Advertisement

The invasive red swamp crayfish (Procambarus clarkii) increases infection of the amphibian chytrid fungus (Batrachochytrium dendrobatidis)

  • Francisco J. OficialdeguiEmail author
  • Marta I. Sánchez
  • Camino Monsalve-Carcaño
  • Luz Boyero
  • Jaime Bosch
Original Paper

Abstract

Emerging infectious diseases are increasingly recognized as a severe threat to wildlife. Chytridiomycosis, caused by Batrachochytrium dendrobatidis (Bd), is considered one of the most important causes for the decline of amphibian populations worldwide. Identifying potential biological reservoirs and characterizing the role they can play in pathogen maintenance is not only important from a scientific point of view, but also relevant from an applied perspective (e.g. disease control strategies), especially when worldwide distributed invasive species are involved. We aimed (1) to analyse the prevalence and infection intensity of Bd in the invasive red swamp crayfish (Procambarus clarkii) across the western Andalusian region in Spain; and (2) to assess whether the presence of crayfish affects the prevalence and infection intensity of Bd in amphibians of Doñana Natural Space (DNS), a localized highly protected area within the Andalusian region. First, we found that infection prevalence in crayfish guts was 1.5% regionally (four out of 267 crayfish were qPCR positive to Bd, all of them belonging to the same Andalusian population); qPCR positives were histologically confirmed by finding zoosporangia of Bd in gastrointestinal walls of the red swamp crayfish. Second, we found a higher prevalence of Bd infection in DNS (19% for crayfish and 28% for amphibians on average), a place with great diversity and abundance of amphibians. Our analyses showed that prevalence of Bd in amphibians was related to the presence of the red swamp crayfish, indicating that this crayfish could be a suitable predictor of Bd infection in co-occurring amphibians. These results suggest that the red swamp crayfish might be a possible reservoir for Bd, representing an additional indirect impact on amphibians, a role that had not been previously recognised in its invasive range.

Keywords

Amphibians Chytridiomycosis Doñana Emerging infectious diseases Histological analysis Non-amphibian host Transmission 

Notes

Acknowledgements

We are strongly grateful to C. Serrano, M. A. Bravo, V. Castaño and R. Arribas for their help in the fieldwork, M. Wass for his help in the laboratory, and C. Díaz-Paniagua and The Monitoring Team on Natural Resources and Processes of the Doñana Biological Station for their valuable and helpful comments. We also thank the Laboratorio de Histología at Museo Nacional de Ciencias Naturales (CSIC) and the Laboratorio de SIG y Teledetección (LAST-EBD) at Estación Biológica de Doñana (CSIC) for providing logistical support. We thank two anonymous reviewers for useful suggestions that helped us to improve the final version of this manuscript. This study was funded by the Andalusian Government (RNM-936) and by Spanish Ministry of Economy and Competitiveness (CGL2015-70070-R). F.J.O. was supported by an Andalusian Government Grant. L.B. was supported by the Basque Government (IT951-16) and the Spanish Ministry for Science, Innovation and Universities (RTI2018-095023-B-I00).

References

  1. Arribas R, Díaz-Paniagua C, Gómez-Mestre I (2014) Ecological consequences of amphibian larvae and their native and alien predators on the community structure of temporary ponds. Freshw Biol 59(9):1996–2008CrossRefGoogle Scholar
  2. Berger L, Speare R, Daszak P et al (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc Natl Acad Sci 95(15):9031–9036CrossRefGoogle Scholar
  3. Berger L, Speare R, Hines HB et al (2004) Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Aust Vet J 82(7):434–439CrossRefGoogle Scholar
  4. Bosch J, Martínez-Solano I (2006) Chytrid fungus infection related to unusual mortalities of Salamandra salamandra and Bufo bufo in the Peñalara Natural Park (Central Spain). Oryx 40:84–89CrossRefGoogle Scholar
  5. Bosch J, Martínez-Solano I, García-París M (2001) Evidence of a chytrid fungus infection involved in the decline of the common midwife toad (Alytes obstetricans) in protected areas of Central Spain. Biol Cons 97:331–337CrossRefGoogle Scholar
  6. Boyle DG, Boyle DB, Olsen V et al (2004) Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis Aquat Org 60(2):141–148CrossRefGoogle Scholar
  7. Brannelly LA, McMahon TA, Hinton M et al (2015a) Batrachochytrium dendrobatidis in natural and farmed Louisiana crayfish populations: prevalence and implications. Dis Aquat Org 112(3):229–235CrossRefGoogle Scholar
  8. Brannelly LA, Hunter DA, Lenger D, Scheele BC, Skerratt LF, Berger L (2015b) Dynamics of chytridiomycosis during the breeding season in an Australian alpine amphibian. PLoS ONE 10(12):e0143629CrossRefGoogle Scholar
  9. Brannelly LA, Webb RJ, Hunter DA et al (2018) Non declining amphibians can be important reservoir hosts for amphibian chytrid fungus. Anim Conserv 21:91–101CrossRefGoogle Scholar
  10. Cruz MJ, Rebelo R, Crespo EG (2006) Effects of an introduced crayfish, Procambarus clarkii, on the distribution of south-western Iberian amphibians in their breeding habitats. Ecography 29(3):329–338CrossRefGoogle Scholar
  11. Dang TD, Searle CL, Blaustein AR (2017) Virulence variation among strains of the emerging infectious fungus Batrachochytrium dendrobatidis (Bd) in multiple amphibian host species. Dis Aquat Org 124(3):233–239CrossRefGoogle Scholar
  12. Daszak P, Cunningham AA, Hyatt AD (2003) Infectious disease and amphibian population declines. Divers Distrib 9(2):141–150CrossRefGoogle Scholar
  13. Díaz-Paniagua C, Gómez-Rodríguez C, Portheault A, De Vries W (2006) Distribución de los anfibios del Parque Nacional de Doñana en función de la densidad y abundancia de los hábitats de reproducción. Revista Española de Herpetología 20:17–30Google Scholar
  14. Díaz-Paniagua C, Fernández-Zamudio R, Florencio M et al (2010) Temporary ponds from Doñana National Park: a system of natural habitats for the preservation of aquatic flora and fauna. Limnetica 29(1):41–58Google Scholar
  15. Doddington BJ, Bosch J, Oliver JA et al (2013) Context-dependent amphibian host population response to an invading pathogen. Ecology 98:1795–1804CrossRefGoogle Scholar
  16. Drury RB, Wallington EA (1980) Preparation and fixation of tissues. Carleton’s Histol Tech 5:41–54Google Scholar
  17. European Commission DG Environment (2007) Interpretation manual of European Union habitats. EUR 27:1–142Google Scholar
  18. Farrer RA, Weinert LA, Bielby J et al (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Natl Acad Sci 108(46):18732–18736CrossRefGoogle Scholar
  19. Ficetola GF, Siesa ME, Padoa-Schioppa E, De Bernardi F (2012) Wetland features, amphibian communities and distribution of the alien crayfish, Procambarus clarkii. Alytes 29(1–4):75–87Google Scholar
  20. Fisher MC, Bosch J, Yin Z et al (2009) Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Mol Ecol 18(3):415–429CrossRefGoogle Scholar
  21. Fisher MC, Henk DA, Briggs CJ et al (2012) Emerging fungal threats to animal, plant and ecosystem health. Nature 484:186–194CrossRefGoogle Scholar
  22. García-Novo F, Marín-Cabrera C (2005) Doñana: Agua y Biosfera. Ministerio de Medio Ambiente, Sevilla (in Spanish) Google Scholar
  23. Garmyn A, van Rooij P, Pasmans F et al (2012) Waterfowl: potential environmental reservoirs of the chytrid fungus Batrachochytrium dendrobatidis. PLoS ONE 7(4):e35038CrossRefGoogle Scholar
  24. Gascon C, Collins J, Moore R et al (2007) Amphibian conservation action plan. IUCN/SSC Amphibian Specialist Group, Gland. ISBN 978-2-8317-1008-2Google Scholar
  25. Gervasi SS, Stephens PR, Hua J et al (2017) Linking ecology and epidemiology to understand predictors of multi-host responses to an emerging pathogen, the amphibian chytrid fungus. PLoS ONE 12(1):e0167882CrossRefGoogle Scholar
  26. Global Invasive Species Database (2018) Species profile: Batrachochytrium dendrobatidis. http://www.iucngisd.org/gisd/species.php?sc=123. Accessed on 19 Dec 2018
  27. Gómez-Rodríguez C (2009) Condicionantes ecológicos de la distribución de anfibios en el Parque Nacional de Doñana. Dissertation, Universidad de SalamancaGoogle Scholar
  28. Hidalgo-Vila J, Díaz-Paniagua C, Marchand MA, Cunningham AA (2012) Batrachochytrium dendrobatidis infection of amphibians in the Doñana National Park, Spain. Dis Aquat Org 98(2):113–119CrossRefGoogle Scholar
  29. Johnson ML, Speare R (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis Aquat Org 65:181–186CrossRefGoogle Scholar
  30. Kilburn VL, Ibáñez R, Green DM (2011) Reptiles as potential vectors and hosts of the amphibian pathogen Batrachochytrium dendrobatidis in Panama. Dis Aquat Org 97:127–134CrossRefGoogle Scholar
  31. Kouba A, Petrusek A, Kozák P (2014) Continental-wide distribution of crayfish species in Europe: update and maps. Knowl Manag Aquat Ecosyst 413:05CrossRefGoogle Scholar
  32. Kriger KM, Hero JM (2007) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. J Zool 271:352–359Google Scholar
  33. Liew N, Moya MJM, Wierzbicki CJ et al (2017) Chytrid fungus infection in zebrafish demonstrates that the pathogen can parasitize non-amphibian vertebrate hosts. Nat Commun 8:15048CrossRefGoogle Scholar
  34. McMahon TA, Brannelly LA, Chatfield MWH et al (2013) Chytrid fungus Batrachochytrium dendrobatidis has non-amphibian hosts and releases chemicals that cause pathology in the absence of infection. Proc Natl Acad Sci 110(1):210–215CrossRefGoogle Scholar
  35. O’Hanlon SJ, Rieux A, Farrer RA et al (2018) Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360:621–627CrossRefGoogle Scholar
  36. Oficialdegui FJ, Clavero M, Sánchez MI et al (2019) Unravelling the global invasion routes of a worldwide invader, the red swamp crayfish (Procambarus clarkii). Freshw Biol.  https://doi.org/10.1111/fwb.13312 (in press) CrossRefGoogle Scholar
  37. Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96(1):9–15CrossRefGoogle Scholar
  38. Ramalho RO, Anastácio PM (2015) Factors inducing overland movement of invasive crayfish (Procambarus clarkii) in a ricefield habitat. Hydrobiologia 746(1):135–146CrossRefGoogle Scholar
  39. Román J (2014) Artificial water points for wildlife management facilitate the spread of red swamp crayfish (Procambarus clarkii). Manag Biol Invasions 5(4):341–348CrossRefGoogle Scholar
  40. Ruggeri J, de Carvalho-e-Silva SP, James TY, Toledo LF (2018) Amphibian chytrid infection is influenced by rainfall seasonality and water availability. Dis Aquat Org 127(2):107–115CrossRefGoogle Scholar
  41. Scheele BC, Hunter DA, Brannelly LA et al (2017) Reservoir-host amplification of disease impact in an endangered amphibian. Conserv Biol 31(3):592–600CrossRefGoogle Scholar
  42. Scheele BC, Pasmans F, Skerratt LF et al (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363(6434):1459–1463CrossRefGoogle Scholar
  43. Skerratt LF, Berger L, Speare R et al (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4(2):125–134CrossRefGoogle Scholar
  44. Speare R, Alford R, Aplin K et al (2001) Nomination for listing of amphibian chytridiomycosis as a key threatening process under the Environment Protection and Biodiversity Conservation Act 1999. In: Speare R (ed) Developing management strategies to control amphibian diseases: decreasing the risks due to communicable diseases. School of Public Health and Tropical Medicine, James Cook University, Townsville, pp 185–196Google Scholar
  45. Stuart SN, Chanson JS, Cox NA et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306(5702):1783–1786CrossRefGoogle Scholar
  46. van Rooij P, Martel A, Haesebrouck F, Pasmans F (2015) Amphibian chytridiomycosis: a review with focus on fungus–host interactions. Vet Res 46(1):137CrossRefGoogle Scholar
  47. Voyles J, Young S, Berger L et al (2009) Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines. Science 326(5952):582–585CrossRefGoogle Scholar
  48. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc Natl Acad Sci 107(21):9689–9694CrossRefGoogle Scholar
  49. Walker SF, Bosch J, Gomez V et al (2010) Factors driving pathogenicity vs. prevalence of amphibian panzootic chytridiomycosis in Iberia. Ecol Lett 13:372–382CrossRefGoogle Scholar
  50. Woolhouse ME, Taylor LH, Haydon DT (2001) Population biology of multihost pathogens. Science 292(5519):1109–1112CrossRefGoogle Scholar
  51. Xie GY, Olson DH, Blaustein AR (2016) Projecting the global distribution of the emerging amphibian fungal pathogen, Batrachochytrium dendrobatidis, based on IPCC climate futures. PLoS ONE 11(8):e0160746CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Wetland EcologyEstación Biológica de Doñana (EBD-CSIC)SevilleSpain
  2. 2.Instituto Universitario de Investigación Marina (INMAR), Campus de Excelencia, Internacional/Global del Mar (CEI·MAR)Universidad de CádizPuerto RealSpain
  3. 3.Museo Nacional de Ciencias Naturales, CSICMadridSpain
  4. 4.Faculty of Science and TechnologyUniversity of the Basque Country (UPV/EHU)LeioaSpain
  5. 5.IKERBASQUE, Basque Foundation for ScienceBilbaoSpain
  6. 6.Research Unit of Biodiversity (CSIC, UO, PA)Oviedo UniversityMieresSpain

Personalised recommendations