The Ecological Ramifications of Disease and Density in the Caribbean Spiny Lobster, Panulirus Argus
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Old Dominion University ODU Digital Commons Biological Sciences Theses & Dissertations Biological Sciences Spring 2003 The cologE ical Ramifications of Disease and Density in the Caribbean Spiny Lobster, Panulirus argus Donald C. Behringer Jr. Old Dominion University Follow this and additional works at: https://digitalcommons.odu.edu/biology_etds Part of the Animal Diseases Commons, Aquaculture and Fisheries Commons, and the Marine Biology Commons Recommended Citation Behringer, Donald C.. "The cE ological Ramifications of Disease and Density in the Caribbean Spiny Lobster, Panulirus argus" (2003). Doctor of Philosophy (PhD), dissertation, Biological Sciences, Old Dominion University, DOI: 10.25777/53r1-mb31 https://digitalcommons.odu.edu/biology_etds/54 This Dissertation is brought to you for free and open access by the Biological Sciences at ODU Digital Commons. It has been accepted for inclusion in Biological Sciences Theses & Dissertations by an authorized administrator of ODU Digital Commons. For more information, please contact [email protected]. THE ECOLOGICAL RAMIFICATIONS OF DISEASE AND DENSITY IN THE CARIBBEAN SPINY LOBSTER, PANULIRUS ARGUS By Donald C. Behringer, Jr. B.S. December 1991, University of Florida A Dissertation Submitted to the Faculty of Old Dominion University in Partial Fulfillment of the Requirement for the Degree of DOCTOR OF PHILOSOPHY ECOLOGICAL SCIENCES OLD DOMINION UNIVERSITY May 2003 Approved'by: Mapk J. Butter, IV (Director) Kent E. Carpenter (Member) D. Shields (Member) Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. ABSTRACT THE ECOLOGICAL RAMIFICATIONS OF DISEASE AND DENSITY IN THE CARIBBEAN SPINY LOBSTER, PANULIRUS ARGUS Donald C. Behringer, Jr. Old Dominion University, 2002 Director: Dr. Mark J. Butler, IV In 1999,1 discovered the first virus known to be pathogenic to any species of lobster. HLV-PA is a pathogenic herpes-like virus that infects juvenile Caribbean spiny lobster, Panulirus argus, in the waters off south Florida (USA), and it alters the behavior and ecology of this species in fundamental ways. Gross signs of HLV-PA infection are lethargy, morbidity, cessation of molting, and discolored, “milky” hemolymph that does not clot. HLV-PA infects the hemocytes of host lobsters, specifically the hyalinocytes and semi-granulocytes, but not the granulocytes. When hemolymph from infected donors was injected into healthy juvenile lobsters, 90% of the healthy individuals became infected within 80 days. In another set of laboratory trials, 40% of the juvenile lobsters that ingested conspecific tissue infected with HLV-PA developed the disease, and in a third experiment wherein transmission by contact or waterborne means was tested, 63% of the lobsters <30 mm carapace length (CL), 33% of lobsters 30-40 mm CL and 10% of lobsters 40-50 mm CL became infected within 80 days. In field surveys from 2000-2001, up to 40% of the juveniles at each of twelve sites (mean = 8%) had the disease. The disease was most prevalent (mean = 16%) among the smallest juveniles (i.e., < 20 mm CL) and, thus far, appears limited to juveniles. However, Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. all of the surveys of disease prevalence are based on gross, visual signs of late stages of infection, and are, therefore, conservative estimates. A diagnostic tool to assess infection at earlier stages has not yet been developed. Field observations and laboratory experiments indicate that healthy juvenile lobsters avoid diseased conspecifics, which is only the second report of such behavior in any animal. The prevalence of the disease in wild lobster populations is not correlated with population density, even when lobsters were experimentally concentrated at sites with artificial shelters. Moreover, enhanced density does not appear to have a detrimental effect on population dynamics such as nutritional condition and short-term residency, likely due to their normal gregariousness. Thus, juvenile spiny lobsters appear to have developed remarkable contradictory behaviors, avoidance of infected conspecifics and gregariousness, both of which may ultimately enhance survival of uninfected lobsters. Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. This dissertation is dedicated to the loves of my life: My wife, Dianne, whose love and support I cherish, and My daughter, Olivia, whose smile makes it all worthwhile Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. V ACKNOWLEDGMENTS I owe a debt of gratitude to numerous people for their inspiration, guidance, brute force labor and not least of all, comradery. The road has been a long one, with numerous hairpin turns and dead-ends, but a trail worth following. Along the way I have experienced and learned a great deal and developed numerous relationships to last a lifetime. To all I will mention and may fail to include, I appreciate every last one of you; you have helped make me who I am. I first thank my parents, for they not only nurtured me through my youth but also instilled in me the values and ideals from which I base my life. Dianne Behringer, my wife and former fellow graduate student, was essential to this dissertation coming to fruition. Her support and encouragement helped me in times of despair and in times of jubilation. She is my foundation. Credit for my basic love of science is undoubtedly owed to my father, Donald Sr., who is a scientist in its purest definition, but Louis Guilette, at the University of Florida, truly inspired me to pursue graduate school with a passion. He is enthralled by what he does and it infuses all those around him. My advisor, Mark Butler, has inspired me in much the same way. He lives and breathes science. He has been a model mentor, both scientifically and personally. I am grateful to have had him as an advisor, a colleague and not the least of all, a friend (oh, and thanks for the financial support, too). This project would have been impossible without the guidance and support of Mark Butler, but also benefited greatly from the aid of Jeffrey Shields. His expertise in the field of pathobiology made possible the inclusion of the virus, HLV-PA, into the Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. project. He gave not only his time and advice, but financial support as well. I also thank mycommittee members, past and present for their advice and guidance: Kent Carpenter, Daniel Dauer, Cynthia Jones, Anthony Provenzano, Simon Therrold, and John Holsinger. My fellow graduate students, past and present, also helped me immeasurably in the field, in the laboratory, and at the bar. Jason Schratwieser and I learned the ropes and had many exhausting field days together and many engaging scientific conversations, here’s to the devastator. Many others helped me in several capacities, so in alphabetical order they were: Dianne Behringer, Scott Donahue, Jason Goldstein, Jamie Heisig- Mitchell, Jennifer Lear, Emmanuel Riclet, and Denice Robertson. I thank Old Dominion University for the support and the opportunity to do this work. I would also like to thank the Keys Marine Laboratory for logistical support and all of the personnel for their advice and assistance. The laboratory aspects of this project would not have been possible without the use of the facilities at the Florida Fish and Wildlife Conservation Commission (FWC) laboratory. I thank John Hunt for his critical assistance and advice, and for making this possible by allowing me access to the laboratory. I also thank the lobster group at FWC: Rodney Bertelsen, Carolyn Cox, Thomas Matthews, and William Sharp, who gave assistance and advice. Lastly, I thank William Hermkind, from whose scientific loins most of those listed here ultimately sprang. His love for the sea, whether studying it, fishing it, or eating it, is contagious. May the rum, coke and lime continue to inspire the science to pour out of us! Reproduced with permission of the copyright owner. Further reproduction prohibited without permission. TABLE OF CONTENTS Page LIST OF TABLES ....... ........................................................................... ....viii LIST OF FIGURES...................................................... ....x Chapter I. INTRODUCTION... ...... ..1 II. A PATHOGENIC HERPES-LIKE VIRUS IN THE CARIBBEAN SPINY LOBSTER, PANULIRUS ARGUS, FROM FLORIDA Introduction ....... 4 Methods ..... 6 Results................... 8 Discussion................................................................................................14 III. HLV-PA IN JUVENILE CARIBBEAN SPINY LOBSTER {PANULIRUS ARGUS) POPULATIONS: BEHAVIORAL ALTERATIONS AND MODES OF TRANSMISSION Introduction........................................................................................ ....18 Methods....................................................................................................25 Results.. ................................. 36 Discussion ..... 44 IV. THE IMPACT OF ARTIFICIALLY ENHANCED DENSITY ON JUVENILE SPINY LOBSTER NUTRITIONAL CONDITION, SHORT TERM RESIDENCY AND DISEASE Introduction. ...... 61 Methods................................ 66 Results.... ....... 76 Discussion................. 88 V. CONCLUSIONS................................................................................. 101 LITERATURE CITED.................................................