Estimation of Cultivable Bacterial Diversity in the Cloacae and Pharynx in Eurasian Griffon Vultures (Gyps fulvus)
- 313 Downloads
In this work, we describe the biodiversity of cloacal and pharynx culture-based bacteria (commensal and pathogenic), in 75 Eurasian griffon vultures (Gyps fulvus) from two geographic areas. We address the question of whether the cultivable microbiota of vultures is organised into assemblages occurring by chance. In addition, we assess bacterial diversity in both anatomic regions and geographic areas. Bacterial diversity was represented by 26 Gram-negative and 20 Gram-positive genera. The most common genera were Escherichia, Enterococcus, Staphylococcus, Clostridium and Lactococcus. Escherichia coli and Enterococcus faecalis were the most common species in cloacal and pharyngeal samples. Staphylococcus and Erysipelothrix were isolated from the pharynx and Salmonella and Corynebacterium from the cloacae, and no Campylobacter was isolated from the cloacal swabs. Ten cloacal swabs were positive for Salmonella, of which five isolates were Salmonella enterica serotype 4,(5),12:i:-, one isolate was S. enterica serotype Derby, three isolates were S. enterica serotype 61:k:1,5,7 and one isolate was S. enterica serotype Infantis. The null modelling approach revealed that the commensal bacteria of vultures are not structured in assemblages. On the other hand, differences in bacterial genus and species richness between cloacal and pharyngeal samples or between geographic areas were clear, with the pharynx in vultures from both geographic areas being richer. The results of this study indicate also that vultures can serve as a reservoir of certain pathogenic zoonotic bacteria. The dissemination of these zoonotic pathogens in wildlife could be prevented by periodic sanitary surveys.
KeywordsGriffon vultures Cloacae Pharynx Bacteria richness Species evenness
This work was funded by project S2009/AGR-1489 of the Madrid Autonomous Community (Spain). The samples of G. fulvus were taken from the Territorial Cooperation Programme Spain-France-Andorra (NECROPIR-EFA 130/09). The authors thank the government institutions (Gestión Ambiental de Navarra S.A.; Gobierno de Navarra; Departament d’Agricultura, Ramaderia, Pesca, Alimentació i Medi Natural of the Generalitat de Catalunya), Grup d’Anellament Calldetenes-Osona, C. Fernández, P. Azkona, M. Carneiro and A. Margalida for the collection of the samples, and A. Casamayor and E. Pulido for their technical assistance. E. Serrano was supported by the postdoctoral program (SFRH/BPD/96637/2013) of the Fundação para a Ciência ea Tecnologia, Portugal.
- 7.Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York, USAGoogle Scholar
- 13.del Hoyo J, Elliot A, Sargatal G (1994) Handbook of the birds of the world. Lynx Edicions, BarcelonaGoogle Scholar
- 14.Development Core Team 3. 1. 1. A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. Available: http://www.R-project.org. Accessed 1 August 2014.
- 17.European Commission decision of 19 July 2007 concerning a financial contribution from the Community towards a survey on the prevalence and antimicrobial resistance of Campylobacter spp. in broiler flocks and on the prevalence of Campylobacter spp. and Salmonella spp. in broiler carcasses to be carried out in the Member States. Official J European Union 2007/516/EC.Google Scholar
- 20.Friedrich A, Szabo I, Dorn C, Schroeter A, Jaber M, Berendonk G, Brom M, Ledwolorz J,Google Scholar
- 25.Gotelli NJ, Graves GR (1996) Null models in ecology. Smithsonian Institution Press, Washington, DC, USAGoogle Scholar
- 27.Gotelli NJ, Entsminger GL (2001) Ecosim: Null Models Software for Ecology, Version 7.72. Acquired Intelligence Inc, & Kesey-Bear http://homepages.together.net/gentsmin/ecosim.htm.
- 29.Grimont PAD, Weill F (2007) Antigenic formulas of the Salmonella serovars, 9th edition 2007. WHO Collaborating Centre for Reference and Research on Salmonella. Institut Pasteur, ParisGoogle Scholar
- 31.Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM (2011) Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 8:887–900CrossRefPubMedGoogle Scholar
- 32.Hird SM, Carstens BC, Cardiff SW, Dittmann DL, Brumfield RT (2014) Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed Cowbird (Molothrus ater). PeerJ 2:e321. DOI 10.7717/peerj.321Google Scholar
- 34.Hugenholtz, P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biol. 3: Reviews0003.Google Scholar
- 36.International Organization for Standardization (2007). ISO 6579: 2002 Amendment 1:2007 Horizontal method for the detection of Salmonella species.Google Scholar
- 39.Kalla GR, Arya PL, Vyas UK (1981) Note on microflora in the respiratory tract of some chicken in Pajasthan. Indian J Animal Sci 51:254–257Google Scholar
- 40.Kalmback ER (1939) American vultures and the toxin of Clostridium botulinum. J Am Vet Med Assoc 94:187–191Google Scholar
- 49.Smibert RM, Krieg NR (1994) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DCGoogle Scholar
- 51.Suárez-Pérez A, Ramírez AS, Rosales RS, Calabuig P, Poveda C, Rosselló-Móra R, Nicholas RAJ, Poveda JB (2012) Mycoplasma neophronis sp. nov., isolated from the upper respiratory tract of Canarian Egyptian vultures (Neophron percnopterus majorensis). Int J Syst Evol Microbiol 62:1321–1325CrossRefPubMedGoogle Scholar
- 57.Wood S (2006) Generalized additive models: an introduction with R. CEC Statistic, Boca Raton, USAGoogle Scholar