Ocean Surface Warming: Impact on Toxic Benthic Dinoflagellates Causing Ciguatera

Abstract

Ciguatera reef fish poisoning is a debilitating human illness in tropical and some subtropical regions. Toxic precursors produced by tropical benthic dinoflagellates are bio‐converted to often more potent toxins and bioaccumulate via the food web in highly sought after table fish. Rising sea surface temperatures are predicted to induce phase shifts on coral reefs. These changes offer increased substrate availability for benthic, toxic dinoflagellates such as Gambierdiscus, Ostreopsis, Prorocentrum and Coolia spp. resulting in range expansions of the causative agents of ciguatera. Ocean currents critically shape the chemical and physical ocean – and coastal environments. Climate change affects wind patterns, which strengthens the East Australian Current forcing warm tropical waters further south. This in turn allows range expansions of ciguatera‐associated dinoflagellates and presumably toxin vectors into nonendemic coastal regions changing the ciguatera‐risk profile for humans and regional and commercial fisheries in affected coastal areas.

Key Concepts:

  • Ciguatera is a human illness induced by trophically converted and accumulated dinoflagellate precursor toxins in sought after tropical – subtropical table fish.

  • Ciguatera‐causing toxins are lipid soluble and heat stable.

  • Climate change leads to rises in sea surface temperatures affecting weather patterns and coastal ecosystems.

  • Climate‐induced ecosystem changes offer new routes for range expansions of toxic, benthic, tropical dinoflagellates and likely toxin vectors through increased suitable substrate availability and geographical expansion of optimal growth temperature.

  • Expansion of toxic dinoflagellates and associated vector species into nonendemic coastal regions has significant socioeconomic implications for humans and fisheries in affected areas.

Keywords: climate change; harmful microalgae; sea surface temperatures (SST); dinoflagellate Gambierdiscus toxicus; ciguatera and ciguatoxins (CTX); marine toxins; global warming; Southern Oscillation Index; East Australian Current (EAC)

Figure 1.

Schematic overview of ocean currents in oceanic regions with endemic ciguatera.

Figure 2.

Schematic overview of oceanic currents off the east coast of Australia and associated sea surface temperature (SST) zones for in current temperatures (black numbers) and surrounding water temperatures (white numbers). (a) Wet season data of SST from mid November 2002 to mid April 2003. (b) Dry season data of SST from mid April to mid November 2003. Data for this figure were derived from the remote‐sensing project conducted by CSIRO between October 1993 and June 2004 (http://www.marine.csiro.au/remotesensing/oceancurrents/delayed/Au_taMS11/#2002).

Figure 3.

Schematic diagram of trophic transfer routes of precursor toxins (gambiertoxins) and biotransformed ciguatoxins (CTX) in marine food webs showing potential toxin vector species involved in ciguatera fish poisoning (CFP).

close

References

Aligizaki K, Nikolaidis G and Fraga S (2008) Is Gambierdiscus expanding to new areas? Harmful Algae 36: 6–7.

Angibaud G, Lévêque J‐M, Laurent D and Gaultier C (2000) Neurological features after consumption of a variety of New Caledonian shellfish (Tectus pyramis). Revue Neurologique 156: 65–66.

Arena P, Levin B, Fleming LE, Friedman MA and Blythe D (2004) A pilot study of the cognitive and psychological correlates of chronic ciguatera poisoning. Harmful Algae 3: 51–60.

Bomber JW, Morton SL, Babinchak JA, Norris DR and Morton JG (1988) Epiphytic dinoflagellates of drift algae – another toxigenic community in the ciguatera food‐chain. Bulletin of Marine Science 43: 204–214.

Botana LM (2000) Seafood and Freshwater Toxins: Pharmacology, Physiology, and Detection. New York: CRC‐Press, 798 pp.

Bruslé J (1997) Ciguatera Fish Poisoning: A Review. Sanitary and Economic Aspects. Paris: Editions INSERM, 147 pp.

Chateau‐Degat ML, Chinain M, Cerf N et al. (2005) Seawater temperature, Gambierdiscus spp.variability and incidence of ciguatera poisoning in French Polynesia. Harmful Algae 4: 1053–1062.

Chinain M, Faust M and Pauillac S (1999) Morphology and molecular analysis of three toxic species of Gambierdiscus (Dinophyceae): G. pacificus, sp. nov., G. australis, sp. nov., and G. polynesiensis, sp. nov. Journal of Phycology 35: 1282–1296.

Colman JR, Dechraoui M‐YB, Dickey RW and Ramsdell JS (2004) Characterization of the developmental toxicity of Caribbean ciguatoxins in finfish embryos. Toxicon 44: 59–66.

Davin WT Jr, Kohler CC and Tindall DR (1988) Ciguatera toxins adversely affect piscivorous fishes. Transactions of the American Fisheries Society 117: 374–384.

Donati AC (2006) Ciguatera poisoning. Fishnote, Northern Territory Government 41: 6.

Edmunds JSG, McCarthy RA and Ramsdell JS (1999) Ciguatoxin reduces larval survival in finfish. Toxicon 37: 1827–1832.

Figueira WF and Booth DJ (2010) Increasing ocean temperatures allow tropical fishes to survive overwinter in temperate waters. Global Change Biology 16: 506–516.

Flemming LE, Broad K, Clement A et al. (2006) Oceans and human health: emerging public health risks in the marine environmnet. Marine Pollution Bulletin 53: 545–560.

Garrard S, Heimann K and Blair D (2008) Assessment of the Threat of Toxic Microalgal Species to the Great Barrier Reef World Heritage Area. Literature review, Reef and Rainforest Research Centre Limited, Cairns.

Gillespie NC, Holmes MJ, Burke JB and Doley J (1985) Distribution and periodicity of Gambierdiscus toxicus in Queensland, Australia. In: Anderson DM, White AW and Baden DG (eds) Toxic Dinoflagellates, pp. 183–188. New York: Elsevier.

Gillespie NC, Lewis RJ, Pearn JH et al. (1986) Ciguatera in Australia – occurrence, clinical‐features, pathophysiology and management. Medical Journal of Australia 145: 584–590.

Hales S, Weinstein P and Woodward A (1999) Ciguatera (fish poisoning), El Nino, and Pacific sea surface temperatures. Ecosystem Health 5: 20–25.

Hall GV, D'Souza RM and Kirk MD (2002) Foodborne disease in the new millennium: out of the frying pan and into the fire? Medical Journal of Australia 177: 614–618.

Hallegraeff GM (2010) Ocean climate change, phytoplankton community responses, and harmful algal blooms: A formidable predictive challenge. Journal of Phycology 46: 220–235.

Hallegraeff GM and Bolsch CJ (1991) Transport of toxic dinoflagellate cysts via ships’ ballast water. Marine Pollution Bulletin 22: 27–30.

Halpern BS, Walbridge S, Selkoe KA et al. (2008) A global map of human impact on marine ecosystems. Science 319: 948–952.

Hays GC, Richardson AJ and Robinson C (2005) Climate change and marine plankton. Trends in Ecology & Evolution 20: 337–344.

Heil CA, Glibert PM and Fan CL (2005) Prorocentrum minimum (Pavillard) Schiller – a review of a harmful algal bloom species of growing worldwide importance. Harmful Algae 4: 449–470.

Heimann K, Sparrow L, Blair D (2008) MTSRF 2.6.1. Report on recorded ciguatera poisoning incidents, distribution, and seasonality based on analysis of database records in fishbase and compiled by the OzFoodNet Working Group. Ciguatera Database Review October 2008‐10‐07.

Hoegh‐Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine and Freshwater Research 50: 839–866.

Hughes L (2003) Climate change and Australia: trends, projections and impacts. Austral Ecology 28: 423–443.

Kelly AM, Kohler CC and Tindall DR (1992) Are crustaceans linked to the ciguatera food‐chain? Environmental Biology of Fishes 33: 275–286.

Kohler ST and Kohler CC (1992) Dead bleached coral provides new surfaces for dinoflagellates implicated in ciguatera fish poisonings. Environmental Biology of Fishes 35: 413–416.

Lewis ND (1986) Epidemiology and impact of ciguatera in the Pacific: a review. Marine Fishery Review 48: 6–13.

Lewis RJ (1992) Ciguatoxins are potent ichthyotoxins. Toxicon 30: 207–211.

Lewis RJ (2006) Ciguatera: Australian perspectives on a global problem. Toxicon 48: 799–809.

Lewis RJ and Holmes MJ (1993) Origin and transfer of toxins involved in ciguatera. Comparative Biochemistry and Physiology C‐Pharmacology Toxicology and Endocrinology 106: 615–628.

Llewellyn LE (2010) Revisiting the association between sea surface temperature and the epidemiology of fish poisoning in the South Pacific: reassessing the link between ciguatera and climate change. Toxicon 56: 691–697.

Lough JM (2000) 1997–98: unprecedented thermal stress to coral reefs? Geophysical Research Letters 27: 4–8.

Lucas RE, Lewis RJ and Taylor JM (1997) Pacific ciguatoxin‐1 associated with a large common‐source outbreak of ciguatera in East Arnhem Land, Australia. Natural Toxins 5: 136–140.

Matsuoka K, Joyce LB, Kotani Y and Matsuyama Y (2003) Modern dinoflagellate cysts in hypertrophic coastal waters of Tokyo Bay, Japan. Journal of Plankton Research 25: 1461–1470.

McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18: 357–367.

McCormack G (2007) Cook Islands Biodiversity Database. Version 2007.2. Rarotonga: R. Cook Islands Natural Heritage Trust, http://cookislands.bishopmuseum.org.

Morton SL, Norris DR and Bomber JW (1992) Effect of temperature, salinity and light‐intensity on the growth and seasonality of toxic dinoflagellates associated with ciguatera. Journal of Experimental Marine Biology and Ecology 157: 79–90.

National Research Council (NRC) (1999) From Monsoons to Microbes: Understanding the Ocean's Role in Human Health. Washington: National Academic Press, 132 pp.

Oke PR and Middleton JH (2001) Nutrient enrichment off Port Stephens: the role of the East Australian Current. Continental Shelf Research 21: 587–606.

Ridgway K and Hill K (2009) The East Australian Current. In: Ploczanska ES, Hobday AJ and Richardson AJ (eds) A Marine Climate Change Impacts and Adaptation Report Card for Australia 2009. NCCARF Publication 05/09. Available at http://www.oceanclimatechange.org.au/content/index.php/site/report_card_extended_2/category/east_australian_current.

Ridgway KR (2007) Long‐term trend and decadal variability of the southward penetration of the East Australian Current. Geophysical Research Letters 34.

Shears NT and Ross PM (2009) Blooms of benthic dinoflagellates of the genus Ostreopsis; an increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae 8: 916–925.

Sumner J and Ross T (2002) A semi‐quantitative seafood safety risk assessment. International Journal of Food Microbiology 77: 55–59.

Tester PA, Feldman RL, Nau AW, Kibler SR and Litaker RW (2010) Ciguatera fish poisoning and sea surface temperatures in the Caribbean Sea and the West Indies. Toxicon 56: 698–710.

Tosteson TR, Ballantine DL and Durst HD (1988) Seasonal frequency of ciguatera barracuda in southwest Puerto Rico. Toxicon 26: 795–801.

Vasconcelos V, Azevedo J, Silva M and Ramos V (2010) Effects of marine toxins on the reproduction and early stages development of aquatic organisms. Marine Drugs 8: 59–79.

Wong C‐K, Hung P, Lee KLH and Kam K‐M (2005) Study of an outbreak of ciguatera fish poisoning in Hong Kong. Toxicon 46: 563–571.

Further Reading

Duarte P and Santana‐Casiano JM (2010) Oceans and the Atmospheric Carbon Content. Berlin: Springer 176 pp.

Hallegraeff GM, Bolch CJS, Hill DRA et al. (2010) Algae of Australia: Phytoplankton of Temperate Coastal Waters. Algae of Australia Series. Canberra, Melbourne: ABRS, Canberra & CSIRO Publishing Melbourne, 432 pp.

Houghton J (2009) Global Warming: The Complete Briefing, 4th edn. Cambridge: Cambridge University Press, 438 pp.

Johnson R (2008) Investigating Climate Change: Scientists’ Search for Answers in a Warming World. Minneapolis, MN: Lerner Publishing, 112 pp.

Kininmonth W (2004) Climate Change: A Natural Hazard. Essex, UK: Multi‐Science Publishing Co Ltd. 207 pp.

Lau WKM and Waliser DE (2011) Intraseasonal Variability in the Atmosphere–Ocean Climate System. Berlin and Heidelberg: Springer Verlag, 436 pp.

Liss PS and Duce RA (2005) The Sea Surface and Global Change. Cambridge: Cambridge University Press, 519 pp.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Heimann, Kirsten, Capper, Angela, and Sparrow, Leanne(Nov 2011) Ocean Surface Warming: Impact on Toxic Benthic Dinoflagellates Causing Ciguatera. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023373]