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Key Factors Influencing the Occurrence and Frequency of Ciguatera ResearchOnline@JCU This file is part of the following work: Sparrow, Leanne (2017) Key factors influencing the occurrence and frequency of ciguatera. PhD Thesis, James Cook University. Access to this file is available from: https://doi.org/10.25903/5d48bba175630 Copyright © 2017 Leanne Sparrow. The author has certified to JCU that they have made a reasonable effort to gain permission and acknowledge the owners of any third party copyright material included in this document. If you believe that this is not the case, please email [email protected] SPARROW, LEANNE B.Arts – Town Planning B.Sc – Marine Biology; M.App.Sc – Phycology KEY FACTORS INFLUENCING THE OCCURRENCE AND FREQUENCY OF CIGUATERA Doctor of Philosophy College of Science and Engineering James Cook University Submitted: 30 July 2017 Acknowledgements The production of this thesis is the end of a long and challenging journey. While I have endured numerous challenges, I have also gained so much more in experiences along the way – there have been so many wonderful people that I had the fortune to meet through tutoring, work and research. Firstly, I would like to acknowledge my supervisors for their support and contributions to experimental design and editorial advice. In particular I would like to thank Kirsten Heimann, apart from her intellectual guidance and support, she has provided emotional, financial, mentoring and friendship over the years prior and during this research – thank you. I would also like to thank Garry Russ and Leone Bielig for the guidance and the supportive chats that kept me sane towards the end. Out in the field the support and interest of the then managers, Kylie and Rob at Orpheus Island Research Station was greatly appreciated. To my 23 volunteers, although most enjoyed glassy conditions on the reef, some experienced a little more in the wet season and I thank you for your enthusiasm, interest, dedication to the combined long hours in the field followed by the wet laboratory and the enjoyable dinners. A particular mention to Nicolas von Alvensleben, who volunteered on all field trips to Orpheus Island, his experience in diving and also prepared dinners for all each night; Kirsten Heimann for her efforts in the field although your wetsuit kept you afloat; Brent King for preparing the boats for the morning tides; Paolo Momigliano for your experience as a diver and morning coffees; Janine Sheaves who volunteered to ii drive the vehicle to and from Taylor’s Beach for the start and end, but also for additional supply drop offs and tired volunteer pickups in the mid-trip transitions, thank you. I would also like to thank Kim Buckle for making those monthly field trips to Magnetic Island enjoyable – working quickly to collect samples before the change in tides at Horseshoe and Nelly Bays, searching for fluorescent pink tape in the Horseshoe Bay sediments, island hire cars – they were some of the magic moments. My journey started with a dream, one that was supported by my parents who were unable to live theirs. My sister gave me strength, wisdom and determination. Without my daughter, I would not have appreciated the joyful moments or survived the trials, hardships and endured the challenges. I am grateful to have the unyielding support and encouragement from my daughter. For this reason, this thesis is dedicated to my mother Mary Sparrow, my sister, Angela along with my amazing daughter, Shauna Leigh and in the loving memory of my father, Alfred Brian Sparrow. iii Statement of the contributions of others My research benefitted from the intellectual and editorial support of my supervisors, Assoc. Prof. Kirsten Heimann, Prof. Garry Russ and Prof. David Blair. Financial support for this research was provided by James Cook University (JCU) College of Science and Engineering. Field sampling for this research was funded through a grant to Assoc. Prof. Kirsten Heimann by the Australian Government’s Marine and Tropical Science Research Facility (MTSRF) Project 2.6.1 – Understanding threats and impacts of invasive pests on the Great Barrier Reef. The author was granted funding from the Australian Geographic Society. This research benefitted from the editorial support of Leone Bielig and statistical support by Prof. Rhondda Jones. Access to the North Queensland Algal Identification and Culturing Facility (NQAIF) was crucial for laboratory work, including microalgal isolation, culturing and maintenance as well as microscopy and experimental work. Mr Stanley Hudson isolated and maintained cultures of benthic toxic dinoflagellates as well as provided training in culture techniques. The table below documents the contribution and extent of intellectual input of each author, including the candidate (Sparrow, Leanne), shown in bold face. iv Chapter Details of publication Nature and extent of the contribution No. on which chapter is of each author, including the based candidate 1 Heimann, K. and Sparrow, Both authors contributed equally to the L. (2015) Chapter 37: In: development of the book chapter, including data Kim, S.-K. [ed] Handbook collecting, draft and editoral as well as preparation of Marine Microalgae of figures and tables. Biotechnology Advances. Elsevier, London, pp. 547- 558 2 Sparrow, L., Heimann, K., Heimann and Sparrow collected the data. Bielig, L., Capper, A., and Sparrow drafted the paper which was revised Blair, D. (in prep). Marine with editorial input from Heimann, Bielig, Capper and Freshwater Research and Blair. Sparrow developed the figures and tables, except Figure which was developed by Sparrow and Capper. 3 Sparrow, L., Heimann, K., Sparrow developed the research question. Data and Connolly, S. R. (in collected by Heimann and Sparrow. Modelling prep). Harmful Algae performed by Connolly. Sparrow drafted the paper which was revised with editorial input from Heimann and Connolly. Sparrow developed figures and tables, excluding modelling tables, which were developed by Connolly. 4 Sparrow, L. and Heimann, Sparrow and Heimann developed the research K. (2016). Journal of question. Sparrow collected field data with Coastal Research, assistance by numerous volunteers. Sparrow 75:1007-1011. performed data analysis, and prepared figures and tables. Sparrow drafted the paper with editorial input from Heimann. 5 Sparrow, L., Momigliano, Sparrow and Heimann developed the research P., Russ, G. R., and question. Sparrow collected the data and Heimann, K. (2017). performed the data analysis with assistance from Harmful Algae 65:52-60 Russ and Empro. Rhondda Jones. Momigliano performed genetic analysis. Sparrow drafted the paper with editorial input from Momigliano, Russ and Heimann. Sparrow developed the figures and tables, except for phylogeny tree which was prepared by Momigliano. 6 Sparrow, L., von Sparrow and Heimann developed the research Alvensleben, N., de Royer, question. Sparrow collected the data with A., and Heimann, K. assistance from de Royer and von Alvensleben. (submitted). Journal of Sparrow and Heimann performed the data experimental marine analysis. Sparrow drafted the paper with editorial biology and ecology input from Heimann, von Alvensleben and de Royer. Figures and tables developed by Sparrow with assistance from Heimann. v Abstract Ciguatera is a human illness caused by ingestion of toxic dinoflagellates. It is endemic to tropical regions, but has expanded globally, facilitated by increased tourism to the tropics and the distribution of frozen fish from the tropics. Fish sourced from the Great Barrier Reef (GBR) and Queensland (Qld) coastal waters are the primary source of ciguatera in Australia, however, environmental drivers of ciguatera remain poorly understood. The main causative dinoflagellate genus, Gambierdiscus, produce ciguatoxins that bioaccumulate through marine food webs. Gambierdiscus species are frequently found on macroalgal substrates and usually co-occur with other benthic dinoflagellates, such as Prorocentrum and Ostreopsis. Gambierdiscus species have been recorded in the GBR (17 ºS, 20 – 25 ºS, 27ºS) and very recently have been recorded as far south as Merimbula (37 ºS), New South Wales (NSW). Eco- physiological drivers for population range expansions are unknown, but increasing sea surface temperatures (SSTs) might facilitate range expansion south. Climate change scenarios predict an increase in frequency and intensity of warmer than average periods and environmental disturbances, which will impact coral reef health. The response of Gambierdiscus and the flow-on effect on ciguatera incidence under predicted climate change conditions are unknown for Qld. The main objective of this thesis was to contribute to the current state of knowledge on ciguatera in Qld, Australia. The focus was on the potential effect of climate, i.e. increased SSTs and environmental stressors, specifically changes in salinity, on the occurrence of ciguatera and the potential for range vi expansion of Gambierdiscus populations southward into colder coastal marine habitats. Warmer SSTs associated with climatic events, such as El Niño and the Pacific Decadal Oscillation (PDO) have been linked to increases in ciguatera incidence for several island nations in the South Pacific region. Coral bleaching is often triggered by warmer SSTs, while disturbances from cyclones and crown-of- thorns starfish (Acanthaster planci) outbreaks frequently co-occur, providing new substrates for macroalgae and associated benthic dinoflagellates to colonise. The effect of altered climate and environmental disturbances on the occurrence of ciguatera
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