Threat Characterization of an Invasive Lung Parasite and a Longstanding Fungal Pathogen to Florida Pygmy Rattlesnake Populations

Background—Snake species native to the southeastern United States face many conservation threats including habitat loss, invasive species, persecution, and infectious diseases. Two emerging invasive pathogens, Ophidiomyces ophiodiicola (Oo) (the causative agent of Snake Fungal Disease) and Raillietiella orientalis (Ro) are prevalent in snake populations of the southeastern U.S. and may contribute to local extinctions (1,2). Oo, a fungal pathogen, and Ro, a lung parasite, utilize an array of snake taxa as hosts, survive wide environmental conditions, and cause chronic and lethal disease outcomes. In the pygmy rattlesnake (Sistrurus miliarius), Oo infections can alter reproductive schedules and increase metabolic rate, febrile responses, and evaporative water loss (3,4). These energetically expensive coping mechanisms may leave snakes with less energy to allocate towards reproduction. Therefore, the sublethal mechanisms of Oo infections indirectly impact populations and coinfections with other pathogens, like Ro, could exacerbate these effects.

The dependence of pygmy rattlesnakes on ectothermic prey makes them vulnerable to Ro infection because this parasite utilizes frogs and lizards as intermediate hosts (5). Pygmy rattlesnakes are also an immunologically naïve host and this lack of an evolutionary history with Ro could augment adverse health impacts. Ro belongs to an understudied class of crustaceans that as adults mostly parasitize the lungs of carnivorous reptiles (6). Ro originated in Southeast Asia and has subsequently invaded Australian and North American snake populations. In North America, Burmese pythons have been supported as the introduction pathway both spatiotemporally and molecularly (2). In native snakes, the infections are more intense than in pythons. The adult parasites grow to over 100 mm in native snakes and the infections can often include over 100 adult parasites in the lungs. Infections cause chronic inflammation, lesions of the lungs, anemia, and pneumonia, all of which are documented in pygmy rattlesnakes, banded water snakes, and indigo snakes (7,8,9). The threat of Ro is a conservation concern as its use of numerous hosts and presence in the pet trade increases the likelihood of rapid dispersal. Precipitous declines of pygmy rattlesnake populations that are spatially and temporally consistent with the initial invasion of Ro indicate population level consequences of infections. For informed habitat management and disease control strategies, I am documenting the host-pathogen dynamics of Oo and Ro in pygmy rattlesnake populations across Florida and assessing the influence of disease on the genomic structure within and between these populations.