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Reproductive and Larval Biology of the Northeastern Pacific

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Reproductive and Larval Biology of the Northeastern Pacific REPRODUCTIVE AND LARVAL BIOLOGY OF THE NORTHEASTERN PACIFIC POLYCHAETE OWENIA COLLARIS (FAMILY OWENIIDAE) IN COOS BAY, OR by TRACEY IRENE SMART 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 2008 ii “Reproductive and Larval Biology of the Northeastern Pacific Polychaete Owenia collaris (Family Oweniidae) in Coos Bay, OR,” a dissertation prepared by Tracey Irene Smart 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: ____________________________________________________________ Barbara A. Roy, Chair of the Examining Committee ________________________________________ Date Committee in Charge: Barbara Roy, Chair Richard Emlet Craig Young Charles Kimmel William Orr Accepted by: ____________________________________________________________ Dean of the Graduate School iii © 2008 Tracey Irene Smart iv An Abstract of the Dissertation of Tracey Irene Smart for the degree of Doctor of Philosophy in the Department of Biology to be taken December 2008 Title: REPRODUCTIVE AND LARVAL BIOLOGY OF THE NORTHEASTERN PACIFIC POLYCHAETE OWENIA COLLARIS (OWENIIDAE) IN COOS BAY, OR Approved: _______________________________________________ Richard B. Emlet Approved: _______________________________________________ Craig M. Young The polychaete worm Owenia collaris (Family Oweniidae) is found in soft sediment habitats along the northeastern Pacific coast, particularly within bays and estuaries. Seasonally, these small tubeworms spawn gametes freely into the water column where they develop into planktotrophic mitraria larvae. After three to four weeks at ambient temperatures, they undergo a dramatic metamorphosis and return to the bottom. The reproductive and larval biology of a population of O. collaris in Coos Bay, OR was investigated over several years. The development of this polychaete has several unusual features, including a stomodeum not derived from the blastopore and continued proliferation of trochoblast descendents, producing simple cilia on monociliated cells. v The description of larval and juvenile structures provided morphological characteristics useful for distinguishing this species from the congener O. fusiformis. The consequences of the unusual larval morphology of O. collaris (i.e. simple cilia, convoluted ciliated band) were investigated by comparing the feeding performance and growth of this species with those of invertebrate larvae representative of the more typical tornaria-type larval forms found in deuterostomes and trochophore-type larval forms found in the lophotrochozoa. Feeding and growth patterns were similar in the convergent mitraria and deuterostome larval forms. In an experiment designed to test the relationship between abiotic factors and the seasonal reproduction, the onset of breeding was cued by photoperiod, but seasonal trends in temperature, alkalinity, food availability for larvae, and salinity may drive reproductive patterns as well. Within the Coos Bay estuary, the intertidal distribution of O. collaris is related to adult salinity tolerances. Low salinity limits horizontal distribution and also reduces potential for reproduction. Most life- history stages are tolerant of a wide range of temperatures, both higher and lower than those typically seen in Coos Bay. There is little evidence to support the hypothesis that sediment characteristics limit distribution within the bay, although settling juveniles show some preference for small grain sizes and may not be able to recruit to mudflats that completely lack these size fractions. vi CURRICULUM VITAE NAME OF AUTHOR: Tracey Irene Smart PLACE OF BIRTH: Marion, OH DATE OF BIRTH: November 18, 1978 GRADUATE AND UNDERGRADUATE SCHOOLS ATTENDED: University of Oregon, Oregon Institute of Marine Biology University of Arizona DEGREES AWARDED: Doctor of Philosophy, December 2008, University of Oregon Master of Science, December, 2003, University of Oregon Bachelor of Science, May 2001, University of Arizona AREAS OF SPECIAL INTEREST: Larval Ecology Reproductive Ecology PROFESSIONAL EXPERIENCE: Research Assistant, 2001-2008, University of Oregon Supervisors: Richard Emlet, Craig Young Teaching Assistant, 2003-2008, University of Oregon Supervisors: Richard Emlet, Nora Terwilliger, Craig Young NSF GK-12 Fellow, 2004-2007, Oregon Institute of Marine Biology Supervisors: Janet Hodder, Patricia Mace, Alan Shanks vii PUBLICATIONS: viii ACKNOWLEDGMENTS I wish to express sincere appreciation to Drs. Richard Emlet and Craig Young for their guidance and support throughout the work embodied by this dissertation. In addition, special thanks are due to Dr. George von Dassow for his technical guidance, advice, and encouragement in choosing to work with a poorly understood species. I would also like to thank Dr. Barbara Roy for her assistance with statistics, composition, and for keeping everyone on track. I also thank Drs. Charles Kimmel and William Orr for their advice and support. This work would not have been possible without the help of many faculty and graduate and undergraduate students at the Oregon Institute of Marine Biology. In particular, I greatly appreciate the help of Shawn Arellano, Katie Bennet, Sandra Brooke, Timothy Davidson, Christina Geierman, Ben Grupe, AnnMarie Jones, Holly Keammerer, Alix Laferriere, Jose Marin Jarrin, Michelle Schuiteman, Ahna Van Gaest, and Maya Wolf. This investigation was partially funded by a National Science Foundation GK-12 grant to Drs. Jan Hodder and Alan Shanks at OIMB and National Science Foundation Biological Oceanography grants to Drs. Richard Emlet and Craig Young. ix TABLE OF CONTENTS Chapter Page I. GENERAL INTRODUCTION ............................................................................ 1 Development of Polychaetes ......................................................................... 1 Larval Performance ....................................................................................... 2 Seasonal Reproduction in Polychaetes ......................................................... 4 Control of Distribution Within Estuaries ...................................................... 4 Scope and Objectives .................................................................................... 5 II. PROPERTIES OF PROTOSTOMY AND DEUTEROSTOMY IN THE EMBRYOGENESIS AND LARVAL DEVELOPMENT OF OWENIA COLLARIS (ANNELIDA: POLYCHAETA) ............................... 8 Introduction ................................................................................................... 8 Materials and Methods .................................................................................. 10 Results ........................................................................................................... 12 General Embryology ................................................................................ 12 Fate of the Blastopore ............................................................................... 15 Prototroch Formation ............................................................................... 17 Larval Development ................................................................................. 20 Metamorphosis ......................................................................................... 23 Juvenile Worm Morphology .................................................................... 26 Discussion ..................................................................................................... 29 Bridge I ......................................................................................................... 33 III. FUNCTIONAL MORPHOLOGY OF CILIATED BANDS: DOES PHYLOGENY OR FORM GOVERN THE PERFORMANCE OF THE LARVAL CILIATED BANDS OF THE POLYCHAETE OWENIA COLLARIS (FAMILY OWENIIDAE)? ........................................ 34 Introduction ................................................................................................... 34 Materials and Methods .................................................................................. 38 Results ........................................................................................................... 43 x Chapter Page Discussion ..................................................................................................... 52 Bridge II ........................................................................................................ 60 IV. ENVIRONMENTAL CUES AND THE REPRODUCTIVE CYCLE OF A TEMPERATE POPULATION OF OWENIA COLLARIS (ANNELIDA: POLYCHAETA) .................................................................. 61 1. Introduction ............................................................................................... 61 2. Materials and Methods .............................................................................. 66 2.1 Natural Reproductive Cycle ............................................................... 66 2.2 Gonad Development Experiment ....................................................... 70 3. Results ....................................................................................................... 74 3.1 Natural Reproductive Cycle ............................................................... 74 3.2 Gonad Development Experiment ....................................................... 80 4. Discussion ................................................................................................
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