Research

There are a growing number of infectious diseases that are negatively impacting wildlife populations. White-nose syndrome is devastating bats in North America, snake fungal disease is causing disfiguring malformations in several US states, and chronic wasting disease is killing cervids.  For amphibians, chytrid fungi and ranaviruses have been primary etiologic agents in widespread and localized die-offs.

The increasing emergence of infectious diseases is caused by a myriad of factors – generally linked to human activities. In particular, the global movement of infected animals (via unclean international trade) is resulting in spillover of novel pathogens to naïve populations on continents. Pathogens also are evolving enhance virulence in captive populations, which can spillover to the wild. 

Humans also affect disease processes by introducing environmental stressors and changing habitat conditions that affect host contact rates. Our goal is to identify the causes of disease emergence and devise disease management strategies that can be used by practitioners to control (or eradicate) outbreaks in wild and captive amphibian populations.

A collage of laboratory images featuring salamanders and their holding spaces.
UT’s JARTU Animal Research Facility facilitates various pathogen experiments in aquatic and terrestrial mesocosms (photos by Todd Amacker).

Research Projects

Current Projects

National Science Foundation, 2021-2025. Resilience Institute Bridging Biological Training and Research (RIBBiTR).

University of Tennessee One Health Initiative. 2021–2022. Socioeconomic epidemiology of disease risk in wildlife trade networks.

US Fish and Wildlife Service, 2019–2022. Competitive State Wildlife Grant (administered by Tennessee Wildlife Resources Agency). The threat of Batrachochytrium salamandrivorans (Bsal) to species of greatest conservation need and proactive development of disease management strategies.

National Science Foundation, 2018–2022. Division of Environmental Biology, Ecology and Evolution of Infectious Diseases Program. Transmission pathways and immunological factors driving invasion potential of the recently discovered pathogen, Batrachochytrium salamandrivorans.

Recently Completed Projects

Georgia Department of Natural Resources (administered by University of Florida), 2018–2020. Surveillance for chimeric ranavirus in southern Georgia.

BAND Foundation, Inc. (administered by the Association of Fish and Wildlife Agencies). 2017–2019. Bsal susceptibility trials for species of conservation concern.


Publications

Book Chapters

Islam R. M., Gray M. J., Peace A. 2021. Identifying the dominant transmission pathway in a multi-stage infection model of the emerging fungal pathogen Batrachochytrium salamandrivorans on the eastern newt. Pages 193-216 in M. I. Teboh-Ewungkem, G. A. Ngwa (eds.), Infectious Diseases and Our Planet, Mathematics of Planet Earth 7, New York: Springer. 

Wilber, M. Q., Johnson, P. T. J. and Briggs, C. J. 2019. ‘When chytrid fungus invades: integrating theory and data to understand disease-induced amphibian declines’, in Wilson, K., Fenton, A., and Tompkins, D. M. (eds) Wildlife Disease Ecology: Linking Theory to Data and Application. Cambridge, United Kingdom: Cambridge University Press.

Gray, M. J. and V. G. Chinchar. 2015. Introduction: History and future of ranaviruses. Pages 1–8 in M. J. Gray and V. G. Chinchar, editors. Ranaviruses: lethal pathogens of ectothermic vertebrates. Springer, New York.

Brunner, J. L., A. Storfer, M. J. Gray, and J. T. Hoverman. 2015. Ranavirus ecology and evolution: from epidemiology to extinction. Pages 71–104 in M. J. Gray and V. G. Chinchar, editors. Ranaviruses: lethal pathogens of ectothermic vertebrates. Springer, New York.

Gray, M. J., J. L. Brunner, J. E. Earl, and E. Ariel. 2015. Design and analysis of ranavirus studies: surveillance and assessing risk. Pages 209–240 in M. J. Gray and V. G. Chinchar, editors. Ranaviruses: lethal pathogens of ectothermic vertebrates. Springer, New York.

Green, D. E., M. J. Gray, and D. L. Miller. 2009. Disease monitoring and biosecurity.  Pages 481–505 in: C. K. Dodd, editor. Amphibian Ecology and Conservation: A Handbook of Techniques. Oxford University Press, Oxford, UK.

Amphibian Disease and Conservation Papers

Gray, M. J., E. D. Carter, J. P. D. Cusaac, A. C. Peterson, R. Whetstone, A. Hertz, M. C. Bletz, D. C. Woodhams, J. Piovia-Scott, J. Romansic, G. Parra Olea, R. Hardman, C. D. McCusker, and D. L. Miller.  In review. Broad host susceptibility of North American amphibian species to Batrachochytrium salamandrivorans suggests high invasion potential. Nature Communications.

Towe, A. E., M. J. Gray, E. D. Carter, R. J. Ossiboff, K. Ash, M. Bohanon, B. A. Bajo, and D. L. Miller. 2021. Batrachochytrium salamandrivorans can devour more than salamanders. Journal of Wildlife Diseases 57(4).​ DOI: 10.7589/JWD-D-20-00214.

Brunner, J. L., D. H. Olson, M. J. Gray, D. L. Miller, and A. L. J. Duffus. 2021. Global patterns of ranavirus detections. FACETS 6(1).

Tompros, A., A. D. Dean, A. Fenton, M. Wilber, E. D. Carter, and M. J. Gray. 2021. Frequency-dependent transmission of Batrachochytrium salamandrivorans in eastern newts. Transboundary and Emerging Diseases. DOI: 10.1111/tbed.14043 .

Olson, D. H., K. H. Hamon, M. J. Gray, R. N. Harris, T. Thompson, M. Iredale, M. Christman, J. Williams, M. J. Adams, and J. Ballard. 2021. Enhanced between-site biosecurity to minimize herpetofaunal disease-causing pathogen transmission. Herpetological Review 52(1), 29–39.  

Cusaac, J. P. W, E. D. Carter, D. C. Woodhams, J. Robert, J. A. Spatz, J. L. Howard, C. Lillard, A. W. Graham, R. D. Hill, S. Reinsch, D. McGinnity, B. Reeves, D. Bemis, R. P. Wilkes, W. B. Sutton, T. B. Waltzek, R. H. Hardman, D. L. Miller, and M. J. Gray. 2021. Emerging Pathogens and a Current-Use Pesticide: Potential Impacts on Eastern Hellbenders. Journal of Aquatic Animal Health. DOI: 10.1002/aah.10117.

Carter ED, Bletz MC, Le Sage M, LaBumbard B, Rollins-Smith LA, Woodhams DC, Miller DL, Gray MJ. 2021. Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans. PLoS Pathogens 17(2): e1009234. https://doi.org/10.1371/journal.ppat.1009234

Wilber MQ, Carter ED, Gray MJ, Briggs CJ. 2021. Putative resistance and tolerance mechanisms have little impact on disease progression for an emerging salamander pathogen. Functional Ecology. https://doi.org/10.1111/1365-2435.13754

Kumar, R., D. A. Malagon, E. D. Carter, D. L. Miller, M. L. Bohanon, J. P. W. Cusaac, A. C. Peterson, and M. J. Gray. 2020. Experimental methodologies can affect pathogenicity of Batrachochytrium salamandrivorans infections. PLoS ONE 15(9): e0235370. https://doi.org/10.1371/journal.pone.0235370​

Robinson, K. A., K. E. Pereira, M. C. Bletz, E. D. Carter, M. J. Gray, J. Piovia-Scott, J. M. Romansic, D. C. Woodhams, and L. Fritz-Laylin. 2020. Isolation and maintenance of Batrachochytrium salamandrivorans cultures. Diseases of Aquatic Organisms 140:1-11.

Pereira, K. E., M. J. Gray, J. L. Kerby, E. H. Campbell Grant, and J. Voyles. 2020. The next threat: how do we stop fungal disease from devastating North American salamanders? Wildlife Professional 14:41-46

Malagon, D. A., L. A. Melara, O. F. Proper, S. Lenhart, E. D. Carter, J. A. Fordyce, A. C. Peterson, D. L. Miller, and M. J. Gray. 2020. Host density and habitat structure influence host contact rates and Batrachochytrium salamandrivorans transmission. Scientific Reports 10, 5584. doi.org/10.1038/s41598-020-62351-x.

Deng, L., Y. Geng, R. Zhao, M. J. Gray, K. Wang, P. OuYang, D. Chen, X. Huang, Z. Chen, C. Huang, Z. Zhong, H. Guo, and J. Fang. In revision. CMTV-like ranavirus infection associated with high mortality of captive catfish-like loach, Triplophysa siluorides in China. Transboundary and Emerging Diseases. doi.org/10.1111/tbed.13473.

Carter, E. D., D. L. Miller, A. C. Peterson, W. B. Sutton, J. P. W. Cusaac, J. A. Spatz, L. Rollins-Smith, L. Reinert, M. Bohanon, L. A. Williams, A. Upchurch, and M. J. Gray. 2019. Conservation risk of Batrachochytrium salamandrivorans to endemic lungless salamanders. Conservation Letters 2019;e12675

Peace, A., S. M. O’Regan, J. A. Spatz, P. N. Reilly, R. D., Hill, E. D. Carter, R. P. Wilkes, T. B. Waltzek, D. L. Miller, and M. J. Gray. 2019. A highly invasive chimeric ranavirus can decimate tadpole populations rapidly through multiple transmission pathways. Ecological Modelling 410:108777.  

Ossiboff, R. J., A. E. Towe, M. A. Brown, A. V. Longo, K. R. Lips, D. L. Miller, E. D. Carter, M. J. Gray, and S. Frasca, Jr. 2019. Differentiating Batrachochytrium dendrobatidis and B. salamandrivorans in amphibian chytridiomycosis using RNAScope® in situ hybridization. Frontiers in Veterinary Science 6:304.

Canessa, S., A. Spitzen-van der Sluijs, T. Stark, B. E. Allen, P. J. Bishop, M. C. Bletz, C. J. Briggs, D. R. Daversa, M. J. Gray, et al. 2019. Conservation decisions under pressure: lessons from an exercise in rapid response to wildlife disease. Conservation Science and Practice 2019;e141

Mosher, B. A., A. B. Brand, A. N. M. Wiewel, D. A. W. Miller, M. J. Gray, D. L. Miller, and E. H. C. Grant. 2019. Estimating occurrence, prevalence, and detection of amphibian pathogens: insights from occupancy models. Journal of Wildlife Diseases 55:563-575.

Casais, R., A. R. Larrinaga, K. P. Dalton, P. Dominguez Lapido, I. Marquez, E. Becares, E. D. Carter, M. J. Gray, D. L. Miller, and A. Balseiro. 2019. Water sports could contribute to the translocation of ranaviruses. Scientific Reports 9:2340.

Gray, M. J., M. C. Allender, K. H. Haman, R. N. Harris, and D. H. Olson. 2018. Facilitating early detection and rapid response: an alert system to combat emerging herpetofaunal diseases. Wildlife Professional, 12:33-35

Adams, M. J., R. N. Harris, E. H. C. Grant, M. J. Gray, M. C. Hopkins, S. A. Inverson, R. Likens, et al. 2018. Prepublication of research results. EcoHealth 15:478-481.

Gray, M. J., J. A. Spatz, E. D. Carter, C. M. Yarber, R. P. Wilkes, and D. L. Miller. 2018. Poor biosecurity could lead to disease outbreaks in animal populations. PLoS ONE 13(3): e0193243.

Claytor, S. C., K. Subramaniam, N. Landrau-Giovannetti, V. G. Chinchar, M. J. Gray, D. L. Miller, C. Mavian, M. Salemi, S. Wisely, T. B. Waltzek. 2017. Ranavirus phylogenomics: signatures of recombination and inversions among bullfrog ranaculture isolates. Virology 511:330-343.
 
Price, S. J., E. Ariel, A. Maclaine, G. M. Rosa, M. J. Gray, J. L. Brunner, and T. W. J. Garner. 2017. From fish to frogs and beyond: Impact and host range of emergent ranaviruses. Virology 511:272-279.
 
Gray, M. J., A. L. J. Duffus, K. H. Haman, R. N. Harris, M. C. Allender, T. A. Thompson, M. R. Christman, A. Sacerdote-Velat, L. A. Sprague, J. M. Williams, and D. L. Miller. 2017. Pathogen surveillance in herpetofaunal populations: guidance on study design, sample collection, biosecurity, and intervention strategies. Herpetological Review 48:334-351.
 
Duffus, A. L. J., H. M. A. Fenton, M. J. Gray, and D. L. Miller. 2017. Investigating amphibian and reptile mortalities: a practical guide for wildlife professionals. Herpetological Review 48:550-557.
 
Grant, E. H., E. Muths, R. A. Katz, S. Canessa, M. J. Adams, J. R. Ballard, L. Berger, C. J. Briggs, J. T. H. Coleman, M. J. Gray, et al. 2017. Using decision analysis to support proactive management of emerging infectious wildlife diseases. Frontiers in Ecology and the Environment doi:10.1002/fee.1481.

Earl, J. E., J. C. Chaney, W. B. Sutton, C. E. Lillard, A. J. Kouba, C. Langhorne, J. Krebs, R. P. Wilkes, R. D. Hill, D. L. Miller, and M. J. Gray. 2016. Ranavirus could facilitate local extinction of rare amphibian species. Oecologia DOI 10.1007/s00442-016-3682-6.
 
Brand, M. D., R. D. Hill, R. Brenes, J. C. Chaney, R. P. Wilkes, L. Grayfer, D. L. Miller, and M. J. Gray. 2016. Water temperature affects susceptibility to ranavirus. EcoHealth 13:350-359.

Geng, Y., M. J. Gray, K. Wang, D. Chen, P. Ouyang, X. Huang, C. He, Z. Zhong, and Z. Yang. 2016. Pathological changes in Andrias davidianus infected with Chinese giant salamander ranavirus. Asian Herpetological Research 7:258-264.
 
Gray, M. J., J. P. Lewis, P. Nanjappa, B. Klocke, F. Pasmans, A. Martel et al. 2015. Batrachochytrium salamandrivorans: The North American response and a call for action.  PLOS Pathogens 11(12): e1005251. doi:10.1371/journal.ppat.1005251.
 
Blackburn, M., J. Wayland, W. H. Smith. J. H. McKenna, M. Harry, M. K. Hamed, M. J. Gray, and D. L. Miller. 2015. First report of ranavirus and Batrachochytrium dendrobatidis in green salamanders (Aneides aeneus) from Virginia, USA. Herpetological Review 46:357-361.
 
Sutton, W. B., M. J. Gray, R. H. Hardman, R. P. Wilkes, A. J. Kouba, and D. L. Miller. 2014. High susceptibility of the endangered dusky gopher frog to ranavirus. Diseases of Aquatic Organisms 112:9-16.
 
Sutton, W. B., M. J. Gray, J. T. Hoverman, R. G. Secrist, P. Super, R. H. Hardman, J. L. Tucker, and D. L. Miller. 2014. Trends in ranavirus prevalence among plethodontid salamanders in the Great Smoky Mountains National Park. EcoHealth DOI: 10.1007/s10393-014-0994-z.
 
Waltzek, T. B., D. L. Miller, M. J. Gray, et al. 2014. New disease records for hatchery-reared sturgeon. I. Expansion of Frog Virus 3 into Scaphirhynchus albusDiseases of Aquatic Organisms 111:219-227.
 
Earl, J. E., and M. J. Gray. 2014. Introduction of ranavirus to isolated wood frog population could cause local extinction. EcoHealth DOI: 10.1007/s10393-014-0950-y.
 
Wheelwright, N. T., M. J. Gray, R. D. Hill, and D. L. Miller  2014. Sudden mass die-off of a large population of wood frog (Lithobates sylvaticus) tadpoles in Maine, USA, likely due to ranavirus. Herpetological Review 45:240-242.
 
Brenes, R., D. L. Miller, T. B. Waltzek, R. P. Wilkes, J. L. Tucker, J. C. Chaney, R. H. Hardman, M. D. Brand, R. R. Huether, and M. J. Gray.  2014. Susceptibility of fish and turtles to three ranaviruses isolated from different ectothermic vertebrate classes. Journal of Aquatic Animal Health 26:118-126.
 
Brenes, R, M. J. Gray, T. B. Waltzek, R. P. Wilkes, and D. L. Miller.  2014. Transmission of ranavirus between ectothermic vertebrate hosts. PLoS ONE 9(3): e92476. doi:10.1371/journal.pone.0092476.
 
Gold, K. K., P. D. Reed, D. A. Bemis, D. L. Miller, M. J. Gray, and M. J. Souza. 2013. Efficacy of common disinfectants and terbinafine HCl at inhibiting the growth of Batrachochytrium dendobatidis in culture. Diseases of Aquatic Organisms 107:77-81.
 
Gray, M. J., and D. L. Miller. 2013. Rise of ranavirus: an emerging pathogen threatens ectothermic vertebrates. Wildlife Professional 7:51-55.
 
Hamed, M. K, M. J. Gray, and D. L. Miller. 2013. First Report of Ranavirus in Plethodontid Salamanders from the Mount Roger’s National Recreation Area, Virginia. Herpetological Review 44:455-457.
 
Richter, S. C., A. N. Drayer, J. R. Strong, C. S. Kross, D. L. Miller and M. J. Gray. 2013. High prevalence of ranavirus infection in permanent constructed wetlands in eastern Kentucky, USA. Herpetological Review 44:464-466.
 
Haislip, N. A., J. T. Hoverman, D. L. Miller, and M. J. Gray. 2012. Natural stressors and disease risk: does the threat of predation increase amphibian susceptibility to ranavirus? Canadian Journal of Zoology 90:893-902.
 
Souza, M. J., M. J. Gray, P. Colclough, and D. L. Miller. 2012. Prevalence of infection by Batrachochytrium dendrobatidis and ranavirus in eastern hellbenders in eastern Tennessee. Journal of Wildlife Diseases 48:560-566.
 
O’Bryan, C. J., M. J. Gray, and C. S. Brooks. 2012. Further presence of ranavirus infection in amphibian populations of Tennessee, USA. Herpetological Review 43:293-295.
 
Gray, M. J., D. L. Miller and J. T. Hoverman. 2012. Reliability of non-lethal surveillance methods for detecting ranavirus infection. Diseases of Aquatic Organisms 99:1-6.
 
Hoverman, J. T., M. J. Gray, D. L. Miller and N. A Haislip. 2011. Widespread occurrence of ranavirus in pond-breeding amphibian populations. EcoHealth DOI: 10.1007/s10393-011-0731-9.
 
Miller, D. L., M. J. Gray, A. Storfer. 2011. Ecopathology of ranaviruses infecting amphibians. Viruses 3:2351-2373.
 
Lesbarrères, D., A. Balseiro, J. Brunner, V. G. Chinchar, A. Duffus, J. Kerby, D. L. Miller, J. Robert, D. M. Schock, T. Waltzek, and M. J. Gray. 2011. Ranavirus: past, present and future. Biology Letters 7: doi: 10.1098/rsbl.2011.0951.
 
Hoverman, J. T., M. J. Gray, N. A. Haislip, and D. L. Miller. 2011. Phylogeny, life history, and ecology contribute to differences in amphibian susceptibility to ranaviruses. EcoHealth 8:301-319.
 
Haislip, N.A., M. J. Gray, J. T. Hoverman, and D. L. Miller. 2011. Development and disease: how susceptibility to an emerging pathogen changes through anuran development. PLoS ONE 6(7): e22307. doi:10.1371/journal.pone.0022307.
 
Hoverman, J. T., M. J. Gray, and D. L. Miller. 2010. Anuran susceptibilities to ranaviruses: the role of species identity, exposure route, and a novel virus isolate. Diseases of Aquatic Organisms 89:97-107.
 
Miller, D. L., and M. J. Gray. 2010. Amphibian decline and mass mortality: The value of visualizing ranavirus in tissue sections. The Veterinary Journal 182:133-134.
 
Gray, M. J., D. L. Miller, and J. T. Hoverman. 2009. Ecology and pathology of amphibian ranaviruses. Diseases of Aquatic Organisms 87:243-266.
 
Gray, M. J., D. L. Miller, and J. T. Hoverman. 2009. First report of Ranavirus infecting lungless salamanders. Herpetological Review 40:316-319.
 
Todd-Thompson, M., D. L. Miller, P. E. Super, and M. J. Gray. 2009. Chytridiomycosis-associated mortality in a Rana palustris collected in Great Smoky Mountains National Park, Tennessee, USA. Herpetological Review 40:321-323.
 
Miller, D. L., M. J. Gray, S. Rajeev, A. C. Schmutzer, E. C. Burton, A. Merrill, and C. A. Baldwin. 2009. Pathologic findings in larval and juvenile anurans inhabiting farm ponds in Tennessee, U.S.A. Journal of Wildlife Diseases 45:314-324.
 
Bryan, L. K., C. A. Baldwin, M. J. Gray, and D. L. Miller. 2009. Efficacy of select disinfectants at inactivating Ranavirus. Diseases of Aquatic Organisms 84:89-94.
 
Burton, E. C., M. J. Gray, A. C. Schmutzer and D. L. Miller. 2009. Differential responses of postmetamorphic amphibians to cattle grazing in wetlands. Journal of Wildlife Management 73:269-277.
 
Schmutzer, A. C., M. J. Gray, E. C. Burton, and D. L. Miller. 2008. Impacts of cattle on amphibian larvae and the aquatic environment. Freshwater Biology 53:2613-2625.
 
Burton, E. C., D. L. Miller, E. L. Styer, and M. J. Gray. 2008. Amphibian ocular malformation associated with Frog virus 3. The Veterinary Journal 177:442-444.
 
Gray, M. J., D. L. Miller, A. C. Schmutzer, and C. A. Baldwin. 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.
 
Gray, M. J., S. Rajeev, D. L. Miller, A. C. Schmutzer, E. C. Burton, E. D. Rogers, and G. J. Hickling. 2007. Preliminary evidence that American bullfrogs (Rana catesbeiana) are suitable hosts for Escherichia coli O157:H7. Applied and Environmental Microbiology 73:4066-4088.
 
Gray, M. J., L. M. Smith, D. L. Miller, and C. R. Bursey. 2007. Influences of agricultural land use on Clinostomum attenuatum metacercariae prevalence in Southern Great Plains amphibians, U.S.A. Herpetological Conservation and Biology 2:23-28.
 
Burton, E. C., M. J. Gray, and A. C. Schmutzer. 2007. Comparison of anuran call survey durations in Tennessee wetlands. Proceedings of the Southeastern Association of Fish and Wildlife Agencies 60:15-18.
 
Miller, D. L., S. Rajeev, M. J. Gray, and C. A. Baldwin. 2007. Frog virus 3 infection, cultured American bullfrogs. Emerging Infectious Diseases 13:342-343.
 
Gray, M. J., and L. M. Smith. 2005. Influence of land use on postmetamorphic body size of playa lake amphibians. Journal of Wildlife Management 69:515-524.
 
Gray, M. J., D. L. Miller, and L. M. Smith. 2005. Coelomic response and signal range of implant transmitters in Bufo cognatusHerpetological Review 36:285-288.
 
Gray, M. J., L. M. Smith, and R. Brenes. 2004. Effects of agricultural cultivation on demographics of Southern High Plains amphibians. Conservation Biology 18:1368-1377.
 
Gray, M. J., L. M. Smith, and R. I. Leyva. 2004. Influence of agricultural landscape structure on a Southern High Plains, USA, amphibian assemblage. Landscape Ecology 19:719-729.
 
Smith, L. M., M. J. Gray, and A. Quarrels. 2004. Diets of newly metamorphosed amphibians in west Texas playas. Southwestern Naturalist 46:257-263.
 
Miller, D. L., C. R. Bursey, M. J. Gray, and L. M. Smith. 2004. Metacercaria of Clinostomum attenuatum (Digenea) in Ambystoma tigrinum mavortiumBufo cognatus, and Spea multiplicata from west Texas. Journal of Helminthology 78:373-376.
 
Gonzalez, Z., D. A. Ray, L. R. McAliley, M. J. Gray, C. Perchellet, L. M. Smith, and L. D. Densmore. 2004. Five polymorphic microsatellite markers for the Great Plains toad, Bufo cognatus. Molecular Ecology Notes 4:9−10.


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