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Sexual Reproduction and Bloom Dynamics of Toxic Dinoflagellates

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SEXUAL REPRODUCTION AND BLOOM DYNAMICS OF TOXIC DINOFLAGELLATES FROM AUSTRALIAN ESTUARINE WATERS by Naomi S. Parker BSc., Grad. Dip. ASOS (Hons), MSc. Submitted in fulfillment of the requirements for the degree of Doctor of Philosophy School of Aquaculture University of Tasmania Hobart June,2002 DECLARATION AND AUTHORITY OF ACCESS This thesis contains no material which has been accepted for the award of a degree or a diploma in any university, and to the best of the author's knowledge and belief, the thesis contains no material previously published or written by another person, except where due acknowledgement is made in the text. This thesis may be made available for loan. Copying of any part of this thesis is prohibited for two years from the date this statement was signed; after that time limited copying is permitted in accordance with the Copyright Act 1968. Naomi S. Parker June 2002 ABSTRACT Of the dinoflagellates known to form toxic blooms in Australian estuaries three, Alexandrium minurum, Alexandrium catenella and Gymnodinium catenatum produce paralytic shellfish toxins that can lead to the potentially fatal paralytic shellfish poisoning in humans. These three species and a fourth dinoflagellate Protoceratium reticulatum all have the capacity to reproduce both by vegetative cell division and by sexual reproduction. The product of sexual reproduction in all cases is a resting cyst, which can sink to the sediments and remain dormant for a time. Resting cyst production results in a coupling between the benthic and pelagic components of estuarine systems and forms an important part of the ecological strategy of dinoflagellates. A variety of aspects of sexual reproduction of these four species were investigated. These included: life cycle description (A. minutum); mating system studies (all four species); assessing the use of sexually compatible strains in high biomass culture systems (A. minutum); experimental studies of encystment and excystment cues (A, minutum and G. catenatum); and a three-year field study of vegetative and sexual reproduction of G. catenatum in an estuary in south-east Tasmania. The complete life cycle of A, minutum was described and was found to be similar to other Alexandrium species. Alexandrium minutum was also found to produce temporary resting cysts in response to cold shock and to have a short (approximately 4 weeks) minimum requisite dormancy period. The mating systems of all four species were investigated. Alexandrium catenella strains from three Australian populations were found to have simple heterothallic mating systems with essentially two mating types. The other three species all had mating systems of greater complexity with gradients of affinity between strains rather than discrete mating types. These mating type affinities were also found to vary over years in A. minutum and G. catenatum. Cluster analysis was demonstrated to be a useful method for describing these gradients. Encystment and excystment of A. minutum and G. catenatum involves both biological and environmental factors. Both these dinoflagellates had defined temperature ranges.. for encystment and excystment and evidence was found for the action of pheromone-like substances in encystment. Low irradiance and low nutrients influenced encystment, and nutrient depletion had a greater effect on encystment of A, minutum than of G. catenatum. The influence of algicidal bacteria on both encystment and excystment was tested for the first time and found to have no effect while low oxygen and low light greatly reduced excystment. The capacity for sexual reproduction by A, rninutum did not significantly effect biomass production in high biomass culture systems while growth rate increased with aeration. In the three year field study, four G. catenatum blooms were observed, two in summer and two in autumn. Sexual reproduction occurred throughout summer blooms but was below detection levels in autumn blooms and probably controlled by temperature. The importance of river flow for dinoflagellate blooms in this system was identified. Dinoflagellate blooms, including G. catenatum, were absent in the first year of the study which may be attributed to increased flushing of the estuary due to high and persistent flow of the Huon River in that year which may also have reduced diatom biomass and subsequent nutrient remineralisation. A dual strategy for the contribution of resting cysts in this system is suggested whereby frequent germination of resting cysts from shallow sediments contributes to bloom populations and overwintering biomass while deeply buried and rarely resuspended resting cysts contribute to long-term survival of the population in the estuary. The results of all investigations for A. minutum and G. catenatum were synthesised into conceptual frameworks of sexual reproduction and bloom dynamics within natural systems. ACKNOWLEDGEMENTS Peter Thompson - Many thanks for all the stimulating scientific discussions, for sharing your wealth of knowledge, and for your encouragement and support. Susan Blackburn - Many thanks for all your work in nurturing both the scientist and the person. Thanks also for your encouragement and advice and for being excited about my research. Kerrie Swadling - Thankyou so much for your advice, support, encouragement, and in particular for your expertise on all things statistical. The staff of Tassal Killala Bay and Tas Blue Mussels - My thanks for all the field work support and for sharing your 'on the ground' expertise with me. Andrew Negri -My thanks for advice and discussions on toxins and toxin analysis and for very prompt return of drafts! Lesley Clementson - Thanks for all the help with the Huon Study, and in particular for your pigment and Access expertise. Pru Bonham -Many thanks for all those cell counts in the first two years, for phytoplankton discussions and enjoyable field trips. The Huon Estuary Study Team - Thanks for providing a great field work environment, in particular thanks to Pru Bonham, Ali Turnbull, Kate Beny, Ros Watson, Don McKenzie, and John Parslow. Mario Tredici and Liliana Rodolfi - My thanks for introducing me to the world of photobioreactors and the beauty of Toscana. Funding - Thanks to CSIRO Marine Research for financial support of my research, in particular for awarding me a top-up scholarship, which enabled me to attend two conferences in Italy and to generally live a little more comfortably. Thanks also to FRDC and LWRRDC for partial funding. Thanks to those who helped with final editing of chapters, Phillip, Ian and Alicja. Jennifer Skerratt - Many thanks for support, encouragement, your companionship during field work, snorkelling, and conferences and for collaboration on the algicidal bacteria experiments. Phillip Tracey -Thanks for the support, the encouragement, the editing, for putting up with me and for oh so many dinners! Kirsten LeMar -Thanks for so much support and understanding and the afternoon cuppas at Fullers. ~ieka'~abart- Thanks for being a great housemate and a wonderful friend - it's the end of a long road, my thanks to you for helping me along it. To my fellow PhD sufferers - Jen, Phil, Kirsten, Thomo, Ross, Martina, Lynda, Richard, Malcolm - for being in the struggle and for showing me it is possible. Fi, Mal, Zoe and Sam - What would I do without you, thanks for the meals, the smiles, the hugs and the warmth of your welcome. Mum, Dad, Andrew, Jillian, Sophie, Lucy and Abby - Thanks for your constant love and support. Jeannie and Cathy - thanks for all your logistic support and for running a very efficient lab! The coffee club - Dion, Ian, Mal, Mal, Stan, Stefano, and Richard - Many thanks for stimulating afternoon conversations, support, laughter, and for helping me stay sane. The Saturday morning coffee crew - Thomo, Scotty, Jen, Phil, Kirsten, Litz, Anth, Goldie, Belinda, Russel, Shavawn, Nev, Kim, Al, Denbeigh, Andrew, etc. etc. you know who you are. Thanks for making Saturday mornings relaxing and enjoyable. Malcolm Brown, Peter Thompson, Sue Blackburn, Dick Martin, Andy Revill, the National Oceans Ofice and the Cookie Consumers -Thanks for the interesting part-time projects which supported me through the final year. Miscellaneous thanks to - Tas Coffee Roasters, Fullers and the Afterword Cafk, Machine Laundry Cafe, and The Retro. DEDICATION This thesis is dedicated to my Grandfather, Ira Mark Parker - who helped me to realise that there's a fascinating world out there and its not as big as it looks - I've finally finished Grandpa! TABLE OF CONTENTS DECLARATIONS ABSTRACT iii ACKNOWLEDGMENTS TABLE OF CONTENTS vii CHAPTER 1: INTRODUCTION GENERALINTRODUCTION 1.1 Reproduction of Dinoflagellates 1.2 Sexual Reproduction of Dinoflagellates 1 -2.1 Mating Systems 1.2.2 Encystrnent 1.2.3 Excystment 1.3 The Role of Sexual Reproduction in the Bloom Dynamics of Dinoflagellates 1.4 ' Australian Toxic Dinoflagellates 1.5 Gymnodinium catenatum 1.6 Alexandrium minutum 1.7 Alexandrium catenella 1 .S * Protoceratium reticulatum RESEARCH AIMSAND CHAPTERSUMMARY REFERENCES CHAPTER 2: THE SEXUAL LIFE CYCLE OF THE TOXIC DINOFLAGELLATE ALEXANDRIUM MINUTUM (DINOPHYCEAE) FROM THE PORT RIVER ESTUARY, SOUTH AUSTRALIA 29 INTRODUCTION 30 METHODS 3 1 2.1 Strain Details 3 1 2.2 Life Cycle Observations 32 2.2.1 Resting Cyst Formation 32 2.2.2 Resting Cyst Germination 32 RESULTS 33 2.3 Life Cycle Observations 33 DISCUSSION 37 , REFERENCES 42 CHAPTER 3: DINOFLAGELLATE MATING SYSTEMS . INTRODUCTION MATERIALSAND METHODS 3.1 Strain Details 3.2 Mating System Determination 3.3 Crossing
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