Widespread Exposure to Mosquitoborne California Serogroup Viruses in Caribou, Arctic Fox, Red Fox, and Polar Bears, Canada.

Northern Canada is warming at 3 times the global rate. Thus, changing diversity and distribution of vectors and pathogens is an increasing health concern. California serogroup (CSG) viruses are mosquitoborne arboviruses; wildlife reservoirs in northern ecosystems have not been identified. We detected CSG virus antibodies in 63% (95% CI 58%-67%) of caribou (n = 517), 4% (95% CI 2%-7%) of Arctic foxes (n = 297), 12% (95% CI 6%-21%) of red foxes (n = 77), and 28% (95% CI 24%-33%) of polar bears (n = 377). Sex, age, and summer temperatures were positively associated with polar bear exposure; location, year, and ecotype were associated with caribou exposure. Exposure was highest in boreal caribou and increased from baseline in polar bears after warmer summers. CSG virus exposure of wildlife is linked to climate change in northern Canada and sustained surveillance could be used to measure human health risks.

Association of Environmental Factors with Seasonal Intensity of Erysipelothrix rhusiopathiae Seropositivity among Arctic Caribou.

Several caribou (Rangifer tarandus) populations have been declining concurrently with increases in infectious diseases in the Arctic. Erysipelothrix rhusiopathiae, a zoonotic bacterium, was first described in 2015 as a notable cause of illness and death among several Arctic wildlife species. We investigated epidemiologic and environmental factors associated with the seroprevalence of E. rhusiopathiae in the Arctic and found that seropositivity was highest during warmer months, peaking in September, and was highest among adult males. Summer seroprevalence increases tracked with the oestrid index from the previous year, icing and snowing events, and precipitation from the same year but decreased with growing degree days in the same year. Seroprevalence of E. rhusiopathiae varied more during the later years of the study. Our findings provide key insights into the influence of environmental factors on disease prevalence that can be instrumental for anticipating and mitigating diseases associated with climate change among Arctic wildlife and human populations.

Brucellosis emergence in the Canadian Arctic.

Brucellosis is an important zoonotic disease affecting animals and subsistence harvesters in the circumarctic. We investigated recent trends (2015-2022) of brucellosis seropositivity in caribou (Rangifer tarandus) and muskoxen (Ovibos moschatus) in the Central Canadian Arctic by using data from community-based wildlife health surveillance programs. The overall sample prevalence of Brucella antibodies was 10.0% (n = 271) in muskoxen and 15.5% (n = 277) in caribou. Sample seroprevalence in muskoxen varied geographically with an increasing trend of exposure on NW Victoria Island (from 0% to 36.8% between 2016 and 2022; Kendall tau = 0.283, p = 0.001). The presence of Brucella suis biovar 4 was confirmed by culture from clinical cases in this area. Our results indicate that Brucella suis biovar 4 continues to circulate in the Central Canadian Arctic in caribou and muskoxen and may be now circulating in muskoxen independently from caribou. These findings highlight the need to better understand the ecology and drivers of brucellosis emergence in Arctic multi-host systems.

Detection and Phylogenetic Analysis of Orf Virus and Muskox Rhadinovirus 1 from Muskoxen (Ovibos moschatus) in the Canadian Arctic.

Orf virus (genus Parapoxvirus) has been associated with gross skin lesions on muskoxen (Ovibos moschatus) from Victoria Island, Nunavut, Canada, where muskox populations are experiencing population declines. Orf virus causes painful proliferative and necrotizing dermatitis upon viral replication and shedding, which may lead to animal morbidity or mortality through secondary infections and starvation. Herpesvirus, known to cause gross lesions on skin and mucosa during active viral replication, has also been documented in muskoxen but to date has not been associated with clinical disease. Our objective was to characterize the variation of orf virus and herpesvirus in wild muskoxen of the Canadian Arctic. Tissue samples including gross skin lesions from the nose, lips, and/or legs were opportunistically collected from muskoxen on Victoria Island, Nunavut and Northwest Territories, and mainland Nunavut, Canada, from 2015 to 2017. Sampled muskoxen varied in age, sex, location, hunt type, and body condition. Tissues from 60 muskoxen were tested for genetic evidence of orf virus and herpesvirus infection using PCR targeting key viral genes. Tissues from 38 muskoxen, including 15 with gross lesions, were also examined for histological evidence of orf virus and herpesvirus infection. Eleven muskoxen (10 from Victoria Island and one from mainland Nunavut) with gross lesions had microscopic lesions consistent with orf virus infection. Muskox rhadinovirus 1, a gammaherpesvirus endemic to muskoxen, was detected in 33 (55%) muskoxen including 17 with gross lesions. In all tissues examined, there was no histological evidence of herpesvirus-specific disease. Sequencing and characterization of amplified PCR products using phylogenetic analysis indicated that a strain of orf virus, which appears to be unique, is likely to be endemic in muskoxen from Victoria Island and mainland Nunavut. Many of the muskoxen are also subclinically infected with a known muskox-endemic strain of herpesvirus.

Next-generation sequencing approach to investigate genome variability of Parapoxvirus in Canadian muskoxen (Ovibos moschatus).

In 2016, the first orf virus, a double-stranded DNA (dsDNA) virus of the genus parapoxvirus, from a muskox was isolated on Victoria Island, Nunavut (NU), Canada. We used deep sequencing on DNA extracted from orf virus-positive tissues from wild muskoxen from locations on Victoria Island and the adjacent mainland. Orf virus sequence reads derived from four samples were nearly identical. The consensus sequences generated from pooled reads of MxOV comprises of a large contiguous sequence (contig) of 131,759 bp and a smaller right terminal contig of 3552 bp, containing all coding sequences identified as Parapoxvirus. Individual gene comparisons reveal that MxOV shares genetic characteristics with reference strains from both sheep and goat origin. Recombination analysis using Bootscan, MAXCHI, GENECONV, CHIMAERA, SISCAN, and RDP algorithms within the RDP4 software predicted recombination events in two virulence factors, and a large 3000 bp segment of the MxOV genome. Partial B2L nucleotide sequences from strains around the world and other North American isolates were compared to MxOV using MUSCLE alignments and RAxML phylogenetic trees. MxOV was identical to our previously characterized isolate, and shared similarity with orf virus isolated from sheep and goats. The phylogenetic grouping of partial B2L nucleotide sequences did not follow the sample geographic distribution. More full genomes of orf virus, or at least full B2L gene squences, in wildlife are needed especially in North America to better understand the epidemiology of the disease in muskoxen.

Metabarcoding of fecal pellets in wild muskox populations reveals negative relationships between microbiome and diet alpha diversity.

Microbiome diversity and diet composition concomitantly influence species health, fitness, immunity, and digestion. In environments where diet varies spatially and temporally, microbiome plasticity may promote rapid host adaptation to available resources. For northern ungulates in particular, metabarcoding of noninvasively collected fecal pellets presents unprecedented insights into their diverse ecological requirements and niches by clarifying the interrelationships of microbiomes, key to deriving nutrients, in context of altered forage availability in changing climates. Muskoxen (Ovibos moschatus) are Arctic-adapted species that experience fluctuating qualities and quantities of vegetation. Geography and seasonality have been noted to influence microbiome composition and diversity in muskoxen, yet it is unclear how their microbiomes intersect with diet. Following observations from other species, we hypothesized increasing diet diversity would result in higher microbiome diversity in muskoxen. We assessed diet composition in muskoxen using three common plant metabarcoding markers and explored correlations with microbiome data. Patterns of dietary diversity and composition were not fully concordant among the markers used, yet all reflected the primary consumption of willows and sedges. Individuals with similar diets had more similar microbiomes, yet in contrast to most literature, yielded negative relationships between microbiome and diet alpha diversity. This negative correlation may reflect the unique capacities of muskoxen to survive solely on high-fiber Arctic forage and provide insight into their resiliency to exploit changing dietary resources in a rapidly warming Arctic altering vegetation diversity.

An integrative and multi-indicator approach for wildlife health applied to an endangered caribou herd.

Assessing wildlife health in remote regions requires a multi-faceted approach, which commonly involves convenient samplings and the need of identifying and targeting relevant and informative indicators. We applied a novel wildlife health framework and critically assessed the value of different indicators for understanding the health status and trends of an endangered tundra caribou population. Samples and data from the Dolphin and Union caribou herd were obtained between 2015 and 2021, from community-based surveillance programs and from captured animals. We documented and categorized indicators into health determinants (infectious diseases and trace elements), processes (cortisol, pathology), and health outcomes (pregnancy and body condition). During a recent period of steep population decline, our results indicated a relatively good body condition and pregnancy rates, and decreasing levels of stress, along with a low adult cow survival. We detected multiple factors as potential contributors to the reduced survival, including Brucella suis biovar 4, Erysipelothrix rhusiopathiae and lower hair trace minerals. These results remark the need of targeted studies to improve detection and investigations on caribou mortalities. We also identified differences in health indicators between captured and hunter sampled caribou, highlighting the importance of accounting for sampling biases. This integrative approach that drew on multiple data sources has provided unprecedented knowledge on the health in this herd and highlights the value of documenting individual animal health to understand causes of wildlife declines.

Draft Genome Assembly of an Iconic Arctic Species: Muskox (Ovibos moschatus).

Muskoxen (Ovibos moschatus) are Arctic species within the Caprinae subfamily that are economically and culturally significant to northern Indigenous communities. Low genetic diversity from repeated genetic bottlenecks, coupled with the effects of Arctic warming (e.g., heat stress, changing forage, pathogen range expansions), present conservation concerns for this species. Reference genome assemblies enhance our ecological and evolutionary understanding of species (which in turn aid conservation efforts). Herein, we provide a full draft reference genome of muskox using Illumina Hiseq data and cross-species scaffolding. The final reference assembly yielded a genome of 2,621,890,883 bp in length, a scaffold N50 of ~13.2 million, and an annotation identifying ~19.3 k genes. The muskox genome assembly and annotation were then used to reconstruct a phylogenetic tree which estimated muskoxen diverged from other ungulate species~12 Mya. To gain insight into the demographic history of muskoxen we also performed pairwise sequentially Markovian coalescent (PSMC) that identified two population bottlenecks coinciding with major glaciation events contributing to the notoriously low genetic variation observed in muskoxen. Overall, this genome assembly provides a foundation for future population genomic studies, such as latitudinal analyses, to explore the capacity of muskoxen to adapt to rapidly changing environments.

Qiviut cortisol is associated with metrics of health and other intrinsic and extrinsic factors in wild muskoxen (Ovibos moschatus).

Glucocorticoid (GC) levels are increasingly and widely used as biomarkers of hypothalamic-pituitary-adrenal (HPA) axis activity to study the effects of environmental changes and other perturbations on wildlife individuals and populations. However, identifying the intrinsic and extrinsic factors that influence GC levels is a key step in endocrinology studies to ensure accurate interpretation of GC responses. In muskoxen, qiviut (fine woolly undercoat hair) cortisol concentration is an integrative biomarker of HPA axis activity over the course of the hair's growth. We gathered data from 219 wild muskoxen harvested in the Canadian Arctic between October 2015 and May 2019. We examined the relationship between qiviut cortisol and various intrinsic (sex, age, body condition and incisor breakage) and extrinsic biotic factors (lungworm and gastrointestinal parasite infections and exposure to bacteria), as well as broader non-specific landscape and temporal features (geographical location, season and year). A Bayesian approach, which allows for the joint estimation of missing values in the data and model parameters estimates, was applied for the statistical analyses. The main findings include the following: (i) higher qiviut cortisol levels in males than in females; (ii) inter-annual variations; (iii) higher qiviut cortisol levels in a declining population compared to a stable population; (iv) a negative association between qiviut cortisol and marrow fat percentage; (v) a relationship between qiviut cortisol and the infection intensity of the lungworm Umingmakstrongylus pallikuukensis, which varied depending on the geographical location; and (vi) no association between qiviut cortisol and other pathogen exposure/infection intensity metrics. This study confirmed and further identified important sources of variability in qiviut cortisol levels, while providing important insights on the relationship between GC levels and pathogen exposure/infection intensity. Results support the use of qiviut cortisol as a tool to monitor temporal changes in HPA axis activity at a population level and to inform management and conservation actions.

Corynebacterium freneyi Bacterial Septicemia Secondary to Contagious Ecthyma in a Wild Muskox (Ovibos moschatus).

A wild muskox (Ovibos moschatus) with dermatitis typical of contagious ecthyma had secondary bacterial septicemia with Corynebacterium freneyi that included laminitis, hepatitis, and suppurative encephalitis. This case supports the association between orf virus infection and fatal secondary infections, which may have contributed to population declines on Victoria Island, Canada.

Range expansion of muskox lungworms track rapid arctic warming: implications for geographic colonization under climate forcing.

Rapid climate warming in the Arctic results in multifaceted disruption of biodiversity, faunal structure, and ecosystem health. Hypotheses have linked range expansion and emergence of parasites and diseases to accelerating warming globally but empirical studies demonstrating causality are rare. Using historical data and recent surveys as baselines, we explored climatological drivers for Arctic warming as determinants of range expansion for two temperature-dependent lungworms, Umingmakstrongylus pallikuukensis and Varestrongylus eleguneniensis, of muskoxen (Ovibos moschatus) and caribou (Rangifer tarandus), in the Canadian Arctic Archipelago from 1980 through 2017. Our field data shows a substantial northward shift of the northern edge of the range for both parasites and increased abundance across the expanded ranges during the last decade. Mechanistic models parameterized with parasites' thermal requirements demonstrated that geographical colonization tracked spatial expansion of permissive environments, with a temporal lag. Subtle differences in life histories, thermal requirements of closely related parasites, climate oscillations and shifting thermal balances across environments influence faunal assembly and biodiversity. Our findings support that persistence of host-parasite assemblages reflects capacities of parasites to utilize host and environmental resources in an ecological arena of fluctuating opportunity (alternating trends in exploration and exploitation) driving shifting boundaries for distribution across spatial and temporal scales.

Correction: Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus).

[This corrects the article DOI: 10.1371/journal.pone.0231724.].

Novel insights into serodiagnosis and epidemiology of Erysipelothrix rhusiopathiae, a newly recognized pathogen in muskoxen (Ovibos moschatus).

BACKGROUND: Muskoxen are a key species of Arctic ecosystems and are important for food security and socio-economic well-being of many Indigenous communities in the Arctic and Subarctic. Between 2009 and 2014, the bacterium Erysipelothrix rhusiopathiae was isolated for the first time in this species in association with multiple mortality events in Canada and Alaska, raising questions regarding the spatiotemporal occurrence of the pathogen and its potential impact on muskox populations. MATERIALS AND METHODS: We adapted a commercial porcine E. rhusiopathiae enzyme-linked immunosorbent assay to test 958 blood samples that were collected from muskoxen from seven regions in Alaska and the Canadian Arctic between 1976 and 2017. The cut-off between negative and positive results was established using mixture-distribution analysis, a data-driven approach. Based on 818 samples for which a serological status could be determined and with complete information, we calculated trends in sample seroprevalences in population time-series and compared them with population trends in the investigated regions. RESULTS: Overall, 219/818 (27.8%, 95% Confidence Interval: 24.7-31.0) samples were classified as positive for exposure to E. rhusiopathiae. There were large variations between years and regions. Seropositive animals were found among the earliest serum samples tested; 1976 in Alaska and 1991 in Canada. In Alaskan muskoxen, sample seroprevalence increased after 2000 and, in two regions, peak seroprevalences occurred simultaneously with population declines. In one of these regions, concurrent unusual mortalities were observed and E. rhusiopathiae was isolated from muskox carcasses. In Canada, there was an increase in sample seroprevalence in two muskox populations following known mortality events that had been attributed to E. rhusiopathiae. CONCLUSION: Our results indicate widespread exposure of muskoxen to E. rhusiopathiae in western Canada and Alaska. Although not new to the Arctic, we documented an increased exposure to the pathogen in several regions concurrent with population declines. Understanding causes for the apparent increased occurrence of this pathogen and its association with large scale mortality events for muskoxen is critical to evaluate the implications for wildlife and wildlife-dependent human populations in the Arctic.

Muskox status, recent variation, and uncertain future.

Muskoxen (Ovibos moschatus) are an integral component of Arctic biodiversity. Given low genetic diversity, their ability to respond to future and rapid Arctic change is unknown, although paleontological history demonstrates adaptability within limits. We discuss status and limitations of current monitoring, and summarize circumpolar status and recent variations, delineating all 55 endemic or translocated populations. Acknowledging uncertainties, global abundance is ca 170 000 muskoxen. Not all populations are thriving. Six populations are in decline, and as recently as the turn of the century, one of these was the largest population in the world, equaling ca 41% of today's total abundance. Climate, diseases, and anthropogenic changes are likely the principal drivers of muskox population change and result in multiple stressors that vary temporally and spatially. Impacts to muskoxen are precipitated by habitat loss/degradation, altered vegetation and species associations, pollution, and harvest. Which elements are relevant for a specific population will vary, as will their cumulative interactions. Our summaries highlight the importance of harmonizing existing data, intensifying long-term monitoring efforts including demographics and health assessments, standardizing and implementing monitoring protocols, and increasing stakeholder engagement/contributions.

Geography, seasonality, and host-associated population structure influence the fecal microbiome of a genetically depauparate Arctic mammal.

The Canadian Arctic is an extreme environment with low floral and faunal diversity characterized by major seasonal shifts in temperature, moisture, and daylight. Muskoxen (Ovibos moschatus) are one of few large herbivores able to survive this harsh environment. Microbiome research of the gastrointestinal tract may hold clues as to how muskoxen exist in the Arctic, but also how this species may respond to rapid environmental changes. In this study, we investigated the effects of season (spring/summer/winter), year (2007-2016), and host genetic structure on population-level microbiome variation in muskoxen from the Canadian Arctic. We utilized 16S rRNA gene sequencing to characterize the fecal microbial communities of 78 male muskoxen encompassing two population genetic clusters. These clusters are defined by Arctic Mainland and Island populations, including the following: (a) two mainland sampling locations of the Northwest Territories and Nunavut and (b) four locations of Victoria Island. Between these geographic populations, we found that differences in the microbiome reflected host-associated genetic cluster with evidence of migration. Within populations, seasonality influenced bacterial diversity with no significant differences between years of sampling. We found evidence of pathogenic bacteria, with significantly higher presence in mainland samples. Our findings demonstrate the effects of seasonality and the role of host population-level structure in driving fecal microbiome differences in a large Arctic mammal.

A Transdisciplinary Approach to Brucella in Muskoxen of the Western Canadian Arctic 1989-2016.

Brucella serostatus was evaluated in 3189 muskoxen sampled between 1989 and 2016 from various locations of the Canadian Arctic archipelago and mainland, near the communities of Sachs Harbour and Ulukhaktok, Northwest Territories, and Cambridge Bay and Kugluktuk, Nunavut. Brucella antibodies were found only in muskoxen sampled around Cambridge Bay, both on southern Victoria Island and on the adjacent mainland (Kent Peninsula). Consistent with participatory epidemiology data documented from local harvesters describing increased Brucella-like syndromes (swollen joints and lameness) and a decreased proportion of juveniles, the apparent Brucella seroprevalence in the sampled muskoxen of the Cambridge Bay area increased from 0.9% (95% CI 0.3-2.1) in the period of 1989-2001 to 5.6% (95% CI 3.3-8.9) in 2010-2016. The zoonotic bacteria Brucella suis biovar 4 was also cultured from tissues of muskoxen sampled on Victoria Island near Ulukhaktok in 1996 (n = 1) and Cambridge Bay in 1998, 2014, and 2016 (n = 3). Overall, our data demonstrate that B. suis biovar 4 is found in muskoxen that are harvested for food and by guided hunts on Victoria Island and Kent Peninsula, adding an important public health dimension to this study. Robust participatory epidemiology data on muskox health and diseases greatly enhanced the interpretation of our Cambridge Bay data and, combined with the serological and microbiological data, provide compelling evidence that the prevalence of B. suis biovar 4 has increased in this area since the late 1990s. This study enhances the available knowledge on Brucella exposure and infection in muskoxen and provides an example of how scientific knowledge and local knowledge can work together to better understand disease status in wildlife.

Inferring the rules of social interaction in migrating caribou.

Social interactions are a significant factor that influence the decision-making of species ranging from humans to bacteria. In the context of animal migration, social interactions may lead to improved decision-making, greater ability to respond to environmental cues, and the cultural transmission of optimal routes. Despite their significance, the precise nature of social interactions in migrating species remains largely unknown. Here we deploy unmanned aerial systems to collect aerial footage of caribou as they undertake their migration from Victoria Island to mainland Canada. Through a Bayesian analysis of trajectories we reveal the fine-scale interaction rules of migrating caribou and show they are attracted to one another and copy directional choices of neighbours, but do not interact through clearly defined metric or topological interaction ranges. By explicitly considering the role of social information on movement decisions we construct a map of near neighbour influence that quantifies the nature of information flow in these herds. These results will inform more realistic, mechanism-based models of migration in caribou and other social ungulates, leading to better predictions of spatial use patterns and responses to changing environmental conditions. Moreover, we anticipate that the protocol we developed here will be broadly applicable to study social behaviour in a wide range of migratory and non-migratory taxa.This article is part of the theme issue 'Collective movement ecology'.

Morphological keys to advance the understanding of protostrongylid biodiversity in caribou (Rangifer spp.) at high latitudes.

The Protostrongylidae is a diverse family of nematodes capable of causing significant respiratory and neuromuscular disease in their ungulate and lagomorph hosts. Establishing the species diversity and abundance of the protostrongylid fauna has been hindered because the first stage larvae, commonly referred as dorsal spined larvae (DSL), that are shed in the feces are morphologically very similar among several genera. We aimed to determine the protostrongylid diversity and distribution in caribou (Rangifer tarandus groenlandicus and R. t. pearyi) in the central and high Canadian Arctic. We first developed, tested and validated a morphological diagnostic guide for the DSL of two important protostrongylids, Parelaphostrongylus andersoni and Varestrongylus eleguneniensis, and then applied this guide to determine the prevalence and intensity of infection of these parasites in fecal samples from 242 caribou. We found that DSL of V. eleguneniensis and P. andersoni can be differentiated morphologically based on the structural differences at the caudal extremity. The presentation and morphology of the dorsal spine, and caudoventral bulging at the start of the tail extension were identified as the key identifying features. The two species were found in caribou on the arctic mainland and southern Victoria Island in single and co-infections, but the prevalence and intensity of infection was low. No protostrongylids were detected in caribou from the high arctic islands. Through this study, we provide a simple, efficient, and robust method to distinguish the DSL of the two protostrongylids, and present the current status of infection in different herds of caribou of the central Canadian Arctic. We report new geographic and host records for P. andersoni infection in Dolphin and Union caribou herd.

Qiviut cortisol in muskoxen as a potential tool for informing conservation strategies.

Muskoxen (Ovibos moschatus) are increasingly subject to multiple new stressors associated with unprecedented climate change and increased anthropogenic activities across much of their range. Hair may provide a measurement of stress hormones (glucocorticoids) over periods of weeks to months. We developed a reliable method to quantify cortisol in the qiviut (wooly undercoat) of muskoxen using liquid chromatography coupled to tandem mass spectrometry. We then applied this technique to determine the natural variability in qiviut cortisol levels among 150 wild muskoxen, and to assess differences between sexes, seasons and years of collection. Qiviut samples were collected from the rump of adult muskoxen by subsistence and sport hunters in seven different locations in Nunavut and the Northwest Territories between 2013 and 2016. Results showed a high inter-individual variability in qiviut cortisol concentrations, with levels ranging from 3.5 to 48.9 pg/mg (median 11.7 pg/mg). Qiviut cortisol levels were significantly higher in males than females, and varied seasonally (summer levels were significantly lower than in fall and winter), and by year (levels significantly increased from 2013 to 2015). These differences may reflect distinct environmental conditions and the diverse stressors experienced, as well as physiological and/or behavioural characteristics. Quantification of qiviut cortisol may serve as a valuable tool for monitoring health and informing conservation and management efforts.