Sharing habitat and sharing diseases?

Arik Hartmann

PhD Student at the University of Florida

November 2022

Ranaviruses are emerging pathogens widely associated with amphibian die-offs, but they also infect reptile and fish hosts, posing a significant threat to entire communities of ectothermic vertebrates (Brunner et al. 2015). These viruses cause hemorrhagic disease in amphibians and outbreaks in amphibian populations can spill over to sympatric reptiles (Brenes et al. 2014). We know very little about the pathology and ecology of Ranavirus in reptile hosts, but chelonians seem especially susceptible, and mortality has been recorded in at least one European snake species (Johnson et al. 2008; von Essen et al. 2020).

Despite a global distribution, most studies of Ranavirus in natural systems comes from temperate regions of the world, which may not directly translate to subtropical and tropical systems that boast higher species diversity and different suites of abiotic conditions. My dissertation work in the Longo Lab at the University of Florida seeks to fill the gaps in knowledge of how Ranavirus (Rv) and other pathogens impact subtropical herp communities. Our research in longleaf pine amphibian communities of north-central Florida has revealed recurring and prolonged outbreaks of Rv in the cool winter and spring months, primarily impacting specialist species like striped newts, Notophthalmus perstriatus, and gopher frogs, Lithobates capito (Hartmann et al. 2022). We have continued to document Rv-related disease and mortality for these species, which have already experienced steep decline across their range (Jensen and Richter 2005; Farmer et al. 2017), but there are now concerns how the virus may be affecting sympatric reptile species.

Ranavirus-infected paedomorphic striped newt from a disease outbreak in 2020. External lesions near the eye and internal hemorrhaging visible on the lateral and ventral surfaces. – Joshua Doby

Of particular concern are gopher tortoises, Gopherus polyphemus, which share their burrows with some of the affected amphibian species, and dozens of potential squamate hosts. Gopher tortoises are fatally susceptible to Rv (Johnson et al. 2008), but the impacts of Ranavirus outbreaks on wild populations of chelonians is largely unexplored. To make matters worse, we documented a mass mortality event of Florida softshell turtles, Apalone ferox, at our sites, possibly due to Rv or the newly described turtle Fraservirus (Waltzek et al. 2022). The ongoing decline of many longleaf-associated snake species may also be driven in-part by emerging disease, and there is a very real potential for co-occurring pathogens to synergistically drive populations towards extinction.

Florida softshell turtles from a mass mortality event. A total of 18 dead turtles were found on the edges of a single pond. Diagnostic work to identify the cause is ongoing. - Arik Hartmann
A juvenile Florida green water snake captured from the same wetland. – Javier Lobon-Rovira

The first step was to screen reptiles within our Rv-impacted sites, so we set up an array of drift fences in uplands and aquatic traps in wetlands to capture snakes and turtles. We collect oral, cloacal, and skin swabs, as well as small volumes of blood to detect for an array of pathogens, and PIT-tag individuals to track infection dynamics over time. With the financial support from the Orianne Society Grant Program for Reptile and Amphibian Conservation in the Southeast, we have sampled over 200 reptiles, comprising 9 snake and 5 turtle species. Pathogen screening has revealed Rv infections in 2 snake and 2 turtle species that are previously unreported, showing that reptiles are not impervious to infections in these systems. We plan to begin screening tortoise samples for Rv in the upcoming months and hope that populations at our sites are unimpacted.

Checking drift fence array with pitfalls, funnel, and box traps in sandhill habitat. - Javier Lobon-Rovira
Grant recipient Arik Hartmann, collecting an oral swab from a young Florida softshell turtle held by UF undergraduate Cory McKinstry. – Javier Lobon-Rovira

Additionally, Longo Lab undergraduate Cory McKinstry has detected the pathogen Ophidiomyces ophiodiicola, which causes Snake Fungal Disease (SFD), in sampled snakes, including visibly diseased pine snakes, Pituophis melanoleucus, and pigmy rattlesnakes, Sistrurus miliarius. We are continuing our sampling and working to understand the extent that Rv and other pathogens have impacted longleaf pine associated reptiles. Thanks to the Orianne Society, the data we generate will be used to inform conservation strategies and disease mitigation for imperiled species. By examining the trends of infections in the herp community and comparing the effects of individual and combined pathogen pressures on host fitness, we are adding substantial knowledge to the impacts of wildlife diseases on populations of southeastern herpetofauna.

Grant recipient Arik Hartmann collects a skin swab from black swamp snake, held by UF undergrad Cory McKinstry. Skin swabs are used to detect the fungus that causes Snake Fungal Disease. - Javier Lobon-Rovira
Ventral view of a sampled pigmy rattlesnake showing the necrotized anal and subcaudal scales, indicative of Snake Fungal Disease. Ophidiomyces infection was confirmed in this individual using qPCR. – Arik Hartmann

Literature Cited

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

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

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

Hartmann AM, Maddox ML, Ossiboff RJ, Longo AV (2022) Sustained Ranavirus Outbreak Causes Mass Mortality and Morbidity of Imperiled Amphibians in Florida. EcoHealth. https://doi.org/10.1007/s10393-021-01572-6

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