Next Article in Journal
The Diet of Eleonora’s Falcons (Falco eleonorae) during the Autumn Migration of Passerine Birds across the Aegean Sea
Previous Article in Journal
Pan Trapping and Malaise Trapping: A Comparison of Bee Collection Techniques in Subalpine Meadows
Previous Article in Special Issue
Wildlife Emergency Response Services Data Provide Insights into Human and Non-Human Threats to Wildlife and the Response to Those Threats
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 16
Issue 9
10.3390/d16090537
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Exposure of American Black Bears (Ursus americanus) to Ticks, Tick-Borne Diseases, and Intestinal Parasites in Wisconsin

by
Nika S. Reichert
1,
Daniela Mathieu
1,
Christopher J. Katz
2 and
Kent A. Hatch
1,*
1
Department of Life Science, Long Island University Post, 720 Northern Boulevard, Brookville, NY 11548, USA
2
Two Rivers Veterinary Hospital, 2339 Roosevelt Avenue, Two Rivers, WI 54241, USA
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(9), 537; https://doi.org/10.3390/d16090537
Submission received: 17 May 2024 / Revised: 5 August 2024 / Accepted: 7 August 2024 / Published: 2 September 2024
(This article belongs to the Special Issue Wildlife Welfare)
Browse Figure
Versions Notes

Abstract

:
We surveyed 159 American black bears (Ursus americanus) over a period of three years for the occurrence of ticks, tick-borne diseases, and intestinal parasites in Wisconsin. We collected blood from the bears to test for the presence of antibodies to Borrelia burgdorferi (Lyme disease), Rickettsia rickettsii (Rocky Mountain spotted fever (RMSF)), Babesia, Ehrlichia, Ehrlichia canis, Brucella canis, and Anaplasma phagocytophilum. We also examined scat samples for intestinal parasites. We commonly found the tick Dermacentor variabilis, but also present the first report of Rhipicephalus sanguineus on black bears. We detected antibodies to Lyme disease and RMSF. We detected antibodies to E. canis for the first time in a bear and both antibodies to R. rickettsii and A. phagocytophilum for the first time in a black bear in Wisconsin. No antibodies for Babesia or Br. canis were detected. We found eggs of the intestinal parasite Baylasascaris transfuga as well as a low number of Toxascara leonina and unknown Capillaria species occurrences in the examined feces.

1. Introduction

We explored the prevalence of ticks, tick-borne diseases, and intestinal parasites in American black bears (Ursus americanus; hereafter, black bear) in two Wisconsin populations. Little is known about the ticks and parasites of black bears in Wisconsin and elsewhere as they have not been widely studied [1,2]. When testing for tick-borne diseases, many previous studies either tested the ticks directly or tested the bears’ blood for the pathogens’ presence. The advantage of testing for the antibody is that the pathogen itself only circulates in the blood for a short time and thus the absence of the pathogen may not be indicative of exposure to the pathogen [1]. The presence of a bacterium in the tick found on a black bear is also not evidence that the pathogen was transferred to the bear. If a tick removed from a bear tests positive for a pathogen, but the pathogen is not found in the blood, it suggests the tick acquired the disease from a different host in a previous life stage [1] and that the bear may not have actually been exposed to the disease. By contrast, testing blood directly for antibodies provides evidence of actual exposure to a disease. Additionally testing for seroprevalence instead of the actual pathogen provides a method of detection long after the pathogen has been eliminated by the host’s immune system and can provide a more comprehensive picture of disease exposure in wildlife.
Black bears have a broad geographic range in North America [3] and are known to carry ticks throughout much of their range. Tick abundance on black bears varies with season, with the highest abundances recorded in the spring and the lowest in the fall [3]. Different ixodid tick species have different lifecycle seasonalities [4], so observed variations in tick abundance may be due to this seasonal effect [1]. Previous studies in Wisconsin found the tick species Dermacentor variabilis, Dermacentor albipictus, and Ixodes scapularis on black bears [2], but it is unknown whether black bears are acting as reservoirs for tick-borne diseases [5]. However, they likely play a significant role in the dispersal of ticks due to the wide ranges covered by black bears, with young males often wandering hundreds of miles and groupings of multiple animals increasing the chances of transmission [6].
Black bears have been recorded carrying the following tick-borne diseases in different states: in New Jersey, Babesia microti, Anaplasma phagocytophilum and Babesia sensu stricto antibodies were recorded in black bear blood [1]; in Wisconsin, a Borellia species that is morphologically similar to Borellia burgdorferi, the primary causative agent of Lyme disease, has been detected [7] in black bear blood; Lyme disease was also detected in black bears on the West Coast [8,9]; in Idaho, Tularemia and Rocky Mountain spotted fever (RMSF) were detected in black bears [10] with RMSF also detected in Maryland [11].
We also looked at the presence of intestinal parasites in black bears. Black bears can have helminth parasites and a variety of cestodes and nematodes [12]. Baylisascaris transfuga is a nematode parasite that occurs worldwide in bear species, and, like all nematodes, it has zoonotic potential [13]. B. transfuga has been detected in all bear species except the spectacled bear, Tremarctos ornatus [14]. Prevalence ranges from 12.5 to 80% in black bears tested in Ontario, Wyoming, Minnesota, Montana, and Alaska [14]. In northern Wisconsin, Manville (1978) found an 89% prevalence of B. transfuga in black bears, reporting no known infections in the south of the US at that time. However, since then, a range of 23–53% prevalence has been reported in Southeastern states [2,15,16,17,18], cementing B. transfuga’s position as a widespread and common parasite of black bears throughout the USA.
Seasonal variations have been recorded in the prevalence of intestinal parasites of brown bears in both Europe and North America with contradictory findings. Štrkolcová et al. (2018) report that the highest prevalence of infection occurs in autumn and the lowest prevalence of infection occurs in spring in central Slovakia [19]. Likewise, in Canada, one study found the highest prevalence in autumn [20], while another found a higher prevalence in summer, peaking from June to August, and a lower prevalence in autumn and winter [21]. Seasonal dynamics may be influenced by hormonal and metabolic changes in black bears that are linked to hibernation [20]. Understanding seasonal dynamics may help predict the spread of these parasites in response to climate change. For example, Baylisascaris eggs can survive temperatures down to −15 °C [13] and have been shown to develop faster in soils at 35 °C than at 25 °C while not developing at 5 °C [22]; so, globally rising temperatures could facilitate an extension of ranges towards the north, resulting in higher levels of infection and increasing the risk of zoonosis of this parasite.
In 2003–2006, we collected data on ticks, tick-borne diseases, and intestinal parasites of black bears in Wisconsin. We present these data to provide additional information on the occurrence of ticks, tick-borne diseases, and intestinal parasites as a follow-up to the single previously published study of the ecto- and endoparasites of black bears in Wisconsin [2]. We also look at the seasonal prevalence of ticks and intestinal parasites.

2. Materials and Methods

2.1. Sampling

A total of 159 American black bears were captured in Lakewood (45°18′2.7″ N, 88°18′24.4″ W) and Hiles (45°42′13.7″ N, 88°58′38.1″ W) Wisconsin, from 2003 to 2006 (see [23] for details on capture and locations). We examined bears for ticks in February and March, May and June, and October and November from 2003 to 2005. In 2006, we only surveyed bears for ticks in February and March. In summer, bears were trapped in culvert traps, baited with ice cream cones. The bears were then assigned an ID number; sex and weight were also recorded. We then placed collars on the bears (Televilt Simplex, TVP Positions AB, Lindesberg Sweden: collars equipped with GPS) and used Telonics antennas and receivers (model TR4 and RA-2AK VHF; Telonics, Inc. Mesa, AZ, USA) to track the bears from a distance. Bears were tracked to their hibernating dens for sample collection in winter. To anesthetize the bears for sample collection, we either administered 4.4–8.8 mg/kg of tiletamine and zolazepam (Telazol; Fort Dodge Laboratories, Fort Dodge, IA, USA) or a 5:1 mixture of ketamine and xylazine (4.6 mg/kg ketamine and 0.9 mg/kg xylazine). We injected the anesthesia via a Dan-Inject CO2 dart pistol (Dan-Inject, Kolding, Denmark) using 3 mL darts with a 2.0 × 40 mm needle. We did not administer oxygen while the bears were under anesthesia but administered more anesthetic when required. We also did not reverse the xylazine. Rather, we returned bears that we sampled in summer to the culvert traps to safely recover from the anesthesia, while bears sampled in winter were returned to their dens to continue hibernation. None of the bears abandoned their dens or young and none displayed signs of disease. We took 20 mL blood samples from the jugular, medial, or lateral saphenous vein of each bear and stored the blood on ice until the sample clotted. The sample was centrifuged the same day until the serum was separated (6 mL of whole blood in EDTA and 14 mL in serum separation tubes, Becton Dickinson Vacutainers San Antonio, TX, USA). The serum was then kept refrigerated at 3 °C during shipment to Michigan State University [23]. The serum was tested for antibodies to the following tick-borne disease agents: Borrelia burgdorferi, Rickettsia rickettsii, Erlichia, Erlichia canis, Babesia, Brucella canis, and Anaplasma phagocytophilum. We were not able to obtain records of the specific tests conducted. We analyzed intestinal parasite eggs at the Two Rivers Veterinary Hospital using fecal flotation with a concentrated sugar solution. Eggs floating in the top layer of the solution were then examined under a microscope to identify the species. This method does not isolate fluke eggs. We examined bears by hand for the presence of adult ticks only and only recorded whether ticks were present or absent. We did not record the number of ticks present on a bear.

2.2. Information on Tests Performed: Sensitivity and Specificity

Blood samples were tested for antibodies for the diseases in question at the Veterinary Diagnostic Laboratory at Michigan State University (MSU). While the lab does not have a record of which tests they used at the time the samples were analyzed, they were able to provide references for current tests used for some of the diseases. Current tests have a 94% sensitivity for B. burgdorferi detection, in samples collected from ticks, rodents, and humans [24,25]; they have a 79.3% sensitivity for Rickettsia collected in human blood samples [26]; and they have a 98% sensitivity for Erlichia in dog and cat samples [27] (references provided by MSU lab). The MSU Lab was not able to provide references for the sensitivities and specificities of the other diseases tested. However, all tests of sensitivity and specificity were performed on species other than black bears and may not be valid for black bears in any case [23].

2.3. Statistical Analysis

We combined the datasets for the two locations as no significant differences in exposure to ticks (p = 0.548) or tick-borne diseases (p = 0.536) were found between them. A bear was considered positive for ticks if at least one tick was found on it. Similarly, a bear was considered positive for intestinal parasites if at least one egg of that parasite was found in its feces. A test for a disease was considered positive if antibodies to the disease were detected in the bear’s serum, indicating that the bear was exposed to the pathogen, though not necessarily that the bear had the disease. As many bears were recaptured at different times of the year, we based our analysis of the tick-borne diseases on the number of tests performed, not the number of bears that were tested. Counts for some tests differ as not every bear was tested for each disease in each year, and some were recaptured and tested multiple times. Nine bears were tested on two different occasions, three were tested on three different dates, and one was tested on four separate occasions. All other diseases (Ehrlichia, R. rickettsii, Babesia, Br. canis, Ehrlichia canis, A. phagocytophilum) except Lyme disease were grouped into a single category because the number of times antibodies were detected was very low. Seasons were defined as follows: summer = May and June; winter = February and March; fall = October and November. We used logistic regression to test for the effects of sex on ticks and intestinal parasites and the effect of season on intestinal parasites. For all regressions, the significance level was p = 0.05 [5].

3. Results

Our results indicate a high degree of seasonality in ticks. We found ticks present on 100% of the bears examined in May and June, but on 0% of bears examined in February and March or October and November for all three years. We also found a significant difference in the number of infested male and female bears (p = 0.0346). The main tick present was Dermacentor variabilis, which was detected 84 times; however, two occurrences of Rhipicephalus sanguineus were also recorded simultaneously with D. variabilis. No Ixode scapularis were detected (Figure 1B, Table 1).
Antibodies to Lyme disease were only detected in 2005 and only in June and October (Figure 1C). Of the 111 tests completed for Lyme disease, 10 were positive giving 9% seroprevalence. For all other tick-borne diseases, the only positive tests occurred in 2005 and only in June and October (Figure 1D). Of the 483 tests performed 18 were positive giving 3.7% seroprevalence of all other tick-borne diseases tested. These tests were positive in low numbers for antibodies: 112 tests for RMSF rendered only 3 positive tests; 4 positive tests were derived out of 39 for E. canis; 1 positive test was derived out of 39 tests for A. phagocytophilum; no positive tests were derived out of the 79 tests for Babesia or the 39 tests for Br. canis. The 73 tests conducted in 2003–2004 for Ehrlichia species antibodies also rendered no positive results (Table 2).
While both a Wald test and a likelihood ratio test found a significant effect of season on the proportion of bears infected with all the intestinal parasites that we detected (W1 = 4.782, p = 0.029; X2 = 5.089, p = 0.024), there was no significant effect of season for the intestinal parasite B. transfuga alone (W1 = 2.071, p = 0.150; X2 = 2.111, p = 0.146). The nematode B. transfuga was found in the feces of 11% of the bears sampled. The highest numbers of infected bears were found in February and June. A low level of positive tests was recorded in each year from 2003 to 2006 (Figure 1E, Table 3). Two occurrences of an unknown capillaria species and three cases of Toxascaris leonina were also found in the testing period. We found no significant difference in the occurrence of intestinal parasites between male and female black bears (p = 0.061).

4. Discussion

4.1. Tick Presence

Although a significant difference in infestation between male and female black bears was detected, this is likely an artifact of the proportion of male and female bears captured in May and June when 100% of the bears had ticks compared to the proportion of male and female bears captured in October, November, February, and March, when 0% of bears were infested. Dermacentor variabilis is a widespread parasite of black bears [1] and this is confirmed by its common occurrence on the black bears of this study. However, it appears ours is the first study to detect Rhipicephalus sanguineus on black bears in the U.S. The only previous finding of this tick on a bear species was reported on an unidentified bear from India [14]. R. sanguineus is commonly found parasitizing dogs, is the most widespread tick in the world [28], and is extremely common in tropical and subtropical climates, probably originating in the tropics or the Mediterranean [29]. While it has spread worldwide, likely through introduction by dogs, it is still rarely found in temperate and cold climates [30,31]. However, it is now considered endemic throughout the USA with varying prevalences in different locations [29]. R. sanguineus is generally rare in Wisconsin [32] with early reports attributing its presence there to dogs traveling from warmer climates like the southern USA [33]. As it is an endophilic tick, it could survive and cause infestations in any heated indoor location throughout the world [30], possibly accounting for our discovery of this tick on Wisconsin black bears. R. sanguineus acts as a vector for animal pathogens like E. canis and Babesia vogeli and significant human pathogens such as R. rickettsii, which causes Rocky Mountain spotted fever in the USA [31]. With this tick being found prevalently year-round in warm climates worldwide, reproducing effectively between 20 °C and 35 °C [28,31], its detection on wildlife in Wisconsin could be indicative of an extension of its range to the north as a result of climate change.
Tick seasonality differs between species and likely explains some of our observed patterns of presence and absence. D. variabilis is active in Nova Scotia and Massachusetts from April to August, with a seasonal peak in May and June. Even with low sampling efforts in October and November, our findings support this pattern of seasonal activity from April to August. The high sampling effort in February would have found ticks if they were present on black bears at that time of year.
Ticks generally enter a non-host-seeking, behavioral diapause in late fall/winter in order to survive the colder temperatures [34]. Especially the endophilic R. sanguineus is unlikely to be actively attached in cold Wisconsin winters, as successful completion of the tick lifecycle following host attachment is unlikely in temperatures below 20 °C [28]. A tick’s life stage can also impact their ability to survive the cold. D. variabilis larvae can survive cold temperature exposure at higher rates than nymphs and adults [35]. Similar to R. sanguineus, in states at a lower latitude like Kentucky and Ohio, D. variabilis ceases host-seeking activities in August and September, respectively [36]. However, a recent study has found both D. variabilis and I. scapularis undertaking host-seeking behavior in the winter months in the central midwestern states of Kansas, Missouri, Oklahoma, and Arkansas [34]. While it is unlikely that tick behavior in these lower latitudes is similar to that of ticks in the more northern states (for example, bimodal activity peaks have been observed from early April to early June and from late June to July in Kentucky, compared to a unimodal peak in May–June observed in the more northern regions of Massachusetts and Nova Scotia [36]), it is possible that adults may actively seek hosts even in more northern latitudes if snow cover is limited and temperatures rise above 4 °C [37,38]. An observation of host-seeking in winter indicates the potential for tick attachment year-round, which may be accentuated by climate change, as it is known to affect temperatures and rainfall in ways likely to favor tick range and active season expansion, possibly leading to a higher risk of transmission of tick-borne diseases [39]. This suggests that monitoring the seasonality and distribution of tick species among wildlife is important for the protection of public health and understanding of the risk of contracting tick-borne diseases.
In more southern locations, D. variabilis’ active season is longer, starting as early as late March in Georgia and ending in September in Ohio [36], which may coincide with an expansion further north as global temperatures rise [30]. However, range extensions may still be limited in other locations by a drop in humidity as temperatures rise, causing a midsummer dip in tick prevalence [36].

4.2. Lyme Disease

The first occurrence of borreliosis in bears in Wisconsin was reported in 1988 when a Borrelia species suspected to be B. burgdorferi was isolated from 17% of black bear kidney and blood samples [7]. Our finding of a 9% prevalence is lower than this previous finding as well as other studies that found B. burgdorferi in 12.6% of black bears in California, Oregon, and Washington [8], 26% seroprevalence in California [9], and a prevalence of 18% in Maryland [11]. However, when tested for the presence of the pathogen itself, 0% of black bears in New Jersey were found to have B. burgdorferi [1,5]. Likewise, Stephenson et al. (2015) also tested directly for B. burgdorferi with zero positives detected [9].
Our detection of Lyme disease in the black bears we studied illustrates the advantage of using serological tests to determine exposure to tick-borne diseases. The two tick species we detected on black bears are not known to transmit Lyme disease. Surprisingly, we did not find Ixodes scapularis on the black bears we examined, though it is known to parasitize black bears throughout the USA [3] and is the most frequent vector of Lyme disease in the Upper Midwest and Northeastern United States [3,40,41,42,43]. Both adults and nymphs can transmit B. burgdorfori [42,44,45]; while I. scapularis in the Upper Midwest are active throughout the period between April and November, adult populations typically peak in April and October [46]. Our May sampling efforts were likely too late to catch the April peak in adult abundance and our sampling effort was lower in the fall, possibly accounting for our lack of detection of adult I. scapularis ticks at that time of year. However, nymph numbers peak in June, when the majority of our tick-positive samples occurred [46]. We likely did not detect bears with attached nymphs because our collection efforts focused on adults, not nymphs, and nymphs are harder to detect with the naked eye due to their small size [1]. Additionally, nymphs and adults feed on their hosts for a limited time. It takes nymphs only 4–5 days to obtain a sufficiently large blood meal, at which point they drop off [37]. For adults, it only takes 7 days to obtain a sufficient blood meal [37]. So, unless I. scapularis tick populations are such that black bears are continuously infested with ticks, detection of ticks or nymphs crawling onto or attached to a black bear may be sporadic; therefore, we may not have detected them at the time the host is captured. However, serological tests are able to detect late-stage Lyme disease since antibodies remain in the blood for several months to years after the bacteria are eliminated [47]. Therefore, the use of serological tests allowed us to detect black bear exposure to Lyme disease, despite the fact that we did not find any I. scapularis nymphs or adults on the black bears we examined.
Human cases of Lyme disease peak in June–July in the United States, with smaller regional variations depending on tick-feeding behavior influenced by environmental factors like temperature, humidity, and rainfall [43]. We found about the same number of bears positive for Lyme antibodies in June and October. However, the only positive samples were from 2005 and sampling efforts in that year were only in June and October. Therefore, as antibodies can last months to years, it is hard to determine whether the apparent seasonality of the presence of Lyme disease in our study is actual, or due to the fact that our sampling was limited to only June and October. However, given that the tests performed in 2003 and 2004 also contained June samples and the number of tests performed in those two years combined was greater than in 2005, if Lyme disease were present in bears at these sites in 2003 and 2004, we should have detected it.
There are a couple of reasons why we might not have detected exposure to B. burgdorferi in black bears sampled in 2003 and 2004. First, this pathogen is spreading among I. scapularis ticks in the upper Midwest and continues to emerge at different sites in different years [40]. It may therefore be that Lyme disease was newly emerging among I. scapularis ticks in 2005 at our study sites. According to the Wisconsin Environmental Public Health Tracking Program [48], there was one reported case of Lyme disease in the two counties containing our study sites in 2003 and none in 2004. In 2005, there were three positive cases in the two counties, while in the rest of Wisconsin, the case numbers from 2005 are more than double those that were reported in 2003, indicating a general uptick of Lyme disease in the state as a whole. Second, even if B. burgdorferi was already endemic at these sites by 2003, the prevalence of B. burgdorferi among years and between sites is highly variable and the prevalence of B. burgdorferi or the ticks that carry it at a site in one year is not predictive of their prevalence at the same site in previous or subsequent years [40,46].

4.3. Other Tick-Borne Diseases

The only positive detections of antibodies for R. rickettsii, E. canis, and A. phagocytophilum occurred in June and October of 2005, since those were the only months sampled that year for exposure to tick-borne diseases. While the sampling effort was much higher in June than in October, the percentage of bears testing positive for antibodies to these organisms were higher in October than in June. However, the prevalence of positive cases of these tick-borne diseases was low.
Cases of RMSF have been reported widely across the USA, including in Wisconsin [49]. However, our finding seems to be the first report of exposure to this disease detected in black bears in Wisconsin. A Rickettsia species has been recorded in ticks collected from black bears in New Jersey [1] and low levels of R. rickettsii were detected in Idaho (2%) and Maryland (6.6%) [10,11], comparable to the levels we recorded in 2005 (7%).
E. canis infects domestic dogs and wild carnivores. Its recognized vectors include D. variables and R. sanguineus. It has been detected in a variety of canid and felid species, raccoons, and some cases in humans [50], but its detection in an Ursid species has not previously been recorded. E. canis is the most common disease of dogs in the Southern US. One study found the highest seroprevalence of E. canis in dogs to be in Texas, Louisiana, Arkansas, and Oklahoma [29]. While there have not been any cases of human disease due to E. canis in the USA, cases have been recorded in Venezuela, Russia, and Costa Rica [51,52]. We detected one positive result for E. canis in our study and this appears to be the first record of exposure to E. canis in any bear species. It has been rarely tested for in black bears, with a previous study in Maryland detecting no positive E. canis results [11]. Testing for Ehrlichia spp had previously been positive for 100% of bears tested in Oklahoma [53] but no specific Ehrlichia species was identified in the study.
A. phagocytophilum is known to occur in Wisconsin and the Upper Midwest [40] and has been detected in wildlife species such as white-tailed deer [54], but this appears to be the first report of exposure to this pathogen in black bears in the state. We detected a 10% prevalence of A. phagocytophilum in black bears, which is similar to the 9.2% prevalence detected in New Jersey [5], and lower than the 21% prevalence detected in Pennsylvania [55]; meanwhile, it is higher than the prevalences detected in black bears in California, Oregon and Washington (4.5%) [8], Maryland (6.7%) [11], and North Carolina (3%) [56]. As A. phagocytophilum is transmitted by Ixodes species [54], it is again interesting that none of these vector ticks were detected on the black bears in our study. However, possible reasons for the lack of detection of these ticks have already been discussed above. Since we did not test for A. phagocytophilum in black bears before 2005, we do not know whether it was present in black bears in 2003 and 2004. Our report of A. phagocytophilum among black bears in Wisconsin suggests that the monitoring of tick-borne diseases may be important to assessing the potential risk to public health and that serological tests are more likely to detect exposure of black bears to A. phagocytophilum than attempting to detect infected ticks on black bears.
The first positive human case of babesiosis in Wisconsin was confirmed in 2001, and since then, the number of cases in the state has risen over time [57]. We detected no positive results for Babesia, which has since been detected at varying levels in black bear blood in New Jersey (7.1%) [1], Oklahoma (6%) [53], and North Carolina (17%) [58]. Our samples were taken only a few years after Babesia was first reported in the state, so it probably was not yet widespread. However, with its detection in black bears from other states in more recent years and the increase in human cases reported in Wisconsin since our samples were collected, future studies on Wisconsin black bear populations may find increased levels of exposure to the pathogen.
Brucella species have previously been detected in grizzly bears [59,60], black bears, and polar bears in Alaska [61]. Br. canis is a common pathogen causing brucellosis in dogs and other canids worldwide. Outbreaks in Wisconsin kennels were previously associated with the US interstate dog trade [62]. While Br. canis can infect carnivores [63], there have not been many studies testing for Br. canis exposure in bears. We did not detect any Br. canis. Similarly, a study by Bronson et al. [11] in Maryland also detected none. This is not necessarily surprising because, when Brucella spp. were previously detected in black bears, prevalence was low, though it was higher in polar and grizzly bears [59,60,61].
While we did not find antibodies to A. phagocytophilum, E. canis, or B. canis in 2003–2004, because we first started testing for these specifically in 2005, we did use a general test for Ehrlichia species in 2003–2004. It is therefore likely that some of these tests would have been positive, had E. canis been present at the time. However, these tests were all negative (Table 2). Anecdotal evidence also supports the likelihood that Lyme disease, ehrlichosis, and anaplasmosis, as well as the presence of I. scapularis, were just emerging at this time in these parts of Wisconsin, since it was at this time that CK first saw Ixodes ticks and his first cases of Lyme disease in his veterinary practice in Two Rivers, Wisconsin (Pers. Obs.). These ticks are now endemic in this area.

4.4. Intestinal Parasites

B. transfuga is a globally distributed intestinal parasite of bears and our study confirms the continued presence of B. transfuga in Wisconsin black bears since Manville’s 1978 study [2], while also providing another data point for mapping its widespread distribution. While the distribution of B. transfuga is fairly well understood, differences in seasonal prevalence are still unclear. The presence/absence of intestinal parasites may be linked to hormonal changes due to hibernation [19]. We collected samples from Wisconsin in February, March, May, June, October, and November, thereby including both the hibernating and active seasons [64,65]. The highest levels of B. transfuga infection were found in June (active) and February (hibernating). While these results would support Borka-Vitális et al. (2017) [66], findings of no significant seasonal differences in B. transfuga infection and refute the idea that intestinal parasite levels are linked to hibernation, it may be that this is due to sampling bias, since February and June had the highest overall sampling effort (Figure 1E).

5. Conclusions

Black bears in Wisconsin had a high degree of tick infestation in summer and low levels in winter. As found in previous studies, we recorded D. variabilis ticks on many of the black bears we sampled. However, this is the first reported case of R. sanguineus ticks for any bear. Similar to other studies, we found positive results for B. burgdorferi, R. rickettsii, and A. phagocytophilum. However, our finding of E. canis is, to our knowledge, the first of its kind for an Ursid species. A Borrelia species had previously been detected in black bears in Wisconsin, but this report of R. rickettsii and A. phagocytophilum appears to be the first record of these pathogens having been present in a black bear in Wisconsin. We also recorded cases of the intestinal parasite B. transfuga throughout the year, with peaks seeming to occur in February and June.
The overall low-level detection of antibodies to the tick-borne diseases tested in our study indicates that black bears are likely not common reservoirs for these diseases and adds additional baseline data on tick-borne diseases in black bears. Nevertheless, the fact that antibodies were detected demonstrates the advantages of using serological tests for tick-borne diseases; this is indicative that there is a possibility of black bears becoming a reservoir for these diseases, and demonstrates the need for further study of black bears and other wildlife to understand the nature and extent of the risk of wildlife reservoirs for tick-borne diseases.

Author Contributions

Conceptualization, K.A.H. and C.J.K.; methodology, K.A.H. and C.J.K.; formal analysis, K.A.H.; investigation, K.A.H. and C.J.K.; resources, K.A.H. and C.J.K.; data curation, K.A.H. and N.S.R.; writing—original draft preparation, N.S.R. and D.M.; writing—review and editing, K.A.H.; supervision, K.A.H.; project administration, K.A.H. and C.J.K.; funding acquisition, C.J.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding. Funding was provided by C.J.K.

Institutional Review Board Statement

Sample collection and analysis was conducted by C.J.K. under the auspices of a Wisconsin Department of National Resources for the scientific collectors’ permit (SCP NER 155). All bears were captured, and all samples were taken with the guidance and assistance of Scott Anderson of the U.S. Forest Service and under the Wisconsin Department of Natural Resources Scientific Collector’s Permit SCP NER 155 and following all state-mandated guidelines for the ethical treatment of animals therein.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors on request.

Acknowledgments

We would like to thank the staff at Two Rivers Veterinary Hospital and Scott Anderson of the U.S. Forest Service for their support and assistance with field work, as well as obtaining and analyzing the samples.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Chern, K.; Bird, M.; Frey, K.; Huffman, J.E. Ticks and Tick-Borne Pathogens of Black Bears (Ursus americanus) in New Jersey. J. Pa. Acad. Sci. 2016, 90, 25–30. [Google Scholar] [CrossRef]
  2. Manville, A.M. Ecto-and endoparasites of the black bear in northern Wisconsin. J. Wildl. Dis. 1978, 14, 97–101. [Google Scholar] [CrossRef]
  3. Tiffin, H.S.; Skvarla, M.J.; Machtinger, E.T. Tick Abundance and Life-Stage Segregation on the American Black Bear (Ursus Americanus). Int. J. Parasitol. Parasites Wildl. 2021, 16, 208–216. [Google Scholar] [CrossRef]
  4. Duscher, G.G.; Feiler, A.; Leschnik, M.; Joachim, A. Seasonal and Spatial Distribution of Ixodid Tick Species Feeding on Naturally Infested Dogs from Eastern Austria and the Influence of Acaricides/Repellents on These Parameters. Parasites Vectors 2013, 6, 76. [Google Scholar] [CrossRef]
  5. Zolnik, C.P.; Makkay, A.M.; Falco, R.C.; Daniels, T.J. American Black Bears as Hosts of Blacklegged Ticks (Acari: Ixodidae) in the Northeastern United States. J. Med. Entomol. 2015, 52, 1103–1110. [Google Scholar] [CrossRef] [PubMed]
  6. Klein, S.L. Hormonal and Immunological Mechanisms Mediating Sex Differences in Parasite Infection. Parasite Immunol. 2004, 26, 247–264. [Google Scholar] [CrossRef]
  7. Kazmierczak, J.J.; Amundson, T.E.; Burgess, E.C. Borreliosis in Free-Ranging Black Bears from Wisconsin. J. Wildl. Dis. 1988, 24, 366–368. [Google Scholar] [CrossRef] [PubMed]
  8. Mortenson, J.A. Serologic Survey of Infectious Disease Agents in Black Bears (Ursus americanus) of California, Oregon, and Washington. Master’s Thesis, Oregon State University, Corvallis, OR, USA, 18 November 1998. [Google Scholar]
  9. Stephenson, N.; Higley, J.M.; Sajecki, J.L.; Chomel, B.B.; Brown, R.N.; Foley, J.E. Demographic Characteristics and Infectious Diseases of a Population of American Black Bears in Humboldt County, California. Vector-Borne Zoonotic Dis. 2015, 15, 116–123. [Google Scholar] [CrossRef]
  10. Binninger, C.E.; Beecham, J.J.; Thomas, L.A.; Winward, L.D. A serologic survey for selected infectious diseases of black bears in Idaho. J. Wildl. Dis. 1980, 16, 423–430. [Google Scholar] [CrossRef] [PubMed]
  11. Bronson, E.; Spiker, H.; Driscoll, C.P. Serosurvey for selected pathogens in free-ranging American black bears (Ursus americanus) in Maryland, USA. J. Wildl. Dis. 2014, 50, 829–836. [Google Scholar] [CrossRef] [PubMed]
  12. Rogers, L.L. Parasites of black bears of the Lake Superior region. J. Wildl. Dis. 1975, 11, 189–192. [Google Scholar] [CrossRef] [PubMed]
  13. Bauer, C. Baylisascariosis—Infections of Animals and Humans with ‘Unusual’ Roundworms. Vet. Parasitol. 2013, 193, 404–412. [Google Scholar] [CrossRef] [PubMed]
  14. Rogers, L.L.; Rogers, S.M. Parasites of Bears: A Review. Bears Their Biol. Manag. 1976, 3, 411. [Google Scholar] [CrossRef]
  15. Crum, J.M.; Nettles, V.F.; Davidson, W.R. Studies on endoparasites of the black bear (Ursus americanus) in the southeastern United States. J. Wildl. Dis. 1978, 14, 178–186. [Google Scholar] [CrossRef] [PubMed]
  16. Foster, G.W.; Cunningham, M.W.; Kinsella, J.M.; Forrester, D.J. Parasitic Helminths of Black Bear Cubs (Ursus americanus) from Florida. J. Parasitol. 2004, 90, 173–175. [Google Scholar] [CrossRef] [PubMed]
  17. Jenness, B. Internal Parasitism in Free-Ranging Black Bears in the Pisgah National Forest. McNair Sch. J. 1997, 1, 23–25. [Google Scholar]
  18. Pence, D.B.; Crum, J.M.; Conti, J.A. Ecological Analyses of Helminth Populations in the Black Bear, Ursus Americanus, from North America. J. Parasitol. 1983, 69, 933. [Google Scholar] [CrossRef]
  19. Štrkolcová, G.; Goldová, M.; Šnábel, V.; Špakulová, M.; Orosová, T.; Halán, M.; Mojžišová, J. A Frequent Roundworm Baylisascaris Transfuga in Overpopulated Brown Bears (Ursus Arctos) in Slovakia: A Problem Worthy of Attention. Acta Parasitol. 2018, 63, 167–174. [Google Scholar] [CrossRef] [PubMed]
  20. Molnár, L.; Königová, A.; Major, P.; Vasilková, Z.; Tomková, M.; Várady, M. Seasonal Pattern of Prevalence and Excretion of Eggs of Baylisascaris Transfuga in the Brown Bear (Ursus Arctos). Animals 2020, 10, 2428. [Google Scholar] [CrossRef]
  21. Clark, J.D.; Loew, F.M.; Burns, K.F. The Use of Dichlorvos as an Anthelmintic in Naturally Parasitized Bears. J. Am. Vet. Med. Assoc. 1969, 155, 1093–1097. [Google Scholar]
  22. Kim, M.-K.; Pyo, K.-H.; Hwang, Y.-S.; Park, K.H.; Hwang, I.G.; Chai, J.-Y.; Shin, E.-H. Effect of Temperature on Embryonation of Ascaris Suum Eggs in an Environmental Chamber. Korean J. Parasitol. 2012, 50, 239–242. [Google Scholar] [CrossRef]
  23. Sikes, A.M.; Katz, C.J.; Hatch, K.A. Exposure of American Black Bears to Various Pathogens in Wisconsin. Ursus 2022, 2022, 1–8. [Google Scholar] [CrossRef]
  24. Clark, K. Borrelia Species in Host-Seeking Ticks and Small Mammals in Northern Florida. J. Clin. Microbiol. 2004, 42, 5076–5086. [Google Scholar] [CrossRef] [PubMed]
  25. Piesman, J.; Johnson, B.J.B.; Happ, C.M.; Mayer, L.W. Detection of Borrelia Burgdorferi in Ticks by Species-Specific Amplification of the Flagellin Gene. Am. J. Trop. Med. Hyg. 1992, 47, 730–741. [Google Scholar] [CrossRef]
  26. Kato, C.Y.; Chung, I.H.; Robinson, L.K.; Austin, A.L.; Dasch, G.A.; Massung, R.F. Assessment of Real-Time PCR Assay for Detection of Rickettsia Spp. and Rickettsia Rickettsii in Banked Clinical Samples. J. Clin. Microbiol. 2013, 51, 314–317. [Google Scholar] [CrossRef] [PubMed]
  27. Qurollo, B.A.; Riggins, D.; Comyn, A.; Zewde, M.T.; Breitschwerdt, E.B. Development and Validation of a Sensitive and Specific sodB -Based Quantitative PCR Assay for Molecular Detection of Ehrlichia Species. J. Clin. Microbiol. 2014, 52, 4030–4032. [Google Scholar] [CrossRef]
  28. Dantas-Torres, F. Biology and Ecology of the Brown Dog Tick, Rhipicephalus Sanguineus. Parasites Vectors 2010, 3, 26. [Google Scholar] [CrossRef]
  29. Beall, M.J.; Alleman, A.R.; Breitschwerdt, E.B.; Cohn, L.A.; Couto, C.G.; Dryden, M.W.; Guptill, L.C.; Iazbik, C.; Kania, S.A.; Lathan, P.; et al. Seroprevalence of Ehrlichia Canis, Ehrlichia Chaffeensis and Ehrlichia Ewingii in Dogs in North America. Parasites Vectors 2012, 5, 29. [Google Scholar] [CrossRef]
  30. Gray, J.S.; Dautel, H.; Estrada-Peña, A.; Kahl, O.; Lindgren, E. Effects of Climate Change on Ticks and Tick-Borne Diseases in Europe. Interdiscip. Perspect. Infect. Dis. 2009, 2009, 593232. [Google Scholar] [CrossRef]
  31. Gray, J.; Dantas-Torres, F.; Estrada-Peña, A.; Levin, M. Systematics and Ecology of the Brown Dog Tick, Rhipicephalus Sanguineus. Ticks Tick-Borne Dis. 2013, 4, 171–180. [Google Scholar] [CrossRef]
  32. Lee, X.; Murphy, D.S.; Hoang Johnson, D.; Paskewitz, S.M. Passive Animal Surveillance to Identify Ticks in Wisconsin, 2011–2017. Insects 2019, 10, 289. [Google Scholar] [CrossRef]
  33. Bishopp, F.C.; Trembley, H.L. Distribution and Hosts of Certain North American Ticks. J. Parasitol. 1945, 31, 1. [Google Scholar] [CrossRef]
  34. Raghavan, R.K.; Koestel, Z.L.; Boorgula, G.; Hroobi, A.; Ganta, R.; Harrington, J.; Goodin, D.; Stich, R.W.; Anderson, G. Unexpected Winter Questing Activity of Ticks in the Central Midwestern United States. PLoS ONE 2021, 16, e0259769. [Google Scholar] [CrossRef] [PubMed]
  35. Rosendale, A.J.; Farrow, D.W.; Dunlevy, M.E.; Fieler, A.M.; Benoit, J.B. Cold Hardiness and Influences of Hibernaculum Conditions on Overwintering Survival of American Dog Tick Larvae. Ticks Tick-Borne Dis. 2016, 7, 1155–1161. [Google Scholar] [CrossRef]
  36. Burg, J.G. Seasonal Activity and Spatial Distribution of Host-seeking Adults of the Tick Dermacentor Variabilis. Med. Vet. Entomol. 2001, 15, 413–421. [Google Scholar] [CrossRef]
  37. Fish, D. 2 Population Ecology of Ixodes Dammini. In Ecology and Environmental Management of Lyme Disease; Ginsberg, H., Ed.; Rutgers University Press: New Brunswick, NJ, USA, 1993; pp. 25–42. ISBN 978-0-8135-5603-1. [Google Scholar]
  38. Duffy, D.C.; Campbell, S.R. Ambient Air Temperature as a Predictor of Activity of Adult Ixodes Scapularis (Acari: Ixodidae). J. Med. Entomol. 1994, 31, 178–180. [Google Scholar] [CrossRef] [PubMed]
  39. Süss, J.; Klaus, C.; Gerstengarbe, F.; Werner, P.C. What Makes Ticks Tick? Climate Change, Ticks, and Tick-Borne Diseases. J. Travel. Med. 2008, 15, 39–45. [Google Scholar] [CrossRef]
  40. Foster, E.; Burtis, J.; Sidge, J.L.; Tsao, J.I.; Bjork, J.; Liu, G.; Neitzel, D.F.; Lee, X.; Paskewitz, S.; Caporale, D.; et al. Inter-Annual Variation in Prevalence of Borrelia Burgdorferi Sensu Stricto and Anaplasma Phagocytophilum in Host-Seeking Ixodes Scapularis (Acari: Ixodidae) at Long-Term Surveillance Sites in the Upper Midwestern United States: Implications for Public Health Practice. Ticks Tick-Borne Dis. 2022, 13, 101886. [Google Scholar] [CrossRef] [PubMed]
  41. Johnson, T.L.; Graham, C.B.; Maes, S.E.; Hojgaard, A.; Fleshman, A.; Boegler, K.A.; Delory, M.J.; Slater, K.S.; Karpathy, S.E.; Bjork, J.K.; et al. Prevalence and Distribution of Seven Human Pathogens in Host-Seeking Ixodes Scapularis (Acari: Ixodidae) Nymphs in Minnesota, USA. Ticks Tick-Borne Dis. 2018, 9, 1499–1507. [Google Scholar] [CrossRef]
  42. Pepin, K.M.; Eisen, R.J.; Mead, P.S.; Piesman, J.; Fish, D.; Hoen, A.G.; Barbour, A.G.; Hamer, S.; Diuk-Wasser, M.A. Geographic Variation in the Relationship between Human Lyme Disease Incidence and Density of Infected Host-Seeking Ixodes Scapularis Nymphs in the Eastern United States. Am. J. Trop. Med. Hyg. 2012, 86, 1062–1071. [Google Scholar] [CrossRef]
  43. Steere, A.C.; Strle, F.; Wormser, G.P.; Hu, L.T.; Branda, J.A.; Hovius, J.W.R.; Li, X.; Mead, P.S. Lyme Borreliosis. Nat. Rev. Dis. Primers 2016, 2, 16090. [Google Scholar] [CrossRef] [PubMed]
  44. Turtinen, L.W.; Kruger, A.N.; Hacker, M.M. Prevalence of Borrelia Burgdorferi in Adult Female Ticks (Ixodes Scapularis), Wisconsin 2010–2013. J. Vector Ecol. 2015, 40, 195–197. [Google Scholar] [CrossRef]
  45. Stafford, K.C.; Cartter, M.L.; Magnarelli, L.A.; Ertel, S.H.; Mshar, P.A. Temporal Correlations between Tick Abundance and Prevalence of Ticks Infected with Borrelia Burgdorferi and Increasing Incidence of Lyme Disease. J. Clin. Microbiol. 1998, 36, 1240–1244. [Google Scholar] [CrossRef]
  46. Burtis, J.C.; Bjork, J.; Johnson, T.L.; Schiffman, E.; Neitzel, D.; Eisen, R.J. Seasonal Activity Patterns of Host-Seeking Ixodes Scapularis (Acari: Ixodidae) in Minnesota, 2015–2017. J. Med. Entomol. 2023, 60, 769–777. [Google Scholar] [CrossRef] [PubMed]
  47. Zajkowska, J. Antibody-Based Techniques for Detection of Lyme Disease: A Challenging Issue. Antib. Technol. J. 2014, 4, 33–44. [Google Scholar] [CrossRef]
  48. Environmental Public Health Data Tracker. Available online: https://dhsgis.wi.gov/DHS/EPHTracker/#/all/Lyme%20Disease/lymeIndex/NOTRACT/Cases/lymeCtyIndex1 (accessed on 15 April 2024).
  49. Masters, E.J.; Olson, G.S.; Weiner, S.J.; Paddock, C.D. Rocky Mountain Spotted Fever: A Clinician’s Dilemma. Arch. Intern. Med. 2003, 163, 769. [Google Scholar] [CrossRef]
  50. André, M.R. Diversity of Anaplasma and Ehrlichia/Neoehrlichia Agents in Terrestrial Wild Carnivores Worldwide: Implications for Human and Domestic Animal Health and Wildlife Conservation. Front. Vet. Sci. 2018, 5, 293. [Google Scholar] [CrossRef]
  51. Bouza-Mora, L.; Dolz, G.; Solórzano-Morales, A.; Romero-Zuñiga, J.J.; Salazar-Sánchez, L.; Labruna, M.B.; Aguiar, D.M. Novel Genotype of Ehrlichia Canis Detected in Samples of Human Blood Bank Donors in Costa Rica. Ticks Tick-Borne Dis. 2017, 8, 36–40. [Google Scholar] [CrossRef] [PubMed]
  52. Pritt, B.S.; Sloan, L.M.; Johnson, D.K.H.; Munderloh, U.G.; Paskewitz, S.M.; McElroy, K.M.; McFadden, J.D.; Binnicker, M.J.; Neitzel, D.F.; Liu, G.; et al. Emergence of a New Pathogenic Ehrlichia Species, Wisconsin and Minnesota, 2009. N. Engl. J. Med. 2011, 365, 422–429. [Google Scholar] [CrossRef]
  53. Skinner, D.; Mitcham, J.R.; Starkey, L.A.; Noden, B.H.; Fairbanks, W.S.; Little, S.E. Prevalence of Babesia spp., Ehrlichia spp., and tick infestations in Oklahoma black bears (Ursus americanus). J. Wildl. Dis. 2017, 53, 781–787. [Google Scholar] [CrossRef]
  54. Michalski, M.; Rosenfield, C.; Erickson, M.; Selle, R.; Bates, K.; Essar, D.; Massung, R. Anaplasma Phagocytophilum in Central and Western Wisconsin: A Molecular Survey. Parasitol. Res. 2006, 99, 694–699. [Google Scholar] [CrossRef] [PubMed]
  55. Schultz, S.M.; Nicholson, W.L.; Comer, J.A.; Childs, J.E.; Humphreys, J.G. Serologic evidence of infection with granulocytic ehrlichiae in black bears in Pennsylvania. J. Wildl. Dis. 2002, 38, 47–53. [Google Scholar] [CrossRef]
  56. Westmoreland, L.S.H.; Stoskopf, M.K.; Maggi, R.G. Prevalence of Anaplasma Phagocytophilum in North Carolina Eastern Black Bears (Ursus americanus). J. Wildl. Dis. 2016, 52, 968–970. [Google Scholar] [CrossRef] [PubMed]
  57. Stein, E.; Elbadawi, L.I.; Kazmierczak, J.; Davis, J.P. Babesiosis Surveillance—Wisconsin, 2001–2015. MMWR Morb. Mortal. Wkly. Rep. 2017, 66, 687–691. [Google Scholar] [CrossRef]
  58. Westmoreland, L.S.H.; Stoskopf, M.K.; Sheppard, E.; DePerno, C.S.; Gould, N.P.; Olfenbuttel, C.; Maggi, R.G. Detection and Prevalence of Babesia Spp. in American Black Bears (Ursus Americanus) from Eastern and Western North Carolina, USA. J. Wildl. Dis. 2019, 55, 678. [Google Scholar] [CrossRef] [PubMed]
  59. Neiland, K.A.; Miller, L.G. Experimental Brucella suis type 4 infections in domestic and wild Alaskan carnivores. J. Wildl. Dis. 1981, 17, 183–189. [Google Scholar] [CrossRef]
  60. Zarnke, R.L.; Ver Hoef, J.M.; DeLong, R.A. Geographic pattern of serum antibody prevalence for Brucella spp. in caribou, grizzly bears, and wolves from Alaska, 1975–1998. J. Wildl. Dis. 2006, 42, 570–577. [Google Scholar] [CrossRef]
  61. O’Hara, T.M.; Holcomb, D.; Elzer, P.; Estepp, J.; Perry, Q.; Hagius, S.; Kirk, C. Brucella species survey in polar bears (Ursus maritimus) of northern Alaska. J. Wildl. Dis. 2010, 46, 687–694. [Google Scholar] [CrossRef]
  62. Brower, A.; Okwumabua, O.; Massengill, C.; Muenks, Q.; Vanderloo, P.; Duster, M.; Homb, K.; Kurth, K. Investigation of the Spread of Brucella Canis via the U.S. Interstate Dog Trade. Int. J. Infect. Dis. 2007, 11, 454–458. [Google Scholar] [CrossRef]
  63. Kosoy, M.; Goodrich, I. Comparative Ecology of Bartonella and Brucella Infections in Wild Carnivores. Front. Vet. Sci. 2019, 5, 322. [Google Scholar] [CrossRef] [PubMed]
  64. Garshelis, D.L.; Noyce, K.V.; Ditmer, M.A.; Coy, P.L.; Tri, A.N.; Laske, T.G.; Iaizzo, P.A. Remarkable Adaptations of the American Black Bear Help Explain Why It Is the Most Common Bear: A Long-Term Study from the Center of Its Range. In Bears of the World; Penteriani, V., Melletti, M., Eds.; Cambridge University Press: Cambridge, UK, 2020; pp. 53–62. ISBN 978-1-108-69257-1. [Google Scholar]
  65. Iaizzo, P.A.; Laske, T.G.; Harlow, H.J.; McCLAY, C.B.; Garshelis, D.L. Wound Healing during Hibernation by Black Bears (Ursus Americanus) in the Wild: Elicitation of Reduced Scar Formation. Integr. Zool. 2012, 7, 48–60. [Google Scholar] [CrossRef] [PubMed]
  66. Borka-Vitális, L.; Domokos, C.; Földvári, G.; Majoros, G. Endoparasites of Brown Bears in Eastern Transylvania, Romania. Ursus 2017, 28, 20–30. [Google Scholar] [CrossRef]
Diversity 16 00537 g001
Figure 1. (A) Males and female black bears captured per year and per month (all years combined for each month). Black bars represent male black bears while open bars represent female black bears. (B) Presence/absence of ticks on black bears per year and per month. Black bars represent ticks present while open bars represent an absence of ticks. (C) Test results for Lyme disease per year and per month. Black bars represent a positive test, while open bars represent a negative test. (D) Test results for all other tick-borne diseases tested per year and per month. Black bars represent a positive test, while open bars represent a negative test. (E) Presence/absence of B. transfuga in black bear feces per year and per month. Black bars represent B. transfuga present, while open bars represent an absence of B. transfuga.
Figure 1. (A) Males and female black bears captured per year and per month (all years combined for each month). Black bars represent male black bears while open bars represent female black bears. (B) Presence/absence of ticks on black bears per year and per month. Black bars represent ticks present while open bars represent an absence of ticks. (C) Test results for Lyme disease per year and per month. Black bars represent a positive test, while open bars represent a negative test. (D) Test results for all other tick-borne diseases tested per year and per month. Black bars represent a positive test, while open bars represent a negative test. (E) Presence/absence of B. transfuga in black bear feces per year and per month. Black bars represent B. transfuga present, while open bars represent an absence of B. transfuga.
Diversity 16 00537 g001
Table 1. The number of black bears sampled and found to have one or more ticks when examined. The total number of bears tested can be obtained by adding the number of male and female bears tested.
Table 1. The number of black bears sampled and found to have one or more ticks when examined. The total number of bears tested can be obtained by adding the number of male and female bears tested.
MonthNo. of Male BearsNo. of Female BearsNo. of Bears with at Least One D. variabilis Tick PresentNo. of Bears with Only One or More R. sanguineus Ticks PresentNo. of Bears with at Least One Each of D. variabilis and R. sanguineus Tick Present
February2935000
March711000
May63900
June44317302
October64000
November12000
Year
200319122500
200427272400
200537363302
20061011000
Total93868202
Table 2. The number of black bears testing positively or negatively for antibodies for Lyme and other tick-borne diseases. “NT” indicates when bears were not tested for antibodies for the pathogen.
Table 2. The number of black bears testing positively or negatively for antibodies for Lyme and other tick-borne diseases. “NT” indicates when bears were not tested for antibodies for the pathogen.
B. burgdorferiEhrlichia spp.A. phagocytophilumE. canisB. canisR. rickettsiiBabesia spp.
MonthTotal No. of Bears TestedNo. of Bears Testing PositiveTotal No. of Bears TestedNo. of Bears Testing PositiveTotal No. of Bears TestedNo. of Bears Testing PositiveTotal No. of Bears TestedNo. of Bears Testing PositiveTotal No. of Bears TestedNo. of Bears Testing PositiveTotal No. of Bears TestedNo. of Bears Testing PositiveTotal No. of Bears TestedNo. of Bears Testing Positive
Feb.210210NTNTNTNTNTNT210210
March4040NTNTNTNTNTNT4040
May8080NTNTNTNTNTNT8080
June746400341341340743400
Oct.54NTNT50535050NTNT
Year
2003240240NTNTNTNTNTNT240240
2004340340NTNTNTNTNTNT340340
20055410150391394390543150
Total112107303913943901123730
Table 3. The number of black bears testing positively for the intestinal parasite B. transfuga.
Table 3. The number of black bears testing positively for the intestinal parasite B. transfuga.
MonthTotal Number of Bears TestedNo. of Bears with B. transfuga Present
February458
March102
May90
June757
October50
November20
Year
2003313
2004485
2005483
2006196
Total14617
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Reichert, N.S.; Mathieu, D.; Katz, C.J.; Hatch, K.A. Exposure of American Black Bears (Ursus americanus) to Ticks, Tick-Borne Diseases, and Intestinal Parasites in Wisconsin. Diversity 2024, 16, 537. https://doi.org/10.3390/d16090537

AMA Style

Reichert NS, Mathieu D, Katz CJ, Hatch KA. Exposure of American Black Bears (Ursus americanus) to Ticks, Tick-Borne Diseases, and Intestinal Parasites in Wisconsin. Diversity. 2024; 16(9):537. https://doi.org/10.3390/d16090537

Chicago/Turabian Style

Reichert, Nika S., Daniela Mathieu, Christopher J. Katz, and Kent A. Hatch. 2024. "Exposure of American Black Bears (Ursus americanus) to Ticks, Tick-Borne Diseases, and Intestinal Parasites in Wisconsin" Diversity 16, no. 9: 537. https://doi.org/10.3390/d16090537

APA Style

Reichert, N. S., Mathieu, D., Katz, C. J., & Hatch, K. A. (2024). Exposure of American Black Bears (Ursus americanus) to Ticks, Tick-Borne Diseases, and Intestinal Parasites in Wisconsin. Diversity, 16(9), 537. https://doi.org/10.3390/d16090537

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop