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Bivalvia Carditidae) THE FLORIDA STATE UNIVERSITY COLLEGE OF ARTS AND SCIENCES REPRODUCTION IN CARD- FJ,OmANA (CONRAD) (BIVALVIA CARDITIDAE) BY MARGARET C. HARVEY A Thesis submitted to the Department of Biological Science in partial fulfillment of the requirements for the degree of Master of Science Degree Awarded Summer Semester, 1995 The members of the Committee approve the thesis of Margaret C. Harvey defended on 19 August 1994. Professor Directing Thesis Committee Member Committee Member Appproved: __L______I_______ of Biological Science ACKNOWLEDGEMENTS I would like to thank the following people for their help with various aspects of my project: S. Cook, here at the University of South Florida in Tampa, for her unlimited patience and technical expertise in formatting this manuscript; Dr. F. James, for help with the morphornetrics, and M.B. Kotrla, K. Riddle, K. Womble and also B. Barfield, of the Panama City Shell Club, for introducing me to my research site. A. Black and D. Watson were most gen- erous in their assistance with the histology. I appreciate the guidance and ad- vice of my committee members, Drs. W. Heard, R. Mariscal, L. Keller, and W. Krebs, and Dr. Heard for some financial support. I also wish to thank Dr. Krebs for both the insightful statistical consultations and his friendship. I am thankful for the $500 grant awarded to me by the Conchological Society of America and to R. Tucker Abbott for his helpful advice. I would like to thank the personnel of Tyndall Air Force Base for allowing me access to the site. Finally, I am deeply grateful for assistance in the field and especially for the unlimited patience and support of M. Palotisi Harvey. iii TABLE OF CONTENTS EXe LIST OF TABLES vi LIST OF FIGURES vii ABSTRACT ix INTRODUCTION 1 Terminology 1 Bivalvia 6 Carditacea: Carditidae: Carditamera floridana 7 MATERIALS AND METHODS 11 Individual Sexuality, Sex Ratio, Sexual Dimorphism in She11 Shape 11 Reproductive System Structure 14 Reproductive Periodicity 14 Histochemistry of Reproductive System 16 Egg Mass and Developmental Stages 17 RESULTS 18 Individual Sexuality, Sex Ratio, Sexual Dimorphism of Shell Shape 18 lndlvldualSexualitvdbW.. 18 Sexual DimorDhism in Shell Shape 18 Reproductive Periodicity 21 AnnualPeriodicitv 21 Svnchronicity Amon2 Jndividuals 25 Tcmucrature and Annual Periodicity 25 Histochemistry of the Reproductive System 31 Structure &&g Reproductive&Ska 31 Vitellov- 31 SourcesdNaturepfMucins 31 Egg Mass and Developmental Stages 35 Counts of Developinv Individuals 40 Develoomental- 40 iv DISCUSSION 43 Oviparity in the Bivalvia 43 Oviparity in Carditamera floridana and Possible Adaptive Significance 44 Individual Sexuality, Sex Ratio, Sexual Dimorphism.. in Shell Shape 47 IndlYKuSexualitvd%BiltiQ 47 Sexual Dimorphism in Shell Shape 49 Reproductive Periodicity 49 Annual- 49 Synchronicity Amone Individuals 51 Temperature and Annual Periodicity 53 Histochemistry of the Reproductive System 53 Structure of Reuroductive Svstem 53 Vitelloeenesis 54 Sourcesan8mQfMucins 55 Egg Mass and Developmental Stages 57 counts. Develouine Individuals 58 DeveloDmental- 59 APPENDIX I Compilation of Oviparous Bivalves Exhibiting Extended Care: Adult Size, Habitat, and Distribution 61 APPENDIX 11 Compilation of Oviparous Bivalves Exhibiting Extended Care: Oocyte Diameters, Notes on Reproduction and Development, and References 65 LITERAWRE CITED 71 BIOGRAPHICAL SKETCH 79 V LIST OF TABLES rn w 1. Comparison of Gonadal States of Male and 23 Female c. floridana 2. Shell Lengths of Juvenile c. floridana 24 3. Kolmogorov-Smirnov s-Sample Test; Column 28 Totals 4. Kolmogorov-Smirnov s-Sample Test 29 5. Histochemical Test Results 34 vi LIST OF FIGURES Eik3m u 1. Map of Study Site 12 2. Size-frequencies of Male and Female c. florldana 19 3. Shape Variables of Male and Female c. foridana 20 4. Reproductive Periodicity 22 5. Synchronicity of Reproduction 26 6. Mean Oocyte Diameters and Seawater Temperatures 30 7. Photo of Histologic Slide of Ovary 33 8. Photo of Histologic Slide of Ovary 33 9. Photo of Unfixed Oocyte 33 10. Photo of Histologic Slide of Ovary 33 11. Photo of Histologic Slide of Kidney 37 12. Photo of Histologic Slide of Kidney 37 13. Photo of Histologic Slide of Ovary 37 14. Photo of Histologic Slide of Ovary 37 15. Photo of C floridam with Egg Mass 39 16. Photo of G. floridana with Egg Mass 39 17. Photo of c. floridana with Egg Mass 39 18. Photo of Live c.floridma Embryo 39 vii A Eiw= 19. Adult Size and Number of Embryos 43 viii ABSTRACT Oviparous reproduction in Carditamera floridana was studied in St. Andrew's Sound, near Mexico Beach, Florida, between May 1992 and February 1994. This species is gonochoristic; the sex ratio is highly skewed toward males in the lowest size range. Shell height plays a greater role in larger fe- males' shape than in males. The reproductive cycle was monophasic between January 1993 and February 1994. Females were spent between 6 April and 6 June. Mean oocyte diameters were greatest between February and March. Synchronicity among females within a sampling period was greatest prior to the spawning event and less evident at other times. There is no evidence of a distinct vitellogenic mechanism. Mucous se- cretions from various tissues are noted and characterized. The egg mass was a sticky, mucilagenous secretion issuing from the right suprabranchial chamber. The right inner ctenidium distends so that the filaments of the ascending and descending lamellae were widely separated. The egg mass passed through the exhalant chamber to the exhalant siphon, to which it remains attached. Development is direct, with the release of crawl- away juvcniles. Density of embryos within an egg mass ranged to a high of approximately 17,000 and appeared to be correlated to some extent with the size of the adult. The egg mass deteriorates over a period of 14 days. ix This oviparous mode of deveIopment is unique in the number of ju- veniles produced, the extent of parental care involved, the subtropical range of the species, and the lack of a distinct vitellogenic mechanism. X INTRODUCTION Terminology Many marine benthic invertebrates are external fertilizers, although representatives of diverse phyla have varying strategies of oviparity, ovo- viviparity, and viviparity. Oviparity is the production of eggs that undergo development after deposition by the parent on the substrate or other firm ob- ject. Ovoviviparity is the production of eggs that undergo development within the body of the parent without a vascular connection between the par- ent and the developing young. Viviparity is production of eggs that undergo development within the body of the parent with a vascular (placental) con- nection between the parent and the developing young (Houghton, 1869). Young may be released either as larvae or juveniles (Mackie, 1984). Several classifications of different modes of larval development of ma- rine benthic invertebrates have been devised to present an integrated and useful descriptive scheme. Thorson's (1946,1950) proposal was broadIy based on the location of larval development, &., pelagic and non-pelagic. Pelagic larvae remain in the plankton throughout development. Thorson also cre- ated terms to make a distinction between larval feeding types within this group. Those larvae that rely on yolk reserves exclusively are lecitllotrophic, whereas planktotrophic larvae take nourishment from planktonic food ex- clusively. Thorson believed that the time spent feeding in the plankton is a further significant distinction. The term planktotrophy was reserved for those planktonic larvae that feed for a relatively long period of time. Nan- 1 pelagic larval developmental types included viviparous forms that were de- fined as undergoing development entirely within the parent, the young being released as juveniles (Sellmer, 1967). Also included in this groups are those larvae that develop completely within an egg-mass, feeding on either yolk re- serves of nurse eggs, and that are released in a juvenile benthic phase. Ockelmann (1965) revised the terminology and presented a classifica- tion that was based in part on studies of over 200 species of marine bivalves. He listed planktotrophic, lecithotrophic, and direct larval developmental types. Planktotrophy referred to those larvae for which feeding on plankton was imperative in order to achieve metamorphosis. Lecithotrophic larvae were stated to rely either solely on yolk reserves up until metamorphosis or to feed on plankton immediately prior to this event, although not by neces- sity. Direct development implied lecithotrophy and the lack of pelagic larval phase. Milcikovsky (1974) recognized four categories of larval development among marine benthic invertebrates: (1)pelagic (occurring in the open sea); (2) demersal (larvae capable of swimming to a limited extent and in which development occurs within the near-substrate water layer or on the substrate itself); (3) direct, and (4)viviparity, The pelagic developmental type was ex- tended to include seven subtypes based on the ecology of various species. Due to the innumerable permutations that exist, Mileikovsky acknowledged the near impossibility of establishing clear distinctions between the four types de- fined. Poccilogony, a polymorphism in development in which there is pre- sent than one distinctive kind of development within the Same sexu- ally reproducing species (Hoagland & Robertson, 1988)~comprises Yet another n L dimension in the classification of larval types. very few cases have been veri- fied, all in Polychaeta. The
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