Skip to main content

Advertisement

Log in

Sustained Ranavirus Outbreak Causes Mass Mortality and Morbidity of Imperiled Amphibians in Florida

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

Abstract

A persistent 2-month long outbreak of Ranavirus in a natural community of amphibians contributed to a mass die-off of gopher frog tadpoles (Lithobates capito) and severe disease in striped newts (Notophthalmus perstriatus) in Florida. Ongoing mortality in L. capito and disease signs in N. perstriatus continued for 5 weeks after the first observation. Hemorrhagic disease and necrosis were diagnosed from pathological examination of L. capito tadpoles. We confirmed detection of a frog virus 3 (FV3)-like Ranavirus via quantitative PCR in all species. Our findings highlight the susceptibility of these species to Rv and the need for long-term disease surveillance during epizootics.

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

Access this article

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

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3

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. https://doi.org/10.1016/j.jviromet.2012.12.012

    Article  CAS  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. https://doi.org/10.3354/dao060141

    Article  CAS  PubMed  Google Scholar 

  • Brenes R, Gray MJ, Waltzek TB, Wilkes RP, Miller DL (2014) Transmission of ranavirus between ectothermic vertebrate hosts. PLoS ONE 9:e92476. https://doi.org/10.1371/journal.pone.0092476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunner JL, Schock DM, Davidson EW, Collins JP (2004) Intraspecific reservoirs: complex life history and the persistence of a lethal ranavirus. Ecology 85:560–566. https://doi.org/10.1890/02-0374

    Article  Google Scholar 

  • Brunner JL, Storfer A, Gray MJ, Hoverman JT (2015) Ranavirus Ecology and Evolution: From Epidemiology to Extinction. In: Ranaviruses Cham: Springer, pp 71–104

    Google Scholar 

  • Cozad RA, Norton TM, Aresco MJ, Allender MC, Hernandez SM (2020) Pathogen surveillance and detection of ranavirus (frog virus 3) in translocated gopher tortoises (Gopherus polyphemus). Journal of Wildlife Diseases 56:679. https://doi.org/10.7589/2019-02-053

    Article  CAS  PubMed  Google Scholar 

  • Dodd CK (1993) Cost of living in an unpredictable environment: the ecology of striped newts Notophthalmus perstriatus during a prolonged drought. Copeia 1993:605. https://doi.org/10.2307/1447221

    Article  Google Scholar 

  • Dodd CK (1996) Use of terrestrial habitats by amphibians in the sandhill uplands of north-central Florida. Alytes 14:42–52

    Google Scholar 

  • Duffus ALJ, Waltzek TB, Stöhr AC, Allender MC, Gotesman M, Whittington RJ, Hick P, Hines MK, Marschang RE (2015) Distribution and Host Range of Ranaviruses. In: Gray MJ, Chinchar VG (eds) Ranaviruses: Lethal Pathogens of Ectothermic Vertebrates Cham: Springer International Publishing, pp 9–57

    Google Scholar 

  • Earl JE, Chaney JC, Sutton WB, Lillard CE, Kouba AJ, Langhorne C, Krebs J, Wilkes RP, Hill RD, Miller DL, Gray MJ (2016) Ranavirus could facilitate local extinction of rare amphibian species. Oecologia 182:611–623. https://doi.org/10.1007/s00442-016-3682-6

    Article  PubMed  Google Scholar 

  • Enge KM, Farmer AL, Mays JD, Castellón TD, Hill PE, Moler PE (2014) Survey of winter-breeding amphibian species. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Lovett E. Williams, Jr. Wildlife Research Laboratory, Gainesville, Florida, USA

  • Farmer AL, Enge KM, Jensen JB, Stevenson DJ, Smith LL (2017) A range-wide assessment of the status and distribution of the striped newt (Notophthalmus perstriatus). Herpetological Conservation and Biology 12:585–598

    Google Scholar 

  • Fisher MC, Garner TWJ (2020) Chytrid fungi and global amphibian declines. Nature Reviews Microbiology. https://doi.org/10.1038/s41579-020-0335-x

    Article  PubMed  Google Scholar 

  • Florida State Wildlife Action Plan (2019) Florida Fish and Wildlife Conservation Commission

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Gray M, Miller D, Hoverman J (2009) Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243–266. https://doi.org/10.3354/dao02138

    Article  PubMed  Google Scholar 

  • Gray M, Miller D, Hoverman J (2012) Reliability of non-lethal surveillance methods for detecting ranavirus infection. Diseases of Aquatic Organisms 99:1–6. https://doi.org/10.3354/dao02436

    Article  CAS  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. https://doi.org/10.1111/j.1749-6632.2002.tb04400.x

    Article  PubMed  Google Scholar 

  • Harp EM, Petranka JW (2006) Ranavirus in wood frogs (Rana sylvatica): potential sources of transmission within and between ponds. Journal of Wildlife Diseases 42:307–318. https://doi.org/10.7589/0090-3558-42.2.307

    Article  PubMed  Google Scholar 

  • Hoverman JT, Gray MJ, Haislip NA, Miller DL (2011) Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth 8:301–319. https://doi.org/10.1007/s10393-011-0717-7

    Article  PubMed  Google Scholar 

  • Hyatt A, Boyle D, Olsen V, Boyle D, Berger L, Obendorf D, Dalton A, Kriger K, Hero M, Hines H, Phillott 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. https://doi.org/10.3354/dao073175

    Article  CAS  PubMed  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 7:10288. https://doi.org/10.1038/s41598-017-10456-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jackson DR, Milstrey EG (1989) The fauna of gopher tortoise burrows. Florida Game and Fresh Water Fish Commission Nongame Wildlife Program, Gopher tortoise relocation symposium proceedings

  • Jensen JB, Richter SC (2005) Rana capito, Gopher Frogs. In: Amphibian Declines: The Conservation Status of United States Species. University of California Press, Berkeley, California, pp 536–538

  • Johnson SA (2002) Life history of the striped newt at a north-central Florida breeding pond. Southeastern Naturalist 1:381–402. https://doi.org/10.1656/1528-7092(2002)001[0381:LHOTSN]2.0.CO;2

    Article  Google Scholar 

  • Johnson AJ, Pessier AP, Wellehan JFX, 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. https://doi.org/10.7589/0090-3558-44.4.851

    Article  CAS  PubMed  Google Scholar 

  • Krysko KL, Burgess JP, Rochford MR, Gillette CR, Cueva D, Enge KM, Somma LA, Stabile JL, Smith DC, Wasilewski JA, Kieckhefer GN III, Granatosky MC, Nielsen SV (2011) Verified non-indigenous amphibians and reptiles in Florida from 1863 through 2010: Outlining the invasion process and identifying invasion pathways and stages. Zootaxa 3028:1. https://doi.org/10.11646/zootaxa.3028.1.1

    Article  Google Scholar 

  • LaClaire LV (1995) Vegetation of selected upland temporary ponds in North and North-central Florida. Bulletin of the Florida Museum of Natural History 38:69–96

    Google Scholar 

  • Landsberg J, Kiryu Y, Tabuchi M, Waltzek T, Enge K, Reintjes-Tolen S, Preston A, Pessier A (2013) Co-infection by alveolate parasites and frog virus 3-like ranavirus during an amphibian larval mortality event in Florida, USA. Dis Aquat Org 105:89–99. https://doi.org/10.3354/dao02625

    Article  Google Scholar 

  • Means RC, Means RPM, Beshel M, Mendyk R, Hill P, Summerford B, Elkert A, Gray MJ, Miller DL (2016) A Conservation Strategy for the Imperiled Western Striped Newt in the Apalachicola National Forest, FL

  • Means RC, Means RPM, Beshel M, Mendyk R, Hill P, Hoffman M, Reichling S, Summerford B (2017) A Conservation Strategy for the Imperiled Western Striped Newt in the Apalachicola National Forest, FL

  • Miller D, Gray M, Storfer A (2011) Ecopathology of Ranaviruses infecting amphibians. Viruses 3:2351–2373. https://doi.org/10.3390/v3112351

    Article  PubMed  PubMed Central  Google Scholar 

  • Noss RF, Platt WJ, Sorrie BA, Weakley AS, Means DB, Costanza J, Peet RK (2015) How global biodiversity hotspots may go unrecognized: lessons from the North American Coastal Plain. Diversity and Distributions 21:236–244. https://doi.org/10.1111/ddi.12278

    Article  Google Scholar 

  • Peace A, O’Regan SM, Spatz JA, Reilly PN, Hill RD, Carter ED, Wilkes RP, Waltzek TB, Miller DL, Gray MJ (2019) A highly invasive chimeric ranavirus can decimate tadpole populations rapidly through multiple transmission pathways. Ecological Modelling 410:108777. https://doi.org/10.1016/j.ecolmodel.2019.108777

    Article  Google Scholar 

  • Petranka JW, Harp EM, Holbrook CT, Hamel JA (2007) Long-term persistence of amphibian populations in a restored wetland complex. Biological Conservation 138:371–380. https://doi.org/10.1016/j.biocon.2007.05.002

    Article  Google Scholar 

  • Rachowicz LJ, Knapp RA, Morgan JAT, Stice MJ, Vredenburg VT, Parker JM, Briggs CJ (2006) Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87:1671–1683. https://doi.org/10.1890/0012-9658(2006)87[1671:EIDAAP]2.0.CO;2

    Article  PubMed  Google Scholar 

  • Rothermel BB, Miller DL, Travis ER, McGuire JLG, Jensen JB, Yabsley MJ (2016) Disease dynamics of red-spotted newts and their anuran prey in a montane pond community. Diseases of Aquatic Organisms 118:113–127. https://doi.org/10.3354/dao02965

    Article  CAS  PubMed  Google Scholar 

  • Scheele BC, Pasmans F, Skerratt LF, Berger L, Martel A (2019) Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363:1459–1463

    Article  CAS  Google Scholar 

  • Schloegel LM, Ferreira CM, James TY, Hipolito M, Longcore JE, Hyatt AD, Yabsley M, Martins AMCRPF, Mazzoni R, Davies AJ, Daszak P (2010) The North American bullfrog as a reservoir for the spread of Batrachochytrium dendrobatidis in Brazil. Animal Conservation 13:53–61. https://doi.org/10.1111/j.1469-1795.2009.00307.x

    Article  Google Scholar 

  • Stegen G, Pasmans F, Schmidt BR, Rouffaer LO, Van Praet S, Schaub M, Canessa S, Laudelout A, Kinet T, Adriaensen C, Haesebrouck F, Bert W, Bossuyt F, Martel A (2017) Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature 544:353–356. https://doi.org/10.1038/nature22059

    Article  CAS  PubMed  Google Scholar 

  • Tompkins DM, Carver S, Jones ME, Krkošek M, Skerratt LF (2015) Emerging infectious diseases of wildlife: a critical perspective. Trends in Parasitology 31:149–159. https://doi.org/10.1016/j.pt.2015.01.007

    Article  PubMed  Google Scholar 

  • U.S. Fish and Wildlife Service (USFWS) (2011) Endangered and threatened wildlife and plants; 12-month finding on a petition to list the Striped Newt as threatened

  • U.S. Fish and Wildlife Service (USFWS) (2016) Endangered and threatened wildlife and plants; review of native species that are candidates for listing as endangered or threatened; annual notice of findings on resubmitted petitions; annual description of progress on listing actions

Download references

Acknowledgements

We thank B. Folt (USGS) and L. Brendel (UF) for helping with sample collection, the staff of the Histology Laboratory at University of Florida's College of Veterinary Medicine for slide preparation, and the staff at Ordway-Swisher Biological Station for facilitating this work. Sampling was carried out under the permission of the Florida Fish and Wildlife Conservation Commission (FWC-LSSC-17-00031B) and the University of Florida’s Institutional Animal Care and Use Committee (#201810502). We thank members of the Longo Lab, S. Cassidy, and two anonymous reviewers for their feedback on previous drafts of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Arik M. Hartmann.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hartmann, A.M., Maddox, M.L., Ossiboff, R.J. et al. Sustained Ranavirus Outbreak Causes Mass Mortality and Morbidity of Imperiled Amphibians in Florida. EcoHealth 19, 8–14 (2022). https://doi.org/10.1007/s10393-021-01572-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10393-021-01572-6

Keywords

Navigation