Krysten L. Schuler

Snake fungal disease: an emerging threat to wild snakes

Since 2006, there has been a marked increase in the number of reports of severe and often fatal fungal skin infections in wild snakes in the eastern USA. The emerging condition, referred to as snake fungal disease (SFD), was initially documented in rattlesnakes, where the infections were believed to pose a risk to the viability of affected populations. The disease is caused by Ophidiomyces ophiodiicola, a fungus recently split from a complex of fungi long referred to as the Chrysosporium anamorph of Nannizziopsis vriesii (CANV). Here we review the current state of knowledge about O. ophiodiicola and SFD. In addition, we provide original findings which demonstrate that O. ophiodiicola is widely distributed in eastern North America, has a broad host range, is the predominant cause of fungal skin infections in wild snakes and often causes mild infections in snakes emerging from hibernation. This new information, together with what is already available in the scientific literature, advances our knowledge of the cause, pathogenesis and ecology of SFD. However, additional research is necessary to elucidate the factors driving the emergence of this disease and develop strategies to mitigate its impacts. This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.

Ad hoc smoothing parameter performance in kernel estimates of GPS-derived home ranges

Accuracy of home-range estimates in animals is influenced by a variety of factors, such as method of analysis and number of locations, but animal space use is less often considered and frequently over-generalized through simulations. Our objective was to assess effect of an ad hoc (h_ad hoc) smoothing parameter in kernel analysis from two species that were predicted to have different patterns of utilization distributions across a range of sample sizes. We evaluated variation in home-range estimates with location data collected from GPS collars on two species: mule deer Odocoileus hemionus and coyotes Canis latrans. We calculated home ranges using 95% and 50% kernel contours using reference (h_ref and h ad hoc smoothing parameters. To evaluate the influence of sample size, we calculated home ranges using both smoothing parameters for random subsamples of 5, 10, 25 and 50% of GPS locations and compared area estimates to estimates for 100% of GPS locations. On mule deer, we also conducted visual relocations using conventional radiotelemetry, which resulted in fewer locations than GPS collars. Area was overestimated at smaller sample sizes, but an interesting pattern was noted with higher relative bias at 60–100 locations than at sample sizes < 50 locations. Relative bias was most likely due to increased smoothing of outer data points. Subsampling allowed us to examine relative bias across a range of samples sizes for the two smoothing parameters. Minimum number of points to obtain a consistent home range estimates varied by smoothing method, species, study duration, and volume contour (95% or 50%). While h_ad hoc performed consistently better over most sample sizes, there may not be a universal recommendation for all studies and species. Behavioral traits resulting in concentrated or disparate space use complicates comparisons among and between species. We suggest researchers examine their point distribution, justify their choice of smoothing parameter, and report their choices for home-range analysis based on their study objectives.

Expansion of an Exotic Species and Concomitant Disease Outbreaks: Pigeon Paramyxovirus in Free-Ranging Eurasian Collared Doves

Eurasian collared doves (Streptopelia decaocto) have expanded their range across the United States since their introduction several decades ago. Recent mortality events in Eurasian collared doves in Arizona and Montana, USA, during the winter of 2009–2010 were the result of pigeon paramyxovirus (PPMV), a novel disease agent. The first instance of mortality by this emerging infectious disease in this species occurred in Florida in 2001 with subsequent disease events in 2006 and 2008. Full diagnostic necropsies were performed on carcasses from the three states. PPMV was identified by RT-PCR and virus isolation and was sequenced to the VIb genotype of avian paramyxovirus-1 (APMV). Other APMVs are common in a variety of free-ranging birds, but concern is warranted because of the potential for commingling of this species with native birds, virus evolution, and threats to domestic poultry. Improved surveillance for wildlife mortality events and efforts to prevent introduction of non-native animals could reduce the threat of introducing new pathogens.

PATHOGEN EXPOSURE AND BLOOD CHEMISTRY IN THE WASHINGTON, USA POPULATION OF NORTHERN SEA OTTERS (ENHYDRA LUTRIS KENYONI)

Abstract Northern sea otters (Enhydra lutris kenyoni) from Washington State, United States were evaluated in 2011 to determine health status and pathogen exposure. Antibodies to Brucella spp. (10%) and influenza A virus (23%) were detected for the first time in this population in 2011. Changes in clinical pathology values (serum chemistries), exposure to pathogens, and overall health of the population over the last decade were assessed by comparing 2011 data to the data collected on this population in 2001–2002. Several serum chemistry parameters were different between study years and sexes but were not clinically significant. The odds of canine distemper virus exposure were higher for otters sampled in 2001–2002 (80%) compared to 2011 (10%); likelihood of exposure significantly increased with age. Prevalence of exposure to Sarcocystis neurona was also higher in 2001–2002 (29%) than in 2011 (0%), but because testing methods varied between study years the results were not directly comparable. Exposure to Leptospira spp. was only observed in 2001–2002. Odds of Toxoplasma gondii exposure were higher for otters sampled in 2011 (97%) than otters in 2001–2002 (58%). Substantial levels of domoic acid (n = 2) and saxitoxin (n = 2) were found in urine or fecal samples from animals sampled in 2011. No evidence of calicivirus or Coxiella burnetii exposure in the Washington population of northern sea otters was found in either 2001–2002 or 2011. Changes in exposure status from 2001–2002 to 2011 suggest that the Washington sea otter population may be dealing with new disease threats (e.g., influenza) while also increasing their susceptibility to diseases that may be highly pathogenic in naïve individuals (e.g., canine distemper).

Acute Lead Toxicosis via Ingestion of Spent Ammunition in a Free-Ranging Cougar (Puma concolor)

Lead toxicity has long been documented and acknowledged as a significant health issue of water birds and avian scavengers. However, few instances of toxic effects to higher mammalian carnivores have been documented. Here we present an acute case of lead toxicity in a free-ranging cougar (Puma concolor) in Oregon.

Tonsillar Biopsy Test for Chronic Wasting Disease: Two Sampling Approaches in Mule Deer and White-tailed Deer

Preclinical antemortem testing of deer (Odocoileus spp.) for chronic wasting disease (CWD) can be important for determining prevalence rates and removing infected individuals from wild populations. Because samples with high numbers of tonsillar follicles are likely to provide earlier detection of CWD than samples with fewer follicles, the method of obtaining follicular samples may be critical when investigating disease prevalence. Between January 2003 and January 2005, white-tailed deer (O. virginianus) in southeast and southwest Minnesota and white-tailed and mule deer (O. hemionus) in Wind Cave National Park, South Dakota, were sampled using dorso-lateral and ventral-medial approaches for collecting tonsillar follicles. We obtained significantly more follicles using a dorso-lateral (median number of follicles=19) rather than a ventral-medial (median number of follicles=5.5) approach. No differences were observed in collection of tonsillar follicles that were related to sex, age class, or species of deer. We recommend the dorso-lateral approach for assessing CWD prevalence in deer populations.

Applicability of Viewshed Analysis to Wildlife Population Estimation

Abstract Population estimations and indices based on roadside or spotlight counts typically require investigators to determine the route with maximum viewing area and calculate area visible from the census route. Viewshed analysis may provide a simpler and more accurate method for determining route, area and population estimate. From September 2000 to August 2001 we observed adult bison from a driving route at The Nature Conservancys Tallgrass Prairie Preserve. We recorded group locations to field test the ability of viewshed analysis to predict the area where bison were visible. We developed viewsheds based on digitized layers of the driving route and for high, low and random points within the Preserve to determine the viewshed with maximum visible area. We developed a population estimate based on number of bison observed and visible area calculated from our driving route. We compared population estimates to known bison populations before and after 1 May 2001 and for our entire study period. Ninety-nine percent (P < 0.001) of bison locations occurred within the viewshed. Our driving route provided the most visible area (81%), followed by viewsheds of high (77%), random (61%) and low (31%) points. Estimated adult bison populations before 1 May 2001 were different (P < 0.001), but similar on and after 1 May 2001 (P = 0.10) to known populations. The estimated population for the entire study was different (P < 0.001) from the mean population size. Viewshed analysis is an efficient method to predict locations of easily observed ungulates and has utility in planning census routes with maximum visible area a priori. We suggest that viewshed analysis provides a more accurate estimation of area visible from census routes and resulting population estimations than conventional surveys.

WILDLIFE HEALTH AND PUBLIC TRUST RESPONSIBILITIES FOR WILDLIFE RESOURCES.

Abstract A significant development in wildlife management is the mounting concern of wildlife professionals and the public about wildlife health and diseases. Concurrently, the wildlife profession is reexamining implications of managing wildlife populations as a public trust and the concomitant obligation to ensure the quality (i.e., health) and sustainability of wildlife. It is an opportune time to emphasize the importance of wildlife health, specifically to advocate for comprehensive and consistent integration of wildlife health in wildlife management. We summarize application of public trust ideas in wildlife population management in the US. We argue that wildlife health is essential to fulfilling public trust administration responsibilities with respect to wildlife, due to the central responsibility of trustees for ensuring the well-being of wildlife species (i.e., the core resources of the trust). Because both health of wildlife and risk perceptions regarding threats posed by wildlife disease to humans and domestic animals are issues of growing concern, managing wildlife disease and risk communication vis-à-vis wildlife health is critical to wildlife trust administration. We conclude that wildlife health professionals play a critical role in protecting the wildlife trust and that current conditions provide opportunities for important contributions by wildlife health professionals in wildlife management.

A review of episodes of zinc phosphide toxicosis in wild geese (Branta spp.) in Oregon (2004−2011)

Epizootic mortality in several geese species, including cackling geese (Branta hutchinsii) and Canada geese (Branta canadensis), has been recognized in the Willamette Valley of Oregon for over a decade. Birds are generally found dead on a body of water or are occasionally observed displaying neurologic clinical signs such as an inability to raise or control the head prior to death. Investigation of these epizootic mortality events has revealed the etiology to be accidental poisoning with the rodenticide zinc phosphide (Zn3P2). Gross and histologic changes are restricted to acute pulmonary congestion and edema, sometimes accompanied by distension of the upper alimentary tract by fresh grass. Geese are unusually susceptible to this pesticide; when combined with an epidemiologic confluence of depredation of specific agricultural crops by rodents and seasonal avian migration pathways, epizootic toxicosis may occur. Diagnosis requires a high index of suspicion, appropriate sample collection and handling, plus specific test calibration for this toxicant. Interagency cooperation, education of farmers regarding pesticide use, and enforcement of regulations has been successful in greatly decreasing these mortality events since 2009.

Genetic Characterization of Sarcoptes scabiei from Black Bears (Ursus americanus) and Other Hosts in the Eastern United States

Abstract Since the early 1990s there has been an increase in the number of cases and geographic expansion of severe mange in the black bear (Ursus americanus) population in Pennsylvania. Although there are 3 species of mites associated with mange in bears, Sarcoptes scabiei has been identified as the etiologic agent in these Pennsylvania cases. Historically, S. scabiei-associated mange in bears has been uncommon and sporadic, although it is widespread and relatively common in canid populations. To better understand this recent emergence of sarcoptic mange in bears in Pennsylvania and nearby states, we genetically characterized S. scabiei samples from black bears in the eastern United States. These sequences were compared with newly acquired S. scabiei sequences from wild canids (red fox [Vulpes vulpes] and coyote [Canis latrans]) and a porcupine (Erethizon dorsatum) from Pennsylvania and Kentucky and also existing sequences in GenBank. The internal transcribed spacer (ITS)-2 region and cytochrome c oxidase subunit 1 (cox1) gene were amplified and sequenced. Twenty-four ITS-2 sequences were obtained from mites from bears (n = 16), red fox (n = 5), coyote (n = 2), and a porcupine. The sequences from bear samples were identical to each other or differed only at polymorphic bases, whereas S. scabiei from canids were more variable, but 2 were identical to S. scabiei sequences from bears. Eighteen cox1 sequences obtained from mites from bears represented 6 novel haplotypes. Phylogenetic analysis of cox1 sequences revealed 4 clades: 2 clades of mites of human origin from Panama or Australia, a clade of mites from rabbits from China, and a large unresolved clade that included the remaining S. scabiei sequences from various hosts and regions, including sequences from the bears from the current study. Although the cox1 gene was more variable than the ITS-2, phylogenetic analyses failed to detect any clustering of S. scabiei from eastern U.S. hosts. Rather, sequences from black bears grouped into a large clade that included S. scabiei from numerous hosts from Europe, Asia, Africa, and Australia. Collectively, these data suggest that the increasing number of S. scabiei cases in northeastern black bears is not due to the emergence and expansion of a single parasite strain.