OCCURRENCE OF MANGE IN AMERICAN BLACK BEARS (URSUS AMERICANUS) IN NEW YORK STATE, USA

Mange, a parasitic skin disease caused by various species of mites, is found in many free-ranging wildlife populations (Pence and Ueckermann 2002) and has been reported sporadically in American black bears (Ursus americanus) since 1970 (e.g., Manville 1978; Yunker et al. 1980; Schmitt et al. 1987; Forrester et al. 1993; Fitzgerald et al. 2008; Peltier et al. 2017). Although other species of mange mites have been described in black bears, Sarcoptes scabiei is the most common etiology and is possibly related to immunocompromised condition after hibernation (Schmitt et al. 1987; Fitzgerald et al. 2008).

In recent years, mange reports have increased in the northeastern US (Sommerer 2014; Peltier et al. 2017; Niedringhaus et al. 2019a, 2019b). In Pennsylvania, reports of mange in black bears have expanded in abundance and geographic distribution since 1991 (Sommerer 2014; Niedringhaus et al. 2019b). Anecdotal reports of mange in black bears in New York State (NYS) have also increased (NYSDEC 2007, 2014). Sarcoptic mange is commonly reported in social carnivores such as coyotes (Canis latrans) and red foxes (Vulpes vulpes, Ko?odziej-Soboci?ska et al. 2014). Black bears, however, are often solitary and demonstrate seasonal denning behavior throughout most of their range.

Unlike most wildlife diseases, which require laboratory diagnosis for detection, mite infestations produce striking alterations in the appearance of animals. Clinical signs of mange include alopecia, poor body condition, epidermal exfoliation, and lichenification (Manville 1978; Schmitt et al. 1987). These changes may be so dramatic that mange in black bears is reported by untrained observers concerned about animal welfare. Behavioral changes, frequently reported in severely infested animals, may increase the likelihood that individuals will loiter in inappropriate habitats, especially near human habitation (Fitzgerald et al. 2008; Jimenez et al. 2010). In such cases, large carnivores such as bears may cause additional complications due to perceived potential aggression. Moreover, sarcoptic mange is a zoonotic disease, making mange a potential public health concern for people and domestic animals. Therefore, the apparent emergence and spread of mange, mainly by S. scabiei mites, in black bears may be of interest to wildlife managers because of potential human–wildlife conflict, in addition to the welfare issues of individual bears.

We aimed to use necropsy and sighting data to assess the current status of mange in NYS black bears and determine relationships of mange cases with geographic location, year, season, sex, age, and reason for laboratory submission of black bears. Wildlife managers, informed of the status of the disease and conditions that may be associated with its spread, can then judge whether an active mange monitoring and management plan is needed to ensure the future health of black bears.

We conducted a retrospective cross-sectional study of two independent data sets related to black bears in NYS from 2009 to 2018: necropsy records of black bears found dead or euthanized and reports of sightings of live black bears with suspected mange. Records consisted of archived materials of the NYS Wildlife Health Program, a collaboration between the Cornell Wildlife Health Lab and the NYS Department of Environmental Conservation (NYSDEC). Necropsy records included information from field reports, gross necropsy, histology, and diagnostic testing of individual bears submitted to the diagnostic laboratories. Field reports of bears found dead from obvious causes as determined by experienced staff were provided without carcasses or tissues. Sighting records of live bears with suspected mange included data reported to the NYSDEC through staff activities or by the public. Because lichenification and hair loss are most likely to be mange and are so obvious, we assumed that sightings of bears with these characteristics of mange produced reliable data regarding the occurrence of the disease.

During fieldwork and diagnostic testing, carcasses or skin samples from bears were examined. Suspect mange cases were defined as animals with the presence of any degree of lichenification and hair loss, with or without compromised body condition (Supplementary Material Table S1). Body condition was categorized by evaluation of fat stores, muscle mass, and bony prominences. Suspect mange cases with carcasses or tissues submitted were confirmed by the presence of mites by skin scraping and microscopic identification on the basis of morphologic features by a parasitologist. Additional variables collected at necropsy included age, sex, geographic location and date of collection, reason for laboratory submission (nuisance, research, accident, hunter, or other causes), and final diagnosis (noninfectious, traumatic, bacterial, and parasitic causes).

We standardized the necropsy data by labeling records according to their appropriate a priori categories (Table S1). Bears were assigned to Southern or Northern zones as defined by hunting regulations (NYSDEC 2018), on the basis of their county of origin. Records were further characterized by year as early (2009–13) or late (2014–18), and each bear was finally assigned to a season (winter: 22 December–20 March; spring: 21 March–23 June; summer: 24 June–22 September; and fall: 23 September–21 December). Ages of bears were estimated by stage of eruption of permanent canine teeth or by laboratory analysis of cementum annuli in premolar teeth (Marks and Erickson 1966; Sauer et al. 1966; Willey 1974). Juvenile bears were defined as individuals under 2 yr old on the basis on the average age of dispersal from mothers; adult bears were defined as individuals ?2 yr old (Lee and Vaughan 2003).

We generated summary statistics for the standardized necropsy data that included percentages of suspect and confirmed mange cases for each segment of the population. After removing records for which unknown or only partial data existed, we assessed significant independencies and proportions between categories from temporal, spatial, submission, sex, and age variables (binned data). We used 14 chi-square analyses (Balestrieri et al. 2006; Thrusfield 2007) with a predetermined experimentwise type I error rate (?=0.05) and applied a Bonferroni correction where P<0.004 was used as the level of significance (Rice 1989; Balestrieri et al. 2006). Strengths in association to binned data were calculated for significant dependencies with an odds ratio (OR; Thrusfield 2007).

The sighting data contained opportunistically collected data on the distribution and characteristics of live black bears with suspected mange. Records included temporal (time and date), spatial (geographic coordinates), and body condition information (Table S1). Because several sighting accounts may have described the same bear, we ensured that repeated sightings were removed by discarding duplicate reports that shared the same phenotypic characteristics, date of report (±15 d), or location of sighting. Sighting reports that shared the same characteristics as cases submitted for necropsy were also removed before comparing and combining the data sets. These cleaning procedures were conducted with the aim that only one record was included (necropsy or sighting) for each bear.

Necropsy and sighting data sets were combined only for descriptive analyses of the spatial and temporal variables. For spatial analysis, we created maps showing mange presence by county. For temporal variables, a seasonal decomposition of time series by Loess analysis was carried out on the monthly number of necropsy cases, sighting cases, and combined cases of mange occurrence using stl function in the forecast package in R (Hyndman et al. 2021) to generate a temporal pattern (Cleveland et al. 1990).

Between 2009 and 2018, 150 dead black bears were reported in NYS (Table 1). Of these, 72 (48.0%) carcasses were submitted for complete necropsy. Forty-nine (32.7%) were male and 42 (28.0%) were female; 59 (39.3%) bears were adults and 42 (28.0%) were juveniles. Most bears (104/150, 69.3%) originated in the Southern Zone. Submissions of black bears varied over time, with peaks occurring in 2012 and 2016; 104/150 (69.3%) submissions occurred from 2014 to 2018 (Table S2). Most bears were submitted in spring (51/150, 34.0%), whereas winter experienced the lowest proportion of submissions (17/150, 11.3%).

Bears were submitted to the diagnostic laboratory for a variety of reasons. Animals involved in a nuisance complaint (54/150, 36.0%) were the most common reason, followed by accidental mortality event (23/150, 15.3%) and disease case (18/150, 12.0%). Other reasons for laboratory submission, such as research and hunted and orphaned animals, constituted 13.3% (20/150) of the data. Reason for submission was not recorded for 35/150 (23.3%) bears; 34 of these were field reports.

Parasitic diseases (47/150, 31.3%) were the most common diagnosis among necropsy records. Trauma (34/150, 22.7%) was the second most common diagnosis, with a higher proportion of males (23/34 cases, 67.6%) than females (8/34 cases, 23.5%). Final diagnosis was not recorded for 35/150 (23.3%) bears; 34 of these were field reports. Most bear carcasses submitted (67/72) were tested for rabies; all were negative.

In the necropsy data, we found 54/150 (36.0%) cases of suspected mange. In 30 cases, all submitted as carcasses, mange was confirmed by the presence of mites. Sarcoptes scabiei was identified in 28 cases; nonspeciated mites were reported in the other two cases. All nonconfirmed mange cases were submitted as field reports with obvious causes of death, such as euthanized due to severe mange (19/24, 79.2%) or trauma (5/24, 20.8%), without carcass or skin tissues submitted. Mange was identified both as the primary cause of mortality and disease (47/54, 87.0%) and secondary to another diagnosis (7/54, 13.0%).

The first case of mange in the necropsy data occurred in 2011 in the Northern Zone; cases increased thereafter in both the Central-Northern and Southern zones (Fig. 1). Overall, of 62 NYS counties, bears affected with mange originated in 17/36 (47.2%) counties with submissions. The Southern Zone had bears with mange present in 8/25 (32.0%) counties with submissions, whereas the Northern Zone had mange cases in 9/11 (81.8%) counties with submissions (Supplementary Material Fig. S1). The necropsy data set revealed that the odds of a bear having mange were four times higher (95% confidence interval [CI], 1.9–8.6; P=0.0004) in the Northern Zone than in the Southern Zone (Table 2).

In the necropsy data, we averaged one new case of mange in bears in NYS each year (Fig. S2). The highest number of mange cases occurred in 2016, which also had the greatest number of bears submitted (Fig. 2). Although the proportions of mange cases were not significantly different by year (?²=15.274; P=0.0837; Fig. S2), the late period (2014–18) had 4.6 (95% CI, 1.9–11.2; P=0.0008) times more mange cases than the early period (2009–13). The highest annual proportions of mange cases among bears occurred in 2014 (6/10, 60%) and 2018 (7/14, 50%). The highest proportion of mange cases in the necropsy data occurred in winter, although proportions of mange cases were not significantly different by season (?²=7.93; P=0.05; Fig. S3).

Of the 54 bears with mange, most were submitted as nuisance complaints (59.3%) or disease cases (27.8%; Table 1). Mange was also found in bears submitted as hunted (7.4%) and accidental event (5.6%) categories. As expected, reason for laboratory submission was significantly associated with mange (Table 2; Fig. S4). Bears submitted for suspected disease had the highest odds of having mange compared with bears submitted for any other reason (OR, 7.4; 95% CI, 2.0–27.4; P=0.0019), whereas bears submitted because of accidental death were less likely to have mange than bears in other categories (OR, 0.1; 95% CI, 0.0–0.4; P=0.001). Bears submitted because of nuisance complaints tended to be more likely to have mange when compared with bears in all other categories, although this association was not significant (OR, 2.6; 95% CI, 1.2-5.5; P=0.0214).

Female bears were 4.1 times more likely (95% CI, 1.7–9.8; P=0.0027) to have mange than male bears (Table 2). Whereas females had mange as the most common diagnosis in necropsy records, males had more trauma with mange as a secondary diagnosis (Table S3): 5/15 (33.3%) male mange cases were trauma with secondary mange. We detected no significant difference in mange cases by age for either sex. However, there were five cases of mange as a primary diagnosis in adult females for each case in juvenile females (Figure S5).

Of the 54 mange cases, only the 30 (55.5%) with carcass submissions had complete necropsy descriptions containing information on skin lesion degree and body condition scores; the remaining 24 were submitted as field reports only. Among the complete necropsy reports, 10/30 (33.3%) were reported as having poor body condition and 18/30 (60.0%) were described as emaciated. Of these 28 animals, 11 (39.3%) had additional parasites such as Baylisascaris transfuga or Dirofilaria ursi, and skin pathogens such as Pelodera spp. and Malassezia spp. Although level of hair loss and lichenification were not reported in all mange cases, 17/30 (56.7%) individuals were described with moderate hair loss, whereas 8/30 (26.7%) had severe hair loss. All cases had corresponding moderate to severe lichenification.

The first public sighting of a mange-afflicted bear was reported to the NYSDEC in 2012, and sightings increased steadily after 2016 (Figs. 1 and 2). Four duplicate sightings and eight sightings of bears subsequently euthanized and submitted for necropsy because of suspected mange were removed from the data, leaving 52 unique sightings of black bears with suspect mange reported in NYS from 2012 to 2018. The eight duplicate sightings of bears submitted for necropsy were not confirmed as mange cases. All sightings except one were of individual live bears. One sighting was of three individuals presumed to be a mangy female with her cubs; we considered this event as one case. Among the sightings, 22/52 (42.3%) cases had mild to moderate hair loss and five of those had poor body condition. Lichenification was not specifically described, but 16/52 (30.8%) had nonspecific labels of mange that probably included both hair loss and lichenification.

Sightings of mange bears occurred in some counties despite a lack of necropsy cases and vice versa (Fig. 1). However, both necropsy and sighting data identified the Southern Zone as a hot spot, with 55/106 (51.9%) of the total mange cases for all NYS being concentrated along the Pennsylvania border. The Northern Zone had a less concentrated distribution of mange cases on the basis of necropsy data, but the sighting data demonstrated a concentration of cases in the southwest region of the Northern Zone.

The monthly patterns of mange cases were similar between the necropsy and sighting data, although there were higher numbers of sightings during early summer compared with the number of necropsy cases (Fig. 3). Mange cases in the necropsy data peaked in late spring, with slight increases of cases in fall and late winter.

The seasonal decomposition of the time-series analysis of the combined data sets revealed an increasing trend across the years of the study and a very defined seasonal pattern of mange with one peak in the middle of each year, followed by two smaller peaks probably related to the fall and late winter peaks (Fig. 4). A small subpeak appeared after the fall peak, probably related to the beginning of winter. Time abnormalities were observed in the middle of 2016 and 2017, corresponding to the higher peaks across years. Of interest, time-series decomposition analyses revealed an increasing trend for sightings of suspected mange bears from 2016 to 2018 (Fig. S6) and a decreasing trend for mange-associated necropsy cases (Fig. S7).

Mange, a parasitic skin infestation by mites, appears to be an emerging disease in black bears in NYS. Although mange has sporadically existed in black bears for decades, mange as a source of mortality has been historically rare (NYSDEC 2007). Until recently, human-induced trauma, including legal harvest and vehicle strikes, constituted the highest cause of black bear mortality (NYSDEC 2007; Bertch and Gibeau 2010). However, our exploration of available data suggests that mange, probably caused by S. scabiei, has become an increasingly common source of reported morbidity and mortality in black bears across NYS.

Sarcoptes scabiei was identified in all cases of confirmed mange in this study. Nevertheless, other species of mites can cause mange in black bears, and our results may not reveal the true scope of mite species causing mange in NYS. Cases of mange confirmed by parasitologists originated mainly in areas where mange appeared for the first time or were sporadic and, therefore, interest in investigating was high. In other areas, mange was diagnosed in the field on the basis of prior experience with the visible characteristics of this disease and further diagnostic workup was not performed. Thus, other species of mites, as well as other skin pathogens, may have been missed. It would be useful to undertake laboratory confirmation of all cases to improve the specificity of surveillance.

The original source of mange in the state is unclear. Transmission may have occurred through direct or indirect contact with affected canids, such as the red fox or other wildlife species (Niedringhaus et al. 2019a). Mange cases in NYS may also have arrived by natural migration of infested bears from Pennsylvania, where cases of mange in black bears have been documented since 1991 (Sommerer 2014; Niedringhaus et al. 2019b). Bear-to-bear transmission has been suggested in areas with high mange prevalence, and increasing bear densities may play a role (Niedringhaus et al. 2019b). Transmission may also occur through indirect contact, such as shared use of infested dens (Ko?odziej-Soboci?ska et al. 2014), that may occur in bears during hibernation. However, we cannot determine the specific route of transmission to NYS bears because we do not have information on the movements or behaviors of the live population during the study period.

Given Pennsylvania mange cases, it is surprising that the first cases in NYS were discovered in the north. Possibly, southern NYS cases went undetected; alternatively, initial northern cases may have been transmitted from canid populations. Black bear mortalities in the Southern Zone were not prioritized for necropsy until 2013 because reports were sporadic and the availability of diagnostic facilities was limited. The spatial associations we identified could also be a function of the underlying bear population dynamics of these two disparate areas. Genetic evidence indicates that multiple S. scabiei strains are circulating among black bears in the northeastern US (Peltier et al. 2017). Comparative genetic analysis of mites from the Southern and Northern zones may help to identify the source(s) of mange in black bears in NYS. An experimental study with systematic sampling and increased disease monitoring at the borders of NYS, particularly with contiguous states with known mange outbreaks, also may be beneficial in assessing disease dynamics that arise from natural interactions among bears.

The incidence of mange in bears generally increased across our study period but, as in other studies, demonstrates an inconsistent pattern. It is known that in some wildlife populations mange epizootics may evolve into enzootic disease (Pence and Ueckermann 2002). Although our data show seasonal variation, it is not clear if the disease is epizootic or enzootic. Standardization of monitoring efforts could be useful to confirm patterns through time.

A seasonal pattern emerged, with mange cases peaking in late spring–early summer and showing slight increases in early fall and late winter. Reports of mange mortalities in late spring–early summer might be a result of increased human activity and observation during this period, making identification of chronic mange in a bear more likely. Bears should be seen less often in winter, as they are denning. Sarcoptic mange might both interfere with bears' building fat reserves prehibernation (suggested by Fitzgerald et al. 2008) and increase use of energy during hibernation; thus, bears with mange may be driven to leave hibernation dens prematurely because of depleted fat reserves (emaciation) as noted by Folk et al. (1972), resulting in the late-winter peak observed. The sighting data revealed similar seasonal patterns to those observed in the necropsy records, particularly in early summer. Therefore, winter and summer may be useful seasons to emphasize enhanced mortality and sighting surveillance, respectively.

Our data suggested that a disproportionate number of adult female black bears contracted mange in NYS compared with male black bears, which is consistent with other reports of mange in bears (Schmitt et al. 1987; Forrester et al. 1993; Fitzgerald et al. 2008). Increased susceptibility of female black bears may be linked to a decreased cellular immune response caused by female hormones or to the reduction of immune function in lactating females (Balestrieri et al. 2006; Yang et al. 2013; Roved et al. 2017). In addition, periods of implantation, gestation, or lactation could present challenges during hibernation, especially due to the high metabolic demand (Hellgren 1998), making females more susceptible to mange.

Severe mange cases are often accompanied by secondary infections (Jimenez et al. 2010). Along with an alteration of cellular immunity during hibernation, low fat reserves may produce a feedback cycle increasing the probability of secondary infections that may result in even higher weight loss (Hellgren 1998; Maslow et al. 2003; Balestrieri et al. 2006). Indeed, we identified concomitant infections with Malassezia sp. and Pelodera sp. in bears with mange exhibiting higher percentages of hair loss and emaciation, similar to previous reports (Salkin et al. 1980; Balestrieri et al. 2006; Fitzgerald et al. 2008). Although B. transfuga has not previously been reported in black bears with mange, it is a common parasite of bears (Catalano et al. 2015), so our finding of coinfection may not be unusual.

Transmission of mites between mother and cubs, as suggested by Schmitt et al. (1987), may explain the presence of mange in juveniles in our data. It is likely that infection begins with the mother and progresses in the juveniles for several months; this might explain why we found no differences by age class. In coyotes, Pence et al. (1983) advised analysis of juvenile cases on the basis of the prevalence in adult canids, given the potential for exposure. Because of differences in social behavior between the species, it is not known how this method would apply to the situation in black bears (Niedringhaus et al. 2019a).

We used two independent data sources to identify patterns of mange in black bears in NYS since 2009. Nevertheless, limitations need to be addressed. Because our data were opportunistically collected, we acknowledge that sampling biases may have influenced our results. Our data do not constitute a random sample, and our sample sizes were low; thus we used univariate statistics with caution and did not use multivariate techniques requiring additional data and departures from the assumptions. In addition, our pooled data may contain two or more records on the same bear despite our best attempts to minimize duplicates. More complete reports and active research in the future might reduce the bias in black bear mange analysis and optimize management actions.

Because of its recent emergence, the public may not be aware of the signs of mange infections in black bears in NYS or that S. scabiei is a public health concern. However, our data suggest that outward signs of mange probably correspond to the presence of the pathogen as confirmed by diagnostic evaluation. In addition to use of a systematic sampling methodology and additional surveillance of mange in a monitoring program, a public outreach component to identify bears with mange may bolster use of sighting data to monitor spread of the pathogen more comprehensively.

Over time, it may become more important to comprehensively assess if or to what extent mange has diffused through the wild black bear population in NYS and how it has affected the welfare of these animals. Additionally, it might be fruitful to test whether mange has had a population-scale impact on black bears both in NYS and across its whole range. It would be informative to assess possible sources of mange for NYS; whether mange is spreading across the state; how mange may affect hunter harvest; and whether wildlife management, agricultural or urban land use, or interactions with other species may have produced environments that have fostered the spread of mange. Although we acknowledge that our results, limited by the available data, may not represent the true historical and contemporary distributions and prevalence of mange in black bears in NYS, we were successful in using archived information to provide a starting place to consider a dedicated monitoring program to identify further emergence and spread of the parasite through NYS.

Supplementary material for this article is online at http://dx.doi.org/10.7589/JWD-D-22-00010.

We thank Niki Dean and Elizabeth Buckles with the Cornell Wildlife Health Lab, as well as Arthur Kirsch, Joseph Okoniewski, and the wildlife biologists of the NYSDEC Big Game Team. We thank the two anonymous reviewers that made improvements to this manuscript. Analysis and writing work were funded by the National Agency for Research and Development Beca Doctorado Nacional 21201076, awarded to Z.R.-S. Wildlife Health Program necropsy investigations were funded by Federal Wildlife Restoration grant W-178-R.