (Bowles and Short 1988; Kwak et al . 1992). In late winter, stream-dwelling individuals collected well before dawn had apparently electively consumed nocturnally drifting amphipods (Bowles and Short 1988). In a laboratory tank, longear sunfish cleaned external fish parasites from a live, heavily infested flathead catfish, suggesting that, like the bluegill, they may serve in nature as commensal cleaners of other fishes (Spall 1970).

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Reproduction: Maturity is reached at age 1+ to 3+ at a minimum size of about 60 mm TL in females and 100 to 140 mm TL for guardian males (Boyer 1969; Carlander 1977; Jennings and Philipp 1992c), but sneaker male phenotypes can mature at age 1+ and 40 to 85 mm TL (Jennings and Philipp 1992c). Spawning is protracted and may include up to six relatively discrete nesting periods occurring from late May to mid-July or August at intervals of about 12 days (Huck and Gunning 1967; Boyer and Vogele 1971; Carlander 1977; Jennings and Philipp 1994). Observations in Missouri reservoirs indicate that spawning temperatures range from 22 to 28◦ C with nest abandonment occurring if water temperature abruptly decreased below or increased above this range (Witt and Marzolf 1954; Boyer and Vogele 1971), but in a Louisiana stream, nesting occurred at 29 to 31◦ C (Huck and Gunning 1967). Flood events (and presumably lowered water temperatures) delayed initiation of spawning, resulted in high nest abandonment, and decreased brood survival in an Illinois stream (Jennings and Philipp 1994). Vitellogenesis was suppressed in wild females exposed to unbleached Kraft mill effluents (paper mills) in the Pearl River, Mississippi, and the number of spawning cycles appeared to be lower than in unexposed females. No reproductive suppression effects were detected in males (Fentress et al . 2006). Males excavate nests by caudal sweeping. The shallow, roughly circular depressional nests range from about 33 to 89 cm diameter, are 3 to 7 cm deep, and are usually placed in areas free of brush or vegetation over sand or gravel at water depths of 20 to 150 cm (up to 3.4 m in reservoirs, Huck and Gunning 1967; Boyer and Vogele 1971; Mueller 1980). Within a population, nesting males tend to be larger than non-nesting males, even though the smaller non-nesting males are mature. Of males nesting, successful males are on average larger than unsuccessful males, suggesting that females prefer large males (Jennings and Philipp 1992b). If male size is equal, females prefer males with longer ear tabs (Goddard and Mathis 1997). Nests are most often colonial (e.g., 2 to 45 nests, <1 m apart), presumably affording subordinate guardian males more access to females, but solitary nests are not uncommon (Boyer and Vogele 1971; Jennings and Philipp 1992b). In some populations, solitary males tend to be larger than colonial males, and their nesting success is equivalent to that of colonial males (Jennings and Philipp 1992b), but in other populations solitary males tend to be smaller than colonial nesters (Boyer 1969). Spawning events in colonies are asynchronous with spawning females entering nests for 1 or 2 days or even as long as 1 week, resulting in some males simultaneously guarding eggs and larvae (Boyer and Vogele 1971; Jennings and Philipp 1994). Nest-guarding males produce gruntlike sounds as part of courtship (Gerald 1971); other reported courtship, spawning, and brood defense and care behaviors appear typical for the genus (e.g., rim circling, lateral threat displays, paired circling). After spawning, the male may alternate egg fanning with caudal sweeping to mix eggs in the substrate, and both males and females engage in frequent substrate biting during nest defense and before circling, respectively (Witt and Marzolf 1954; Huck and Gunning 1967; Boyer 1969; Boyer and Vogele 1971). During a spawning event, a female spawns with a given male about 20 times for 20 to 29 minutes, depositing 7 to 20 eggs with each dip into the nest; several females may ultimately spawn in a single nest. Females may spawn with one male and then enter another nest to spawn with another male (Boyer and Vogele 1971). Spawning pairs are frequently interrupted by sneaker male morphs, neighboring nesting males, or males of other Lepomis spp. attempting to steal fertilizations (Huck and Gunning 1967; Boyer and Vogele 1971; Jennings and Philipp 2002). Although patchily distributed, sneaker male morphs are documented in Illinois stream populations (Jennings and Philipp 1992c, 2002). Observations of two ostensible females spawning simultaneously with a male (Boyer 1969; Boyer and Vogele 1971) suggest that the sneaker tactic may be more widespread than is currently documented. Ovaries of mature females contain several distinct sizes and developmental stages of ova, and the mature ovarian eggs are apparently large for Lepomis, averaging 1.55 to 2.00 mm diameter (Boyer 1969; Yeager 1981). Fecundity increases with female size, but relationships are apparently unquantified. Estimates of numbers of spawned ova for three size classes of females in two Missouri reservoirs were 1417 to 3600 eggs (≤100 mm TL), 3440 to 4136 eggs (101–129 mm TL), and 4213 eggs (≥130 mm TL) (Boyer 1969). Most of the adhesive, fertilized eggs in a colony hatch in about a week, but time to hatching may extend for 12 days or more at 25◦ C (Huck and Gunning 1967; Boyer 1969). Numbers of eggs in 12 nests ranged from 608 to 2756, and numbers of larvae in six successful nests averaged 465 (range 3 to 1132). Larvae at hatching are of 5.0 to 5.2 mm TL, and advanced larvae in a nest ranged from 5.8 to 7.5 mm TL (mean = 6.9 mm TL) (Boyer 1969; Boyer and Vogele 1971; Yeager 1981). Successful males guard and vigorously defend the eggs and larvae for up to 9 days, depending on developmental rate of offspring (Jennings and Philipp 1994). While nest guarding, males feed opportunistically, consuming large numbers of longear sunfish eggs, high volumes of detritus, and nearby aquatic insects (Boyer 1969; Boyer and Vogele 1971). Larval swim-up and dispersal occur at 7.3 to 7.6 mm TL about 6 to 8 days after hatching (22–25◦ C, presumably) (Huck and Gunning 1967; Boyer and Vogele 1971; Yeager 1981). Larval fin development is apparently more rapid than in most other Lepomis (Taber 1969; Yeager 1981). After

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leaving the nest, fry from several nests initially merge to form large schools in dense cover but later separate into small groups or as single individuals (Boyer and Vogele 1971). Nest associates: Redfin shiner, L. umbratilis (Snelson and Pflieger 1975). Freshwater mussel host: Confirmed host to A. suborbiculata, L. siliquoidea, M. nervosa, P. grandis, Strophitus subvexus, and V. nebulosa (Penn 1939; Haag and Warren 1997; Howells 1997; O’Dee and Watters 2000). Putative host to L. recta, S. undulatus, T. lividus, U. imbecillis, and Villosa contricta (unpublished sources in OSUDM 2006). Conservation status: The longear sunfish as currently conceived appears secure throughout its range (Warren et al . 2000; NatureServe 2006, but latter includes L. peltastes), but the status of evolutionarily significant units or undescribed taxa in northern Mexico is of concern (Miller 2005). Because of evidence of polytypy, a comprehensive characterization of variability across the geographic range is needed to clarify the conservation status of the Rio Grande and other suspected forms of the longear sunfish. Similar species: See accounts on dollar sunfish and northern longear sunfish. The redbreast sunfish lacks blue spots on the sides and has rows of red-brown spots on upper side and a longer, narrower ear flap that is black to its edge. The pumpkinseed has bold spots on the second dorsal fin and long, pointed pectoral fins, and a stiff posterior edge on the gill cover (Page and Burr 1991). Systematic notes: Lepomis megalotis is included in a clade with L. peltastes and L. marginatus (Near et al . 2004, 2005), but relationships among these species are unresolved (see accounts on these species). L. megalotis is polytypic. In a morphological analysis of variation that did not include breeding colors (Barlow 1980), four subspecies (not including L. peltastes) were delimited: L. m. megalotis, L. m. breviceps, L. m. aquilensis (Rio Grande to Brazos River, Texas), and an undescribed subspecies (Little River, Oklahoma and southwestern Arkansas). L. m. megalotis was differentiated into four races: eastern Gulf race, Ozark race, Central and Interior Lowland race, and Coosa River race. The subspecies L. m. breviceps was differentiated into two races: Upper Arkansas and Missouri basin race and east Texas race. Differences in breeding colors and opercular tab orientation occur in middle Missouri River and upper White River populations (Pflieger 1971). Analysis of nuclear-encoded allozyme loci confirmed genetic distinctiveness of the southwestern populations (L. m. aquilensis and L. m. breviceps) from L. m. megalotis, suggested intergradation or retained ancestral polymorphisms in the Ozark Highlands between L.m. breviceps and L. m. megalotis, and indicated considerable divergence within L. m. megalotis (Jennings and Philipp 1992a). A fifth subspecies, L. m. occidentalis, from the Rio Grande system (Bailey 1938), could not be differentiated meristically or morphometrically from L. m. aquilensis (Barlow 1980), but striking differences in breeding colors in Rio Grande populations suggest that additional taxa are present (Miller 2005). Importance to humans: Despite its relatively small size, the longear sunfish is of considerable importance in stream fisheries where it can comprise a large proportion of the creel (up to 37% by weight) (e.g., Mississippi, Missouri, Tennessee). It vigorously attacks a variety of live baits, small spinners, dry flies, and popping bugs, and is a scrappy fighter when taken on light tackle. Larger specimens also provide a tasty morsel for the table (Etnier and Starnes 1993; Pflieger 1997; Ross 2001). In reservoirs, young-of-the-year longear sunfish are an important forage fish for largemouth bass, particularly for 5 to 20 cm bass during summer and fall (Applegate et al . 1967).

13.8.9 Lepomis microlophus (Gunther) ¨ 13.8.9.1 Redear sunfish Characteristics: See generic account for general characteristics. Body moderately deep, compressed, depth 0.42 to 0.50 of SL. Mouth moderate, terminal, oblique, supramaxilla small (>3 times and ≤4 times length of maxilla), upper jaw extends almost to, or to, anterior edge of eye. No wavy blue or dark lines on cheek and opercle; soft dorsal, anal, and caudal fins not marked with dark brown wavy lines or orange spots. Opercular flap, short, moderately flexible with black center bordered above and below in white or light slate and posteriorly by prominent red (male) to orange (female) crescent (often pale in young). Pectoral fin long and pointed, tip extending far past eye when laid across cheek. Gill rakers short, 9 to 11, longest about two times greatest width. Lateral line complete. Lateral scales, 34 to 47; rows above lateral line, 6 to

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8; rows below lateral line, 13 to 16; cheek scale rows, 3 to 6; caudal peduncle scale rows, 16 to 22; pectoral rays, 13 to 16. Pharyngeal arches extremely broad, heavy with large rounded, molariform teeth. Teeth present or absent on palatine. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Bailey 1938; Trautman 1981; Mabee 1993). Size and age: Size at age 1 is highly variable among habitats and across latitudes, varying from about 30 to 185 mm TL (median 86.5 mm TL). Large individuals measure 200 to 250 mm TL, weigh about 200 to 300 g, and can attain age 6+ to 9+ (maximum 269 mm TL, age 11+) (Schoffman 1939; Carlander 1977; Trautman 1981; Page and Burr 1991; Sammons et al . 2006). World angling record, 2.48 kg, South Carolina (IGFA 2006). Coloration: Bright red or orange spot on light colored edge of ear flap (best developed on large adult). Light gold-green above; dusky gray spots (adults) or bars (young) on sides; white to yellow below. Fins mostly clear, some dark mottling in second dorsal fin of adult. Breeding male brassy gold with dusky pelvic fins (Page and Burr 1991). Native range: The redear sunfish is native to the Atlantic and Gulf Slope drainages from about the Savannah River, South Carolina, to the Nueces River, Texas, and ranges in the Mississippi River basin north from the Gulf to southern Indiana and Illinois (Page and Burr 1991). The species is now widely introduced and established in the eastern and western United States, usually in reservoirs, including the Colorado River basin and Pacific Slope drainages (Page and Burr 1991; Fuller et al . 1999). After the introduction of the nonnative redear sunfish, native pumpkinseed in a southern Michigan lake experienced a 56% decline in abundance (Huckins et al . 2000). Habitat: The redear sunfish inhabits ponds, oxbows, swamps, lakes, and reservoirs and the sluggish pools and backwaters of small to medium size rivers (Page and Burr 1991). The species is much more abundant in clear, vegetated backwaters than in turbid, hypoxic backwaters or flowing main channels of streams and rivers (Beecher et al . 1977; Pflieger 1997; Rutherford et al . 2001; Miranda and Lucas 2004). Redear sunfish, known from salinities up to 20 ppt, acclimate physiologically more quickly to salinity changes (1 hour, ≤8 ppt) relative to congeners and Micropterus (12 hours), and are among the most euryhaline centrarchids. This physiological adaptation may allow redear sunfish to withstand the rapidly changing salinities of tidal rivers (Peterson 1988). Food: The redear sunfish is highly specialized for crushing hard-bodied prey such as snails, small bivalves, and ostracods, earning it the appellation of “shellcracker” among anglers. Similar to the pumpkinseed, the species possesses heavy pharyngeal jaw bones that are equipped with molariform teeth, enlarged muscles, and specialized neuromuscular adaptations (Lauder 1983a,b, 1986; Wainwright and Lauder 1992; Huckins 1997). In contrast to the pumpkinseed, the redear sunfish uses the crushing apparatus on all prey types as evidenced by muscular activity patterns, but the pumpkinseed displays the crushing pattern only when feeding on snails (Lauder 1983a,b). Redear sunfish also appear better adapted for hard-bodied prey than pumpkinseed. At a given size, redear sunfish have more robust pharyngeal structures and possess about twice the shell crushing capacity of pumpkinseed, and hence, can consume larger (and harder) snails than similarsized pumpkinseed (Huckins 1997). In laboratory choice experiments, redear sunfish discriminated against thick-shelled snail species and chose thin-shelled snail species (Stein et al . 1984). Young redear sunfish undergo a dramatic and rapid shift in diet from soft-bodied invertebrates to high numbers of snails as they grow from 25 to 75 mm TL. As principally benthic feeders, redear sunfish are certainly not limited to feeding on snails but also consume large numbers of larval dipterans and burrowing mayflies, amphipods, larval odonates, and a variety of other invertebrates (McCormick 1940; Chable 1947; Wilbur 1969; Desselle et al . 1978; Huckins 1997; VanderKooy et al . 2000). Feeding occurs frequently and apparently at random throughout the day (Wilbur 1969). Reproduction: Maturity is reached at age 0+ or 2+ in females at 100 to 164 mm TL (Schoffman 1939; Wilbur 1969; Carlander 1977; Adams and Kilambi 1979). Spawning in Florida begins in late February or early March as water temperatures reach 21◦ C, and continues for 6 to 7 months and may involve up to five synchronous spawning peaks (Wilbur 1969). Over the reproductive season, spawning may cease for periods of 1 to 3 weeks. Nests are most abundant at water temperatures of 23.8 to 26.7◦ C, but nesting may continue up to 32.2◦ C (Clugston 1966). In less southerly latitudes, spawning occurs from about May to July or August (Adams and Kilambi 1979). Males excavate nests by caudal sweeping, the nests are colonial (<1 m apart), and colonies often contain nests of congeners (Childers 1967). Nests may be placed in shallow water (<0.5 m) (Clugston 1966), although the redear sunfish frequently nests in somewhat deeper water than most Lepomis (1 to >2 m, Wilbur 1969). Nests are 25 to 61 cm in diameter and 5 to 10 cm deep and constructed in bottoms of sand,

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gravel, or mud (Wilbur 1969). Nest-guarding males produce popping sounds (presumably with the jaw and pharyngeal bones) that are directed at the sides and head of females during courtship (Gerald 1971; see account on L. gibbosus). Little else is apparently known about nest-building, spawning, or nest-guarding behaviors. In ponds, female bluegills, the males of which have completely black opercular flaps, interbred with redear sunfish males when their red, white, and black opercular flaps were removed, but females did not interbreed when redear male flaps were intact (Childers 1967). Mature ovarian eggs range from 0.60 to 1.30 mm diameter (Adams and Kilambi 1979) and water-hardened, fertilized eggs from 1.3 to 1.6 mm diameter (Meyer 1970). Fecundity increases with female size. The relationships between potential batch fecundity (Y) and total length (X) are described by the functions, ln10 Y = 5.95424 + 0.01967X and log Y = 263.75 + 1.7109 log X (formulas from Adams and Kilambi (1979), n = 15, R2 = 0.90, and from Wilbur (1969), based on means from eight length classes, 82 females, R2 = 0.88, respectively). At 182 mm TL, a female can potentially produce 13,824 to 17,812 mature eggs in a single batch (range: 7513 to 12,943 eggs at 151 mm TL to 23,316 to 25,437 eggs at 213 mm TL, respectively). Eggs hatch in 50.3 hours at 23.8◦ C, 26.6 to 28.1 hours at 28.5◦ C; newly hatched larvae are 3.3 to 3.8 mm TL and reach swim-up in about 3 days at 4.78 to 5.80 mm TL (Childers 1967; Meyer 1970; Yeager 1981). Nest associates: None known. Freshwater mussel host: Confirmed host to A. neislerii (O’Brien and Williams 2002). Putative host to L. teres (unpublished sources in OSUDM 2006). Conservation status: The redear sunfish is apparently secure throughout its range (but see section on systematic notes), except for peripheral populations in Illinois that are considered imperiled (NatureServe 2006). Historically, abundant, widely distributed redear populations occurred in lakes on the large Yazoo River alluvial floodplain in Mississippi. Now, the species has practically disappeared from these lentic habitats apparently in response to increased turbidity from agricultural activities (Miranda and Lucas 2004). Similar species: The pumpkinseed has bold spots on the second dorsal fin, wavy blue lines on the cheek and opercle, and a stiff rear edge on the gill cover. The longear, northern longear, and dollar sunfishes have short, rounded pectoral fins, wavy blue lines on the cheek and opercle, and a long ear flap (Page and Burr 1991). Systematic notes: Lepomis microlophus is sister to the species pair, L. punctatus and L. miniatus (Near et al . 2004). On the basis of shared behavioral and morphological specializations for mollusk-crushing, L. gibbosus was proposed previously as sister to L. microlophus (Bailey 1938; Mabee 1993). Two subspecies of the redear sunfish, L. m. microlophus and an undescribed subspecies, are recognized based on essentially nonoverlapping scale counts, pectoral fin length differences, and opercular flap coloration (Bailey 1938). The range of the two subspecies is not entirely clear from the original work (Bailey 1938), but the undescribed subspecies occurs in the Mississippi River Valley westward to the San Marcos River, Texas, and perhaps east in the middle Gulf Slope to southern Mississippi, and L. m. microlophus occurs in eastern Gulf and Atlantic Slope drainages of Alabama, Georgia, and Florida (Page and Burr 1991). Phylogeographic analyses using mtDNA haplotypes along the southeastern seaboard of the United States revealed genetic discontinuities that were largely congruent with boundaries identified by morphological differentiation (Bailey 1938; Bermingham and Avise 1986). The widespread practice of moving and stocking redear sunfish in the southern United States may have obscured the boundaries of the two forms, but clarification of their current status awaits thorough genetic and morphological comparisons. Importance to humans: The redear sunfish, the “shellcracker” to many anglers, is a popular sport fish that is often stocked in combination with largemouth bass and bluegill in ponds and reservoirs. Because of its bottom-feeding habits, the species fills a niche little used by other Lepomis, and redear sunfish do not tend to overcrowd and stunt in ponds as do bluegill. The fast growth rate, large size, and mild flavor combine to make them a highly desirable pan fish. The redear sunfish is often one of the primary fish in sunfish sport fisheries and can account for a substantial portion (up to 66%) of the sunfish harvest by weight in southern lakes and reservoirs (Schramm et al . 1985; Crawford and Allen 2006; Sammons et al . 2006). From 1976 to 1981, 36 to 332 thousand kilograms of redear sunfish were harvested annually by commercial fishing operations in Lake Okeechobee, Florida, constituting about 8% of the total commercial catch over this period (Schramm et al . 1985). The species is less likely to be taken on artificial lures than bluegill but readily takes worms and other natural baits fished near the bottom. Nesting males are taken in large number by anglers (Wilbur 1969; Etnier and Starnes 1993; Ross 2001). Nonnative snails and bivalves (e.g., Asian clam, Corbicula fluminea) are often exploited

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as food by redear sunfish (Moyle 2002), and the species is used effectively as a native biological control for snails that serve as intermediate hosts to detrimental parasites of pond-raised channel catfish (Ledford and Kelly 2006).

13.8.10 Lepomis miniatus Jordan 13.8.10.1 Redspotted sunfish Characteristics: See generic account for general characteristics. Body deep, compressed, depth 0.45 to 0.50 of SL. Mouth moderate, terminal, oblique, supramaxilla small (>3 times and ≤4 times length of maxilla), upper jaw extending just to or slightly beyond anterior margin of eye. Iridescent turquoise crescent outlining ventral curvature of red or dark eye. No wavy blue lines on head. Two to three diffuse bars often radiate posterior to the eye, and small spots on head, if present, most prominent on the preopercle and subopercle, often diffuse or coalesce to form dark, short streaks. Body in breeding males with horizontal rows of red-orange spots (one per scale) below the lateral line; black specks rarely present. Opercular flap, stiff, short with black center narrowly bordered above and below by pale white, posterior edge with narrow pale white border, often lacking; dorsal edge of flap red-orange in breeding males. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Gill rakers moderate to long, 8 to 11, longest about two to four times greatest width. Lateral line complete. Lateral scales, (33)35 to 41(42); rows above lateral line, (4)6 to 7(8); rows below lateral line, (11)12 to 14(15); cheek scale rows 4 to 6(7); breast scale rows (11)12 to 15(18); caudal peduncle scale rows, (15)18 to 21(22); pectoral rays (12)13 to 14(15). Pharyngeal arches narrow with sharply pointed teeth. Teeth present or absent on palatine bones. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Bailey 1938; Warren 1992; Mabee 1993). Size and age: Typically reach 30 to 80 mm TL at age 1. Large individuals measure 133 to 153 mm TL and attain age 4+ (maximum about 164 mm TL) (Carlander 1977; Warren 1992; Roberts et al . 2004). Coloration: Ear flap, short, black with narrow dorsal and ventral white edges (suffused in orange in breeding male). Sides with red-orange, horizontal rows of spots, best developed at level of pectoral fin in breeding males. Ventral curvature of dark or red eye outlined with iridescent turquoise crescent (in life), a characteristic unique to L. miniatus and L. punctatus. Dark olive above; pale to yellow on breast and anterior belly. Breeding males with red-orange on breast, anterior belly, and pale circular to quadrate blotch above ear flap; dusky to dark pelvic fins; distal one-half to one-third of soft dorsal, soft anal, and caudal fins suffused with red-orange to reddish brown and narrowly edged in silvery, creamy, pinkish, or white margins (Page and Burr 1991; Warren 1992). Native range: The redspotted sunfish is native to the Illinois River, Illinois (relictual population, Burr and Page 1986), and south in the Mississippi River Valley to the Gulf Slope. On the Gulf Slope, the species occurs from the Nueces River, Texas, to, and inclusive of, the Mobile Basin, Alabama (Warren 1992). The introduced or native status of individuals from the Devils River (Rio Grande drainage), Texas, is equivocal (Warren 1990). Populations in drainages of the Florida Panhandle (inclusive of drainages from the Perdido to Apalachicola rivers), upper Coosa River tributaries (Alabama River drainage), and Lookout Creek (Tennessee River drainage) form a zone of contact in which individuals cannot be clearly identified morphologically as redspotted or spotted sunfishes (Warren 1992). Habitat: The redspotted sunfish inhabits well-vegetated ponds, lakes, and slow-flowing pools of creeks and small to medium rivers, being most abundant in natural floodplain lakes (Page and Burr 1991), where it tolerates periodic hypoxic conditions (<1 mg/l DO, Killgore and Hoover 2001). Removal of aquatic vegetation by grass carp (C. idella) in a eutrophic Texas reservoir resulted in almost complete elimination of redspotted sunfish (Bettoli et al . 1993). The species also occurs in coastal habitats of low salinity (usually <4 ppt), where it can be one of the most abundant centrarchids (Desselle et al . 1978; Peterson and Ross 1991). Length–weight relationships were not different between two populations experiencing annual salinities ranging from 1 to 10 ppt (average = 4) and 0 to 4 ppt annually (average = 0.91), respectively, suggesting that oligohaline conditions produce little or no metabolic consequences for the species (Peterson 1991; Peterson and Ross 1991). Food: The redspotted sunfish is an invertivore that forages primarily in submerged aquatic vegetation and bottom sediments but can also exploit surface prey. The most comprehensive food studies were conducted in low-salinity coastal environments with marine faunal elements (Lake Pontchartrain, Louisiana, and Davis Bayou, Mississippi). In oligohaline habitats, adult

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fish (>60 mm SL) feed on mud crabs, isopods, amphipods, and a variety of aquatic insects (dipteran larvae, caddisfly larvae, terrestrial insects) (Desselle et al . 1978). In a freshwater stream, food consisted primarily of adult and larval insects (Robison and Buchanan 1984). Small fish (≤60 mm SL) feed initially on copepods, midges, cladocera, mysid shrimp, and mayfly larvae, gradually transitioning to higher consumption of larger crustaceans and insects (Desselle et al . 1978; VanderKooy et al . 2000). Reproduction: The reproductive biology of the redspotted sunfish is not well studied but is presumably similar to that of its sister species, the spotted sunfish, L. punctatus. Spawning is protracted. Nesting activity was observed from early April to August in Texas, May to early August in Illinois, and in July in Missouri (Forbes and Richardson 1920; Robison and Buchanan 1984; Pflieger 1997; Roberts et al . 2004). When transferred from experimental ponds in Illinois to indoor aquaria, males and females spawned in artificial nests in August (Roberts et al . 2004). In Missouri streams, nests are placed in a few centimeters of water among stems of water willow over a bottom of sand and gravel. Some males nest solitarily, but two or more males often build adjacent or even confluent nests (Pflieger 1997). Eggs hatch in about 36 hours at 26◦ C, and larvae reach swim-up about 4 to 5 days after hatching (Roberts et al . 2004). Nest associates: None known. Freshwater mussel host: None known. Conservation status: The redspotted sunfish is secure throughout its range (Warren et al . 2000), but peripheral northern populations are considered vulnerable (Indiana, Tennessee) or imperiled (Illinois and Kentucky) (NatureServe 2006) because of losses of populations and lowland habitats (Smith 1979; Burr and Warren 1986; Burr et al . 1988). Similar species: The spotted sunfish lacks rows of red or yellow spots on the sides and has discrete black specks, often numerous, on head and body. The bantam sunfish lacks rows of red or yellow spots on the sides, lacks a brassy-red patch above the ear flap, has a black spot in the posterior second dorsal fin (in juveniles), and has an interrupted or incomplete lateral line. The longear, northern longear, dollar, and redbreast sunfishes have wavy blue lines on the cheek, longer ear flaps, and short, thick to knobby gill rakers (Page and Burr 1991). Systematic notes: Lepomis miniatus is the sister species of L. punctatus (Near et al . 2004, 2005). Although long recognized as distinct (Jordan 1877), L. miniatus was considered a subspecies of L. punctatus throughout most of the twentieth century (Bailey 1938; Bailey et al . 1954). Morphological (meristics, pigmentation, breeding color) and genetic (nuclear-encoded allozyme loci and mitochondrial and nuclear DNA) data support recognition of L. miniatus as a distinct species (Warren 1989, 1992; Bermingham and Avise 1986; Near et al . 2004, 2005). Populations from the Perdido River, Alabama, east to the Apalachicola river and those in upper Coosa River tributaries (Alabama River drainage) and Lookout Creek (Tennessee River drainage) show scale counts that are intermediate morphologically between the two species. Genetic distance analyses from nuclear-encoded allozyme loci, pigmentation patterns, and breeding colors suggest closer affinity of these contact zone populations to L. punctatus, but population sampling was limited for the allozyme analyses (Warren 1989, 1992). Whether these contact zone populations represent past or ongoing introgression and retained ancestral polymorphisms or a distinct evolutionary lineage awaits further analyses. Importance to humans: The redspotted sunfish, although providing sport, is generally too small to be a significant pan fish. Even so, the species contributes to the bream creel, particularly for bank anglers using cane poles in wetlands, backwaters, and small, lowland streams. The species is most often taken using worms or crickets but may also be taken at the surface on popping bugs. The flesh is firm and mild (Etnier and Starnes 1993).

13.8.11 Lepomis peltastes Cope 13.8.11.1 Northern longear sunfish Characteristics: See generic account for general characteristics. Deep, compressed body, depth 0.42 to 0.53 of SL. Mouth moderately large, oblique, jaws subequal, supramaxilla small (>3 times and ≤4 times length of maxilla), upper jaw extends to about center of eye, always beyond anterior edge of eye. Wavy blue lines on cheek and opercle of adult. Opercular flap long, flexible, pointing upward with black center edged above and below in yellow or white, posterior edge often

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with red spot; lower border usually wider than upper. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Short, thick, knoblike gill rakers, 12 to 14, longest about equal (adults) to two (young) times greatest width. Lateral line often incomplete or interrupted behind posterior base of dorsal fin. Lateral scales, (31)35 to 37(41); rows above lateral line, 5 to 6(7); rows below lateral line, (11)12 to 13(14); cheek scale rows, 4 to 6(7); caudal peduncle scale rows, (14)17 to 19(21); pectoral rays, (11)12 to 13(14). Pharyngeal arches narrow with pointed teeth. No teeth on endopterygoid, ectopterygoid, palatine, or glossohyal (tongue) bones (Bailey 1938; Gruchy and Scott 1966; Scott and Crossman 1973; Barlow 1980; Trautman 1981; Becker 1983; Mabee 1993; Bailey et al . 2004). Size and age: Typically reach 30 to 48 mm TL at age 1. Large individuals measure 96 to 102 mm TL and attain age 4+ (maximum about 150 mm TL, 9+ years) (Hubbs and Cooper 1935; Scott and Crossman 1973; Becker 1983; Jennings and Philipp 1992c). Coloration: Similar to L. megalotis, but black ear flap edged in yellow (or red), the lower edge often wider than upper (Barlow 1980; Trautman 1981; Page and Burr 1991). Native range: The northern longear sunfish occurs in the St. Lawrence-Great Lakes drainages from southern Quebec, western New York, northwestern Pennsylvania, northern Ohio and Indiana, the Lower Peninsula of Michigan, eastern Wisconsin, northern Minnesota, and southern Ontario (including Hudson Bay system). The species occurs, or occurred historically, in scattered localities in the Mississippi River basin in northwestern Wisconsin, northeastern Illinois, Minnesota, and Iowa (Smith 1979; Trautman 1981; Becker 1983; Underhill 1986; Jennings and Philipp 1992a; Bailey et al . 2004). Habitat: The northern longear sunfish inhabits pools of clear, shallow streams and moderate sized rivers as well as ponds and lakes (Scott and Crossman 1973; Trautman 1981; Becker 1983). The species avoids densely vegetated littoral habitats and sediment-laden, turbid habitats. In southern Michigan, northern longear sunfish occurred in greatest abundance in lakes containing shoreline benches of exposed marl sediments and was rare or absent in lakes with organic-laden sediments or dense aquatic vegetation covering shallow (<2 m) littoral zones, regardless of sediment type (Laughlin and Werner 1980). Within a lake, most large individuals (>75 mm TL) occur in sparsely to moderately vegetated habitats, and small individuals (<38 mm TL) concentrate in the most densely vegetated areas. The species decreased dramatically in distribution and abundance in tributaries and shallows of Lake Erie as those habitats received increased sediment loads in the twentieth century (Trautman 1981). Food: The northern longear sunfish is a benthic invertivore. In a summer diet study, lake-dwelling adults (>75 mm TL) primarily consumed dragonfly and mayfly larvae and amphipods. The species uses a sit-and-wait foraging strategy, remaining still and close to the bottom, apparently keying in on the slight movements of cryptic or burrowing prey (Laughlin and Werner 1980). Reproduction: Maturity is reached at age 2+ at 45 to 75 mm SL, occasional large individuals mature at age 1+ (Hubbs and Cooper 1935; Jennings and Philipp 1992c). In experimental ponds, both males and females matured at age 1+, but sneaker male phenotypes (e.g., drab coloration, large gonads) matured at a smaller size (40–60 mm TL) than parental males (60 mm TL) (Jennings and Philipp 1992c). Spawning is protracted (late May to August) with peaks in July (Hubbs and Cooper 1935; Keenleyside 1972; Dupuis and Keenleyside 1988). Nest building and spawning occur as water temperatures exceed 20◦ C, but lengthening photoperiod in spring is most strongly associated with initiation of nest-building behaviors in males. Out-of-season nest building occurred under experimental conditions of long photoperiod (16 hours) and warm water temperatures (25◦ C). Under a long photoperiod and cold temperature (11–13◦ C), some males began but did not complete nests; no males built nests under a short photoperiod (8 hours) regardless of temperature (Smith 1970). Most nest-guarding males are 73 to 111 mm TL (Keenleyside 1971; Dupuis and Keenleyside 1988). Males excavate small saucer-shaped nests (average 33 cm diameter) with caudal sweeping over areas of mixed sand and gravel or where gravel substrate is covered by silt, which is swept away by the males before spawning. Nests are usually close to shore in shallow water (10–60 cm) with little current and are often near aquatic vegetation or overhanging shrubs (Bietz 1981; Dupuis and Keenleyside 1988). Although a few males nest solitarily (<4%), most males excavate their nest in close proximity to other nesting males to form dense colonial aggregations of rim-to-rim hexagonally shaped nests (<20 to 100+ nests) (Keenleyside 1972; Bietz 1981; Dupuis and Keenleyside 1988). Colonies are formed when new males (peripheral males) excavate nests around those of early nesting males (central males). Colonies are definitely social aggregations

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because formation occurs in the absence of habitat limitation (Bietz 1981). Breeding is synchronous in colonies, and over the long breeding season five or six distinct spawning periods occur. Males spawning later in the breeding season obtain larger numbers of larvae (average 750) than those breeding earlier (<300) (Dupuis and Keenleyside 1988). Likewise, males spawning first during a given breeding period obtain more larvae than those nesting on the second or third day. Agonistic, courtship, spawning, and nest defense behaviors are well documented (e.g., opercular spreads, tail-beating, bites, nest circling, dipping), and form a large part of the foundation for our knowledge of reproductive biology and behavior in the genus (Keenleyside 1967, 1971, 1972; Steele and Keenleyside 1971). Nest preparation is accomplished in <24 hours, but females arrive on the spawning grounds before all nests are completed. Females are usually courted by several males (e.g., courtship circles with shivers and vibrations) but may also spawn in a male’s nest without any overt courtship (Keenleyside 1967; Steele and Keenleyside 1971). Females often spawn with several males during a spawning event and often enter a nest to eat eggs before being chased away by the guardian male (Keenleyside 1972; Dupuis and Keenleyside 1988). Females can visually distinguish conspecific from other Lepomis males (Steele and Keenleyside 1971), suggesting an ability to chose mates. Likewise, nesting males can visually distinguish conspecific from other Lepomis females, but nonnesting males show weaker discrimination between conspecific and other Lepomis females (Keenleyside 1971). Within colonies, females spawn preferentially with males nesting early within a spawning period and those with centrally located nests. Females also appear to choose larger over smaller males. Solitary nesting males are larger than and as successful as colonial males in obtaining eggs and larvae (Dupuis and Keenleyside 1988). These patterns suggest that nesting colonies arise so that males unlikely to attract females (i.e. smaller, peripheral guardian males) increase their exposure to and probability of spawning with females attracted to centrally located males (Bietz 1981; Dupuis and Keenleyside 1988). Up to five or six small sneaker males, which can be numerous around some nests (50+ individuals), frequently interrupt a spawning pair en masse in an attempt to steal fertilizations (Keenleyside 1972; Dupuis and Keenleyside 1988). The frequency of intrusions into nests by neighboring guardian males is also high (average, one per minute) (Keenleyside 1972). Spawning occurs over a 2- to 3-day period, males guard and fan the eggs, which hatch in 2 to 3 days, and continue guarding the larvae until they reach swim-up and disperse about 4 to 6 days after hatching. Males may then abandon the nest or begin cleaning and preparing it for another spawning (Dupuis and Keenleyside 1988). Nest associates: Redfin shiner, L. umbratilis (Noltie and Smith 1988). Freshwater mussel host: None known (see longear sunfish, Lepomis megalotis). Conservation status: The northern longear sunfish is apparently secure throughout the center of its native range (e.g., Lower Peninsula of Michigan). The species occurs primarily in scattered and isolated populations in the eastern and western parts of its range, where population declines and losses are documented (e.g., Ohio, Trautman 1981; Wisconsin, Becker 1983). The species is rare and considered critically imperiled in New York and Pennsylvania, imperiled in Quebec and Wisconsin, and vulnerable in Ontario (Scott and Crossman 1973; Becker 1983; Smith 1985; NatureServe 2006). Similar species: See accounts on longear sunfish and dollar sunfish. Systematic notes: Lepomis peltastes, only recently elevated to species status (Bailey et al . 2004), is in a clade with L. megalotis, and L. marginatus, but relationships among the taxa are unresolved (see accounts on L. megalotis and L. marginatus; Jennings and Philipp 1992a; Near et al . 2004, 2005). L. peltastes was long considered a dwarf form of L. megalotis (e.g., Hubbs and Cooper 1935) even though there is apparently no evidence of intergradation between the two (Smith 1979; Trautman 1981). In a phenetic cluster analysis using 47 meristic and morphological variables, populations of L. peltastes formed a basal cluster that was highly distinctive from all populations of L. megalotis (Barlow 1980). Interestingly, specimens from the Muskingum River (Ohio River basin) clustered with L. peltastes, suggesting that the southern geographic limits of the species are incompletely known. Frequency data from nuclear-encoded allozyme loci did not separate L. peltastes from L. m. megalotis (Jennings and Philipp 1992c). Nevertheless, the two clearly differ in morphological and life history traits (i.e. growth, maturity, reproductive investment) (Barlow 1980; Jennings and Philipp 1992a,b,c; Bailey et al . 2004). Importance to humans: The northern longear sunfish does not reach a size of interest to anglers; however, the breeding males are among the most stunningly beautiful of all North American freshwater fish. Although extremely aggressive toward conspecifics, it is otherwise easy to keep and breed in the laboratory or hobbyist’s aquaria (e.g., Keenleyside 1967;

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Bietz 1981). Studies of the northern longear sunfish increased our understanding of the social, agonistic, and reproductive behaviors and ecology for the genus and highlighted the value of freshwater fishes, especially centrarchids, as models for sociobiological research (e.g., Keenleyside 1967, 1971,1972; Smith 1970; Steele and Keenleyside 1971; Bietz 1981; Dupuis and Keenleyside 1988; Jennings and Philipp 1992a,c).

13.8.12 Lepomis punctatus (Valenciennes) 13.8.12.1 Spotted sunfish Characteristics: See generic account for general characteristics. Body deep, compressed, depth 0.45 to 0.50 of SL. Mouth moderate, terminal, oblique, supramaxilla small (>3 times and ≤4 times length of maxilla), upper jaw extending just to or slightly beyond anterior margin of eye. Iridescent turquoise colored crescent outlining ventral curvature of eye. No wavy blue or dark lines on head and no horizontal rows of red-orange spots on sides. Discrete, small dark spots form irregular horizontal rows on sides of body and dorsum, especially prevalent on lower sides. Cheek and opercle often speckled with black spots. Opercular flap, stiff, short with black center outlined above and below by narrow white edges (yellow-orange to pinkish-orange in breeding males), posterior margin edged with narrow pale white border, often lacking. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Gill rakers moderate to long, 8 to 11, longest about three to five times greatest width. Lateral line complete. Lateral scales, (37)38 to 44(47); rows above lateral line, (6)7 to 8(9); rows below lateral line, (12)13 to 15(16); cheek scale rows, (4)5 to 7(8); breast scale rows, (14)15 to 18(20); caudal peduncle scale rows, (7)8 to 10; pectoral rays, (12)13 to 14(15). Pharyngeal arches narrow with sharply pointed teeth. Teeth present or absent on palatine bones. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Bailey 1938; Warren 1992; Etnier and Starnes 1993; Mabee 1993). Size and age: Typically reach about 30 to 50 mm TL or more at age 1. Large individuals measure 165 to 180 mm TL, weigh 105 to 140 g (maximum 207 mm TL, 376 g), and presumably attain age 4+ to 5+, but estimates of size at age and maximum longevity are problematic (Caldwell et al . 1957; Page and Burr 1991; Warren 1992; Marcy et al . 2005). Coloration: Ear flap, short, black with white to yellow edges. Head and sides with many discrete, black specks, most prominent on lower sides. Ventral curvature of dark or red eye outlined with iridescent turquoise crescent, a characteristic unique to L. punctatus and L. miniatus. Dark olive above; pale to butterscotch yellow on breast and anterior belly; clear to dusky fins; very narrow silvery, creamy, pinkish, or white margins on median fins. Darkly pigmented breeding males with a pale patch above ear flap and dusky to dark pelvic fins (Page and Burr 1991; Warren 1992). Native range: The spotted sunfish is native to the Coastal Plain from the Cape Fear River, North Carolina, south in Atlantic Slope drainages to the Everglades and north and west in East Gulf Slope drainages to the Ocklockonee River, Georgia and Florida. From the Perdido River, Alabama, east to the Apalachicola River Basin the spotted sunfish forms a contact zone with the redspotted sunfish (see account on L. miniatus). Habitat: The spotted sunfish inhabits pools of small to medium rivers and heavily vegetated ponds, lakes, and swamps (Page and Burr 1991). In streams, the species is most often associated with instream wood, stumps, or undercut banks in slow current and soft substrates (Meffe and Sheldon 1988; Marcy et al . 2005). On the North Carolina Coastal Plain, the spotted sunfish is the most common and widely distributed centrarchid in first- to fourth-order streams and is also common, especially the young-of-the-year, in beaver ponds (Snodgrass and Meffe 1999). In Florida, the species occurs in abundance in densely vegetated springs, spring runs, and spring-fed rivers (Hubbs and Allen 1943; Carr 1946; Swift et al . 1977). Spotted sunfish are also the most abundant and ubiquitous centrarchid in the Everglades region, where the species accounts for the second highest biomass of all carnivorous fishes within wet-prairie habitats (Clugston 1966; Loftus and Kushlan 1987; Turner et al . 1999). In large pool habitats, adults are often observed in open water during the day, moving inshore at night; juveniles tend to stay in dense vegetation (Hubbs and Allen 1943; Loftus and Kushlan 1987). The species can penetrate waters up to at least 12.5 ppt and is a relatively common inhabitant of coastal tidewater and oligohaline habitats (Kilby 1955; Loftus and Kushlan 1987). Genetic analyses of Everglades populations suggest that the species is adept at immigrating en masse into seasonally dry habitats once the habitats are reinundated (McElroy et al . 2003).

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Food: The spotted sunfish is an opportunistic invertivore, picking invertebrates from the surface, aquatic plants, the bottom, and the stream drift. In North Carolina streams, adults (>45 mm SL) feed primarily on terrestrial invertebrates, midge larvae, mayflies, and decapods and occasionally on snails, bivalves, and fish (Sheldon and Meffe 1993; Marcy et al . 2005). Smaller individuals consume more midge larvae, along with aquatic and terrestrial insects, and a few water mites, amphipods, and copepods. Limited stomach analyses in a Florida spring indicated concentrated foraging in aquatic plant beds and associated sediments. Midge larvae, caddisfly larvae, freshwater shrimp, and isopods dominated the diet (Caldwell et al . 1957). Stomachs often contain substantial volumes of plant and algal matter (Caldwell et al . 1957; Marcy et al . 2005), presumably ingested incidentally while gleaning invertebrates from aquatic plants. Reproduction: Maturity is reached at age 1+ and a size of about 50 to 55 mm TL (Carr 1946; Caldwell et al . 1957). Most actively spawning females are 76 to 101 mm TL (maximum >127 mm TL), and nest-guarding males are 84 to 178 mm TL (Carr 1946; DeWoody et al . 2000a). In North Carolina, spawning occurs from late May to late July at water temperatures of 24 to 27◦ C (Marcy et al . 2005). The spawning season is prolonged in the Florida Everglades with nesting occurring from March to November (temperatures from 17.7–33.3◦ C), but lengthy pauses in spawning occur during this period, presumably in association with water temperatures exceeding 30◦ C (Clugston 1966; Loftus and Kushlan 1987). In near-constant temperature spring-fed streams in Florida (22.8◦ C), some individuals appear to be spawning year round because ripe males, ripe females, and juveniles are taken in every month of the year. However, gonads of the majority of individuals in these environments are well developed between March and August (Kilby 1955; Caldwell et al . 1957). Males use caudal sweeping over sand or sand mixed with pebbles and snail shells to excavate relatively small nests (15–61 cm diameter, 25–50 cm deep). Nests are placed in shallow water (10–38 cm) near or against the bank (Carr 1946; Clugston 1966; Marcy et al . 2005) and tend to be solitary in small streams, but males may also aggregate their nests into groups of two or more (Hubbs and Allen 1943; Carr 1946; DeWoody et al . 2000a). During courtship, males frequently flash their solid black ventral fins at nearby females and rush toward females, ultimately driving spawning-ready females to the nest. Males mate with multiple females and continue to accept eggs for up to 3 days after spawning begins. During this period males frequently orient head down with the snout thrust into the gravel in an apparent inspection of the eggs. In a North Carolina stream population, conservative estimates from genetic maternity analyses indicated that a male spawns with an average of four females (range, one to six) (DeWoody et al . 2000a). Evidence was suggestive, though not conclusive, that larger males received eggs from more females than smaller males. In the same population, paternity analyses revealed the occurrence of nest takeovers by guardian males, and the presence in low frequencies (5–15%) of precociously mature sneaker males (DeWoody et al . 2000a). Cuckoldry, however, was estimated at only 1.3% of all offspring examined. Other spawning, nest-guarding, and associated behaviors are typical of the genus (Carr 1946). Female size and fecundity relationships are apparently not quantified. Water-hardened, fertilized eggs are 1.4 to 1.8 mm in diameter, adhesive (often adhering to fine roots along the shoreline side of the nest), demersal, and dark brownish olive to pale transparent amber in color (Carr 1946; Marcy et al . 2005). The male constantly fans the eggs until they hatch (2.0–2.2 days; presumed temperature of 20–24◦ C; hatchling length, 4 mm TL). About 10 days after hatching, swim-up larvae (6.5–7.0 mm TL) begin leaving the nest over a 2-day period and briefly form loose schools in the surrounding area before dispersing (Carr 1946). Anecdotal accounts suggest that guardian males are among the most pugnacious and tenacious defenders of eggs and larvae among centrarchids (Hubbs and Allen 1943; Carr 1946; Clugston 1966). Nest associates: Golden shiner, N. crysoleucas (Carr 1946). Freshwater mussel host: None known. Conservation status: The spotted sunfish is currently stable (Warren et al . 2000) but is considered vulnerable in North Carolina, the northern periphery of its range (NatureServe 2006). Similar species: See account on redspotted sunfish. The redspotted sunfish lacks distinct black specks on head and body (Page and Burr 1991; Warren 1992). Systematic notes: Lepomis punctatus is the sister species of L. miniatus (Near et al . 2004, 2005) (see account on L. miniatus). Importance to humans: Most spotted sunfish are caught incidentally by bluegill and redear sunfish anglers, but the spotted sunfish is a consistent part of the panfish creel in many Florida waters (e.g., Suwannee River). Although of relatively small

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size, the species aggressively attacks live baits, such as crickets, mealworms, or Catalpa worms, or small popping bugs. When taken on ultralight gear, the species puts up a scrappy fight, and as table fare, the flesh is excellent (FFWCC 2006).

13.8.13 Lepomis symmetricus Forbes 13.8.13.1 Bantam sunfish Characteristics: See generic account for general characteristics. Body deep, compressed, depth 0.48 to 0.53 of SL. Mouth moderately large, supramaxilla small (>3 times and ≤4 times length of maxilla), upper jaw extending beyond anterior edge of eye. Black spot posterior of soft dorsal fin in young, diminishing with growth, absent in large adults. Lacks the bright coloration of other Lepomis. Opercular flap short, stiff, and black with pale posterior margin. Very long slender gill rakers, 12 to 15, longest about six to eight times greatest width. Pectoral fin short and rounded, tip usually not reaching eye when laid forward across cheek. Lateral line usually incomplete (1–18 scales unpored) or interrupted (up to 6 times). Lateral scales, (30)32 to 36(40); rows above lateral line, 5 to 7; rows below lateral line, 12 to 14; cheek scale rows, (4)5(6); caudal peduncle scale rows, (17)18 to 21(22); pectoral rays, (11)12 to 13. Pharyngeal arches narrow with small, blunt subconical teeth. Teeth on palatine bones. No teeth on endopterygoid, ectopterygoid, or glossohyal (tongue) bones (Bailey 1938; Burr 1977; Page and Burr 1991; Etnier and Starnes 1993; Mabee 1993). Size and age: Typically reach 34 to 46 mm SL at age 1. Large individuals measure 55 to 64 mm SL, and few live beyond age 2+ (maximum, 93 mm TL, age 3+) (Burr 1977; Page and Burr 1991). The bantam sunfish is the smallest and has the shortest maximum lifespan of any Lepomis. Growth differences between males and females are minimal (Burr 1977). Coloration: Ear flap, short, black with light edge. Lacks bright coloration of other Lepomis. Dusky green above and on sides; yellow flecks and scattered small dark brown spots (adult) or chainlike bars (young) on sides; yellow-brown below. Anal and dorsal fins, red in young, clear to dusky in adults (Burr 1977; Page and Burr 1991) Native range: The bantam sunfish is native to drainages of the Mississippi Embayment and lower Ohio River Valley from Illinois and western Indiana to the Gulf of Mexico and the Gulf Coastal Plain from Bay St. Louis, Mississippi, to the Colorado River, Texas (Page and Burr 1991). A post-Pleistocene relict population in the Illinois River is now extirpated as are populations in the lower Wabash River (Illinois and Indiana) (Burr 1977; Burr and Page 1986, 1991; NatureServe 2006). The species is most common in Louisiana and east Texas and a few scattered, relatively undisturbed remnant floodplain lakes and wetland systems in the lower Mississippi River alluvial valley (e.g., Wolf and Horseshoe Lakes, Illinois; Mingo Swamp, Missouri; Murphys Pond, Kentucky; Reelfoot Lake, Tennessee) (Burr 1977; Burr and Warren 1986; Burr et al . 1988; Etnier and Starnes 1993; Pflieger 1997). Habitat: The bantam sunfish is a phytophilic species occurring almost exclusively in oxbow lakes, floodplain ponds, overflow swamps, and sloughs that are characterized by standing timber, submerged logs, and dense beds of aquatic plants (Burr 1977; Page and Burr 1991). Substantial populations can also occur in large, shallow eutrophic reservoirs (Bettoli et al . 1993) and freshwater coastal marshes (Gelwick et al . 2001). The species occupies the shallow (15–120 cm) heavily vegetated margins of lentic habitats over mud, detritus, and decayed plant material (Burr 1977) and is tolerant of hypoxic conditions associated with dense aquatic plants beds (<1 mg/l DO, Gelwick et al . 2001; Killgore and Hoover 2001). Removal of aquatic vegetation in Lake Conroe, Texas, by nonnative grass carp (C. idella) resulted in a population collapse of the bantam sunfish (Bettoli et al . 1993). The species can apparently migrate across flooded lowlands during major flood events (Mississippi River flood, 1993), resulting in establishment of founder populations in formerly unoccupied habitats (Burr et al . 1996). Food: The bantam sunfish is an opportunistic invertivore. Adult (>40 mm SL) diets are predominated by odonate larvae, amphipods, hemipterans, dipteran larvae, mayflies, and gastropods. The diet of juvenile bantam sunfish (<30 mm TL) is similar to that of the adult, but includes higher consumption (to 40 mm TL) of microcrustaceans and midge larvae and lacks gastropods. Terrestrial or surface-dwelling insects (hemipterans) in stomachs indicate that some surface feeding occurs. Seasonally consumed foods include heavy use of gastropods in winter and spring and hemipterans in summer (Burr 1977).

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Reproduction: The female bantam sunfish matures at 34 to 45 mm SL at an age of 11 to 13 months; mature males are at least of age 1+ and ≥40 mm SL (Burr 1977). In captivity with optimal feeding, sexual maturity is reached in as little as 5 to 7 months (Wetzel 2007). Few other Lepomis (e.g., green and orangespotted sunfishes) consistently mature at such small sizes. The bantam sunfish also differs from congeners, particularly sympatric species, in its earlier and shorter spawning period, relatively small mature ova, and low batch fecundity. Males and females in breeding condition are present from mid-April to early June with peak breeding condition occurring in May at water temperatures of 18 to 22◦ C. In aquaria, males used caudal sweeping and the anal fin to excavate nests (70–120 mm diameter, 2 cm deep) over both sand and gravel, but in natural settings nests are excavated over fibrous root material in dense aquatic vegetation or over mud and leaf litter (Robison 1975; Zeman and Burr 2004; Wetzel 2007). Nests are closely spaced (about 40 cm apart), and as territorial boundaries are established, neighboring males are intensely aggressive (e.g., biting attacks) and display frequently (e.g., opercle flaring) toward neighboring nesting males (Wetzel 2007). In aquaria, if females are unresponsive to courtship, the nest-guarding male will nip, nudge, badger, opercle flare, and continuously circle the female, ultimately killing her (Burr 1977; Zeman and Burr 2004; Wetzel 2007). Receptive females rotate and flash the ventral surface toward the male, and in response, he repeatedly rushes to her and back to the nest until she follows. Once over the nest, the pair circles and spawns for about 30 minutes, at which time the male chases the female away. After spawning, males may engage in brief bouts of caudal sweeping and begin interspersing fanning of the eggs with aggressive displays and actions toward neighboring males. Spawning in aquaria occurred at about dawn at water temperatures of 22 to 26◦ C. The mature ova are translucent orange in color and range from 0.6 to 0.9 mm in diameter; fertilized eggs are adhesive (Burr 1977; Zeman and Burr 2004; Wetzel 2007). Fecundity increases with female size. The relationship between potential batch fecundity (Y) and adjusted body weight (X, total weight minus ovaries and viscera) is described by the linear function, Y = −50.94 + 210.7X (n = 14, R2 = 0.67; for SL, log10 Y = −2.785 + 3.383 log10 X, R2 = 0.44; formulas from Burr 1977). At 2.44 g (ca. 42 mm SL), a female can potentially produce 463 mature eggs in a single batch (range: 248 eggs at 1.42 g, ca. 34 mm SL, to 1544 eggs at 7.57 g, ca. 52 mm SL). The male defends eggs and larvae for about 6 to 7 days. Eggs hatch in 26 to 36 hours at 22 to 26◦ C and reach swim-up about 5 days post hatch. Males defend the eggs and young with aggression noticeably increasing as the fry reach swim-up. Larvae begin leaving the nest by ascending in the water column and at dusk take refuge and feed in vegetation beds. Male defense of the young continues to be high until the larvae ascend into the vegetation (Zeman and Burr 2004; Wetzel 2007). Nest associates: None known. Freshwater mussel host: None known. Conservation status: The bantam sunfish is likely much less widespread and abundant in the lowlands of the Mississippi Embayment and Gulf Coastal Plain than historically because of extensive channelization of streams and drainage of wetlands in the last century. Extirpations of northern populations in the Illinois and lower Wabash rivers exemplify effects of wetland habitat loss (Burr 1977; Zeman and Burr 2004). The species is considered critically imperiled in Indiana and Illinois, imperiled in Missouri and Oklahoma, and vulnerable in Texas and Arkansas (NatureServe 2006). Similar species: Other Lepomis lack the dark spot at the rear of the second dorsal fin (diminishing with growth, absent in large adults) (except the bluegill and green sunfish). The green sunfish is more elongate, has a larger mouth, and has yellow-orange edges on its fins. The bluegill is more compressed, has a longer pectoral fin, and has a dark edge on its ear flap (Page and Burr 1991). Systematic notes: Lepomis symmetricus forms a sister pair with L. cyanellus (Near et al . 2004, 2005). Interestingly, the sister pair comprises the smallest and second largest Lepomis and their ranges are sympatric. In a comprehensive study of morphological variation (Burr 1977), L. symmetricus showed surprisingly little variability, particularly given its distribution in isolated patches over a large geographic area. Variation in average counts showed a north–south clinal pattern. Populations in the Wabash River drainage were most aberrant, averaging higher scale and lower fin-ray counts. Importance to humans: The bantam sunfish does not reach a size of interest to anglers. Ecologically, the presence and abundance of the species within its native range is a decided indicator of functioning, relatively intact wetland ecosystems.

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13.9 Micropterus Lac´ep`ede The genus Micropterus, collectively referred to as the black basses, is a monophyletic clade of eight species and is sister to the genus Lepomis (Near et al . 2004, 2005). The natural range of extant species encompasses most of eastern North America east of the Rocky Mountains, reaching northward to the Great Lakes, St. Lawrence River, and Hudson Bay drainages of Canada and eastward and southward in the Mississippi River basin, Atlantic Slope, and Gulf of Mexico drainages west to the Rio Grande and Rio Sota la Marina in Mexico (Robbins and MacCrimmon 1974; Page and Burr 1991; Miller 2005). A large fossil species, Micropterus †relictus Cavender and Smith, is estimated to have weighed over 5.5 kg and is known from Late Pliocene-Early Pleistocene deposits in Lake Chapala, Jalisco, Mexico, a location south of the native range of all other fossil or extant centrarchids (Smith et al . 1975; Miller and Smith 1986). The smallmouth bass, largemouth bass, Florida bass, and to a lesser extent, the spotted bass form a quadtuplet of the most sought-after and valued freshwater sport fishes in North America. Other Micropterus are gaining sport fishing acclaim and popularity as unique, range-restricted fishes associated with beautiful, natural stream settings (e.g., Guadalupe bass, Shoal bass, Suwannee bass). No recreational fishery likely exceeds in economic scale the fishery targeting black basses (Ridgway and Philipp 2002). Of all anglers who fished in freshwater in 2001 (excluding the Great Lakes), 38% sought one or more species of black bass (Leonard 2005). The black bass recreational fishery ranked first among freshwater species in the number of anglers (10.7 million) and time spent fishing (nearly 160 million days). In the Great Lakes, black bass are second only to perch in the numbers of anglers (589,000 anglers) and time spent fishing (6.4 million days). Estimated direct expenditures (e.g., travel, lodging, equipment) associated with black bass fishing (excluding the Great Lakes) exceeded $10.1 billion (US) in 2001, and generated additional tens of billions of dollars more in indirect economic output and taxes (USFWS 2002; ASA 2005). The reproductive behavior and biology of Micropterus are typical for the family in many ways but depart in others. The existence of extended parental care (see next paragraph), alternating mating systems (see account on Micropterus dolomieu), and biparental care (see account on Micropterus salmoides) distinguish the genus from other centrarchids. Unlike their sister genus Lepomis, Micropterus do not develop bright breeding colors, and obvious sexual dimorphism of any kind is minimal. During spawning, differential darkening or intensification of pigment patterns occurs in breeding males and females (Carr 1942; Breder and Rosen 1966; Heidinger 1975; Miller 1975; Trautman 1981; Williams and Burgess 1999). As in Lepomis, changes in pigment pattern in the female likely function as submissive signals to the male. Micropterus males are solitary nesters, usually establishing well-spaced territories and using caudal sweeping and other fin movements to excavate a typical, depressional centrarchid nest. Nests are most often constructed at the base of or near simple cover (Carr 1942; Neves 1975; Vogele 1975a, 1981; Winemiller and Taylor 1982; Wiegmann et al . 1992; Hunt and Annett 2002; Hunt et al . 2002). Nest-site fidelity in Micropterus is apparently high. Males may use nesting areas year after year with individual males often returning to within a few meters of their previous year’s nest site or reusing the same nest in subsequent years (Carr 1942; Vogele 1975a; Ridgway et al . 1991a, 2002; Rejwan et al . 1997, 1999; Hunt et al . 2002; Ridgway et al . 2002; Waters and Noble 2004). In courtship, Micropterus males use leading or guiding courtship behaviors to attract females to the nest, often leaving the nest to approach, but not charge, the ripe female (Carr 1942; Ridgway et al . 1989). In contrast to all other centrarchids, Micropterus males stay with their brood well after the swim-up stage and continue to guard free-swimming swarms of young, termed fry balls, until the young reach sizes of about 25 to 30 mm TL (e.g., Kramer and Smith 1962; Miller 1975; Vogele 1975a; Elliott 1976; Brown and Colgan 1985a; Friesen and Ridgway 2000). Large Micropterus males tenaciously guard their eggs, yolk-sac fry, free-swimming fry, and juveniles (Hubbs and Bailey 1938; Ridgway 1988; Wiegmann et al . 1992; Wiegmann and Baylis 1995; Steinhart et al . 2005). For example, males excluded from their nests by exclosures stayed nearby for 11 days and immediately began guarding the young on removal of the nest exclosures (Neves 1975). Although poorly documented in some species (e.g., Guadalupe and Shoal basses), the total period of parental care for successful males (spawning through fry dispersal) can last for 2 to 7 or more weeks (Hubbs and Bailey 1938; Kramer and Smith 1962; Pflieger 1966a; Miller 1975; Vogele 1975a; Cooke et al . 2006) but is highly variable even within a population in a single spawning season and among years (e.g., 19 to 45 days; Ridgway and Friesen 1992). Variability is largely a function of changes in water temperature, and hence larval developmental rate, but also involves interactive effects of the time of nesting (early versus late), size of male, and energy depletion in males. Large mature males tend to nest earlier at lower water temperatures and invest longer periods in parental care (through swim-up) than do small mature males (Ridgway and Friesen 1992).

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The Micropterus male must patrol larger and larger areas as the fry balls forage increasing distances away from the nest (Ridgway 1988; Scott et al . 1997). Fry balls of Micropterus from single broods contain from several hundred to over ten thousand individuals (Kramer and Smith 1962; Friesen and Ridgway 2000). Individual broods often merge to form even larger groups of intermingled multiple broods of one or more black bass species, aggregations that cover extensive areas, and are under constant protection by one or more males (Carr 1942; Kramer and Smith 1962; Allan and Romero 1975; Vogele 1975a). Free-swimming juveniles of largemouth bass and perhaps other black basses are less oriented toward the nest than smallmouth bass; the juveniles leave the area of the nest and become increasingly mobile, feeding constantly during daylight hours and seeking cover at night (Carr 1942; Kramer and Smith 1962; Elliott 1976; Brown 1984, 1985; Brown and Colgan 1984). The increasing mobility of the roaming juveniles places high diurnal energy demands on the guardian males (Cooke et al . 2002a). Generic characteristics: Elongate, slightly compressed body, depth usually <0.28 of TL. Dusky to black blotch at rear of gill cover (no long opercular flap). Dark, diagonal lines radiating from snout and back of eye to edge of opercle. Clear to olive-yellow fins; dusky spots on median fins. Mouth large, extending at least to below center of eye (in adults), supramaxilla large, well developed (≤2 times length of maxilla). Opercle with two flat projections, lower longer than upper. Emarginate caudal fin. Dorsal fin moderately to deeply emarginate, spiny portion continuous with to almost separate from soft-rayed portion. Long dorsal fin, usually 10 spines (9–10), 12 to 15 rays, usually 22 to 25 total; and short anal fin, 3 spines, 10 to 11 rays, 13 to 15 total. Dorsal fin base about two times longer than anal fin base. Pectoral fin rounded, rays 13 to 18. Preopercle margin entire. Gill rakers moderate in length, 5 to 11. Ctenoid scales. Lateral line complete; lateral line scales, ≥55. Vertebrae, usually 32(30–33) (14 or 15 + 17 or 18). Branchiostegal rays, 6. Pyloric caeca single or branched. Teeth present on palatine (villiform) and ectopterygoid. Teeth absent on endopterygoid and present or absent on glossohyal (tongue) bones (Bailey 1938; Hubbs and Bailey 1940, 1942; Bailey and Hubbs 1949; Bryan 1969; Page and Burr 1991; Mabee 1993; Williams and Burgess 1999). Similar species: Species of Micropterus have three anal fin spines that separate them from all other centrarchids except Lepomis and Enneacanthus. Micropterus have emarginate caudal fins (versus rounded in Enneacanthus) and elongate, slightly compressed bodies with ≥55 lateral scales (versus deep, compressed body and <55 lateral line scales in Enneacanthus and Lepomis).

13.9.1 Micropterus cataractae Williams and Burgess 13.9.1.1 Shoal bass Characteristics: See generic account for general characteristics. Elongate, slightly compressed body, depth 0.20 to 0.26 of TL, increasing with size. Mouth large, terminal, lower jaw slightly projecting, upper jaw reaches to posterior edge of eye in adult. Outline of spinous dorsal fin curved. Juncture of soft and spiny dorsal fins slightly emarginate, broadly connected. Shortest dorsal spine at emargination of fin, usually >0.6 times length of longest spine. Dorsal soft rays, usually 12, 10 to 13; anal soft rays, usually 10, 9 to 11. Gill rakers, usually 7, 6 to 9. Lateral scales, (65)72 to 77(81); rows above lateral line 8 to 9(12); rows below lateral line, (15)17 to 20(24); cheek scale rows, (11)13 to 15(18); caudal peduncle scale rows, (27)30 to 33(35); pectoral rays, (14)16 to 17. Small splintlike scales on interradial membranes at anal and second dorsal fin bases (>60 mm SL). Pyloric caeca, single, rarely branched, usually 12, 8 to 14. Tooth patch absent (a few teeth rarely present) on glossohyal (tongue) bone (Wright 1967; Williams and Burgess 1999; Kassler et al . 2002). Size and age: Typically reach 60 to 109 mm TL (average, 66–96 mm) at age 1 (Parsons and Crittenden 1959; Wright 1967; Hurst 1969). Young-of-the-year stocked in ponds in June at 21 to 24 mm TL reached 142 to 169 mm TL by December (Smitherman and Ramsey 1972). Large individuals reach 380 to 450 mm TL, weigh 0.8 to 1.1 kg, and attain age 6+ to 8+ (maximum about 523 mm TL and 10+ years) (Parsons and Crittenden 1959; Wright 1967; Hurst 1969; Smitherman and Ramsey 1972; Page and Burr 1991; Gilbert 1992a; Williams and Burgess 1999). World angling record, 3.99 kg, Florida (IGFA 2006). Coloration: Body with 10 to 15 midlateral and 6 to 8 dorsolateral, dark vertically elongate blotches, becoming gradually more quadrate posteriorly. Interspaces between midlateral blotches about equal to width of individual blotches,

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and supralateral blotches extend into interspaces between lateral blotches (may be obscured by dark dorsum). The vertically elongate blotches form a distinctive “tiger stripe” pattern. Large square to rectangular basicaudal blotch is usually present. Dusky to dark spots on ventrolateral scales frequently coalesce to form wavy lines. Iris typically bright red. Ground coloration above and on sides of head and body olive green to dark olive to black; body white to cream colored below (Williams and Burgess 1999). Native range: The shoal bass is native to the Apalachicola and Chipola rivers in western Florida, the Chattahoochee River in eastern Alabama and western Georgia, and the Flint River in southwestern Georgia (Page and Burr 1991; Williams and Burgess 1999). In the 1970s, the species was introduced intentionally by state fisheries personnel into the Ocmulgee River (Altamaha River drainage), Georgia, where it is now established along 88 km of the main channel and adjacent tributaries (Williams and Burgess 1999). Habitat: The shoal bass, as the name implies, is a frequent inhabitant of shoal areas of rivers and large streams (Williams and Burgess 1999). Although individuals of all sizes occur in both pools and shoals, as a percentage of the Micropterus assemblage, shoal bass are better represented in shoals. In the Chipola River, Florida, the ratio of age-0 and adult shoal bass to largemouth bass was greater in shoals than in pools (Wheeler and Allen 2003), results consistent with observations elsewhere (Wright 1967). The ratio of age-0 shoal bass to age-0 largemouth bass was 6.9:1 in shoals and 1.4:1 in pools, suggesting shoal habitat as important spawning or nursery areas. Age-0 shoal bass were associated with higher than average percentage of rocky substrate in pools, but not shoals, and larger shoal bass were associated with higher than average percentage of rocky substrate in pools and shoals. Neither was associated with lower than average current speeds in either pools or shoals (Wheeler and Allen 2003). Food: The shoal bass is a top carnivore, exploiting benthic and water column prey (Wright 1967; Hurst 1969; Wheeler and Allen 2003). Adult food consists primarily of fishes (e.g., darters, madtom catfish, minnows, Lepomis spp.), crayfishes, and to a much lesser extent, insects. Fish and crayfish comprise >90% of the diet biomass in fish >140 mm TL. At 40 to 140 mm TL, small shoal bass transition from diets dominated by aquatic insect larvae (e.g., mayflies) to increased consumption of fish and crayfish (Wright 1967; Wheeler and Allen 2003). Reproduction: Females reach maturity at minimum sizes of 152 to 189 mm SL and age 2+, but most mature at age 3+ (Wright 1967; Hurst 1969; Hurst et al . 1975). On the basis of occurrence of ripe, partially spent, or recently spent females and observations in ponds, spawning occurs from April to May (perhaps into June) at water temperatures from 18.0 to 26.0◦ C. Ripe, presumably prespawning, females are taken at temperatures as low as 14.4◦ C in early April (Wright 1967; Hurst 1969; Smitherman and Ramsey 1972; Williams and Burgess 1999). Nests are circular depressions about 30 to 92 cm in diameter and 5 to 15 cm deep. In streams, nests are located in shallow water (20–45 cm deep) of pools upstream of riffles or in eddies adjacent to shoals, and in culture ponds, nests were excavated at water depths of 76 to 130 cm over clay, soft clay rubble, or plant roots (Wright 1967; Hurst 1969; Williams and Burgess 1999). Males reportedly vigorously guard the nest (Williams and Burgess 1999). Observations of a single spawning pair indicated an apparently typical Micropterus spawning sequence that lasted about 45 minutes and resulted in deposition of about 1000 large (2-mm diameter), amber-colored, adhesive eggs. While over the nest, the pair assumed a blotched coloration of dark green vertical bars on a background color of bronze. Other nests contained 500 to 3000 ova (Williams and Burgess 1999). Fecundity increases with female size but is not well quantified. The number of eggs (unclear whether total or mature) in five mature females ranged from 5396 eggs at 314 mm SL and 884 g to 21,799 eggs at 442 mm SL and 2314 g (Wright 1967). Eggs hatch in about 2 days at 21.1◦ C (Smitherman and Ramsey 1972), and yolk-sac larvae, averaging 4.4 mm TL, form tight aggregations in the nest bottom. The larvae reach swim-up about 7 days after hatching and disperse about 12 to 14 days after hatching (Smitherman and Ramsey 1972; Williams and Burgess 1999). Nest associates: None known. Freshwater mussel host: None known. Conservation status: The shoal bass is vulnerable throughout its native range (Warren et al . 2000). The species is considered critically imperiled in Florida, imperiled in Alabama, and vulnerable in Georgia (NatureServe 2006). In the Chattahoochee River, the shoal bass has disappeared from most of the main channel and declined in tributaries because of impoundments eliminating shoal habitats, increased sedimentation, and water quality degradation. Its former distributional

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extent in the Apalachicola and Flint rivers is also reduced by impoundments and channel dredging (Williams and Burgess 1999; Johnston 2004). Similar species: Superficially similar to redeye bass and spotted bass. Shoal bass (92% of specimens) lack a tooth patch on the tongue (versus oval to elongate patch in spotted bass and redeye bass). In adult shoal bass, the anterior half to two-thirds of the body has dark, vertically elongated, midlateral blotches that are separated by lighter areas approximately equal to the width of the blotch (versus irregular to more quadrate blotches in redeye bass); blotches usually confluent to form a midlateral stripe in spotted bass. Shoal bass also lack white outer edges on the caudal fin (present in redeye bass) and have higher caudal peduncle scale counts (Page and Burr 1991; Gilbert 1992a; Williams and Burgess 1999). Systematic notes: Micropterus cataractae is a member of a “Gulf of Mexico” clade of Micropterus, including all other Micropterus except M. dolomieu and Micropterus punctulatus (Kassler et al . 2002; Near et al . 2003, 2004). Relationships within the clade are not well resolved with M. cataractae placed as basal to the entire clade, sister to Micropterus coosae, sister to Micropterus notius, or basal to a clade inclusive of M. notius, M. p. henshalli,Micropterus treculi , and M. salmoides + Micropterus floridanus (Kassler et al . 2002; Near et al . 2003, 2004). Importance to humans: Shoal bass are the signature fish of a productive sport fishery in the Flint River, Georgia, particularly in the upper river (Davis 2006). Anglers wade fish the shoals using fly rods and crayfish-like flies or light to medium spinning gear with a variety of spinners, crayfish imitations, popping bugs, or other bass lures. The fast water habits of the shoal bass, a restricted native range, a scrappy fighting ability, and the propensity to take a fly and dive into the rocks, all combine for an exciting and specialty black bass catch. Supplemental stocking of shoal bass is being undertaken to augment the population in the lower Flint River (Davis 2006).

13.9.2 Micropterus coosae Hubbs and Bailey 13.9.2.1 Redeye bass Characteristics: See generic account for general characteristics. Elongate body, depth 0.20 to 0.24 of TL, increasing with size. Mouth large, terminal, lower jaw slightly projecting, upper jaw extends little or not at all beyond posterior edge of eye. Outline of spinous dorsal fin curved. Juncture of soft and spiny dorsal fins slightly emarginate, broadly connected. Shortest dorsal spine at emargination of fin, usually >0.75 times length of longest spine. Dorsal soft rays, usually 12, 11 to 14; anal soft rays, usually 10, 9 to 11. Gill rakers, (6)7 to 8. Lateral scales, (58)67 to 72(77); rows above lateral line, (7)8 to 9(13); rows below lateral line, (11)14 to 17(21); cheek scale rows, (8)12 to 13(16); caudal peduncle scale rows, (24)26 to 30(31); pectoral rays, (13)15 to 16(17). Small splintlike scales on interradial membranes at anal and second dorsal fin bases (>60 mm SL). Pyloric caeca, usually unbranched, 7 to 12. Teeth present or absent on glossohyal (tongue) bone (Hubbs and Bailey 1940; Ramsey and Smitherman 1972; Turner et al . 1991; Williams and Burgess 1999; Kassler et al . 2002). Size and age: Averages 49 to 63 mm TL (range, 38–68 mm) at age 1 in streams. Growth in ponds and reservoirs can be much higher (≥125 mm TL at age 1) (Parsons 1954; Gwinner et al . 1975; Catchings 1979; Barwick and Moore 1983). Young-of-the-year (22–25 mm TL) stocked in forage-supplemented ponds in June reached 134 mm TL by midDecember (Smitherman and Ramsey 1972; Smitherman 1975) and in some reservoirs individuals average 122 to 125 mm TL at age 1 (Barwick and Moore 1983). Few redeye bass reach 325 mm TL, exceed 225 g, and attain age 5+ to 7+ (maximum about 470 mm TL, 1.44 kg, and age 10+) (Parsons 1954; Smitherman 1975; Carlander 1977; Barwick and Moore 1983; Page and Burr 1991; Etnier and Starnes 1993; Boschung and Mayden 2004; OutdoorAlabama 2006). Redeye bass are perhaps the slowest growing Micropterus. The maximum size attained even in the fastest-growing reservoir populations suggests genetically based size limitations (Barwick and Moore 1983; Moyle 2002). Coloration: Uniquely, among all Micropterus, the outer margins of the caudal fin lobes in redeye bass are narrowly depigmented (in life iridescent white or frosted orange in color, may be less obvious in large individuals) (Ramsey 1975). Color above olive to deep bronze. Back to lateral midline marked with dark, vertically elongate, diamond-shaped to irregularly quadrate blotches, most evident in young, fading with age. Rows of dark spots usually evident on lower sides. Yellow-white ventral area. Iris characteristically red. Breeding males with aqua-blue to blue-green cast on lower half of head and ventral area. Young-of-the-year soft dorsal fin, caudal fin, and front of anal fin tinged brick red to orange; caudal

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fin lacks sharply contrasting tricolored pigmentation (Ramsey and Smitherman 1972; Page and Burr 1991; Turner et al . 1991; Etnier and Starnes 1993; Mettee et al . 1996; Boschung and Mayden 2004). Native range: The redeye bass is native above the Fall Line from the Savannah, Altamaha, and Chattahoochee rivers and the upper Mobile Basin (Coosa, Cahaba, Tallapoosa, and Black Warrior rivers) in North Carolina, South Carolina, Georgia, Tennessee, and Alabama (Page and Burr 1991; Williams and Burgess 1999). The native or introduced status of the species in the Santee River drainage, North and South Carolina, is uncertain (Warren et al . 2000), but preliminary genetic analyses suggest that the population(s) in the Saluda River is introduced (F. C. Rohde personal communication, Division of Marine Fishes, North Carolina). From about 1940 through the 1960s, the species was introduced outside its native range and is now established in tributaries of the Tennessee and Cumberland rivers, Tennessee and Kentucky, and in several drainages in California (Fuller et al . 1999; Moyle 2002). Although often debated as native rather than introduced (e.g., Clay 1975; Koppelman and Garrett 2002), established populations in Martins Fork Cumberland River, Kentucky, were introduced deliberately by state fisheries personnel around 1950 from stock obtained in Georgia (Burr and Warren 1986). In Tennessee and Cumberland river streams, introduced redeye bass have hybridized extensively and likely introgressed with native smallmouth bass (Turner et al . 1991; Pipas and Bulow 1998). Some superabundant stream populations of redeye bass developed after introductions in California, where the species is associated with declines of native minnows, suckers, salamanders, and ranid frogs (Fuller et al . 1999; Moyle 2002). Habitat: The redeye bass inhabits rocky, small upland creeks and small to medium upland rivers, where it is associated with pools, boulders, undercut banks, and water willow beds (Parsons 1954; Page and Burr 1991; Pipas and Bulow 1998; Moyle 2002). The species can be common even in the smallest headwater stream where few other fish and no other Micropterus occur (Parsons 1954; Ramsey 1975; Pipas and Bulow 1998). The redeye bass has been viewed traditionally as potentially providing a fishery in waters too cool and small for other Micropterus but too warm for trout (e.g., Parsons 1954; Carlander 1977). These conditions, however, are not prerequisites for establishment of thriving redeye bass populations in nonnative habitats (Pipas and Bulow 1998; Moyle 2002). Indirect evidence suggests that redeye bass make large upstream migrations to tributaries to spawn in the spring (and conversely downstream fall migrations to winter habitat) (Parsons 1954). Redeye bass are generally intolerant of ponds and most reservoirs (Parsons 1954; Wood et al . 1956; Webb and Reeves 1975; Moyle 2002; but see Barwick and Moore 1983). Food: The redeye bass is an opportunistic carnivore, feeding from the surface to the bottom. The summer diet in streams consists primarily of terrestrial insects and crayfish. To a lesser extent, stream-dwelling redeye bass also consume small fishes (e.g., minnows and darters), aquatic insects, and salamanders (Parsons 1954; Smitherman 1975; Gwinner et al . 1975). Large redeye bass (>216 mm TL) in oligotrophic reservoirs in South Carolina are primarily piscivorous (Barwick and Moore 1983). Reproduction: Maturity is reached at a minimum size of 120 mm TL at age 3+ in females and age 4+ in males in streams, but faster growing pond-cultured individuals matured at age 1+ (Parsons 1954; Smitherman 1975). Spawning extends from April to early July as water temperatures reach 18 to 21◦ C (Parsons 1954; Smitherman and Ramsey 1972; Gwinner et al . 1975). Practically nothing is published on male or female reproductive behaviors, and overall knowledge about the reproductive biology of redeye bass is at best sketchy. Nests are shallow, circular depressions in coarse gravel at the heads of pools (Parsons 1954). Fertilized, water-hardened eggs average 3.5 mm in diameter (Smitherman and Ramsey 1972). Relationships between female size and fecundity are unquantified. Two females of 145 and 205 mm TL contained 2084 and 2334 eggs, respectively (Parsons 1954). Eggs hatch in about 2 days at 22.8◦ C; yolk-sac larvae are 6.0 mm TL, and larvae are free swimming at 7 to 8 mm TL about 5 days after hatching (Smitherman and Ramsey 1972). An anecdotal account suggests that fry school for a short time relative to most Micropterus (Parsons 1954). In a culture pond, complete breakup of schools occurred at 16 to 25 mm TL about 14 days after swim-up, but school breakup began as early as 6 days after swim-up (Smitherman and Ramsey 1972). Nest associates: None known. Freshwater mussel host: Confirmed host to L. altilis, Lampsilis perovalis, V. nebulosa, and V. vibex (Haag and Warren 1997; Haag et al . 1999). Conservation status: The redeye bass is secure throughout its range (Warren et al . 2000), but native populations on the periphery of the range are considered vulnerable (Tennessee) or critically imperiled (North Carolina) (NatureServe

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2006). Obversely, the past introduction and establishment of redeye bass outside its native range now threatens the genetic integrity of populations of native Micropterus (Turner et al . 1991; Pipas and Bulow 1998). Similar species: See accounts on Suwannee bass and spotted bass. Differs from all other Micropterus in having the outer margins of the caudal fin lobes narrowly depigmented (iridescent white or frosted orange in life) (Ramsey 1975; Page and Burr 1991). Systematic notes: Micropterus coosae is a member of a “Gulf of Mexico” clade of Micropterus, including all other Micropterus except M. dolomieu and M. punctulatus (Near et al . 2003, 2004). Relationships within the clade are not well resolved with M. coosae placed as basal to the clade, sister to M. cataractae, sister to M. punctulatus henshalli (the Alabama spotted bass), or basal to M. notius, M. treculi, and M. salmoides + M. floridanus (Kassler et al . 2002; Near et al . 2003). Similarities in form, color, behavior, and ecology led most morphological taxonomists to relate M. coosae to M. dolomieu or M. punctulatus (e.g., Hubbs and Bailey 1940; Ramsey 1975). Data from nuclear-encoded allozyme loci and mitochondrial DNA reveal significant genetic substructuring among populations now known as redeye bass and strongly suggest the existence of multiple, and perhaps specifically distinct, evolutionary lineages (Kassler et al . 2002; Koppelman and Garrett 2002). The evolutionary relationships among populations of redeye bass, and of redeye bass to other Micropterus, particularly the Alabama spotted bass (see account on M. punctulatus), await thorough genetic evaluation. Importance to humans: The attractive redeye bass is regarded as a somewhat wary, but scrappy fighter in small, wadeable streams, where it provides an exciting catch on ultralight gear combined with small lures and spinners, popping bugs and flies, or natural bait (Parsons 1954; Etnier and Starnes 1993). In its small stream habitat, redeye bass populations can provide a minimal catch-and-release fishery, but slow growth rates limit establishment of harvestable stream fisheries (Pipas and Bulow 1998).

13.9.3 Micropterus dolomieu (Lac´ep`ede) 13.9.3.1 Smallmouth bass Characteristics: Elongate, slightly compressed body, depth 0.18 to 0.28 of TL, decreasing with size. Mouth large, terminal, lower jaw slightly projecting, upper jaw extends at least to below center of eye but not beyond posterior edge of eye. Outline of spinous dorsal fin curved. Juncture of soft and spiny dorsal fins slightly emarginate, broadly connected. Shortest dorsal spine at emargination of fin, usually >0.5 times the length of the longest spine. Dorsal soft rays, usually 13 or 14, 10 to 15; anal soft rays, usually 11, 9 to 12. Gill rakers, 6 to 8. Lateral scales, (64)69 to 77(81); rows above lateral line, (10)12 to 13(15); rows below lateral line, (16)19 to 23(32); cheek scale rows, (13)15 to 18(20); caudal peduncle scale rows, (26)29 to 31(33); pectoral rays, (13)16 to 17(18). Small splintlike scales on interradial membranes at anal and second dorsal fin bases (>60 mm SL). Pyloric caeca, unbranched, about 10 to 15. Teeth present or absent on glossohyal (tongue) bone (Bailey 1938; Hubbs and Bailey 1938, 1940; Smitherman and Ramsey 1972; Turner et al . 1991; Kassler et al . 2002). Size and age: Size at age 1 is highly variable among habitats and across latitudes and ranges from 40 to 188 mm TL (median 92 mm TL) (Beamesderfer and North 1995). Large individuals can exceed 400 mm TL, weigh 1.5 to 2.5 kg, and attain age 6+ to 12+ (maximum 686 mm TL, 5.2 kg, and age 14+) (Scott and Crossman 1973; Carlander 1977; Paragamian 1984; Page and Burr 1991; Weathers and Bain 1992; Beamesderfer and North 1995; MacMillan et al . 2002). World angling record, 4.93 kg, Tennessee (IGFA 2006). Growth rates are similar between males and females (Carlander 1977). Coloration: No dark lateral band. Dark brown with numerous bronze markings on scales, often with 8 to 16 indistinct vertical bars on a yellow-green to brown side. Olive brown with bronze specks above, yellow to white below. Iris usually reddish. Large male is green-brown to bronze with dark mottling on back and dark vertical bars on the side. Young (<50 mm TL) boldly patterned with vertical bars and blotches and distinct, contrasting tricolored caudal fin markings (yellowish base, black middle, whitish distal edge) (Page and Burr 1991; Etnier and Starnes 1993; Ross 2001). Native range: The smallmouth bass is native to the St. Lawrence-Great Lakes, Hudson Bay (Red River), and Mississippi River basins from southern Quebec to North Dakota and south to northern Alabama and eastern Oklahoma (Hubbs and Bailey 1938; Page and Burr 1991). The species has been introduced widely and is now established throughout southern Canada and the United States, except in Atlantic and Gulf Slope drainages, where it is rare from south of Virginia to

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eastern Texas (MacCrimmon and Robbins 1975; Page and Burr 1991; Jenkins and Burkhead 1994; Snyder et al . 1996; Fuller et al . 1999). Nonnative smallmouth bass can hybridize and introgress with native species of Micropterus, ultimately compromising the genetic integrity of the native bass, and as a top predator, smallmouth bass may have profound direct and indirect impacts on native fishes and whole aquatic ecosystems. The most egregious case of introgression involves the near total genetic swamping of the range-restricted Guadalupe bass, M. treculi (Whitmore and Butler 1982; Whitmore 1983; Whitmore and Hellier 1988; Morizot et al . 1991; Pierce and Van Den Avyle 1997; Koppelman and Garrett 2002). Predation effects by nonnative smallmouth bass in Canadian lakes resulted in dramatic changes in food–web dynamics and shifted the native top predator, the lake trout (Salvelinus namaycush), from a primary diet of littoral fishes to zooplankton. The consequences for the affected lake trout populations are potentially severe (Vander Zanden et al . 1999, 2004). Established, nonnative populations of smallmouth bass are also implicated in loss in diversity of nongame freshwater fishes, impacts on migrating salmon, and declines in native amphibians (Bennett et al . 1991; Tabor et al . 1993; Chapleau and Findlay 1997; Findlay et al . 2000; MacRae and Jackson 2001; Jackson 2002; Moyle 2002; Fritts and Pearsons 2004, 2006; Weidel et al . 2007). Habitat: The smallmouth bass inhabits clear, cool, runs and pools of small to large rocky rivers and the rocky shorelines of lakes and reservoirs (Page and Burr 1991). Although frequently and justifiably described as inhabiting clearer and cooler waters than other Micropterus, co-occurrence with congeners across the large north-to-south range is common (e.g., Funk 1975), but abundances of smallmouth bass among mesohabitats often differ from co-occurring Micropterus. For example, in a Kentucky reservoir with three Micropterus species, smallmouth bass tended to be most abundant and largemouth bass least abundant in the oligotrophic section, and spotted bass showed highest abundance in both mesotrophic and oligotrophic sections (Buynak et al . 1989). Similarly, in Ozark Border streams in Missouri, abundance of smallmouth bass is related inversely to percent pool area and maximum summer water temperature, a pattern opposite to that observed for largemouth bass (Sowa and Rabeni 1995). Across its broad range, the smallmouth bass occupies a wide variety of habitats depending on life stage, food availability, and habitat conditions, but the most consistent physical habitat association for adults in rivers, lakes, and reservoirs is proximity to submerged cover (e.g., steep drop-offs, ledges, crevices, boulders, stumps, logs, logjams). Juveniles are often associated with large substrates relative to their body size, but can also use a wide range of currents, depths, substrates, and cover types. The habitat, environmental tolerances, bioenergetics, and spatial ecology of the smallmouth bass from hatching to adult in both lake and riverine environments are documented extensively. Here the focus is to briefly introduce aspects of smallmouth bass movement in lake and riverine environments and some effects of temperature, pH, and DO on the species. A wealth of detailed information is available in the references cited in this account and many other original sources, reviews, and syntheses (e.g., Robbins and MacCrimmon 1974; Coble 1975; Coutant 1975; MacCrimmon and Robbins 1981; Rankin 1986; McClendon and Rabeni 1987; Bain et al . 1988; Leonard and Orth 1988; Simonson and Swenson 1990; DeAngelis et al . 1991, 1993; Lobb and Orth 1991; Lyons 1991; Armour 1993; Jager et al . 1993; Barrett and Maughan 1994; Smale and Rabeni 1995b; Walters and Wilson 1996; Peterson and Kwak 1999; Zweifel et al . 1999; Cooke et al . 2000b, 2002b; Philipp and Ridgway 2002; Whitledge et al . 2006; Brewer et al . 2007; Dunlop et al . 2007). In lakes and streams, smallmouth bass rather consistently remain in home areas in summer but can make seasonal movements to specific wintering areas and traverse relatively long distances in apparent exploratory movements (e.g., 66 km) or to return to a home area after being displaced (e.g., Funk 1957; Fajen 1962; Reynolds 1965; Carlander 1977; Gerber and Haynes 1988; Kraai et al . 1991; Peterson and Rabeni 1996; Ridgway and Shuter 1996; Hayes et al . 1997; Lyons and Kanehl 2002; Bunt et al . 2002; Ridgway et al . 2002; VanArnum et al . 2004). In summer, adults in lakes or reservoirs occupy persistent (weeks to months) postspawning home activity areas (0.2–43 ha) that are usually along rocky shorelines (or areas of steep bottom relief), but during this time individuals may frequently shift areas occupied and, in some cases, move extensively and apparently randomly (Hubert and Lackey 1980; Kraai et al . 1991; Savitz et al . 1993; Demers et al . 1996; Cole and Moring 1997). The size of the activity area is related positively to fish size; larger fish tend to include depths >4 m in their activity areas, and at least some individuals occupy distinctive diurnal and nocturnal activity areas (Emery 1973; Savitz et al . 1993; Cole and Moring 1997). In Lake Opeongo, Ontario, smallmouth bass use the largest recorded summer home ranges among centrarchids. Average postnesting home range area is 247 ha for males and 409 ha females, but core use areas (50% use) are smaller (38.4 ha) and similar between sexes. Individual male summer home ranges show high coincidence from year to year, indicating that males in the lake return from nesting areas to the same home ranges over multiple years (Ridgway and Shuter 1996; Ridgway et al . 2002). Daytime movements within these large home ranges are extensive, averaging 4.8 km over 6- to 16-hour periods (about 483 m/h), but there is little activity at

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night (Ridgway et al . 2002). The differences in home range size estimates among smallmouth bass in different lakes may be attributable to methods used to estimate home range (e.g., Savitz et al . 1993; Cole and Moring 1997; Ridgway et al . 2002) but may also reflect differences in resource availability (e.g., forage, cover) or in population-specific adaptations. Riverine smallmouth bass also show high persistence in relatively small areas throughout the summer months, but fall movement to winter habitats varies among populations (review by Lyons and Kanehl 2002). In a Missouri stream, postspawning home ranges and intrapool movement of adults were greater in summer (0.09 to 0.67 ha, up to 980 m/d at 27.5◦ C) than in winter (0.06 to 0.22 ha, 120 m/d at 4◦ C), but fish generally used the same stream sections in winter and summer, moving elsewhere only during the spawning season (Todd and Rabeni 1989). In small Ouachita Mountain streams, interpool movement of smallmouth bass in summer was high, with 35% of marked individuals moving among adjacent pools over a 3-day observation period (Lonzarich et al . 2000). Similarly, recolonization rates after complete removal were high; pool populations reached pre-removal abundances in 40 days (Lonzarich et al . 1998). Some populations of riverine smallmouth bass, particularly those in areas with severe winters, make fall migrations of several to over 100 km to wintering habitats (usually to downstream bodies of water) (e.g., Langhurst and Schoenike 1990; Peterson and Rabeni 1996; Cooke et al . 2000a; Lyons and Kanehl 2002; Schreer and Cooke 2002). Movement to wintering areas can involve numerous short movements with rest periods of several days, or long distances may be covered in short periods (Lyons and Kanehl 2002). For example, a smallmouth bass migrating to downstream wintering habitats in Wisconsin moved 19 km in 24 hours (Langhurst and Schoenike 1990). Latitudinal differences in temperature and regional variation in annual temperatures exert considerable influence on smallmouth bass distribution, abundance, growth, and survival. A model using temperature, food availability, and lake depth to predict young-of-the-year growth and winter mortality accurately delimited the northern distributional limit of the species (Shuter and Post 1990). Average July temperatures <15◦ C prevent young-of-the-year from reaching sufficient size to overwinter, precluding long-term viability of populations on the northern edge of the range (Shuter et al . 1980). At northern latitudes, a short-growing season and long, cold winters combined with variability in food availability (e.g., low productivity, high competition) and hence energy reserves can dramatically increase overwinter mortality (to 100%) of young-of-the-year smallmouth bass (Oliver et al . 1979; Shuter et al . 1989; Lyons 1997; Curry et al . 2005). In an analysis of data for 409 smallmouth bass populations across North America, age at length was correlated negatively with mean air temperature (and degree days >10◦ C) (Beamesderfer and North 1995). In a study of 129 geographically widespread populations, temperature-related climate differences were significantly related to growth and were most influential in the first 4 years of life (Dunlop and Shuter 2006). On a regional scale, population structure of smallmouth bass in the Laurentian Great Lakes closely tracked changes in water temperatures over several decades. Notably, steep declines in growth and year-class strength occurred with minor temperature shifts (mean shifts <3◦ C) caused by global climate events (i.e. peak La Ni˜na cooling effects and eruption of Mount Pinatubo, Philippines in 1992; King et al . 1999; Casselman et al . 2002). In the upper Mississippi River, first-year growth was also influenced strongly by temperature variation over a 14-year period (Swenson et al . 2002). When temperature effects were considered independent of water velocity, modeled first-year growth increased an estimated 7 mm for each 100–degree day increase in growing season temperatures. At even smaller spatial scales, rapid water temperature changes associated with sporadic flooding events in streams can dramatically reduce the probability of survival in larval smallmouth bass by affecting their ability to negotiate current and effectively forage (Larimore 2002). Similarly, minor wind-induced increases in temperature (0.6–1.3◦ C) (and zooplankton abundance) in downwind areas of northern lakes are implicated, although not conclusively so, in nest-site selection by males and in faster growth of young (Kaevats et al . 2005). Smallmouth bass are among the most sensitive of the centrarchids to reduced pH. Field and laboratory studies demonstrate reproductive impairment at pH <6.0 and total curtailment of recruitment at pH <5.5, depending in part on antagonistic effects of Al and Ca concentrations, fish size, and energy reserves (Rahel and Magnuson 1983; Kwain et al . 1984; Cunningham and Shuter 1986; Kane and Rabeni 1987; Hill et al . 1988; Holtze and Hutchinson 1989; Shuter and Ihssen 1991; Snucins and Shuter 1991). After experimental stocking of adults in small northern lakes, population estimates over three spawning seasons indicated no recruitment at pH 4.9 to 5.2, and population size was low at pH 5.4 (4–12% of number stocked) relative to a lake with pH 5.9 (41–55%) (Snucins and Shuter 1991). Complete mortality of smallmouth bass larvae and post larvae occurred within 3 days at pH 5.1 and 180 µg/l Al and within 5 days at pH 5.5 and 203 µg/l Al (Kane and Rabeni 1987). In post swim-up larvae (3–36 days old), survival (relative to controls at pH 7) declined to 43% at pH 5.7 and to near zero at pH 5.0 (Hill et al . 1988). Natural stress of overwinter starvation is significantly augmented even by moderate exposures to nonlethal low pH, but tolerance increases with body size and Ca concentration (Cunningham and Shuter 1986; Shuter et al . 1989; Shuter and Ihssen 1991). An exposure to pH 5.5 increases overwinter starvation loss by

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16%, a loss rate that could significantly affect viability of smallmouth bass populations by increasing young-of-the-year starvation (Shuter et al . 1989). Smallmouth bass are more sensitive to hypoxia than many other centrarchids. Of five tested centrarchids (three Lepomis spp. and largemouth bass), smallmouth bass showed the highest critical DO concentration (average, 1.19 mg/l at 26◦ C) (Smale and Rabeni 1995a). Across graded levels of hypoxia, blood plasma adrenalines and noradrenalines, which are indicators of stress, dramatically increased in the blood of smallmouth bass but not largemouth bass. Increases in ventilation rate and decreases in cardiac output also were more pronounced in smallmouth bass than in largemouth bass (Furimsky et al . 2003). The differential physiological responses of the two species to hypoxia are likely attributable to differences in the ability of their blood to bind DO (Cech et al . 1979; Furimsky et al . 2003). Food: The smallmouth bass is an opportunistic, top carnivore, feeding from the surface to the bottom. The biomass of the adult diet is predominately fish, and if available, crayfish, but adult smallmouth bass also consume an occasional terrestrial vertebrate (e.g., frog) and a wide variety of aquatic and terrestrial insects, the latter being most commonly eaten in small lakes and streams. In lakes and reservoirs with few crayfishes, individuals of >100 mm TL almost exclusively eat fish (e.g., clupeids, Lepomis, yellow perch), but if crayfish are present, individuals of <300 mm TL consume large volumes of crayfish (Applegate et al . 1967; Hubert 1977; Danehy and Ringler 1991; Gilliland et al . 1991; Scott and Angermeier 1998; Liao et al . 2002; Dunlop et al . 2005b). Young smallmouth bass initially consume microcrustaceans and a wide variety of small aquatic insects, especially dipteran and mayfly larvae, and other invertebrates but transition between 20 and 100 mm TL to the adult diet. The breadth and extent of diet and timing of ontogenetic dietary shifts vary considerably in smallmouth bass in response to interactions among habitat quality, competition, and prey availability (e.g., Hubbs and Bailey 1938; Applegate et al . 1967; Clady 1974; Carlander 1977; George and Hadley 1979; Probst et al . 1984; Angermeier 1985; Livingstone and Rabeni 1991; Easton and Orth 1992; Rabeni 1992; Roell and Orth 1993; Sabo and Orth 1994, 2002; Sabo et al . 1996; Easton et al . 1996; Pelham et al . 2001; Orth and Newcomb 2002; Pert et al . 2002; Olson and Young 2003; Dunlop et al . 2005b). In streams, energy from crayfishes may provide over half the total production of smallmouth bass and over 60% of the energy of adult smallmouth bass, the remainder being obtained from fishes, particularly cyprinids such as stonerollers (Campostoma sp.) (Rabeni 1992). In these systems, smallmouth bass can remove about a third of crayfish production and nearly two-thirds of the biomass of crayfishes of vulnerable size. Most crayfish eaten are between 14 and 46 mm (carapace length), even though the available size range of crayfish in the streams is much larger and changes seasonally (Rabeni 1992; Roell and Orth 1993). Interestingly, in a Missouri stream, the size of smallmouth bass and the size of crayfishes eaten were not related. Gape limitation or other morphological constraints apparently were not operative, but rather, there was an optimum size range of crayfishes common to all sizes of bass (>100 mm TL) (Probst et al . 1984). In a northern lake and associated laboratory research, size of crayfish prey was related positively to smallmouth bass size, but complex interactions of substrate type and crayfish size, sex, and life stage affected bass selectivity (Stein 1977). Smallmouth bass foraging behaviors appear well adapted for benthic prey. Compared to largemouth bass, foraging smallmouth bass keep the body more horizontal in inspecting the bottom, remain closer to the substrate, and use biting actions more often in feeding. The species uses combinations of suction feeding and grasping and jerking to dislodge crayfishes from rock crevices, but largemouth bass rely primarily on suction feeding (Winemiller and Taylor 1987). Smallmouth bass are primarily diurnal in habit with activity typically greatly diminishing at night. Feeding and activity peaks are often noted at dawn or dusk, but fish can feed opportunistically over a 24-hour period (Munther 1970; Reynolds and Casterlin 1976b; Helfman 1981; Gerber and Haynes 1988; Todd and Rabeni 1989; Kwak et al . 1992; Johnson and Dropkin 1993; Demers et al . 1996; Ridgway et al . 2002). Nighttime samples taken in the fall in a Pennsylvania river revealed food in stomachs (primarily mayfly larvae and crayfish by weight) of over 60% of smallmouth bass examined (65–346 mm TL, n = 60) (Johnson and Dropkin 1993). Nighttime angling in summer in the Tennessee River, Alabama, accounts for a substantial proportion of the smallmouth bass catch (Weathers and Bain 1992), also suggesting nighttime feeding or at least a propensity to feed at night. Prey consumption by smallmouth bass is affected by turbidity. The reactive distance of smallmouth bass (99 mm TL) to 10-mm prey (dipteran larvae) decreased exponentially from about 65 to 10 cm as turbidity increased from <5 to 40 NTU (at 49 lux) in laboratory trials (Sweka and Hartman 2003). As highly effective top predators, smallmouth bass can cause shifts in fish assemblages, redistribution or elimination of prey, and dramatic changes in prey behavior. In small Ontario lakes, the presence of smallmouth bass was linked to reduced abundance, altered habitat use, and extirpation of a suite of small-bodied fishes, primarily cyprinids and brook stickleback (MacRae and Jackson 2001). Similar direct and indirect interactions of small-bodied fishes and predation by

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smallmouth bass are documented across lakes in southern Canada and the northeastern United States (e.g., Chapleau and Findlay 1997; Whittier et al . 1997; Whittier and Kincaid 1999; Vander Zanden et al . 1999, 2004; Findlay et al . 2000; Jackson 2002; Morbey et al . 2007). In experimental and natural streams, several small-bodied fish species shifted habitat use from deep pools to the refuge of shallow-flowing habitats when smallmouth bass were present (Schlosser 1988a,b, but see Harvey et al . 1988). In experimental tanks with smallmouth bass, the benthic-dwelling johnny darter (Etheostoma nigrum) reduced activity to 6% of that observed in tanks without bass, spending most of the time under tile shelters. Even after removal of the bass, darters remained inactive and under shelters for about 24 hours, indicative of a strong residual effect of the predator’s presence (Rahel and Stein 1988). In field and laboratory trials, predation risk from smallmouth bass induced shifts in microdistribution (e.g., larger substrate use, hiding in burrows) and behavior (e.g., reduced walking, climbing, and feeding) of small lake-dwelling crayfish, and in experimental streams, the presence of smallmouth bass reduced crayfish activity, aggressive behaviors, and pool use (Stein and Magnuson 1976; Stein 1977; Mather and Stein 1993). Interestingly, daytime larval minnow abundance was influenced differentially by the presence of juvenile and adult smallmouth bass in natural and experimentally manipulated stream pools. Minnow larvae were less abundant in pools with juvenile smallmouth bass and more abundant in pools with adult smallmouth bass. The presence of adult smallmouth bass in a pool apparently reduced the risk to larval fish of predation from juvenile bass and other predators (e.g., Lepomis) (Harvey 1991b). Reproduction: Depending in part on latitude, females mature minimally at age 3+ to 7+ (≥220 mm TL) and males at age 2 + to 5+ (≥200 mm TL) (Carlander 1977; Hubert and Mitchell 1979; Vogele 1981; Serns 1984; Raffetto et al . 1990; Ridgway and Friesen 1992; Wiegmann et al . 1992; Dunlop et al . 2005a,b). Male size appears more important than age in attaining maturity (Wiegmann et al . 1997; Dunlop et al . 2005a). Many smallmouth bass populations make regular spring migrations to spawning areas and exhibit a high degree of nestsite fidelity. Patterns of spring movements, some involving relatively long distances (5–75 km), from wintering to spawning areas are documented in populations inhabiting streams, rivers, lakes, and reservoirs (e.g., Reynolds 1965; Hubert and Lackey 1980; Todd and Rabeni 1989; Kraai et al . 1991). Movement associated with spawning appears to be population or context specific, perhaps reflecting suitability and availability of nesting sites. Individuals may move to spawning areas and stay until fall, move to spawning areas and then return to home areas after spawning, or spawn in the general area where they occur all year (e.g., Pflieger 1975; Todd and Rabeni 1989; Lyons and Kanehl 2002). Some lake-dwelling populations make large, regular spring migrations of >10 km into lake tributaries to spawn, returning to the lake after reproduction (Lyons and Kanehl 2002), and others consistently use nesting areas within a lake that are spatially distinct from nonspawning home areas. Over a multiyear, multigenerational field study in a Canadian lake, >71% of renesting smallmouth bass males returned to within 100-m linear distance of their previous year’s nest site, even though nest habitats were not limiting. In subsequent years, about 35% returned to within 20 m of their original nest site, nesting largely in or adjacent to their old nest (Ridgway et al . 1991a, 2002). Nest aggregations along lake shorelines are consistently patchy across years (Rejwan et al . 1997), indicative of selection of specific nesting areas, and genetic analyses of offspring from individual nests further support high nest-site fidelity in the species (Gross et al . 1994). In natural settings, smallmouth bass spawn from about April to mid-July at southern latitudes and mid-May to mid-June on the northern edge of the range (Pflieger 1966a, 1975; Neves 1975; Hubert and Mitchell 1979; Vogele 1981; Wrenn 1984; Graham and Orth 1986; Ridgway and Friesen 1992). A second spawning period or multiple renestings may occur, especially if early broods are lost because of high flows and temperature decreases (Beeman 1924; Surber 1943; Pflieger 1966a, 1975; Coble 1975; Neves 1975; Lukas and Orth 1995; Cooke et al . 2003a, 2006). Spawning activity and active nests span a broad range of temperatures (12.0–26.7◦ C); however, most spawning is initiated as water temperatures gradually rise and exceed 15◦ C, and peak spawning continues to 22◦ C (e.g., Pflieger 1966a; Smitherman and Ramsey 1972; Neves 1975; Carlander 1977; Shuter et al . 1980; Vogele 1981; Wrenn 1984; Graham and Orth 1986; Cooke et al . 2003a). Large mature males nest earlier (i.e. at lower temperatures and fewer accumulated degree days >10◦ C before spawning) than small mature males; females show similar size-related timing in spawning (Ridgway et al . 1991b; Wiegmann et al . 1992; Baylis et al . 1993; Lukas and Orth 1995). Smallmouth bass from the Tennessee River exposed to water temperatures of 2.6, 5.2, and 8.0◦ C above ambient temperature (beginning in December) showed spawning peaks of 9, 16, and 25 days, respectively, before control fish exposed to ambient river water temperatures (Wrenn 1984). Likewise, in a thermally unstable, but heated effluent canal in Lake Erie, spawning of smallmouth bass was advanced about 1 month relative to spawning in the lake (Cooke et al . 2003a). Simulated, compressed winter conditions (short photoperiods, temperatures ∼ 6◦ C) followed by

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20 to 22 days of exposure to increasing photoperiod (14 hours) and temperature (18◦ C) induces out-of-season spawning, but increasing temperature alone does not appear to induce spawning (Cantin and Bromage 1991). Male smallmouth bass establish a territory and use caudal sweeping to excavate a circular depressional nest down to coarse gravel–cobble substrates, bedrock, or even hard clay. Nests average 45 to 93 cm in diameter and are often near (or just downstream of) rocky or woody cover. In lakes and reservoirs, nests are usually placed in water <4.0 m deep (to 6.7 m). In streams, nests are placed in low-velocity habitats, usually in water <0.75 m deep (Surber 1943; Pflieger 1966a; Neves 1975; Vogele and Rainwater 1975; Carlander 1977; Vogele 1981; Winemiller and Taylor 1982; Lukas and Orth 1995; Bozek et al . 2002; Orth and Newcomb 2002; Saunders et al . 2002; Bozek et al . 2002; Steinhart et al . 2005). In riverine habitats, smallmouth bass nests generally are spaced widely, rarely exceeding 3/100 m, although average internest distances of 4.2 m are reported (Surber 1943; Pflieger 1966a, 1975; Coble 1975; Lukas and Orth 1995; Knotek and Orth 1998). In lakes, nesting areas are patchily, but nonrandomly, distributed, and highest nest densities occur in areas with >17.0◦ C water temperatures and high shoreline complexity (Rejwan et al . 1997). Within a nesting area in lakes, densities are usually 1 to 5 nests/100 m of shoreline, but even when highly concentrated, nest density rarely exceeds 7 nests/100 m of shoreline (Vogele 1981; Scott 1996; Rejwan et al . 1997, 1999; Saunders et al . 2002). Nest spacing in lakes matches the shape and size of the male’s territory (≥18 m apart) and the area needed for foraging of the free-swimming brood but is much greater than that predicted for randomly established nests (Scott 1996). Greater internest spacing and presence of cover increases the probability of mating success of male smallmouth bass (Winemiller and Taylor 1982; Wiegmann et al . 1992). Once the nest is prepared, the male engages in long periods of fanning with the pectoral and median fins. The male intersperses bouts of fanning with frequent reorientation of his longitudinal axis by pivoting the body around the center of the nest (45–900 /turn; 0.5–1.2 turns/s), the pivots being an apparent effort to detect rivals or females around the nest (Beeman 1924; Pflieger 1966a; Winemiller and Taylor 1982). Depending in part on availability of females, elapsed time between nest construction and egg deposition is usually 2 days, but ranges from a few hours up to 16 days (Pflieger 1966a; Wrenn 1984; Ridgway et al . 1991b). Males periodically leave the nest to locate spawning-ready females and once located, use push–lead behaviors (jaw displays, contact nips) to direct the female to the nest (Ridgway et al . 1989). During courtship and spawning, the male’s iris becomes bright red, and the female develops a series of dark vertical bars or mottlings against a light background that are lacking in the breeding male (Breder and Rosen 1966; Schneider 1971; Ridgway et al . 1989). In response to male courtship, the spawning-ready female assumes a head-down posture and under coaxing from the male slowly moves toward the nest, where the pair begins circling high above the nest (male below, female above), slowly descending toward the nest as they circle. Ultimately, the pair starts circling the nest rim (female inside, male outside). During circling, the male contact nips the female’s opercle and ventral area (pelvic fins to vent). Finally, the two settle to the substrate, the female performs a body wave (i.e. a gentle swinging of her head and caudal peduncle from side to side while in an upright position and close beside the male), tilts to the side, places her vent near the male’s vent, and quivers while releasing eggs. The male remains upright during milt release. After egg release, the female rises above the nest in a head-down posture. The complete sequence of rim circling, male to female contact nips, and female quivering occurs repeatedly with brief pauses in between sequences (Schneider 1971; Ridgway et al . 1989). The complete spawning bout with a female can last >2 hours and involve 103 female shudders at 30- to 60-second intervals with up to 50 eggs released per shudder. On completion of the bout, the male drives the female from the nest (Reighard 1906; Schneider 1971; Neves 1975). Multiple complete spawning observations, female batch fecundity, and egg developmental stages in nests in natural settings indicate that most males mate with one female, but some males may mate sequentially (or simultaneously) with more than one female (Beeman 1924; Hubbs and Bailey 1938; Neves 1975; Vogele 1981; Ridgway et al . 1989; Wiegmann et al . 1992). Large guardian males are more likely to successfully attract and spawn with females, but in some populations, many males of various sizes build nests but are unsuccessful in attracting mates (Winemiller and Taylor 1982; Wiegmann et al . 1992; Baylis et al . 1993). Of males spawning with females, large guardian males receive more eggs and defend the brood more tenaciously than small guardian males, ultimately producing larger broods, which may in part explain the apparent female mate preference for larger males (Neves 1975; Ridgway and Friesen 1992; Lukas and Orth 1995; Wiegmann and Baylis 1995; Wiegmann et al . 1992, 1997; Knotek and Orth 1998). Mature ovarian eggs average from 1.60 to 2.75 mm diameter, and fertilized, water-hardened eggs from 2.0 to 3.5 mm diameter (Meyer 1970; Smitherman and Ramsey 1972; Hubert 1976; Vogele 1981; Wrenn 1984; Cooke et al . 2006). Fecundity increases with female weight, length, and age (Clady 1975; Hubert 1976; Kilambi et al . 1977; Vogele 1981; Serns 1984; Dunlop et al . 2005b). Bimodal egg size classes occur in ovaries of spawning-ready females, suggesting that females have the potential to spawn multiple batches of eggs in a single spawning season. However, over the relatively short

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spawning season secondary stage ova do not appear to mature after the initial batch is spawned, being resorbed in summer (Hubert and Mitchell 1979; Vogele 1981). The relationship between potential batch fecundity (Y) and total weight or length (X) are described by the linear functions, Y = −1, 347 + 13.65X, where X is weight in grams (n = 21, R2 = 0.85), or Y = −1225.15 + 59.39X, where X is TL (n = 74, R2 = 0.39) (formulas from Vogele 1981 and Raffetto et al . 1990, respectively; see also, Hubert 1976; Kilambi et al . 1977; Dunlop et al . 2005b). At 549 g (about 335 mm TL), a female can potentially produce 6147 mature eggs in a single batch (range: 1724 eggs at 221 g to 21,467 eggs at 1471 g). Average number of eggs per nest ranges from 2149 to 7757 (>19, 000 in some nests) (Pflieger 1966a; Clady 1975; Neves 1975; Vogele 1981; Raffetto et al . 1990; Wiegmann et al . 1992). The adhesive, grayish white to pale yellow fertilized eggs hatch in 6.4 days at 16◦ C (2.4 days at 22◦ C, from formula in Shuter et al . 1980). Larvae are 4.4 to 6.8 mm TL at hatching, and depending on water temperature, are free swimming at a size of 8.1 to 10.1 mm TL in 4 to 16 days after hatching (Reighard 1906; Beeman 1924; Tester 1930; Hubbs and Bailey 1938; Meyer 1970; Hardy 1978; Shuter et al . 1980; Vogele 1981; Wrenn 1984; Ridgway and Friesen 1992). At swim-up, smallmouth bass fry begin a diel cycle of moving away from the nest at dawn and returning to the nest at dusk, and the guardian male shows parallel behavior (Ridgway 1988). During the swim-up phase, the brood disperses over about 13.4 m2 relative to the guardian male’s nest range of 22.7 m2 . Later, during the juvenile guarding phase, the brood disperses in the day time over 82.4 m2 , and the male over 176.9 m2 . At dusk, fry and male ranges decrease to 3.1 and 20.7 m2 , respectively. The male apparently responds to changes in brood dispersal and not vice versa, because the diurnal contraction and expansion of the brood continues when males are removed (Scott et al . 1997). Juvenile smallmouth bass show nest-site fidelity. In an Ontario lake, age-0 smallmouth bass dispersed little beyond 200 m of their nest of origin by fall, a time long after parental males ceased brood guarding (Gross and Kapuscinski 1997; Ridgway et al . 2002). Likewise, stream-dwelling age-0 smallmouth bass appear to remain near the spawning areas for the first summer of life (Lyons and Kanehl 2002). Male smallmouth bass guard and vigorously defend the nest, eggs, and larvae 24 h/d for 2 to 7 or more weeks, depending in part on male size and energy reserves, spawning time, and water temperatures (e.g., Pflieger 1966a; Neves 1975; Vogele 1981; Hinch and Collins 1991; Ridgway and Friesen 1992; Scott et al . 1997; Knotek and Orth 1998; Cooke et al . 2002a; Cooke et al . 2006). Over eight nesting seasons in a northern lake, average duration of male parental care ranged from 9.4 to 16.4 days (up to 21 days) before swim-up and 9.2 to 11.8 days after swim-up (up to 27 days) (Ridgway and Friesen 1992). Male defense behaviors and swimming activity increase as the offspring progress from egg to hatching, peak before swim-up, and begin to decrease after swim-up (Ridgway 1988; Ongarato and Snucins 1993; Cooke et al . 2002a). Nevertheless, males shift from active and close defense of a brood confined to the nest before swim-up to more distant but vigilant patrolling of dispersed larvae and juveniles (Scott et al . 1997). Guardian male feeding is curtailed or at least dramatically reduced, which in turn reduces and perhaps depletes energy reserves (Hinch and Collins 1991; Gillooly and Baylis 1999; Mackereth et al . 1999; Cooke et al . 2002a; Steinhart et al . 2005). Large males show higher intensity and longer duration of offspring defense; small guardian males can abandon the brood early or may show little or no defense of juveniles, perhaps as a result of reduced or depleted energy reserves (Ridgway and Friesen 1992; Philipp et al . 1997; Mackereth et al . 1999). Males experiencing brood loss from simulated predation also show less nest defense and are more likely to completely abandon the brood (Philipp et al . 1997; Suski et al . 2003). Compelling evidence of an alternating life history strategy is documented for a smallmouth bass population in Nebish Lake, Wisconsin. Unlike the alternative reproductive strategy of cuckoldry seen in some male Lepomis, successive generations of male smallmouth bass in this population alternate their age at first reproduction between ages 3 and 4 (Raffetto et al . 1990; et al .Wiegmann et al . 1992, 1997; Baylis et al . 1993). Micropterus males are typically iteroparous (reproducing in multiple years), but males in this closed population are essentially semelparous (reproducing once in a lifetime). Reproduction can begin at age 3, but the life history decision for time of first reproduction is conditional on male size at age 3, with large age-3 males being likely to reproduce, and small age-3 males being likely to delay reproduction until age 4 or older. In turn, size at age 3 is determined largely in early ontogeny and is likely a function of birth date. Large, older males (age 4 or older) spawn earlier (average about 4–5 days) in the spring than mature, spawning age-3 males. The late spawning, age-3 males are more likely to produce a cohort of small age-3 males that in turn are more likely to delay reproduction until age 4 or older. Conversely, small age-3 males that delay reproduction until age 4 (or older) are more likely to produce a cohort of large, reproductively active age-3 males. Hence, an alternation of time to maturation is sustained over multiple years and appears to be mediated by just a few days difference in birth date (Baylis et al . 1993; Wiegmann et al . 1997). Nest associates: Longnose gar, Lepisosteus osseus (Goff 1984); common shiner, Luxilus cornutus (Hunter and Wisby 1961); orangethroat darter, Etheostoma spectabile (Pflieger 1966b).

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Freshwater mussel host: Confirmed host to A. ligamentina, L. cardium, L. fasciola, L. higginsii, L. radiata, L. rafinesqueana, L. reeviana, L. siliquoidea, and V. iris (Coker et al . 1921; Zale and Neves 1982; Waller and Holland-Bartels 1988; Barnhart and Roberts 1997; O’Dee and Watters 2000). Putative host to Lampsilis abrupta and Lexingtonia dolabelloides (unpublished sources in OSUDM 2006). Conservation status: The smallmouth bass is secure throughout its range, but native populations in Kansas, along the western periphery of the natural range, are considered vulnerable (NatureServe 2006). Similar species: Spotted bass have a black midlateral stripe (no vertical bars) and rows of black spots along the lower sides; redeye bass have white or orange edges on the caudal fin lobes and rows of black spots along the lower sides; Florida bass and largemouth bass have a dark, midlateral stripe, a deep notch between the soft and spiny dorsal fins, and in adults, the mouth reaches beyond the rear margin of the eye (Page and Burr 1991). Systematic notes: Micropterus dolomieu and M. punctulatus form a sister pair, which is basal to all other Micropterus (Kassler et al . 2002; Near et al . 2003, 2004, 2005). Morphological taxonomists traditionally related M. dolomieu to M. coosae (Hubbs and Bailey 1940; Ramsey 1975). Although only two subspecies of M. dolomieu are usually recognized, the species as currently conceived appears to consist of several distinct evolutionary lineages. The subspecies M. d. velox was described from tributaries of the Arkansas River in southwestern Missouri, northeastern Oklahoma, and northwestern Arkansas based on color, body shape, and modal differences in dorsal ray counts (Hubbs and Bailey 1940). Intergrade populations between M. d. dolomieu and M. d. velox were considered tentatively to occupy the remainder of the southern Ozark and Ouachita uplands, exclusive of the lower Missouri River, and M. d. dolomieu the remainder of the range. Limited sampling of mitochondrial and nuclear DNA sequences did not detect geographic differences among M. dolomieu populations (Kassler et al . 2002; Near et al . 2003, 2004), but nuclear-encoded allozyme loci provide evidence for significant genetic substructuring in the Ozark and Ouachita uplands (Stark and Echelle 1998). Three different clades of M. dolomieu inhabiting the Ozark and Ouachita uplands are evident: (1) the Ouachita smallmouth bass in the Little and Ouachita river drainages; (2) the Neosho smallmouth bass from the southwestern Ozarks in the Neosho and Illinois rivers and smaller tributaries of the middle Arkansas River; and (3) a clade comprising all other populations on the Ozark Plateau (White, Black, St. Francis, Meramec, and Missouri rivers). The latter clade was similar genetically to populations from the upper Mississippi and Ohio River basins (Stark and Echelle 1998). Importance to humans: The smallmouth bass is rivaled only by the Florida bass and the largemouth bass as the most sought-after and valued species in the black bass recreational fishery. Until at least 1932, tons of smallmouth bass were taken commercially by hook and line and by net in Canada, until the species was restricted as a noncommercial sport fish (Scott and Crossman 1973). The smallmouth bass reaches a relatively large size, is an intense, strong fighter when hooked, and over its broad distribution flourishes in high-quality lakes, reservoirs, and upland rivers and streams, all attractive attributes to recreational anglers. As a primary North American recreational fish, the smallmouth bass is the focus of intense fisheries research and management efforts increasingly aimed at maintaining quality- and trophy-size catches for anglers (e.g., Reed et al . 1991; Beamesderfer and North 1995; Kubacki et al . 2002; Noble 2002). Not unexpectedly, techniques for catching smallmouth bass are the subject of a continuous stream of media from the recreational fishing industry (e.g., magazine articles, books, videos). Like other black bass the species is taken by a number of methods including dry flies, wet flies, popping bugs, lures, spinners, jigs, and plastic worms. Effective natural baits include leeches, soft crayfish, hellgrammites, minnow-tipped jigs, frogs, and salamanders. Although most often taken in lakes and reservoirs, smallmouth bass anglers, particularly a growing contingent of fly fishers seeking a quality fishing experience, wade or fish from small boats and canoes in scenic upland streams and rivers (Becker 1983; Etnier and Starnes 1993; Pflieger 1997). The flesh is white, firm, and flaky with fine flavor, being regarded by gourmets as superior table fare (Becker 1983).

13.9.4 Micropterus floridanus Lesueur 13.9.4.1 Florida bass Characteristics: See generic account for general characteristics. Elongate, slightly compressed body, depth about 0.24 to 0.29 of TL, increasing with size. Mouth large, terminal, lower jaw slightly projecting, upper jaw extends beyond

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posterior edge of eye in adults. Outline of spinous dorsal fin sharply angular. Juncture of soft and spiny dorsal fins deeply emarginate, almost separate. Shortest dorsal spine at emargination of fin, usually 0.3 to 0.4 times the length of longest spine, membranes between short spines deeply incised. Dorsal soft rays, usually 13, 12 to 14; anal soft rays, usually 11, 10 to 12. Gill rakers, 6 to 9. Scales average smaller than largemouth bass. Lateral scales, (65)69 to 73(76); rows above lateral line, (7)8 to 9(10); rows below lateral line, (15)17 to 18(21); cheek scale rows, (10)11 to 13(14); caudal peduncle scale rows, (27)28 to 31(33); pectoral rays, 14 to 15(16). No small splintlike scales on interradial membranes at anal and second dorsal fin bases. Pyloric caeca branched at bases, 26 to 43 or more. Tooth patch absent (rarely a few teeth) on glossohyal (tongue) bone (Bailey and Hubbs 1949; Buchanan 1973; Chew 1974; Ramsey 1975; Kassler et al . 2002). Size and age: Size at age 1 ranges from 142 to 310 mm TL for males and 116 to 330 mm TL for females (Allen et al . 2002). Age and weights of trophy Florida bass (n = 810, ≥4.5 kg) obtained from taxidermists across Florida revealed a maximum age of 16 (average 9.7 years), a maximum weight of 7.9 kg (average 5.0 kg), and a maximum length of 762 mm TL (average 661 mm) (Crawford et al . 2002). Florida state record, 7.85 kg (FFWCC 2006). Females grow faster and live longer than males; nearly all large individuals of Florida bass (>400 mm TL) are females (Allen et al . 2002; Crawford et al . 2002; Bonvechio et al . 2005; all cited studies include a few likely populations of M. floridanus × M. salmoides intergrades in northern Florida). Coloration: Broad dark olive to olive black, midlateral stripe on caudal peduncle becoming disrupted anteriorly into a series of more or less distinct blotches, the midlateral stripe often faint in large adults. Silver to brassy green above (brownish in tea-stained water) with dark olive mottling. Scattered dark specks on lower sides; whitish below. Iris brown. Young (<50 mm TL) with bicolored caudal fin markings (whitish basally, dark distally) (Bailey and Hubbs 1949; Chew 1974; Page and Burr 1991). Native range: The Florida bass is native to peninsular Florida (Bailey and Hubbs 1949; Philipp et al . 1981, 1983; Page and Burr 1991). The Florida bass and largemouth bass have an extensive hybrid zone across the southeastern United States in large part as a result of stocking of Florida bass outside its native range (see account on M. salmoides). Habitat: The Florida bass inhabits clear vegetated lakes, reservoirs, canals, ponds, swamps, and backwaters, as well as pools of creeks and small to large rivers (Page and Burr 1991). Adults often center home activity areas in close association with structure (e.g., logs, piers) or mixed beds of emergent and submergent aquatic macrophytes but also frequent open water without cover (McLane 1948; Mesing and Wicker 1986; Colle et al . 1989; Bruno et al . 1990). Young Florida bass are usually most abundant in shallow (<2 m) densely vegetated areas (McLane 1948; Chew 1974; Allen and Tugend 2002). Maximal home activity area of radio-tagged adult Florida bass in two lakes was 5.2 ha, averaging about 1.2 ha for fish tracked over multiple months and seasons. Fish size was related positively to home area, and mean daily movements decreased at seasonal high and low temperatures (Mesing and Wicker 1986). Home activity areas were generally narrow and paralleled the shore for distances of 50 to 2364 m. Most activity (70–90%) was <300 m from the geometric center of the home use area. The largest fish (>600 mm TL) occupied the same home areas for over a year. Nevertheless, considerable offshore movement occurred, and many fishes were not located in littoral areas for long periods, suggesting that a significant proportion of Florida bass used open water extensively (Mesing and Wicker 1986). In a lake lacking aquatic macrophytes, some radio-tagged Florida bass consistently used offshore home areas at depths >3.5 m. The offshore home activity areas lacked any natural or artificial structures. The offshore fish had larger home activity areas (mean 21.0 ha, range 0.6–39.5 ha) than similar-sized fish occupying shallow (<2.0 m) inshore home areas associated with standing timber (mean 4.1 ha, range 1.0–9.8 ha). Although much Florida bass activity is associated with dawn and dusk, movement occurs throughout the day. Interestingly, nocturnal movement of Florida bass can be high, extending into the early morning hours, especially when water temperatures exceed 18◦ C (Mesing and Wicker 1986; Colle et al . 1989). The Florida bass, having evolved in a subtropical climate, is more adapted to high temperatures and apparently less adapted to low temperatures than its temperate climate sister species, the largemouth bass. The Florida bass, along with the bluegill, has the highest reported critical thermal maxima among centrarchids, exceeding 41◦ C (acclimation temperatures >30◦ C, Fields et al . 1987; Beitinger et al . 2000). Hatching success of eggs and early development of larvae in Florida bass require greater thermal input than in largemouth bass (Philipp et al . 1985a). When held for 5 days at 2◦ C, Florida bass showed higher mortality rates (48%) than largemouth bass (0%), and in Illinois ponds, Florida bass showed significantly

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lower overwinter survival than largemouth bass (Carmichael et al . 1988; Philipp and Whitt 1991). The differences in response to temperatures between the two species appear to be linked to divergence in gene regulatory processes (Philipp et al . 1983, 1985b; Parker et al . 1985). Florida bass occur and persist in highly acidic lakes (pH 3.7–4.5, ≤2 mg/l Ca) with relatively high total Al concentrations (≤200 µg/l), water quality conditions unfavorable for many fishes. Growth and body condition are reduced in acidic lakes relative to populations in circumneutral lakes, but changes in blood plasma osmolarity and electrolytes, associated with pH-related stress, are not substantial. Young-of-the-year Florida bass, but no small bluegill or redear sunfish, occurred even in the most acidic lakes studied. The physiological basis for the acid tolerance of the Florida bass is unknown (Canfield et al . 1985). Food: The Florida bass is a top carnivore. Adults (>300 mm TL) feed about equally on fish (e.g., other centrarchids, clupeids, anchovies, topminnows, lake chubsuckers, silversides, minnows, darters) and decapods (crayfish and grass shrimp, if available) (McLane 1948, 1950; Chew 1974; Schramm and Maceina 1986; Huskey and Turingan 2001; Crawford et al . 2002). Young-of-the-year (13–30 mm TL) feed heavily on cladocerans, copepods, amphipods, and aquatic insects but with growth (31–75 mm TL) cease zooplankton use and begin including higher volumes of grass shrimp and fish (e.g., mosquitofish, silversides, topminnows). By 75 mm TL, fish and decapods constitute most of the diet biomass (Carr 1942; Chew 1974; Huskey and Turingan 2001; Allen and Tugend 2002). Florida bass feed by using combinations of ram (i.e. rapid acceleration of the body) and suction (i.e. rapid expansion of buccal cavity) strike modes on prey (Sass and Motta 2002). Feeding activity appears to occur randomly during the day (Chew 1974), and in captivity, Florida bass digestion rates are rapid (relative to warmouth, L. gulosus), and individuals feed voraciously even when considerable food from previous meals remains in the stomach (Hunt 1960). In the St. Johns River, Florida, early naturalists reported groups of hundreds to thousands of Florida bass pursuing and feeding on enormous schools of threadfin shad. Attacks by the bass on the shad resulted in the surface boiling with activity for several minutes at a time (McLane 1948). Focal animal observations on Florida bass (<300 mm TL) in canals revealed that 75% of the individuals occurred in hunting groups. Large individuals (>300 TL) hunted only with groups of other bass, but small individuals (<300 mm TL) hunted in mixed species groups with similar-sized bluegills (Annett 1998). The mixed groups searched, lunged into vegetation, and struck at schools of small fishes together. The bass-only groups typically oriented toward and surrounded a vegetated area, then one bass flushed a prey fish, and the entire group then pursued the prey. The group then moved to another vegetated patch and repeated the sequence of behaviors (Annett 1998), all of which are suggestive of group foraging if not cooperation. Reproduction: Maturity is reached at age 1+ to 3+ and 254 to 299 mm TL (Chew 1974). In experimental ponds in southern Florida, individuals matured and spawned at 9 months (Clugston 1964). Gonadal development, as evidenced by gonadosomatic changes and sex hormone levels, begins increasing in November and peaks in February and March (Gross et al . 2002; Sep´ulveda et al . 2002). Lake-dwelling Florida bass engage in spawning movements (≤3 km) to nesting areas protected from wind and wave action, then return to prespawning home areas after spawning (Mesing and Wicker 1986; Colle et al . 1989; Bruno et al . 1990). When low temperatures interrupted spawning activities, fish returned to their home areas in a lake, and then as temperatures rose, returned to the same canal to reinitiate spawning (Mesing and Wicker 1986). Spawning can occur as early as December in southern Florida, as water temperatures cool to about 18.3◦ C, but peak spawning is generally from February to April at water temperatures between about 18.0 and 21.1◦ C (as low as 14◦ C, up to about 27.8◦ C) (Clugston 1966; Chew 1974). In experimental ponds in Illinois, average duration of the spawning period as estimated from age differences in young was 21 days (range, 13–71 days), but initiation of spawning occurred 7 to 11 days later than largemouth bass occupying the same ponds (Isely et al . 1987). Males excavate nests using strong lateral undulations of the body. To further shape the nest, males position their head in the center of the nest and pivot around the nest while rapidly beating the pectoral, soft dorsal, and caudal fins (Carr 1942). Nests are oval (30–60 cm long, 20–55 cm wide), located in water 30 to 75 cm deep (range 10 cm to 2 m), and spaced as close as 1.5 m apart but usually ≥2.5 m apart (Carr 1942; Clugston 1966; Bruno et al . 1990). Males usually build nests near simple cover (e.g., log, overhanging tree limb, near cattail roots) over firm substrates if available. In lakes with bottoms of unconsolidated organic matter, males construct nests on spatterdock rhizomes, firm detritus in emergent grasses, and palmetto leaves over submergent vegetation (Carr 1942; Bruno et al . 1990). Anecdotal evidence suggests some degree of year-to-year nest site fidelity (Carr 1942). Early in the season, intervals of 4 to 5 days may occur between nest construction and spawning, but as the spawning intensifies, nests are constructed and receive eggs within a few hours (Carr 1942). Most spawning appears

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to take place in late afternoon (Carr 1942; Chew 1974; Isaac et al . 1998). During prespawning, males leave the nest to locate and guide spawning-ready females back to the nest (Carr 1942). Once at the nest, the female, often much larger than the male, circles the nest with the male, during which time he gently nips and butts her head, tail, and sides to push her toward the nest. The male continues to swim actively around and to nip and bump the female; paired female and male circling can last for 10 to 20 or more minutes. The color pattern of both fish becomes more definite and vivid as they circle and enter the nest to spawn. The female then takes a position over the center of the nest, head downward and tilted slightly to the side. Ultimately, the male takes a position along the side of the female with their vents close, both shudder violently for about 10 seconds, including 15 to 20 jerks from side to side, and release eggs and milt. On spawning, the male inspects the nest, and after a 3- to 5-minute pause, the pair repeats the sequence of behaviors for another spawning episode. A pair may spawn for 2 to 4 hours and include 6 to 13 separate spawning acts, after which the female appears exhausted and has difficulty maintaining her position off the bottom (Carr 1942; Chew 1974; Isaac et al . 1998). In indoor raceways in which eggs were removed after each completed pairing, males participated in one to four separate spawning events during 8 days of observation (Isaac et al . 1998). Of 19 observed spawnings, only one female Florida bass spawned with each male, although females visited nesting sites of several males before spawning with a male (Isaac et al . 1998). On completion of spawning the male begins to energetically fan the eggs day and night, reducing or ceasing fanning activity when the eggs hatch. Mature ovarian eggs average 1.5 mm diameter, and fertilized eggs, 1.59 mm diameter (range, 1.49–1.67, Carr 1942; Chew 1974). Fecundity is apparently unquantified but is likely similar to the largemouth bass. The adhesive, orange-colored, fertilized eggs begin hatching in about 1.9 days at 22.2◦ C (Carr 1942; Chew 1974). Newly hatched, nearly transparent larvae are 3.4 mm TL, and depending on temperature, larvae are free swimming about 5 to 7 days after hatching at 6.5 to 7.2 mm TL. Male parental care from spawning through fry dispersal from the nest is 10 to 11 days (Carr 1942), but the time males spend guarding free-swimming juveniles is unknown. Biparental care is not documented in Florida bass, but observations of two individuals guarding a single nest for several days (Carr 1942; Miller 1975) are suggestive (e.g., DeWoody et al . 2000b). Nest associates: Lake chubsucker, E. sucetta (Carr 1942); taillight shiner, Notropis maculatus (Chew 1974); golden shiner, N. crysoleucas (Chew 1974). Freshwater mussel host: Confirmed host to E. buckleyi , E. icterina, L. straminea claibornensis, L. siliquoidea, L. teres, M. nervosa, U. imbecilis, V. lienosa, V. iris (reported as V. nebulosa) and V. villosa (Neves et al . 1985; Keller and Ruessler 1997, experimental hosts from hatchery stock were presumably Florida bass, A. E. Keller, U.S. Environmental Protection Agency, personal communication). Conservation status: The Florida bass is secure throughout its range (Warren et al . 2000; NatureServe 2006). Similar species: All other species of Micropterus, except the largemouth bass, have more confluent dorsal fins, upper jaws that reach to, or barely past, the center of the eye, and unbranched pyloric caeca. The largemouth bass, except in a broad area of intergradation in the southern United States, differs in usually having 59 to 66 lateral line scales and 26 to 28 scales around the caudal peduncle (Page and Burr 1991). Systematic notes: Micropterus floridanus forms a sister pair with M. salmoides (Kassler et al . 2002; Near et al . 2003, 2004). Although long regarded as a subspecies of M. salmoides, nuclear-encoded allozyme loci, mitochondrial DNA, and nuclear DNA all indicate that M. floridanus is a distinct species (Philipp et al . 1983; Nedbal and Philipp 1994; Kassler et al . 2002; Near et al . 2003, 2004). Importance to humans: The Florida bass and its sister species, the largemouth bass, are the core of the multibillion dollar black bass recreational fishery. The Florida bass is the most popular sport fish in Florida and its value as a sport fish in the state has prompted a movement toward increased management and catch-and-release fishing (FFWCC 2006). The large maximum size obtained by Florida bass in warm waters provides anglers with a real prospect of catching a trophy-sized black bass. In many Florida lakes and reservoirs anglers routinely catch Florida bass fish weighing 8 to 10 or more pounds (3.6 to 4.5 or more kilograms) (Crawford et al . 2002; FFWCC 2006). Although several studies suggest that Florida bass are more difficult to catch than the largemouth bass (Zolcynski and Davies 1976; Kleinsasser et al . 1990; Garrett 2002), the Florida bass will aggressively and explosively strike most kinds of artificial lures or live baits. Most individuals are taken on plastic worms, surface plugs, spinnerbaits, crankbaits, bass bugs, and minnows. The meat is white, flaky, and low in oil content (FFWCC 2006).

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13.9.5 Micropterus notius Bailey and Hubbs 13.9.5.1 Suwannee bass Characteristics: See generic account for general characteristics. Elongate, slightly compressed, but robust body, depth 0.26 to 0.27 of TL. Mouth large, terminal, lower jaw slightly projecting, upper jaw extends to posterior margin of eye in adults. Outline of spinous dorsal fin curved. Juncture of soft and spiny dorsal fins slightly emarginate, broadly connected. Shortest dorsal spine at emargination of fin, usually >0.6 times length of longest spine. Dorsal soft rays, 12 to 13; anal soft rays, 10 to 11. Gill rakers, usually 5. Relatively large scales. Lateral scales, 57 to 65; rows above lateral line, 6 to 9; rows below lateral line, 14 to 19; cheek scale rows, 9 to 15; caudal peduncle scale rows, 27 to 31; pectoral rays, (15)16(17). Small splintlike scales on interradial membranes at anal and second dorsal fin bases (>60 mm SL). Pyloric caeca single, rarely branched, 10 to 13. Tooth patch on glossohyal (tongue) bone (Bailey and Hubbs 1949; Ramsey and Smitherman 1972; Page and Burr 1991; Kassler et al . 2002). Size and age: Size at age 1 ranges from 146 to 206 mm TL. Large individuals are >305 mm TL, weigh 400 g, and reach age 7+ (maximum 402 mm TL and age 9+ for males, age 12+ for females) (Bass and Hitt 1973; Page and Burr 1991; Cailteux et al . 2002; Bonvechio et al . 2005). World angling record, 1.75 kg, Florida (IGFA 2006). Females grow faster and live longer than males, and in a given population, 60% to 100% of individuals >305 mm TL are females (Bonvechio et al . 2005). Coloration: Color similar to M. salmoides but usually brown overall, and sides marked with about 12 vertically elongate, lateral blotches. Blotches anteriorly are much wider than their interspaces, becoming more confluent with age. The blotches fuse on the caudal peduncle to form a relatively uniform, wide lateral band. Ventrolateral longitudinal streaks are weakly developed. Iris red. Young with a series of thin, closely spaced vertical bars along the sides of the body. Cheeks, breast, and lower sides colored brilliant turquoise blue in nesting males, less so in non-nesting individuals (Bailey and Hubbs 1949; Gilbert 1978; Page and Burr 1991). Native range: The Suwannee bass is native to the Suwannee and Ochlockonee Rivers, Florida and Georgia (MacCrimmon and Robbins 1975; Page and Burr 1991). The provenance of populations in the Wacissa (Aucilla River drainage), Wakulla, and St. Marks rivers of Florida is uncertain (Koppelman and Garrett 2002; Cailteux et al . 2002; Bonvechio et al . 2005) but, given the lack of historical records, are likely introduced. Electrofishing catch data indicate that the species is most abundant in the Wacissa River (Aucilla River drainage) and Santa Fe River (Suwannee River drainage) (Schramm and Maceina 1986; Cailteux et al . 2002; Bonvechio et al . 2005). Habitat: The Suwannee bass occurs in a variety of habitats in cool, clear, spring-fed rivers, which characteristically have limestone substrates (often covered with sand); alkaline, hard water; relatively stable thermal regimes; and dense submersed macrophyte beds (Bass and Hitt 1973; Gilbert 1978; Schramm and Maceina 1986; Cailteux et al . 2002). In the Santa Fe River, individuals (>150 mm TL) are associated with fallen trees over sandy substrate; shallow bedrock riffles (0.7–3.0 m deep); vegetated (eelgrass), gravel–sand riffles; deep vertical rock drop-offs (to 3 m); and shallow, sandy, gently sloping vegetated banks (0.5–1.0 m deep). Small individuals are most common around fallen trees but occur in a variety of flowing and nonflowing habitats (Schramm and Maceina 1986). Individuals also occupy spring runs of river tributaries where they seek cover under dense overhanging or floating vegetation (Gilbert 1978). Food: The Suwannee bass is a top carnivore, extensively exploiting crayfishes for food. Crayfishes are the predominant food of individuals >150 mm TL, and for large fish (>300 mm TL), the diet is almost exclusively crayfishes. Fish rank second and freshwater shrimp third in importance in the diet; other crustacea, such as blue crabs, and a few aquatic insect larvae are also consumed. Juveniles (<150 mm TL) consume crayfish but also eat other invertebrates (grass shrimp, amphipods, aquatic insects) and some small fish (Bass and Hitt 1973; Gilbert 1978; Schramm and Maceina 1986; Cailteux et al . 2002). Size-adjusted throat width of the Suwannee bass is larger than that of Florida bass (or Florida × largemouth bass hybrids), allowing Suwannee bass (>167 mm TL) to consume larger prey items at a given size than the sympatric congener. Stomach contents of 142 Suwannee bass sampled in daylight hours from May to August revealed no obvious feeding periodicity (Schramm and Maceina 1986).

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Reproduction: Size and age at maturity are not well documented, and little is published on reproductive behavior and biology of this unique, range-restricted Micropterus. Gonads of the sexes are distinguishable at minimum sizes of 125 mm SL in males and 142 mm SL in females, but the smallest females reported with mature ova are ≥215 mm SL (Bass and Hitt 1973). On the basis of female reproductive condition and other observations, spawning apparently begins in February or March as water temperatures reach 18 to 20◦ C and continues into June. Females with ripe ova are taken from February to May, spent females begin to appear in April with the largest numbers occurring in May. Suwannee bass nests in rivers have been noted in April, and spawning occurred in experimental ponds in Alabama in early April (Bailey and Hubbs 1949; Hellier 1967; Smitherman and Ramsey 1972; Bass and Hitt 1973). Young <25 mm TL are taken from April to July (Hellier 1967). Shallow circular depressions are excavated along stream edges “in typical sunfish fashion,” and the male “guards the incubating ova” (Hurst et al . 1975) for an unspecified time. Fecundity increases with female size but is not well quantified. Estimated total ova of 18 gravid females (215–285 mm SL) ranged from 2520 to over 12,229 per individual and averaged 5397 (Bass and Hitt 1973). Fertilized eggs are 2.0 mm in diameter and hatch in about 3 to 4 days at 20◦ C. Yolk-sac larvae are 5.5 mm TL and reach 6.5 to 7.5 mm TL about 6 days after hatching (presumably swim-up stage) (Smitherman and Ramsey 1972). Nest associates: None known. Freshwater mussel host: Confirmed host to V. iris (reported as V. nebulosa, Neves et al . 1985). Conservation status: Because of its restricted range, the Suwannee bass is regarded as vulnerable throughout its native range (Warren et al . 2000; Koppelman and Garrett 2002) and is considered imperiled in Georgia and vulnerable in Florida (NatureServe 2006). Nevertheless, the species does not appear to have experienced declines in abundance or distribution in historical times (e.g., Santa Fe River, Bass and Hitt 1973; Bass 1974; Schramm and Maceina 1986; Bonvechio et al . 2005). Moreover, the present range includes more independent river systems than were known historically, and some of these rivers support high abundances of the species (Cailteux et al . 2002; Bonvechio et al . 2005). Similar species: The largemouth bass and the Florida bass have a deep notch between the spiny and soft dorsal fins, and the pyloric caeca are branched (Page and Burr 1991). Young Suwannee bass have closely spaced, elongate vertical bars along the sides of the body (versus solid longitudinal stripe in young largemouth bass and Florida bass) (Gilbert 1978). Systematic notes: Micropterus notius is a member of a “Gulf of Mexico” clade of Micropterus, including all other Micropterus except M. dolomieu and M. punctulatus (Kassler et al . 2002; Near et al . 2003, 2004). Relationships within the clade are not well resolved, with M. notius placed as basal to the entire clade, sister to M. cataractae, or sister to M. treculi and M. salmoides × M. floridanus (Kassler et al . 2002; Near et al . 2003, 2004). Similarities in form and color led most morphological taxonomists to relate M. notius to M. punctulatus (e.g., Bailey and Hubbs 1949; Ramsey 1975). Importance to humans: Decades before its scientific description, the Suwannee bass was recognized as unique and sought by local Florida anglers, who knew where and how to fish for the species (Swift et al . 1977). Even though relatively small, Suwannee bass are regarded as strong fighters when caught on light tackle. Individuals are taken on small crayfish-colored spinnerbaits, crankbaits, plastic worms, and jigs and live baits (e.g., dobsonfly larvae, crayfish). A limited, but specialty, black bass fishery exists in the lower Santa Fe River where Suwannee bass provide a small portion of the sport fish catch (dominated by redbreast sunfish) but constitute over a third of the total catch of Micropterus (Bass and Hitt 1973). In the crystal clear, flowing waters of the Wacissa River, float fishers, using light fly fishing gear and wet flies mimicking bait fish, regard the Suwannee bass as a challenging catch in an exceptionally high-quality environment (Ferrin 2006). The meat is reportedly white, flaky, and flavorful (FFWCC 2006).

13.9.6 Micropterus punctulatus (Rafinesque) 13.9.6.1 Spotted bass Characteristics: See generic account for general characteristics. Elongate, slightly compressed body, depth 0.17 to 0.27 of TL, increasing with size. Mouth large, terminal, lower jaw slightly projecting, upper jaw extends little or not at all beyond

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posterior edge of eye. Outline of spinous dorsal fin curved. Juncture of soft and spiny dorsal fins slightly emarginate, broadly connected. Shortest dorsal spine at emargination of fin, usually 0.4 to 0.9 times the length of longest spine. Dorsal soft rays, usually 12 or 13, 11 to 14; anal soft rays, usually 10, 9 to 11. Gill rakers, 5 to 7. Lateral scales, (55)60 to 75(79); rows above lateral line, (6)7 to 9(11); rows below lateral line, (11)13 to 18(22); cheek scale rows, (10)13 to 18(20); caudal peduncle scale rows, (21)25 to 31(32); pectoral rays, (13)15 to 17(18). Small splintlike scales on interradial membranes at anal and second dorsal fin bases (>60 mm SL). Pyloric caeca, single, rarely branched, 10 to 13. Tooth patch present on glossohyal (tongue) bone (Hubbs 1927; Hubbs and Bailey 1940, 1942; Applegate 1966; Bryan 1969; Ramsey and Smitherman 1972; Williams and Burgess 1999). Size and age: Size at age 1 averages about 113 mm TL but varies considerably among habitats and across the geographic range (population averages range from 66 to 216 mm TL) (Vogele 1975b; Webb and Reeves 1975; Carlander 1977; Olmsted and Kilambi 1978; DiCenzo et al . 1995; Pflieger 1997; Maceina and Bayne 2001). Growth rate trends higher in reservoirs than in streams (Vogele 1975b), and the Alabama spotted bass, M. p. henshalli, lives longer and reaches a larger size than the northern subspecies, M. p. punctulatus (DiCenzo et al . 1995). However, the Alabama spotted bass may represent a distinct taxon and perhaps be only distantly related to M. punctulatus (e.g., Kassler et al . 2002). Few individuals exceed 425 mm TL, 2.0 kg, and ages 6+ (maximum about 640 mm TL and age 11+) (Gilbert 1973; Webb and Reeves 1975; Carlander 1977; Olmsted and Kilambi 1978; Page and Burr 1991; DiCenzo et al . 1995; Wiens et al . 1996; Maceina and Bayne 2001). World angling record, 4.65 kg, California (IGFA 2006). Females of the Alabama spotted bass, M. p. henshalli, and perhaps other spotted bass populations (e.g., Ryan et al . 1970), can live longer than males (age 8+ versus age 5+) and after the third year show faster growth and weigh more than males (Webb and Reeves 1975). Coloration: Rows of small black spots on yellow-white lower sides form horizontal lines. Dark midlateral stripe or series of partly joined blotches along light olive to yellowish green side. Caudal spot dark, darkest on young. Light green-gold dorsally with dark olive, often diamond-shaped mottlings. Young (<50 mm TL) with distinct tricolored caudal fin markings (yellowish base, dark middle, whitish edge) (Trautman 1981; Page and Burr 1991). Native range: The spotted bass is native to the Mississippi River basin from southern Ohio and West Virginia to southeastern Kansas and south to the Gulf and in Gulf drainages from the Choctawhatchee River, Alabama and Florida, west to the Guadalupe River, Texas (Robbins and MacCrimmon 1974; Page and Burr 1991; Miller 2005). Populations in the Apalachicola River Basin were likely introduced (Bailey and Hubbs 1949; Williams and Burgess 1999). The spotted bass was widely introduced and is established outside its native range across most of the southern half of the western United States and in some river systems has rapidly expanded its range after introduction (e.g., Missouri River) (Robbins and MacCrimmon 1974; Pflieger 1997; Fuller et al . 1999; Moyle 2002). Hybridization and introgression can be extensive when nonnative M. punctulatus are introduced into native populations of M. dolomieu (Koppelman 1994; Pierce and Van Den Avyle 1997; Avise et al . 1997). Data from nuclear-encoded allozymes and mitochondrial DNA haplotypes revealed a remarkable pattern of faunal turnover and introgressive swamping of the native M. dolomieu by the nonnative M. punctulatus in a northeastern Georgia reservoir (Hiwassee River drainage, Avise et al . 1997). In only 10 to 15 years after the introduction of M. punctulatus, the M. dolomieu population declined dramatically. Even more surprising was the finding that >95% of remaining M. dolomieu mtDNA haplotypes (and nuclear alleles) in the lake population were found in fishes of hybrid ancestry between the introduced and native Micropterus. Similar patterns indicative of introgressive swamping occurred when M. punctulatus was introduced into a native population of M. dolomieu in South Moreau Creek (Missouri River drainage), Missouri (Koppelman 1994), and are suggested for introductions of M. p. henshalli into a native population of M. coosae in Keowee Reservoir (Savannah River drainage), South Carolina (Barwick et al . 2006). Habitat: The spotted bass inhabits gravelly flowing pools and runs of creeks and small to medium rivers and reservoirs (Page and Burr 1991). In streams, spotted bass are commonly associated with low-velocity pools, particularly those with vegetation, log complexes, rootwads, or undercut banks (Lobb and Orth 1991; Scott and Angermeier 1998; Tillma et al . 1998; Horton and Guy 2002; Horton et al . 2004). The habitat requirements of the species can be broadly characterized as intermediate between those of the smallmouth bass and largemouth bass. The spotted bass is associated with warmer, more turbid water than smallmouth bass, and faster, less productive waters than the largemouth bass (Trautman 1981; Layher et al . 1987; Pflieger 1997). Nevertheless, spotted bass frequently co-occur with largemouth bass, smallmouth bass, and redeye bass but generally show some spatial segregation from co-occurring Micropterus, in cover type,

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longitudinal distribution, or water depth (e.g., Viosca 1931; Vogele 1975b; Trautman 1981; Buynak et al . 1989; Matthews et al . 1992; Pflieger 1997; Scott and Angermeier 1998; Sammons and Bettoli 1999; Long and Fisher 2005). For example, spotted bass were widely distributed in a Virginia impoundment, but occurred most commonly in areas with fine substrate and woody debris, undercut banks, and bank vegetation as cover, avoiding the steep drop-offs and rocky shorelines frequented by smallmouth bass (Scott and Angermeier 1998). In southern US reservoirs, spotted bass are most abundant in oligo-mesotrophic reservoirs or oligo-mesotrophic reaches of reservoirs with abundance decreasing as eutrophication increases; an opposite pattern occurs for largemouth bass abundance (Buynak et al . 1989; Greene and Maceina 2000; Maceina and Bayne 2001). Although spotted bass may enter relatively high-salinity coastal environments (≤10 ppt), they infrequently occur in coastal marshes with salinities >4 ppt (Peterson 1988, 1991; Peterson and Ross 1991). Relatively little is known about movements of spotted bass. In some populations, indirect evidence suggests massive upstream movement in spring from reservoirs and rivers into tributaries to spawn, followed by a gradual downstream drift of most adults and young to overwinter in large, lower-gradient habitats (Vogele 1975b; Trautman 1981). The average home activity area of radio-tagged spotted bass tracked over multiple seasons in a Kansas stream was 0.39 ha (range, 0.06–1.2 ha). Activity area was correlated positively with body size, and activity areas of up to six fish showed simultaneous overlap. During summer and winter, fish typically remained in one pool, but during spring and fall, fish crossed riffles and moved among pools (Horton and Guy 2002). Food: The spotted bass is an opportunistic carnivore, exploiting prey from the bottom to the water’s surface. The adult diet is dominated in biomass by crayfish if present, fish (e.g., clupeids, darters, minnows, catfishes), and to a lesser extent, immature aquatic insects (Applegate et al . 1967; Gilbert 1973; Vogele 1975b; Scott and Angermeier 1998). Depending on prey availability, consumption of large numbers and volumes of immature aquatic insects may continue up to 150 mm TL or larger. Spotted bass may exploit relatively large numbers and volumes of terrestrial insects (e.g., hymenoptera, beetles, flies, adult odonates) (Smith and Page 1969; Ryan et al . 1970; Vogele 1975a; Scott and Angermeier 1998). The young initially depend on zooplankton (cladocerans and copepods) with juveniles transitioning from large immature aquatic (e.g., mayflies, diptera) insects to fish and crayfish at 50 to 100 mm TL (Applegate et al . 1967; Clady and Luker 1982; Matthews et al . 1992; Scott and Angermeier 1998). Spotted bass are relatively inactive at night, staying close to cover, but move frequently throughout the day (Horton et al . 2004). Even so, diet data reveal no clear diel feeding patterns except for an increase in terrestrial insects in the diet during the day (Scott and Angermeier 1998). Reproduction: Maturity can be reached as early as age 1+ in fast-growing populations, but most individuals do not mature until age 2+ to 3+ (Gilbert 1973; Olmsted 1974; Vogele 1975a,b). Depending in part on latitude and water temperature, spawning occurs over a 1- to 2-month period from March to May or early June, with the most intensive nesting occurring within about 2 weeks of initial spawning activity (Ryan et al . 1970; Gilbert 1973; Olmsted 1974; Vogele 1975a; Sammons et al . 1999; Greene and Maceina 2000). Active nests have been observed at temperatures as low as 12.8◦ C, but most spawning occurs between 14◦ C and 23◦ C (Howland 1932a; Ryan et al . 1970; Smitherman and Ramsey 1972; Gilbert 1973; Olmsted 1974; Vogele 1975a,b; Aasen and Henry 1981; Sammons et al . 1999). The male excavates a solitary, depressional, roughly circular nest by caudal sweeping and removing material with his mouth (Breder and Rosen 1966); nests are spaced widely with densities ranging from 0.5 to 11.3/100 m of shoreline. Most but not all nests are located near cover (e.g., rock overhangs, stumps, submerged tree bases) (Vogele 1975a; Vogele and Rainwater 1975). Nests are 38 to 76 cm in diameter, are located at average water depths of 2.3 to 3.7 m (range, 0.9–6.7 m), and are usually swept out over hard substrates (e.g., sand and gravel, solid rock ledges, flat rocks), but compacted soil and exposed root hairs of flooded trees are also used (Vogele 1975a,b; Aasen and Henry 1981). Males may excavate and defend one to four nest sites for up to 3 days before egg deposition. Limited evidence from tagged males suggests year-to-year fidelity to specific nesting areas (Vogele 1975a). Courtship and spawning are generally typical of other Micropterus, but published documentation is not extensive (e.g., male guiding of female, paired circling) (Miller 1975; Vogele 1975a,b, citing Howland 1932b). Once a female is attracted to the nest, the male guides her in circles about the nest (female inside, male outside), repeatedly biting at her opercle and vent. During courtship, the midlateral stripe in the female disappears (Miller 1975). Courtship behaviors continue for 20 minutes to 1 hour before egg deposition begins. Ultimately, the female deposits eggs (for 1.5 to 5 seconds) by tilting on her side, and the male releases milt in an upright position as is typical for most centrarchids. Courtship and spawning sequences between pairs may require up to 3.5 hours for completion (Vogele 1975a). Most spawning observations involved a single male and female. After spawning, males immediately begin fanning the eggs and continue defending the eggs from numerous, persistent Lepomis and other predators (Vogele 1975a). Mature ovarian eggs range from 1.30 to 2.20 mm diameter (Gilbert

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1973; Vogele 1975a) and fertilized, water-hardened eggs range from 1.60 to 2.30 mm diameter (Smitherman and Ramsey 1972; Vogele 1975a). Fecundity increases with female size. The relationship between potential batch fecundity (Y) and total length (X) is described by the function, log10 Y = −8.222 + 4.779 log10 X(n = 48, R2 = 0.71, data from Olmsted 1974 and Vogele 1975a). At 347 mm TL, a female can potentially produce 8284 mature eggs in a single batch (range: 1728 eggs at 250 mm TL to 26,906 eggs at 444 mm TL, respectively). The adhesive, fertilized eggs hatch in 5 days at 14.4◦ C to 15.6◦ C (Vogele 1975a). Larvae are free swimming at 6.0 to 7.5 mm TL in 4 days and 8 days after hatching at 25◦ C and 15 to 18◦ C, respectively (Vogele 1975a; DiCenzo and Bettoli 1995). Fry emerging from the nest form compact schools that are guarded by the parental male for up to 4 weeks. Schools with fry from different nests may merge into a single large school and be guarded by two parental males. The schools break up as fry reach about 30 mm TL (Vogele 1975a). In hatchery ponds, males apparently exhibited less parental care, abandoning the fry shortly after swim-up (Smitherman and Ramsey 1972; Vogele 1975b). Nest associates: None known. Freshwater mussel host: Confirmed host to L. altilis, L. perovalis, Lampsilis subangulata, V. iris, V. nebulosa, and V. vibex (Neves et al . 1985; Haag and Warren 1997; Haag et al . 1999; O’Brien and Brim Box 1999). Putative host to L. abrupta (unpublished sources in OSUDM 2006). Conservation status: The spotted bass is secure throughout its range, but peripheral populations in Illinois are considered vulnerable (Warren et al . 2000; NatureServe 2006). Lack of resolution of the genetic relationships among populations now regarded as M. punctulatus is of primary conservation concern (Kassler et al . 2002; see section on systematic notes). Similar species: Shoal bass has dark vertically elongate bars on sides and lacks patch of teeth on tongue; redeye bass has white to orange upper and lower edges on caudal fin lobes and young has red medial fins; largemouth bass and Florida bass lack rows of black spots on lower sides and have a deep notch between spiny and soft dorsal fins; young of these species have a bicolored caudal fin (white, black edge); smallmouth bass lacks a distinct lateral stripe (Page and Burr 1991). Systematic notes: Micropterus punctulatus and M. dolomieu form a sister pair that is basal to all other Micropterus (Kassler et al . 2002; Near et al . 2003, 2004, 2005). As currently conceived, the long-presumed polytypy of M. punctulatus (Hubbs and Bailey 1940) appears to subsume two relatively distantly related and divergent species of Micropterus. Morphological and genetic data indicate that a small-scaled form, the Alabama spotted bass (nominal M. p. henshalli ), occurs in Mobile Basin (Hubbs and Bailey 1940; Gilbert 1973; Kassler et al . 2002). Although intergrades between M. p. punctulatus and M. p. henshalli were suggested from limited samples from west of Mobile Basin to the Lake Pontchartrain system (Hubbs and Bailey 1940), more extensive meristic data revealed no evidence of intergradation in that region (Gilbert 1973). However, individuals above the Fall Line in Mobile Basin were assigned to M. p. henshalli and those below the Fall Line were interpreted as intergrades between M. p. henshalli and M. p. punctulatus (Gilbert 1973). The putative intergrades could just as easily represent in situ differentiation of quasi-isolated populations of Alabama spotted bass, rather than intergradation. Importantly, mitochondrial DNA analyses from limited population sampling indicate that the form in Mobile Basin is highly divergent from M. p. punctulatus (e.g., fixed allelic differences at multiple gene loci, fixed haplotype differences, sequence divergence of 10.3%) and is genetically most similar to M. coosae (Kassler et al . 2002). Unfortunately, M. p. henshalli has been introduced outside the native range in Mobile Basin and has introgressed with native Micropterus (Pierce and Van Den Avyle 1997). The resolution of the relationships of the Alabama spotted bass to other Micropterus awaits a thorough genetic analysis across populations in the Mobile Basin. The subspecies M. p. wichitae, ostensibly restricted to a single stream in the Red River drainage, Oklahoma (Hubbs and Bailey 1940), was based on M. punctulatus × M. dolomieu hybrids and is not valid (Cofer 1995). The subspecies M. p. punctulatus occupies the remainder of the range (Gilbert 1973). Importance to humans: Ecologically, the spotted bass can function as the only top carnivore in small, even intermittent, headwater streams and is often the dominant top predator in large rivers and reservoirs (Cross 1967; Trautman 1981; Pflieger 1997). The spotted bass is also a popular sport fish in streams and reservoirs throughout the southeastern United States. The species is sought in streams by anglers favoring fly fishing or ultralight tackle (Cross 1967; Ross 2001). The largest spotted bass are taken in reservoirs and spillways where food availability is higher than in most streams (Ross

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2001). In southern US reservoirs, spotted bass can be the dominant or co-dominant Micropterus and constitutes a sizable proportion of the black bass catch (e.g., 60%) and harvest (e.g., 50%) (Webb and Reeves 1975; Novinger 1987; Buynak et al . 1989, 1991; DiCenzo et al . 1995; Pflieger 1997; Sammons et al . 1999; Sammons and Bettoli 1999; Long and Fisher 2005). The spotted bass often co-occurs with the largemouth bass or smallmouth bass in reservoirs, where most management effort is usually focused on the latter two species (e.g., Maceina and Bayne 2001; Long and Fisher 2005). Because of its slower growth and high abundance in some reservoirs, fishery managers combine liberalized harvest of spotted bass with increased length limits for largemouth bass (or smallmouth bass) to reduce exploitation and to increase the size of the latter (e.g., Buynak et al . 1991; Long and Fisher 2005). The spotted bass takes the same lures (e.g., spinner baits, plastic worms, jigs, crank baits) and live baits (e.g., minnows, crayfishes, salamanders) as other black bass. Anglers consider their strike more aggressive and their fight more spirited than that of the largemouth bass (Ross 2001).

13.9.7 Micropterus salmoides Lac´ep`ede 13.9.7.1 Largemouth bass Characteristics: See generic account for general characteristics. Elongate, slightly compressed body, depth 0.24 to 0.29 of TL, increasing with size. Mouth large, terminal, lower jaw slightly projecting, upper jaw extends beyond posterior edge of eye in adults. Outline of spiny dorsal fin sharply angular. Juncture of soft and spiny dorsal fins deeply emarginate, almost separate. Shortest dorsal spine at emargination of fin, usually 0.3 to 0.4 times length of longest spine, membranes between short spines deeply incised. Dorsal soft rays, usually 13 or 14, 11 to 15; anal soft rays, usually 11 or 12, 10 to 14. Gill rakers, 7 to 9. Lateral scales, (55)58 to 67(72); rows above lateral line, 7 to 8(9); rows below lateral line, 13 to 17; cheek scale rows, 9 to 11(13); caudal peduncle scale rows, (24)26 to 28(30); pectoral rays, (13)14 to 15(17). No small splintlike scales on interradial membranes at anal and second dorsal fin bases. Pyloric caeca branched at base, 12 to 45. Tooth patch usually absent on glossohyal (tongue) bone, but tooth patch present or absent in San Antonio and Nueces rivers, southwest Texas, and present in ≥50% of specimens in the Rio Grande system, Mexico and Texas (Hubbs and Bailey 1940; Bailey and Hubbs 1949; Applegate 1966; Keast and Webb 1966; Buchanan 1973; Chew 1974; Edwards 1980; Kassler et al . 2002). Size and age: Size at age 1 is highly variable among habitats and across latitudes, ranging from 33 to 271 mm TL (median 102 mm TL) (Carlander 1977; McCauley and Kilgour 1990; Beamesderfer and North 1995; Garvey et al . 2003). Critical periods causing differential size, growth, and survival for age-0 cohorts include time of hatching, onset of piscivory, accumulation of lipids in the fall, and the ability to survive predation, starvation, or both over the first winter (DeAngelis and Coutant 1982; Gutreuter and Anderson 1985; Miranda and Hubbard 1994a,b; Ludsin and DeVries 1997; Maceina and Bettoli 1998; Garvey et al . 1998; Post et al . 1998; Fullerton et al . 2000; Garvey et al . 2000, 2002; see section on habitat). Large individuals can exceed 550 mm TL, weigh >3.5 kg, and attain age 8+ to 15+ (Carlander 1977; Beamesderfer and North 1995). The oldest largemouth bass and longest-lived Micropterus is a 23- or 24-year-old individual (584 mm TL) from New York (Green and Heidinger 1994). The world angling record for all Micropterus (and all centrarchids) is a largemouth bass weighing 10.1 kg (∼ 787 mm TL) that was caught in Georgia in 1932 (IGFA 2006). At least in some populations, older females (age 4+) are longer than males, and most older individuals are females (Webb and Reeves 1975; Carlander 1977). Coloration: Broad olive or olive black midlateral stripe formed of confluent or nearly confluent blotches. Silver to brassy green (brownish in tea-stained water) above with dark olive mottling. Scattered dark specks on lower sides; whitish below. Iris brown. Young (<50 mm TL) with bicolored caudal fin markings (whitish base, dark distally) (Bailey and Hubbs 1949; Page and Burr 1991; Etnier and Starnes 1993; Jenkins and Burkhead 1994). Native range: The largemouth bass is native to the St. Lawrence-Great Lakes, Hudson Bay (Red River), and Mississippi River basins from southern Quebec to Minnesota and south to the Gulf of Mexico and in Gulf drainages from about Mississippi or Alabama west to the Rio Grande and Soto la Marina in northeastern Mexico (Page and Burr 1991; Miller 2005). On the Atlantic Slope, early introductions of “largemouth bass” in many drainages obscured the northern limit of the native range (Jenkins and Burkhead 1994). Critical evaluation of early records and reports and evaluation of nuclearencoded allozyme data across Virginia suggests that the species occurred historically on the Atlantic Slope to the Tar

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River of North Carolina but not beyond (Jenkins and Burkhead 1994; Dutton et al . 2005). A broad area of hybridization between the largemouth bass and the Florida bass occurs across the southeastern United States. Before extensive stocking of Florida bass into the range of the largemouth bass, meristic variation indicated a relatively narrow hybrid zone between the two species from the Savannah River south to the St. Mary’s River on the Atlantic Slope and from the Choctawhatchee and St. Andrews bays east to the Suwannee River on the Gulf Slope (Bailey and Hubbs 1949). Genetic data incorporating many reservoir and a few riverine populations prescribe a broader area of hybridization, extending from at least central Texas eastward across parts of Louisiana and Arkansas, and most of Mississippi, Alabama, northern Florida, Georgia, and well northward on the Atlantic Slope to Virginia and Maryland. The large extent of the hybrid zone is primarily the result of repeated, deliberate introductions of Florida bass into the range of the largemouth bass, but the extent of natural, isolated populations of pure M. salmoides within this broad hybrid zone is uncertain (Philipp et al . 1981, 1983; Maceina et al . 1988; Morizot et al . 1991; Philipp 1991; Dunham et al . 1992; Brown and Murphy 1994; Bulak et al . 1995; et al .Gelwick et al . 1995; Whitmore and Craft 1996; Dutton et al . 2005; Lutz-Carillo et al . 2006). The largemouth bass, its sister species, the Florida bass, or genetic admixtures of the two species have been introduced and are established in much of North America from southern Canada to Mexico. The species is also established in the Caribbean, Oceania, Asia, Africa, Europe, and South America (Robbins and MacCrimmon 1974; Holˇc´ık 1991; Fuller et al . 1999). The largemouth bass is one of eight fishes included in the top 100 of the world’s worst invasive alien species (Cambray 2003) because of its negative effects on native fishes and ability to literally change ecosystem function (e.g., Whittier et al . 1997; Rahel 2000; Skelton 2000; Findlay et al . 2000; Gratwicke and Marshall 2001; Jackson 2002; Moyle 2002). Habitat: The largemouth bass inhabits lakes, ponds, swamps, marshes, and backwaters and pools of creeks, and small to large rivers as well as impoundments (Page and Burr 1991). Generally, the largemouth bass is adapted to warmer, more eutrophic waters than other Micropterus, except the Florida bass. Even so, the largemouth bass frequently co-occurs with other black basses, but in those cases the Micropterus assemblage often shows shifts in species-relative abundances among mesohabitats (e.g., Rutherford et al . 2001, see accounts on M. dolomieu and M. punctulatus). The species occurs and often thrives in an array of lacustrine habitats including saline marshes along the Gulf of Mexico and Atlantic Coast (Peterson and Meador 1994); bottomland hardwood swamps and associated floodplain lakes (Rutherford et al . 2001); and vegetated glacial lakes (Werner et al . 1977). Over its broad range, the species tends toward highest abundance in warm eutrophic, vegetated reservoirs or the most eutrophic sections within a reservoir (Robbins and MacCrimmon 1974; Durocher et al . 1984; Buynak et al . 1989; Maceina and Bettoli 1998; Allen 1999; Allen et al . 1999; Greene and Maceina 2000; Maceina and Bayne 2001; Brown and Maceina 2002). In swamps, lakes, and reservoirs, young and adult largemouth bass are associated with shallow shorelines (usually <3 m deep) around aquatic macrophyte beds, logs, or other cover, but the young use gravel substrates and steep shoreline slopes if vegetation or other cover is not present (e.g., Werner et al . 1977; Schlagenhaft and Murphy 1985; Matthews et al . 1992; Annett et al . 1996; Demers et al . 1996; Hayse and Wissing 1996; Irwin et al . 1997, 2002; Miranda and Pugh 1997; Essington and Kitchell 1999; Sammons and Bettoli 1999; Irwin and Noble 2000; Rutherford et al . 2001; Olson et al . 2003). Young largemouth bass in lakes and reservoirs move inshore at night and offshore during the day; such diel movement is lessened if inshore cover is present (Werner et al . 1977; Irwin and Noble 2000). In riverine habits, both young and adult largemouth bass occupy a variety of habitats but are most common in deep pools or low-velocity habitats near undercut banks, instream wood, overhanging and aquatic vegetation, or other cover (e.g., Killgore et al . 1989; Sowa and Rabeni 1995; LaPointe et al . 2007). The physical habitat needs, environmental tolerances, and spatial ecology of nearly all life stages of the largemouth bass, particularly for populations in reservoirs, are one of the most well studied of any fish species in North America, being rivaled only by some salmonids (e.g., rainbow trout) and the bluegill. Here, the focus is to briefly introduce aspects of largemouth bass movement in lakes and rivers, relate some broad effects of temperature, and highlight tolerances to salinity, hypoxia, and pH. These and other habitat-associated topics on largemouth bass are available in the references cited in this account and many other sources (e.g., Dahlberg et al . 1968; Glass 1968; Beamish 1970; Aggus and Elliot 1975; Coutant 1975; Heidinger 1975; Siler and Clugston 1975; Farlinger and Beamish 1977; Bennett 1979; McCormick and Wegner 1981; Lemons and Cranshaw 1985; Fields et al . 1987; Johnson et al . 1988; Koppelman et al . 1988; Kolok 1991, 1992; Smale and Rabeni 1995b; Raibley et al . 1997b; Miranda and Dibble 2002; Parkos and Wahl 2002). The largemouth bass exhibits directed movement (homing) over relatively long distances, movement to and from wintering (and spawning) areas, and persistent association with home activity areas over long periods. Movement is related to water temperature with activity generally being lowest at temperature extremes of midsummer and midwinter (Warden

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and Lorio 1975; Carlson 1992; Nack et al . 1993; Richardson-Heft et al . 2000; Karchesky and Bennett 2004; Hasler et al . 2007). During winter in an iced-over northern lake, acoustically tagged largemouth bass stayed in a deep basin in the lake, but moved in spring to a shallow basin (Hasler et al . 2007). In both seasons bass formed multi-individual aggregations (individuals <2 m apart) during the day. Aggregations, especially in winter, lasted for several hours a day, and male–female associations were greater than expected by chance (Hasler et al . 2007). Tracking studies suggest that largemouth bass, when moving from one activity area to another, travel along the deepest bottom contours (e.g., submerged creek channels) in shallow lacustrine habitats or in the low-velocity currents along shorelines in flowing rivers (Warden and Lorio 1975; Karchesky and Bennett 2004). In displacement studies, about 26% to 43% of individuals return to their original place of capture; some individuals require months to return and others a few days even if displacement distances are similar (Parker and Hasler 1959; Stang et al . 1996; Richardson-Heft et al . 2000; Ridgway 2002; Wilde 2003). Many individuals displaced in the upper Chesapeake Bay traveled at least 15 to 21 km across the bay to return to their original place of capture, although return times tended to take longer in fall (228 days) than in spring (65 days) (Richardson-Heft et al . 2000). In the same study, mean daily movement of 78 displaced radio-tagged largemouth bass was up to 1.45 km/d and maximal movement was 8.37 km/d. Other studies of the species document even longer distance movements (16–64 km) to consistently used winter refuges (or spawning areas) to avoid extreme flows, wave action, and temperature conditions (Funk 1957; Raibley et al . 1997a; Nack et al . 1993; Gent et al . 1995; Irwin et al . 2002; Karchesky and Bennett 2004). Postspawning summer and fall home range areas of largemouth bass in an Ontario lake averaged 16.7 to 17.6 ha (Ridgway 2002). Studies of riverine or other lake-dwelling populations generally reveal high persistence (8–110 days) in even smaller areas (150 linear stream meters, 0.18–3.0 ha). However, movements out of these high-use areas for extended periods, movements among high-use areas, and extensive ostensibly random movements without establishment of apparent activity areas are also common (e.g., Lewis and Flickinger 1967; Warden and Lorio 1975; Winter 1977; Savitz et al . 1983, 1993; Meador and Kelso 1989; Bain and Boltz 1992; Gatz and Adams 1994; Rogers and Bergersen 1995; Demers et al . 1996; Essington and Kitchell 1999; Karchesky and Bennett 2004). Temperature exerts considerable influence on largemouth bass populations across the broad band of latitude comprising the total range of the species. The species has a relatively high critical thermal maxima of 38.5 to 40.9◦ C (acclimated at >30◦ C, Smith and Scott 1975; Fields et al . 1987; Beitinger et al . 2000; Currie et al . 1998, 2004), so that high temperatures are not particularly limiting. In contrast, the summer thermal regime or, alternatively, the duration and severity of winters profoundly affect the distribution, growth, and survival of largemouth bass. In a synthesis of growth data across North America (from Carlander 1977), over half the latitudinal variation in growth (size at age) for largemouth bass (including Florida bass) was accounted for by differences in monthly mean air temperatures (degree days >10◦ C) across a north–south latitudinal gradient (McCauley and Kilgour 1990). The northern distributional limit for the largemouth bass was estimated as a thermal unit isocline of 550 degree days above 10◦ C in extreme southern Canada. In a model incorporating data for largemouth bass populations across North America (again including a few Florida bass), age to reach 300 mm TL was correlated negatively with mean air temperature (also degree days >10◦ C and latitude), and instantaneous natural mortality rate was correlated positively with mean air temperature (Beamesderfer and North 1995). Likewise, average length by fall of age-0 largemouth bass is related positively to latitude and presumably temperature (Garvey et al . 2003). Temperature effects are directly or indirectly related to several critical events in the first year of life including hatch date, length of growing season, transition to piscivory, fall lipid accumulation, winter food availability, and the duration and severity of winter (Kramer and Smith 1960a, 1962; Adams et al . 1982a,b; Isely et al . 1987; Miranda and Hubbard 1994a,b; Ludsin and DeVries 1997; Post et al . 1998; Wright et al . 1999; Fullerton et al . 2000; Jackson and Noble 2000; Fuhr et al . 2002; Philipp et al . 2002). For age-0 fish, winter is often a huge survival bottleneck because of complex interactions of winter severity, food availability, and predation. When water temperatures are <6◦ C for extended periods, feeding is stopped or is infrequent and small individuals experience greater proportional energy loss and increased mortality relative to large individuals (Garvey et al . 1998). If low temperature conditions are prolonged, energy reserves built up in summer and fall can be depleted in small individuals regardless of winter food availability (Wright et al . 1999). Under less severe winter conditions, warm or fluctuating winter temperatures may exacerbate metabolic costs of young fish during a period of reduced food availability (e.g., fish prey too large) and increased predation risk (Ludsin and DeVries 1997). Common garden and winter simulation experiments measuring differential growth and survival among largemouth bass from different latitudes provide compelling evidence of genetic adaptation to local temperature regimes (and other local environmental factors). When stocks of largemouth bass from Wisconsin, Illinois, and Texas were compared in common garden experiments, the local native stock consistently had higher growth, survival, and reproductive fitness

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than transplanted nonnative stocks (Philipp et al . 2002). In laboratory experiments, 92% to 100% of age-0 largemouth bass from Alabama died when subjected to simulated temperatures, lengths, and photoperiods of an intermediate (Ohio) and long (Wisconsin) winter, but similar-sized Ohio and Wisconsin stocks survived a simulated Alabama winter. Energy depletion measured as weight loss showed a gradient with fed individuals from all three sources maintaining or gaining weight under the Alabama winter, maintaining weight under the Ohio winter, and losing weight under the Wisconsin winter. Winter survival was also size mediated with small fish suffering higher mortality than large fish under both the Alabama and Wisconsin winters (Wright et al . 1999; Fullerton et al . 2000), results consistent with experimental studies in ponds and empirical observations in reservoirs (Miranda and Hubbard 1994a; Ludsin and DeVries 1997). Coastal populations of largemouth bass frequent oligohaline marsh systems along the Atlantic and Gulf coasts. These populations are at least moderately tolerant of prolonged saline conditions (usually <8 ppt) and show differences in salinity selection, physiology, and growth relative to freshwater populations (Meador and Kelso 1990a,b; Peterson 1991; Peterson and Ross 1991; Peterson and Meador 1994; Krause 2002; Peer et al . 2006). Effects of <4 ppt salinity on blood plasma level concentrations in adult coastal marsh and freshwater largemouth bass populations in Louisiana are minimal, and acclimation does not affect salinity preferences (to 5 ppt), suggesting efficient osmoregulation in low salinities (Meador and Kelso 1990b). Young-of-the-year of freshwater and coastal marsh largemouth bass preferred 0-ppt salinity over a gradient (0, 3, 6, 9, 12 ppt). Adult marsh largemouth bass had significantly more observations at 3 ppt, and freshwater bass had significantly more observations at 0 ppt, although both selected 3 ppt most often (Meador and Kelso 1989). Relative to freshwater populations, coastal marsh largemouth bass can reduce osmoregulatory stress at 8 ppt salinity by conserving adenosine triphosphate (ATP), reducing active ion transport, and tolerating elevated plasma ion levels (Meador and Kelso 1990b). Young-of-the-year coastal marsh largemouth bass appear even better able to maintain osmoregulatory function than adults up to 12-ppt salinity, but mortality is severe with 48-hour exposures to 16 ppt (Susanto and Peterson 1996). Exposure to 12-ppt salinity in laboratory trials caused adults from coastal marsh and freshwater populations to cease feeding and die within 7 days (Meador and Kelso 1990b). Coastal marsh largemouth bass also exhibit small size and reduced length at age, but maintain excellent condition (relative weight) year round, indicating that they are not stressed physicochemically by marsh environments (Meador and Kelso 1990a). Marsh-dwelling largemouth bass also exhibit a decided growth response to increasing salinities. In Louisiana coastal populations, growth in length is reduced at 0-ppt salinity and increased at 8 ppt relative to freshwater largemouth bass (Meador and Kelso 1990a). In Mobile Bay, Alabama, first-year growth of largemouth bass along a freshwater to mesohaline gradient of sites was higher in individuals within or adjacent to brackish waters (Peer et al . 2006). A short, rotund body is characteristic of coastal largemouth bass (Hallerman et al . 1986; Meador and Kelso 1990a), reflecting a redistribution of somatic growth relative to freshwater populations. The body form may be related to being shifted from a position as a cruising top predator in freshwaters to a secondary predator restricted to highly structured edges to avoid larger predators in these piscivore-rich habitats (Meador and Kelso 1990a). Osmoregulatory adaptations, differential growth responses, and body form suggest genetic differences between coastal and freshwater largemouth bass, but no profound biochemical genetic differences emerged in populations examined thus far (Hallerman et al . 1986). Oligohaline marsh populations in Mobile Bay possess higher genetic heterozygosities relative to upstream freshwater populations (Hallerman et al . 1986), possibly reflecting adaptation to a more dynamic physicochemical environment (Peterson and Meador 1994; Peer et al . 2006). The largemouth bass is tolerant of low DO levels, avoiding only extreme hypoxia and its associated physiological costs. In natural settings, individuals apparently move to streams or other oxygenated refugia to avoid winter-associated low oxygen levels in northern lakes and bogs, reinvading these habitats when DO levels increase in summer (Tonn and Magnuson 1982; Rahel 1984). Likewise, the species appears to avoid hypoxic conditions in densely vegetated southern reservoirs and wetlands during summer temperature extremes (Rutherford et al . 2001; Killgore and Hoover 2001). Hypoxia tolerance in the species is size mediated such that small individuals can use more hypoxic waters than large individuals (Moss and Scott 1961; Cech et al . 1979; Burleson et al . 2001). This is a potentially important factor for young largemouth bass forced by competition or predation to occupy marginal habitats (Burleson et al . 2001). Nevertheless, largemouth bass across a range of sizes (23–3000 g at 24◦ C) avoid extreme hypoxic conditions, seeking water with >27% air saturation (ca. >2.4 mg/l DO) (Burleson et al . 2001) but show little or no avoidance to DO concentrations as low as 3.0 mg/l (19–20◦ C) (Whitmore et al . 1960). In laboratory trials largemouth bass show relatively low average critical DO levels (24-hr survival or cessation of ventilation) of 0.70 to 1.2 mg/l (Moss and Scott 1961; Smale and Rabeni 1995a). Embryos develop and hatch at DO levels as low as 1.0, 1.1, and 1.3 mg/l at 15, 20, 25◦ C but concentrations below 2.0, 2.1, and 2.8 at these respective temperatures significantly lowered survival; most mortality occurred during hatching when oxygen demand is presumably

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higher (Dudley and Eipper 1975). At 20 and 23◦ C, DO concentrations as low as 35% saturation are adequate for larvae, but growth is reduced at ≤70% saturation, and at ≤50% saturation hatching of eggs is premature and first feeding delayed (Carlson and Siefert 1974). Hypoxic conditions impose other physiological costs and constraints on largemouth bass. Diurnal low oxygen levels (2.5 to 4.1 mg/l at about 20◦ C), simulating early morning reductions in DO concentration, produce measurable, stress-related changes in serum proteins, reduce food consumption, cause digestive interference, and increase ventilation rates in largemouth bass (Bouck and Ball 1965). Hypoxic conditions (<5 mg/l at 26◦ C) reduce growth rate and food consumption of small largemouth bass (62–85 mm TL), but food conversion efficiencies are not affected except at extremely low DO concentrations (4 mg/l; Stewart et al . 1967). Swimming ability of small largemouth bass decreases with decreasing temperature under hypoxic conditions (Katz et al . 1959; Dahlberg et al . 1968). For example, juveniles (93–100 TL) were able to swim against a current of 3.8 cm/s for 1 day at DO levels of 2.05 mg/l at 25◦ C, but were unable to swim against the same current at 2.8 mg/l at 20◦ C or at 5 mg/l at 17◦ C. Maximum sustained swimming speed of juveniles was reduced at oxygen concentrations <5 to 6 mg/l (at 25◦ C) (Dahlberg et al . 1968). Intraspecific differences in tolerances of geographically disparate populations of largemouth bass to low DO are notable. For example, largemouth bass from Wisconsin showed lower hypoxia tolerance than largemouth bass from Missouri streams (critical levels of 1.01 versus 0.70 mg/l DO, respectively) (Smale and Rabeni 1995a). In another example, swimming performance and routine oxygen consumption differed between largemouth bass stocks from Illinois and Wisconsin in trials at different temperatures. Notably, hybrid individuals between the stocks showed reduced performance relative to locally adapted stocks, particularly at higher temperatures. In essence, the hybrid stocks displayed performance impairment rather than hybrid vigor, which emphasizes the importance of adaptation to local environmental conditions in largemouth bass (Cooke et al . 2001a; Cooke and Philipp 2005, 2006). Adult largemouth bass are generally more tolerant of lowered pH than egg, larval, and juvenile stages. For example, adults nested and spawned each year as pH in an experimental lake was decreased gradually from 6.1 to 4.7 over several years (Little Rock Lake, WI), but the percentage of nests producing swim-up fry declined significantly with decreasing pH. At pH 5.1, percentage of nests producing swim-up fry fell below that observed in the reference basin and overwinter survival decreased, and no swim-up fry were observed at pH 4.7, a lower limit consistent with laboratory and additional in situ tests (Eaton et al . 1992; Brezonik et al . 1993). In a related laboratory study, juvenile largemouth bass (6.7 g) osmoregulated and survived up to 30 days at pH ≥4.5 but lost osmoregulatory control at pH 4.0 and died within a few days (McCormick et al . 1989). Young-of-the-year (2.5–4.5 g) were subjected (at 3.8◦ C with a simulated spring increase to 18◦ C) to a graded series of pH (4.5–8.0), two Ca concentrations (1.5 and 13.4 mg/l), and two monomeric Al concentrations (6 and 30 µg/l) for 113 days (McCormick and Jensen 1992; Leino and McCormick 1993). Survival probabilities were most affected at low Ca and high Al levels and were correlated with decreased osmoregulatory function and gill damage. For example, fish at pH 5.0 and high Al levels had a 56% chance of survival to day 84 compared to a 99% chance for fish at the same pH with no Al. Laboratory analyses of behavioral repertoires of young-of-the-year largemouth bass acclimated to decreasing pH suggest that values <6.1 may increase energy demands. At low pH extremes, feeding and swimming activity of young-of-the-year is reduced (Orsatti and Colgan 1987), ultimately increasing risk of starvation. Food: The largemouth bass is an opportunistic top carnivore, exploiting prey from the bottom to the surface. Adults feed primarily on fishes (e.g., clupeids, yellow perch, Lepomis spp., silversides, minnows, topminnows, darters); crayfish and grass shrimp (if available); and large aquatic insects (e.g., odonate and mayfly larvae), including winged adults (Applegate et al . 1967; Olmsted 1974; Carlander 1977; Hubert 1977; Cochran and Adelman 1982; Huskey and Turingan 2001; Pope et al . 2001; Sammons and Maceina 2006). In their first summer of life, largemouth bass young-of-the-year shift from an initial diet of microcrustaceans to begin exploiting a variety of aquatic insect larvae, especially diptera larvae and pupae and some fish at about 30 to 70 mm TL. Between about 30 and 100 mm TL, individuals begin a usually rapid transition to a diet predominated by small fishes and if available, amphipods, crayfish, or grass shrimp (Keast 1965; Applegate et al . 1967; Miller and Kramer 1971; Timmons et al . 1980; Keast 1985b,c; Keast and Eadie 1985; Matthews et al . 1992; Olson et al . 1995; Olson 1996; Miranda and Pugh 1997; Huskey and Turingan 2001; Pelham et al . 2001). In fast-growing individuals or cohorts spawned early, the shift to piscivory occurs in the first summer of life, but if food availability or prey size is limiting the shift can be delayed (Kramer and Smith 1960a; Timmons et al . 1980; Miller and Storck 1984; Keast and Eadie 1985; Phillipps et al . 1995; Olson 1996; Ludsin and DeVries 1997). For example, in a densely vegetated southern reservoir, most juvenile largemouth bass delayed the shift to piscivory until 140 mm TL, relative to ≥60 mm TL after vegetation removal, a delay presumably associated with limited availability of fish prey in the dense

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vegetation (Bettoli et al . 1992). Similarly, late-hatched individuals may not find enough fish prey of suitable size and exploit insect or even zooplankton prey for much of the first year of life (e.g., Phillips et al . 1995). Regardless of age, the largemouth bass is adept at exploiting available food resources, feeding almost solely on invertebrates if fish are unavailable or opportunistically preying on vertebrates of terrestrial origin to augment the diet (i.e. salamanders, frogs, snakes, shrews, voles, mice, and birds; Clady 1974; Carlander 1977; Cochran and Adelman 1982; Becker 1983; Hodgson et al . 1997; Schindler et al . 1997; Ernst and Ernst 2003). In some populations, terrestrial vertebrates contribute substantially to the diet (Clady 1974; Hodgson et al . 1997). If large size differences exist among young, or alternate fish prey are unavailable, cannibalism also can contribute a major portion of the juvenile or adult diet, most often involving consumption of youngof-the-year or age-1 bass (e.g., Kramer and Smith 1962; Applegate et al . 1967; Clady 1974; Timmons et al . 1980; Cochran and Adelman 1982; Hodgson and Kitchell 1987; Olson et al . 1995; Hodgson et al . 1997; Schindler et al . 1997; Post et al . 1998; Pothoven et al . 1999; Pine et al . 2000). Activity and feeding patterns of largemouth bass are characterized by peaks at or just before dawn, midday, and dusk (Olmsted 1974; Reynolds and Casterlin 1976b; Demers et al . 1996). Young-of-the-year, still under the protection of guardian males, and recently dispersed young forage continuously throughout the day, resting at night in cover in shallow water (Elliott 1976; Helfman 1981). Intermediate-size largemouth bass (ca. 6–20 cm) often forage during the day in groups (up to 50) and simultaneously attack schools of prey fishes (Helfman 1981; Becker 1983; Sowa and Rabeni 1995). In adults, feeding tends to show crepuscular peaks, but nocturnal activity, movement, and presumably foraging can be high and extend well after dusk into the early morning hours, especially at high summer water temperatures (>27◦ C) (Olmsted 1974; Warden and Lorio 1975; Helfman 1981; Demers et al . 1996). Although feeding and movement decline as water temperature decreases, largemouth bass actively feed and can grow during the winter at temperatures ≥6◦ C (Bennett and Gibbons 1972; Olmsted 1974; Warden and Lorio 1975; Hubert 1977; Etnier and Starnes 1993; Garvey et al . 1998; Fullerton et al . 2000). The behavior, functional morphology, bioenergetics, and other aspects of the trophic biology and ecology of the largemouth bass are among the most extensively documented of any North American freshwater fish. Aspects of learning and foraging adaptability; prey detection; chemical alarm cues; and predator effects are introduced here. The interested reader is encouraged to consult papers cited in this account on these and other feeding-related topics, including for example, Lewis et al . 1961, 1974; Laurence 1969, 1972; Beamish 1972; Niimi 1972a,b; Niimi and Beamish 1974; Heidinger and Crawford 1977; Rice et al . 1983; Brown and Colgan 1984; Rice and Cochran 1984; Webb 1986; Hoyle and Keast 1987, 1988; Wahl and Stein 1989; Hambright 1991; Hambright et al . 1991; Hodgson et al . 1991; Trebitz 1991; Wainwright and Lauder 1992; He et al . 1994; Richard and Wainwright 1995; Wainwright and Richard 1995; Wainwright and Shaw 1999; Zweifel et al . 1999; Essington et al . 2000; and Garvey and Marschall 2003. Largemouth bass quickly learn to locate, capture, and handle novel prey items, even when shifted from simple to structurally complex habitats. The species can switch among modes of ram strike feeding for water column prey (Norton and Brainerd 1993), suction feeding for benthic prey in crevices, and biting for exposed benthic prey (Nyberg 1971; Winemiller and Taylor 1987). In experimental settings, largemouth bass shifted from a cruising–searching–foraging strategy to an ambush strategy for fish prey as vegetation density was increased (Savino and Stein 1989a,b). Young largemouth bass, often forced into structurally complex habitats to avoid predation, rapidly learned to change foraging tactics in experimental settings. When switched from intermediate to highly structured habitats, the young bass initially used tactics from the previous habitat in the new habitat to capture damselfly nymphs, but individuals modified search and prey selection strategies in a few days to increase capture efficiency in the most structurally complex habitat (Anderson 1984). Learning also plays a role in foraging success of postlarval largemouth bass. Hatchlings raised on natural food (live zooplankton) for 9 weeks were significantly more efficient predators when exposed to live fish than were fry raised on artificial diets. Apparently the fry fed natural foods learned critical aspects of a behavioral repertoire necessary to efficiently capture live fishes. Even so, with exposures to natural diets the artificial diet group improved prey capture efficiency with experience (Colgan et al . 1986). In natural settings, the survival to age-1 of stocked pellet-fed largemouth bass is lower than that of individuals fed minnows before stocking (Heidinger and Brooks 2002), providing indirect support for the laboratory findings. The largemouth bass is a highly vigilant, visual predator but responses to prey or potential predators vary with size, type, and movement of the visual target, light intensity, and water clarity. In choice experiments between close and distant stationary prey, largemouth bass (290 mm TL) chose the closer of two prey of equal size, suggesting that they can judge distances and the absolute size of their prey (or potential predator) (Howick and O’Brien 1983). Largemouth bass also can

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visually assess the differential risk posed by different aerial predators. Cardiac responses of largemouth bass exposed to a blue heron, a predator with size-restricted predation ability on bass, were greater in smaller more vulnerable largemouth bass than in less vulnerable larger largemouth bass. Bass response to an osprey predator with ability to consume larger fish than a blue heron was also size mediated, but the responses were more extreme than in the heron exposures, and individuals of all sizes required more time for recovery (Cooke et al . 2003b). Largemouth bass can see effectively even at relatively low light levels. As light level decreases, adults (290 mm TL) show no obvious decline in reactive distance (>120 cm) to motionless bluegill (60 mm TL) prey until light is <5 lux (Howick and O’Brien 1983); then reactive distances decrease steeply to about 33 cm at 0.195 lux. At low light intensity, differences in reactive distances to prey from 30 to 90 mm TL are minimal. Reactive distances increase when largemouth bass are exposed to moving versus stationary prey of similar size. For example, reactive distances of individual bass of 280 to 300 mm TL to crayfish (at 200 lux) increases linearly with crayfish size (17–29 cm carapace length) but reactive distances to moving crayfish is nearly double that of stationary crayfish (Crowl 1989). As prey size increases to about 65 mm TL, reactive distances to moving and stationary prey types converge (Howick and O’Brien 1983). As turbidity increases reactive distance to crayfish prey (17–29 cm carapace length, at 200 lux) decreases from >150 cm at 3 JTU to about 30 cm at 17 JTU; at the higher turbidity, crayfish size or movement does not increase reactive distances. In turbid water, largemouth bass attacked rectangular stones used to assess prey recognition, a behavior never observed under clear water conditions (Crowl 1989). In another water clarity experiment, largemouth bass (83–130 mm FL) showed a trend of decreased capture rates of fathead minnows as turbidities increased from 1 to 70 NTU (at 430 to 538 lux), the trend driven primarily by a decrease in vulnerability of the smallest size class of prey (26–30 mm FL). Even so, only the most extreme turbidity tested showed a significant reduction in minnow capture rates (Reid et al . 1999). Experimental studies indicate that largemouth bass are not totally dependent on vision for feeding but can integrate nonvisual senses with vision to capture and assess palatability of prey. The pharyngeal teeth of largemouth bass are in close association with numerous taste buds, and this association is linked closely with whether a potential food item is ultimately rejected or swallowed (Linser et al . 1998). At light intensities ranging from full moonlight (0.003 lux) to low-intensity daylight (312 lux), adult largemouth bass located and ate 95 to 100% of offered live fish prey in 15-minute trials in large tanks. Foraging success declined to 62% and was highly variable under starlight (0.00026 lux) and further declined to 0% in total darkness (0 lux), but when the total darkness trial was extended to 1 hour, capture success increased to 2.5%. From these results, the threshold for visual feeding by largemouth bass (light intensity at 50% prey capture success) is estimated at 0.00016 lux (McMahon and Holanov 1995), much less than that implied by reactive distance studies (e.g., 1.49 lux, Howick and O’Brien 1983), and suggests that nonvisual senses, such as the lateral line, play a role in prey detection and capture. In an experiment testing the role of the lateral line in feeding, largemouth bass were subjected to a visual stimulus (food) and a lateral line stimulus (water jet) directed at various regions of the head. The water jet, with or without the visual stimulus, always elicited an orientation movement and bite toward the stimulus. In individuals with the lateral line pharmacologically ablated, there was no response to the water jet. The orientation and bite were interpreted as unconditioned responses to lateral line stimulation by the water jet with potential importance to prey location (Janssen and Corcoran 1993). In another feeding experiment, largemouth bass were lateral line ablated, bilaterally blinded, or both, and the distances of first orientation to live fish prey and strike measured. Relative to controls, the lateral line–ablated individuals showed decreased distance of first orientation and strike (i.e. both positions closer to prey). Blinded individuals showed even further decreases in first orientation and strike positions. Strike success (prey capture) decreased along a gradient from 79% in controls, 70% in lateral line–ablated individuals, 59% in blinded individuals, and near 0% in blinded, lateral line–ablated individuals. Without input from the lateral line the threshold at which the bass responds to prey apparently is raised (distance to orientation and strike positions reduced), and the lateral line alone provides sufficient information at the closest ranges to successfully capture prey (New and Kang 2000; New 2002). Largemouth bass respond to chemical alarm cues, which are released from damaged individuals of heterospecifics (e.g., cyprinids). Juvenile bass undergo an ontogenetic shift in response to heterospecific chemical cues, which coincides with shifts in diet and habitat use. Antipredator responses are supplanted by foraging responses at the time juvenile fish switch from invertivory to piscivory and are large enough to avoid predation from large piscivores. In laboratory and field trials, invertivorous young-of-the-year largemouth bass exhibited significant antipredator responses (e.g., freezing, dropping to substrate) to chemical alarm cues of finescale dace and green sunfish, but larger piscivorous individuals exhibited foraging responses to the same cues. In field trials, small largemouth bass (30–60 mm SL) actively avoided areas injected with dace extract, but slightly larger individuals (61–81 mm SL) were attracted to these areas (Brown et al . 2001, 2002).

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Even though largemouth bass are highly adaptable foragers, the degree of structural complexity of the habitat affects their foraging success. In a variety of experiments, very dense aquatic vegetation (e.g., >270 stems/m2 ) decreases feeding success of largemouth bass (e.g., increased search times, reduced attack rate), but foraging success in intermediate densities is comparable to success rates in low-density or open-water habitats (Savino and Stein 1982, 1989a,b; Anderson 1984; Schramm and Zale 1985; Gotceitas and Colgan 1987, 1989; Hayse and Wissing 1996; Valley and Bremigan 2002). Aspects of growth form, architecture, and spatial heterogeneity of vegetation (or other cover) also affect foraging success of the species (Dibble and Harrel 1997; Valley and Bremigan 2002). Juvenile and adult bass showed dramatic shifts in use of macroinvertebrates and fishes in enclosures of Eurasian milfoil compared to pondweed, the shifts being attributed to differences in the fine architecture of the plant growth forms (Dibble and Harrel 1997). Likewise, attack and consumption rates of largemouth bass on bluegill prey were decreased in monoculture aquatic macrophyte beds forming surface canopies relative to diverse beds with growth dispersed throughout the water column (Valley and Bremigan 2002). In field settings, changes in prey vulnerabilities and prey assemblages with sudden shifts in density and composition of aquatic plant communities can lead to large changes in the diet and in the most densely vegetated habitats can even reduce growth (e.g., delay shift to piscivory) and condition in largemouth bass populations (Wiley et al . 1984; Bettoli et al . 1991, 1992; Dibble et al . 1996; Wrenn et al . 1996; Miranda and Pugh 1997; Pothoven et al . 1999; Unmuth et al . 1999; Brown and Maceina 2002; Sammons and Maceina 2006). The largemouth bass is considered a keystone species in many streams and lakes because of their profound effects as predators on prey habitat use, community structure, and trophic-level biomasses (e.g., Carpenter et al . 1987; Harvey 1991a; Mittelbach et al . 1995; Power et al . 1996; Schindler et al . 1997; Jackson 2002; Miranda and Dibble 2002). The striking patterns of complementary distribution of adult largemouth bass and small-bodied fishes and their interaction as predator and prey formed the foundation for much of our understanding of the importance of biotic interactions in structuring fish assemblages in streams and lakes (e.g., Werner 1977; Werner et al . 1977, 1983; Power and Matthews 1983; Mittelbach 1983, 1984a, 1986; Power et al . 1985; Werner and Hall 1988; Mittelbach et al . 1995). The direct and indirect effects of largemouth bass on aquatic communities have been demonstrated in laboratory experiments, in artificial streams, and in manipulations and empirical studies in streams and lakes. Largemouth bass elicit strong predator avoidance behaviors from many fishes and other aquatic organisms, behaviors that can produce indirect effects on other components of the community. Laboratory and field studies, most often involving Lepomis, document dramatic changes in foraging behavior and habitat use of prey fishes faced with predation risk from largemouth bass (e.g., Savino and Stein 1982, 1989a,b; Morgan and Colgan 1987; Morgan 1988; DeVries 1990; Gotceitas 1990b; Gotceitas and Colgan 1990; Harvey 1991a; Matthews et al . 1994; Hayse and Wissing 1996). The foraging strategy of prey fish in the presence of bass may shift from an optimal foraging pattern to one minimizing the ratio of mortality rate to foraging rate (e.g., form more compact shoals, increased time in cover or shallow water, increased swimming rate, decreased foraging rate). Experiments in artificial streams using two grazers, a minnow (Campostoma anomalum), and a crayfish (Orconectes virilis), with and without largemouth bass, exemplify the potential direct and indirect effects of the species. In the presence of largemouth bass, the minnows formed tighter schools, used shallower habitats, and avoided grazing in pools with bass. Crayfish reduced risk from bass predation by foraging at night, hiding in burrows in the daytime, or avoiding pools used most by the bass (Gelwick 2000); similar reductions in activity and habitat use is documented in other studies of crayfish response to largemouth bass (Hill and Lodge 1994; Garvey et al . 1994). Algal growth in the experimental stream was also greater in treatments with largemouth bass and grazers than with grazers alone, suggesting that the bass indirectly affected algal productivity by reducing activity levels and locations of grazers (Gelwick 2000) and supporting results in mesocosm experiments on macrophyte–crayfish–bass interactions (Hill and Lodge 1995). Empirical and manipulative studies in natural stream settings closely parallel laboratory and artificial stream findings of the effects of largemouth bass on stream communities. In stream pools, the distribution of adult largemouth bass is correlated negatively with many small-bodied stream fishes, providing indirect evidence of a bass effect on potential prey species (Power and Matthews 1983; Power et al . 1985; Harvey et al . 1988; Matthews et al . 1994). When adult largemouth bass were added to or removed from stream pools, prey fishes responded with changes in abundance and habitat use, but the response was size mediated. With addition of bass to pools, juvenile Lepomis (16–80 mm TL) rapidly moved to shallow water, but larger Lepomis did not appreciably alter their depth distributions. Within a stream pool, the abundance of small stream fishes (16–80 mm TL) decreased with increased bass abundance, and abundance of large fish (>80 mm TL) increased with increased bass abundance. Small fishes remaining in bass-containing pools occupied shallow pool margins, but those in pools without bass used the entire pool. Larval minnows and larval Lepomis were only found in pools that

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contained, or had contained, largemouth bass. Experimental manipulation of bass and Lepomis larvae in stream pools indicated that bass presence enhanced short-term survival of the larvae, likely an indirect effect of the shift in small fishes that prey on the larvae (Harvey 1991a). A particularly strong seasonal interaction can occur between largemouth bass, an algae-grazing minnow (Campostoma anomalum), and attached algae in stream pools. Large schools of Campostoma grazing in stream pools can dramatically reduce algal biomass and composition on stream substrates (Power and Matthews 1983; Matthews et al . 1987; Power et al . 1988) and influence the life histories of other invertebrates as well (Vaughn et al . 1993). In a small prairie-margin stream in Oklahoma, largemouth bass (>70 mm SL) and Campostoma showed complementary distributions among stream pools with differential crops of periphyton during summer low flow (Power and Matthews 1983; Power et al . 1985). Pools with bass had lush standing crops of epiphyton covering rocky substrates, but in the Campostoma pools, epiphyton was confined to pool margins, and most rocky substrates were bare. Experimental addition of bass to pools caused Campostoma to immediately emigrate from the pool or move to shallow water margins of the pool. Those that did remain in bass pools spent significantly less time in feeding and more time in cover than they did before bass were added. After bass addition, the standing crop of algae in pools increased significantly within 10 to 13 days (Power et al . 1985). The pattern of abundance of adult largemouth bass and small fishes in streams is congruent with that observed in lake communities. Several studies demonstrate the shift of juvenile bluegill to vegetated or shallow littoral zones as a refuge from predation by Micropterus (e.g., Savino and Stein 1982, 1989a,b; DeVries 1990; Gotceitas 1990b; Gotceitas and Colgan 1990) and others demonstrate the indirect effects of largemouth bass on the zooplankton prey of bluegills or other Lepomis (e.g., Hambright et al . 1986; Werner and Hall 1988; Turner and Mittelbach 1990; Hambright 1994). For example, in pond experiments using largemouth bass and small bluegills, the bass induced a habitat shift in small bluegill, resulting in size distributions skewed toward larger bluegill, a direct predation effect of bass. In turn, the shift to larger bluegill produced pronounced differences in zooplankton abundance and size structure (e.g., three cladocerans and the phantom midge became more abundant in the bass treatment), an indirect effect of bass on the aquatic community (Turner and Mittelbach 1990). A long-term lake study in which largemouth bass were eliminated by a natural event (1978) and then reintroduced (1986) is further illustration of their role as keystone species in some lakes (Mittelbach et al . 1995; see also Carpenter et al . 1987; Hall and Ehlinger 1989; Drenner et al . 2002). Elimination of bass was followed by a dramatic increase in planktivorous fish (e.g., golden shiner, 400,000/lake), the disappearance of large zooplankton, and the appearance of many small-bodied cladocerans, states which were maintained throughout the period of absence of the bass. On reintroduction of largemouth bass, the lake steadily returned to its previous state. Planktivore numbers decreased by two orders of magnitude (golden shiners being practically eliminated), large-bodied zooplankton reappeared and dominated the zooplankton, and the suite of small-bodied cladocerans disappeared. Total zooplankton biomass increased 10-fold and water clarity increased significantly. Reproduction: Maturity is usually reached by age 2+ to 4+ at minimum sizes of about 250 to 300 mm TL but can occur at age 1+ in fast-growing populations or be delayed until age 5+ in cool north temperate waters (Bryant and Houser 1971; Webb and Reeves 1975; Carlander 1977; Becker 1983). Spawning activity can begin in early spring at a water temperature as low as 12◦ C, but most individuals initiate spawning after the water temperature reaches and exceeds 15◦ C. The spawning season extends over 2 to 10 weeks, peaks between water temperatures of 15 and 21◦ C, and winds down as waters warm to and consistently exceed 24◦ C. Spawning occurs from mid-May to mid-June or even early July at north temperate latitudes and shifts to earlier dates at progressively lower latitudes (e.g., mid-March to May or early June in Mississippi and Alabama) (Kramer and Smith 1960a; Allan and Romero 1975; Becker 1983; Miller and Storck 1984; Isely et al . 1987; Goodgame and Miranda 1993; Annett et al . 1996; Post et al . 1998; Sammons et al . 1999; Greene and Maceina 2000; Cooke et al . 2006). Large adult male and female largemouth bass spawn before smaller adults. The earlier hatched young of large bass often gain and maintain a distinct size advantage over the later hatched young of smaller bass, a size advantage that may increase probability of survival to age 1+ (Miller and Storck 1984; Miranda and Muncy 1987; Goodgame and Miranda 1993; Phillips et al . 1995; Ludsin and DeVries 1997; Sammons et al . 1999; Pine et al . 2000). Males use caudal sweeping to excavate circular, depressional nests (0.6–1.0 m diameter) 1 to 2 days before spawning (Kramer and Smith 1962; Cooke et al . 2001b). Males can successfully sweep out nests over a variety of substrates (e.g., silt to boulders, stump tops, logs, clay slabs), but coarse gravel and sand and the roots and stems of aquatic vegetation are substrates most often used (Reighard 1906; Miller and Kramer 1971; Allan and Romero 1975; Annett et al .

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1996; Hunt et al . 2002). Most males select nest sites near simple cover (e.g., horizontal log, tree trunk) where they suffer less nest intrusion by brood predators and expend less effort in aggressive actions than males selecting sites near complex cover (e.g., brush piles, patches of aquatic macrophytes) (Annett et al . 1996; Hunt et al . 2002). Although a few nests have been reported from >6 m depth, most nests are placed in water <4 m deep with average or median depths ranging from 0.40 to 2.1 m (Kramer and Smith 1962; Miller and Kramer 1971; Allan and Romero 1975; Heidinger 1975; Vogele and Rainwater 1975; Hunt et al . 2002). Largemouth bass males are solitary nesters. Average internest spacing ranged from 6.2 to 9.4 m in an Arkansas reservoir or about 15 nests/100 m transect (Hunt and Annett 2002), but other studies reported much lower densities of <1 to 3.0 nests/100 m of shoreline (Vogele and Rainwater 1975). Courting males may leave the nest for extended periods and approach a nearby female, using gentle nudges to her opercular area to direct her toward the nest (Cooke et al . 2001b). Males may also seem to lose buoyancy, float upward, and turn on their side to flash their lighter ventral side toward nearby females, which also appears to attract the female to the nest (Allan and Romero 1975). While courting the female or guarding embryos or fry in the nest, parental males engage in a number of vigilant and aggressive behaviors (e.g., hovering, pivoting, nest circling, opercle flaring, chasing, biting, parallel swims) (Allan and Romero 1975; Hunt 1995). Once the female is led to the nest, the male uses nips and nudges near her vent and opercle to encourage egg deposition (Cooke et al . 2001b). The pair ultimately assumes the head-to-head, broadside orientation of most centrarchids for spawning (Reighard 1906; Allan and Romero 1975). Spawning activity can be intense, involving up to 123 shudders per hour, and a complete spawning sequence with a single female including pauses between spawning bouts can last for over 3.5 hours (Cooke et al . 2001b). After the female departs the nest, the male immediately begins vigilance behaviors (e.g., pivoting) and gentle fanning of the eggs. Although males may occasionally mate with more than one female (Reighard 1906), most mating is monogamous. In a North Carolina population subjected to genetic parentage analysis, eggs in 23 of 26 nests were exclusively or almost exclusively composed of full-sib progeny, the products of one male and one female; the other three nests were indicative of serial monogamy (one male with two or three females; DeWoody et al . 2000b). In tagged individuals in experimental ponds, six of seven male largemouth bass spawned with one female and only one male spawned with two females (Cooke et al . 2001b). Ovaries begin development for the next spawning season in the fall and continue developing over winter (Olmsted 1974; Brown and Murphy 2004, Florida bass × largemouth bass hybrids). Mature ovarian eggs are 0.75 to 1.56 mm diameter, and the yellow to orange, fertilized, water-hardened eggs average 1.60 to 2.09 mm diameter, increasing in diameter with female size (Kelley 1962; Meyer 1970; Merriner 1971a; Cooke et al . 2006). Fecundity increases with female size, and ovaries apparently contain one distinct mode of mature ova, suggesting that females release a single batch of eggs (Kelley 1962; Olmsted 1974). The relationship between potential batch fecundity (Y) and total length (X) is described by the power function, Y = 0.00003X3.4067 (n = 36, R2 = 0.70, data from Kelley 1962 and Olmsted 1974). At 388 mm TL, a female can potentially produce 19,792 mature eggs in a single batch (range: 4550 eggs at 252 mm TL to 54,732 eggs at 523 TL). The adhesive, fertilized eggs hatch in about 3 to 4 days at 18 to 21◦ C (Kramer and Smith 1960a; Laurence 1969; Allan and Romero 1975). Newly hatched larvae are 3.6 to 4.1 mm TL (Cooke et al . 2006) and at 19◦ C average 6.2 mm TL (range, 5.9–6.3 mm TL) at the swim-up stage 6.75 days after hatching (Kramer and Smith 1960a; Meyer 1970; Goodgame and Miranda 1993). Male largemouth bass invest 20 to 39 days in parental care from spawning to fry dispersal (Kramer and Smith 1962; Cooke et al . 2006). Male defensive behaviors and hence activity and energy expenditures increase through the embryo to swim-up stages (Hunt 1995; Cooke et al . 2006). Largemouth bass fry begin leaving the nest about 8 to 11 days after spawning by forming initially tight schools or fry balls that begin to forage away from the nest area. The male bass guards the fry balls by constantly patrolling the areas around the moving fry ball. With growth of the fry, the brood association becomes looser and two or more broods may join, further increasing the peripheral area the male must patrol. The fry remain in swarms until they reach about 28 to 33 mm TL (Kramer and Smith 1962; Allan and Romero 1975; Elliott 1976; Colgan and Brown 1988; Annett et al . 1996). Relative to similar-age rock bass fry, largemouth bass fry display reduced predator avoidance responses during their first 3 weeks of free swimming, responses related directly to the extended period of protection provided to the fry by male largemouth bass. About 45 to 50 days after swim-up and after the guarding male parent has left, largemouth bass fry develop agonistic behaviors toward conspecifics, coincidental with the breakup of the large swarms of fry into solitary individuals or pairs (Brown 1984). Juvenile largemouth bass show evidence of natal fidelity. Tagged age-0 largemouth bass in a reservoir remained within a 250-m home range during their first year of life, and 79 to 90% of recaptures were within 58 m of release sites. Of a small number of recaptured yearlings (second summer of life), 56% were still within 58 m of the release site of the previous year (Copeland and Noble 1994; Jackson et al . 2002).

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Biparental care is documented in a largemouth bass population in a North Carolina stream. Most of 26 nests examined were attended by a female and a guardian male (DeWoody et al . 2000b). The attendant female generally faced the nest from 1 to 2 m distance with the attendant male over the nest, but these positions were occasionally reversed. The guardian male showed no aggression toward the female, and the attendant female actively chased away conspecific nest intruders and predators. Nests with attendant females occurred across several stages of brood development, indicating that female nest guarding extended well past spawning and incubation of eggs to the free-swimming fry stage of the brood. A few nests that lacked parental males were guarded solely by females. Biparental care in largemouth bass (or other Micropterus) populations is not a general occurrence across populations (Cooke et al . 2006), but observation of two individual Florida bass guarding a single nest for 3 days (Carr 1942) and other anecdotal accounts (Miller 1975) suggest that some as yet undocumented degree of biparental care may exist in other populations of largemouth bass or other species of Micropterus. The existence of biparental care in the largemouth bass is consistent with several reproductive life history traits (i.e. large body size, large eggs, sexual monomorphism, monogamy, extended parental care; DeWoody et al . 2000b). Nest associates: Golden shiner, N. crysoleucas (Kramer and Smith 1960b). Freshwater mussel host: Confirmed host to A. ligamentina, A. neislerii, A. plicata, A. suborbiculata, A. ferussacianus, E. complanata, E. fisheriana, L. altilis, L. cardium, L. higginsii, Lampsilis ornata, L. perovalis, L. rafinesqueana, L. siliquoidea, L. subangulata, L. complanata, L. recta, L. subrostrata, M. nervosa, P. grandis, S. undulatus, S. subvexus, V. iris (reported as V. nebulosa), V. nebulosa, and V. vibex (Lefevre and Curtis 1910, 1912; Young 1911; Howard 1914, 1922; Reuling 1919; Coker et al . 1921; Howard and Anson 1922; Arey 1923, 1932; Penn 1939; Neves et al . 1985; Waller et al . 1985; Waller and Holland-Bartels 1988; Barnhart and Roberts 1997; Haag and Warren 1997; Hove et al . 1997; Haag et al . 1999; O’Brien and Brim Box 1999; Watters and O’Dee 1999; Khym and Layzer 2000; O’Dee and Watters 2000; O’Brien and Williams 2002; Van Snik Gray et al . 2002; Haag and Warren 2003). Putative host to L. abrupta (unpublished sources in OSUDM 2006). Conservation status: Although secure within most of its native range and widely established outside its native range, the largemouth bass is not without major conservation concerns. The genetic integrity of the species in the southern United States is threatened by the widespread and decades-long practice of stocking nonnative Florida bass (or Florida-largemouth hybrids) on top of existing native largemouth bass populations (Philipp et al . 2002). Where introduced, Florida bass often rapidly and substantially introgress with native largemouth bass populations, eventually producing hybrid populations with high potential for loss in reproductive fitness and loss in adaptation to local conditions (Philipp et al . 1985a, 2002; Fields et al . 1987; Cooke et al . 2001a; Kassler et al . 2002; see account on Micropterus floridanus). Even largemouth bass populations in relatively close geographic proximity can differ significantly with respect to growth, survival, reproductive fitness, or physiological responses to the environment, reflecting the adaptation of the stock to the region in which it evolved (Philipp and Claussen 1995; Cooke et al . 2001a; Cooke and Philipp 2005, 2006). At least some native populations of largemouth bass in Mexico and perhaps southwest Texas likely represent distinct taxa that could be threatened by further introductions of nonnative largemouth bass or congeners (Edwards 1980; Miller 2005; Lutz-Carillo et al . 2006). Two tasks appear primary to the conservation of the genetic integrity of native largemouth bass (Philipp et al . 2002): identification of the number and geographic distribution of genetic stocks across the native range of the species and the reconstruction of native stocks now lost or contaminated by past (and present) stocking of nonnative Florida bass, intergrades, or even nonlocal stocks of largemouth bass. Similar species: All other species of Micropterus, except the Florida bass, have more confluent dorsal fins, upper jaws that reach to or barely past the eye, and unbranched pyloric caeca (Page and Burr 1991; see account on Florida bass). Systematic notes: Micropterus salmoides forms a sister pair with M. floridanus (Near et al . 2004, 2005; see account on M. floridanus). At least some native populations of Micropterus, currently under the name M. salmoides, in the Rio Grande system, appear to represent distinct, but formally unrecognized taxa (Bailey and Hubbs 1949; Edwards 1980; Miller 2005). Importance to humans: The largemouth bass is the most popular and economically significant freshwater sport fish in North America, perhaps rivaled only by the rainbow trout in its local, regional, and ultimately national economic and social impact. Over its broad native and introduced range in North America, the largemouth bass was the primary impetus over the last 30 years for the founding of hundreds of bass-focused fishing clubs and national angler associations

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and federations, all of which effectively lobby local, state, and federal agencies and governments and influence fisheries management and conservation (Dean 1996; Shupp 2002; Chen et al . 2003; Schramm and Hunt 2007). Broad ecological and habitat tolerances, explosive and aggressive attacks on just about any moving natural or artificial bait, a relatively large size, and excellent table qualities combine as winning characteristics among anglers. Anglers successfully take largemouth bass day or night, across seasons, and in almost every conceivable type of water condition (e.g., Heidinger 1975; Becker 1983; Etnier and Starnes 1993). Largemouth bass anglers range from subsistence fishers in rural areas to a growing cadre of amateur and professional anglers following regional and national largemouth bass tournament trails to compete for hundreds to hundreds of thousands of dollars in cash and prizes (Ross 2001; Shupp 2002; Leonard 2005; Schramm and Hunt 2007). Bass tournaments are often sponsored by large media and corporate interests and broadcast nationally as sporting events. Tournament sponsors manufacture and distribute highly specialized bass fishing equipment (e.g., bass powerboats), bass fishing television shows, “how-to” bass fishing videos, and print media, all of which renders largemouth bass fishing both a spectator and a participatory sport (Ridgway and Philipp 2002). For decades, the largemouth bass in combination with the bluegill has formed the core predator–prey combination used in management of warmwater ponds and small public and private warmwater impoundments (Bennett 1948; Swingle 1949). Historically, the species supported commercial fisheries in the Great Lakes, Ohio, and Illinois (Mills et al . 1966; Trautman 1981; Scott and Crossman 1973). For example, before 1900, thousands of barrels of largemouth bass were taken commercially from impoundments in Ohio, and in 1897, an estimated 13,000 pounds of largemouth bass were taken commercially from lakes along the Illinois River.

13.9.8 Micropterus treculi (Vaillant and Bocourt) 13.9.8.1 Guadalupe bass Characteristics: See generic account for general characteristics. Elongate, slightly compressed body depth 0.20 to 0.25 of TL. Mouth large, terminal, lower jaw slightly projecting, upper jaw extends to rear half of eye (in adults). Outline of spinous dorsal fin curved. Juncture of soft and spiny dorsal fins slightly emarginate, broadly connected. Shortest dorsal spine at emargination of fin, 0.5 to 0.6 times length of longest spine. Dorsal soft rays, usually 12, 11 to 13; anal soft rays, usually 10, 9 to 11. Gill rakers, 8. Lateral scales, (55)61 to 69; rows above lateral line (7)8 to 9(10); rows below lateral line, (14)15 to 18(20); cheek scale rows, (10)12 to 14(18); caudal peduncle scale rows, (23)26 to 27(29); pectoral rays, (14)15 to 16. Small scales on interradial membranes at anal and second dorsal fin bases (>60 mm SL). Pyloric caeca, single, usually 10 to 11, (8–13). Tooth patch present on glossohyal (tongue) bone (Hubbs 1927; Hubbs and Bailey 1942; Edwards 1980; Kassler et al . 2002). Size and age: Age 0+ fish average from 82 to 103 mm TL at age 1 (Edwards 1980). Large individuals weigh 500 to 1000 g and attain 250 to 330 mm TL; few live beyond age 3+ (maximum about 400 mm TL, age 6+) (Boyer et al . 1977; Edwards 1980; Page and Burr 1991; Koppelman and Garrett 2002). World angling record, 1.67 kg, Texas (IGFA 2006). The oldest individuals in a population are generally females (Edwards 1980). Coloration: Similar to spotted bass but has 10 to 12 dark vertical blotches along side (diamond shaped posteriorly and darkest in young), usually 16 pectoral rays, and 26 to 27 caudal peduncle scale rows (Edwards 1980; Page and Burr 1991). Native range: The Guadalupe bass is native to the Edwards Plateau in the Brazos, Colorado, Guadalupe, and San Antonio river drainages, Texas (MacCrimmon and Robbins 1975; Page and Burr 1991; Koppelman and Garrett 2002). Established populations in the Nueces River, Texas, were introduced deliberately in 1973 (Koppelman and Garrett 2002). Habitat: The Guadalupe bass inhabits gravel riffles, runs, and flowing pools of clear creeks and small to medium rivers (Edwards 1980; Page and Burr 1991). The species is most common in flowing waters of streams (6–22 m wide) in association with large rocks, cypress roots, stumps, or other cover. Individuals overwinter in deep pools with currents, move in spring to shallow, but flowing, backwaters to spawn, and then to deep runs and flowing pools. The species avoids the constant thermal environments of headsprings, extremely silted streams, and the smallest headwater streams. Survival is poor in hypolimnetic-release tailwaters and most reservoirs, except in variable-level reservoirs that provide flowing conditions for at least part of the year (Edwards 1980).

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Food: The Guadalupe bass is an opportunistic top carnivore (Edwards 1980). The adult (>90 mm SL) diet is dominated by small fishes, mostly minnows (e.g., Notropis, Cyprinella, Campostoma) and other centrarchids, but also includes large numbers of mayfly, dragonfly, dipteran, hemipteran, and megalopteran larvae, a few bees and wasps, and an occasional amphibian. Large adults (>150 mm SL) consume relatively large volumes of crayfish. Fish prey associated with flowing water (e.g., blacktail shiner, darters, channel catfish) are taken most often, an indication of the primary foraging habitat of Guadalupe bass. By volume, the diet of young bass (15–30 mm SL) is dominated by mayfly, odonate, and hemipteran larvae. In bass between 30 and 90 mm SL, increasing volumes of fish are consumed, but invertebrates remain important components of the diet of bass <135 mm SL (Edwards 1980). Dietary comparisons between sympatric populations of Guadalupe bass and largemouth bass indicated decreasing similarity with growth in the numbers and volumes of diet items shared. Where spotted and largemouth basses occurred in sympatry with Guadalupe bass, Guadalupe bass diets were most similar among seasons to those of the spotted bass (Edwards 1980). Reproduction: Maturity is reached minimally in males at 97 mm TL and age 1+ and in females at 128 mm SL and age 2+ (Hurst et al . 1975; Edwards 1980); reported maturation of a female at 70 mm SL (Hurst et al . 1975) is perhaps feasible but needs further confirmation (Edwards 1980). With the possible exception of the redeye bass, Guadalupe bass apparently mature at smaller sizes than any other Micropterus. Spawning initiation and duration are not well documented, but various observations suggest a mid-March to June spawning period. Male and female gonadosomatic ratios peak in spring, but some individuals taken in summer continue to have elevated ratios. In mid-March, a male was observed guarding a nest and eggs (water temperature 14–17◦ C), and many large males and females emit freely flowing sex products at that time. Young <30 mm SL are taken from May through August, and recently spent females are observed as late as July (et al . Hurst et al . 1975; Boyer et al . 1977; Edwards 1980). Nesting areas are apart from, but always near, a source of slow to moderately flowing water (i.e. backwaters with water inflow) (Edwards 1980). A single observed depressional nest was oval shaped (41 × 50 cm, 10 cm in depth), placed 1 m from shore on a sloping bank at a water depth of 69 cm and current speed of about 0.3 m/s. The nest was swept into the hard black soil of the creek bank and lined with 5 cm diameter limestone rubble that was covered partially by sticks and leaves. The nest was guarded by a relatively large (280 mm TL) male, and a second individual, suspected to be a female, was also observed near the nest. The nest contained 1406 adhesive eggs, most of which were adhered to the sticks and leaves (Boyer et al . 1977). Apparently, nothing else is published on nest building, courtship, spawning, or parental care behaviors. Mature ovarian eggs average from 1.50 to 2.25 mm in diameter, and fertilized water-hardened eggs average 2.1 mm in diameter (Boyer et al . 1977; Edwards 1980). Fecundity increases with female size. The relationship between potential batch fecundity (Y) and standard length (X) is described by the linear function, Y = 29.98X − 3072.20 (Guadalupe River; Y = 34.28X − 4144.08, Llano River; Y = 57.85X − 5920.62, LBJ reservoir, equations from Edwards 1980). At 203 mm SL, a female can potentially produce 3013 mature eggs in a single batch (range: 765 eggs at 128 mm SL to 5262 eggs at 278 mm SL, respectively). With growth, young Guadalupe bass occupy increasingly faster and deeper water during their first summer, shifting to deeper-flowing pools to overwinter (Edwards 1980). Nest associates: None known. Freshwater mussel host: None known. Conservation status: The Guadalupe bass is vulnerable throughout its native range (Warren et al . 2000; NatureServe 2006). The species has declined dramatically in recent history because of decreased stream flow, reservoir construction, habitat degradation, and extensive, introgressive hybridization with nonnative smallmouth bass (Edwards 1980; Whitmore and Butler 1982; Whitmore 1983; Morizot et al . 1991; Koppelman and Garrett 2002). Genetic contamination of the Guadalupe bass from hybridization with nonnative smallmouth bass is pervasive throughout its range, and only five natural populations remain free from introgressive hybridization (Koppelman and Garrett 2002). Genetically uncontaminated Guadalupe bass are being stocked in an attempt to numerically and reproductively overwhelm the hybrid swarms (Koppelman and Garrett 2002). Similar species: See account on spotted bass and the section on coloration. Systematic notes: Micropterus treculi is a member of a “Gulf of Mexico” clade of Micropterus, including all other Micropterus except M. dolomieu and M. punctulatus (Near et al . 2003, 2004). Although relationships within the clade are

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not well resolved, phylogenetic analyses usually recover M. treculi as sister to M. salmoides+M. floridanus (Kassler et al . 2002; Near et al . 2003, 2004, 2005). On the basis of morphology, taxonomists usually related M. treculi to M. punctulatus (e.g., Hubbs and Bailey 1942; Hubbs 1954; Ramsey 1975). Importance to humans: The Guadalupe bass is designated the State Fish of Texas in recognition of the unique character of both the species and its habitat. Although small relative to congeners, the species is the focus of a popular sport fishery on the Edwards Plateau. The species provides good sport using ultralight gear with spinners and other small bass lures that are fished in riffle areas, flowing pools, or deep eddies below riffles (Boyer et al . 1977). The fishery provides the angler with an agile fast water fish occurring in attractive, natural stream settings (Koppelman and Garrett 2002).

13.10 Pomoxis Rafinesque The genus Pomoxis, consisting of the sister pair Pomoxis annularis and Pomoxis nigromaculatus, is sister to a clade inclusive of the genera Archoplites and Ambloplites (Near et al . 2004, 2005). The natural range of the genus, collectively called the crappies, encompasses North America east of the Rocky Mountains from southern Canada to the Gulf of Mexico, excluding the Atlantic Slope from southern Virginia northward (Page and Burr 1991). A fossil species, Pomoxis †lanei Hibbard, is known from Miocene deposits in Kansas and Nebraska with the oldest formations being the Rhino Hill Quarry and is dated at 6.6 mya (million years ago) (Uyeno and Miller 1963; Schultz et al . 1982; Cross et al . 1986). Another undescribed fossil species presumably representing Pomoxis was reported from material collected at the Wakeeney local fauna (Ogallala Formation) in Kansas dating to about 12 mya (Wilson 1968; Tedford et al . 1987). The white crappie and black crappie show wide overlap in distribution across their large ranges and frequently cooccur in the same water body. Nuclear-encoded allozyme data indicate that some sympatric populations of white crappies and black crappies in reservoirs introgress through hybridization, although other sympatric populations do not (Maceina and Greenbaum 1988; Hooe and Buck 1991; Dunham et al . 1994; Epifanio and Philipp 1994; Smith et al . 1994, 1995; Travnichek et al . 1996). Estimates of the degree of hybridization among reservoirs is variable (e.g., none to >40% of individuals,), but second-generation (or higher) hybrids are usually less common than first-generation hybrids and contribute little to recruitment (Smith et al . 1994; Dunham et al . 1994; Travnichek et al . 1996). Within-reservoir differences in species abundances and habitats or among-reservoir differences in physicochemical characteristics are not related in any obvious way to the degree of hybridization. Some speculate that hybridization may be related to contact between the species in artificial environments where habitats or physical conditions limit species recognition or species segregation during spawning, particularly in geographical areas at the historical border of the range of the white crappie (Travnichek et al . 1996, 1997; Epifanio et al . 1999). A hallmark of the genus Pomoxis is the capacity of both species to maintain high recruitment and rapid growth to harvestable sizes under high mortality or fishery exploitation rates. Sustainable sport fishery exploitation rates of crappies as high as 40 to 60% per year are observed in many impoundments (Colvin 1991; Larson et al . 1991), but because of their capability to proliferate, crappies are prone to overpopulation and stunting, especially in small or resource-limited reservoirs (Hooe and Buck 1991; Hooe et al . 1994). Crappies were exploited commercially in natural lakes from Florida to Canada well into the twentieth century (e.g., Schoffman 1940, 1960, 1965; Huish 1954; Scott and Crossman 1973; Trautman 1981; Schramm et al . 1985). From 1938 to 1955, crappies were liberally harvested in a commercial fishery in Reelfoot Lake, Tennessee, and supported a thriving sport fishery. Soon after cessation of commercial fishing the population was reportedly overrun by smaller crappies (Schoffman 1960, 1965). As recently as 1976 to 1981, the black crappie was commercially fished in Lake Okeechobee, Florida. Commercial fishers and anglers removed about 3.8 million kg of the species (about 833,000 kg/yr; 65% of annual average standing crop) from the lake until the fishery collapsed in 1981 because of highly variable recruitment (Schramm et al . 1985; Miller et al . 1990). From a management perspective, and in spite of the ability to proliferate, a perplexing characteristic of the genus is the near unpredictability of survival of fishes beyond their first year of life. Annual recruitment of both crappie species is notoriously erratic, often quasi-cyclical, and highly variable from year to year within a given population. Variability in postspawning larval abundance and subsequent recruitment of both crappie species can often be related to complex interactions among population dynamics and lake conditions or reservoir operations. These often involve combinations of factors such as larval densities, hatch times, harvest rates, water body productivity, prespawning water temperatures,

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water retention time, water elevation, or dam discharge rates that may predict crappie recruitment in some, but not other waters (e.g., Beam 1983; McDonough and Buchanan 1991; Mitzner 1991; Allen and Miranda 1998, 2001; Maceina and Stimpert 1998; Sammons and Bettoli 1998; Miranda and Allen 2000; Pine and Allen 2001; Sammons et al . 2001, 2002; Dubuc and DeVries 2002; Maceina 2003; St. John and Black 2004; Dockendorf and Allen 2005; Bunnell et al . 2006). The black crappie and white crappie support a popular sport fishery and on a kilogram per hectare basis are the most harvested fish in reservoirs of the United States (Miranda 1999). Of all freshwater anglers (exclusive of the Great Lakes) in the United States, an estimated 24% (6.7 million) of anglers spent 21% (95 million days) of fishing days seeking crappies (USFWS 2002). These percentages compare favorably with popularity of sport fisheries for catfish, panfish, and trout. On some southern US reservoirs much if not most (>30%) of the angling effort is directed at crappies (e.g., Larson et al . 1991; Reed and Davies 1991; St. John and Black 2004). A growing contingency of crappie anglers are considered “specialists,” similar to many black bass anglers, because they fish year round for crappies to the near exclusion of other species. The relatively recent advent of crappie clubs and fishing tournaments, dubbed crappiethons, are further evidence of the continued and growing popularity of sport fishing for these centrarchids (Larson et al . 1991; Allen and Miranda 1996). Generic characteristics: Deep, extremely compressed body, depth about 0.33 to 0.48 of SL. Long to very long predorsal region with sharp dip over eye in dorsal profile. Dorsal fin base equal to or shorter than distance from center of eye to dorsal fin origin. Head small. Eye large, diameter equal to or slightly greater than snout length. No black teardrop; no black spot in soft dorsal fin. Dorsoposterior margin of opercle shallowly emarginate. Preopercle posterior margin serrate. Long dorsal fin, 6 to 8 spines, 13 to 18 rays, 20 to 24 total; and long anal fin, 5 to 8 spines, 14 to 18 rays, 23 to 24 total. Spiny and soft dorsal and anal fins continuous, smoothly rounded, similar in length, and nearly symmetrical. Emarginate to shallowly forked caudal fin. Rounded pectoral fin. Long, slender gill rakers, 25 to 32. Ctenoid scales. Lateral line complete. Lateral line scales, 34 to 50; cheek scale rows, 5 to 6; branchiostegal rays, 7. Teeth on entopterygoid and glossohyal (tongue, two patches) bones (Bailey 1938; Keast 1968a; Trautman 1981; Becker 1983; Smith 1985; Page and Burr 1991; Etnier and Starnes 1993; Mabee 1993; Jenkins and Burkhead 1994; Smith et al . 1995). Similar species: See account on flier.

13.10.1 Pomoxis annularis Rafinesque 13.10.1.1 White crappie Characteristics: See generic account for general characteristics. Deep, extremely compressed body, depth usually 0.33 to 0.48 of SL. Very long predorsal region with sharp dip over eye in dorsal profile. Dorsal fin base shorter than distance from center of eye to dorsal fin origin. Large, supraterminal, oblique mouth, lower jaw projecting, supramaxilla moderate (≤2 times length of maxilla), upper jaw reaching to or slightly beyond middle of eye. Opercular spot black. Long dorsal fin, (4)5 to 6(8) spines, (12)14 to 15(16) rays; and long anal fin, 6 to 7(8) spines, 16 to 19 rays. Pectoral rays, (14)15(16); vertebrae, 30 to 32(14+18) (Bailey 1938; Trautman 1981; Becker 1983; Page and Burr 1991; Etnier and Starnes 1993; Mabee 1993; Jenkins and Burkhead 1994; Smith et al . 1995). Size and age: Typically reach 131 to 173 mm TL at age 1, but first-year growth is highly variable across latitudes and among habitats (range, 58–310 mm TL, Siefert 1969a; Carlander 1977). Large individuals measure 350 to 400 mm TL, weigh 500 to 800 g, and reach age 6+ to 8+ (maximum 530 mm TL, age 9+) (Carlander 1977; Page and Burr 1991; Etnier and Starnes 1993). World angling record, 2.35 kg, Mississippi (IGFA 2006). Coloration: Gray-green above with silvery blue sides and upper back vaguely barred with about 6 to 10 chainlike double vertical bands (widest at top) as well as dark blotches and green flecks. Chainlike bars and mottling often faint in individuals from turbid water. Whitish to silvery below. Dorsal, anal, and caudal fins with many wavy dark bands and spots. Males become darker during the breeding season (Page and Burr 1991; Etnier and Starnes 1993). Native range: The white crappie is native to the Great Lakes, Hudson Bay (Red River), and Mississippi River basins from New York and southern Ontario west to Minnesota and South Dakota and south to the Gulf of Mexico and in Gulf drainages from Mobile Bay, Georgia and Alabama, west to the Nueces River, Texas (Page and Burr 1991). The species has been introduced and is established over most of the coterminous United States (Fuller et al . 1999).

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Habitat: The white crappie inhabits sand- and mud-bottomed pools and backwaters of creeks and small to large rivers, lakes, ponds, and reservoirs (Page and Burr 1991). The greater adaptability of the white crappie to turbid waters than the black crappie is often noted. Higher relative abundance or success in turbid habitats suggests that the white crappie is more adapted to turbid conditions than the black crappie (e.g., Carlander 1977; Trautman 1981; Ellison 1984; Etnier and Starnes 1993; Miranda and Lucas 2004). Even though the difference in turbidity tolerance is frequently noted, both crappie species occur in turbid and clear water habitats, and an obvious mechanism or adaptation explaining the apparent difference in tolerance is lacking (e.g., Barefield and Ziebell 1986). Some indirect evidence (e.g., growth, survival) suggests that white crappies can feed more efficiently in turbid waters than black crappies or that white crappies compete poorly in clear waters with other centrarchids (e.g., Carlander 1977; Ellison 1984; Pope 1996). White crappies move extensively, often show distinct diel activity patterns, and can show persistent occupation of home activity areas in the summer. In rivers in Missouri, tagged individuals covered 34 to 42 km in 21 to 91 days (Funk 1957) and others have noted movements up to 30 km (review in Hansen 1951; Siefert 1969a). Increased movement in spring and early summer is attributed to aggregation in spawning areas and postspawning foraging (Guy et al . 1994). Adult white crappies show high levels of nocturnal activity (see section on food), but overall patterns of movement and activity vary seasonally and daily among seasons (e.g., Hansen 1951; Morgan 1954; Greene and Murphy 1974; Markham et al . 1991; Guy et al . 1994). In an Ohio reservoir, diel movement of large white crappie (271–352 mm TL) in summer rapidly increased at dusk when light intensity was zero, peaked at night (average 47 m/h), and declined at dawn. Movement was low throughout the day (average 17 m/h). During the day, the species was associated with steeply sloped bottoms and the presence of structure (e.g., tree stumps, logs, rocks). Individuals tended to occupy deeper water during the day than at night (e.g., 5.4 vs 4.3 m, respectively), generally staying within 0.5 m of the bottom. Median summer home activity areas were 0.49 to 0.63 ha during the day and 1.25 ha at night (Markham et al . 1991). In a shallow, homogeneous glacial lake in South Dakota, movement patterns of large radio-tagged white crappie tracked from April to September were more extensive and less patterned. Over the tracking period, median movement was 73.2 m/h (range: 0–1,523 m/h) and was highest in May (102.1 m/h) and July (82.4 m/h). Diel movement patterns were indistinct or variable, but tended to peak at dawn and dusk. Median home activity area was large relative to the reservoir study (15.8 ha) and varied considerably (range: 0.1–85.0 ha) (Guy et al . 1994). The larger home range, relative to the other study, was attributed to greater foraging demands or the lack of cover and bottom structure in the homogeneous habitat of the lake. Cover or structure tends to hold individuals within a limited area for prolonged periods (Markham et al . 1991; Guy et al . 1994). Food: The white crappie is primarily a midwater, particulate-feeding zooplanktivore and invertivore that shifts to piscivory at a relatively large size (∼ 160 mm TL) compared to other piscivorous centrarchids (O’Brien et al . 1984). Numerous, long gill rakers likely play an important functional role in the extended period of zooplanktivory (Wright et al . 1983). Food of large individuals (>160 mm TL) consists primarily of small fishes (e.g., clupeids, other white crappies and sunfishes, minnows, silversides), zooplankton, immature aquatic insects (e.g., chironomid larvae and pupae, burrowing mayflies), and amphipods (e.g., Hansen 1951; Morgan 1954; Hoopes 1960; Whiteside 1964; Siefert 1969a; Mathur 1972; Greene and Murphy 1974; Ellison 1984; Muoneke et al . 1992). Large white crappies are among the best documented of any centrarchid for their nocturnal feeding and high levels of nocturnal activity (see section on habitat). Large individuals feed at dusk, sporadically throughout the night, and intensively at dawn, feeding very little or not at all during the day (Childers and Shoemaker 1953; Greene and Murphy 1974). In lentic waters, intermediate-size fish (80–150 mm TL) are pelagic zooplanktivores that begin feeding at or near dawn and continue feeding throughout the day (O’Brien et al . 1984; Wright and O’Brien 1984). These pelagic-dwelling individuals can make diel vertical migrations to exploit vertically migrating zooplankton and dipteran larvae and pupae and to respond to changing levels of temperature, light, and DO (O’Brien et al . 1984). Empirical associations of white crappie abundance and abundance of other fishes in wild populations and mesocosm experiments indicate that 130 to 199 mm TL white crappie are highly effective predators that rapidly find and eat larval fishes (e.g., bluegills, walleye). Predation by white crappies is so effective it could drastically limit recruitment of the prey fish species (Kim and DeVries 2001; Quist et al . 2003). Young-of-the-year white crappies feed most heavily during daylight hours on crustacean zooplankton (e.g., copepods and cladocerans) and small dipteran larvae and pupae, but some feeding occurs continuously over a 24-hour period (Siefert 1968, 1969a; Mathur and Robbins 1971; Overmann et al . 1980; DeVries et al . 1998). Individuals can actively search for, pursue, and capture zooplankton prey down to water temperatures of at least 7◦ C (O’Brien et al . 1986).

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The white crappie is adapted behaviorally and visually for detecting zooplankton prey, but foraging success is affected by prey size, prey movement, light intensity, and turbidity. White crappies use a stereotyped saltatory (pause-travel) search strategy in which they visually locate and attack individual prey. In this strategy, they search briefly for a prey item while stationary and, if they do not locate prey, swim a short distance before stopping to scan again (O’Brien 1979; O’Brien et al . 1986, 1989; Browman and O’Brien 1992). The white crappie retina has a high density of cones in the far temporal region along the eye’s horizontal meridian, an apparent adaptation for detecting open-water zooplankton. Highest probabilities and maximum distances that white crappie will pursue small zooplankters (1–2 mm) are concentrated in a 60-degree forward-directed pie-shaped wedge of limited height (Browman et al . 1990) in which the species is better able to discriminate the absolute size of prey (O’Brien et al . 1985). The wedge-shaped field of maximum foraging corresponds well with the position of the high-density photoreceptor region on the retina (Browman et al . 1990). Under well-lit, lowturbidity conditions (80 lux, 1 NTU), the distance at which individuals (∼ 160 mm TL) can detect prey (reactive distance) increases from about 4 to 30 cm as prey size increases from 1 to 3 mm, and reactive distance for moving prey increases about threefold. For 3-mm prey, white crappie reactive distance is little affected by decreases in illumination from 106 to 10 lux, but from 10 lux to 0.97 lux, reactive distance decreases from about 25 to 6 cm. Differences in reactive distance across prey sizes (1–3 mm) at the lowest light intensities are minimal. Reactive distance to a 2.4-mm prey at 80 lux decreases as an approximate log function of turbidity from about 20 cm at 1 NTU to 5 cm at 33 NTU (Wright and O’Brien 1984). Reproduction: Maturity is usually reached at age 2+ to age 3+ and a minimum size of about 140–180 mm TL, although stunted individuals in dense populations reportedly spawn at 110 mm TL (Morgan 1951a, 1954; Whiteside 1964; Hansen 1951; Siefert 1969a; Trautman 1981). The white crappie is among the earliest, lowest-temperature spawners in the family. The testes and ovaries enlarge and continue developing in the fall and over winter (Morgan 1951b; Whiteside 1964), which is likely an adaptation for early spawning. Spawning occurs at water temperatures of 11 to 27◦ C with most spawning taking place at 16 to 20◦ C. The duration of the spawning period is variable, lasting from 17 to 53 days, and depending on latitude, spawning activity occurs from late March to June or mid-July (Hansen 1951; Morgan 1954; Whiteside 1964; Siefert 1969a; Carlander 1977; McDonough and Buchanan 1991; Pope and DeVries 1994; Travnichek et al . 1996; Sammons et al . 2001). Year-to-year fidelity to nesting areas is not apparent (Hansen 1965). Male white crappies have less fastidious nest-building habits than some centrarchids. Males establish individual territories but apparently do not use caudal sweeping to clear the nesting area. The male remains upright with the abdomen touching or nearly touching the substrate and uses vigorous 3- to 5-second bursts of fin and body movements to sweep out a roughly circular area (about 15–30 cm diameter), actions which remove only the loosest bottom material. Nest-clearing stops before the well-defined depression typical of most centrarchids is created (Hansen 1965; Siefert 1968). Interestingly and atypical among centrarchids, the female often engages in similar nest cleaning behaviors just before spawning and after egg deposition. Substrate at the nest site appears less important to the male than being near some protective cover or bottom vegetation (Siefert 1968). Nests are located on sod clumps, clay, gravel, rock piles, hollows made among aquatic plants, filamentous algae, or roots as well as the surfaces of boulders, rootwads, and submerged brush or trees (Hansen 1943, 1951, 1965; Breder and Rosen 1966). Nests are placed at water depths of 0.1 to 1.5 m (anecdotally up to 6 m, Hansen 1965). Nest spacings suggest colonies (35–50 nests/colony, 46–76 cm apart), and solitary nests are rare (3 of 150), but nests along shorelines (3–15 nests) are in linear arrangements up to 1.2 m apart (Hansen 1965). Nest-guarding males repeatedly repulse approaching females until the female finally stops retreating from the male’s territory when chased, and the male accepts the female (Siefert 1968). The female circles the nest alone but ultimately moves over the bottom of the nest in a head-to-head, broadside position with the male. As both quiver and move forward with vents touching, she slides under the male, causing the pair to move in a curve as gametes are released. Each quivering act lasts about 4 seconds with intervals of 30 seconds to 20 minutes, at which time females often leave the nest. Spawning with a single female can continue from 45 minutes to 2.5 hours (Siefert 1968). In spawning pens, one female spawned in the nest of two different males, and on two occasions an intruding male joined a spawning female and guardian male to steal fertilizations (Siefert 1968). Eggs in two distinct stages of development in two nests suggested that multiple spawnings occurred over a 2-day period (Siefert 1968). Male white crappie remain relatively motionless over the nest and apparently do not engage in rim circling, but do display (opercle flare) to neighboring males or rush and attack (butt, snap, bite) territorially intruding males and females (Hansen 1965; Siefert 1968). During incubation, the male fans the eggs with constant motion of the pectoral fins (Hansen 1943; Breder and Rosen 1966). Fertilized eggs, which are almost completely covered with minute debris, often occur in clumps of three or more and are attached to gravel, leaves, twigs,

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grass, algae, or plants in and well outside the periphery of and even above the nest (Hansen 1943, 1965; Siefert 1968). Mature ovarian eggs are small, ranging from 0.82 to 0.92 mm in diameter, and fertilized water-hardened eggs average 0.89 mm diameter (Hansen 1943; Morgan 1954; Whiteside 1964). Size-adjusted batch fecundities are higher than any other centrarchid except the black crappie (see accounts on Archoplites and Centrarchus), but female fecundity shows high interannual variation within populations and high variation among populations (Mathur et al . 1979; Dubuc and DeVries 2002; Bunnell et al . 2005). Some females retain ripe eggs throughout the spawning period (Morgan 1954; Whiteside 1964), and gonadosomatic values and larval densities may each show two or more temporally separate peaks (Dubuc and DeVries 2002), patterns which are suggestive of partial release of a single batch over a protracted period, production of two or more batches by a female, or asynchrony in maturation of females. Fecundity increases with female size. The relationship between number of mature eggs (Y) and TL (X) is described by the function log Y = −5.301 + 4.24 log X (formula from data in Morgan 1954, average of 20 length classes, 159–330 mm TL, for 50 females, R2 = 0.87, see also Mathur et al . 1979). At a mean size of 230 cm TL, a female potentially can produce 51,609 mature eggs in a single batch (range: 10,787 eggs at 159 cm TL to 238,506 eggs at 330 cm TL). Hatching occurs in 1.8 to 2.1 days at 18.3 to 19.4◦ C (3.9 days at 14.4◦ C, about 1 day at 22.8◦ C) (Morgan 1954; Siefert 1968). Hatchlings are of 1.22 to 2.74 mm TL, and swim-up larvae disperse on average at 4 days post hatch (range: 2.1 to 6.8 days) at a size of 4.1 to 4.6 mm TL (Morgan 1954; Siefert 1968, 1969b; Sweatman and Kohler 1991; Browman and O’Brien 1992). Male parental care from egg deposition to dispersal typically lasts for 6 days, but, on the basis of developmental information, could range from 4 days at 22 to 23◦ C to 11 days at 14 to 15◦ C (Siefert 1968). Larvae disperse from nesting areas to forage in open water (Siefert 1969a; Overmann et al . 1980). Nest associates: None known. Freshwater mussel host: Confirmed host to A. ligamentina, A. plicata, A. suborbiculata, E. complanata, L. cardium, L. siliquoidea, L. complanata, and L. recta (Young 1911; Lefevre and Curtis 1912; Howard 1914; Coker et al . 1921; Barnhart and Roberts 1997). Putative host to L. reeveiana (unpublished sources in OSUDM 2006). Conservation status: The white crappie is secure throughout its native range (Warren et al . 2000; NatureServe 2006). Similar species: The black crappie has a shorter predorsal region, usually 7 to 8 dorsal spines, and no dark bars on sides. These phenotypic characters are not entirely reliable in separating the two crappie species where both species and their hybrids co-occur (Dunham et al . 1994; Smith et al . 1995). Systematic notes: Pomoxis annularis forms a sister pair with P. nigromaculatus. The pair is basal to a clade comprised of the genera Archoplites and Ambloplites (Roe et al . 2002; Near et al . 2004, 2005). Comparative studies of variation across the range of P. annularis are lacking. Importance to humans: White crappies are a popular sport fish and like black crappies can maintain recruitment and growth that can sustain extremely high levels of exploitation as sport fisheries (e.g., 60% for age 3 and older fish, Colvin 1991). In southern reservoirs, many thousands of crappies are harvested by anglers in the weeks before spawning when fishes, loosely aggregated near cover, go on a feeding spree, perhaps in response to rising water temperatures or preparatory to spawning (Etnier and Starnes 1993; Allen and Miranda 1996; Miranda and Dorr 2000; Dorr et al . 2002). During this time, white crappies are taken easily by anglers using small jigs, streamers, or minnows fished near underwater structure, where fishes are often caught one after the other. Later in spring, white crappies appear most vulnerable to night fishing with minnows below lanterns (Etnier and Starnes 1993).

13.10.2 Pomoxis nigromaculatus (Lesueur) 13.10.2.1 Black crappie Characteristics: See generic account for general characteristics. Deep, extremely compressed body, depth usually 0.37 to 0.45 of SL. Long predorsal region with sharp dip over eye in dorsal profile. Dorsal fin base about equal to or greater than distance from posterior rim of eye to dorsal fin origin. Large, supraterminal, strongly oblique mouth, lower jaw projecting, supramaxilla moderate (≤2 times length of maxilla), upper jaw reaching to or slightly beyond middle of eye. Opercular spot black. Silvery sides profusely speckled and mottled. Long dorsal fin, usually (6)7 to 8(10) spines, 14 to 16 rays; and

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long anal fin, 6 to 7(8) spines, 16 to 19 rays. Pectoral rays, (13)14(15); vertebrae, 31 to 33(14 + 18 or 19) (Bailey 1938; Keast and Webb 1966; Trautman 1981; Becker 1983; Page and Burr 1991; Etnier and Starnes 1993; Mabee 1993; Jenkins and Burkhead 1994; Smith et al . 1995). Size and age: Typically reach 122 to 160 mm TL at age 1 but first-year growth is highly variable among habitats and apparently less so among latitudes (range, 48–301 mm TL, Carlander 1977). Large individuals measure 300 to 400 mm TL, weigh 400 to 500 g, and reach age 6+ to 8+ (maximum 560 mm TL, 2.72 kg, age 13+) (Carlander 1977; Page and Burr 1991; Etnier and Starnes 1993). World angling record, 2.05 kg, Nebraska and Virginia (IGFA 2006). Coloration: Gray-green above with upper back and silvery blue sides marked with wavy black lines, dark blotches, and green flecks. Silvery below. Dorsal, anal, and caudal fins with many wavy black bands and pale spots. Males become darker during the breeding season (Page and Burr 1991; Etnier and Starnes 1993; Jenkins and Burkhead 1994). The presence of a black predorsal stripe (colloquially known as the black-nose or black-stripe crappie) in some individuals is the expression of a dominant trait controlled by a single gene (Gomelsky et al . 2005). Native range: The native range presumably includes Atlantic Slope drainages from Virginia to Florida, Gulf Slope drainages west to Texas, and the St. Lawrence River-Great Lakes and Mississippi basins from Quebec to Manitoba and south to the Gulf of Mexico (Page and Burr 1991). The wide introduction and establishment of the black crappie renders accurate determination of the native range difficult (Page and Burr 1991; Fuller et al . 1999). As the introduced black crappie became abundant in some California waters, the only native centrarchid, the Sacramento perch, declined or disappeared (Moyle 2002). Historical shifts in distribution and relative abundance suggest that the black crappie has declined or has been replaced by the white crappie because of increased turbidity of waters (e.g., South Dakota, Carlander 1977; Illinois, Smith 1979; Ohio, Trautman 1981; Wisconsin, Becker 1983). In some reservoirs, the black crappie hybridizes extensively with the white crappie (see account on P. annularis). Habitat: The black crappie inhabits lakes, ponds, sloughs, and backwaters and pools of streams and rivers. The species is most common in lowland habitats, large reservoirs, and navigation pools of large rivers but is rare in upland rivers and streams. The black crappie is usually associated with clear waters, absence of noticeable current, and abundant cover (e.g., aquatic vegetation, submerged timber) (Carlander 1977; Werner et al . 1977; Conrow et al . 1990; Page and Burr 1991; McDonough and Buchanan 1991; Keast and Fox 1992; Etnier and Starnes 1993; Pflieger 1997). The species is apparently moderately tolerant of oligohaline conditions, occasionally entering tidal waters (usually <5.0-ppt salinity) to feed on small fish and shrimp (Rozas and Hackney 1984; Moyle 2002). In a whole-lake acidification experiment, black crappies nested from pH 5.6 to 4.7, but no larvae or post larvae were observed at pH 4.7 (Eaton et al . 1992; see also McCormick et al . 1989). Along a bog lake successional gradient in Wisconsin, the species was rare or absent in lakes with pH <6.0 (Rahel 1984). Field and laboratory observations indicate that the black crappie is tolerant of long exposures to extremely low temperatures (<1◦ C) and DO (ca. 1 ppm), particularly in winter (e.g., Cooper and Washburn 1946; Moyle and Clothier 1959; Siefert and Herman 1977; Carlson and Herman 1978; Knights et al . 1995). Black crappies move to shift seasonal habitats or track resources, to avoid extreme physical conditions, and in response to environmental changes. In the St. Johns River, Florida, 38% of recaptured individuals emigrated at least 5 km from the point of capture, and three fish traveled over 99 km (Snyder and Haynes 1987 in Parsons and Reed 2005). In a series of small, interconnected glacial lakes, up to 92% of recaptured black crappies had emigrated from the lake of origin to another lake (Parsons and Reed 2005). In Wisconsin, radio-tagged black crappies moved among a series of small, shallow finger lakes to overwinter in oxygenated refuges that were distinct from summer and fall activity areas. Individuals avoided areas with DO concentrations <2 mg/l despite physiological advantages of warmer water temperatures (>1◦ C) and lower currents in those areas (Knights et al . 1995). In a South Dakota lake, mean movement in spring and summer was highest in April and July (about 130 m/h), and highest diel movement was at night and early morning. Increased movement also was correlated highly with increased barometric pressure (Guy et al . 1992). Food: The black crappie is primarily a midwater invertivore, usually shifting to piscivory at a relatively late age and large size compared to other piscivorous centrarchids (up to age 3+ in northern populations) (Seaburg and Moyle 1964; Keast and Webb 1966; Keast 1985c). A variety of fishes (e.g., centrarchids, minnows, yellow perch, clupeids), aquatic insects (e.g., chironomid, mayfly, and odonate larvae), and crustaceans (e.g., amphipods, freshwater shrimp) usually dominate diets of the largest individuals (>160 mm TL). Winged insects are occasionally taken in the summer months (McCormick

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1940; Reid 1950b; Seaburg and Moyle 1964; Keast and Webb 1966; Keast 1968a, 1985c; Ball and Kilambi 1972; Becker 1983; Ellison 1984; Keast and Fox 1992; Liao et al . 2002). The zooplankton-dominated diet of young black crappie can be continued until individuals reach a relatively large size (160–200 mm TL), a feeding strategy likely associated with the possession of numerous, long gill rakers (Keast and Webb 1966; et al .Keast 1968a, 1980, 1985c; Bulkley et al . 1976; Overmann et al . 1980; Ellison 1984; Hanson and Qadri 1984; Schael et al . 1991; Pope and Willis 1998; Pine and Allen 2001; Dubuc and DeVries 2002; see account on P. annularis). Young-of-the-year tend toward diurnal or crepuscular feeding, but both adults and young may feed at virtually any hour of the day or night. Large black crappies are one of the most active nocturnal feeders among centrarchids; during the day, individuals may remain in the same location for several hours or all day. Peak movement and feeding occur at dawn or dusk, but movement and feeding also peak at night (Childers and Shoemaker 1953; Keast 1968a; Helfman 1981; Ellison 1984; Guy et al . 1992; Keast and Fox 1992; Shoup et al . 2004). Black crappies often exploit small dipteran larvae (Chaoborus) and pupae (Chironomus) as these insects rise in the water column at dusk and night (Keast 1968a; Keast and Fox 1992). Individuals tend to move to deeper offshore waters during the day and shallower depths or inshore waters at night, presumably to feed, but the extent of these movements and movement patterns varies seasonally (Helfman 1981; Guy et al . 1992; Keast and Fox 1992). The black crappie can feed actively at water temperatures as low as 6.5◦ C (Keast 1968b). Reproduction: Maturity is reached at age 2+ to 4+ and a minimum size of about 178 mm TL (Huish 1954; Cooke et al . 2006). Most nesting and spawning occur at water temperatures of 14 to 22◦ C (to 26◦ C) with peak activity (most active nests) at about 18◦ C (Carlson and Herman 1978; Becker 1983; Colgan and Brown 1988; Pine and Allen 2001; Cooke et al . 2006). Spawning is most protracted in Florida, occurring over a 12-week period from late January to May with peaks in March and April. The spawning season is later (April to June or even July in northern lakes) and shorter (21 to 37 days) at more northerly latitudes (Reid 1950b; Huish 1954; Becker 1983; Keast 1985c; Pope et al . 1996; Travnichek et al . 1996; Pope and Willis 1998; Pine and Allen 2001; Cooke et al . 2006). The ovaries enlarge and continue developing in the fall and over winter (Schloemer 1947; Morgan 1951a), which is likely an adaptation for early spring spawning. In South Dakota waters, male black crappies move 0.4 to 6.0 km to establish spawning sites (Pope and Willis 1997). In the spawning area, the male establishes a territory and prepares a saucer-shaped depressional nest (20 to 23 cm diameter) in variable substrates (gravel, sand, clay, or even softer) and water depths (0.25 to 6.1 m). Nests are placed in areas protected from wind and waves, usually at the base of vegetation (e.g., cattails), near the edge of floating or emergent plant beds, or near other simple cover (e.g., logs) (Reid 1950b; Carlander 1977; Siefert and Herman 1977; Pope and Willis 1997). Nests may be closely spaced (3.3 nests/m2 ) or more loosely aggregated (1.8 m apart) (Breder and Rosen 1966; Carlander 1977; Becker 1983). Reproductive behaviors are presumably similar to those of the white crappie, but little detail is available for comparison. In experimental tanks with two nesting males, females on occasion spawned with both males and in one instance, a male spawned with two females (Siefert and Herman 1977). Eggs are demersal, adhesive, and whitish to yellowish in color (Scott and Crossman 1973; Barwick 1981). Mature ovarian eggs range from 0.68 to 1.05 mm diameter, waterhardened eggs average 0.93 mm diameter (range: 0.7591–1.03 mm), and water-hardened, fertilized eggs average 1.27 mm diameter (Merriner 1971a; Barwick 1981; Cooke et al . 2006). Size-adjusted batch fecundities are higher than any other centrarchid except the white crappie (see accounts on Archoplites and Centrarchus), but female fecundity can be highly variable between years or among populations (Dubuc and DeVries 2002). One to three distinct size classes of maturing ova are reported in ovaries of mature females, suggesting that some females may produce multiple batches of eggs (Barwick 1981; Pope et al . 1996). In controlled settings, the number of eggs released per spawn (average 66,130/243 mm TL female; Siefert and Herman 1977) falls within the range estimated for a 246 mm TL female (see subsequent), suggesting single-batch production. Fecundity increases with female size. The relationship between number of mature eggs (Y) and TL (X) is described by the power functions log Y = −3.0196 + 3.243 log X and log Y = −6.2192 + 4.6580 log TL (formulas from Barwick 1981, n = 59, R2 = 0.57, and Baker and Heidinger 1994, n = 11, R2 = 0.74, respectively). At a mean size of 246 mm TL, a female potentially can produce 54,225 to 82,751 mature eggs in a single batch (range: 10,836–13,168 eggs at 159 mm TL to 143,368–334,396 eggs at 332 mm TL). Hatching occurs in 2.4 days at 18.3◦ C, newly hatched larvae are 2.3 mm TL, and swim-up larvae are about 4 to 5 mm TL (Merriner 1971b; Siefert 1969b; Bulkley et al . 1976; Chatry and Conner 1980; Brown and Colgan 1985b). Black crappie maintained overwinter at DO concentrations as low as 2.6 mg/l successfully spawned (larvae survived to swim-up) during a simulated spring-to-summer rise in temperature (Carlson and Herman 1978). Spawning did not occur in trials with constant DO of 1.8 mg/l or diurnally fluctuating levels of 1.8 to 4.1 mg/l. No differences in number of embryos, hatching success, or survival through swim-up were detected at DO

Centrarchid identification and natural history

475

levels as low as 2.5 mg/l, but at that level individuals started and finished spawning earlier (i.e. at lower temperatures) than those exposed to higher DO concentrations (Siefert and Herman 1977). The male vigorously guards the nest, eggs, and larvae from predation by frequent nest predators, especially Lepomis spp. At the northern edge of the range, the entire cycle of male parental care lasts for about 7 to 11 days from egg deposition until swim-up larvae disperse (Colgan and Brown 1988; Cooke et al . 2006). The male feeds opportunistically during this period on invertebrates occurring on vegetation near the nest (e.g., amphipods) (Reid 1950b; Colgan and Brown 1988; Breder and Rosen 1966). Nest associates: None known. Freshwater mussel host: Confirmed host to A. ligamentina, A. plicata, A. ferussacianus, and L. siliquoidea (Howard 1914, 1922; Coker et al . 1921; Hove et al . 1997). Putative host to L. compressa (unpublished sources in OSUDM 2006). Conservation status: The black crappie is secure throughout its native range (Warren et al . 2000; NatureServe 2006). Similar species: The white crappie has a longer predorsal region, usually six dorsal spines, and vague but usually discernible dark bars on sides (see account on white crappie). Systematic notes: Pomoxis nigromaculatus forms a sister pair with P. annularis (see account on P. annularis). Comparative analyses across the range of the species are lacking. Importance to humans: Catchability, edibility, and liberal catch limits in most waters make the black crappie a highly sought and important sport fish throughout its rather large range. The species is easily caught on minnows, worms, and a variety of artificial lures; dry flies are taken occasionally. Black crappies tend to aggregate and at dusk are often caught one after the other as quickly as the hook can be rebaited. Because it remains active in cold waters, the species is also a popular target for ice fishing enthusiasts (Scott and Crossman 1973; Becker 1983). The flesh is white, flaky, and tasty, comparing favorably as table fare with the highly acclaimed walleye (Sander vitreum) (Scott and Crossman 1973; Becker 1983).

13.11 Identification keys to genera and species Dichotomous keys are presented for identification of genera within the family and species within each genus. The characters used primarily follow and are illustrated in Becker (1983), Page and Burr (1991), Etnier and Starnes (1993), Jenkins and Burkhead (1994), Pflieger (1997), Ross (2001), Boschung and Mayden (2004), Marcy et al . (2005), and other taxa-specific sources given in the generic and species accounts. The species keys here are aimed primarily at identifying adults. Young individuals of many centrarchids can be a challenge to correctly identify to species, but illustrations and characters useful in differentiating juveniles are available in Ramsey and Smitherman (1972), Etnier and Starnes (1993), and Jenkins and Burkhead (1994).

13.11.1 Key to genera of Centrarchidae 1a.

Anal fin with 4 to 5 or more spines. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

1b. Anal fin with 3 spines. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 2a.

Anal fin base shorter than dorsal fin base; anal fin with 12 or fewer soft rays; moderately laterally compressed to elongate body. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

476

Centrarchid fishes

2b. Anal fin base about equal to dorsal fin base; anal fin with 13 or more soft rays; deep, laterally compressed body. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 3a.

Caudal fin bilobed or concave; scales ctenoid; gill rakers long or moderately long, 7 or more on first arch. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

3b. Caudal fin rounded; scales cycloid (scale shape percoid-like with anterior margin truncate and scalloped but ctenii are lacking); gill rakers moderately long, stout, 5 to 7 on first arch. Acantharchus pomotis, mud sunfish 4a.

Red eye in life. Gill rakers moderately long, 7 to 16 on first arch; branchiostegal rays usually 6. Dorsal fin with 10 to 12 spines, 11 to 12 rays; anal fin with 5 to 7 spines, 10 to 11 rays. Ambloplites

4b. Eye not red in life. Gill rakers long, slender, 25 to 29 on first arch; branchiostegal rays usually 7. Dorsal fin with 12 to 14, usually 13 spines, 10 to 12 rays; anal fin with 6 to 8, usually 7 spines, 10 to 12 rays. Archoplites interruptus, Sacramento perch 5a.

Dorsal fin with 5 to 8 spines, 14 to 16 rays; anal fin with 6 spines, 17 to 19 rays; no teardrop; laterally compressed oblong body; rounded pectoral fin. Pomoxis

5b. Dorsal fin with 11 to 13 spines, 12 to 15 rays; anal fin with 7 to 8 spines, 13 to 17 rays; large black teardrop; short, deep extremely laterally compressed body; long, pointed pectoral fin. Centrarchus macropterus, flier 6a.

Body elongate, depth goes into SL three or more times; lateral scale rows 55 or more; dorsal fins nearly separate, deeply notched. Micropterus

6b. Body deeper, laterally compressed, depth goes into SL less than three times; lateral scale rows less than 55; dorsal fins continuous. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7a.

Caudal fin truncate or rounded, not concave or bilobed; black teardrop. Enneacanthus

7b. Caudal fin concave or bilobed; no black teardrop. Lepomis

13.11.2 Key to species of Ambloplites 1a.

Cheek naked or partly scaled, if present cheek scales are tiny or small and deeply embedded; body often with distinct round pale spots (iridescent gold to white in life) on upper side and head (found only in the Roanoke, Tar, and Neuse river drainages of Virginia and North Carolina). Ambloplites cavifrons, Roanoke bass

Centrarchid identification and natural history

477

1b. Cheek fully scaled, the scales moderate to large size and only slightly to moderately embedded; body lacking distinct pale spots. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2a.

Color pattern of sides of body dominated by freckled pattern (scattered dark brown spots); no black edge on anal fin of large male (found only in the White River basin, Arkansas and Missouri, and Sac and Pomme de Terre drainages of the Osage River basin). Ambloplites constellatus, Ozark bass

2b. Sides lack freckled pattern but are dominated by regularly arranged horizontal rows of brown-black spots or broad irregular vertical dark blotches; distinctive black edge on anal fin of large male, present or absent. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 3a.

Color pattern of sides of juveniles and adults dominated by broad irregular vertical brownish or grayish blotches; large male lacks black edged anal fin; breast scale rows (between bases of pectoral fins) usually ≤20. Ambloplites ariommus, shadow bass

3b. Color pattern of sides of adults dominated by regularly arranged horizontal rows of brown-black spots (young patterned similar to A. ariommus); large male with distinctive black edge on anal fin; breast scale rows (between bases of pectoral fins) usually 21 to 25. Ambloplites rupestris, rock bass

13.11.3 Key to species of Enneacanthus 1a.

Six distinct bold black bars on sides contrast with pale to opalescent ground color, often with rose or pink blush; first bar on head passes through eye, forming a distinct black teardrop; the third black bar, extending from the anterior dorsal fin to the pelvic fin forms a distinct black blotch on the first 2 to 3 anterior membranes of the spiny dorsal fin; sixth bar on caudal peduncle is often faint; 3 to 4 incomplete bars often occur between complete bars; juncture of spiny and soft dorsal fin noticeably notched; second dorsal and anal fin not enlarged in breeding male. Enneacanthus chaetodon, blackbanded sunfish

1b. Sides of body lack distinct bold black vertical bars on light background (may have dark to faint bars on dusky background); anterior dorsal fin membranes lack distinct black blotch, fin membranes mostly with uniformly dusky or dark pigmentation with rows of pale spots in soft-rayed portion; dorsal fin smooth in profile, not deeply notched; second dorsal and anal fins enlarged in breeding male. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2a.

Body side pattern of males dominated by 5 to 8 dark to faint vertical bars (darkest on large individuals); rows of greenish-copperish to purple-gold crescent-shaped spots along side; black spot on ear tab larger than eye pupil; usually 19 to 22 scales around caudal peduncle Enneacanthus obesus, banded sunfish

2b. Body side pattern of large young and adults dominated by rows of iridescent blue, silver, or pale round spots; bars on sides indistinct in adults; black spot on ear tab two-thirds the size of eye pupil; usually 16 to 18 scales around caudal peduncle. Enneacanthus gloriosus, bluespotted sunfish

478

Centrarchid fishes

13.11.4 Key to species of Pomoxis 1a.

Dorsal fin base shorter than distance from eye to dorsal fin origin; dorsal spines, usually 5 to 6; cheek scale rows, usually 4 to 5; mottling on sides forming 8 to 10 dark, irregular, but discernible, vertical bars. Pomoxis annularis, white crappie

1b. Dorsal fin base about as long as distance from eye to dorsal fin origin; dorsal spines, usually 7 to 8; cheek scale rows, usually 6; sides randomly mottled with dark pigment (may be vertically barred in young). Pomoxis nigromaculatus, black crappie

13.11.5 Key to species of Lepomis 1a.

Sensory pits on top of head between eyes greatly enlarged, their width about equal to distance between them; sensory pores on edge of opercle greatly elongated, slit-like; ear flap, elongate, flexible, angled upward, black with wide white edge; gill rakers, long, slender, length of longest about 4 to 5 times their basal width. Lepomis humilis, orangespotted sunfish

1b. Sensory pits between eyes not greatly enlarged, their width much less than the distance between them; sensory pores on edge of preopercle, not slit-like; ear flap size, orientation, and pigmentation variable; gill rakers variable. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 2a.

Pectoral fins long and moderately sharply pointed, extending to or beyond anterior rim of eye when bent forward. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

2b. Pectoral fins shorter with tips rounded, not extending to anterior rim of eye when bent forward. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 3a.

Large dark spot at rear of dorsal fin (faint in young); ear flap black to margin; gill rakers long, slender, length of longest four or more times their basal width; dark bars on sides (absent in turbid water; thin and chainlike in young). Lepomis macrochirus, bluegill

3b. No dark spot at rear of dorsal fin; sides usually with scattered dark spots (may form single vertical bars in young); ear flap with pale margin or spot at tip; gill rakers short, longest about two times longer than basal width. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 4a.

Pectoral fins long, extending to about 3 to 5 scale rows below dorsal fin base when angled upward; second dorsal fin with many bold dark brown wavy lines and spots; wavy blue lines on cheek and opercle of adult; sides below lateral line marked with dusky spots (orange in life); body of adults deep, depth about 0.5 of SL; profile of head in adults rounded. Lepomis gibbosus, pumpkinseed

4b. Pectoral fins very long, extending to or beyond dorsal fin base when angled upward; second dorsal fin uniform or with vague dark mottling but lacks bold wavy lines or spots; no blue lines on cheek and opercle; sides below lateral line uniformly pigmented, not marked with dusky spots; body of adults somewhat elongate, depth about 0.4 of SL in adults; profile of head more or less pointed. Lepomis microlophus, redear sunfish

Centrarchid identification and natural history

5a.

479

Tooth patch on tongue; 3 to 4 dark bars (red-brown in life) radiating backward from eye across cheeks and opercles. Lepomis gulosus, warmouth

5b. No tooth patch on tongue; no dark bars radiating backward from eye. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 6a.

Lateral line incomplete or interrupted; gill rakers long, slender, longest 6 to 8 times longer than their basal width; dark spot usually at rear of soft dorsal fin (indistinct in large specimens); coloration relatively subdued, dusky, no bright blue, red, orange, or yellow colors on head or body; small, adults usually <75 mm SL. Lepomis symmetricus, bantam sunfish

6b. Lateral line complete, not interrupted (occasionally interrupted in Lepomis peltastes, which has short, stubby gill rakers and wavy blue lines on cheek and opercle); dorsal spot variable; coloration variable. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7a.

Mouth relatively large and moderately oblique, the upper jaw extending well past anterior rim of eye in large specimens. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

7b. Mouth relatively small and moderately to very oblique, the upper jaw seldom extending past anterior rim of eye. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 8a.

Ear flap short, the black portion inflexible and appearing as a round spot, posterior edges pale; large dark spot usually evident at rear of dorsal and anal fins; gill rakers long and slender, length of longest 4 to 6 times their basal width; lateral scales, usually 45 to 50; scales below lateral line, usually 16 to 19; body relatively elongate, robust, and basslike. Lepomis cyanellus, green sunfish

8b. Ear flap long, narrow, and flexible in adults, black to posterior margin, outlined above and below by pale or blue lines; no large dark spot at rear of dorsal or anal fin; gill rakers moderate, length of longest two times basal width in adults; lateral scales, usually 41 to 50; scales below lateral line, usually 14 to 16; body deep, not basslike. Lepomis auritus, redbreast sunfish 9a.

Ear flap, elongate, thin, and flexible; wavy blue to blue-green lines on cheek and opercle in life; gill rakers, short, stubby, knoblike, length of longest about equal to their basal width in adults. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

9b. Ear flap short, stiff; no wavy blue lines on cheek and opercle; gill rakers not stubby or knoblike, moderate to long, length of longest about two to six times their basal width. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 10a.

Ear flap with black center, bordered in pale to white, angled upward at about 45 degrees and in adult males posterior edge marked with red spot; lateral scales, usually 35 to 37; pectoral rays, usually 12 to 13 (found only in Great Lakes basin and a few scattered localities in the upper Mississippi basin). Lepomis peltastes, northern longear sunfish

10b. Ear flap, variously oriented, with black center and pale to white borders, but lacks distinct posterior red spot (not found in Great Lakes basin). Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

480

11a.

Centrarchid fishes

Cheek scales, usually 3 to 4; pectoral rays, usually 12 to 13; ear flap often angled noticeably upward, center black and often flecked with silver or greenish streaks, margin pale white to greenish; lateral line brick red in life; bluegreen marks (brown in preserved fish) on lower side of head tend to be broken, appearing as freckles or short streaks; body profile somewhat rounded, greatest depth usually beneath or behind the dorsal fin origin. Lepomis marginatus, dollar sunfish

11b. Cheek scales, usually 5 to 6; pectoral rays, usually 13 to 14; ear flap orientation variable, usually horizontal or angled slightly upward, center black, entire margin whitish, flushed with orange-red, or with 2 to 9 red spots scattered along the margin (some populations lack pale margins); lateral line not red in life; blue-green marks (brown in preserved fish) on lower side of head tend to form long continuous streaks; body profile more elongate, the greatest depth usually before the dorsal fin origin in specimens <150 mm SL. Lepomis megalotis, longear sunfish 12a.

Discrete black spots on scales form irregular horizontal rows of spots on sides and dorsum, especially prevalent on lower sides; cheek and opercle often speckled with small discrete dark spots; breeding males lack red-orange on breast, belly, and on sides (these may be yellowish to pinkish); breast scale rows, usually 15 to 18; cheek scales, usually 5 to 7; scales above lateral line, usually, 7 to 8; scales below lateral line, 13 to 15; caudal peduncle scales, usually 8 to 10. Lepomis punctatus, spotted sunfish

12b. Pale areas (red-orange in breeding males) at anterior scale bases form horizontal rows of triangular-shaped spots along sides; discrete black spots lacking at scale bases; cheek and opercle lack speckling of small discrete dark spots (often with a few dusky to dark streaks); breeding males with red-orange color on sides, breast, belly, dorsal margin of ear tab, and quadrate patch on side above ear tab; breast scales, usually 12 to 15; cheek scales, usually 4 to 6; scales above lateral line, usually, 6 to 7; scales below lateral line, 12 to 14; caudal peduncle scales, usually 7 to 9. Lepomis miniatus, redspotted sunfish

13.11.6 Key to species of Micropterus 1a.

Spinous and soft dorsal fins separated by deep notch, if connected, only by a small membrane; length of last dorsal spine less than half the length of longest dorsal spine; upper jaw extends beyond posterior rim of eye in adults; dark lateral band present; caudal fin of juveniles bicolored, the base lighter than posterior portion; pyloric caeca branched at base. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

1b. Dark lateral band present or absent, sides often marked by conjoined blotches or vertically elongate bars; spinous and soft dorsal fins well connected, the notch between the fins shallow; length of last spine more than half the length of longest spine; upper jaw usually not extending beyond posterior rim of eye; caudal fin of juveniles tricolored, often sharply contrasted dark middle region separating orange or yellow base from white (or clear) posterior (faint to lacking in M. coosae), with or without prominent tail spot; pyloric caeca unbranched. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2a.

Lateral scales, usually 69 to 73; caudal peduncle scales, usually 28 to 31 scales (occurs as a native only in peninsular Florida, but widely introduced in the southern United States) Micropterus floridanus, Florida bass

2b. Lateral scales, usually 58 to 67; caudal peduncle scales, usually 26 to 28.

Centrarchid identification and natural history

481

Micropterus salmoides, largemouth bass 3a.

Side uniformly pigmented or with series of broad, indistinct vertical bars, lower sides without distinct rows of horizontal spots, juveniles lack a distinct black caudal spot; scales above lateral line, usually 12 to 13; scales below the lateral line, usually 19 to 23. Micropterus dolomieu, smallmouth bass

3b. Side with a distinct narrow midlateral horizontal band (or series of partly joined quadrate blotches) or a midlateral band consisting of a series of vertically elongate blotches (may be indistinct); juveniles may or may not have a distinct caudal spot; scales above lateral line, usually 6 to 9; scales below lateral line, usually <20. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 4a.

Side with a dark, usually distinct and narrow, midlateral horizontal stripe (or series of partly joined blotches, not elongated vertically) and lower sides with rows of small black spots; middle band on caudal fin and black caudal spot of juveniles distinct; tooth patch on tongue. Micropterus punctulatus, spotted bass

4b. Side with a series of vertically elongate to quadrate blotches (often indistinct or faint in adults). Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 5a.

Caudal fin orange with white (or clear) upper and lower outer edges; tail spot prominent in juveniles; tooth patch on tongue; sides marked with dark confluent irregular blotches or stripe; tinges of red or orange on fins; young lacking sharply contrasting caudal fin pigmentation; 5 to 8 well-developed rows of dark spots on ventrolateral scales. Micropterus coosae, redeye bass

5b. Caudal fin without white (or clear) upper and lower outer lobes; tooth patch on tongue present or absent. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6 6a.

No tooth patch on tongue; sides marked with 10 to 15 dark vertically elongate midlateral bars with 6 to 8 supralateral bars extending into the interspaces of the midlateral bars; 5 to 7 rows of weakly developed spots on ventrolateral scales, frequently forming wavy lines; quadrate to rectangular dark tail spot in adults, lacking or faint in young; caudal peduncle scales, usually 30 to 33; lateral line scales, usually 72 to 77 (found as native only in the Apalachicola River system, Alabama and Georgia). Micropterus cataractae, shoal bass

6b. Tooth patch on tongue; sides variously marked; caudal peduncle scales, usually <31; lateral line scales, usually <69. Go to . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7 7a.

Upper jaw extending to or beyond rear margin of eye in adults; sides marked with a series of about 12 vertically elongate lateral blotches, anteriorly much wider than interspaces, fusing on the caudal peduncle, to form a relatively uniform lateral band; caudal spot prominent in young; caudal peduncle scales, usually 27 to 31; lateral line scales, usually 57 to 65 (found as native only in Suwannee and Ochlockonee river systems, Florida). Micropterus notius, Suwannee bass

7b. Upper jaw extending to or slightly beyond middle of eye; sides marked with a series of about 13 vertically elongate lateral blotches, being broadly diamond shaped, especially on the caudal peduncle; dark spots on scales form distinct continuous lines on lower sides; caudal spot prominent in young; caudal peduncle scales, usually 26 to 27; lateral line scales, usually 61 to 69 (found only on the Edwards Plateau of Texas in the Brazos, Colorado, Guadalupe, and San Antonio rivers and upper Nueces River, where introduced). Micropterus treculi, Guadalupe bass

482

Centrarchid fishes

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Centrarchidae Species List with Latin Name and Common Name

Acantharchus pomotis, mud sunfish Ambloplites ariommus, shadow bass Ambloplites cavifrons, Roanoke bass Ambloplites constellatus, Ozark bass Ambloplites ruprestris, rock bass Archoplites interruptus, Sacramento perch Centrarchus macropterus, flier Enneacanthus chaetodon, blackbanded sunfish Enneacanthus gloriosus, bluespotted sunfish Enneacanthus obesus, banded sunfish Pomoxis annularis, white crappie Pomoxis nigromaculatus, black crappie Lepomis auritus, redbreast sunfish Lepomis cyanellus, green sunfish Lepomis gibbosus, pumpkinseed Lepomis gulosus, warmouth Lepomis humilis, orangespotted sunfish Lepomis macrochirus, bluegill Lepomis marginatus, dollar sunfish Lepomis megalotis, longear sunfish Lepomis microlophus, redear sunfish Lepomis miniatus, redspotted sunfish Lepomis peltastes, northern longear sunfish Lepomis punctatus, spotted sunfish Lepomis symmetricus, bantam sunfish Micropterus henshalli, Alabama bass∗ Micropterus cataractae, shoal bass Micropterus coosae, redeye bass Micropterus dolomieu, smallmouth bass Micropterus floridanus, Florida largemouth bass Micropterus notius, Suwannee bass Micropterus punctulatus, spotted bass Micropterus salmoides, largemouth bass Micropterus treculi, Guadalupe bass

∗

Note: M. henshalli (Alabama bass) was elevated to the species level in 2008 when this book was “in press”. Hence, in this book and index it is referred to as a subspecies of M. punctulatus (spotted bass). 535

Index

Note: Only Latin binomials have been used here. Please consult the previous page for a complete species list with common names cross-referenced with Latin binomials. Activity levels, 181–183, 192–193, 272–273 Aggregations, See Schooling Alternative reproductive tactics, 47, 90–100 Angling quality, 326–327 Anurans, 144 Aquaculture, See Culture Aquatic plant management, 328 Archoplites clarki, 2, 7, 10–12 Archoplites molarus, 2, 8, 10–12 Archoplites taylori, 2, 10–12 Assortative mating, 44 Barriers to hybridization, 43–51 Behavioral thermoregulation, 248–249 Bioenergetic models, 165–196, 283 application, 167–168, 283 evolution, 169 parameterization, 169 validation, 170, 196 Bioenergetics, 151, 165–197 Biogeography and distribitions, 5–12, 26–30, 41–42, 270–271, 283, 375 Blood physiology, 208–238 Body size, 90, 95–99, 108–114, 136, 139–140, 178–181, 189, 192, 219, 225, 248–249, 280 Boreocentrarchus smithi, 2, 6, 10 Bourgeois, 90–93 Cardiovascular physiology, 229–238, 240–242 Catch-and-release, 147, 224–226, 317, 327, 343–345 Centrarchidae, 1–31 Centrarchinae, 17–19 Chemical ecology, 144 Cladistics, 12–26 Colonial nesting, 137–138 Coloration, 44 Commercial fishing, 312–316, 346 Community ecology, 134, 148, 155 Compensatory growth, 173–175 Competition, 84, 106, 118–119, 136, 148–149 Competitive angling events, 318–319, 345–346 Condition indices, 189–190 Conservation status, 358

536

Conservation threats climate change, 283, 354 exotic species, 347 exploitation, 143, 147, 148, 340 flow variation, 353–354 habitat alteration, 148, 283, 349, 352 hybridization, 60–61, 144 introductions, 144, 355–357, 359 migration barriers, 329, 353 water quality degradation, 349–351 Costs of reproduction, 99, 137–139 Courtship sequence, 44–46 Creel survey, 144 Critical periods, 121–123 Critical swimming speeds, 216–217 Cuckoldry, 93–96, 139 Culture, 59, 223 brood stock, 295–296, 300–303, economics, 305 facilities, 294 harvesting and processing, 300, 305 potential, 306 techniques, 293–294, 299, 301–305 Dam removal, 329 Developmental biology, 52–56, 107–108, 193–194 Diets. See Feeding ecology Digestion, 175–176 Dimorphism, 100 Disease, 302, 355–356 Dissolved oxygen, 115, 219, 267–268 Diversity, 1–3, 31, 70, 76, 80, 90, 154, 375 DNA, 21–26, 28, 30, 122 Ecomorphology, 70–85 Ecosystem management, 343 Early life history, 105–123, See Natural history accounts Ambloplites ruprestris, 107 Archoplites interruptus, 105 L. auritus, 108 L. cyanellus, 108 L. gibbosus, 107 L. gulosus, 108

Index

Early life history (Continued) L. microlophus, 107–108 L. punctatus, M. dolomieu, 107, 141 M. floridanus, 107, 141 M. punctulatus, 107, 141 M. salmoides, 107, 141–143 P. annularis, 107–108 P. nigromaculatus, 107–108 Eggs, 48, 109–111, 114, 193–194 Energetics, 115–122, 171, 277, See Bioenergetics Energy density, 184 Environmental variation, 115–120, 283 Eutrophication, 351 Excretion, 184 Exercise, 224–225, 237 Exotic centrarchids, 356 Extant species, 2–4 Extinct species, 2–3, 5–12 Feeding modes, 70–72, 149 Feeding ecology, 171, 274–276, See Natural history accounts Ambloplites ruprestris, 81 Archoplites interruptus, 81 Lepomis spp., 76–79, 81, 135 L. cyanellus, 135 L. gibbosus, 76–79, 135 L. gulosus, 135 L. humilis, 135 L. macrochirus, 84–85, 135 L. marginatus, 135 L. megalotis, 135 L. microlophus, 76–79, 135 L. miniatus, 135 L. peltastes, 135 L. punctatus, 135 L. symmetricus, 135 Micropterus spp., 81, 85, 107, 140–142 M. salmoides, 73, 107 Pomoxis spp., 108 P. annularis, 81, 146–147 P. nigromaculatus, 81, 146–147 Fertilization, 48, 96, 139, 297 Fins, 81–85 Floods, 116 Food consumption rates, 171–173 Food production, 293 Food web dynamics, 149, 151–154 Foraging behavior, 137 Fossils, 5–12 Functional morphology, 70 Gametic incompatibilities, 48 Genetic incompatibilities, 42–43 Genetics, 21–26, 28, 30, 39, 41, 52–56, 58, 62, 78, 92–96, 122 Gizzard shad, 152–154

Gonads, 90, 99, 191 Growth, 93, 105–122, 142, 173–175, 184–188, 190, 272, 276 Habitat use, 278–279, See Natural history accounts Ambloplites ruprestris, 145 Lepomis spp., 135–137 L. cyanellus, 135 L. gibbosus, 44, 135 L. gulosus, 135 L. humilis, 135 L. macrochirus, 44, 135, 279 L. marginatus, 135 L. megalotis, 135 L. microlophus, 135 L. miniatus, 135 L. peltastes, 135 L. punctatus, 135 L. symmetricus, 135 M. dolomieu, 278 M. salmoides, 274, 278 P. annularis, 146 P. nigromaculatus, 146 Haldanes rule, 51–52 Harvest regulations, See Management Hatcheries, See Culture Hatching, 108–113, 146 Hormones, 90, 94, 99, 176 Human dimensions, 325, 329 Hybridization, 39–62, 147, 296 Hybrid inviability, 59–51 Hybrid sterility, 56 Hydrology, 117, 148 Hypoxia, 115, 183, 227–229, 232, 267–268 Ice, 265–266 Ice fishing, 276 Identification keys, 375, 475–481 Genera of Centrarchidae, 475 Ambloplites, 476 Enneacanthus, 477 Lepomis, 478–479 Micropterus, 480–481 Pomoxis, 478 Incubation time, 108–113 Introductions, 144 Introgression, 48, 60 Jaws, 71–80 Lepominae, 2, 10–30 Lepomis kansasensis, 2, 8, 10–12 Lepomis serratus, 2, 8, 10–12 Life history, 100, 105–113, 270–271 Life stage events, 106 Locomotion, 81–85

537

538

Index

Management, 113, 139–140, 165 Management strategies and tools bioenergetic modeling, 165 creel limits, 323–324, 342 gear restrictions, 342, 347 sanctuaries, 143, 342–343 seasonal limits, 323, 342 size limits, 323, 341 the future, 329 Maturation, 99, 138–139, 141 Maximum body size, 189 Metabolic rate, 166, 176–178, 209, 220–222, 268–269 Micropterinae, 3, 10–30 Migration, 107, 118, 121 Molecular clock, 49–50 Morphology, 5–21, 70 mouth, 71 Mortality, 105–106, 121–122, 139, 191, 343 Movement, 273–274, 278 Natural history accounts, 377–475 Acantharchus pomotis, 377–379 Ambloplites ariommus, 380–382 Ambloplites cavifrons, 382–384 Ambloplites constellatus, 384–386 Ambloplites ruprestris, 386–389 Archoplites interruptus, 389–391 Centrarchus macropterus, 392–393 Enneacanthus chaetodon, 394–396 Enneacanthus gloriosus, 396–398 Enneacanthus obesus, 398–400 Lepomis auritus, 402–403 Lepomis cyanellus, 404–406 Lepomis gibbosus, 406–409 Lepomis gulosus, 409–411 Lepomis humilis, 411–413 Lepomis macrochirus, 413–418 Lepomis marginatus, 418–420 Lepomis megalotis, 420–423 Lepomis microlophus, 423–426 Lepomis miniatus, 426–427 Lepomis peltastes, 427–430 Lepomis punctatus, 430–432 Lepomis symmetricus, 432–433 Micropterus cataractae, 435–437 Micropterus coosae, 437–439 Micropterus dolomieu, 439–446 Micropterus floridanus, 446–449 Micropterus notius, 450–451 Micropterus punctulatus, 451–455 Micropterus salmoides, 455–466 Micropterus treculi, 466–468 Pomoxis annularis, 469–472 Pomoxis nigromaculatus, 472–475 Nomenclature, 1–4 Nutrition, 299–300, 302, 305

Ontogenetic habitat shifts, 136, 149 Optimal foraging theory, 136 Oxygen consumption, See Metabolic rate Parasites, 307–308, 355–356 Parasitic mating tactics, 90–94 Parental care, 107–108, 142, 145, 192–193 Paternity, 94 pH, 145, 148 Phylogeny, 12–29, 98–99 Phylogeography, 26–30 Physiological baseline values, 208–213 Physiological recovery, 226 Physiological tolerances, 116, 145, 208–213, 243–244 Piscivory, 106–107, 122, 140 Plioplarchus septemspinosus, 2, 6, 10–12 Plioplarchus sexspinosus, 2, 6, 10–12 Plioplarchus whitei, 2, 6, 10 Pollution, 145, 183, 250–251, 349 Pomoxis lanei, 2, 7, 10–12 Ponds, 139–140, 149, 293, 307 Population dynamics, 108–121, 139, 143, 147, 155 Precipitation, 117 Predation, 106, 119, 136, 144, 149–151, 230, 281 Prey availability, 137, 143 Prey capture, 71–76 Prey energy density, 175 Prey processing, 76–80 Recreational fisheries, 316–323, 340, 376 Recreation fishing impacts, 140, 143, 147, 340 Recruitment (factors influencing), 108–121, 142, 150 abiotic, 114–118, 120–121, 150 biotic, 118–121 interactions, 120–121 Reproductive energetics, 191–193 Reproductive isolation, 43–51 Reproduction, 376, See Natural history accounts Ambloplites ruprestris, 93, 107, 145 Archoplites interruptus, 105 Lepomis spp., 107, 109, 137–139 L. auritus, 93, 109 L. cyanellus, 109 L. gibbosus, 92, 107, 109 L. humilis, 109–110 L. macrochirus, 92–96, 107, 138 L. marginatus, 93 L. microlophus, 107 L. megalotis, 92, 138 L. punctatus, 92 Micropterus spp., 107, 109, 140 M. dolomieu, 93, 107, 141, 193 M. floridanus, 107, 141 M. punctulatus, 107, 141 M. salmoides, 93, 107, 141, 193 Pomoxis spp., 107

Index

Reservoirs, 146, 327–328 Resource use, 70–73 Round goby, 347–348 Salinity, 116 Sanctuaries, 143 Schooling, 183, 277–278 Sedimentation, 351 Sensory biology, 44 Sex rations, 56–57 Sneaker, 47, 92–94 Social interactions, 98–100, 138, 183 Sound production, 45–46 Spawning, 93, 107, 141, See Reproduction Spawning temperature, 108–113, 141 Speciation, 39, 41, 50, 58 Species accounts, 377–475 Species list, 1–3 Species recognition, 44–46 Sperm, 48, 90, 92–93 Starvation, 184–188, 190, 220, 280 Stock-recruitment relationships, 113, 142, 146 Stocking, 139, 293, 355 Stress, 183, 222–239 Stunting, 190 Subspecies, 4–6 Sustainable fisheries, 326–327, 329 Swimming, 81–85, 193, 208, 213–222, 269–270

539

Taxomony, 1–30, 62 Acantharchus pomotis, 1, 12–26 Ambloplites spp., 1, 12–26 Archoplites interruptus, 1, 12–26 Centrarchus macropterus, 1, 12–26 Enneacanthus spp., 1, 12–26 Lepomis spp., 1, 12–26 Micropterus spp., 2, 12–26 Pomoxis spp., 2, 12–26 Territories, 90 Thermal biology, 114–115, 176, 178–181, 191, 196, 215–218, 232–237, 242–250, 350 Thermal preferenda, 244–247 Triploids, 299 Trophic cascades, 152–153 Trophic polymorphism, 84–85, 137 Turbidity, 115, 146, 154, 183, 232, 350 Ventilation, 210, 232 Winter biology, 114, 122, 143, 146, 191, 264–283 Winterkill, 267–268, 279–282 Year class strength, 122 Zebra mussels, 348