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Predation on Planktonic Marine Invertebrate Larvae

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Predation on Planktonic Marine Invertebrate Larvae PREDATION ON PLANKTONIC MARINE INVERTEBRATE LARVAE by KEVIN BRETr JOHNSON A DISSERTATION Presented to the Department ofBiology and the Graduate School ofthe University of Oregon in partial fulfillment of the requirements for the degree of Doctor of Philosophy June 1998 11 "Predation on Planktonic Marine Invertebrate Larvae," a dissertation prepared by Kevin B. Johnson in partial fulfillment of the requirements for . the Doctor of Philosophy degree in the Department of Biology. This dissertation has been approved and accepted by: L5!lka (i8 Date Committee in charge: Dr. Alan L. Shanks, Chair Dr. William E. Bradshaw Dr. Stephen S. Rumrill Dr. Lynda P. Shapiro Dr. Cathy Whitlock Accepted by: Vice Provost and Dean of the Graduate School v CURRICULUM VITAE NAME OF AUTHOR: Kevin Brett Johnson PLACE OF ~IRTH: Fullerton, California DATE OF BIRTH: December 31, 1968 GRADUATE AND UNDERGRADUATE SCHOOLS ATTENDED: University ofOregon Brigham Young University DEGREES AWARDED: Doctor ofPhilosophy in Biology, 1998, University ofOregon Bachelor of Science in Zoology, 1992, Brigham Young University AREAS OF SPECIAL INTEREST: Larval Ecology Invertebrate Zoology Marine Biology Life-History Evolution Natural History PROFESSIONAL EXPERIENCE: Research Assistant, Oregon Institute of Marine Biology and Department ofBiology, University of Oregon, Eugene, 1994-1998 Graduate Teaching Fellow, Oregon Institute of Marine Biology and Department ofBiology, University of Oregon, Eugene, 1992-1997 Teaching Assistant, Zoology Department, Brigham Young University, Provo, 1991-1992 Missionary, Church ofJesus Christ ofLatter-Day Saints, 1988-1990 VI AWARDS AND HONORS: Western Society of Naturalists Paper Competition, Honorable Mention, 1997 Department of Defense, Fellowship Program, Honorable Mention, 1995, Brigham Young University, 'Y' scholar, 1987 Boy Scouts ofAmerica, Eagle Scout, 1986 International Thespian Society, Inductee, 1985 GRANTS: American Museum of Natural History, 1995 VB PUBLICATIONS: Bradshaw, W. B., and K. B. Johnson. 1995. Initiation of Metamorphosis in the Pitcher-Plant Mosquito: Effects of Larval Growth History. Ecology 76:2055-2065. Johnson, K. B. 1998a. The Nemertea. In press in A. L. Shanks, editor. Identifying Planktonic Invertebrate Larvae ofthe Coos Bay Estuary. Oregon Institute of Marine Biology, Charleston, Oregon, USA. Johnson, K. B. 1998b. The Phoronida. In press in A. L. Shanks, editor. Identifying Planktonic Invertebrate Larvae ofthe Coos Bay Estuary. Oregon Institute of Marine Biology, Charleston, Oregon, USA. Johnson, K. B. 1998c. The Sipuncula. In press in A. L. Shanks, editor. Identifying Planktonic Invertebrate Larvae ofthe Coos Bay Estuary. Oregon Institute of Marine Biology, Charleston, Oregon, USA. Johnson, K. B., and L. A. Brink. 1998. Predation on bivalve veligers by polychaete larvae. Biological Bulletin 194: In press. Johnson, K. B., and A. L. Shanks. 1996. In situ measurements of predation upon larvae of benthic marine invertebrates. The American Zoologist 36:72A (Meeting abstract). Johnson, K. B., and A. L. Shanks. 1997. The importance ofprey densities and background plankton in studies of predation on invertebrate larvae. Marine Ecology Progress Series 158:293-296. Smith, D. L., and K. B. Johnson. 1996. A Guide to Marine Coastal Plankton and Marine Invertebrate Larvae, Second Edition. KendalllHunt, Dubuque, Iowa, USA. VIll ACKNOWLEDGEMENTS I express sincere thanks to the following individuals for their contributions to this dissertation. Alan Shanks provided adept guidance . and was an excellent advisor. My Dissertation Advisory Committee greatly improved my research and publications. A special thanks goes to Steve Rumrill, who first pointed out to me the need for research on larval mortality. Barbara Butler was invaluable in acquiring reference material. I appreciate the support ofthe staff, students, and faculty at the Oregon Institute of Marine Biology. Bruno Pernet assisted in the culture and maintenance of scaleworm larvae. The staff and facilities at Friday Harbor Laboratories were instrumental to my field experiments. Funding for this research was provided by an American Museum of Natural History Lerner-Gray Fund award to KBJ and NSF award #OCE-9521093 to ALS. Thanks to Lee Braithwaite at Brigham Young University for inspiring me, guiding me, and introducing me to marine plankton and invertebrate larvae. Jim and Bonnie Thompson have supported my work and I am thankful. I would like to thank my parents, Royle and Sue Johnson, for encouraging me to pursue my dreams and teaching me how. Finally, I want to express appreciation to my wife Colleen for unfailing support and to my daughter Bethany for helping me keep things in perspective. IX TABLE OF CONTENTS Chapter Page I. GENERAL INTRODUCTION.. .. .. 1 Selected References 13 I I. THE IMPORTANCE OF PREY DENSITIES AND BACKGROUND PLANKTON IN STUDIES OF PREDATION ON INVERTEBRATE LARVAE. .. .. ID Abstract ID Introduction. ............................... 21 Methods 22 Results. ................................... 29 Discussion ................................. 31 Selected References .......................... 33 Bridge. .................................... 35 III. PREDATION ON BIVALVE VELIGERS BY POLYCHAETE LARVAE. .................... 36 Abstract 36 Introduction.. ~ ............................. '37 Materials and Methods 40 Results. ................................... 44 Discussion ................................. 49 Summary.................................. 52 Selected References .......................... 53 Bridge. .................................... 56 IV. THE IMPORTANCE OF ENCOUNTER RADIUS AND PREY SWIMMING SPEED IN PLANKTONIC ENCOUNTER MODELS. ........................ 58 Abstract 58 Introduction. ............................... 59 Methods ,.. .. 64 Results. ................................... 66 Discussion ................................. 68 Conclusion. ................................ 73 x TABLE OF CONTENTS, Continued Selected References .......................... 75 Bridge. .................................... 78 V. PREDATIO!'f ON PLANKTONIC MARINE AND ESTUARINE INVERTEBRATE LARVAE. .. ..... .. 79 Abstract 79 Introduction. ............................... 81 Methods. .................... .. ............ ro Results .................................... 102 Discussion. ................................ 114 Selected References .......................... 145 VI. CONCLUDING SUMMARY ..................... 154 BIBLIOGRAPHY. ..................................... 157 Xl LIST OF TABLES Table Page Chapter III 1. Mean Number of Crassostrea gigas Veliger Larvae in Individual Guts of Predatory Larval Polychaetes .......................... 48 Chapter V 1. Summary of Observational Experiments............ 2. Summary of Seeded Predators in Manipulation Experiments ................... 100 3. Mean Recovery of Marked Larvae in Observational Experiments ................... 105 4. Predation on Marked Bivalve Veliger Larvae from Observational Experiments............... 106 5. Background Plankton in Observational Experiments.. 109 6. Manipulation Experiment: Predators on Marked Pluteus (P) and Marked Veliger (V) Larvae by Treatment......................... 113 7. Predator Encounter Radiuses ( R) and Predator and Prey Swimming Speeds (v and u, Respectively)....... 8. Estimates of Marked Pluteus Encounters with Predators in Observational Experiments............ 123 9. Estimates of Marked Veliger Encounters with Predators in Observational Experiments............ 125 10. Encounter Estimates of Specified Predators with Wild Invertebrate Larvae in Corral Assemblages Over 24 H.................... 132 Xll LIST OF FIGURES Figure Page Chapter II 1. Pre'dator-Induced Mortality as a Function ofPrey Density ............................. 24 2. For Three Predator-Prey Combinations, Percent Prey Mortality at Densities Selected Based Upon Observed Predation in Prey Density Experiments . Chapter III 1. Veliger Predation. ............................. 46 Chapter IV 1. Body Radius of Suspension-Feeding Trochophore Larva ofA. vittata, Synonymous with Encounter Radius R . 2. The Number of Captured Prey in Arctonoe vittata Trochophores Vs. Log Prey Density . 3. The Number ofPrey in Arcton6e vittata Trochophores Vs. Log Prey Density . 4. Encounter Prediction Curves for the GS and CR Encounter Models 71 Chapter V 1. In Situ Corrals: Deployment and Dimensions. ...... 94 2. Field ofView from Sample Sorting with Myriad Phytoplankton and Background Plankton, Viewed Under White Light. .................. 103 XlII LIST OF FIGURES, Continued Figure Page Chapter V 3. The Effects ofPrey Density and ;Background Plankton on Larval Mortality. .................... 112 4. Mean Number of Bivalve Veligers Consumed by the Hydromedusa Proboscidactyla flavicirrata in Laboratory Experiments. ..................... 115 5. Laboratory Predation by Proboscidactyla flavicirrata on Small, Large, and Mixed (Large and Small) Bivalve Veligers ............................... 116 6. Capture of a Bivalve Veliger by the Heterotrophic Dinoflagellate Noctiluca scintillans 139 I~ I 1 CHAPTER I GENERAL INTRODUCTION . Many marine and estuarine invertebrates have complex life cycles and produce planktonic larvae which reside in the water column for hours to months (Levin and Bridges, 1995). Larvae may develop from free­ spawned ova or be released from adults or egg cases after a period of brooding or encapsulation. A single adult invertebrate can produce vast numbers of these planktonic propagules. For example, during a single spawning season one
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