{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T10:38:49Z","timestamp":1790419129852,"version":"4.1.0"},"reference-count":42,"publisher":"American Society for Microbiology","issue":"10","license":[{"start":{"date-parts":[[2016,5,15]],"date-time":"2016-05-15T00:00:00Z","timestamp":1463270400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"DOI":"10.13039\/100015865","name":"Organismo Autonomo de Parques Nacionales","doi-asserted-by":"crossref","award":["OAPN 035\/2009"],"award-info":[{"award-number":["OAPN 035\/2009"]}],"id":[{"id":"10.13039\/100015865","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100003339","name":"MINECO | Spanish Council of Research","doi-asserted-by":"publisher","award":["JAE-PRE"],"award-info":[{"award-number":["JAE-PRE"]}],"id":[{"id":"10.13039\/501100003339","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["Appl Environ Microbiol"],"published-print":{"date-parts":[[2016,5,15]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Avian botulism kills thousands of waterbirds every year, including endangered species, but information about the differences between species in vulnerability to botulism outbreaks and the capacity to act as carriers of<jats:named-content content-type=\"genus-species\">Clostridium botulinum<\/jats:named-content>is still poorly known. Here, we estimated the vulnerability to botulism of 11 waterbird species from Mediterranean wetlands by comparing the number of affected birds with the census of individuals at risk. The capacity of different species to act as carriers was studied by detecting the presence of the<jats:named-content content-type=\"genus-species\">C. botulinum<\/jats:named-content>type C\/D botulinum neurotoxin (BoNT) gene in fecal samples and prey items of waterbirds in the wild and by the serial sampling of cloacal swabs of birds affected by botulism. We found differences among species in their vulnerabilities to botulism, probably related to feeding habits, season of arrival, turnover, and, possibly, phylogenetic resilience. The globally endangered white-headed duck (<jats:named-content content-type=\"genus-species\">Oxyura leucocephala<\/jats:named-content>) showed mortality rates in the studied outbreaks of 7% and 17% of the maximum census, which highlights botulism as a risk factor for the conservation of the species. Invasive water snails, such as<jats:named-content content-type=\"genus-species\">Physa acuta<\/jats:named-content>, may be important drivers in botulism epidemiology, because 30% of samples tested positive for the BoNT gene during outbreaks. Finally, our results show that birds may excrete the pathogen for up to 7 days, and some individuals can do it for longer periods. Rails and ducks excreted<jats:named-content content-type=\"genus-species\">C. botulinum<\/jats:named-content>more often and for longer times than gulls, which could be related to their digestive physiology (i.e., cecum development).<\/jats:p><jats:p><jats:bold>IMPORTANCE<\/jats:bold>Botulism is an important cause of mortality in waterbirds, including some endangered species. The global climate change may have consequences in the ecology of wetlands that favor the occurrence of botulism outbreaks. Here, we offer some information to understand the ecology of this disease that can be useful to cope with these global changes in the future. We have found that some species (i.e., coots and dabbling ducks) are more vulnerable to botulism and have a more relevant role in the onset and amplification of the outbreaks than other species (i.e., flamingos and grebes). Feeding habits can explain these differences in part; in addition to the well-known role of necrophagous fly maggots, we found here that water snails are frequent carriers of<jats:named-content content-type=\"genus-species\">Clostridium botulinum<\/jats:named-content>. This is relevant, because these water snails can thrive in eutrophic and polluted wetlands, exacerbating other changes driven by climate change in wetlands.<\/jats:p>","DOI":"10.1128\/aem.00119-16","type":"journal-article","created":{"date-parts":[[2016,3,26]],"date-time":"2016-03-26T01:25:16Z","timestamp":1458955516000},"page":"3092-3099","update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":37,"title":["Differences in the Vulnerability of Waterbird Species to Botulism Outbreaks in Mediterranean Wetlands: an Assessment of Ecological and Physiological Factors"],"prefix":"10.1128","volume":"82","author":[{"given":"I.","family":"Anza","sequence":"first","affiliation":[{"name":"Instituto de Investigaci\u00f3n en Recursos Cineg\u00e9ticos (IREC), CSIC-UCLM-JCCM, Ciudad Real, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"D.","family":"Vidal","sequence":"additional","affiliation":[{"name":"Departamento de Ciencias M\u00e9dicas, Facultad de Medicina, Universidad de Castilla-La Mancha, Ciudad Real, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"J.","family":"Feliu","sequence":"additional","affiliation":[{"name":"Instituto de Investigaci\u00f3n en Recursos Cineg\u00e9ticos (IREC), CSIC-UCLM-JCCM, Ciudad Real, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"E.","family":"Crespo","sequence":"additional","affiliation":[{"name":"Centro de Recuperaci\u00f3n de Fauna El Chaparrillo (JCCM), Ciudad Real, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R.","family":"Mateo","sequence":"additional","affiliation":[{"name":"Instituto de Investigaci\u00f3n en Recursos Cineg\u00e9ticos (IREC), CSIC-UCLM-JCCM, Ciudad Real, Spain"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_2_2_2","first-page":"271","volume-title":"Field manual of wildlife disease. General procedures and diseases of birds","author":"Rocke TE","year":"1999","unstructured":"Rocke TE, Friend M. 1999. Avian botulism, p 271\u2013281. In Friend M, Franson JD (ed), Field manual of wildlife disease. General procedures and diseases of birds. USGS National Wildlife Health Center, Washington, DC."},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.anaerobe.2014.01.002"},{"key":"e_1_3_2_4_2","first-page":"422","volume-title":"Waterbirds around the world","author":"Rocke TE","year":"2006","unstructured":"Rocke TE. 2006. The global importance of avian botulism, p 422\u2013426. In Boere GC, Galbraith CA, Stroud DA (ed), Waterbirds around the world. The Stationery Office, Edinburgh, United Kingdom."},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.07568-11"},{"key":"e_1_3_2_6_2","unstructured":"Reed TM Rocke TE. 1992. The role of avian carcasses in botulism epizootics. Wildl Soc Bull 20:175-182. http:\/\/pubs.er.usgs.gov\/publication\/1003989."},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-33.2.181"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1093\/auk\/118.2.290"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-44.3.781"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-46.2.499"},{"key":"e_1_3_2_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jglr.2014.01.001"},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.01191-13"},{"key":"e_1_3_2_13_2","first-page":"783","article-title":"Distribution of the white-headed duck Oxyura leucocephala is affected by environmental factors in a Mediterranean wetland","volume":"51","author":"Ati\u00e9nzar F","year":"2012","unstructured":"Ati\u00e9nzar F, Ant\u00f3n-Pardo M, Armengol X, Barba E. 2012. Distribution of the white-headed duck Oxyura leucocephala is affected by environmental factors in a Mediterranean wetland. Zool Stud 51:783\u2013792.","journal-title":"Zool Stud"},{"key":"e_1_3_2_14_2","first-page":"70","article-title":"Preference of the white-headed duck Oxyura leucocephala for wastewater reservoirs in the Judean plain, Israel","volume":"29","author":"Hadad E","year":"2007","unstructured":"Hadad E, Moyal C. 2007. Preference of the white-headed duck Oxyura leucocephala for wastewater reservoirs in the Judean plain, Israel. Sandgrouse 29:70\u201378.","journal-title":"Sandgrouse"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.00949-14"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1675\/1524-4695(2003)026[0013:SUAMAA]2.0.CO;2"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrmicro3295"},{"key":"e_1_3_2_18_2","unstructured":"Centers for Disease Control and Prevention (CDC). 1998. Botulism in the United States 1899\u20131996. In Handbook for epidemiologists clinicians and laboratory workers. Centers for Disease Control and Prevention Atlanta GA. http:\/\/www.cdc.gov\/ncidod\/dbmd\/diseaseinfo\/files\/botulism.PDF."},{"key":"e_1_3_2_19_2","volume-title":"Identification guide to European nonpasserines","author":"Baker K","year":"1993","unstructured":"Baker K (ed). 1993. Identification guide to European nonpasserines. British Trust for Ornithology, London, United Kingdom."},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1177\/1040638711416847"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00217-007-0746-1"},{"key":"e_1_3_2_22_2","first-page":"173","article-title":"Botulismo aviar en zonas h\u00famedas de la campi\u00f1a de Sevilla y C\u00f3rdoba","volume":"4","author":"Contreras de Vera A","year":"1987","unstructured":"Contreras de Vera A, Le\u00f3n-Vizca\u00edno L, Carranza J, Hermoso de Mendoza M, Garrido F. 1987. Botulismo aviar en zonas h\u00famedas de la campi\u00f1a de Sevilla y C\u00f3rdoba. Med Vet 4:173\u2013179.","journal-title":"Med Vet"},{"key":"e_1_3_2_23_2","volume-title":"The complete birds of the Western Palearctic on CD-ROM","author":"Cramp S","year":"1998","unstructured":"Cramp S. 1998. The complete birds of the Western Palearctic on CD-ROM. Oxford University Press, Oxford, United Kingdom."},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.7589\/0090-3558-12.1.116"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1897\/04-614R.1"},{"key":"e_1_3_2_26_2","unstructured":"Getchell RG Bowser PR. 2006. Ecology of type E botulism within dreissenid mussel beds. 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Experimentally induced toxicoinfectious botulism in horses and foals. 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