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Muskox status, recent variation, and uncertain future

  • Christine CuylerEmail author
  • Janice RowellEmail author
  • Jan Adamczewski
  • Morgan Anderson
  • John Blake
  • Tord Bretten
  • Vincent Brodeur
  • Mitch Campbell
  • Sylvia L. Checkley
  • H. Dean Cluff
  • Steeve D. Côté
  • Tracy Davison
  • Mathieu Dumond
  • Barrie Ford
  • Alexander Gruzdev
  • Anne Gunn
  • Patrick Jones
  • Susan Kutz
  • Lisa-Marie Leclerc
  • Conor Mallory
  • Fabien Mavrot
  • Jesper Bruun Mosbacher
  • Innokentiy Mikhailovich Okhlopkov
  • Patricia Reynolds
  • Niels Martin Schmidt
  • Taras Sipko
  • Mike Suitor
  • Matilde Tomaselli
  • Bjørnar Ytrehus
Open Access
Terrestrial Biodiversity in a Rapidly Changing Arctic

Abstract

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.

Keywords

Abundance Circumpolar Drivers Ovibos Population status Trends 

Introduction

For the past 50 years, the Arctic has been warming twice as fast as the rest of the world creating a climate that today is warmer, wetter, and increasingly more variable (AMAP 2017). Apprehension about the impact of changing climate on Arctic ecosystems is growing in the face of many unknowns. This paper focuses on the muskox (Ovibos moschatus), a large-bodied herbivore that plays a central role in many Arctic ecosystems. It is physiologically and behaviorally adapted to living year-round in the Arctic. Today, muskox populations (endemic and translocated/re-introduced) inhabit a range that extends from sub- to high Arctic (56°–83°N) environments (Fig. 1).
Fig. 1

Global overview of current distribution and origin of muskox populations: endemic, translocated, and mixed. Translocated includes introduced and re-introduced, i.e., to range once occupied either in recent or distant past. Mixed is translocation to an area with endemic muskoxen. Numbering corresponds with Table 1, and indicates an administrative region, a management unit, or a population. The provided boundaries are guidelines, often reflecting administrative or political regions. They are not a precise distribution/extent for a specific population, e.g., since muskoxen can and do travel across sea-ice, even the islands are not strict boundaries. The muskox distribution in central Canada around 60°N is uncertain owing to anecdotal observations and low animal density. Populations 3, 7, 19, 34, and 36 originated as range expansions by translocated populations. Zackenberg Station is the red star in NE Greenland (see Electronic Supplementary Materials S1, Muskoxen: Past and present). Dashed line is the Arctic Circle

Muskoxen have an intrinsic connection with the culture, traditions, and heritage of Arctic indigenous peoples, a connection that continues to evolve (Tomaselli et al. 2018a). They are an important food resource in an area of increasing food insecurity and they provide diverse economic opportunities where few exist (Kutz et al. 2017).

Two subspecies, O.m. wardi and O.m. moschatus, are commonly recognized and referred to as ‘White-Faced’ and ‘Barren-Ground,’ respectively (van Coeverden de Groot 2001), and recent studies have identified genetic separation between the two (Hansen et al. 2018). We therefore refer to the two subspecies throughout this study.

In 2014, the Muskox Expert Network (MOXNET) emerged from the mammalian component of the terrestrial Circumpolar Biodiversity Monitoring Program (CBMP). Participants from seven circumpolar countries, representing government and non-governmental agencies, indigenous peoples, businesses, and academics, came together to establish a network of experts for the sharing and exchange of information on muskoxen. This paper is a MOXNET collaborative compilation of the current information on muskoxen. Following the protocols outlined in the Arctic Terrestrial Biodiversity Monitoring Plan (CBMP Terrestrial Steering Group 2015), we present estimates and information on muskox population abundance and distribution, and discuss demographics, spatial distribution, health, and genetic diversity. Within this context, we identify primary drivers of change and stressors potentially influencing muskox population dynamics along with important knowledge gaps. Finally, we summarize key findings and suggest recommendations in an effort to foster sustainable muskox populations throughout the circumpolar north during a changing and uncertain future.

Methods

We updated the global distribution and origins of muskox populations reported in Kutz et al. (2017) and added current population/region boundaries. The boundaries provided often reflect administrative or political regions rather than specific muskox populations and their actual distribution within a region. Therefore, these boundaries do not necessarily reflect population structures, and are likely to change as protocols for standardizing biologically meaningful population boundaries are established and implemented.

We compiled current abundance estimates for the 55 geographic regions with muskox populations (Table 1). These estimates include all age classes. The majority (80%) of our population sizes are based on surveys within the past decade. Further, over half of these were monitored recently, i.e., in the period 2016–2019 (54.5%; n = 30) and 25.5% (n = 14) within 2009–2015. Where geographic regions surveyed subareas piecemeal, a sum total estimate was provided for the region. Electronic Supplementary Materials contain details on recent and past abundance estimates for each population (Excel Table S3).
Table 1

Global overview of muskox populations, location, subspecies designation, CAFF Arctic zone (CAFF 2013), last survey year, population size, and recent variation (suggested trend) within the last 10 years (Electronic Supplementary Materials, Excel Table S3 contains details)

Country/Muskox population

Figure 1 no.

Subspecies

CAFF Arctic zone

Last survey year

Population sizea

Recent variation

USA—Alaska

 Nunivak Island

1

wardi

Low

2015

740

Stable

 Nelson Island

2

wardi

Low

2018

444

Stable

 Yukon Kuskokwim Delta

3

wardi

Low

2017

252

Increasingb

 Seward Peninsula

4

wardi

Low

2017

2353

Stable

 Cape Thompson

5

wardi

Low

2017

227

Decreasing

 North East

6

wardi

Low

2018

285

Increasing

 Total Alaska

    

ca 4301

 

Canada Mainland

 Yukon

      

  Yukon North slope

7

wardi

Low

2018

344

Increasing

 Northwest Territories

      

  Inuvik

8

moschatus

Low/sub

2009

2855

Stable

  Sahtu

9

moschatus

Sub

1997

1457

Increasing

  North Great Slave

10

moschatus

Sub

2018

8098

Increasing

  South Great Slave

11

moschatus

Sub

2011

164

Increasingc

 Nunavut

      

  MX-09

12

moschatus

Low

2018

539

Stable

  MX-11d

13

moschatus

Low

2013

13 592

Unknown

  Thelon, MX-12

14

moschatus

Low/sub

1994

1095

Decreasing

  MX-13

15

moschatus

Low/sub

2010

4736

Increasing

  MX-10e

16

moschatus

High/low

2013

3685

Increasing

  Boothia Peninsula MX-08

17

wardi

High

2018

3649

Increasing

 Quebec (Nunavik)

      

  Ungava Bay

18

wardi

Low

2019

3000

Increasing

  Eastern Hudson Bay

19

wardi

Low/sub

2016

1000

Increasing

Canada Arctic Archipelago f

 Northwest Territories

  Banks Is.

20

wardi

High

2014

14 021

Decreasing

  NW. Victoria Is.

21

wardi

High

2015

14 547

Stable

  Melville Is. Complexg

22

wardi

High

2012

3716

Increasing

 Nunavut

      

  E. Victoria Is. MX-07

23

wardi

High

2014

10 026

Decreasing

  Pr. Wales/Somerset Is.g MX-06

24

wardi

High

2016

3052

Unknown

  Bathurst Is. Complexg MX-05

25

wardi

High

2013

1888

Increasing

  Ringnes & Cornwall Is. MX-03

26

wardi

High

2007

21

Unknown

  Axel Heiberg Is. MX-02

27

wardi

High

2007

4237

Unknown

  Ellesmere Is. MX-01

28

wardi

High

2015

11 315

Increasing

  Devon Is. MX-04

29

wardi

High

2016

1963

Increasing

  Total Canada

    

ca 109 000

 

Greenland

 Inglefield Land

30

wardi

High

2000

273

Unknown

 Cape Atholl

31

wardi

High

2017

212

Stable

 Sigguk (Svartenhuk)

32

wardi

Low

2002

193

Unknown

 Naternaq

33

wardi

Low

2004

112

Unknown

 Sisimiut

34

wardi

Low

2018

2622

Unknown

 Kangerlussuaq

35

wardi

Low

2018

20 334

Unknown

 Nuuk

36

wardi

Low

2016

14

Unknown

 Ivittuut

37

wardi

Low

2017

812

Decreasingh

 Nanortalik

38

wardi

Sub

2018

32

Increasing

 Inner Kangertittivaq Fjord

39

wardi

High

2004

562

Unknown

 Jameson Land

40

wardi

High

2000

1761

Unknown

 North East Greenland

41

wardi

High

1992

12 500

Unknown

 Total Greenland

    

ca 39 427

 

Scandinavia

 Norway: Dovre

42

wardi

Not Arctic

2018

244

Stable

 Sweden: Rogen Nature Reserve

43

wardi

Not Arctic

2017

10

Unknown

 Total Scandinavia

    

ca 254

 

Russia

 Yamal Peninsulai

44

wardi

Low

2017

300

Increasing

 Taimyr Peninsula

45

wardi

Low

2017

12 100

Increasing

 Begicheva Islandj

46

wardi

Low

2017

230

Stable

 Putorana Plateau

47

wardi

Sub

2004

20

Unknown

 Anabarskay

48

wardi

Low/sub

2017

1040

Increasing

 Bulunskayk

49

wardi

Low/sub

2017

700

Increasing

 Indigirskay

50

wardi

Low/sub

2017

350

Increasing

 Kolymskay

51

wardi

Low/sub

2017

30

Increasing

 Magadan Oblast

52

wardi

Sub

2015

16

Unknown

 Magadan Omulevka River

53

wardi

Sub

2015

6

Unknown

 Chukotkal

54

wardi

Low

2017

4

Decreasing

 Wrangel Island

55

wardi

Low

2018

1000

Increasing

 Total Russia

    

ca 15 796

 

GLOBAL TOTAL MUSKOXEN

    

ca 168 778

 

aSize indicates a recent estimate or a minimum/total count (see Electronic Supplementary Materials, Excel Table S3)

bLocal knowledge and observations indicate increasing abundance and distribution

cRecent variation is for 2018; based on increasing number of opportunistic sightings, possibly stabilizing by 2018

dCurrently includes Kugluktuk, Queen Maud, Contwoyto Lake, and two old regions: MX-14 and MX-19. Kuglugtuk sub-area, last surveyed in 2013, may be increasing

eCurrently includes King William Is, Adelaide Peninsula, and two old regions: MX-17 and MX-20

fOnly major island names provided

gMelville Is. complex, includes Melville, Prince Patrick, and Eglinton Islands. Bathurst Is. complex includes Bathurst, Cornwallis, Little Cornwallis, Helena, Sherard-Osborn, Cameron, Vanier, Massey, and Alexander Islands. Prince of Wales/Somerset Island also includes Russell, Prescott, and Pandora Islands

hHarvest management induced decline

i2016, An additional 60 muskoxen were translocated from the Aviary (captive breeding facility)

j2017-Survey method permitted more accurate count than previously, thus not assumed an increase in herd size

k2017, An additional 22 muskoxen translocated to the Lena River Delta

1Although muskoxen have been released several times (most recently in 2010), bears/humans cause high mortality

Statistical trend analyses for abundance of a specific population were rarely possible, because surveys were often too infrequent, had unavailable estimates of variance, or had different methods or effort between surveys. Thus, we provide the most recent abundance estimate (Table 1), and used abundance changes over the last 10 years (Electronic Supplementary Materials, Excel Table S3) to reveal recent variation, suggesting possible trends (Fig. 2). Estimates, counts, and recent variation were corroborated by local experts (regional biologists, research scientists) wherever possible (Electronic Supplementary Materials, Muskoxen: Past and present, and Excel Table S3). Recent variation/trend was labeled unknown if the estimate/count was older than 10 years, a recent once-only effort, or involved ≤ 20 individuals and additional expert knowledge was unavailable.
Fig. 2

Global overview of recent variation in muskox abundance. Numbering corresponds with Table 1 and indicates an administrative region or population. The provided boundaries are guidelines and not precise distributions of a given population. Zackenberg Station is the red star in NE Greenland (see Electronic Supplementary Materials S1, Muskoxen: Past and present). Dashed line is the Arctic Circle

Results and discussion

Of all the Focal Ecosystem Component (FEC) attributes prioritized for terrestrial mammals in the Arctic Terrestrial Biodiversity Monitoring Plan (Christensen et al. 2013), estimates of muskox abundance comprise the most extensive data available both geographically and temporally. Despite the limitations and inconsistencies in the data, our best approximation of current global abundance is 170 000 muskoxen, of which 71% are endemic (Table 1). While some populations are in decline (e.g., Banks and Victoria islands), others have expanded their range or experienced increases typical of translocated populations (see Electronic Supplementary Materials, Muskoxen: Past and present S1, and Excel Table S3). Occasionally, a stable or decreasing population trend is the result of wildlife management interventions designed around specific goals (e.g., Nunivak Island and Ivittuut respectively, see Electronic Supplementary Materials S1, Muskoxen: Past and present). Translocations over the past century have resulted in a circumpolar distribution of muskoxen, and all re-introduced/translocated animals have been O.m. wardi (see Electronic Supplementary Materials, Excel Table S3). The combined number of re-introduced, translocated, and endemic O.m. wardi (e.g., 132 557) now vastly outnumber O.m. moschatus (e.g., 36 221), which remain confined primarily to mainland Canada. Nevertheless, endemic muskoxen (both O.m. wardi and O.m. moschatus) still outnumber re-introduced/translocated muskoxen, e.g., 119 479 to 49 026, respectively (the mixed population of Inglefield Land not included). Given already low genetic variability among endemic sources (Groves 1997; Holm et al. 1999) and the relatively few individuals captured for translocations (often from the same geographic source), future studies may reveal exacerbated low variability in several translocated populations. More information on successful and failed translocations is available in Electronic Supplementary Materials (S1 Muskoxen: Past and present).

Our circumpolar estimate of 170 000 is greater than previous estimates of 134 000–137 000 (IUCN 2008), ca 135 000 (Gunn et al. 2013), and 111 000–135 000 (Kutz et al. 2017), and represents our best approximation given all data ambiguities. The compiled abundance surveys commonly gave estimates that contained all age classes. Thus, we were unable to provide a circumpolar estimate of only reproductive adults, although this is the criterion implemented by IUCN.

We could suggest recent trends for 38 out of our 55 muskox populations/regions based on variation over the past decade (Fig. 2). Of these, 23 appear to be increasing. These represent 36.2% (n = 61 104) of present global abundance. Similarly, nine populations appear stable and six decreasing, representing 13.1% (n = 22 164) and 15.5% (n = 26 185), respectively, of present global abundance. It is worth noting that two of the declining populations were once the largest endemic populations in the world, i.e., Banks and East Victoria islands in Canada. At the turn of the century, these two combined totaled ca 87 000 muskoxen, but today they are ca 24 000 (see Electronic Supplementary Materials, Excel Table S3). Mortality events caused by infectious agents have been identified in both regions (see Electronic Supplementary Materials S1, Muskoxen: Past and present). The fact that recent trends are unknown for a further 17 populations (35.1%; n = 59 322) makes it difficult to interpret the true impact of these declines relative to the total global population. Regardless, it is clear that population status can change quickly.

Abundance

We recognize that natural fluctuations in population size are normal, often unpredictable, and not always synonymous with long-term trends, and thus abundance data and suggested trends are not without their limitations. Regardless, they provide some context where previously little existed. Muskox ranges are remote and cover vast areas, often crossing jurisdictional boundaries. Few are near human settlements or airports, making aerial surveys expensive and logistically difficult. Sample counts using line or strip transects are commonly used to estimate muskox abundance. However, area coverage varies and so does precision. For example, the coefficient of variation (CV) for 17 estimates on Banks Island (Canada) averaged 11% but was 30% for two surveys on the mainland (Queen Maud Gulf coast, Canada). Additionally, detection (sightability) of muskoxen present on a survey line varies. Detection is affected by distance from survey line, group size, terrain features determining viewing distance, weather conditions, and type of background (e.g., variations in the ratio of snow cover to bare ground/boulders/vegetation poking through snow surface), as well as animal movements or lack thereof. Observer ability, fatigue, and airsickness also influence the detection of animals present on a survey line. Poor sightability can underestimate population abundance.

Assessment of trends in muskox abundance over time and across regions is complicated further by variable survey methods and inconsistent survey efforts (extent of area covered) within the same region. The recent change to Nunavut’s muskox management units/regions exacerbates existing obstacles to making trend assessments. Among study areas, different survey methods are often employed. For example, Nelson Island, AK, is a relatively small survey area. Here, by using small aircraft and employing photography with close line spacing, surveys produce results that approximate a total count (Jones 2015). On Banks Island, strip-transect fixed-wing surveys with consistent methods and coverage have been used since the 1980s (Davison et al. 2017). However, due to changes in terrain across the Canadian High Arctic, surveys of muskoxen in Nunavut have employed both helicopter-based distance-sampling methods (Jenkins et al. 2011) and fixed-wing strip-transect methods (Anderson and Kingsley 2017). A complex terrain and financial constraints challenge Greenland surveys. Unsystematic ground counts have been typical, although there have been some fixed-wing or helicopter strip counts, and recently, the Sisimiut and Kangerlussuaq populations were assessed using helicopter-based distance sampling. Regardless, with the exception of Zackenberg and Ivittuut, Greenland surveys are infrequent or provide a one-time snapshot for now. While a more consistent approach on a large scale is desirable for surveys of muskoxen, local and regional conditions and topography, together with limitations of funds and staff, mean that the mosaic of survey methods is likely to continue. Recognizing these difficulties, the goal remains a standardization of field methods, the absence of which makes rigorous statistical trend analyses impossible. We must establish and implement protocols for defining what constitutes a muskox population, thus forming the basis for consistent, uniformly defined survey areas. We also require standardized monitoring protocols, among these, how to incorporate the traditional and local knowledge that can supplement infrequent surveys. Once standards for the above gain broader acceptance and implementation, comparing trends across regions can be done with statistical confidence and certainty.

Demographics

Annual recruitment affects future population trend (Schmidt et al. 2015), regardless of present abundance. The ultimate influence of drivers and stressors on muskox populations is how these affect vital rates for calf births, calf survival, and adult survival. These three rates are integral to population trends. Knowledge about muskox demographics is however hard to obtain, as demographic monitoring is not widespread and published data are scarce. The necessary ground-based surveys, ideally incorporating the use of telemetry (collared animals), are logistically difficult and usually expensive. Studies to date involve only small populations, or areas of high density. Additionally, group composition varies depending on season (Schmidt et al. 2015), which confounds comparison of sex and age structure surveys. The natural mortality rate for adults, although unknown, may be approximated for a specific population if average life expectancy is available.

Monitoring demographics is among the protocols outlined in the Arctic Terrestrial Biodiversity Monitoring Plan (Christensen et al. 2013). We recognize that reliable demographic information is vital for developing relevant management strategies and policy. Consistent, standardized approaches for gathering seasonal demographics are essential for accurately interpreting abundance trends and will enhance our ability to compare population dynamics across regions.

Spatial distribution and genetic diversity

Although generally not considered migratory, seasonal distributions of muskoxen can span broad geographic regions (Fig. 1). To take advantage of forage quality and accessibility, groups may move between winter and summer ranges (Tener 1960; Gunn and Fournier 2000), while in other areas habitat heterogeneity allows muskoxen a more sedentary lifestyle (Schmidt et al. 2016). Further, striking shifts in range use have also been observed, with muskoxen in northeastern Alaska having expanded their range into adjacent regions and vacating originally occupied areas (Reynolds 2011). Mixed groups will occasionally leave to colonize an entirely different region (Cuyler pers. comm.), even moving across glacial barriers (Schmidt et al. 2016). The wide dispersion of this species and these relatively unpredictable movements impede survey efforts, especially when coupled with infrequent surveys (Adamczewski in Kutz et al. 2017).

Muskoxen are among a handful of Arctic species that survived major shifts in climate (Raghavan et al. 2014). The archeological record, supported by genetic data (MacPhee et al. 2005), provides evidence that muskoxen have been through several population bottlenecks and extirpation events that are best explained by non-anthropogenic causes, e.g., environmental change (Campos et al. 2010). This has left present day muskoxen challenged by low genetic variability (Hansen et al. 2018) and extremely low diversity in the major histocompatibility complex, potentially impacting their ability to respond to infectious disease (Gordeeva et al. 2009; Cooley et al. 2011; Thulin et al. 2011). A better understanding of muskox genetics would be instrumental in steering future management and conservation efforts.

Health

Although the need for monitoring disease in muskoxen was recognized almost 80 years ago (Jennov 1941), attention to muskox diseases is relatively new with only sporadic accounts of infectious diseases and parasites in the early literature (Tener 1965; Mathiesen et al. 1985). Recent documentation has occurred in connection with declining populations where emerging pathogens and shifting disease dynamics have been observed. For example, acute and extensive infectious disease associated summer mortalities in Alaska and Canada coincided with population declines of up to 85% (Kutz et al. 2015; Forde et al. 2016), and outbreaks of Pasteurella spp., Mycoplasma spp., and parapox virus in muskoxen in the Dovrefjell, Norway, have been identified in declining populations (Ytrehus et al. 2008, 2015; Handeland et al. 2014). Changing pathogen distribution and disease dynamics have also been observed with climate-driven range expansion of the lung nematode Umingmakstrongylus pallikuukensis in the Northwest Territories and Nunavut (Kutz et al. 2013a, b; Kafle et al. 2017), the emergence of parapox virus, and increasing observations of Brucella-like lesions on Victoria Island, Canada (Tomaselli et al. 2016). We are just starting to recognize the extent and importance of disease in muskox population dynamics. To provide information on the prevalence, significance, and role disease plays in muskox population dynamics, we acknowledge the need to adopt standardized health assessment protocols, systematically document local knowledge on muskox health, and the use of more advanced modeling methodologies. Subsequent development of assessments for general population health would complement surveys for abundance. The Electronic Supplementary Materials (Tables S1, S2) provide an up-to-date overview of pathogens and diseases described in muskoxen.

Drivers and knowledge gaps

The vulnerability and resilience of muskoxen and associated knowledge gaps were discussed extensively at the 2016 muskox health ecology symposium (Kutz et al. 2017). Here, we define a driver as a major change that generates stressors. We regard stressors as typically regional events or conditions that create impacts locally for specific populations. These impacts bring about changes in populations, including demographics, movement and dispersal patterns, health. The CBMP Freshwater group identified climate and human activity as the most influential factors changing the hydrology, pollutions, and biochemistry of regions (Lento et al. 2018), all of which will affect herbivores, including muskoxen.

Climate change

The consequences of climate change on life in the Arctic are diverse, multifaceted, and largely unknown. We summarize here stressors and effects with the greatest potential to alter muskox population dynamics.

Stressors: Stochastic events and weather extremes

For over half a century, changes in calf productivity and survival have been linked to annual variability in regional weather patterns (Tener 1965; Miller and Russell 1975). Increasing temperatures, especially in fall and winter, increase the likelihood of extreme weather events including deeper than average snow depths (Gunn et al. 1989; Reynolds 1998), ice-crust formation (Forchhammer and Boertmann 1993), and rain-on-snow events (Gunn et al. 1989; Putkonen et al. 2009). All can reduce feed availability and increase the energetic cost of foraging, which may lead to increased mortality and decreased calf recruitment (Parker et al. 1975; Gunn and Adamczewski 2003; Miller and Barry 2009). Analyses of long-term datasets reveal a more complex and less predictable association between winter precipitation, ice-crust formation, and muskox population dynamics (Forchhammer and Boertmann 1993; Schmidt et al. 2015). This reinforces the importance of considering the impact of both temporal and spatial scale on interpretations of individual studies and datasets (Post et al. 2009; Bölter and Müller 2016). Examples include the regional-scale decline in muskox abundance, of more than 90%, after three consecutive winters of record snowfall in the Bathurst Island Complex (Miller 1998), and on a smaller spatial and temporal scale, the Alaskan tidal surge which entombed 55 muskoxen in ice (Adams in Kutz et al. 2017; Berger et al. 2018). The impact of increasing frequency, distribution, severity, and extent of stochastic events on population dynamics remains a serious knowledge gap for this species.

Muskoxen are well adapted to life in cold, dry habitats and there is a tendency to think of cold environments as essential to their survival. However, there is wide thermal variability within their endemic habitat (mean summer maximums of 21°–27 °C to mean winter minimums of − 34 °C: Tener 1965). On the Canadian Arctic mainland, muskoxen are currently extending their range southward (Adamczewski in Kutz et al. 2017), and translocated animals (both captive and wild) have survived in a variety of habitats both warmer and wetter than their traditional range (Lent 1999). There are currently seven muskox populations living in CAFF’s designated Sub Arctic Zone, and a further two that live in non-arctic zones (Fig. 1, Table 1). Local conditions, like availability of shade, shallow water for wading, and snow patches, may mitigate the effects of warm ambient temperatures (Cuyler pers. comm.). Regardless, increases in heat and humidity can precipitate serious adverse effects, especially when these co-occur with other stressors (e.g., pathogens, nutrient deficiencies, disturbance, and predation) or during sensitive periods (i.e., calving, rut) (Ytrehus et al. 2008, 2015). Shifts in temperature and precipitation regimes are predicted for the Arctic, and carry the possibility of influencing muskox reproduction and survival.

Impacts: Changing vegetation, species associations, and disease

Changing vegetation diversity, abundance, composition, and phenology in the Arctic are all well documented (Sturm et al. 2001; Walker et al. 2006; Bjørkman et al. 2020). Landscape-scale changes in vegetation (e.g., shrubification), affect ecosystems at multiple trophic levels (Myers-Smith et al. 2011; Mod and Luoto 2016) and have generated concerns about trophic mismatch (Kirby and Post 2013). Before we can address the effects of climate change on forage quantity and quality, we need to understand the impact of normal grazing on these matrices under differing animal densities and at multiple scales. Muskox grazing can alter carbon dioxide and methane fluxes (Falk et al. 2015), redistribute nutrients (Murray 1991; Mosbacher et al. 2016), alter plant community composition (Mosbacher et al. 2018), sometimes mitigate shrubification (Post and Pedersen 2008), and enhance graminoid production (Mosbech et al. 2018). In addition to vegetation biomass, an understanding of the complete nutrient value of the vegetation and its correlation with population health is currently lacking. Trace mineral deficiencies in wild ruminants predispose them to a range of subclinical ailments including poor reproductive performance, immunosuppression, and anemia (Blake et al. 1991; Afema et al. 2017), all of which makes them more vulnerable to pathogens, predation, and weather. Monitoring programs need to incorporate a clear, unified criterion for defining and evaluating grazing disturbances on vegetation at multiple temporal and spatial scales. Establishing baseline reference ranges for the complete nutrient value (including an approximate range of possible year-to-year variations) of muskox forages throughout the north is an essential compliment to these data.

Changes in temperature and precipitation are likely to influence the trophic context faced by muskoxen, not just from changes in vegetation, but potentially from mosquitoes and other biting insects. Although the role of insect harassment on caribou ecology is relatively well documented (Raponi et al. 2018), their role in muskox ecology is not. Simultaneously, the northward expansion or changing densities of species, ranging from potential predators to herbivore competitors or species capable of altering ecosystems (e.g., beaver Castor canadensis: Tape et al. 2018) is unprecedented in our time and presents unknown, unevaluated risks and/or benefits. Historically, wolves (Canis lupus) were considered the main predator in muskox ecosystems (Marquard-Petersen 1998; Gunn and Adamczewski 2003; Mech 2011). Now, documentation of grizzly bear (Ursus arctos) predation, originally considered a sporadic occurrence, is increasing in some regions (Gunn and Adamczewski 2003; Arthur and Del Vecchio 2017). Grizzly bears are a more important predator than wolves in northeastern Alaska (Reynolds et al. 2002). Information on muskox predator–prey relationships, especially in multi-prey situations, is necessary to understand and predict population trends.

Changing patterns of infectious and non-infectious disease have been documented across several muskox populations in the last decade. Climate warming is behind some changes, while causes in other instances are less well understood. Through morbidity, reproductive failure, and mortality, pathogens, whether introduced or endemic, are likely to play a role in changing the distribution and dynamics of muskox populations. Furthermore, none of the specified stressors is acting in isolation. Ultimately, environmental and nutritional factors may be enabling infectious agents to cause overt disease, or alternatively subclinical disease, which may predispose individuals to a host of stressors, and through complex interactions determine the cumulative impact on muskox population dynamics.

Anthropogenic change

A consequence of warming temperatures in the Arctic is the overall increase in human activity, especially in previously inaccessible habitats. Predicting how muskoxen will respond to the greater human presence is difficult.

The impact of increasing industrial pursuits (oil and gas, open pit mines), as well as their associated pollutants (Gamberg and Scheuhammer 1994) or pollutants accumulating from more southern locations (Salisbury et al. 1992), need to be documented and monitored, especially considering the role of muskox in subsistence food economies.

Today’s greater access to a previously remote Arctic has also contributed to the increasing appeal of the Arctic as a tourist destination. While expanding tourism provides new economic opportunities to northern residents, it is also associated with serious challenges, including but not limited to, environmental degradation and increasing problems with waste disposal and pollution from greater ship and air traffic (CAFF 2013).

At the local community level, climate change in the Arctic has sometimes made areas less predictably accessible depending on the season (Kutz pers. comm.), while elsewhere opportunities to access remote terrain have expanded with modern modes of transportation, and contributed to a proliferation of summerhouses and year-round use (Cuyler pers. comm.).

Food insecurity in northern communities is a growing concern and a significant public health problem (Ruscio et al. 2015). With decreasing access to subsistence and traditional foods, northern communities are seeking sustainable alternatives. Some are considering or have begun implementing agricultural practices, including livestock production (Caviezel et al. 2017). Livestock creates a new source of competition for muskox food resources, and avenues for the introduction of novel pathogens.

Hunting contributed to the muskox decline of the early 1900s (Lent 1999). Muskox harvesting, whether strictly for subsistence or for broader commercial enterprises, must be carefully monitored and sustainable yields enforced. Today, most, but not all, muskox harvests are regulated. Enforcement, however, is often a difficult task, owing to large uninhabited areas, insufficient resources and people (e.g., six hunting officers for all of Greenland; Cuyler pers. comm.). Levels of hunter compliance are not well known. Recently, global markets for muskox qiviut wool, also known as ‘Arctic Gold,’ have grown rapidly (Jørgensen 2019). The low availability of qiviut relative to current demand has driven prices up sharply for raw winter skins and ultimately qiviut wool (Jørgensen 2019). For hunters, this has created opportunities for large instant profits. Although illegal in Greenland, killing muskoxen for just their winter skins, and out-of-season harvesting using prohibited methods occurs (Cuyler pers. comm.) Assuming global demand for qiviut wool will continue rising, even vigilant monitoring and enforcement may not be enough to ensure continued sustainable use of present muskoxen populations. The new market situation may require regulation of the trade in muskox skins. Simultaneously, reliable harvest data are scarce, making it difficult to document the numbers of muskoxen taken or the economic contribution to northern communities. Further, depending on the type of harvest, it may affect muskox group composition and ultimately population dynamics (Rockwood 2015), yet an assessment of effects on muskox abundance and demographics is difficult without reliable harvest data. We also generally lack effective user-friendly models to determine sustainable harvesting levels and thresholds (Cuyler pers. comm.). The concept of adaptive management (Madsen et al. 2017) might be a suitable platform to help ensure appropriate regulations development, while taking into account all stakeholders. A market economy can drive population changes, either by exerting a negative downward pressure (Berger et al. 2013), or by encouraging northern communities to consider the economic potential, and thus bolster conservation efforts. Developing strategies to facilitate cooperative management between agencies and local communities will foster the latter outcome, e.g., the PISUNA (2014) initiative as implemented in Greenland.

Key findings and next steps

This is the first summary containing current information for all muskoxen populations. Recognizing the limitations inherent in these data, we estimate global abundance of muskoxen at ca 170 000. Climate, diseases, and anthropogenic changes, singly or any interaction thereof, constitute the major foreseeable challenges for muskoxen. Which elements become critical for a specific population will vary and depend on a host of local interacting variables, which may be difficult to predict or mitigate, e.g., stochastic weather events.

There is an acute need to increase the frequency of surveys and standardize the variety of existing monitoring protocols, including consistent definitions and methodology for how survey areas and range limits are determined, especially how populations are defined. We need more data and standardized protocols on demographics and harvest specific to each population. Wherever possible, new monitoring initiatives must include health assessment metrics, local weather events, and increased traditional knowledge contributions.

The most effective path forward is to leverage existing resources. Multidisciplinary approaches will enable the most rapid gains in the shortest period. Using MOXNET membership, collaborative initiatives can be developed regionally and internationally to address the next steps.

Establishing standardized protocols can begin by building on recognized practices such as those developed by the CARMA network for caribou (CircumArctic Rangifer Monitoring & Assessment) (Gunn and Russell 2008; Gunn and Nixon 2008; Kutz et al. 2013a). Further development would incorporate new, innovative approaches for monitoring health and disease, include integration of traditional ecological knowledge and community-based monitoring, and expand scope and range with emerging technologies (Kutz et al. 2017). To be effective these protocols must incorporate from inception to implementation, local input through strategies such as co-management programs, hunter participation, and local knowledge (Tomaselli et al. 2018a, b).

While MOXNET is an organization with a primary focus on muskoxen, multidisciplinary input is necessary to incorporate an ecosystem approach, e.g., abiotic monitoring, specifically the intensity and extent of adverse weather events; monitoring changes in vegetation and the impact of grazing at multiple temporal and spatial scales; monitoring the impact of changing species’ boundaries on predator/prey relationships. Only through an interdisciplinary lens can we identify and exploit existing opportunities. For example, the low genetic diversity and widespread translocations/re-introductions of muskoxen around the Arctic create the opportunity of almost unprecedented investigations into the plasticity of muskox traits (morphological, phenological, behavioral, etc.) relative to a variety of environmental conditions, all while holding evolutionary history as a constant.

Finally, we need to facilitate data sharing with a collaborative focus on the establishment of a circumpolar database, its infrastructure, and management. This will enable the harmonization of existing data sources, feed into the creation of predictive models, and prioritize future research directions.

Notes

Acknowledgements

We thank Marlene Doyle (Environment and Climate Change Canada) for initiating the MOXNET network, and with Mallory Carpenter laying the beginnings of the muskox database. We thank Jukka Wagnholt from Greenland Institute of Natural Resources, Nuuk, Greenland, for assistance with figures. DANCEA (Danish Cooperation for Environment in the Arctic) and co-funding from authors’ Institutions supported the establishment of MOXNET network. All authors are members of the CBMP international muskox knowledge network, MOXNET.

Supplementary material

13280_2019_1205_MOESM1_ESM.pdf (1.2 mb)
Supplementary material 1 (PDF 1260 kb)
13280_2019_1205_MOESM2_ESM.xlsx (88 kb)
Supplementary material 2 (XLSX 88 kb)

References

  1. Afema, J.A., K.B. Beckmen, S.M. Arthur, K.B. Huntington, and J.A. Mazet. 2017. Disease complexity in a declining Alaskan Muskox (Ovibos moschatus) population. Journal of Wildlife Diseases 53: 311–329.CrossRefGoogle Scholar
  2. AMAP. 2017. Snow, water, ice and permafrost in the Arctic (SWIPA) 2017. Arctic Monitoring and Assessment Programme (AMAP), Oslo, Norway. www.amap.no/swipa2017.
  3. Anderson, M., and M.C.S. Kingsley. 2017. Distribution and abundance of muskoxen (Ovibos moschatus) and Peary caribou (Rangifer tarandus pearyi) on Graham, Buckingham, and southern Ellesmere islands, March 2015. Rangifer 37: 97–114.CrossRefGoogle Scholar
  4. Arthur, S.M., and P.A. Del Vecchio. 2017. Effects of grizzly bear predation on muskoxen in northeastern Alaska. Ursus 28: 81–91.CrossRefGoogle Scholar
  5. Berger, J., B. Buuveibaatar, and C. Mishra. 2013. Globalization of the cashmere market and the decline of large mammals in Central Asia. Conservation Biology 27: 679–689.CrossRefGoogle Scholar
  6. Berger, J., C. Hartway, A. Gruzdev, and M. Johnson. 2018. Climate degradation and extreme icing events constrain like in cold-adapted mammals. Scientific Reports, Nature 8: 1156.  https://doi.org/10.1038/s41598-018-19416-9.CrossRefGoogle Scholar
  7. Bjørkman, A.D., M.G. Criado, I.H. Myers-Smith, V. Ravolainen, I.S. Jónsdóttir, K.B. Westergaard, J. Lawler, M. Aronsson, B. Bennett, H. Gardfjell, S. Heiðmarsson, L. Stewart, and S. Normand. 2020. Status and trends in Arctic vegetation: evidence from experimental warming and long-term monitoring. Ambio.  https://doi.org/10.1007/s13280-019-01161-6.Google Scholar
  8. Blake, J.E., B.D. McLean, and A. Gunn. 1991. Yersiniosis in free-ranging muskoxen on Banks Island, Northwest Territories, Canada. Journal of Wildlife Diseases 27: 527–533.CrossRefGoogle Scholar
  9. Bölter, M., and F. Müller. 2016. Resilience in polar ecosystems: From drivers to impacts and changes. Polar Science 10: 52–59.CrossRefGoogle Scholar
  10. CAFF. 2013. Arctic Biodiversity Assessment. Report for Policy Makers. Conservation of Arctic Flora and Fauna, Akureyri, Iceland.Google Scholar
  11. Campos, P.F., E. Willerslev, A. Sher, L. Orlando, E. Axelsson, A. Tikhonov, K. Aaris-Sørensen, A.D. Greenwood, et al. 2010. Ancient DNA analyses exclude humans as the driving force behind late Pleistocene musk ox (Ovibos moschatus) population dynamics. Proceedings of the National Academy of Sciences of the United States of America 107: 5675–5680.CrossRefGoogle Scholar
  12. Caviezel, C., M. Hunziker, and N. Kuhn. 2017. Bequest of the Norseman—The potential for agricultural intensification and expansion in Southern Greenland under climate change. Land.  https://doi.org/10.3390/land6040087.Google Scholar
  13. CBMP Terrestrial Steering Group. 2015. Arctic Terrestrial Biodiversity Monitoring Plan 2014: Annual report on the implementation of the Circumpolar Biodiversity Monitoring Program’s Arctic Terrestrial Biodiversity Monitoring Plan (CBMP-Terrestrial Plan). CAFF Monitoring Report Nr. 16. CAFF International Secretariat, Akureyri, Iceland. ISBN 978-9935-431-43-1.Google Scholar
  14. Christensen, T., J. Payne, M. Doyle, G. Ibarguchi, J. Taylor, N.M. Schmidt, M. Gill, M. Svoboda, et al. 2013. The Arctic Terrestrial Biodiversity Monitoring Plan. CAFF Monitoring Series Report Nr. 7. CAFF International Secretariat. Akureyri, Iceland. ISBN 978-9935-431-26-4.Google Scholar
  15. Cooley, D., M. Branigan, B. Elkin, S. Kutz, D. Paetkau, and P. Reynolds. 2011. To mix or not to mix: management implication sof expanding muskox populations. Poster presentation at 13th AUC Yellowknife 2011, NWT, Canada.Google Scholar
  16. Davison, T., J. Williams, and J. Adamczewski. 2017. Aerial Survey of Peary Caribou (Rangifer tarandus pearyi) and Muskoxen (Ovibos moschatus) on Banks Island, July 2014. Environment and Natural Resources, Government of the Northwest Territories, Inuvik, NT. Manuscript Report No. 270.Google Scholar
  17. Falk, J.M., N.M. Schmidt, T.R. Christensen, and L. Strøm. 2015. Large herbivore grazing affects the vegetation structure and greenhouse gas balance in a high arctic mire. Environmental Research Letters 10: 045001.CrossRefGoogle Scholar
  18. Forchhammer, M., and D. Boertmann. 1993. The muskoxen Ovibos moschatus in north and northeast Greenland: Population trends and the influence of abiotic parameters on population dynamics. Ecography 16: 299–308.CrossRefGoogle Scholar
  19. Forde, T.L., K. Orsel, R.N. Zadoks, R. Biek, L.G. Adams, S.L. Checkley, T. Davison, J. De Buck, et al. 2016. Bacterial genomics reveal the complex epidemiology of an emerging pathogen in Arctic and Boreal Ungulates. Frontiers in Microbiology.  https://doi.org/10.3389/fmicb.2016.01759.Google Scholar
  20. Gamberg, M., and A.M. Scheuhammer. 1994. Cadmium in caribou and muskoxen from the Canadian Yukon and Northwest territories. Science of the Total Environment 143: 221–234.CrossRefGoogle Scholar
  21. Gordeeva, N.V., T.P. Sipko, and A.P. Gruzdev. 2009. Microsatellite DNA variability in the populations of muskoxen Ovibos moschatus transplanted into the Russian north. Russian Journal of Genetics Genetika 45: 817–825.  https://doi.org/10.1134/s1022795409070096.CrossRefGoogle Scholar
  22. Groves, P. 1997. Intraspecific variation in mitochondrial DNA of muskoxen, based on control-region sequences. Canadian Journal of Zoology 75: 568–575.CrossRefGoogle Scholar
  23. Gunn, A., and J. Adamczewski. 2003. Muskox (Ovibos moschatus). In Wild mammals of North America Biology, Management and Conservation, ed. G.A. Feldhamer, B.C. Thompson, and J.A. Chapman, 1076–1094. Baltimore: Johns Hopkins University Press.Google Scholar
  24. Gunn, A., J. Eamer, P. Reynolds, T.P. Sipko, and A.R. Gruzdev. 2013. Muskoxen. In: Arctic Report Card 2013. https://www.arctic.noaa.gov/reportcard.
  25. Gunn, A. and B. Fournier. 2000. Calf survival and seasonal migrations of a mainland muskox population (File Report No 124). Northwest Territories Department of Resources, Wildlife and Economic Development, Yellowknife, Canada.Google Scholar
  26. Gunn, A., F.L. Miller, and B. McLean. 1989. Evidence for and possible causes of increased mortality of bull muskoxen during severe winters. Canadian Journal of Zoology 67: 1106–1111.CrossRefGoogle Scholar
  27. Gunn, A., and W. Nixon (editors). 2008. Rangifer Health and Body Condition Manual. Report to CircumArctic Rangifer Monitoring and Assessment (CARMA) Network. Retrieved 15 February, 2019, from www.caff.is/images/_Organized/CARMA/Resources/Field_Protocols/RangiferHealthBodyConditionManualforwebe42d.pdf.
  28. Gunn, A., and D. Russell (editors). 2008. Monitoring Rangifer herds (Population dynamics): Manual. Report to CircumArctic Rangifer Monitoring and Assessment (CARMA) Network. Retrieved 15 February, 2019, from www.caff.is/images/_Organized/CARMA/Resources/Field_Protocols/demographymanual42d.pdf.
  29. Handeland, K., T. Tengs, B. Kokotovic, T. Vikøren, R.D. Ayling, B. Bergsjø, and T. Bretten. 2014. Mycoplasma ovipneumoniae - a primary cause of severe pneumonia epizootics in the Norwegian Muskox (Ovibos moschatus) population. PLoS ONE 9: e106116.CrossRefGoogle Scholar
  30. Hansen, C.C.R., C. Hvilsom, N.M. Schmidt, P. Aastrup, P.J. Van Coeverden de Groot, H.R. Siegismund, and R. Heller. 2018. The muskox lost a substantial part of its genetic diversity on its long road to Greenland. Current Biology 28: 1–7.CrossRefGoogle Scholar
  31. Holm, L.E., M.C. Forchhammer, and J.J. Boomsma. 1999. Low genetic variation in muskoxen (Ovibos moschatus) from western Greenland using microsatellites. Molecular Ecology 8: 675–679.CrossRefGoogle Scholar
  32. Jenkins, D., M. Campbell, G. Hope, J. Goorts, and P. McLoughlin. 2011. Recent trends in abundance of Peary Caribou (Rangifer tarandus pearyi) and muskoxen (Ovibos moschatus) in the Canadian Arctic Archipelago, Nunavut. Department of Environment, Government of Nunavut, Wildlife Report No. 1. Pond Inlet, Nunavut. 184 pp.Google Scholar
  33. Jennov, J.G. 1941. Redegørelse vedrørende moskuoksebestanden i Nordøstgrønland. Royal Danish Library, Polar Library, Copenhagen, Denmark. 16 pp. (in Danish).Google Scholar
  34. Jones, P. 2015. Unit 18 muskox. In Muskox management report of survey and inventory activities 1 July 2012–30 June 2014. ed. P. Harper and L.A. McCarthy, Chapter 1, 1–7. Juneau, AK: Alaska Department of Fish and Game, Species Management Report ADF&G/DWC/SMR-2015-2.Google Scholar
  35. Jørgensen, T.J. 2019. Det arktiske guld. Sermitsiaq AG, 19 January 2019, Nuuk, Greenland. (in Danish) https://sermitsiaq.ag/node/210985.
  36. Kafle, P., J. Sullivan, G.G. Verocai, and S.J. Kutz. 2017. Experimental Life-Cycle of Varestrongylus eleguneniensis (Nematoda: Protostrongylidae) in a Captive Reindeer (Rangifer tarandus tarandus) and a Muskox (Ovibos moschatus moschatus). Journal of Parasitology 103: 584–587.CrossRefGoogle Scholar
  37. Kirby, J., and E. Post. 2013. Capital and income breeding traits differentiate trophic match-mismatch dynamics in large herbivores. Physiological Transactions of the Royal society B 368: 20120484.  https://doi.org/10.1098/rstb.2012.0484.CrossRefGoogle Scholar
  38. Kutz, S., T. Bollinger, M. Branigan, S. Checkley, T. Davison, M. Dumond, and K. Orsel. 2015. Erysipelothrix rhusiopathiae associated with recent widespread muskox mortalities in the Canadian Arctic. The Canadian Veterinary Journal 56: 560–563.Google Scholar
  39. Kutz, S.J., S. Checkley, G.G. Verocai, M. Dumond, E.P. Hoberg, R. Peacock, J.P. Wu, K. Orsel, et al. 2013a. Invasion, establishment, and range expansion of two parasitic nematodes in the Canadian Arctic. Global Change Biology 19: 3254–3262.Google Scholar
  40. Kutz, S., J. Ducrocq, C. Cuyler, B. Elkin, A. Gunn, L. Kolpashikov, D. Russell, and R.G. White. 2013b. Standardized monitoring of Rangifer health during International Polar Year. Rangifer 33: 91–114.CrossRefGoogle Scholar
  41. Kutz, S., J. Rowell, J. Adamczewski, A. Gunn, C. Cuyler, O.A. Aleuy, M. Austin, J. Berger, et al. 2017. Muskox Health Ecology Symposium 2016: Gathering to share knowledge on Umingmak in a time of rapid change. Arctic 70: 225–236.CrossRefGoogle Scholar
  42. Lent, P.C. 1999. Muskoxen and their hunters: A History, 324. Norman: University of Oklahoma Press.Google Scholar
  43. Lento, J., J. Culp, W. Goedkoop, K. Christoffersen, E. Fefilova, G. Guðbergsson, P. Liljaniemi, S. Sandøy, et al. 2018. Arctic Freshwater Biodiversity Monitoring Plan: Annual Report 2017 and Work Plan 2018. CAFF Monitoring Report No. 26. CAFF International Secretariat, Akureyri, Iceland, ISBN: 978-9935-431-67-7.Google Scholar
  44. MacPhee, R.D., A.N. Tikhonov, D. Mol, and A.D. Greenwood. 2005. Late Quaternary loss of genetic diversity in muskox (Ovibos). BMC Evolutionary Biology 5: 49.CrossRefGoogle Scholar
  45. Madsen, J., J.H. Williams, F.A. Johnson, I.M. Tombre, S. Dereliev, and E. Kuijken. 2017. Implementation of the first adaptive management plan for a European migratory waterbird population: The case of the Svalbard pink-footed goose Anser brachyrhynchus. Ambio 46: 275–289.CrossRefGoogle Scholar
  46. Marquard-Petersen, U. 1998. Food habits of artic wolves in Greenland. Journal of Mammalogy 79: 236–244.CrossRefGoogle Scholar
  47. Mathiesen, S.D., T. Jørgensen, T. Traavik, and A.S. Blix. 1985. On contagious ecthyma and its treatment in muskoxen. Acta Veterinaria Scandinavica 26: 120–126.Google Scholar
  48. Mech, L.D. 2011. Gray wolf (Canis lupus) movements and behaviour around a kill site and implication for GPS collars studies. Canadian Field-Naturalist 125: 353–356.CrossRefGoogle Scholar
  49. Miller, F.L. 1998. Status of Peary caribou and muskox populations within the Bathurst Island complex, south-central Queen Elizabeth Islands, Northwest Territories, July 1996. Canadian Wildlife Service Technical Report Series No. 317.Google Scholar
  50. Miller, F.L., and S.J. Barry. 2009. Long-term control of Peary caribou numbers by unpredictable, exceptionally severe snow or ice conditions in a non-equilibrium grazing system. Arctic 62: 175–189.CrossRefGoogle Scholar
  51. Miller, F.L., and R.H. Russell. 1975. Aerial surveys of Peary caribou and muskoxen on Bathurst Island, Northwest Territories, 1973 and 1974. Progress Notes, Canadian Wildlife Service 44: 1–8.Google Scholar
  52. Mod, H.K., and M. Luoto. 2016. Arctic shrubification mediates the impacts of warming climate on changes to tundra vegetation. Environmental Research Letters 11: 124028.CrossRefGoogle Scholar
  53. Mosbacher, J.B., D.K. Kristensen, A. Michelsen, M. Stelvig, and N.M. Schmidt. 2016. Quantifying muskox biomass and nitrogen removal and deposition in a High tundra ecosystem. Arctic, Antarctic, and Alpine Research 48: 229–240.CrossRefGoogle Scholar
  54. Mosbacher, J.B., A. Michelsen, M. Stelvig, H. Hjermstad-Sollerud, and N.M. Schmidt. 2018. Muskoxen modify plant abundance, phenology, and nitrogen dynamics in a High Arctic fen. Ecosystems.  https://doi.org/10.1007/s10021-018-0323-4.Google Scholar
  55. Mosbech, A., K.L. Johansen, T.A. Davidson, M. Appelt, B. Grønnow, C. Cuyler, P. Lyngs, and J. Flora. 2018. On the crucial importance of a small bird: The ecosystem services of the little auk (Alle alle) population in Northwest Greenland in a long-term perspective. Ambio 47: 226–243.  https://doi.org/10.1007/s13280-018-1035-x.CrossRefGoogle Scholar
  56. Murray, J.L. 1991. Biomass allocation and nutrient pool in major muskoxen-grazed communities in Sverdrup Pass (75°N), Ellesmere Island, N.W.T. MS Thesis. Toronto, Canada: University of Toronto.Google Scholar
  57. Myers-Smith, I.H., B.C. Forbes, M. Wilmking, M. Hallinger, T. Lantz, D. Blok, K.D. Tape, M. Macias-Fauria, et al. 2011. Shrub expansion in tundra ecosystems: Dynamics, impacts and research priorities. Environmental Research Letters 6: 045509.  https://doi.org/10.1088/1748-9326/6/4/045509.CrossRefGoogle Scholar
  58. Parker, G.R., D. C. Thomas, E. Broughton, and D. R. Gray. 1975. Crashes of muskox and Peary caribou populations in 1973–74 on the Parry Islands, Arctic Canada. Progress Notes, Canadian Wildlife Service 56:1–10.Google Scholar
  59. PISUNA. 2014. Lokal dokumentation og forvaltning af de levende ressourcer: Vejledning til brugere. Piniakkanik Sumiiffinni Nalunaarsuineq. Greenland Self-Rule. January. (in Danish/Greenlandic).Google Scholar
  60. Post, E., M.C. Forchhammer, M.S. Bret-Harte, T.V. Callaghan, T.R. Christensen, B. Elberling, A.D. Fox, O. Gilg, et al. 2009. Ecological dynamics across the Arctic associated with recent climate change. Science 325: 1355–1358.CrossRefGoogle Scholar
  61. Post, E., and C. Pedersen. 2008. Opposing plant community responses to warming with and without herbivores. Proceedings of the National Academy of Sciences 105: 12353–12358.CrossRefGoogle Scholar
  62. Putkonen, J., T.C. Grenfell, K. Rennert, C. Bitz, P. Jacobson, and D. Russell. 2009. Rain on Snow: Little Understood Killer in the North. Eos, Transactions American Geophysical Union 90: 221–222.CrossRefGoogle Scholar
  63. Raghavan, M., M. DeGiorgio, A. Albrechtsen, I. Moltke, P. Skoglund, T.S. Korneliussen, B. Gronnow, M. Appelt, et al. 2014. The genetic prehistory of the New World Arctic. Science 345: 1255832.Google Scholar
  64. Raponi, M., D.V. Beresford, J.A. Schaefer, I.D. Thompson, P.A. Wiebe, A.R. Rodgers, and J.M. Fryxell. 2018. Biting flies and activity of caribou in the boreal forest. Journal of Wildlife Management 82: 833–839.CrossRefGoogle Scholar
  65. Reynolds, P.E. 1998. Dynamics and range expansion of a reestablished muskox population. Journal of Wildlife Management 62: 734–744.CrossRefGoogle Scholar
  66. Reynolds, P.E. 2011. 2011 pre-calving census of muskoxen in Arctic National Wildlife Refuge 26C and adjacent regions. U.S Fish and Wildlife Refuge, Arctic National Wildlife Refuge report. Fairbanks, Alaska.Google Scholar
  67. Reynolds, P.E., H.V. Reynolds, and R.T. Shideler. 2002. Predation and multiple kills of muskoxen by grizzly bears. Ursus 13: 789.Google Scholar
  68. Rockwood, L.L. 2015. Introduction to population ecology, 2nd ed. New Jersey: Wiley-Blackwell.Google Scholar
  69. Ruscio, B.A., M. Brubaker, J. Glasser, W. Hueston, and T.W. Hennessy. 2015. One Health—a strategy for resilience in a changing arctic. International Journal of Circumpolar Health 74: 27913.CrossRefGoogle Scholar
  70. Salisbury, C.D.C., A.C.E. Fesser, J.D. Macneil, J.R. Patterson, J.Z. Adamczewski, P.F. Flood, and A. Gunn. 1992. Trace metal and pesticide levels in muskoxen from Victoria Island, Northwest Territories, Canada. International Journal of Environmental Analytical Chemistry 48: 209–215.CrossRefGoogle Scholar
  71. Schmidt, N.M., S.H. Pedersen, J.B. Mosbacher, and L.H. Hansen. 2015. Long-term patterns of muskox (Ovibos moschatus) demographics in High Greenland. Polar Biology 38: 1667–1675.CrossRefGoogle Scholar
  72. Schmidt, N.M., F.M. van Beest, J.B. Mosbacher, M. Stelvig, L.H. Hansen, and C. Grøndahl. 2016. Ungulate movement in an extreme seasonal environment: Year-round movement patterns of high-arctic muskoxen. Wildlife Biology 22: 253–267.CrossRefGoogle Scholar
  73. Sturm, M., C. Racine, and K. Tape. 2001. Climate change: Increasing shrub abundance in the Arctic. Nature 411: 546–547.CrossRefGoogle Scholar
  74. Tape, K.D., B.M. Jones, C.D. Arp, I. Nitze, and G. Grosse. 2018. Tundra be dammed: Beaver colonization of the Arctic. Global Change Biology 24: 4478–4488.CrossRefGoogle Scholar
  75. Tener, J.S. 1960. A study of the muskox (Ovibos moschatus) in relation to its environment. PhD Thesis. Vancouver, Canada: Department of Zoology, University of British Columbia.Google Scholar
  76. Tener, J.S. 1965. Muskoxen: A biological and taxonomic review. Canadian Wildlife Service Monograph Serial Number 2. Department of Northern of Affairs and Natural Resources, Ottawa, Canada.Google Scholar
  77. Thulin, C.G., L. Englund, G. Ericsson, and G. Spong. 2011. The impact of founder events and introductions on genetic variation in the muskox Ovibos moschatus in Sweden. Acta Theriologica 56: 305–314.CrossRefGoogle Scholar
  78. Tomaselli, M., C. Dalton, P.J. Duignan, S. Kutz, F. van der Meer, P. Kafle, O. Surujballi, C. Turcotte, et al. 2016. Contagious Ecthyma, Rangiferine Brucellosis, and Lungworm infection in a Muskox (Ovibos moschatus) from the Canadian Arctic, 2014. Journal of Wildlife Diseases 52: 719–724.CrossRefGoogle Scholar
  79. Tomaselli, M., C. Gerlach, S. Kutz, S. Checkley, and the community of Iqualuktutiaq. 2018a. Iqaluktutiaq Voices: Local Perspectives about the Importance of Muskoxen, Contemporary and Traditional Use and Practices. Arctic 71: 1–14.CrossRefGoogle Scholar
  80. Tomaselli, M., S. Kutz, C. Gerlach, and S. Checkley. 2018b. Local knowledge to enhance wildlife population health surveillance: Conserving muskoxen and caribou in the Canadian Arctic. Biological Conservation 217: 337–348.CrossRefGoogle Scholar
  81. van Coeverden de Groot, P.J. 2001. Conservation Genetic Implications of Microsatellite Variation in the Muskox Ovibos moschatus: the Effect of Refugial Isolation and the Arctic Ocean on Genetic Structure. PhD Thesis. Kingston, Ontario, Canada: Queen’s University.Google Scholar
  82. Walker, M.D., C.H. Wahren, R.D. Hollister, G.H. Henry, L.E. Ahlquist, J.M. Alatalo, and H.E. Epstein. 2006. Plant community responses to experimental warming across the tundra biome. Proceedings of the National Academy of Sciences 103: 1342–1346.CrossRefGoogle Scholar
  83. Ytrehus, B., T. Bretten, B. Bergsjø, and K. Isaksen. 2008. Fatal pneumonia epizootic in musk ox (Ovibos moschatus) in a period of extraordinary weather conditions. EcoHealth 5: 213–223.CrossRefGoogle Scholar
  84. Ytrehus, B., R.K. Davidson, and K. Isaksen. 2015. Single causative factor for severe pneumonia epizootics in muskoxen? EcoHealth 12: 395–397.CrossRefGoogle Scholar

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© The Author(s) 2019

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Christine Cuyler
    • 1
    Email author
  • Janice Rowell
    • 2
    Email author
  • Jan Adamczewski
    • 3
  • Morgan Anderson
    • 4
  • John Blake
    • 5
  • Tord Bretten
    • 6
  • Vincent Brodeur
    • 7
  • Mitch Campbell
    • 8
  • Sylvia L. Checkley
    • 9
  • H. Dean Cluff
    • 10
  • Steeve D. Côté
    • 11
  • Tracy Davison
    • 12
  • Mathieu Dumond
    • 13
  • Barrie Ford
    • 14
  • Alexander Gruzdev
    • 15
  • Anne Gunn
    • 16
  • Patrick Jones
    • 17
  • Susan Kutz
    • 9
  • Lisa-Marie Leclerc
    • 18
  • Conor Mallory
    • 19
  • Fabien Mavrot
    • 9
  • Jesper Bruun Mosbacher
    • 9
  • Innokentiy Mikhailovich Okhlopkov
    • 20
  • Patricia Reynolds
    • 21
  • Niels Martin Schmidt
    • 22
  • Taras Sipko
    • 23
  • Mike Suitor
    • 24
  • Matilde Tomaselli
    • 25
  • Bjørnar Ytrehus
    • 26
  1. 1.Greenland Institute of Natural ResourcesNuukGreenland
  2. 2.School of Natural Resources and ExtensionUniversity of Alaska FairbanksFairbanksUSA
  3. 3.Wildlife DivisionEnvironment and Natural Resources, Government of Northwest TerritoriesYellowknifeCanada
  4. 4.BC Ministry of Forests, Lands, Natural Resources Operations and Rural DevelopmentPrince GeorgeCanada
  5. 5.Animal Resources CenterUniversity of Alaska FairbanksFairbanksUSA
  6. 6.Norwegian Environment AgencyTrondheimNorway
  7. 7.Department of Wildlife Management of Northern QuébecMinistry of Forests, Wildlife and Parks of QuébecChibougamauCanada
  8. 8.Department of EnvironmentGovernment of NunavutArviatCanada
  9. 9.Department of Ecosystem and Public Health, Faculty of Veterinary MedicineUniversity of CalgaryCalgaryCanada
  10. 10.Environment and Natural Resources, Government of the Northwest TerritoriesYellowknifeCanada
  11. 11.Département de biologie & Centre for Northern StudiesUniversité LavalQuébecCanada
  12. 12.Department of Environment and Natural ResourcesWildlife ManagementInuvikCanada
  13. 13.Umingmak Productions Inc.KugluktukCanada
  14. 14.Nunavik Research CentreMakivik CorporationKuujjuaqCanada
  15. 15.Wrangel Island State ReservePevekRussia
  16. 16.Salt Spring IslandCanada
  17. 17.Division of Wildlife ConservationAlaska Department of Fish and GameBethelUSA
  18. 18.Department of EnvironmentGovernment of NunavutKugluktukCanada
  19. 19.Department of EnvironmentGovernment of NunavutIglulikCanada
  20. 20.Institute of Biological Problems of Cryolithozone of the Siberian Branch of Russian Academy of Science (IBPC SB RAS)YakutskRussia
  21. 21.FairbanksUSA
  22. 22.Arctic Research Centre, Department of BioscienceAarhus UniversityRoskildeDenmark
  23. 23.Severtsov Institute of Ecology and EvolutionRussian Academy of SciencesMoscowRussia
  24. 24.Inuvialuit and Migratory CaribouFish and Wildlife, Environment YukonDawson CityCanada
  25. 25.Polar Knowledge Canada, Canadian High Arctic Research StationCambridge BayCanada
  26. 26.Norwegian Institute for Nature Research (NINA)TrondheimNorway

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