Skip to main content

Advertisement

SpringerLink
Log in

Pathogen Dynamics in an Invasive Frog Compared to Native Species

  • Original Contribution
  • Published:
EcoHealth Aims and scope Submit manuscript

Abstract

Emerging infectious diseases threaten the survival of wildlife populations and species around the world. In particular, amphibians are experiencing population declines and species extinctions primarily in response to two pathogens, the fungus Batrachochytrium dendrobatidis (Bd) and the iridovirus Ranavirus (Rv). Here, we use field surveys and quantitative (q)PCR to compare infection intensity and prevalence of Bd and Rv across species and seasons on Jekyll Island, a barrier island off the coast of Georgia, USA. We collected oral and skin swabs for 1 year from four anuran species and three families, including two native hylids (Hyla cinerea and Hyla squirella), a native ranid (Rana sphenocephala), and the invasive rain frog Eleutherodactylus planirostris. Bd infection dynamics did not vary significantly over sampling months, but Rv prevalence and intensity were significantly higher in fall 2014 compared to spring 2015. Additionally, Rv prevalence and intensity were significantly higher in E. planirostris than in the other three species. Our study highlights the potential role of invasive amphibians as drivers of disease dynamics and demonstrates the importance of pathogen surveillance across multiple time periods and species to accurately capture the infectious disease landscape.

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

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  • Allender MC, Bunick D, Mitchell MA (2013) Development and validation of TaqMan quantitative PCR for detection of frog virus 3-like virus in eastern box turtles (Terrapene carolina carolina). Journal of Virological Methods 188:121–125

    Article  CAS  PubMed  Google Scholar 

  • Bataille A, Cashins SD, Grogan L, Skerratt LF, Hunter D, McFadden M, Scheele B, Brannelly LA, Macris A, Harlow PS, Bell S, Berger L, Waldman B (2015) Susceptibility of amphibians to chytridiomycosis is associated with MHC class II conformation. Proceedings B 282:20143127

    Google Scholar 

  • Bayley A, Hill B, Feist S (2013) Susceptibility of the European common frog Rana temporaria to a panel of ranavirus isolates from fish and amphibian hosts. Diseases of Aquatic Organisms 103:171–183

    Article  PubMed  Google Scholar 

  • Beard KH, Price EA, Pitt WC (2009) Biology and impacts of Pacific Island invasive species. 5. Eleutherodactylus coqui, the Coqui Frog (Anura: Leptodactylidae). Pacific Science 63:297–316

    Article  Google Scholar 

  • Berger L, Hyatt A, Speare R, Longcore J (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 68:51–63

    Article  PubMed  Google Scholar 

  • Berger L, Speare R, Daszak P, Green DE, Cunningham AA, Goggin CL, Slocombe R, Ragan MA, Hyatt AD, McDonald KR, Hines HB, Lips KR, Marantelli G, Parkes H (1998) Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences of the United States of America 95:9031–9036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bielby J, Cooper N, Cunningham A, Garner TWJ, Purvis A (2008) Predicting susceptibility to future declines in the world’s frogs. Conservation Letters 1:82–90

    Article  Google Scholar 

  • Boughton RG, Staiger J, Franz R (2000) Use of PVC pipe refugia as a sampling technique for Hylid treefrogs. The American Midland Naturalist 180:168–177

    Article  Google Scholar 

  • Bowden TJ, Thompson KD, Morgan AL, Gratacap RML, Nikoskelainen S (2007) Seasonal variation and the immune response: a fish perspective. Fish and Shellfish Immunology 22:695–706.

    Article  PubMed  Google Scholar 

  • Boyle D, Boyle D, Olsen V, Morgan J, Hyatt A (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 

  • Brand MD, Hill RD, Brenes R, Chaney JC, Wilkes RP, Grayfer L, Miller DL, Gray MJ (2016) Water temperature affects susceptibility to ranavirus. EcoHealth 13:350–359

    Article  PubMed  Google Scholar 

  • Brannelly LA, Chatfield MWH, Richards-Zawacki CL (2012) Field and laboratory studies of the susceptibility of the Green Treefrog (Hyla cinerea) to Batrachochytrium dendrobatidis infection. Public Library of Sciences One 7:e38473

    CAS  Google Scholar 

  • Brenes R, Gray MJ, Waltzek TB, Wilkes RP, Miller DL (2014) Transmission of ranavirus between ectothermic vertebrate hosts. Public Library of Sciences One 9:e92476

    Google Scholar 

  • Brunner JL, Storfer A, Gray MJ, Hoverman JT (2015) Ranavirus ecology and evolution: from epidemiology to extinction. In: Matthew J. Gray and V. Gregory Chinchar (Eds) Ranaviruses. Springer, Heidelberg, pp 71–104

  • Brunner JL, Beaty L, Guitard A, Russell D (2017) Heterogeneities in the infection process drive ranavirus transmission. Ecology 98:576–582

    Article  PubMed  Google Scholar 

  • Casadevall A, Pirofski L (2001) Host–pathogen interactions: the Attributes of virulence. The Journal of Infectious Diseases 184:337–344

    Article  CAS  PubMed  Google Scholar 

  • Cheng TL, Rovito SM, Wake DB, Vredenburg VT (2011) Coincident mass extirpation of neotropical amphibians with the emergence of the infectious fungal pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America 108:9502–9507

    Article  PubMed  PubMed Central  Google Scholar 

  • Chinchar VG (2002) Ranaviruses (family Iridoviridae): emerging cold-blooded killers. Archives of Virology 147:447–470

    Article  CAS  PubMed  Google Scholar 

  • Crawford AJ, Lips KR, Bermingham E (2010) Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences of the United States of America 107:13777–13782

    Article  PubMed  PubMed Central  Google Scholar 

  • Crowl TA, Crist TO, Parmenter RR, Belovsky G, Lugo AE (2008) The spread of invasive species and infectious disease as drivers of ecosystem change. Frontiers in Ecology and the Environment 6:238–246

    Article  Google Scholar 

  • Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  • Daszak P, Berger L, Cunningham AA, Hyatt AD, Green E, Speare R (2003) Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5:735–748

    Article  Google Scholar 

  • Daszak P, Scott DE, Kilpatrick AM, Faggioni C, Gibbons JW, Porter D (2005) Amphibian population declines at Savannah River Site are linked to climate, not chytridiomycosis. Ecology 86:3232–3237

    Article  Google Scholar 

  • Dowell SF (2001) Seasonal variation in host susceptibility and cycles of certain infectious diseases. Emerging Infectious Diseases 7:369–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frankham R (2008) Inbreeding and extinction: island populations. Conservation Biology 12:665–675

    Article  Google Scholar 

  • Gervasi S, Gondhalekar C, Olson DH, Blaustein AR (2013) Host identity matters in the amphibian-Batrachochytrium dendrobatidis system: fine-scale patterns of variation in responses to a multi-host pathogen. Public Library of Sciences One 8:e54490

    CAS  Google Scholar 

  • Gray M, Miller D, Schmutzer A, Baldwin C (2007) Frog virus 3 prevalence in tadpole populations inhabiting cattle-access and non-access wetlands in Tennessee, USA. Diseases of Aquatic Organisms 77:97–103

    Article  PubMed  Google Scholar 

  • Gray MJ, Miller DL, Hoverman JT (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243–266

    Article  PubMed  Google Scholar 

  • Green DE, Converse KA, Schrader AK (2002) Epizootiology of sixty-four amphibian morbidity and mortality events in the USA, 1996–2001. Annals of the New York Academy of Sciences 969:323–339

    Article  PubMed  Google Scholar 

  • Hanselmann R, Rodríguez A, Lampo M, Fajardo-Ramos L, Alonso Aguirre A, Marm Kilpatrick A, Paul Rodríguez J, Daszak P (2004) Presence of an emerging pathogen of amphibians in introduced bullfrogs Rana catesbeiana in Venezuela. Biological Conservation 120:115–119

    Article  Google Scholar 

  • Heinicke MP, Diaz LM, Hedges SB (2011) Origin of invasive Florida frogs traced to Cuba. Biology Letters 7:407–410

    Article  PubMed  PubMed Central  Google Scholar 

  • Horner AA, Hoffman EA, Tye MR, Hether TD, Savage AE (2017) Cryptic chytridiomycosis linked to climate and genetic variation in amphibian populations of the southeastern United States. Public Library of Sciences One 12:e0175843

    Google Scholar 

  • Hoverman JT, Gray MJ, Miller DL (2010) Anuran susceptibilities to ranaviruses: role of species identity, exposure route, and a novel virus isolate. Diseases of Aquatic Organisms 89:97–107

    Article  PubMed  Google Scholar 

  • Hoverman JT, Gray MJ, Miller DL, Haislip NA (2012) Widespread occurrence of ranavirus in pond-breeding amphibian populations. Ecohealth 9:36–48

    Article  PubMed  Google Scholar 

  • Hoyt JH (1967) Barrier island formation. Geological Society of America Bulletin 78:1125–1136

    Article  Google Scholar 

  • Isidoro-Ayza M, Lorch JM, Grear DA, Winzeler M, Calhoun DL, Barichivich WJ (2017) Pathogenic lineage of Perkinsea associated with mass mortality of frogs across the United States. Scientific Reports 7:1–10

    Article  CAS  Google Scholar 

  • Johnson AJ, Pessier AP, Wellehan JF, Childress A, Norton TM, Stedman NL, Bloom DC, Belzer W, Titus VR, Wagner R, Brooks JW, Spratt J, Jacobson ER (2008) Ranavirus infection of free-ranging and captive box turtles and tortoises in the United States. Journal of Wildlife Diseases 44:851–863

    Article  CAS  PubMed  Google Scholar 

  • Johnson PTJ, Rohr JR, Hoverman JT, Kellermanns E, Bowerman J, Lunde KB (2012) Living fast and dying of infection: host life history drives interspecific variation in infection and disease risk. Ecology Letters 15:235–242

    Article  PubMed  Google Scholar 

  • Jones KKE, Patel NGN, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karwacki E, Atkinson M, Ossiboff R, Savage A (2018) Novel quantitative PCR assay specific for the emerging Perkinsea amphibian pathogen reveals seasonal infection dynamics. Diseases of Aquatic Organisms 129:85–98

    Article  CAS  PubMed  Google Scholar 

  • Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468:647–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kiesecker JM, Blaustein AR, Belden LK (2001) Complex causes of amphibian population declines. Nature 410:681–684

    Article  CAS  PubMed  Google Scholar 

  • Kriger KM, Hero JM (2007) Large-scale seasonal variation in the prevalence and severity of chytridiomycosis. Journal of Zoology 271:352–359

    Google Scholar 

  • Landsberg JH, Kiryu Y, Tabuchi M, Waltzek TB, Enge KM, Reintjes-Tolen S, Preston A, Pessier AP (2013) Co-infection by alveolate parasites and frog virus 3-like ranavirus during an amphibian larval mortality event in Florida, USA. Diseases of Aquatic Organisms 105:89–99

    Article  PubMed  Google Scholar 

  • Lesbarrères D, Balseiro A, Brunner J, Chinchar VG, Duffus A, Kerby J, Miller DL, Robert J, Schock DM, Waltzek T, Gray MJ (2012) Ranavirus: past, present and future. Biology Letters 8:481–483.

    Article  PubMed  Google Scholar 

  • Lips KR, Mendelson III JR, Muñoz-Alonso A, Canseco-Márquez L, Mulcahy DG (2004) Amphibian population declines in montane southern Mexico: resurveys of historical localities. Biological Conservation 119:555–564

    Article  Google Scholar 

  • Lips KR, Diffendorfer J, Mendelson JR, Sears MW (2008) Riding the wave: RECONCILING the roles of disease and climate change in amphibian declines. Public Library of Sciences Biology 6:e72

    Google Scholar 

  • Meade T (2008) Lithobates sphenocephalus sphenocephalus (On-line). Animal Diversity Web. http://animaldiversity.org/accounts/Lithobates_sphenocephalus_sphenocephalus/. Accessed March 2018

  • Miller D, Gray M, Storfer A (2011) Ecopathology of ranaviruses infecting amphibians. Viruses 3:2351–2373

    PubMed  Google Scholar 

  • Moutou F, Pastoret PP (2010) Invasive reptiles and amphibians. Revue Scientifique et Technique 29:235–240

    CAS  PubMed  Google Scholar 

  • Nichols M. 2008. Hyla cinerea (On-line). Animal Diversity Web. http://animaldiversity.org/accounts/Hyla_cinerea/. Accessed March 2018

  • Olson CA, Beard KH, Pitt WC (2012) Biology and impacts of Pacific Island invasive species. 8. Eleutherodactylus planirostris, the greenhouse frog (Anura: Eleutherodactylidae) 1. Pacific Science 66:255–271

    Article  Google Scholar 

  • Olson DH, Aanensen DM, Ronnenberg KL, Powell CI, Walker SF, Bielby J, Garner TWJ, Weaver G, Fisher MC, Fisher MC (2013) Mapping the global emergence of Batrachochytrium dendrobatidis, the amphibian chytrid fungus. Public Library of Sciences One 8:e56802

    CAS  Google Scholar 

  • Piotrowski JS, Annis SL, Longcore JE (2004) Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96:9–15

    Article  PubMed  Google Scholar 

  • Pitt W, Vice D, Pitzler M (2005) Challenges of invasive reptiles and amphibians. Wildlife Damage Management Conference 84:112–119

    Google Scholar 

  • Pounds AJ, Bustamante MR, Coloma LA, Consuegra JA, Fogden MPL, Foster PN, La Marca E, Masters KL, Merino-Viteri A, Puschendorf R, Ron SR, Arturo Sanchez-Azofeifa G, Still CJ, Young BE (2006) Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/

  • Rizkalla CE (2010) Increasing detections of Batrachochytrium dendrobatidis in Central Florida, USA. Herpetological Review 41:180–181

    Google Scholar 

  • Robert J, Abramowitz L, Gantress J, Morales HD (2007). Xenopus laevis: a possible vector of ranavirus infection? Journal of Wildlife Diseases 43:645–652

    Article  CAS  PubMed  Google Scholar 

  • Rojas S, Richards K, Jancovich J, Davidson E (2005) Influence of temperature on ranavirus infection in larval salamanders Ambystoma tigrinum. Diseases of Aquatic Organisms 63:95–100

    Article  PubMed  Google Scholar 

  • Rosa GM, Sabino-Pinto J, Laurentino TG, Martel A, Pasmans F, Rebelo R, Griffiths RA, Stöhr AC, Marschang RE, Price SJ, Garner TW (2017) Impact of asynchronous emergence of two lethal pathogens on amphibian assemblages. Scientific Reports 7:43260

    Article  PubMed  PubMed Central  Google Scholar 

  • Rothermel B, Walls S, Mitchell J, Dodd C, Irwin L, Green D, Vazquez V, Petranka J, Stevenson D (2008) Widespread occurrence of the amphibian chytrid fungus Batrachochytrium dendrobatidis in the southeastern USA. Diseases of Aquatic Organisms 82:3–18

    Article  PubMed  Google Scholar 

  • Ruggeri J, Longo AV, Gaiarsa MP, Alencar LR, Lambertini C, Leite DS, Carvalho-e-Silva SP, Zamudio KR, Toledo LF, Martins M (2015) Seasonal variation in population abundance and chytrid infection in stream-dwelling frogs of the Brazilian Atlantic forest. PloS One 10:e0130554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savage AE, Sredl MJ, Zamudio KR (2011) Disease dynamics vary spatially and temporally in a North American amphibian. Biological Conservation 144:1910–1915

    Article  Google Scholar 

  • Savage AE, Zamudio KR (2011) MHC genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences of the United States of America 108:16705–16710

    Article  PubMed  PubMed Central  Google Scholar 

  • Savage AE, Becker CG, Zamudio KR (2015) Linking genetic and environmental factors in amphibian disease risk. Evolutionary Applications 8:560–572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Savage AE, Mulder KP, Torres T, Wells S (2018) Lost but not forgotten: MHC genotypes predict overwinter survival despite depauperate MHC diversity in a declining frog. Conservation Genetics 19:309–322

    Article  CAS  Google Scholar 

  • Schloegel LM, Picco AM, Kilpatrick AM, Davies AJ, Hyatt AD, Daszak P (2009) Magnitude of the US trade in amphibians and presence of Batrachochytrium dendrobatidis and ranavirus infection in imported North American bullfrogs (Rana catesbeiana). Biological Conservation 142:1420–1426

    Article  Google Scholar 

  • Searle CL, Gervasi SS, Hua J, Hammond JI, Relyea RA, Olson DH, Blaustein AR (2011) Differential host susceptibility to Batrachochytrium dendrobatidis, an emerging amphibian pathogen. Conservation Biology 25:965–974

    Article  CAS  PubMed  Google Scholar 

  • Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, Hines HB, Kenyon N (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. Ecohealth 4:125–134

    Article  Google Scholar 

  • Strauss A, White A, Boots M (2012) Invading with biological weapons: The importance of disease-mediated invasions. Functional Ecology 26:1249–1261

    Article  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786

    Article  CAS  PubMed  Google Scholar 

  • Virden T (2003) Hyla squirella (On-line). Animal Diversity Web. http://animaldiversity.org/accounts/Hyla_squirella/. Accessed March 2018

  • Vredenburg VT, Briggs CJ (2009) Chytrid Swab Protocol. AmphibiaWeb. https://amphibiaweb.org/chytrid/swab_protocol.html. Accessed June 2018

  • Zapata A, Varas A, Torroba M (1992) Seasonal variations in the immune system of lower vertebrates. Immunology Today 13:142–147

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Ethan Berman whose young passion for the health of amphibian populations inspired the design and financial support for this project. Ethan contacted Dr. Kimberly Andrews [author and then Research Coordinator at the Georgia Sea Turtle Center (GSTC)] in 2013 with a request for an internship to start an amphibian project. Dr. Terry Norton, DVM and GSTC Director, led the design on the sampling protocols for swab collection and issued the training for field personnel. We further thank the Jekyll Island Foundation for receiving private donations that made this project possible and for administering those funds. Personnel support was issued by the Jekyll Island Authority Georgia Sea Turtle Center, and field sampling was conducted by AmeriCorps members (Rick Bauer, Justin Fowler, Katie Parson, Hannah Royal, Sloane Wiggers, Miranda Miller, Kristin Hay, and Lindsey Gordon) who conducted their terms of service with the GSTC, including author KWC. Specifically, we thank Lisa Harrelson and Joseph Colbert who were instrumental in the design and the launch of field sampling in the first year of the project. We thank interns from the College of Coastal Georgia (Nicole DeSha), the University of Boston (Lucy McGinnis), the University of Georgia (Ethan Cooper), and the University of Georgia graduate students Darren Fraser, Lance Paden, and Davide Zailo who assisted AmeriCorps members and GSTC staff in field surveys and sample preservation. We also thank the University of Central Florida’s EXCEL and RAMP programs and the AAP department for their financial support throughout this project, members of the Savage Lab for providing valuable feedback on this manuscript, Ariel Horner for training, and Veronica Urgiles for assistance with ArcGIS.

Author information

Authors and Affiliations

  1. Department of Biology, University of Central Florida, 4110 Libra Dr, Orlando, FL, 32816, USA

    Brenda Rivera, Matthew S. Atkinson & Anna E. Savage

  2. Wyoming Natural Diversity Database, University of Wyoming, 1000 E. University Ave, Laramie, WY, 82071, USA

    Katrina Cook

  3. Odum School of Ecology, University of Georgia, UGA Marine Extension, Brunswick, GA, 31520, USA

    Kimberly Andrews

Authors
  1. Brenda Rivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katrina Cook
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kimberly Andrews
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matthew S. Atkinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anna E. Savage
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna E. Savage.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rivera, B., Cook, K., Andrews, K. et al. Pathogen Dynamics in an Invasive Frog Compared to Native Species. EcoHealth 16, 222–234 (2019). https://doi.org/10.1007/s10393-019-01432-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-019-01432-4

Keywords

Search

Navigation