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The Reproductive Ecology of a Northeastern Pacific

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THE REPRODUCTIVE ECOLOGY OF A NORTHEASTERN PACIFIC NUDIBRANCH, JANOLUS FUSCUS, WITH AN EXAMINATION OF ITS ENDOPARASITIC COPEPOD, ISMAILA BELCIKI by MAYA WOLF A DISSERTATION Presented to the Department of Biology and the Graduate School of the University of Oregon in partial fulfillment of the requirements for the degree of Doctor of Philosophy December 2010 DISSERTATION APPROVAL PAGE Student: Maya Wolf Title: The Reproductive Ecology of a Northeastern Pacific Nudibranch, Janolus fuscus, with an Examination of Its Endoparasitic Copepod, Ismaila belciki This dissertation has been accepted and approved in partial fulfillment of the requirements for the Doctor of Philosophy degree in the Department of Biology by: Barbara Roy Chairperson Craig Young Advisor Richard Emlet Member Sandra Brooke Member Frances White Outside Member and Richard Linton Vice President for Research and Graduate Studies/Dean of the Graduate School Original approval signatures are on file with the University of Oregon Graduate School. Degree awarded December 2010 ii © 2010 Maya Wolf iii DISSERTATION ABSTRACT Maya Wolf Doctor of Philosophy Department of Biology December 2010 Title: The Reproductive Ecology of a Northeastern Pacific Nudibranch, Janolus fuscus, with an Examination of Its Endoparasitic Copepod, Ismaila belciki Approved: _______________________________________________ Dr. Craig M. Young The arminacean nudibranch Janolus fuscus (family Zephyrinidae) is found in rocky intertidal habitats along the northeast Pacific coast. Adult J. fuscus are conspicuous from April to October but absent in the early winter at two sites, North Cove and Fossil Pt., in the Coos Bay region of Oregon. Over four years of intertidal surveys at these sites, the density of J. fuscus peaked with the abundance of their bryozoan prey, Bugula pacifica and Tricellaria circumternata, in spring and summer, while adult absence in winter was correlated with strong winter storms. To describe the timing of development and determine the life cycle of J. fuscus, embryos and larvae were reared in the laboratory and examined with light, scanning electron, and confocal microscopy. Larvae reared in the lab and juveniles collected from the field were monitored to quantify growth. Janolus fuscus exhibited typical spiral cleavage and hatched as planktotrophic veligers that grew for over a month before they reached competency, settled, and metamorphosed on their prey, B. pacifica. Juvenile growth was rapid, and adults reached maximum sizes of over 50 mm before dying. These demographic and developmental studies suggest that J. fuscus is a subannual species with a life span of approximately five iv months. Janolus fuscus is often infected with an endoparasitic copepod, Ismaila belciki. In the field, prevalence of I. belciki increased with host density and size. The distribution of I. belciki was weakly aggregated in the host population. The large female parasite was generally found in the anterior portion of the host hemocoel, and one or more dwarf males were typically associated with each female. Infected J. fuscus produced significantly smaller egg masses with fewer larvae than did uninfected individuals. Infection did not influence growth rate but did cause decreased survival in older nudibranchs. To examine the life cycle of I. belciki, naupliar larvae were reared in the lab and incubated with potential hosts. Additionally, copepodid stages were described from dissected J. fuscus collected from the field. Ismaila belciki has a least three planktotrophic naupliar stages and four copepodid stages in its life cycle. v CURRICULUM VITAE NAME OF AUTHOR: Maya Wolf GRADUATE AND UNDERGRADUATE SCHOOLS ATTENDED: University of Oregon, Eugene College of Charleston, Charleston, South Carolina DEGREES AWARDED: Doctor of Philosophy, Biology, 2010, University of Oregon Bachelor of Science, Marine Biology, 2004, College of Charleston AREAS OF SPECIAL INTEREST: Larval Ecology Reproductive Ecology Parasitology PROFESSIONAL EXPERIENCE: Research Assistant, University of Oregon, 2004-2010 Supervisor, Craig Young Teaching Assistant, University of Oregon, 2005-2007 Supervisors: Richard Emlet, Nora Terwilliger, Craig Young, Charlie Hunter NSF GK-12 Fellow, Oregon Institute of Marine Biology, 2006-2008 Supervisors: Jan Hodder, Patricia Mace, Alan Shanks Administrative Outreach Coordinator GTF, University of Oregon, 2009-2010 Supervisors: Joyce Croes, Jan Hodder, Craig Young vi GRANTS, AWARDS, AND HONORS: Neil Richmond Fellowship, Oregon Institute of Marine Biology, 2005, 2009 Meritous Presentation Award, American Society of Parasitologists, 2008 Paul and Helen Weiser Memorial Fellowship, University of Oregon, 2009 PUBLICATIONS: Wolf, M. and A. Laferierre. 2009. Crawl into inquiry based learning: hermit crab experiments. Science Activities, Fall issue. Wolf, M. 2008. Seastar flip experiment. Northwest Aquatic Marine Educators. Scuttlebutt. Pp 4-5. vii ACKNOWLEDGMENTS I wish to express sincere appreciation to my advisor, Craig Young, for his substantial support and advice throughout the work embodied by this dissertation and for encouraging me to participate in a variety of activities, including courses at other institutions, that greatly enriched my graduate experience. Craig Young and Sandra Brooke provided welcome opportunities to participate in deep-sea research cruises and projects. I wish to thank Richard Emlet for graciously allowing me use of his laboratory facilities, for statistical advice and editing, and for instruction and enthusiasm in all things larval. I extend my gratitude also to Bitty Roy, Frances White, and Alan Shanks for their statistical expertise, inspiring ideas in experimental design, and expressions of enthusiasm for this project. The work would not have been possible without Sandra Brooke, Tracey Smart, Shawn Arellano, Ahna van Gaest, Paul Dunn, and Laurel Hiebert for their help in the field, for discussing experimental design and statistics and especially for editing parts of this dissertation. Armand Kuris and Ryan Hechinger, who kindly hosted me for a term in the Kuris lab and invited me to participate in the parasitology course at UCSB. They provided invaluable insights into the world of parasites. Drs. Svetlana Maslakova and George von Dassow welcomed me into their laboratory, trained me on the confocal microscope, and assisted with other related techniques. I thank Dr. Cynthia Trowbridge for editing a chapter of this dissertation, for enlightening discussions about sea slugs, and for providing the opportunity to participate in research abroad. Dr. Terue C. Kihara from the Universidade de Sao Paulo shared her experience on the staining copepod exoskeletons and Dr. Geoffrey Boxshall of the Natural History Museum assisted in the identification of contaminants in cultures. Dr. Dave Bilderback assisted in viii identifying bryozoan species. I thank Dr. Jeff Goddard for encouragement and for sharing unpublished data on Janolus fuscus in North Cove. Scott Groth served as my diving partner and shared his amazing in situ photographs of sea slugs. Heidi Harris provided GIS expertise and help in finding intertidal maps. I wish to thank Barb Butler and the University of Oregon librarians for helping me acquire a constant stream of literature for this dissertation. This work would not have been possible without the help of many graduate and undergraduate students at the Oregon Institute of Marine Biology, especially Heather Austin, Katie Bennett, Sam Bund, Zair Burris, Ezzy Cooper, Paul Cziko, Christina Geierman, Ben Grupe, Mike Holmes, AnnMarie Jones, Holly Keammerer, Alix Laferriere, Ryan Lenz, Josh Lord, Jose Marin Jarrin, Sara Matthews, Myndee McNeil, Wyatt Miller, Annie Pollard, Kristina Sawyer, Stephanie Schroeder, and Kira Treiberg. Salary support during this investigation came in part from a National Science Foundation GK-12 grant to Drs. Jan Hodder and Alan Shanks and National Science Foundation grants to Dr. Craig Young. Last, I must thank my incredibly supportive family, including the Wolf, Punnett, Estridge, Rodenbush, and Watts clans and my awesome husband, Sean Watts for his endless patience and love. ix To Jo and Ed Wolf and Sean Watts for their love, support and patience. And To Betsy who read “Girls Can Be Anything” to me when I was young. x TABLE OF CONTENTS Chapter Page I. GENERAL INTRODUCTION ............................................................................... 1 Opisthobranch Demography .................................................................................. 1 Development and Growth of Opisthobranchs........................................................ 3 Splanchnotrophid Copepods .................................................................................. 4 Copepod Life Cycles.............................................................................................. 5 Scope and Objectives ............................................................................................. 6 II. THE DEMOGRAPHY OF A NORTHEAST PACIFIC NUDIBRANCH, JANOLUS FUSCUS, IN RELATION TO PREY ABUNDANCE AND STORM EFFECTS ............................................................................................................... 9 Problem .................................................................................................................. 9 Methods.................................................................................................................. 12 Sites .................................................................................................................
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