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The Evolutionary Ecology of Venomous Catfishes, with a Focus on Members of the North American Family Ictaluridae (Teleostei: Siluriformes)

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The Evolutionary Ecology of Venomous Catfishes, with a Focus on Members of the North American Family Ictaluridae (Teleostei: Siluriformes) THE EVOLUTIONARY ECOLOGY OF VENOMOUS CATFISHES, WITH A FOCUS ON MEMBERS OF THE NORTH AMERICAN FAMILY ICTALURIDAE (TELEOSTEI: SILURIFORMES) by Jeremy J. Wright A dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy (Ecology and Evolutionary Biology) in the University of Michigan 2012 Doctoral Committee: Professor William L. Fink, Co-Chair Associate Professor Thomas F. Duda, Jr., Co-Chair Professor Mark D. Hunter Emeritus Professor Gerald R. Smith ACKNOWLEDGEMENTS The completion of this work would not have been possible without the contributions of a number of people who were gracious enough to offer their assistance and support over the course of my time as a Ph.D. student at the University of Michigan. First and foremost is my wife, Jacqueline, who has unprotestingly been conscripted as a field assistant, sounding board and source for research ideas and methodological improvement, reviewer and editor of manuscripts, and constant source of encouragement. It is no exaggeration to say that this research would not be what it is without her input and assistance. My dissertation committee has provided invaluable encouragement, advice, and logistical support throughout the process of formulating and executing the research contained herein. Bill Fink (initially my committee’s sole chair) deserves credit for first encouraging me to pursue the area of venomous fish research, which has proved enormously fruitful in terms of projects, publications and professional interactions and recognition. His enthusiasm for the research program that I’ve developed, as well as his trust in my ability to complete these and other research projects during my time at the University of Michigan, have always been greatly appreciated. Tom Duda (co-chair) generously provided lab space for many of the preparations and experiments necessary to this research, as well as greatly enhancing my understanding of and ability to implement a number of molecular techniques which, while not necessarily directly involved in the following chapters, have nevertheless allowed for the pursuit of a number of additional ii research projects and a broader understanding of the tools and techniques available to augment future studies of venom production in fishes. Jerry Smith has always been available for the discussion of research ideas and methodology, and has provided innumerable suggestions that have served to improve the scope and rigor of the research presented here. In the early years of my Ph.D. study, Jerry was also instrumental in collecting Michigan catfishes, both through his knowledge of localities in the area that were likely to produce the specimens that I required, and often the contribution of his time to physically help me in the field. Finally, Mark Hunter has offered valuable perspective (both ecological and evolutionary) and suggestions for research directions, such that I entered committee meetings with excitement, rather than the trepidation that precedes so many of these discussions, knowing that his thoughts and suggestions for improvement would invariably lead to a stronger finished product. Additional improvements to various aspects of this dissertation were inspired by conversations with former and current members of the UMMZ fish division’s “FishClub”, including Doug Nelson, Prosanta Chakrabarty, Clyde Barbour, Peter Esselman, Peter McIntyre, Ron Oldfield, Solomon David, and Katherine Birkett. My gratitude is also due to a number of additional people who have contributed their time and efforts to help me in acquiring live fishes. Nicole and Tim Matos enthusiastically allowed themselves to be led on tours of some of the more…”interesting” areas of the southern United States in search of catfishes, in the process pioneering a new and very effective seining method and contributing to some of my fondest memories related to this work. Thanks “Stompy”; thanks “Hulk”. “Pous” Mcguinness provided constant encouragement and good cheer in times when it appeared that collecting efforts iii in certain regions and localities would be futile. Field assistance was also, at various times, provided by family (Ty, Sue and Max Ruhland; Bill and Michelle Kelly), friends (Sam and Kassia Martin), colleagues (Wayne Starnes and Morgan Raley, North Carolina State Natural History Museum; Katherine Birkett, University of Michigan School of Natural Resources), and members of state wildelife agencies (Bill Collart, North Carolina Wildlife Resources Commission; Brad Utrup, Michigan Department of Natural Resources). Tanganyikan Synodontis specimens used in the completion of Chapter 5 were kindly obtained for me by David Assemany (The Aquarium Shop, Royal Oak, MI) and Jim Ellenberger (Mainly Cichlids, Santa Clara, CA). Funding for this research was provided by a number of sources, most substantially by the University of Michigan Museum of Zoology, through the Carl L. and Laura Hubbs Fellowship, Hinsdale and Walker Scholarships, and the UMMZ Fish Division Graduate Student Research Fund. Additional support was provided by the Horace H. Rackham School of Graduate Studies through two (precandidate and candidate) Graduate Student Research Grants, and several Graduate Student Travel Grants that have allowed me to present this research and gain valuable feedback at professional society meetings. Finally, a Raney Award from the American Society of Ichthyologists and Herpetologists supplemented costs associated with travel and collection of specimens required for the completion of Chapter 4. Several natural resources agencies, including the Alabama Department of Conservation and Natural Resources, Arkansas Game and Fish Commission, Kentucky Department of Fish and Wildlife Resources, Michigan Department of Natural Resources, North Carolina Wildlife Resources Commission, and Tennessee Wildlife Resources iv Agency provided scientific collecting permits which were used to obtain the specimens used in this research. The University of Michigan Committee on the Use and Care of Animals (UCUCA) regulations and Guidelines provided approval for all experimental procedures involving live animals were approved under UCUCA protocol numbers 09713, 10249, and 10504. v TABLE OF CONTENTS Acknowledgements ............................................................................................................. ii List of Tables ..................................................................................................................... ix List of Figures .................................................................................................................... xi Abstract ........................................................................................................................... xvii Chapter 1. The Venom Glands of Fishes: A Review and Discussion of Their Classification as Adaptive Traits.....................................................................................................................1 Abstract ....................................................................................................................1 Introduction ..............................................................................................................2 Venom Gland and Delivery System Morphology ...................................................4 Gross Morphology .......................................................................................4 Cellular Morphology ....................................................................................6 Piscine Axillary Glands ...........................................................................................8 Gross Morphology .......................................................................................8 Cellular Morphology ....................................................................................9 Possible Function .........................................................................................9 Pharmacology and Toxicology of Piscine Venoms ...............................................10 Chemistry of Piscine Venoms ................................................................................12 Proteins ......................................................................................................12 Other Toxic Components ...........................................................................14 Chemical Complexity of Piscine Venoms .................................................14 Do Piscine Venom Glands Fit Existing Definitions of Adaptive Traits? ..............16 Teleonomic Definitions .............................................................................16 Derived Trait Definitions ...........................................................................19 Selective Spread Definitions ......................................................................22 Nonhistorical Definitions ...........................................................................23 Selective Advantage? .................................................................................25 Summary ................................................................................................................27 Acknowledgements ................................................................................................28 Literature Cited ......................................................................................................36 2. Diversity, Phylogenetic Distribution, and Origins of Venomous Catfishes ..................45
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