Differences in the vulnerability of waterbird species to botulism outbreaks in Mediterranean wetlands: An assessment of ecological and physiological factors

Applied and Environmental Microbiology

Volumn 82, Issue 10, 2016, Pages 3092-3099

  Anza, I ^a   Vidal, D ^b   Feliu, J ^a   Crespo, E ^c   Mateo, R ^a  

^a INSTITUTO DE INVESTIGACIÓN EN RECURSOS CINEGÉTICOS IREC CSIC UCLM JCCM   (Spain)

^b UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^c Centro de Recuperación de Fauna El Chaparrillo JCCM   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BIRDS; CONSERVATION; GENES; PHYSIOLOGY; RISK PERCEPTION; SURVEYS; WETLANDS;

BOTULINUM NEUROTOXINS; CLOSTRIDIUM BOTULINUM; ENDANGERED SPECIES; FECAL SAMPLES; FEEDING HABITS; MORTALITY RATE; PHYSIOLOGICAL FACTORS; RISK FACTORS;

CLOSTRIDIUM;

BIOLOGICAL SURVEY; DISEASE RESISTANCE; DISEASE VECTOR; ENDANGERED SPECIES; MEDITERRANEAN ENVIRONMENT; MORTALITY; PEST OUTBREAK; PHYLOGENETICS; RISK FACTOR; SNAIL; TOXIC SUBSTANCE; TOXIN; VULNERABILITY; WATERFOWL; WETLAND;

ANAS; AVES; CERITHIDEA RHIZOPHORARUM; CLOSTRIDIUM BOTULINUM; OXYURA LEUCOCEPHALA; PHYSA ACUTA;

BOTULINUM TOXIN; BOTULINUM TOXIN TYPE C; BOTULINUM TOXIN TYPE D;

ANIMAL; BACTERIAL SHEDDING; BIRD; BIRD DISEASES; BOTULISM; CLASSIFICATION; CLOSTRIDIUM BOTULINUM; DISEASE PREDISPOSITION; EPIDEMIC; FECES; GENETICS; HETEROZYGOTE; ISOLATION AND PURIFICATION; MICROBIOLOGY; SNAIL; SOUTHERN EUROPE; TIME FACTOR; VETERINARY; WETLAND;

ANIMALS; BACTERIAL SHEDDING; BIRD DISEASES; BIRDS; BOTULINUM TOXINS; BOTULISM; CARRIER STATE; CLOSTRIDIUM BOTULINUM; DISEASE OUTBREAKS; DISEASE SUSCEPTIBILITY; FECES; MEDITERRANEAN REGION; SNAILS; TIME FACTORS; WETLANDS;

EID: 84966692187     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00119-16     Document Type: Article

References (42)

1. Rocke TE, Friend M. 1999. Avian botulism, p 271-281. In Friend M, Franson JD (ed), Field manual of wildlife disease. General procedures and diseases of birds. USGS National Wildlife Health Center, Washington, DC.
2. Anza I, Skarin H, Vidal D, Lindberg A, Båverud V, Mateo R. 2014. The same clade of Clostridium botulinum strains is causing avian botulism in southern and northern Europe. Anaerobe 26:20-23. http://dx.doi.org/10.1016/j.anaerobe.2014.01.002.
3. Rocke TE. 2006. The global importance of avian botulism, p 422-426. In Boere GC, Galbraith CA, Stroud DA (ed), Waterbirds around the world. The Stationery Office, Edinburgh, United Kingdom.
4. Woudstra C, Skarin H, Anniballi F, Fenicia L, Bano L, Drigo I, Koene M, Bäyon-Auboyer MH, Buffereau JP, De Medici D, Fach P. 2012. Neurotoxin gene profiling of Clostridium botulinum types C and D native to different countries within Europe. Appl Environ Microbiol 78:3120-3127. http://dx.doi.org/10.1128/AEM.07568-11.
5. 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.
6. Wobeser G. 1997. Avian botulism: another perspective. J Wildl Dis 33: 181-186. http://dx.doi.org/10.7589/0090-3558-33.2.181.
7. Friend M, McLean RG, Dein FJ. 2001. Disease emergence in birds: challenges for the twenty-first century. Auk 118:290-303.
8. Chou SJ, Shieh YC, Yu CY. 2008. Hematologic and biochemistry values for black-faced spoonbills (Platalea minor) with and recovering from botulism. J Wildl Dis 44:781-784. http://dx.doi.org/10.7589/0090-3558-44.3.781.
9. Work TM, Klavitter JL, Reynolds MH, Blehert D. 2010. Avian botulism: a case study in translocated endangered Laysan ducks (Anas laysanensis) on Midway Atoll. J Wildl Dis 46:499-506. http://dx.doi.org/10.7589/0090-3558-46.2.499.
10. Shutt JL, Andrews DW, Weseloh DVC, Moore DJ, Hebert CE, Campbell GD, Williams K. 2014. The importance of island surveys in documenting disease-related mortality and botulism E in Great Lakes colonial waterbirds. J Great Lakes Res 40:58-63. http://dx.doi.org/10.1016/j.jglr.2014.01.001.
11. Vidal D, Anza I, Taggart MA, Perez-Ramírez E, Crespo E, Hofle U, Mateo R. 2013. Environmental factors influencing the prevalence of Clostridium botulinum type C in nonpermanent Mediterranean wetlands. Appl Environ Microbiol 79:4264-4271. http://dx.doi.org/10.1128/AEM.01191-13.
12. Atiénzar F, Antón-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 51:783-792.
13. Hadad E, Moyal C. 2007. Preference of the white-headed duck Oxyura leucocephala for wastewater reservoirs in the Judean plain, Israel. Sandgrouse 29:70-78.
14. Anza I, Vidal D, Laguna C, Díaz-Sánchez S, Sánchez S, Chicote A, Florín M, Mateo R. 2014. Eutrophication and bacterial pathogens as risk factors for avian botulism outbreaks in wetlands receiving effluents from urban wastewater treatment plants. Appl Environ Microbiol 15:4251-4259. http://dx.doi.org/10.1128/AEM.00949-14.
15. Adams SG, Conly FM, Gratto-Trevor CL, Cash KJ, Bollinger T. 2003. Shorebird use and mortality at a large Canadian prairie lake impacted by botulism. Waterbirds 26:13-25. http://dx.doi.org/10.1675/1524-4695(2003)026[0013:SUAMAA]2.0.CO;2.
16. Rossetto O, Pirazzini M, Montecucco C. 2014. Botulinum neurotoxins: genetic, structural and mechanistic insights. Nat Rev Microbiol 12:535-549. http://dx.doi.org/10.1038/nrmicro3295.
17. Centers for Disease Control and Prevention (CDC). 1998. Botulism in the United States, 1899-1996. 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.
18. Baker K (ed). 1993. Identification guide to European nonpasserines. British Trust for Ornithology, London, United Kingdom.
19. Vidal D, Taggart MA, Badiola I, Mateo R. 2011. Real-time polymerase chain reaction for the detection of toxigenic Clostridium botulinum type C1 in waterbird and sediment samples: comparison with other PCR techniques. J Vet Diag Invest 23:942-946. http://dx.doi.org/10.1177/1040638711416847.
20. Sánchez-Hernández L, Cifuentes A, Jiménez B, Mateo R, González R.2008. Detection of Clostridium botulinum neurotoxin coding genes: analysis of PCR products by real-time versus capillary gel electrophoresis methods. Eur Food Res Technol 227:495-502. http://dx.doi.org/10.1007/s00217-007-0746-1.
21. Contreras de Vera A, León-Vizcaíno L, Carranza J, Hermoso de Mendoza M, Garrido F. 1987. Botulismo aviar en zonas húmedas de la campiña de Sevilla y Córdoba. Med Vet 4:173-179.
22. Cramp S. 1998. The complete birds of the Western Palearctic on CDROM. Oxford University Press, Oxford, United Kingdom.
23. Duncan RM, Jensen WL. 1976. A relationship between avian carcasses and living invertebrates in the epizootiology of avian botulism. J Wildl Dis 12:116-126. http://dx.doi.org/10.7589/0090-3558-12.1.116.
24. Bernot RJ, Kennedy EE, Lamberti GA. 2005. Effects of ionic liquids on the survival, movement, and feeding behavior of the freshwater snail Physa acuta. Environ Toxicol Chem 24:1759-1765. http://dx.doi.org/10.1897/04-614R.1.
25. Getchell RG, Bowser PR. 2006. Ecology of type E botulism within dreissenid mussel beds. Aquat Invaders 17:1-8. http://www.eeb.cornell.edu/ecologymarinedisease/Members_Finfish_Getchell_files/Getchell%26Bowser'06-AquaticInvaders.pdf.
26. Deville AS, Grémillet D, Gauthier-Clerc M, Guillemain M, Von Houwald F, Gardelli B, Béchet A. 2013. Nonlinear feeding functional responses in the greater flamingo (Phoenicopterus roseus) predict immediate negative impact of wetland degradation on this flagship species. Ecol Evol 3:1413-1425. http://dx.doi.org/10.1002/ece3.554.
27. Rodríguez-Pérez H, Green AJ. 2006. Waterbird impacts on widgeongrass Ruppia maritima in a Mediterranean wetland: comparing big groups and seasonal effects. Oikos 112:525-534. http://dx.doi.org/10.1111/j.0030-1299.2006.14307.x.
28. Varo N, Green AJ, Sánchez MI, Ramos C, Gómez J, Amat JA. 2011. Behavioral and population responses to changing availability of Artemia prey by molting black-necked grebes, Podiceps nigricollis. Hydrobiologia 664:163-171. http://dx.doi.org/10.1007/s10750-010-0596-x.
29. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han KL, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri Y. 2008. A phylogenomic study of birds reveals their evolutionary history. Science 320:1763-1768. http://dx.doi.org/10.1126/science.1157704.
30. Clench MH, Mathias JR. 1995. The avian cecum: a review. Wilson Bull 107:93-121.
31. Rocke TE, Converse K, Meteyer C, Mclean RG. 2005. The impact of disease in the American white pelican in North America. Waterbirds 28: 87-94.
32. Pradel R, Rioux N, Tamisier A, Lebreton JD. 1997. Individual turnover among wintering teal in Camargue: a mark-recapture study. J Wildlife Manag 61:816-821. http://dx.doi.org/10.2307/3802189.
33. Hardy SP, Kaldhusdal M. 2013. Type C and C/D toxigenic Clostridium botulinum is not normally present in the intestine of healthy broilers. Vet Microbiol 30:466-468. http://dx.doi.org/10.1016/j.vetmic.2013.03.022.
34. Green AJ, Figuerola J, Sánchez MI. 2002. Implications of waterbird ecology for the dispersal of aquatic organisms. Acta Oecol (Montrouge) 23:177-189. http://dx.doi.org/10.1016/S1146-609X(02)01149-9.
35. Charalambidou I, Santamaría L. 2002. Waterbirds as endozoochorous dispersers of aquatic organisms: a review of experimental evidence. Acta Oecol (Montrouge) 23:165-176. http://dx.doi.org/10.1016/S1146-609X(02)01148-7.
36. Nogales M, Medina FM, Quilis V, González-Rodríguez M. 2001. Ecological and biogeographical implications of yellow-legged gulls (Larus cachinnans Pallas) as seed dispersers of Rubia fruticosa Ait. (Rubiaceae) in the Canary Islands. J Biogeogr 28:1137-1145. http://dx.doi.org/10.1046/j.1365-2699.2001.00622.x.
37. Skarin H, Lindberg A, Blomqvist G, Aspán A, Båverud V. 2010. Molecular characterization and comparison of Clostridium botulinum typeC avian strains. Avian Pathol 39:511-518. http://dx.doi.org/10.1080/03079457.2010.526923.
38. Clench MH, Mathias JR. 1992. Intestinal transit: how can it be delayed long enough for birds to act as long-distance dispersal agents?. Auk 109:3-6.
39. Swerczek TW. 1980. Experimentally induced toxicoinfectious botulism in horses and foals. Am J Vet Res 41:348-350.
40. Dohms JE, Allen PH, Rosenberger JK. 1982. Cases of type C botulism in broiler chickens. Avian Dis 26:204-210. http://dx.doi.org/10.2307/1590044.
41. Miyazaki S, Sakaguchi G. 1978. Experimental botulism in chickens: the cecum as the site of production and absorption of botulinum toxin. Jpn J Med Sci Biol 31:1-15. http://dx.doi.org/10.7883/yoken1952.31.1.
42. Lindström M, Korkeala H. 2006. Laboratory diagnostics of botulism. Clin Microbiol Rev 19:298-314. http://dx.doi.org/10.1128/CMR.19.2.298-314.2006.