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Proquest Dissertations Library and Archives Bibliotheque et 1*1 Canada Archives Canada Published Heritage Direction du Branch Patrimoine de I'edition 395 Wellington Street 395, rue Wellington OttawaONK1A0N4 OttawaONK1A0N4 Canada Canada Your file Votre reference ISBN: 978-0-494-80776-7 Our file Notre reference ISBN: 978-0-494-80776-7 NOTICE: AVIS: The author has granted a non­ L'auteur a accorde une licence non exclusive exclusive license allowing Library and permettant a la Bibliotheque et Archives Archives Canada to reproduce, Canada de reproduire, publier, archiver, publish, archive, preserve, conserve, sauvegarder, conserver, transmettre au public communicate to the public by par telecommunication ou par I'lnternet, preter, telecommunication or on the Internet, distribuer et vendre des theses partout dans le loan, distribute and sell theses monde, a des fins commerciales ou autres, sur worldwide, for commercial or non­ support microforme, papier, electronique et/ou commercial purposes, in microform, autres formats. paper, electronic and/or any other formats. The author retains copyright L'auteur conserve la propriete du droit d'auteur ownership and moral rights in this et des droits moraux qui protege cette these. Ni thesis. Neither the thesis nor la these ni des extraits substantiels de celle-ci substantial extracts from it may be ne doivent etre imprimes ou autrement printed or otherwise reproduced reproduits sans son autorisation. without the author's permission. In compliance with the Canadian Conformement a la loi canadienne sur la Privacy Act some supporting forms protection de la vie privee, quelques may have been removed from this formulaires secondaires ont ete enleves de thesis. cette these. While these forms may be included Bien que ces formulaires aient inclus dans in the document page count, their la pagination, il n'y aura aucun contenu removal does not represent any loss manquant. of content from the thesis. 1+1 Canada Effect of spatial and environmental factors on the reproductive cycle of the brittle star, Ophiopholis aculeata, based on a new maturity stage index By ©Gina Doyle A thesis submitted to the School of Graduate Studies in partial fulfillment of the requirements for the degree of Master of Science Ocean Sciences Centre and Department of Biology, Memorial University, St. John's (Newfoundland and Labrador) Canada 10 February 2011 Abstract Monthly collections of the brittle star Ophiopholis aculeata were made and individuals were analyzed using traditional methods (gonad indices, gametogenic stages and oocyte diameters), along with a newly developed quantitative method coined the 'maturity stage index' (MSI). The MSI was statistically related to conventional methods of studying reproduction, but provided greater sensitivity for fine-scale and inter-individual comparisons. This allowed the study of reproductive synchrony in O. aculeata over several scales: (1) within a given habitat, (2) between adjoining habitats, (3) among individuals in each habitat, and (4) within and among natural clusters of individuals. Complementary laboratory trials were conducted to further examine the influence of temperature and spatial distribution on gametogenesis. Ophiopholis aculeata exhibited an annual gametogenic cycle with spawning in late summer. Significant differences were seen between habitats and among individuals in certain months, and synchrony was generally greater around the time of spawning and in nearby/grouped individuals. Laboratory experiments indicated that temperature is unlikely to act as a proximate reproductive cue, and phytoplankton is probably the major environmental factor mediating the annual reproduction of O. aculeata. Together, field and laboratory findings further evidenced the synergistic roles of exogenous factors and inter-individual communication in coordinating the reproductive cycle of marine invertebrates. ii Acknowledgements I would like to thank my supervisor Annie Mercier, as well as Jean-Frangois Hamel, for all their guidance throughout the process of researching and writing my thesis. Their patience, passion, support and wisdom were the pillars of this project, and I cannot thank them enough for always knowing how to encourage me. I would also like to thank my committee member Bob Hooper, for supporting me in a million different ways, from helping with field work, to coordinating my graduate research course, to all the encouraging meetings, emails and phone calls. I attribute my sanity to you. Thanks to my committee member Dave Innes and to all anonymous reviewers, for their hard work on manuscript and thesis revisions and for helping me realize the potential of my research. Thanks to Patrick Gagnon, for his financial and logistical support with field work. I am indebted to the following people, who have generously assisted me in various ways throughout my research and analysis process: Ocean Sciences Centre Laboratory Services (Jim Deveraux, Jerry Ennis, Damian Whitten, Danny Au, Matthew Pittman), OSC Field Services (Bob O'Donnell, Phil Sargent, William Coffey), the Marine Institute's Centre for Aquaculture and Development (especially Heather Manual, Chris Dawe and Jason Nichols), Connie Short, Judy Foote, Robert Guest, Don Deibel, Ray Thompson, Kyle Matheson, Scott Caines, Christine Vickers and Nikita Laite. iii Special thanks to Justin So and Zhao Sun, for showing me the ropes in grad school and for all their help in the lab these past few years. I also appreciate the support of my family and friends in both my personal and professional lives. Finally, a huge thank you to William Coffey, for tolerating/encouraging/indulging me these past few years, for all his love, patience, and good cooking, and for always being there to listen. IV Table of Contents Abstract ii Acknowledgements iii Table of Contents v List of Tables viii List of Figures ix List of abbreviations and symbols xv Co-authorship statement xvi Chapter 1 - Introduction 1-1 1.1 Reproductive biology of benthic invertebrates 1-1 1.2 The study of reproductive periodicity and synchrony in echinoderms 1-2 1.3 The reproductive biology of ophiuroids 1-5 1.4 The biology and reproduction of Ophiopholis aculeata 1-9 1.5 Research objectives 1-12 1.6 References 1-13 Chapter 2 - A quantitative study of ovarian development in an ophiuroid and a holothuroid using a newly developed maturity index 2-1 2.1 Abstract 2-1 2.2 Introduction 2-2 2.3 Materials and methods 2-7 2.3.1 Sample collection 2-7 2.3.2 Biometrical analysis 2-8 2.3.3 Traditional methods 2-8 2.3.4 Maturity stage index (MSI) 2-11 2.3.5 Applicability using another species 2-13 2.3.6 Statistical analyses 2-14 2.4 Results 2-14 2.4.1 Comparison of MSI obtained with different formulas 2-15 2.4.2 Comparison between MSI and other methods 2-17 v 2.4.3 Determination of MSI in another species 2-17 2.5 Discussion 2-18 2.6 Acknowledgements 2-26 2.7 References 2-27 2.8 Tables 2-33 2.9 Figures 2-34 Chapter 3 - Influence of spatial distribution and environmental factors on the reproduction of the brittle star Ophiopholis aculeata (Echinodermata: Ophiuroidea) 3-1 3.1 Abstract 3-1 3.2 Introduction 3-2 3.3 Materials and methods 3-11 3.3.1 Sample site 3-11 3.3.2 Reproductive cycle in rock and rhodolith habitats 3-11 3.3.3 Laboratory experiments 3-13 3.3.4 Biometrical analysis 3-16 3.3.5 Gonad index 3-17 3.3.6 Histology 3-17 3.3.7 Quantitative analysis of oogenesis 3-18 3.3.8 Statistical analyses 3-19 3.4 Results 3-20 3.4.1 Sex ratio 3-20 3.4.2 Maturity Stage Index (MSI) 3-20 3.4.3 Field study - rock and rhodolith habitats 3-20 3.4.4 Laboratory study 3-29 3.4.5 Environmental parameters 3-34 3.5 Discussion 3-35 3.6 Acknowledgements 3-48 3.7 References 3-49 3.8 Figures 3-59 VI Chapter 4 - Conclusions and perspectives 4-1 4.1 Major findings 4-1 4.2 Main issues and possible solutions 4-4 4.3 Future research 4-8 4.4 References 4-11 Appendix A - Male gametogenic stages in Ophiopholis aculeata 5-1 VII List of Tables Table 2-1. Research methods used in various studies on ophiuroid reproduction, where 'Gl' represents gonad indices, 'staging' represents the use of visual gametogenic stages, 'Ml' represents a qualitative maturity index, and 'OSFD' represents oocyte size frequency distribution. This list provides only some of the most recent studies, and is not exhaustive 2-33 VIII List of Figures Figure 2-1. Oogenic stages in female Ophiopholis aculeata, where A = early growth (with oogonia [O] growing from the germinal epithelium [GE]), B = growth (with early vitellogenic [EV] oocytes), C = mature (with vitellogenic [V] oocytes, and D= spent (with residual [R] oocytes). Scale bar represents 400 urn 2-34 Figure 2-2. Maturation stage indices (MSI) obtained with the different formulas with corresponding oogenic stages of Ophiopholis aculeata, where EG = earth growth, G = growth, M = mature, and S = spent. Data presented as mean +standard error, n = 5-53 2-35 Figure 2-3. Mean MSI of female Ophiopholis aculeata (± standard error; n = 8-16) with corresponding proportion of individuals in each oogenic stage (early growth, growth, mature and spent; n = 5-53) throughout the sampling period 2-36 Figure 2-4. Plots of oocyte density (oocytes • mm'2), oocyte diameter (urn), gonad index (% wet weight) and maturity stage index (MSI) across oogenic stages for Ophiopholis aculeata, where EG = early growth, G = growth, M = mature, and S = spent. In the box plots, the horizontal line shows the median, the lower and upper limits of the boxes represent the 25th and 75th percentiles, whiskers represent the 10th and 90th percentiles and outliers appear as open circles. The scatter plot shows mean and standard error, n = 5-53.
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