Snake Fungal Disease in Free-Ranging Northern Pine Snakes (Pituophis melanoleucus melanoleucus) in New Jersey: Lesions, Severity of Sores and Investigator's Perceptions.

Ophidiomyces ophidiicola, the fungus causing snake fungal disease (SFD), has been identified in northern pine snakes (Pituophis melanoleucus) in New Jersey. In this paper, we (1) review the positivity rate of SFD on different locations on snakes' bodies, (2) determine the relationship between the sores and quantitative polymerase chain reaction (qPCR) positivity rates, and (3) explore the relationship between the investigators' clinical evaluation of the severity of sores, their evaluation of the likelihood of the sores being positive, and the qPCR positivity of SFD for the sores. Swabbing the sores was more effective at determining whether the snakes tested positive for O. ophidiicola than ventrum swabbing alone. The perception of the severity of the sores did not relate to qPCR positivity for O. ophidiicola. We suggest that the assessment of the rate of SFD among snakes in the wild needs to include the sampling of snakes with no clinical signs, as well as those with sores, and the swabbing of all the sores collectively. Clear terminology for sores, the identification of clinical signs of SFD, and distinguishing the rates of O. ophidiicola by PCR testing should be adopted. Overall, the pine snakes exhibited a higher rate of sores and positivity of O. ophidiicola swabs by PCR testing compared to the other snakes.

Soil Reservoir Dynamics of Ophidiomyces ophidiicola, the Causative Agent of Snake Fungal Disease.

Wildlife diseases pose an ever-growing threat to global biodiversity. Understanding how wildlife pathogens are distributed in the environment and the ability of pathogens to form environmental reservoirs is critical to understanding and predicting disease dynamics within host populations. Snake fungal disease (SFD) is an emerging conservation threat to North American snake populations. The causative agent, Ophidiomyces ophidiicola (Oo), is detectable in environmentally derived soils. However, little is known about the distribution of Oo in the environment and the persistence and growth of Oo in soils. Here, we use quantitative PCR to detect Oo in soil samples collected from five snake dens. We compare the detection rates between soils collected from within underground snake hibernacula and associated, adjacent topsoil samples. Additionally, we used microcosm growth assays to assess the growth of Oo in soils and investigate whether the detection and growth of Oo are related to abiotic parameters and microbial communities of soil samples. We found that Oo is significantly more likely to be detected in hibernaculum soils compared to topsoils. We also found that Oo was capable of growth in sterile soil, but no growth occurred in soils with an active microbial community. A number of fungal genera were more abundant in soils that did not permit growth of Oo, versus those that did. Our results suggest that soils may display a high degree of both general and specific suppression of Oo in the environment. Harnessing environmental suppression presents opportunities to mitigate the impacts of SFD in wild snake populations.

A paradigm for information needed to protect at-risk species: northern pine snake (Pituophis melanoleucus) in the pine barrens as a case study.

New methods of examining the risk to endangered, threatened and rare species are required to identify vulnerability. A paradigm for examining risk is presented that describes anthropogenic threats, species activities, and vulnerabilities, and uses Northern pine snakes (Pituophis melanoleucus) in the New Jersey Pine Barrens as a case study. The paradigm includes (1) conceptual model of natural, anthropogenic, and interactive stressors, (2) template of the functional attributes of threats from human activities, and (3) template of effects from different human activities. Pine snake behavior throughout the year was used to examine the temporal overlap in high snake vulnerability periods and desired human activities in a shared habitat. New data on autumn behavior of pine snakes are also provided. Passive integrated transponders (PIT tag) tracking technology indicated that the fall basking activity period is both longer in duration, and at a higher intensity than previously presumed. During the autumn, individual snakes moved in and out of dens an average of 6 times over a two-month period. Younger snakes at a small hibernaculum were more active than those at hibernacula with larger and older snakes. The high activity period of pine snakes overlaps with the timing of preferred off-road-vehicle (ORV) use, controlled burns, and other human activities, increasing snake vulnerability, potentially causing behavioral disruptions, injury, and death. The conceptual model illustrating relationships between attributes of human activity and effects may be utilized to determine risks to other listed species, and those of special concern in different habitats. This paradigm also provides managers with template tools to assess risks to species that may also be used to provide information to the public.

Hatchling survival to breeding age in Northern Pine Snakes (Pituophis melanoleucus) in the New Jersey Pine Barrens: Human effects on recruitment from 1986 to 2017.

To conserve threatened/endangered species, we need to understand the factors contributing to reproductive success and recruitment to reproductive stage. Obtaining this information is difficult for snakes because they are secretive, are not easy to locate at the same stage each year, and are sometimes sparsely distributed. We determined nest fate, hatchling growth and survival to age 5 years, and recruitment to breeding age of Northern Pine Snakes (Pituophis melanoleucus) in New Jersey Pine Barrens from 1986 to 2017. Pine Snakes are 'threatened' in New Jersey and in other states, and are at risk because of increased human population, habitat loss, predation, and poaching. Age of first-breeding was 4-years, based on snout-vent length of gravid and laying females, and snout-vent length of females followed as hatchlings to 5-years. Mean clutch size (+ 1 SE) was 9.5 + 0.3 (N = 53). The annual percent of nests in which eggs hatched averaged 25% (N = 288 nests), and varied among 5-year periods (5% to 30%/year). Of lab-reared hatchlings released into natal nests (N = 90), 26% (2015) and 32% (2016) reached hibernacula excavated in 2016 and 2017. The sex ratio of hatchlings reaching hibernation sites (N = 181) between 1986 and 2015 was skewed toward females (74/106, 59% females), and varied among 5-year periods (47-75% females). Once hatchlings reached a hibernaculum, there was a sex-related difference in survival. For hatchlings reaching a monitored hibernaculum, survival to 3-years was 35% in females and 40% in males, and to 4-years was 25% in females and 33% in males. Using these data, only 10% of females reached 3 years (first possible breeding age), and 7% survived to 4-years. Methodological problems with determining survival rates during these early critical years are discussed.

Fidelity of northern pine snakes (Pituophis m. melanoleucus) to natural and artificial hibernation sites in the New Jersey Pine Barrens.

Environmental managers require information on whether human-made hibernacula are used by rare snakes before constructing large numbers of them as mitigation measures. Fidelity of northern pine snakes (Pituophis m. melanoleucus) was examined in a 6-year study in the New Jersey Pine Barrens to determine whether they used natural and artificial hibernacula equally. Pine snakes used both artificial (human-made) and natural (snake-adapted) hibernacula. Most natural hibernacula were in abandoned burrows of large mammals. Occupancy rates were similar between natural and artificial hibernacula. Only 6 of 27 radio-tracked snakes did not shift hibernacula between years, whereas 78% shifted sites at least once, and fidelity from one year to the next was 42%. For snakes that switched hibernacula (n = 21), one switched among artificial hibernacula, 14 (65%) switched among natural hibernacula, and 6 (29%) switched from artificial to natural hibernacula. Data indicate that most pine snakes switch among hibernacula, mainly selecting natural hibernacula, suggesting that artificial dens are used, but protecting natural hibernacula should be a higher conservation priority.