Key factors influencing the occurrence and frequency of ciguatera

Sparrow, Leanne (2017) Key factors influencing the occurrence and frequency of ciguatera. PhD thesis, James Cook University.

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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 °S, 20 – 25 °S, 27°S) and very recently have been recorded as far south as Merimbula (37 °S), 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 expansion of Gambierdiscus populations southward into colder coastal marine habitats.

Warmer SSTs associated with climatic events, such as El Nino 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 in Qld has not been explored previously. A desk study was conducted on ciguatera cases reported in an Australian government publicly accessible health database. Data were analysed and related to records of climate and environmental disturbances during the same period. Ciguatera cases were higher in the PDO warm phase than in the cool phase, and coral bleaching significantly lowered incidence of ciguatera cases in the year of bleaching. The large range of latitude on Qld east coast (10 – 28 °S) made identification of clear links between ciguatera outbreaks and El Nino and other disturbance events difficult to identify. Thus, drivers of Gambierdiscus population responses to environmental changes need to be identified.

Macroalgal substrate preferences of Gambierdiscus, in terms of phyla and the chemical and structural defences of macroalgae against colonisation of Gambierdiscus remain unclear. Abundances of Gambierdiscus have been reported in the northern and southern regions of the GBR, but not in the central GBR. Field surveys conducted for at inshore and mid-shelf reef sites in the central GBR investigated benthic dinoflagellate abundances and preferences of Gambierdiscus for different macroalgal substrates, based on thallus form and grazing pressures. There appeared to be no macroalgal substrate preference of Gambierdiscus, but abundance of Gambierdiscus varied with sites. In the absence of substrate preference and with the propensity of macroalgae to colonise substrates, benthic dinoflagellates are likely to expand populations southward into new geographic regions.

Temperature and salinity can physiologically challenge survival of benthic dinoflagellates and thus expansion of geographic range. On the GBR, inshore reefs experience more variable temperatures and salinities relative to reefs further offshore, and such variations are often influenced by environmental disturbances. In the central GBR, field surveys found that Gambierdiscus co-occur with high abundances of Prorocentrum and Ostreopsis, however, it remains unclear whether mixed benthic dinoflagellate assemblages have a positive effect on growth of Gambierdiscus populations in periods of environmental stress. Fully factorial experiments were conducted to investigate firstly, the effect of temperature and salinity on two strains of G. carpenteri isolated from GBR waters (NQAIF116 and NQAIF380); and secondly, the effect of salinity and the presence of a mixed benthic dinoflagellate assemblage on the population growth of the inshore G. carpenteri strain, NQAIF116. NQAIF116 showed a greater potential for range expansion southward into colder estuarine environments. Range expansion, however, would not lead to an increase in incidence of ciguatera unless the benthic dinoflagellates were taken up by resident fish populations, a possibility which requires further research.

It is thought that the summer occurrence of G. carpenteri in southern waters off Merimbula, NSW was caused by transport of the dinoflagellate by the East Australian Current (EAC), which can reach further south in a warmer climate. Temperature and salinity changes could affect the biochemical profile of Gambierdiscus species transported into more southern waters, potentially affecting their nutritional qualities, such as their long-chain polyunsaturated fatty acids (LC-PUFAs) which are essential components in marine food webs. Large-scale cultures of G. carpenteri, Prorocentrum lima and Ostreopsis sp. were set up to investigate whether temperature and salinity, which appeared to drive population growth in small-scale cultures, would affect nutritional profiles of these dinoflagellates. Culture nutrient status was kept replete for nitrate and phosphate. Growth and nutrient uptake rates of dinoflagellates were measured every second day in cultures with replete levels of nitrate and phosphate. Temperature and salinity changes had negligible effects on Total Fatty Acids (FA), Saturated Fatty Acids (SFA), Monounsaturated Fatty Acids (MUFA) and Polyunsaturated Fatty Acids (PUFA) in G. carpenteri, P. lima and Ostreopsis sp. This suggests that benthic dinoflagellates remain a good source of essential LC-PUFAs even in conditions of changed temperature and salinity. Population growth rate of P. lima (a species that has been implicated in diarrhetic shellfish poisoning) is temperature and salinity tolerant. This could have implications for oyster beds in NSW. Population growth rate of Ostreopsis was salinity-tolerant, but affected slightly by temperature, while population growth rate of G. carpenteri was temperature-tolerant, but negatively affected by lower salinity. This has implications for the potential of ciguatoxin transfer, the rate of which is considered high in offshore waters, but relatively low in inshore and estuary waters. This suggests that a useful extension of the present research would be to investigate toxin production in dinoflagellates under temperature and salinity stress.

As predicted climate change conditions will impact on coral reef health, generating more substrate on the GBR for macroalgae and associated benthic dinoflagellate assemblages to colonise. The principle aim of research in this thesis was to better understand potential drivers of ciguatera occurrence and the effect of predicted climate change on the potential range expansion of benthic dinoflagellates into new geographic regions. This was achieved by investigating ocean-scale and decadal-scale environmental changes and environmental disturbances with respect to a unique, long-term dataset on reported ciguatera cases for Qld (chapter 3), evaluating distribution and substrate preferences of potentially harmful benthic dinoflagellates (chapter 4), investigating responses to temperature and salinity changes on population growth of dinoflagellates (chapter 5) and investigating nutritional value of benthic dinoflagellates at a lower salinity and temperature, as a novel approach to evaluate potential uptake of ciguatoxins into marine food webs (chapter 6). These findings have improved our understanding of the influence of ocean-scale climatic processes in predicting ciguatera occurrence, and data suggest a potential for southward geographic expansion of ciguatera occurrence into more southern coastal environments as climate changes.

Item ID: 59145
Item Type: Thesis (PhD)
Keywords: ciguatera, climate change, coral bleaching, disease management, disturbance events, environmental drivers, fisheries, Gambierdiscus, grazers, macroalgae substrates, Ostreopsis, Prorocentrum, public health
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Copyright Information: Copyright © 2017 Leanne Sparrow.
Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 1: Heimann, Kirsten, and Sparrow, Leanne (2015) Ciguatera: Tropical Reef Fish Poisoning. In: Kim, Se-Kwon, (ed.) Handbook of Marine Microalgae: Biotechnolgy Advances. Academic Press, London, UK, pp. 547-558.

Chapter 4: Sparrow, Leanne, and Heimann, Kirsten (2016) Key environmental factors in the management of ciguatera. Journal of Coastal Research, Special Issue 75. pp. 1007-1011.

Chapter 5: Sparrow, Leanne, Momigliano, Paolo, Russ, Garry R., and Heimann, Kirsten (2017) Effects of temperature, salinity and composition of the dinoflagellate assemblage on the growth of Gambierdiscus carpenteri isolated from the Great Barrier Reef. Harmful Algae, 65. pp. 52-60.

Date Deposited: 06 Aug 2019 00:19
FoR Codes: 06 BIOLOGICAL SCIENCES > 0607 Plant Biology > 060701 Phycology (incl Marine Grasses) @ 34%
06 BIOLOGICAL SCIENCES > 0605 Microbiology > 060502 Infectious Agents @ 33%
05 ENVIRONMENTAL SCIENCES > 0502 Environmental Science and Management > 050206 Environmental Monitoring @ 33%
SEO Codes: 96 ENVIRONMENT > 9604 Control of Pests, Diseases and Exotic Species > 960402 Control of Animal Pests, Diseases and Exotic Species in Coastal and Estuarine Environments @ 35%
96 ENVIRONMENT > 9605 Ecosystem Assessment and Management > 960507 Ecosystem Assessment and Management of Marine Environments @ 35%
92 HEALTH > 9204 Public Health (excl. Specific Population Health) > 920499 Public Health (excl. Specific Population Health) not elsewhere classified @ 30%
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