Skip to main content

Advertisement

SpringerLink
Log in

The Absence of Zoonotic Agents in Invasive Bullfrogs (Lithobates catesbeianus) in Belgium and The Netherlands

  • Short Communication
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Exotic invasive bullfrogs (Lithobates catesbeianus) are considered to exert a considerable negative impact on native amphibian communities. This can be due to competition and predation, but they are also a notorious source of the infectious diseases chytridiomycosis and ranavirosis, affecting amphibian populations globally. Little is known regarding their carriage of other microbial agents that might be transferred to humans or other animals. In this study we determined the occurrence of the amphibian pathogens Ranavirus and Batrachochytrium dendrobatidis and of the zoonotic agents Coxiella burnetii, Neospora caninum, Leptospira sp., Toxoplasma gondii, Mycoplasma sp., Campylobacter sp., Salmonella sp. and extended-spectrum beta-lactamase producing Escherichia coli in 164 bullfrogs from three populations in Belgium and The Netherlands. Although B. dendrobatidis was present at a high prevalence of 63%, mean infection loads were low with an average of 10.9 genomic equivalents (SD 35.5), confirming the role of bullfrogs as B. dendrobatidis carriers, but questioning their role as primary reservoirs for B. dendrobatidis transmission to native amphibian communities. All tested samples were negative for the other infectious agents examined. These results suggest a limited role of bullfrogs as carrier of these pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

References

  • Boyle DG, Boyle DB, Olsen V, Morgan JA, Hyatt AD (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Diseases of Aquatic Organisms 60:141-148.

    Article  CAS  PubMed  Google Scholar 

  • Chambers DL, Hulse AC (2006) Salmonella serovars in the herpetofauna of Indiana County, Pennsylvania. Applied and Environmental Microbiology 72:3771-3773.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chiu CH, Ou JT (1996) Rapid identification of Salmonella serovars in feces by specific detection of virulence genes, invA and spvC, by an enrichment broth culture-multiplex PCR combination assay. Journal of Clinical Microbiology 34:2619-2622.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Clarkson LS, Tobin-D’angelo M, Shuler C, Hanna S, Benson J, Voetsch AC (2010) Sporadic Salmonella enterica serotype Javiana infections in Georgia and Tennessee: a hypothesis-generating study. Epidemiology and Infection 138:340-346.

    Article  CAS  PubMed  Google Scholar 

  • Diesch SL, McCulloch WF, Braun JL, Ellinghausen HC (1966) Leptospires from frog kidneys. Nature 209:939-940.

    Article  CAS  PubMed  Google Scholar 

  • Diesch SL, McCulloch WF, Braun JL, Davis JR (1970) Detection and ecology of leptospirosis in Iowa wildlife. Journal of Wildlife Diseases 6:275-288.

    Article  CAS  PubMed  Google Scholar 

  • Doubledee RA, Muller EB, Nisbet RM (2003) Bullfrogs, disturbance regimes, and the persistence of California red-legged frogs. Journal of Wildlife Management 67: 424-438.

    Article  Google Scholar 

  • Everard CO, Tota B, Bassett D, Alis C (1979) Salmonella in wildlife from Trinidad and Grenada. World International Journal of Wildlife Diseases 15:213-219.

    Article  CAS  Google Scholar 

  • Everard CO, Carrington DG, Korver H, Everard JD (1988) Leptospires in the marine toad (Bufo marinus) on Barbados. Journal of Wildlife Diseases 24:334-338.

    Article  CAS  PubMed  Google Scholar 

  • Everard CO, Carrington DG, Korver H, Burke R, Everard JD, Gravekamp C (1990) Leptospires in the whistling frog (Eleutherodactylus johnstonei) on Barbados. Journal of Tropical Medicine Hygiene 93:140-145.

    CAS  PubMed  Google Scholar 

  • Ficetola GF, Coic C, Detaint M, Berroneau M, Lorvelec O, Miaud C (2007) Pattern of distribution of the American bullfrog Rana catesbeiana in Europe. Biological Invasions 9:767-72.

    Article  Google Scholar 

  • Garmyn A, Haesebrouck F, Hellebuyck T, Smet A, Pasmans F, Butaye P, Martel A (2011) Presence of extended-spectrum beta-lactamase-producing Escherichia coli in wild geese. Journal of Antimicrobial Chemotherapy 7:1643-1644.

    Article  Google Scholar 

  • Garner TWJ, Perkins MW, Govindarajulu P, Seglie D, Walker S, Cunningham AA, Fischer MC (2006) The emerging amphibian pathogen Batrachochytrium dendrobatidis globally infects introduced populations of the North American bullfrog, Rana catesbeiana. Biological Letters 2:455-459.

    Article  Google Scholar 

  • Govindarajulu P, Altwegg R, Anholt BR (2005) Matrix model investigation of invasive species control: bullfrogs on Vancouver Island. Ecological Applications 15: 2161-2170.

    Article  Google Scholar 

  • Gravekamp C, Korver H, Montgomery J, Everard CO, Carrington D, Ellis WA, Terpstra WJ (1991) Leptospires isolated from toads and frogs on the island of Barbados. Zentrablatt für Bakteriologie 275:403-411.

    Article  CAS  Google Scholar 

  • Guenther S, Ewers C, Wieler LH (2011) Extended-spectrum Beta-lactamase producing E. coli in wildlife, yet another form of environmental pollution? Frontiers in Microbiology 2:246.

    Article  PubMed Central  PubMed  Google Scholar 

  • Hyatt AD, Boyle DG, Olsen V, Boyle DB, Berger L, Obendrof D, Dalton A, Kriger K, Hero M, Hines H, Philott R, Campbell R, Marantelli G, Gleason F, Colling A (2007) Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 73: 175-192.

    Article  CAS  PubMed  Google Scholar 

  • Johnson PTJ, McKenzie VJ, Peterson AC, Kerbie JL, Brown J, Blaustien AR, Jackson T (2011) Regional decline of an iconic amphibian associated with elevation, land-use change, and invasive species. Conservation Biology 25: 556-566.

    Article  PubMed  Google Scholar 

  • Jooris R (2002) Exoten onder de inheemse herpetofauna. Bulletin Institutional Royal Science Natural Belgique Biologie 72:223-228.

    Google Scholar 

  • Kiesecker JM, Blaustein AR (1998) Effects of introduced bullfrogs and smallmouth bass on microhabitat use, growth, and survival of native red-legged frogs (Rana aurora). Conservation Biology 12:776-787.

    Article  Google Scholar 

  • Kupferberg SJ (1997) Bullfrog (Rana catesbeiana) invasion of a California River: the role of larval competition. Ecology 78: 1736-1751.

    Google Scholar 

  • Linton D, Owen RJ, Stanley J (1996) Rapid identification by PCR of the genus Campylobacter and of five Campylobacter species enteropathogenic for man and animals. Research Microbiology 147:707-718.

    Article  CAS  Google Scholar 

  • Liu X, Rohr JR, Li Y (2013) Climate, vegetation, introduced hosts and trade shape a global wildlife pandemic. Proceedings of the Royal Society B 280: 20122506.

    Article  PubMed Central  PubMed  Google Scholar 

  • Louette G, Devisscher S, Adriaens T (2012) Control of invasive American bullfrog Lithobates catesbeianus in small shallow water bodies. European Journal of Wildlife Research DOI 10.1007/s10344-012-0655-x.

    Google Scholar 

  • Luja VH, Rodriguez-Estrella R (2010) The invasive bullfrog Lithobates catesbeianus in oases of Baja California Sur, Mexico: potential effects in a fragile ecosystem. Biological invasions 12: 2979-2983.

    Article  Google Scholar 

  • Mao J, Hedrick RP, Chichar VB (1997) Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229:212-20.

    Article  CAS  PubMed  Google Scholar 

  • Martel A, Sharifian Fard M, Van Rooij P, Jooris R, Boone F, Haesebrouck F, Van Rooij D, Pasmans F (2012) Road-killed Common Toads (Bufo bufo) in Flanders (Belgium) reveal low prevalence of ranaviruses and Batrachochytrium dendrobatidis. Journal of Wildlife Diseases 48: 835-839.

    Article  PubMed  Google Scholar 

  • McMahon TA, Brannelly LA, Chatfield MWH, Johnson PTJ, Joseph MB, McKenzie VJ, Richards-Zawacki CL, Venesky MD, Rohr JR (2013) Chytrid fungus Batrachochytrium dendrobatidis has nonamphibian hosts and releases chemicals that cause pathology in the absence of infection. Proceedings of the National Academy of Sciences of the United States of America 110: 210-215.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pasmans F, Muijsers M, Maes S, Van Rooij P, Brutyn M, Ducatelle R, Haesebrouck F, Martel A (2010) Chytridiomycosis related mortality in a midwife toad (Alytes obstetricans) in Belgium. Vlaams Diergeneeskundig Tijdschrift 79: 460-462.

    Google Scholar 

  • Pearl CA, Adamas MJ, Bury RB, McCreary B (2004) Asymmetrical effects of introduced bullfrogs (Rana catesbeiana) on native ranid frogs in Oregon. Copeia 1: 11-20.

    Article  Google Scholar 

  • Savard P, Perl TM (2012) A call for action: managing the emergence of multidrug-resistant Enterobacteriaceae in the acute care settings. Current Opinions in Infectious Diseases 25:371-377.

    Article  Google Scholar 

  • Sharifian-Fard M, Pasmans F, Adriaensen C, Devisscher S, Adriaens T, Louette G, Martel A (2011) Ranavirosis in invasive bullfrogs, Belgium. Emerging Infectious Diseases 17:2371-2371.

    Article  PubMed Central  PubMed  Google Scholar 

  • Sharma VK, Kaura YK, Singh IP (1974) Frogs as carriers of Salmonella and Edwardsiella. Antonie van Leeuwenhoek Journal of Microbiology 40:171-175.

    Article  CAS  Google Scholar 

  • Singh S, Sharma VD, Sethi MS (1979) Toads as a reservoirs of Salmonellae: prevalence and antibiogram. International Journal Zoonoses 6:82-84.

    CAS  Google Scholar 

  • Van Kuppleveld FJM, van der Logt JTM, Angulo AF, van Zoest MJ, Quint WGV, Niesters HGM, Galama JDM, Melchers WJG (1992) Genus- and species-specific identification of mycoplasmas by 16S rRNA amplification. Applied and Environmental Microbiology 58:2606–2615.

    Google Scholar 

  • Veenvliet P (1996) Brulkikkers (Rana castebeiana) in Nederland: storm in een glas slootwater? Lacerta 54:168-172.

    Google Scholar 

  • Veenvliet P (2009) Amerikaanse brulkikker. Rana catesbeiana. In: De amfibieën en reptielen van Nederland—Nederlandse fauna 9, Creemers RC, van Delft JJCW, RAVON (editors), Leiden, Nederland: Nationaal Museum Naturalis, European Invertebrate Survey.

  • Zupanovic Z, Lopez G, Hyatt AE, Green B, Bartran G, Parkes H, Whittington RJ, Speare R (1998) Giant toads Bufo marinus in Australia and Venezuela have antibodies against ‘ranaviruses’. Diseases of Aquatic Organisms 32:1-8.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was partly performed in the framework of EU Interreg IVA project IVA-VLANED-2.31 ‘Invasieve exoten in Vlaanderen en Zuid-Nederland (INVEXO)’.

Author information

Authors and Affiliations

  1. Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820, Merelbeke, Belgium

    An Martel, Connie Adriaensen, Mojdeh Sharifian-Fard & Frank Pasmans

  2. RAVON, Nijmegen, The Netherlands

    Annemarieke Spitzen-van der Sluijs

  3. Research Institute for Nature and Forest, Brussels, Belgium

    Gerald Louette & Kristof Baert

  4. Natuurbalans-Limes Divergens, Nijmegen, The Netherlands

    Ben Crombaghs

  5. Department of Obstetrics, Reproduction and Herd Health, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium

    Jeroen Dewulf

Authors
  1. An Martel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Connie Adriaensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mojdeh Sharifian-Fard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Annemarieke Spitzen-van der Sluijs
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gerald Louette
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kristof Baert
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ben Crombaghs
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jeroen Dewulf
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Frank Pasmans
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to An Martel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martel, A., Adriaensen, C., Sharifian-Fard, M. et al. The Absence of Zoonotic Agents in Invasive Bullfrogs (Lithobates catesbeianus) in Belgium and The Netherlands. EcoHealth 10, 344–347 (2013). https://doi.org/10.1007/s10393-013-0864-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-013-0864-0

Keywords

Search

Navigation