HEMATOLOGY IN AN EASTERN MASSASAUGA (<i>SISTRURUS CATENATUS</i>) POPULATION AND THE EMERGENCE OF<i>OPHIDIOMYCES</i>IN ILLINOIS, USA

Allender, Matthew C.; Phillips, Christopher A.; Baker, Sarah J.; Wylie, Daniel B.; Narotsky, Amy; Dreslik, Michael J.

doi:10.7589/2015-02-049

Cited by 29 publications

(25 citation statements)

References 34 publications

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“…A fungal pathogen causing growing concern is Ophidiomyces ophiodiicola , the species responsible for snake fungal disease (SFD; Lorch et al , Allender et al ). The earliest known record of SFD is from a museum specimen collected in 2000 from southern Illinois (Allender et al ). Snake fungal disease has now been recorded in 6 snake families representing over 30 species throughout most of the eastern half of the United States and captive snakes in parts of the United Kingdom, Germany, and Australia (Tetzlaff et al , Allender et al , Lorch et al ).…”

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confidence: 99%

“…Knowledge of O. ophiodiicola ecology (Allender et al 2015d, McCoy et al 2017, geographic distribution (Allender et al 2015d, Lorch et al 2016, detection (Allender et al 2016a), pathogenesis (Lorch et al 2015, Allender et al 2015a, and snake hematology (Allender et al 2015c(Allender et al , 2016b has increased over the last few years. However, unbiased estimates of O. ophiodiicola prevalence in host populations are still lacking.…”

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Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk

et al. 2017

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Pathogenic fungi have become a global concern to wildlife populations over the last 2 decades. However, the threat of snake fungal disease (SFD; caused by Ophidiomyces ophiodiicola) to snake populations is still largely unknown. From 2014-2016, we monitored 3 disjunct populations of the federally threated eastern massasauga (Sistrurus catenatus) in Michigan, USA. We used clinical signs of SFD, quantitative TaqMan polymerase chain reaction (qPCR), repeated sampling of individuals and sites, and single-season occupancy models to estimate site-specific prevalence of Ophidiomyces. Point estimates of Ophidiomyces prevalence in 2016 were larger at the northernmost study site (0.17, 95% CI ¼ 0.04-0.50), where 17 of 34 snakes were implanted with radio-transmitters, and smaller at southern sites (0.03, 95% CI ¼ 0.00-0.19). However, Ophidiomyces prevalence was not different between snakes with transmitters and snakes without transmitters. Swabbing snakes with 1 applicator resulted in a high probability of failure in detecting Ophidiomyces DNA for individuals with clinical signs of SFD and the probability was even higher for individuals without clinical signs of SFD. Repeated sampling of individuals reduced the probability of obtaining a false-negative qPCR result by 72% for snakes with clinical signs and 12% for snakes without clinical signs when we swabbed individuals with 5 applicators. We recommend resampling individuals and sites as a sampling design for estimating fine-scale, site-specific Ophidiomyces prevalence and population-level responses to SFD. If clinical signs are used as a surrogate for SFD, we recommend researchers standardize diagnosis of clinical signs of SFD by providing technicians adequate field training and educational materials, and minimize the number of observers recording clinical signs. We discourage the use of radio-telemetry methods where SFD occurs unless sterile surgical, handling, and equipment protocols can be ensured and the benefits to the population from such activities outweigh the increased health risks to individuals. Ó 2017 The Wildlife Society.

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Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk

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“…This is the first study to document the metabolic and hydric consequences of Oo infection, representing an important advancement in understanding how host physiology may affect disease outcomes in snakes with SFD. Awareness of the magnitude of the energetic costs of coping with Oo infection may be particularly relevant for the management of imperiled snake populations whose persistence is threatened by SFD (Clark et al, ), including the closely related eastern massasauga ( S. catenatus ; Allender et al, ).…”

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An emerging fungal pathogen is associated with increased resting metabolic rate and total evaporative water loss rate in a winter‐active snake

et al. 2019

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1. Energy allocation trade-offs associated with mounting metabolically costly immune responses may serve as sublethal mechanisms by which pathogens reduce host fitness. The emergence of cutaneous fungal pathogens, which invade the skin of their host and have the potential to disturb energy and water balance, highlight the importance of host physiology in determining individual-and populationlevel effects of disease. Snake fungal disease (SFD, ophidiomycosis), caused by the fungal pathogenOphidiomyces ophiodiicola (Oo), is an emerging disease afflicting wild snake populations throughout eastern North America. Emaciation and dehydration are phenotypic correlates of SFD, but it is unknown if such declines in host condition occur via effects of Oo infection on host physiology (i.e. increased rates of metabolism and evaporative water loss respectively).3. We used flow-through respirometry to assess the energetic and hydric consequences of natural Oo infection in winter-active pygmy rattlesnakes Sistrurus miliarius. We measured resting metabolic rate (CO 2 production rate) and total evaporative water loss rate of winter-acclimatized S. miliarius as a function of SFD status and acute temperature (17, 25 and 32°C). We also used regression models characterizing individual variation in the thermal-sensitivity of resting metabolic rate to predict the theoretical effects of behavioural fever on daily resting CO 2 production by free-ranging S. miliarius with SFD in winter. Natural infection byOo was associated with significant increases in resting metabolic rate (30%-45%) and total evaporative water loss rate (30%-40%) across all measurement temperatures. Under simulated scenarios of behavioural fever, Oo infection was predicted to increase daily resting CO 2 production rate by 58%-102%. 5. Our results are consistent with the hypothesis that the immune response to Oo infection is energetically costly and may contribute to declining host condition. Our modelling efforts combining the cumulative effects of increased immune activity and increased body temperature on metabolism represent a novel approach in quantifying the total daily energetic cost of infection in ectothermic vertebrates undergoing behavioural fever. | 487Functional Ecology AGUGLIARO et AL.

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“…Given the growing number of threats faced by reptile species including global climate change and emerging pathogens, studies such as this provide important baseline data on immune function of these taxa. Worldwide declines in snake populations have already been noted (Reading et al, 2010), and an emerging fungal pathogen (snake fungal disease) has shown the potential to cause high rates of mortality in sensitive species (Allender et al, 2016). A more complete understanding of immune function in snakes is therefore critical to their conservation.…”

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Characterization of serum complement immune activity in the prairie rattlesnake (Crotalus viridis)

Baker

Merchant

2018

JoBAZ

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Background: Reptile populations face a growing number of threats including global climate change and emerging pathogens. Unfortunately, research investigating the reptile immune system lags behind other taxa groups, hindering our ability to predict or mitigate species' response to threats. Baseline studies are critical for our understanding of reptile immune response and overall health of wild populations. Results: Treatment of unsensitized sheep red blood cells (SRBCs) with plasma collected from captive prairie rattlesnakes (Crotalus viridis) resulted in volume-dependent hemolysis, with a CH 50 of 0.23 ± 0.01 mL. Kinetic analyses at different temperatures revealed that the hemolysis was relatively rapid, with 50% of hemolytic activity occurring within 15 min (25°C), 18 min (35°C), or 23 min (15°C), and near maximum hemolysis within 60-90 min at all three temperatures. A comparative thermal profile revealed that complement activity was low at 5°C, but increased sharply at 10 and 15°C, and was maximal at 20-30°C. A steep decline in activity was noted at temperatures > 30°C. Mild heat treatment of the snake plasma (56°C, 30 min) or treatment with proteases completely abolished the hemolytic activity. In addition, inclusion of 5 mM EDTA inhibited 90% of the hemolysis, but the activity could be reconstituted with the addition of 15 mM Ca 2+ or Mg 2+ , but not Ba 2+ , Cu 2+ , or Fe 2+. Furthermore, the hemolysis was unaffected in the presence of 20 mM methylamine, indicating that the alternative mechanism of complement activation is responsible for the observed activities. Conclusions: Rattlesnakes show a relatively robust innate immune response as measured by hemolysis of SRBCs. However, hemolytic activity is reduced at high temperatures, indicating that rising global temperatures may have immune consequences for snake species, making them more vulnerable to known and emerging pathogens.

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HEMATOLOGY IN AN EASTERN MASSASAUGA (SISTRURUS CATENATUS) POPULATION AND THE EMERGENCE OFOPHIDIOMYCESIN ILLINOIS, USA

Cited by 29 publications

References 34 publications

Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk

Estimation of Ophidiomyces prevalence to evaluate snake fungal disease risk

An emerging fungal pathogen is associated with increased resting metabolic rate and total evaporative water loss rate in a winter‐active snake

Characterization of serum complement immune activity in the prairie rattlesnake (Crotalus viridis)

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