Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Avian-botulism risk in waterbird breeding colonies and implications for environmental water management

K. J. Brandis https://orcid.org/0000-0001-6807-0142 A E , J. Spencer A B C , B. Wolfenden B C and D. Palmer D
+ Author Affiliations
- Author Affiliations

A Centre for Ecosystem Science, School of Biological, Earth and Environmental Science, University of New South Wales, NSW 2052, Australia.

B Department of Planning, Industry and Environment PO Box 29, Lidcombe, NSW 1825, Australia.

C Institute Land, Water and Society, School of Environmental Sciences, Charles Sturt University, Albury, NSW 2640, Australia

D Department of Primary Industries and Regional Development (DPIRD) Diagnostics and Laboratory Services, Sustainability and Biosecurity, South Perth, WA 6151, Australia.

E Corresponding author. Email: kate.brandis@unsw.edu.au

Marine and Freshwater Research 71(2) 179-190 https://doi.org/10.1071/MF18446
Submitted: 21 November 2018  Accepted: 2 October 2019   Published: 18 December 2019

Abstract

Avian botulism poses a significant risk to waterbird health in Australian wetlands. This paralytic, often fatal, disease occurs when birds ingest a neurotoxin produced by the bacterium Clostridium botulinum. Our current understanding of avian botulism comes largely from studies in the northern hemisphere, with many of these studies linking outbreaks of avian botulism with poor water quality. The Murray–Darling Basin provides the most important breeding habitat for colonial waterbirds in Australia, but the frequency of large-scale breeding events has declined, and waterbird populations are near record-low numbers. Avian botulism has the capacity to have significant impacts on waterbird recruitment if not managed appropriately. We propose that environmental water-management strategies that aim to maintain water quality through flow delivery to waterbird colonies could mitigate the risk of botulism outbreaks and contribute to waterbird population recovery.


References

Adams, S. G., Conly, F. M., Gratto-Trevor, C. L., Cash, K. J., and Bollinger, T. (2003). Shorebird use and mortality at a large Canadian prairie lake impacted by botulism. Waterbirds 26, 13–25.
Shorebird use and mortality at a large Canadian prairie lake impacted by botulism.Crossref | GoogleScholarGoogle Scholar |

Allen, M., Babiker, M., Chen, Y., de Coninck, H., Connors, S., van Diemen, R., Dube, O. P., Ebi, K. L., Engelbrecht, F., Ferrat, M., Ford, J., Forster, P., Fuss, S., Guillén Bolaños, T., Harold, J., Hoegh-Guldberg, O., Hourcade, J.-C., Huppmann, D., Jacob, D., Jiang, K., Johansen, T. G., Kainuma, M., de Kleijne, K., Kriegler, E., Ley, D., Liverman, D., Mahowald, N., Masson-Delmotte, V., Matthews, J. B. R., R. Millar, Mintenbeck, K., Morelli, A., Moufouma-Okia, W., Mundaca, L., Nicolai, M., Okereke, C., Pathak, M., Payne, A., Pidcock, R., Pirani, A., Poloczanska, E., Pörtner, H. O., Revi, A., Riahi, K., Roberts, D. C., Rogelj, J., Roy, J., Seneviratne, S. I., Shukla, P. R., Skea, J., Slade, R., Shindell, D., Singh, C., Solecki, W., Steg, L., Taylor, M., Tschakert, P., Waisman, H., Warren, R., Zhai, P., and Zickfeld, K. (2018). Summary for policymakers. In ‘Global Warming of 1.5°C. An IPCC Special Report on the Impacts of Global Warming of 1.5°C above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty’. (Eds V. Masson-Delmotte, P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P. R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J. B. R. Matthews, Y. Chen, X. Zhou, M. I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield.) (World Meteorological Organisation: Geneva, Switzerland.) Available at https://www.ipcc.ch/site/assets/uploads/sites/2/2019/05/SR15_SPM_version_report_LR.pdf [Verified 13 December 2019].

Anza, I., Vidal, D., Laguna, C., Diaz-Sanchez, S., Sanchez, S., Chicote, A., Florin, M., and Mateo, R. (2014). Eutrophication and bacterial pathogens as risk factors for avian botulism outbreaks in wetlands receiving effluents from urban wastewater treatment plants. Applied and Environmental Microbiology 80, 4251–4259.
Eutrophication and bacterial pathogens as risk factors for avian botulism outbreaks in wetlands receiving effluents from urban wastewater treatment plants.Crossref | GoogleScholarGoogle Scholar | 24795377PubMed |

Arthington, A. H., and Pusey, B. J. (2003). Flow restoration and protection in Australian Rivers. River Research and Applications 19, 377–395.
Flow restoration and protection in Australian Rivers.Crossref | GoogleScholarGoogle Scholar |

Babinszky, G., Csitari, G., and Jozsa, S. (2008). Observations on environmental factors in connection with avian botulism outbreaks in a Hungarian wetland habitat. Acta Microbiologica et Immunologica Hungarica 55, 455–464.
Observations on environmental factors in connection with avian botulism outbreaks in a Hungarian wetland habitat.Crossref | GoogleScholarGoogle Scholar | 19130753PubMed |

Barnum, D. A., Elder, J. F., Stephens, D., and Friend, F. (2002). ‘The Salton Sea.’ (Springer Science+Business Media, B.V.)10.1007/978-94-017-3459-2

Brand, C. J., Schmitt, S. M., Duncan, R. M., and Cooley, T. M. (1988). An outbreak of type E botulism among common loons (Gavia immer) in Michigan’s upper peninsula. Journal of Wildlife Diseases 24, 471–476.
An outbreak of type E botulism among common loons (Gavia immer) in Michigan’s upper peninsula.Crossref | GoogleScholarGoogle Scholar | 3411704PubMed |

Brandis, K. (2010). Colonial Waterbird Breeding in Australia: wetlands, water requirements and environmental flows. Ph.D. Thesis, University of New South Wales, Sydney, NSW, Australia.

Brandis, K., Bino, G., Spencer, J., Ramp, D., and Kingsford, R. T. (2018). Decline in colonial waterbird breeding highlights loss of Ramsar wetland function. Biological Conservation 225, 22–30.
Decline in colonial waterbird breeding highlights loss of Ramsar wetland function.Crossref | GoogleScholarGoogle Scholar |

Chipault, J. G., White, C. L., Blehert, D. S., Jennings, S. K., and Strom, S. M. (2015). Avian botulism type E in waterbirds in Lake Michigan, 2010–13. Journal of Great Lakes Research 41, 659–664.
Avian botulism type E in waterbirds in Lake Michigan, 2010–13.Crossref | GoogleScholarGoogle Scholar |

Contreras de Vera, A., García Fernandez, A., Cubero Pablo, M. J., and León-Vizcaino, L. (1991). Low prevalence of C botulinum in Spanish wetlands with a tidal regime. The Veterinary Record 128, 187–188.
Low prevalence of C botulinum in Spanish wetlands with a tidal regime.Crossref | GoogleScholarGoogle Scholar | 2031295PubMed |

Davidson, N. C. (2014). How much wetland has the world lost? Long-term and recent trends in global wetland area. Marine and Freshwater Research 65, 934–941.
How much wetland has the world lost? Long-term and recent trends in global wetland area.Crossref | GoogleScholarGoogle Scholar |

Dodds, K. L. (1993). Clostridium botulinum in foods. In ‘Clostridium botulinum: Ecology and Control in Foods’. (Eds A. H. W. Hauschild and K. L. Dodds.) pp. 53–68 (Marcel Dekker, Inc.: New York, NY, USA.)

Eales, C. E., and Gillespie, J. M. (1947). The isolation of Clostridium botulinum Type A from Victorian soils. Australian Journal of Science 10, 20–21.
| 20267540PubMed |

Espelund, M., and Klaveness, D. (2014). Botulism outbreaks in natural environments: an update. Frontiers in Microbiology 5, 287.
Botulism outbreaks in natural environments: an update.Crossref | GoogleScholarGoogle Scholar | 24966853PubMed |

Evelsizer, D. D., Bollinger, T. K., Dufour, K. W., and Clark, R. G. (2010). Survival of radio-marked mallards in relation to management of avian botulism. Journal of Wildlife Diseases 46, 864–877.
Survival of radio-marked mallards in relation to management of avian botulism.Crossref | GoogleScholarGoogle Scholar | 20688692PubMed |

Finlayson, C. M., and Rea, N. (1999). Reasons for the loss and degradation of Australian wetlands. Wetlands Ecology and Management 7, 1–11.
Reasons for the loss and degradation of Australian wetlands.Crossref | GoogleScholarGoogle Scholar |

Friend, M. (2002). Avian disease at the Salton Sea. Hydrobiologia 473, 293–306.
Avian disease at the Salton Sea.Crossref | GoogleScholarGoogle Scholar |

Friend, M. (2006). ‘Disease Emergence and Resurgence: the Wildlife–Human Connection.’ (US Geological Survey: Reston, VA, USA.)

Friend, M., McClean, R. G., and Dein, F. J. (2001). Disease emergence in birds: challenges for the twenty-first century. Auk 118, 290–303.
Disease emergence in birds: challenges for the twenty-first century.Crossref | GoogleScholarGoogle Scholar |

Galvin, J. W., Hollier, T. J., Bodinnar, K. D., and Bunn, C. M. (1985). An outbreak of botulism in wild waterbirds in southern Australia. Journal of Wildlife Diseases 21, 347–350.
An outbreak of botulism in wild waterbirds in southern Australia.Crossref | GoogleScholarGoogle Scholar | 4078968PubMed |

Gordon, A. N., and Field, H. E. (2006). A cross-jurisdictional model for targeted surveillance of wild bird species. Final report to the Wildlife and Exotic Disease Preparedness Program. Animal Research Institute, Biosecurity Sciences Laboratory, Department of Primary Industries and Fisheries Queensland, Queensland Government.

Grillo, T., Cox-Witton, K., and Post, L. (2013). Animal health surveillance quarterly report. Australian Wildlife Health Network 17, 7–8.

Haq, I., and Suhadi, F. (1981). Incidence of Clostridium botulinum in coastal and inland areas of West Java. Japanese Journal of Medical Science & Biology 34, 231–235.
Incidence of Clostridium botulinum in coastal and inland areas of West Java.Crossref | GoogleScholarGoogle Scholar |

Huss, H. H. (1980). Distribution of Clostridium botulinum. Applied and Environmental Microbiology 39, 764–769.
| 6990867PubMed |

Jang, I., Kang, M. S., Kim, H. R., Oh, J. Y., Lee, J. I., Lee, H. S., and Kwon, Y. K. (2014). Occurrence of avian botulism in Korea during the period from June to September 2012. Avian Diseases 58, 666–669.
Occurrence of avian botulism in Korea during the period from June to September 2012.Crossref | GoogleScholarGoogle Scholar | 25619016PubMed |

Kalmbach, E. R. (1938). ‘Botulism, a Recurring Hazard to Waterfowl: with Notes on Recent Outbreaks in the United States and Canada, and Australia.’ (US Department of Agriculture: Washington, DC, USA.)

Kingsford, R. T., and Auld, K. M. (2005). Waterbird breeding and environmental flow management in the Macquarie Marshes, arid Australia. River Research and Applications 21, 187–200.
Waterbird breeding and environmental flow management in the Macquarie Marshes, arid Australia.Crossref | GoogleScholarGoogle Scholar |

Kingsford, R. T., and Johnson, W. (1998). Impact of water diversions on colonially nesting waterbirds in the Macquarie Marshes of Arid Australia. Colonial Waterbirds 21, 159–170.
Impact of water diversions on colonially nesting waterbirds in the Macquarie Marshes of Arid Australia.Crossref | GoogleScholarGoogle Scholar |

Kingsford, R. T., and Norman, F. I. (2002). Australian waterbirds: products of the continent’s ecology. Emu 102, 47–69.
Australian waterbirds: products of the continent’s ecology.Crossref | GoogleScholarGoogle Scholar |

Kingsford, R. T., and Thomas, R. F. (2004). Destruction of wetlands and waterbird populations by dams and irrigation on the Murrumbidgee River in arid Australia. Environmental Management 34, 383–396.
Destruction of wetlands and waterbird populations by dams and irrigation on the Murrumbidgee River in arid Australia.Crossref | GoogleScholarGoogle Scholar | 15520895PubMed |

Leslie, D. (2001). Effect of river management on colonially nesting waterbirds in the Barmah–Millewa forest, south-eastern Australia. Regulated Rivers: Research and Management 17, 21–36.
Effect of river management on colonially nesting waterbirds in the Barmah–Millewa forest, south-eastern Australia.Crossref | GoogleScholarGoogle Scholar |

Lloyd, C. S., Thomas, G. J., Macdonald, J. W., Borland, E. D., Standring, K., and Smart, J. L. (1976). Wild bird mortality caused by botulism in Britain, 1975. Biological Conservation 10, 119–129.
Wild bird mortality caused by botulism in Britain, 1975.Crossref | GoogleScholarGoogle Scholar |

Mackle, I. J., Halcomb, E., and Parr, M. J. A. (2001). Severe adult botulism. Anaesthesia and Intensive Care 29, 297–300.
Severe adult botulism.Crossref | GoogleScholarGoogle Scholar | 11439805PubMed |

McLaughlin, G. (2003). Type E botulism in the Great Lakes: conference overview. (USGS National Wildlife Health Center.) Available at https://seagrant.sunysb.edu/botulism/pdfs/Proc03/9-Overview.pdf [Verified 19 November 2018].

Miyazaki, S., and Sakaguchi, G. (1978). Experimental botulism in chickens: the cecum as the site of production and absorption of botulinum toxin. Japanese Journal of Medical Science & Biology 31, 1–15.
Experimental botulism in chickens: the cecum as the site of production and absorption of botulinum toxin.Crossref | GoogleScholarGoogle Scholar |

Murphy, T., and Peterson, H. G. (2003). Approaches towards environmental restoration. In ‘Freshwater Management: Global Versus Local Perspective’. (Eds M. Kumagai and W. F. Vincent.) pp. 83–114. (Springer-Verlag: Tokyo, Japan.)

Murphy, T., Lawson, A., Nalewajko, C., Murkin, H., Ross, L., Oguma, K., and McIntyre, T. (2000). Algal toxins: initiators of avian botulism? Environmental Toxicology 15, 558–567.
Algal toxins: initiators of avian botulism?Crossref | GoogleScholarGoogle Scholar |

Murray–Darling Basin Authority (2012). ‘Basin Plan 2012.’ (MDBA: Canberra, ACT, Australia.)

Murray–Darling Basin Authority (2014). ‘Basin-wide Environmental Watering Strategy.’ (MDBA: Canberra, ACT, Australia.)

Neimanis, A., Gavier-Widen, D., Leighton, F., Bollinger, T., Rocke, T., and Morner, T. (2007). An outbreak of type C botulism in herring gulls (Larus argentatus) in southeastern Sweden. Journal of Wildlife Diseases 43, 327–336.
An outbreak of type C botulism in herring gulls (Larus argentatus) in southeastern Sweden.Crossref | GoogleScholarGoogle Scholar | 17699071PubMed |

Ono, T., Azuma, R., Kato, T., Takeuchi, S., and Suto, T. (1982). Outbreaks of type C botulism in waterfowl in Japan. National Institute of Animal Health Quarterly 22, 102–114.
| 6761593PubMed |

Porter, J. L., Kinsgsford, R. T., and Brandis, K. J. (2016). Aerial Survey of Wetland Birds in Eastern Australia – October 2016, annual summary report, University of New South Wales, Sydney, NSW, Australia.

Pullar, M. E. (1934). Enzootic botulism amongst wild birds. Australian Veterinary Journal 10, 128–135.
Enzootic botulism amongst wild birds.Crossref | GoogleScholarGoogle Scholar |

Reed, T. M., and Rocke, T. E. (1992). The role of avian carcasses in botulism epizootics. Wildlife Society Bulletin 20, 175–182.

Rocke, T. E. (2006). The global importance of avian botulism. In ‘Waterbirds around the World’. (Eds G. C. Boere, C. A. Galbraith, and D. A. Stroud.) pp. 422–426. (The Stationery Office: Edinburgh, UK.)

Rocke, T. E., and Bollinger, T. K. (2007). Chapter 21: avian botulism. In ‘Infectious Diseases of Wild Birds’. (Ed. N. J. Thomas, T. D. Hunter, and C. T. Atkinson.) pp. 377–416. (Blackwell Publishing: Ames, IA, USA)

Rocke, T. E., and Friend, M. (1999). Chapter 38: avian botulism. In ‘Field Manual of Wildlife Diseases’. (Ed. E. A. Ciganovich.) pp. 271–282. (US Geological Survey: Madison, WI, USA.)

Rocke, T. E., and Samuel, M. D. (1999). Water and sediment characteristics associated with avian botulism outbreaks in wetlands. The Journal of Wildlife Management 63, 1249–1260.
Water and sediment characteristics associated with avian botulism outbreaks in wetlands.Crossref | GoogleScholarGoogle Scholar |

Rocke, T. E., Euliss, N. H., and Samuel, M. D. (1999). Environmental characteristics associated with the occurrence of avian botulism in wetland of a northern California refuge. The Journal of Wildlife Management 63, 358–368.
Environmental characteristics associated with the occurrence of avian botulism in wetland of a northern California refuge.Crossref | GoogleScholarGoogle Scholar |

Rocke, T. E., Samuel, M. D., Swift, P. K., and Yarris, G. S. (2000). Efficacy of a type C botulism vaccine in green-winged teal. Journal of Wildlife Diseases 36, 489–493.
Efficacy of a type C botulism vaccine in green-winged teal.Crossref | GoogleScholarGoogle Scholar | 10941734PubMed |

Rocke, T., Converse, K., Meteyer, C., and McLean, B. (2005). The impact of disease in the American white pelican in North America. Waterbirds 28, 87–94.
The impact of disease in the American white pelican in North America.Crossref | GoogleScholarGoogle Scholar |

Sandler, R. J., Rocke, T. E., Samuel, M. D., and Yuill, T. M. (1993). Seasonal prevalence of Clostridium botulinum Type C in sediments of a northern Californian wetland. Journal of Wildlife Diseases 29, 533–539.
Seasonal prevalence of Clostridium botulinum Type C in sediments of a northern Californian wetland.Crossref | GoogleScholarGoogle Scholar | 8258850PubMed |

Shin, N. R., Byun, S. H., Chun, J. H., Shin, J. H., Kim, Y. J., Kim, J. H., Rhie, G. E., Chung, H. M., Mo, I. P., and Yoo, C. K. (2010). An outbreak of type C botulism in waterbirds: Incheon, Korea. Journal of Wildlife Diseases 46, 912–917.
An outbreak of type C botulism in waterbirds: Incheon, Korea.Crossref | GoogleScholarGoogle Scholar | 20688696PubMed |

Son, K., Lim, Y. K., Woo, C., Wang, S.-J., Kim, Y., Oem, J.-K., Jheong, W., and Jeong, J. (2018). Minimizing an outbreak of avian botulism (Clostridium botulinum type C) in Incheon, South Korea. The Journal of Veterinary Medical Science 80, 553–556.
Minimizing an outbreak of avian botulism (Clostridium botulinum type C) in Incheon, South Korea.Crossref | GoogleScholarGoogle Scholar | 29375088PubMed |

Soos, C., and Wobeser, G. (2006). Identification of primary substrate in the initiation of avian botulism outbreaks. The Journal of Wildlife Management 70, 43–53.
Identification of primary substrate in the initiation of avian botulism outbreaks.Crossref | GoogleScholarGoogle Scholar |

Tanasugarn, L. (1979). Clostridium botulinum on the Gulf of Thailand. Applied and Environmental Microbiology 37, 194–197.
| 373623PubMed |

US Geological Survey (1995). National Wildlife Health Center quarterly wildlife mortality report July 1995 to September 1995. (Wildlife Disease Association.) Available at https://www.wildlifedisease.org/wda/PUBLICATIONS/WDANewsletter/Archive.aspx [Verified 2 December 2019].

US Geological Survey (1999). ‘Field Manual of Wildlife Diseases.’ (US Department of the Interior and USGS: Madison, WI, USA.)

Victorian Government (2014). ‘Avian Botulism Information Kit.’ (Department of Environment and Primary Industries: Melbourne, Vic., Australia.)

Vidal, D., Anza, I., Taggart, M. A., Perez-Ramirez, E., Crespo, E., Hofle, U., and Mateo, R. (2013). Environmental factors influencing the prevalence of a Clostridium botulinum type C/D mosaic strain in nonpermanent Mediterranean wetlands. Applied and Environmental Microbiology 79, 4264–4271.
Environmental factors influencing the prevalence of a Clostridium botulinum type C/D mosaic strain in nonpermanent Mediterranean wetlands.Crossref | GoogleScholarGoogle Scholar | 23645197PubMed |

Wildlife Health Australia (2019a). Botulism in Australian waterbirds fact sheet. (WHA.) Available at https://www.wildlifehealthaustralia.com.au/FactSheets.aspx [Verified 15 August 2018].

Wildlife Health Australia (2019b). Diagnosis of avian botulism in Australia. Fact sheet. (WHA.) Available at https://www.wildlifehealthaustralia.com.au/FactSheets.aspx [Verified 15 August 2018].

Włodarczyk, R., Minias, P., Kukier, E., Grenda, T., Smietanka, K., and Janiszewski, T. (2014). The first case of a major avian type C botulism outbreak in Poland. Avian Diseases 58, 488–490.
The first case of a major avian type C botulism outbreak in Poland.Crossref | GoogleScholarGoogle Scholar | 25518447PubMed |

Wobeser, G. A. (1997). Botulism. In ‘Diseases of Wild Waterfowl’. pp. 149–161. (Springer: Boston, MA, USA)

Wobeser, G., Rainnie, D. J., Smith-Windsor, T. B., and Bogdan, G. (1983). Avian botulism during late autumn and early spring in Saskatchewan. Journal of Wildlife Diseases 19, 90–94.
Avian botulism during late autumn and early spring in Saskatchewan.Crossref | GoogleScholarGoogle Scholar | 6887447PubMed |

Wobeser, G., Marsden, S., and MacFarlane, R. J. (1987). Occurrence of toxigenic Clostridium botulinum Type C in the soil of wetlands in Saskatchewan. Journal of Wildlife Diseases 23, 67–76.
Occurrence of toxigenic Clostridium botulinum Type C in the soil of wetlands in Saskatchewan.Crossref | GoogleScholarGoogle Scholar | 3546742PubMed |

Woodall, P. F. (1982). Botulism outbreak in waterbirds at Seven-Mile Lagoon in south-east Queensland. Australian Wildlife Research 9, 533–539.
Botulism outbreak in waterbirds at Seven-Mile Lagoon in south-east Queensland.Crossref | GoogleScholarGoogle Scholar |

Woodall, P. F. (1985). Waterbird populations in the Brisbane region, 1972–83, and correlates with rainfall and water heights. Australian Wildlife Research 12, 495–506.
Waterbird populations in the Brisbane region, 1972–83, and correlates with rainfall and water heights.Crossref | GoogleScholarGoogle Scholar |

Work, T. M., Dagenais, J., Rameyer, R., and Breeden, R. (2015). Mortality patterns in endangered Hawaiian geese (Nene; Branta sandvicensis). Journal of Wildlife Diseases 51, 688–695.
Mortality patterns in endangered Hawaiian geese (Nene; Branta sandvicensis).Crossref | GoogleScholarGoogle Scholar | 26161721PubMed |

Wurtsbaugh, W. A. (2011) Relationships between eutrophication, cyanobacteria blooms and avian botulism mortalities in the Great Salt Lake. (Watershed Sciences Faculty Publications.) Available at https://digitalcommons.usu.edu/wats_facpub/880 [Verified 5 November 2018].

Yule, A. M., Barker, I. K., Austin, J. W., and Moccia, R. D. (2006). Toxicity of Clostridium botulinum Type E neurotoxin to Great Lakes fish: implications of avian botulism. Journal of Wildlife Diseases 42, 479–493.
Toxicity of Clostridium botulinum Type E neurotoxin to Great Lakes fish: implications of avian botulism.Crossref | GoogleScholarGoogle Scholar | 17092878PubMed |