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Mosquitoes as a Potential Vector of Ranavirus Transmission in Terrestrial Turtles

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Abstract

Ranaviruses are significant pathogens of amphibians, reptiles, and fishes, contributing to mass mortality events worldwide. Despite an increasing focus on ranavirus ecology, our understanding of ranavirus transmission, especially among reptilian hosts, remains limited. For example, experimental evidence for oral transmission of the virus in chelonians is mixed. Consequently, vector-borne transmission has been hypothesized in terrestrial turtle species. To test this hypothesis, mosquitoes captured during a 2012/2013 ranavirus outbreak in box turtles from southwestern Indiana were pooled by genus and tested for ranavirus DNA using qPCR. Two of 30 pools tested positive for ranavirus. Additionally, an individual Aedes sp. mosquito observed engorging on a box turtle also tested positive for ranavirus. Although our approach does not rule out the possibility that the sequenced ranavirus was simply from virus in bloodmeal, it does suggests that mosquitoes may be involved in virus transmission as a mechanical or biological vector among ectothermic vertebrates. While additional studies are needed to elucidate the exact role of mosquitoes in ranavirus ecology, our study suggests that a greater focus on vector-borne transmission may be necessary to fully understand ranaviral disease dynamics in herpetofauna.

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References

  • Allender MC, Abd-Eldaim M, Schumacher J, McRuer, D, Christian LS, Kennedy M (2011) PCR prevalence of Ranavirus in free ranging eastern box turtles (Terrapene carolina carolina) at rehabilitation centers in three southeastern US states. Journal of Wildlife Diseases 47:759-764

    Article  PubMed  Google Scholar 

  • Allender MC, Fry MM, Irizarry AR, Craig L, Johnson AJ, Jones M (2006) Intracytoplasmic inclusions in circulating leukocytes from an eastern box turtle (Terrapene carolina carolina) with iridoviral infection. Journal of Wildlife Diseases 42:677-684

    Article  PubMed  Google Scholar 

  • Allender MC, Mitchell MM, McRuer D, Christian S, Byrd J (2013) Prevalence, clinical signs, and natural history characteristics of frog virus 3-like infections in eastern box turtles (Terrapene carolina carolina). Herpetological Conservation and Biology 8:308-320

    Google Scholar 

  • Alto BW, Juliano SA (2001) Precipitation and temperature effects on populations of Aedes albopictus (Diptera: Culicidae): implications for range expansion. Journal of Medical Entomology 38:646

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barker CM, Paulson SL, Cantrell S, Davis BS (2003) Habitat Preferences and Phenology of Ochlerotatus triseriatus and Aedes albopictus (Diptera: Culicidae) in Southwestern Virginia. Journal of Medical Entomology 40:403-410

    Article  CAS  PubMed  Google Scholar 

  • Bataille A, Cunningham AA, Cedeña V, Pitaño L, Constantinou A, Kramer LD, Goodman SJ (2009) Natural colonization and adaptation of a mosquito species in Galápagos and its implication for disease threats to endemic wildlife. Proceedings of the National Academy of Sciences 106:10230-10235

    Article  CAS  Google Scholar 

  • Behncke H, Stöhr AC, Heckers KO, Ball I, Marschang RE (2013) Mass-mortality in green striped tree dragons (Japalura spendida) associated with multiple viral infections. Veterinary Record. doi:10.1136/vr.101545

    PubMed  Google Scholar 

  • Belzer WR, Seibert S (2011) A natural history of Ranavirus in an eastern box turtle population. Turtle and Tortoise Newsletter 15:18-25

    Google Scholar 

  • Brenes R, Gray MJ, Waltzek TB, Wilkes RP, Miller DL (2014) Transmission of ranavirus between ectothermic vertebrate hosts. PLOS ONE 3:e92476

    Article  Google Scholar 

  • Brunner JL, Richards K, Collins JP (2005) Dose and host characteristics influence virulence of ranavirus infection. Oecologia 144:399-406

    Article  PubMed  Google Scholar 

  • Brunner JL, Schock DM, Collins JP (2007) Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95

    Article  CAS  PubMed  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

    Article  Google Scholar 

  • Crans WJ, Rockel EG (1968) The mosquitoes attracted to turtles. Mosquito News. 28:332-337

    Google Scholar 

  • Dalrymple JM, Joung OP, Eldggridge BF, Russel PK (1972) Ecology of arboviruses in a Maryland freshwater swamp. American Journal of Epidemiology 96:129-140

    CAS  PubMed  Google Scholar 

  • De Voe R, Geissler K, Elmore S, Rotstein D, Lewbart G, Guy J (2004) Ranavirus-associated morbidity and mortality in a group of captive eastern box turtles (Terrapene carolina carolina). Journal of Zoo and Wildlife Medicine 35:534-543

    Article  PubMed  Google Scholar 

  • Farnsworth SD, Seigel RA (2013) Responses, movements, and survival of relocated box turtles during contruction of the intercounty connector highway in Maryland. Transportation Research Record 2362:1-8

    Article  Google Scholar 

  • Greer AL, Collins JP (2007) Sensitivity of a diagnostic test for amphibian ranavirus varies with sampling protocol. Journal of Wildlife Diseases 43:525-532

    Article  PubMed  Google Scholar 

  • Gruia-Gray J, Desser SS (1992) Cytopathological observation and epizootiologyt of frog erythrocytic virus in bullfrogs (Rana catesbieana). Journal of Wildlife Diseases 28:34-41

    Article  CAS  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

    Article  PubMed  Google Scholar 

  • Hayes J (1965) New host record for Aedes canadensis. Mosquito News 21:179-187

    Google Scholar 

  • Jancovich JK, Bremont M, Touchman JW, Jacobs BL (2010) Evidence for multiple recent host species shifts among the ranaviruses (family Iridoviridae). Journal of Virology 84:2636-2647

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jancovich JK, Davidson EW, Morado JF, Jacobs BL, Collins JP (1997) Isolation of a lethal virus from the endangered tiger salamander Ambystoma tigrinum stebbinsi. Diseases of Aquatic Organisms 31:161-167

    Article  Google Scholar 

  • Johnson AJ, Pessier AP, Wellehan JF, Childress A, Norton TM, Stedman NL, Wagner R (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 A, Pessier A, Jacobson E (2007) Experimental transmission and induction of ranaviral disease in western ornate box turtles (Terrapene ornata ornata) and red-eared sliders (Trachemys scripta elegans). Veterinary Pathology Online 44:285-297

    Article  CAS  Google Scholar 

  • Mao J, Hedrick RP, Chinchar VG (1997) Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229:212-220

    Article  CAS  PubMed  Google Scholar 

  • Marra PP, Griffing S, Caffrey C, Kilpatrick AM, McLean R, Brand C, Saito E, Dupuis AP, Kramer L, Novak R (2004) West Nile Virus and wildlife. BioScience 54:393-402

    Article  Google Scholar 

  • Marshchang RE (2011) Viruses infective reptiles. Viruses 3:2087-2126

    Article  Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Molaei G, Andreadis TG, Armstrong PM, Diuk-Wasser M (2008) Host-feedig patterns of potential mosquito vectors in Connecticut, USA: molecular analysis of bloodmeals from 23 species of Aedes, Anopholes, Coquillettidia, Psorophora, and Uranotaenia. Journal of Medical Entomology 45:1143-1151

    Article  CAS  PubMed  Google Scholar 

  • Nasci RS, Fischer M, Lindsey NP, Lanciotti RS, Savage HM, Komar N, McAllister JC, Mutebi J-P, Lavelle JM, Zeilinski-Gutierrez E, Petersen LR (2013) West Nile Virus in the United States: Guidelines for surveillance, prevention, and control. Center for Disease Control, Fort Collins, Colorado

    Google Scholar 

  • Pearman PB, Garner TW, Straub M, Greber UF (2004) Response of the Italian agile frog (Rana latastei) to a Ranavirus, frog virus 3: a model for viral emergence in naive populations. Journal of Wildlife Diseases 40:660-669

    Article  PubMed  Google Scholar 

  • Roberts DR, Laughlin LL, Hsheih P, Legters LJ (1997) DDT, global strategies, and a malaria control crisis in South America. Emerging Infectious Diseases 3:295-302

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Springs Harbor Press, Cold Springs Harbor, New York

    Google Scholar 

  • Stöhr A, Blahak S, Heckers KO, Wiechert J, Behncke H, Mathes K, Günther P, Swart P, Ball I, Rüschoff B, Marschange RE (2013) Ranavirus infections associated with skin lesions in lizards. Veterinary Research 44:84

    Article  PubMed Central  PubMed  Google Scholar 

  • Swanson J, Lancaster M, Anderson J, Crandell M, Haramis L, Grimstad P, Kitron U (2000) Overwintering and establishment of Aedes albopictus (Diptera: Culicidae) in an urban La Crosse virus enzootic site in Illinois. Journal of Medical Entomology 37:454-460

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28:2731-2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3 – new capabilities and interfaces. Nucleic Acids Research 40:e115

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Whittington RJ, Becker JA, Dennis MM (2010) Iridovirus infections in finfish – critical review with emphasis on ranaviruses. Journal of Fish Diseases 33:95-122

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful for the assistance of C. Bienz, K. DeRolf, O. Hernandez-Gomez, M. Hiatt, S. Klueh-Mundy, J. Keith, B. and V. McCoy, J. Mirtl, F. Owens, S. Raiman, A. Rohde, J. Rucker and his amazing turtle dogs, K. Smith, A. Wang, M. Wedge, V. Wuerthner, B. Zinman, and C. Rich. Support was provided by the Indiana Department of Natural Resources, Division of Fish and Wildlife, Wildlife Diversity Section, State Wildlife Improvement Grant E2-14-WDP001 and the Department of Forestry and Natural Resources, Purdue University. Turtles were collected and housed under the auspices of the Indiana Department of Natural Resources and the United States Fish and Wildlife Services and sampled under IACUC protocol 1303000835 from Purdue University.

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Correspondence to Steven J. A. Kimble.

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S. J. A. Kimble and A. K. Karna contributed equally to this work.

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Kimble, S.J.A., Karna, A.K., Johnson, A.J. et al. Mosquitoes as a Potential Vector of Ranavirus Transmission in Terrestrial Turtles. EcoHealth 12, 334–338 (2015). https://doi.org/10.1007/s10393-014-0974-3

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  • DOI: https://doi.org/10.1007/s10393-014-0974-3

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