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.
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
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
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
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
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
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
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
Belzer WR, Seibert S (2011) A natural history of Ranavirus in an eastern box turtle population. Turtle and Tortoise Newsletter 15:18-25
Brenes R, Gray MJ, Waltzek TB, Wilkes RP, Miller DL (2014) Transmission of ranavirus between ectothermic vertebrate hosts. PLOS ONE 3:e92476
Brunner JL, Richards K, Collins JP (2005) Dose and host characteristics influence virulence of ranavirus infection. Oecologia 144:399-406
Brunner JL, Schock DM, Collins JP (2007) Transmission dynamics of the amphibian ranavirus Ambystoma tigrinum virus. Diseases of Aquatic Organisms 77:87-95
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
Crans WJ, Rockel EG (1968) The mosquitoes attracted to turtles. Mosquito News. 28:332-337
Dalrymple JM, Joung OP, Eldggridge BF, Russel PK (1972) Ecology of arboviruses in a Maryland freshwater swamp. American Journal of Epidemiology 96:129-140
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
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
Greer AL, Collins JP (2007) Sensitivity of a diagnostic test for amphibian ranavirus varies with sampling protocol. Journal of Wildlife Diseases 43:525-532
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
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
Hayes J (1965) New host record for Aedes canadensis. Mosquito News 21:179-187
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
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
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
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
Mao J, Hedrick RP, Chinchar VG (1997) Molecular characterization, sequence analysis, and taxonomic position of newly isolated fish iridoviruses. Virology 229:212-220
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
Marshchang RE (2011) Viruses infective reptiles. Viruses 3:2087-2126
Miller D, Gray M, Storfer A (2011) Ecopathology of ranaviruses infecting amphibians. Viruses 3:2351-2373
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
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
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
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
Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Springs Harbor Press, Cold Springs Harbor, New York
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
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
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
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
Whittington RJ, Becker JA, Dennis MM (2010) Iridovirus infections in finfish – critical review with emphasis on ranaviruses. Journal of Fish Diseases 33:95-122
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
S. J. A. Kimble and A. K. Karna contributed equally to this work.
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10393-014-0974-3