key: cord-0857955-wzls78wi authors: Pilfold, Nicholas W.; Richardson, Evan S.; Ellis, John; Jenkins, Emily; Scandrett, W. Brad; Hernández‐Ortiz, Adrián; Buhler, Kayla; McGeachy, David; Al‐Adhami, Batol; Konecsni, Kelly; Lobanov, Vladislav A.; Owen, Megan A.; Rideout, Bruce; Lunn, Nicholas J. title: Long‐term increases in pathogen seroprevalence in polar bears (Ursus maritimus) influenced by climate change date: 2021-07-22 journal: Glob Chang Biol DOI: 10.1111/gcb.15537 sha: 03fd0fbc85a7b76118f939196fcbc37ca00eeb81 doc_id: 857955 cord_uid: wzls78wi The influence of climate change on wildlife disease dynamics is a burgeoning conservation and human health issue, but few long‐term studies empirically link climate to pathogen prevalence. Polar bears (Ursus maritimus) are vulnerable to the negative impacts of sea ice loss as a result of accelerated Arctic warming. While studies have associated changes in polar bear body condition, reproductive output, survival, and abundance to reductions in sea ice, no long‐term studies have documented the impact of climate change on pathogen exposure. We examined 425 serum samples from 381 adult polar bears, collected in western Hudson Bay (WH), Canada, for antibodies to selected pathogens across three time periods: 1986–1989 (n = 157), 1995–1998 (n = 159) and 2015–2017 (n = 109). We ran serological assays for antibodies to seven pathogens: Toxoplasma gondii, Neospora caninum, Trichinella spp., Francisella tularensis, Bordetella bronchiseptica, canine morbillivirus (CDV) and canine parvovirus (CPV). Seroprevalence of zoonotic parasites (T. gondii, Trichinella spp.) and bacterial pathogens (F. tularensis, B. bronchiseptica) increased significantly between 1986–1989 and 1995–1998, ranging from +6.2% to +20.8%, with T. gondii continuing to increase into 2015–2017 (+25.8% overall). Seroprevalence of viral pathogens (CDV, CPV) and N. caninum did not change with time. Toxoplasma gondii seroprevalence was higher following wetter summers, while seroprevalences of Trichinella spp. and B. bronchiseptica were positively correlated with hotter summers. Seroprevalence of antibodies to F. tularensis increased following years polar bears spent more days on land, and polar bears previously captured in human settlements were more likely to be seropositive for Trichinella spp. As the Arctic has warmed due to climate change, zoonotic pathogen exposure in WH polar bears has increased, driven by numerous altered ecosystem pathways. Pathogens can impact the health of wildlife in a range of ways, from sublethal effects to eruptive disease outbreaks causing significant population declines (Alexander & Appel, 1994; Sasan et al., 2019; Rijks et al., 2005) . Concomitant exposure and multi-pathogen infections can also alter host response, potentially compounding the burden on the immune system (Cox, 2001; Pedersen & Fenton, 2007) . Therefore, factors that influence pathogen persistence are important considerations for conservation management. This is imperative with respect to zoonotic pathogens, which can cause significant health challenges in humans (Shereen et al., 2020) , with cascading impacts on the conservation of wildlife (Hockings et al., 2020; Lindsey et al., 2020) . Climate change is expected to amplify some pathogens in wildlife, with warming temperatures and changing precipitation regimes potentially causing an increase in pathogen persistence, prevalence, emergence, and transmission (Altizer et al., 2013) . However, hostpathogen ecology, including density-dependent processes and vectors, needs careful examination for the role of climate (Harvell et al., 2009; McDonald et al., 2016; Ogden & Lindsay, 2016) . Despite the recent rise in climate-disease interaction studies (Altizer et al., 2013) , and the formation of a crisis discipline ('Conservation Medicine'; Aguirre et al., 2002) , there remains a paucity of long-term empirical studies associating the prevalence of wildlife disease with climatic factors. Because not all pathogens respond to changes in climate in the same way (Karvonen et al., 2010; Lafferty, 2009; Menge et al., 2016) , further empirical study is necessary to improve forecasting models. The Arctic is an important ecosystem for monitoring climatedisease interactions because it is warming twice as fast as the rest of the planet (Cohen et al., 2014) , is relatively simple with low species diversity (Post et al., 2013) and many northern people depend on the traditional harvest of wildlife which can lead to zoonotic exposure risk (McDonald et al., 1990; Møller et al., 2010) . Recent Arctic studies have shown linkages between climate change and the life cycles of endoparasites (Hoar et al., 2012; Kutz et al., 2005) , ectoparasites (Descamps, 2013; Larsson et al., 2007) and biting insects (Culler et al., 2015) . Although there has been a long history of investigations into disease prevalence in Arctic wildlife (Connell, 1949; Elton, 1931) , the majority have been cross-sectional rather than longitudinal (Carlsson et al., 2019; Clausen & Hjort, 1986; Dick & Belosevic, 1978; Elmore et al., 2016) . While calls have been made for Arctic climate-disease interaction studies (Bradley et al., 2005; Burek et al., 2008) , logistical challenges have been a major barrier to long-term, repeat sample collection. Polar bears (Ursus maritimus) are a widely dispersed apex carnivore, with a species range covering the circumpolar Arctic and extending across more than 35 degrees of latitude (PBSG, 2018) . Given their range and trophic position, polar bears may be a sentinel species for changing disease dynamics in the Arctic (Stirling & Derocher, 2012) . Jensen et al. (2010) reported an increase in the seroprevalence of Toxoplasma gondii in polar bears from Svalbard, Norway from 24.3% in the 1990s (Oksanen et al., 2009 ), to 47.6% in 2006 . Jensen et al. (2010 speculated that the increase was linked to enhanced survival of oocysts in warmer water from the North Atlantic Current. Atwood et al. (2017) documented an increase in the seroprevalence of T. gondii and Coxiella burnetii in polar bears from the southern Beaufort Sea, 2007 Sea, -2014 . Polar bears that spent summer and fall on land were found to be seven times more likely to be seropositive for T. gondii than those that stayed on the sea ice (Atwood et al., 2017) , and to have a heightened immune system response (Whiteman et al., 2019) . As increased use of land was related to sea ice loss as a consequence of climate change (Atwood, Peacock, et al., 2016; Gleason & Rode, 2009 ), Atwood et al. (2017) was the first polar bear study to link an ecosystem pathway for increased pathogen prevalence to climate change. Polar bears in western Hudson Bay (WH), Canada migrate to and from land annually, following the melt and refreeze patterns F I G U R E 1 Study area of western Hudson Bay, Canada. Hudson Bay has undergone significant changes in sea ice cover, summer air temperatures and precipitation regimes, 1986-2017. The thick dashed black line is the mean on-ice home range of polar bears based on adult female movement (McCall et al., 2014) , with July mean sea ice concentrations during study periods overlaid from oldest to newest. The hatched polygon represents the approximate terrestrial range of polar bears during ice-free months of sea ice in the Bay (Derocher & Stirling, 1990a) . Between 1979 and 2014, the number of ice-free days in WH increased 8.6 days/ decade (Stern & Laidre, 2016) , altering polar bear migratory phenology (Castro de la Guardia et al., 2017; Cherry et al., 2013) . While on land, polar bears forage opportunistically on a variety of terrestrial foods (Derocher et al., 1993; Russell, 1975) , but lose approximately 1 kg of mass per day (Pilfold et al., 2016) . As a result, longer ice-free seasons in Hudson Bay are correlated with decreases in body condition, reproductive output and survival of polar bears (Derocher & Stirling, 1995; Lunn et al., 2016; Regehr et al., 2007; Sciullo et al., 2016) . Additionally, increased time on land is positively correlated with human-polar bear interactions in communities (Towns et al., 2009 ). However, the consequences of climate change and longer icefree seasons on pathogen exposure in WH polar bears are unknown. The objectives of this study were to examine whether the seroprevalence of seven pathogens in WH polar bears has changed over a 32-year period (1986-2017) , and assess any temporal trends in seropositivity against biotic and abiotic variables for potential influential drivers of changes in pathogen exposure. It has been shown that sex and age can influence seroprevalence to some pathogens in polar bears (Jensen et al., 2010; Oksanen et al., 2009; Rah et al., 2005) . Additionally, while sea ice has been the primary focus for climate interaction studies in polar bears (Stirling & Derocher, 2012) , the Hudson Bay ecosystem is also undergoing changes in air temperature and precipitation regimes (Macrae et al., 2014; Figure 1 ). We aimed to infer which factors are most influential to changing pathogen exposure in polar bears through a serological analysis from the longest continuously studied polar bear population in the world. Hudson Bay is a shallow inland sea (Jones & Anderson, 1994) , with a seasonal sea ice regime that influences the climate dynamics of the ecosystem (Rouse, 1998) . Between 1986 and 2017, annual mean (±SE) air temperature as recorded at Churchill Airport, Manitoba (Churchill A, Station ID 5060600, 58°44'24.0"N, 94°04'12.0"W, Environment Canada, 2020) was -6.30 ± 0.07°C, with a mean air temperature of 9.90 ± 0.06°C in summer (June-September) and -22.7 ± 0.1°C in winter (December-March). Mean annual precipitation between 1986 and 2017 was 412.2 ± 3.1 mm. The proportion of precipitation falling during summer increased over the study period, along with air temperature (Figure 1 ). During the winter, Hudson Bay is ice-covered. WH polar bears occupy and travel over much of the Bay, with mean annual home ranges for adult females of approximately 230,000-380,000 km 2 (McCall et al., 2014; Figure 1 ). Sea ice break-up begins in May and the Bay is ice-free by August, forcing WH bears to spend the summer and fall onshore. WH polar bears congregate during the ice-free months along the western coastline of Hudson Bay in the lowlands (Derocher & Stirling, 1990a; Stirling et al., 2004) , which are dominated by poorly drained peat bog plateaus and channel fens, with a mixture of open-canopy spruce-lichen woodlands (Macrae et al., 2014) . During the ice-free period, WH polar bears can also be found near human settlements, in particular Churchill, MB, which employs the Polar Bear Alert Program to minimize human-polar bear conflict by intercepting bears that come close to town (Kearney, 1989; Towns et al., 2009 ). Samples were collected in 1986 Samples were collected in -1989 Samples were collected in , 1995 Samples were collected in -1998 Samples were collected in and 2015 Samples were collected in -2017 as part of ongoing, long-term studies of WH polar bears . Bears were located by helicopter and chemically immobilized via remote injection following standard protocols (Stirling et al., 1989) . A vestigial premolar was extracted for age estimation (Calvert & Ramsay, 1988 ) from previously unmarked bears older than 1 year. Blood was drawn from a femoral vein using a 30 or 60 ml syringe within half an hour of capture, immediately transferred into red/grey SST tubes and kept in a cooler until it was spun in a centrifuge to separate the serum at the end of each day. All capture and handling methods were reviewed and approved annually by the Environment and Climate Change Canada Western and Northern Animal Care Committee. Sera were stored at -70°C until needed. Freezers were monitored with alarm systems to ensure serum samples did not undergo freeze-thaw cycles. While we did not analyse for the possible influence of sample degradation over time, we were confident that storage at -70°C prevented proteolysis and had negligible impact on our ability to detect antibodies (Cecchini et al., 1992; Dard et al., 2017) . We focused the analysis on sera from adult polar bears (≥5 years) and when possible, balanced samples between males and females, within and over years (Table 1) . Negative control sera were obtained in 2019 from two adult male polar bears (aged 5 and 7 years) born and raised in captivity at the Toronto Zoo. We ran serological assays to detect exposure to seven pathogens (Table 2) : T. gondii, Neospora caninum, Trichinella spp., Francisella tularensis, Bordetella bronchiseptica, canine morbillivirus (CDV) and canine parvovirus (CPV). We selected these pathogens in order to have representation from parasitic, bacterial and viral diseases. We selected pathogens well-documented in polar bears for comparison of seroprevalence across their range (T. gondii, Trichinella spp., CDV), pathogens with minimal documentation for follow-up (N. caninum, F. tularensis) and pathogens that have not been surveyed before (B. bronchiseptica, CPV) to provide a baseline for future monitoring. IgG antibodies against T. gondii were detected using a commercial indirect-ELISA (iELISA) kit (ID Screen ® Toxoplasmosis Indirect Multi-species, IDvet Innovative Diagnostics) that has shown high specificity for T. gondii and non-cross reactivity with N. caninum (ID Vet, 2020) . In addition to kit controls and negative controls from captive polar bears, serum samples previously collected from wolverines and known to be positive and/or negative by molecular methods (Sharma et al., 2019) were used as internal controls. Results were obtained as sample/positive percentage (S/P%), calculated using the optical density (OD) of the positive and negative kit controls, and the OD of test samples using the following formula: S/P% = [(OD sample -OD negative control)/(OD positive control -OD negative control)] ×100. S/P% values of ≥50 were considered positive. Serum samples were tested for the presence of antibodies to N. caninum using a commercially available competitive-ELISA (cELISA) kit (Neospora Caninum Antibody Test Kit cELISA, Veterinary Medical Research & Development), in which both the antigen and monoclonal antibody conjugate have shown high specificity to N. caninum and non-cross reactivity with T. gondii or Sarcocystis spp. (Baszler et al., 1996 MaxiSorp 96-well plates (Thermo Fisher Scientific) coated overnight at 2°C-8°C with excretory-secretory (E-S) antigen of T. spiralis first-stage larvae diluted in carbonate/bicarbonate buffer (pH 9.6). Washing of ELISA plates was performed with Tris-buffered saline containing 0.05% Tween-20 (TBST). After coating with antigen, the plates were washed, then blocked for 2 h at room temperature with 2% bovine serum albumin (BSA; Sigma-Aldrich) in Tris-buffered saline. All polar bear sera used in this study were initially tested by cELISA using plates coated with 50 ng/well of the E-S antigen. Immune serum from a pig experimentally infected with T. spiralis served as a positive repeatability control. A microagglutination assay (MAT) was used to detect IgM and IgG antibodies for F. tularensis (Sato et al., 1990) . Serum samples from Arctic foxes (Vulpes lagopus) that were previously tested with a MAT were used as positive and negative controls. A high positive control (1:1024), low positive control (1:128) and negative control were used for each run. Titres ≥1:128 were considered positive. An ELISA for B. bronchiseptica-reactive IgG antibodies was performed as previously described using anti-canine IgG as the conjugate (Ellis et al., , 2021 . A previously determined cut-off value of 15 OD units, which was based on the testing of positive and negative dog sera, was used as an indicator of biologically significant antibody response after exposure to B. bronchiseptica antigens (Ellis et al., , 2021 Serum antibodies reactive with CDV were detected in an immunoperoxidase plaque staining assay that was conducted according to previously described methods (Soma et al., 2001) , with minor modi- Seroprevalence of each pathogen between 1986-1989 (n = 157), 1995-1998 (n = 159) , and 2015-2017 (n = 109), and co-occurrence between pathogens, were compared using a Pearson chi-square. Polar bears were sampled a maximum of once per year, but some individuals were sampled multiple times within a time period (1986-1989, 1995-1998, 2015-2017 To examine which factors were influential to changes in pathogen exposure in polar bears, we considered potentially influential sets of biological and climatic variables on an annual time scale (Tables 3 and 4 ). Biological variables included age, sex, weight, body condition and conflict history of the bear. Briefly, the variable 'Age' was estimated from the cementum layers of an extracted vestigial premolar (Calvert & Ramsay, 1988) , while 'Sex' was determined in the field. Polar bears were given a subjective fatness rating of 1-5 at the time of capture ; bears rated 1-2 were considered in 'Poor' condition, bears rated 3 were 'Average' and bears rated 4-5 were considered in 'Good' condition. Prior to modelling, TA B L E 3 Covariates used to model the likelihood of pathogen seropositivity in adult polar bears of Western Hudson Bay, Canada, 1986 Canada, -2017 Name Age 5-31 Age of polar bear via tooth histology (Calvert & Ramsay, 1988) Sex 1/0 Field determination with females as reference category (0) Poor a 1/0 Polar bears rated 1 or 2 on five-point body condition index Good a 1/0 Polar bears rated 4 or 5 on five-point body condition index Canada, 2020) . All WH polar bears migrate to land during the icefree period, and migration phenology correlates with thresholds of sea ice concentration (Cherry et al., 2013; Stirling et al., 1999) . The variable 'IceFree' was the number of days in a year of less than 15% sea ice concentration as determined by SSM/I with a spatial grain of 25 km 2 (Cavalieri et al., 1996) , within the on-ice home range of WH polar bears (McCall et al., 2014) . We used a threshold of 15% sea ice concentration as it aligns with the climatic definition of 'ice-free' (Parkinson et al., 1999) , and is a conservative measure of the total number of days polar bears likely spent on land. Lastly, all climatic measurements were taken from the year prior to the year of the serum sample. Temporal lags were tested out to 3 years from year of sample, and a 1-year lag resulted in the best fit (Table S1) . We related the seroprevalence (1/0) of pathogens that showed significant change over time to variables using binomial (logit link) generalized linear mixed models, and the same constrained set of a priori models for each pathogen, balanced for equal representation of all variables (Tables S2 and S3) . We included Bear ID as a random effect to control for repeat samples from the same individuals. Prior to modelling, we mean-centred continuous covariates about zero, and examined Pearson correlation coefficients for any pairs of factors that had a coefficient >0.7. To assess the relative influence of biological and climatic factors, we used Akaike's information criterion for small samples (AIC C ; Burnham & Anderson, 2002) . We evaluated sets of biological and climatic factors separately, and identified top factors for each as having an AIC C w i ≥ 0.60. To assess the comparative strength of biological and climatic factors on their influence on disease exposure, we combined top biological and climatic factors into one model, and used log-likelihood ratio tests and conditional-R 2 (Nakagawa & Schielzeth, 2013) Sex was a top factor in the seroprevalence of both Trichinella spp. (AIC C w i = 0.83) and B. bronchiseptica (AIC C w i = 1.00 (Table 7) . Mean summer temperature was a top factor in the seropreva- (Table 7) . Climate change is expected to increase the severity and scope of outbreaks of some diseases in wildlife, as warmer and wetter con- suggesting that terrestrial exposure may be an important factor in T. gondii seroprevalence (Atwood et al. 2017 Bay watershed (Labelle et al., 2001; . However, while Canada lynx range includes the Hudson Bay lowlands (Vashon, 2016) , the current status of lynx in the WH study area is unknown. Observations by trappers have been rare (L. Fishback, personal communication, August 11, 2020), and lynx are the only endemic carnivore not detected by trail cameras that have been operating along the coast of Wapusk National Park since 2011 (D. Clark, personal communication, August 11, 2020; Clark et al., 2019) . Like other Arctic carnivores, polar bears may also be exposed to T. gondii through the consumption of tissue cysts in intermediate host species, and precipitation may modulate exposure. On the sea ice, ringed seals (Pusa hispida) are the primary prey for WH polar bears , and ringed seals in Canada have been documented with T. gondii seroprevalences ranging from 10% to 26% Reiling et al., 2019; Simon et al., 2011) . Surface run-off contaminated with T. gondii oocysts into coastal marine environments is a suspected source of infection for marine mammals in the Arctic . Higher precipitation during the summer months coincides with the hyperphagic feeding period for ringed seals (Young & Ferguson, 2013) , which may increase exposure to T. gondii oocysts lodged in the alimentary canal of filter feeding fish (Massie et al., 2010) . Alternatively, T. gondii exposure for polar bears could involve the consumption of terrestrial intermediate hosts such as Arctic fox (V. lagopus; Prestrud et al., 2007) or Arctic-nesting migratory lesser snow geese (Chen caerulescens; Bachand et al., 2019; Elmore et al., 2015) . While observations of Arctic fox consumption are very rare in Hudson Bay (but see Richardson & Brook, 2004) , snow geese are preyed upon in the summer months by some polar bears in WH (Gormezano & Rockwell, 2013) . In years with higher summer precipitation, plant growth is enhanced and nesting survival of snow geese improves (Lecomte et al., 2009) , which may bolster goose populations and encounter rates for polar bears. Neospora caninum is a tissue-dwelling coccidian parasite closely related to T. gondii, but neosporosis has only been recognized for about 30 years (Dubey et al., 2007) . Atwood et al. (2017) was the first to report N. caninum antibodies in polar bears, recorded in 3.7% for terrestrial mammalian transmission of T. gondii (Dubey, 2010) , to our knowledge has not been demonstrated for N. caninum. If this was a potential route of exposure for bears, caribou (Rangifer tarandus) and ringed seals may contribute to exposure. Caribou were found in 10% of WH polar bear scats collected on land (Gormezano & Rockwell, 2013) , and ringed seals are the main prey on the sea ice. Neospora caninum-like DNA was reported in the tissue of 26% ringed seals in eastern Hudson Bay (Reiling et al., 2019) , while more than 80% of the Quaminuriaq caribou herd of Hudson Bay were reported as N. caninum seropositive (Carlsson et al., 2019) . However, if feeding on intermediate hosts exposed polar bears to N. caninum, we would expect a seroprevalence comparable to T. gondii. The N. caninum seroprevalence we observed aligns with the generally lower oocyst shedding pattern observed in canids (Dubey & Schares, 2011) , and likely reflects the overall level circulating in the Hudson Bay ecosystem. Trichinella spp. have a long history of documentation in polar bears, and previous studies found prevalences comparable to our study (Asbakk et al., 2010; Larsen & Kjos-Hanssen, 1983; Naidenko et al., 2013; Rah et al., 2005) . Our results are consistent with previous findings that Trichinella spp. seroprevalence increases with age in polar bears, although we did not find uniformity between sexes (Asbakk et al., 2010; Rah et al., 2005) ; rather, males had higher seroprevalence than females. Due to the low Trichinella spp. prevalence in arctic marine mammals (Jenkins et al., 2013) , transmission to polar bears likely relies on hunting or scavenging terrestrial carnivores (Richardson & Brook, 2004) or cannibalism (Forbes, 2000; Larsen & Kjos-Hanssen, 1983) . The finding that older males are more likely to be seropositive supports cannibalism as a mode of transmission, as cannibalism is more frequently observed in adult males (Taylor et al., 1985) . Dietary studies from scat remains also suggest that WH polar bears more frequently cannibalize their own than consume other terrestrial carnivores (Derocher et al., 1993; Gormezano & Rockwell, 2013; Russell, 1975) . Trichinella spp. seroprevalence in WH polar bears was positively correlated to both warmer summer and winter temperatures across all time periods, but was not correlated to annual temperatures, suggesting a season-specific response. Although serology cannot differentiate amongst Trichinella spp., it is most probable that the species in this study are Trichinella nativa and/or Trichinella-T6, which are freeze-tolerant and the most common sylvatic taxa found in wildlife in Canada (Gajadhar & Forbes, 2010) . Mean annual minimum winter temperatures during our study ranged between -30.0°C and -24.9°C. Environmental exposure to temperatures below -20°C is suggested to reduce the survival of T. nativa and Trichinella-T6 larvae in muscle tissue, with optimal long-term survival in the range of 0°C to -20°C (Pozio, 2016) . It is therefore possible that under reduced extreme winter cold as seen in our study, the survival of Trichinella spp. increased. Furthermore, carcasses freeze more quickly in extreme cold, likely reducing the consumption of muscle tissue by scavengers. Stirling and Øritsland (1995) observed that in -25°C weather, polar bears will generally abandon a seal carcass after the fat is stripped. Under reduced extreme cold in winter, Trichinella parasites may survive longer in the muscle tissue of infected carcasses, and carcasses may remain available for consumption longer, potentially infecting a greater number of bears. Arctic research has focused on the cold tolerance of Trichinella spp. as a limit to their range (Masuoka et al., 2009; Pozio, 2016) , but there has been little research on the effect of summer temperature. Warmer summer air temperatures in Hudson Bay likely increase the probability of heat stress for polar bears (Øritsland et al., 1974) that are near the southern end of their range. Heat stress in endotherms alters the endocrine system, increasing corticoids and depressing the inflammatory response (Morley & Lewis, 2014) , which may compromise immunity to parasite invasion. Although long-term survival of cold-tolerant T. nativa and Trichinella-T6 may decrease with warming, host immune response may also subsequently diminish when exposed to warming beyond their thermal tolerance. We suggest future studies of Trichinella spp. in wildlife include a measure of thermal stress to establish its potential role in pathogen transmission. Both of the bacterial pathogens we surveyed, F. tularensis and B. bronchiseptica, increased in seroprevalence between 1986-1989 and 1995-1998 . Little research has been conducted for either of these pathogens in polar bears. Atwood et al. (2017) reported low seroprevalences of F. tularensis in Southern Beaufort Sea polar bears, with less than 5% of bears sampled having antibodies. In our study, prevalence was 8-12 times higher, with more than 60% of polar bears seropositive in 2015-2017. The terrestrial life cycle of F. tularensis involves transmission by biting insects such as ticks, mosquitoes and flies (Feldman, 2003) , lagomorph and rodent reservoirs such as muskrats (Ondatra zibethicus; Martin et al., 1982) and/ or through water-borne transmission in wetland areas (Eliasson et al., 2006) . All WH polar bears spend at least 3-4 months on land annually, whereas only 20% of Beaufort Sea polar bears come to shore, and stay on average for 2 months (Atwood, Marcot, et al., 2016) . Beaufort Sea polar bears may partly explain the large regional difference in F. tularensis seroprevalence. During summer, WH polar bears are found along the coast of Hudson Bay (Derocher & Stirling, 1990a) , with bears sighted around the town of Churchill on the coastline, and farther inland in Wapusk National Park (Stapleton et al., 2014) . Francisella tularensis seroprevalence was lower for WH polar bears that had been previously captured near the town of Churchill. It is possible that polar bears in closer proximity to the coast find refuge from deer flies and horseflies (Tabanidae), which use peatland habitats for key aspects of their life cycle (McElligott & Lewis, 1996) . However, although polar bears demographically segregate, with males staying along the coast (Derocher & Stirling, 1990b) and adult females using inland areas (Derocher & Stirling, 1990a) , we did not find any significant difference in F. tularensis seroprevalence of males (49%) and females (55%). Increased time on land as a result of more ice-free days in Hudson Bay was positively correlated with F. tularensis seroprevalence. In the Hudson Bay lowlands, mosquitoes (Culicidae) emerge in June and peak in mid-July, whereas horseflies and deer flies begin to emerge in July and peak in early August (Park, 2017; Twinn et al., 1948) . Longer time on land may increase seasonal exposure to biting insects, and polar bears forced onto land earlier may overlap with peak abundances of mosquitoes. Additionally, more time on land likely increases use of terrestrial water bodies, which may expose polar bears to water-borne F. tularensis or facilitate close contact with other reservoir hosts, such as rodents. Francisella tularensis antibodies were also more likely in polar bears in better body condition. As body condition and immune function are positively correlated in polar bears (Whiteman et al., 2019) , we may be detecting increased antibodies to F. tularensis in bears in better condition. Alternatively, these bears could have been more likely to survive exposure without developing clinical disease. As longer ice-free periods are expected to reduce polar bear body condition (Castro de la Guardia et al., 2013) , future declines in sea ice may hinder antibody response against F. tularensis and/or lead to more clinical tularaemia, which can be fatal. Bordetella bronchiseptica is a highly infectious respiratory pathogen well documented in laboratory and domestic animals (Goodnow, 1980) , but little is known about its presence in wildlife. (Appel & Gillespie, 1972; Gordon & Angrick, 1986 ). The steady CDV and CPV seroprevalence over time may reflect the optimal conditions in Hudson Bay for long-term virus survival, creating a stable endemic condition, rather than eruptive outbreaks. There is some evidence from other ecosystems of the influence of climate on the prevalence and virulence of CDV and CPV (Kelman et al., 2020; Munson et al., 2008) ; however, evidence for environmental regulation remains scant, warranting further investigation. The source of CDV and CPV in polar bears remains unclear and both exist as quasispecies, suggesting they could be of ursine origin, or derived from other carnivores, such as canids, wild or domestic. Between 1987 and 2011, the WH polar bear population declined from 1187 individuals to 806 . However, the change was not linear. Rapid decline occurred between the mid-1980s and mid-1990s, when several measures of polar bear health including body condition, reproductive output and survival decreased (Derocher & Stirling, 1995; Regehr et al., 2007) . These indices subsequently stabilized in the mid-2000s . Additionally, Boonstra et al. (2020) found a shift in the stress axis of polar bears between 1983-1990 and 1991-2015. In our study, we found a similar temporal pattern in the change in the seroprevalence of T. gondii, F. tularensis and B. bronchiseptica. We do not have direct evidence for the virulence of these pathogens in polar bears, and therefore cannot associate pathogen exposure with survival. However, some exposure patterns suggest the potential for negative impacts on the population if exposure leads to disease. For example, co-occurrence between T. gondii and N. caninum was higher than expected by chance. Both protozoan parasites can cause spontaneous abortions in some species (Dubey, 2010; Dubey et al., 2007) , suggesting a potential impact on the reproductive output of polar bears. In addition, these parasites can cause clinical neurological disease and more subtle behavioural changes. We suggest that these protozoans have potential roles in the population health of polar bears, and should be included in conservation management considerations (Atwood, Marcot, et al., 2016) . All of the zoonotic pathogens we surveyed increased in seroprevalence between -1989 -1998 -2017 average, each polar bear in our study had antibodies to three of four zoonotic pathogens. We consider polar bears to be sentinel species for all pathogens, and a potential source of human exposure for F. tularensis, Trichinella spp. and T. gondii, all of which have been recorded in communities in northern Canada (MacLean et al., 1989; McDonald et al., 1990; Messier et al., 2012) . In particular, 70% of bears had antibodies to Trichinella spp. in 2015-2017, supporting the risk for human exposure if polar bear meat is consumed raw or undercooked . Adult male polar bears that were previously captured in human settlements were four times more likely to be Trichinella spp. seropositive. All samples were collected during a period when male bears were preferentially targeted in subsistence hunts as part of a 2:1, male-biased harvest management plan (Taylor et al., 2008) . Congruently, male polar bears that enter human settlements in the Arctic are at an increased risk of being harvested (Dyck, 2006) . We note that serology only indicates exposure rather than active infection; however, larvae of Trichinella can survive for years in muscle tissue, and bears are a known source of human exposure to Trichinella (Rostami et al., 2017) . Therefore, we recommend Hudson Bay communities employ precautionary measures to reduce the risk of exposure to zoonotic pathogens when handling and consuming polar bears, including, but not limited to, handling carcasses with gloves and/or washing hands after handling, disinfecting harvesting tools following use, ensuring that meat remains frozen to -20°C or colder for at least 3 days prior to consumption (to inactive cysts of T. gondii) and thoroughly cooking the meat before eating (the only reliable means to inactivate freeze-tolerant Trichinella spp.). The potential for increased exposure to zoonotic pathogens for both people and animals highlights the utility of a One Health approach in the Arctic (Ruscio et al., 2015) , which considers the interconnectedness between people, wildlife and ecosystem change. Globally, the majority of emerging infectious diseases affecting people are zoonotic and are increasing with time (Jones et al., 2008) , mainly as a result of agriculture, forestry, urbanization and other land-use changes (Gibb et al., 2020; Keesing et al., 2010) . In the Arctic, direct anthropogenic land-use change is minimal, while the effects of climate change are accelerated. The increases in seroprevalence of zoonotic pathogens in polar bears were all associated with environmental conditions undergoing climate change in both the terrestrial and marine ecosystems. This suggests that climate change can alter zoonotic pathogen prevalence in the absence of land-use change, especially in depauperate systems. As the pathogens and ecosystem pathways we monitored are common to many species globally, polar bears may once again be a harbinger of the coming impacts of climate change to wildlife health. Financial support for the serological analyses was provided by the The data that support the findings of this study are available from the corresponding author upon reasonable request. Nicholas W. 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