Why musk deer is endangered

Around 6 months of age, young Himalayan musk deer are weaned and able to consume food from their surroundings, becoming completely independent.

Young deer become sexually mature by 16 to 24 months of age. Parental investment is minimal in Himalayan musk deer. Young deer nurse from their mothers when necessary but otherwise stay in hiding, unaccompanied by either parent.

Himalayan musk deer typically live for 10 to 14 years in the wild. Nyambayar, et al. Himalayan musk deer are solitary, terricolous creatures that usually try to conceal themselves in vegetation. They are primarily active during the morning and evening hours, often when feeding. Himalayan musk deer have a distinctive bounding gait. They can jump as far as 6 m, which is advantageous when being chased by slower predators.

Some cervids , including the Himalayan musk deer, tend to designate certain areas as latrines, choosing a spot used only for deification. They urinate elsewhere. Although the reason for this behavior is unknown, it is increasingly practiced during the mating season. Himalayan musk deer are sedentary, occupying small home ranges of up 0. Male Himalayan musk deer are quite territorial of other males and fight those which attempt to enter their territory.

Members of this species are thought to use latrine sites and other strong-smelling secretions to mark their territory. Green, ; "Himalayan musk deer Moschus moschiferus moschiferus ", Himalayan musk deer have a highly acute sense of smell. As a result, males mark their territories by rubbing their caudal gland against vegetation. This secretion also deters rivals during the breeding season. Himalayan musk deer make a double hiss sound when alarmed and may even scream when wounded.

They are also alerted danger through their good sense of hearing. Himalayan musk deer are herbivores and feed on what is seasonally available. Accordingly, they eat grasses, forbs, mosses, lichen, twigs, shoots, and plant leaves. They are ruminants, so they can quickly leave feeding grounds if threatened and further digest their food at a later time when safe from harm. Occasionally, Himalayan musk deer travel great distances at night to forage for food. They may travel 3 to 7 km per night, but they always return to their usual territories by daybreak.

Himalayan musk deer attempt to conceal themselves within vegetation to avoid predators. The dull brown color of their coats minimizes their chance of detection. Predators include leopard , lynx , yellow-throated marten , red fox , grey wolf , wild dogs, and humans.

Large birds of prey also occasionally kill young musk deer. In contrast to these prior studies, we did a number of things to ensure our occurrence records and habitat analyses produced high quality data. First, we used recent genetic analysis 35 , 38 , 39 to confirm the populations of Kashmir musk deer and Himalayan musk deer in southern parts of the greater Himalaya.

Second, we obtained distributional data of KMD by systematically surveying five protected areas in Nepal, three in India, and one in Pakistan between and Third, we searched for the locations of musk deer latrines which are set up only in high quality habitat.

The deer uses latrine sites regularly throughout the year for defecation, for establishing communications with conspecifics, and to maintain territory 35 , Based on their unique location and repeated use, we suggest that latrine sites represent high quality habitat sites for musk deer, which is in contrast with opportunistic sightings which can capture low quality habitat in the data and unverified locations when analysis is based on occurrence records maintained by public domain like GBIF.

In this study, we modelled the distribution of the least studied endangered Kashmir musk deer with the following objectives: 1 understand the current and expected future distribution of the species under different climatic scenarios, 2 identify potential climatic refugia for the species, and 3 determine the adequacy of the existing network of protected areas for protecting this species in future. Out of 22 selected covariates, we selected for species distribution modeling, four were found to have disproportionately high influence in determining the distribution of the KMD Fig.

The relative influence of the predictors in Kashmir musk deer distribution; predictors are listed on y-axis. We started our model construction process with 26 potential predictors Table 1. However, four of these covariates land cover, aspect, altitude and distance to the nearest water source were not available for future climate scenarios at our desired spatial resolution or required enormous computational resources. The remaining 22 predictors Table 1 were used to develop the model.

The prediction of the species distribution models yielded probability of occurrence or habitat suitability Fig. However, the suitable habitats do not occur in a continuum throughout the high Himalaya.

Suitable habitats are located west of Annapurna Himalaya range including Mustang hereafter Annapurna region , west of Annapurna region hereafter, west Nepal , the northern part of Uttarakhand state of India hereafter, Uttarakhand , west of Uttarakhand in Himachal Pradesh hereafter Himachal , the Kashmir region of India and Pakistan hereafter, Kashmir region , and along and close to the northeast border between Pakistan and Afghanistan hereafter, Pak-Afghan border.

Additionally, small patch of suitable habitat observed in Lubu area in China nearby north west border between Nepal and China. Few patches of suitable habitat occur in the the eastern half of Nepal and their adjacent area in Tibet as this area supports the closely related Himalayan musk deer.

Habitat suitability is displayed as a continuous quantity between zero and one. The probability surface was generated by species distribution models built with Maximum Entropy MaxEnt Models using R 3.

The continuous patches of high quality habitat are located in Pak-Afghan border, Kashmir region, Uttarakhand and in Annapurna region. In other regions Himachal, west Nepal, west of Kashmir region suitable habitats are presented in different fragments. The areas where suitable and highly suitable habitats are presented also include marginally suitable habitat 0. When predicted distribution under future climate change scenarios are examined collectively, northwards shifting and disappearance of habitat were observed.

In west Nepal and Uttarakhand, the habitat shifts northward, resulting a continuous distribution of highly suitable habitats in north part of both areas west Nepal and Uttarakhand and their adjacent areas in Tibet in future in all four RCP scenarios in s and s.

However, the extent of suitable habitat will differ in four scenarios. In s RCP 2. In RCP 2. In RCP 4. In all four scenarios during s, the suitable habitat from Pak-Afghan border, Kashmir region and Himachal region will disappear. In the Pak-Afghan border, Pakistan, Kashmir region, and central Nepal regions only marginally suitable are predicted to be present in future during s and s Fig.

Estimated habitat suitability in and under various climate change scenarios. The prediction was made for the entire Himalaya see Fig. All maps were plotted using R 3. By , habitat in RCP 4. The habitat in RCP 2. RCP 4. RCP 2. Except in 8. More habitat is expected to be available for KMD in Uttarakhand, west Nepal and their associated areas in Tibet in future.

Change in area of suitable habitats in future. The total area of all three types of suitable habitats was computed for all climate scenarios: RCP 2.

A small fraction of KMDs range now or likely in the future Fig. If a site provides current and predicted future suitability, it carries higher conservation value because it could serve the purpose of a climate refugia potentially allowing that local population of KMD from needing to migrate to survive.

Fraction of the projected species range that is inside currently designated protected areas. This fraction was computed as the area of the range inside a protected areas divided by the total range area. Climate refugia and protected areas. Climate refugia are assumed to occur where the current species range overlaps with the predicted future range.

Spatial distributions of climate refugia for s a and for s b under RCP 8. Next to each of these maps are two pie charts that display what fraction of the species current range remains as a potential climate refugia red pie and the fraction of that climate refugia that is located inside protected areas green pie.

The growth limiting factor for the species of trees in KMD Kashmir Musk Deer habitat is the moisture available during the pre-monsoon season 43 , 44 , 45 , 46 , In the southern Himalaya, moisture comes from precipitation arising from the Indian Ocean mainly during summer, making high rainfall in the eastern Himalaya leaving the western Himalaya drier than eastern Himalaya. During winter, the westerly winds from the Mediterranean sea brings more precipitation in the form of snow to the western Himalaya, but less to the eastern Himalaya The massive mountain range acts as a barrier to air flow from south to north, resulting in a dry and treeless Tibet Most of the coniferous trees respond negatively with temperature when temperature increase above 6.

Spruce Picea smithiana , fir Abies pindrow , yew Taxus wallichiana , bluepine Pinus wallichiana , Himalayan birch Betula utilis and rhododendron Rhododendron campanulatum etc. Growth of these trees are limited by moisture in pre-monsoon 43 , 44 , 45 , Our finding also suggests that Himalayan trees are more responsive to changes in the regime of precipitation than temperature. The strong influence of precipitation to KMD distribution likely results from the sensitivity of forests supporting KMD sites to adequate rainfall.

The distributional boundaries we predicted are echoed by recent studies: Singh et al. West Nepal, Uttarakhand, Kashmir region, and Pak-Afghan border will support highly suitable and suitable habitat.

Although temperature will keep rising, precipitation is predicted to behave differently depending on the amount of moisture in the air, where it comes from, and the convergence of air currents 55 , In the range of KMD, sites that are unsuitable today to the north of Uttarakhand and western Nepal will receive more pre-monsoon moisture in future see Supplementary Note. This explains why those currently uninhabited areas show a suitable sites in future climates Fig.

Not surprisingly this huge area and its diverse topography manifests in a very complex climate system that is not well understood This distinct dynamism of temperature and precipitation due to geographical differences between the western regions Kashmir and Pak-Afghan and the eastern region Uttarakhand and west Nepal are enough to justify the reason behind loss of habitat of KMD west of Uttarakhand Kashmir region, Afghanistan and Pakistan in future s and s.

Contrary to our finding, Khadka et al. Therefore, Khadka et al. The unrealistic future projection of musk deer by Khadka et al. Collectively, these lines of arguments and evidences support our finding that current species range of KMD will respond to future climate in a complex fashion, which is different from a species that is primarily controlled by temperature. We show that all kinds of habitats in Kashmir region, Himachal and Pak-Afghan border will be the ones showing the first sign of climate change; they will decline in the s and s.

There are a few reasons why prior modeling studies e. Pelage color is not a reliable metric for identifying species of musk deer. Pelage color may vary within a species and it changes with season. Different species can look alike as well as individuals of the same might look different Fecal pellets are not uniquely identified at a species level.

Occurrences based on opportunistic sightings and anecdotal information has the potential to hamper the model as such occurrences have a higher chance of being incorrect or falling in lower quality habitat than our systematic survey of latrines. Khadka et al. In water scarce environments, a small difference in moisture availability can make a difference in habitat quality. Such ecological expectations can also be inferred from the fact that forest cover is an important factor to KMD given their timid nature 30 and vegetation growth is largely influenced by moisture in dry environments 60 , 61 , 62 , 63 , Large portions of the suitable habitat of musk deer are located outside PAs where anthropogenic pressure are highly threatening biodiversity 65 , Musk deer evolved 4 million years ago in Tibetan plateau 67 and survived until now despite various climate changes during the Quaternary period as well as after remarkable geological process in Asia including upliftment of Himalaya 68 , Climatic refugia are a plausible explanation for its survival through different climate changes, allowing the species later to disperse in the mountains of Asia when situation slowly normalized.

Another plausible explanation for the survival relates to the ability of a species to cope with the changing environment and its interaction with other species. Unfortunately, the velocity of the climate change is faster than the response of the species is Therefore, the role of climate refugia is always crucial.

The extinction of megafauna, such as woolly mammoth Mammuthus primigenius and Giant deer Megaloceros giganteus during the late Quaternary period was mainly because they could not find such refugia to survive through the glacial-interglacial cycle In the case of KMD, about quarter of the current range can serve as climate refugia in future s and s. These refugia are situated in Uttarakhand, west Nepal and west of Annapurna region.

The greater Himalaya are often called the roof of the world and they extend from northern Pakistan to north east India throughout Nepal, Bhutan and the southern part of Tibet. Western disturbances from the west arise from the Mediterranean Sea and dominate the climate of western Himalaya during winter. During summer, the dominant weather pattern is driven by moisture arising from the Indian Ocean 48 , 72 , In Uttarakhand and west Nepal, the climate is different than Kashmir and Pak-Afghan as it is influenced by both south west monsoon and westerly storms The different weather phenomena in western and eastern Himalaya has resulted in a drier west and wetter east Hence, species composition are different in both regions of Himalaya.

Western Himalaya temperate forests exhibits both broadleaf and conifer forest where spruce Picea smithiana , fir Abies pindrow , yew Taxus wallichiana , bluepine Pinus wallichiana and rhododendron Rhododendron campanulatum are common species.

In eastern Himalaya, eastern Himalayan broadleaf forests, eastern Himalaya subalpine conifer foersts, northern trinagle temperate forests and northeastern Himalayan subalpine conifer forests form temperate forest 76 , 77 , Western tragopan Trogopan melanocephalus , cheer pheasant Catreus wallichii , Kashmir musk deer M.

Following the genetic study of the samples collected in the Nuristan region of Afghanistan and the Mustang region of Annapurna Himalaya range in Nepal Singh et al. We determined the geographic coordinates of latrines between these two distribution limits of KMD in South Asia. In total, we collected 45 latrine samples in Nepal, 61 in India, 21 in Pakistan, and 9 in Afghanistan Fig.

Latrines, which serves as an indisputable evidence of deer presence, can easily be distinguished from the excreta of other animals; they have the heaps of old and fresh pellets with a musky smell 42 , 79 , 80 , 81 , and the pellets are much smaller and cylindrical compared to that of goat Capra aegagrus and sheep Ovis aries.

Musk deer are shy, nocturnal and crepuscular forest-dweller species During the day, they hide in vegetation. Hence, musk deer are mostly inconspicuous to human. However, musk deer develop latrines by defecating repeatedly at a single site to maintain communication for various proposes 81 , 83 , Geographical locations of latrine sites were determined first in Mustang, Nepal.

Occurrence records from remaining four protected areas of Nepal were collected by random sightings of latrine sites and animals by the game scouts and rangers working in each protected area. For India and Pakistan, we used a retrospective study design.

Coordinates of latrine sites systematically collected for Alpine musk deer from Uttarakhand, India and from Pakistan by co-author of this paper from to were considered to be KMD instead of Alpine musk deer. Data in Pakistan were collected from systematically distributed quadrats. Additionally, published literature was reviewed and presence locations of musk deer from Afghanistan and Dachigam National Park, Kashmir region, India were extracted by scanning and georeferencing previously produced range maps Fig.

Based on our understanding of the distribution and ecology of KMD, we supplemented this standard set of potential covariates with additional relevant variables Table 1. In total, 26 covariates were applied to the first set of models.

Our initial modeling exercise indicated that several of these covariates secured a very low variable importance. Some of these minimally important covariates also had other problems. This turned out to be computationally intensive. We also adapted filter i. This approach was useful in optimizing the model coefficients such that a more stable model is trained. Specifically, we tested spatial transferability of the models by comparing various model evaluation metrics 86 , 87 , The goal here is to find a model that performs in both training and testing regions similarly.

With various regularization multipliers, we found that a value of 2 minimizes the delta AIC difference in AIC of the models in training vs testing regions. Finally, we selected 22 variables for processing our model to understand present distribution of the KMD. Because these cookies are strictly necessary to deliver the website, refuseing them will have impact how our site functions.

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We compared the images of musk deer taken by the first author of this paper from the Mustang, Annapurna Conservation Area hereafter Mustang in November Additionally, we also analyzed photographs of the skin and carcasses confiscated from poachers by the ACA office, Mustang.

Contrasting evidence of musk deer from Mustang Fig. We also examined the fresh pellets of musk deer from the Kaski area Fig. Mustang is located in west, Manang in the east and Kaski in the south of Annapurna Himalayas range. Photographs of unidentified musk deer from Mustang, Nepal. Different pelage color of Himalayan musk deer captured by camera traps in Manang, Annapurna Conservation Area, Nepal during summer and winter.

Species in the genus Moschus are cold-adapted large herbivores occurring commonly at higher elevations in central Asia mountains. Because of their cold and high-altitude adaptations to specialized habitat requirements, they are a unique group to make attractive grouping for taxonomic status evaluation. At present seven species of musk deer; Anhui musk deer M. Three species; Alpine musk deer, Himalayan musk deer and black musk deer have so far been reported from the Nepal 11 , 12 , However, these records are primarily based on earlier observations from neighboring Uttarakhand, India and the Tibet Autonomous Region of China hereafter Tibet from presence-only surveys or from anecdotal information 8.

Cryptic species like musk deer are extremely difficult to identify using only morphological information. With the advancement of molecular technology in taxonomic research, identifying cryptic taxa has become easier Six out of the seven species of musk deer have been distinguished in China based on molecular technologies These technologies are not yet widely applied in south Asia, especially in the Himalayas.

Recently, with the introduction of molecular methods in taxonomic studies, several species of fauna have been discovered or re-described from the Nepal Himalaya 16 , 17 , 18 , 19 , From the beginning, our study based on mtDNA indicated that there was discovering a new species of musk deer from Mustang. Our preliminary analysis of the sequence of cytochrome b Cytb sequences from the fresh pellets of musk deer collected from Mustang showed different clades compared to the samples at Manang and Kaski.

Our excitement increased when the genetic sequence of musk deer from Mustang did not match the genetic sequence of six other known species of musk deer: Anhui musk deer, forest musk deer, alpine musk deer, black musk deer, Himalayan musk deer hereafter HMD , and Siberian musk deer.

However, there was still one species of musk deer that remained to be compared, that was Kashmir musk deer hereafter KMD. KMD is the only recorded species of musk deer from Kashmir and surrounding regions of India, Pakistan, and Afghanistan and it is also the least known musk deer species 9 , A scenario was developing indicating that the species found in Mustang could be a new species of the musk deer because of its distinct morphological characteristics and the sizeable geographical distance between Mustang, Nepal and Kashmir, India.

Further, recent studies of musk deer from southern parts of Himalaya including Nepal suggested a possibility of new species 22 , 23 , After we gathered all the preliminary evidences, our team started to follow the deer and setting camera traps on the latrine sites and collecting fresh pellets samples. By using this approach, we hoped to understand genetics of the musk deer found in Mustang and Manang. Here, we describe the presence of M. The aligned dataset of Cytb sequence contained a branch points sequence bps including variable sites and 68 parsimony informative sites, and a total of 12 unique haplotypes 4 Cytb haplotypes from Mustang, 6 from Manang and 2 from Ghandruk.

Molecular data analysis suggests that the population of musk deer in Mustang is genetically similar to the KMD sample collected from Nuristan, Afghanistan and nested together in a BI Bayesian Inference tree Fig. The uncorrected genetic divergence of the Cytb gene sequences between musk deer population of Mustang, Nepal and Nuristan, Afghanistan was 0.

The genetic divergences between M. Whereas, the maximum genetic difference of M. Similarly, the uncorrected genetic divergence in the Cytb gene sequences between musk deer population of M.

Based on these phylogenetic results, the musk deer populations of the eastern ACA represent Himalayan musk deer M. All three phylogenetic trees Figs 3 and S1 , S2 showed that M.

Similarly, analysis from all three phylogenetic trees indicated that M. These results show a clustering of musk deer species indicating that M. Sample names correspond to those given in Table 1. For clarity, branches that representing individuals with the same taxonomic unit were collapsed. Grey triangles refers to M. At latrine sites, we recorded musk deer in every camera because musk deer visit their latrine sites to defecate and to mark their territories for establishing chemical communications.

We recorded a total of 53 photographs 27 of males and 26 of female , including 15 one-minute video in Mustang, 22 images and 7 one-minute videos from Lubra and 31 images and 8 one-minute video from Marpha. Most of the videos and images were captured at dusk, night or dawn. We used 14 images 8 of males and 6 of females and 4 one-minute videos 1 of a male and 3 of females which were captured in daylight in Mustang in the analysis.

A total one-minute videos and photographs were collected from trail cameras set in Manang to study behavior at latrine sites. Of these, 20 images 12 of males and 8 of females and two one-minute videos 1 of a male and 1 of a female were used to identify pelage color.

All of the images and videos from Manang and Mustang were taken between hrs. These photographs had similar patterns of light and were free of tree shadows. These two species had very different pelage coloration which were highly variable in pelage color compared to each other. The KMD had a distinctive pelage color compared to all other musk deer species Table 2.

It has a white color patch running from chin to chest; a black spot on the throat; light brown nape; a light copper colored dorsal surface of the trunk and vaguely spotted; lower parts of the limbs are white; front inner edge of the thigh and rump are predominantly black; and the ears outside are grey-black tipped with white.

It lacks white patches on the neck, and only the juveniles were vaguely spotted Table 2. The images of musk deer from summer May-July depicted brown color and black color in winter October-November Moreover, some images showed light white patches on the neck Supplementary Fig S3. KMD from Mustang had a light copper color on the dorsal surface and white patches on the neck. Dorsal surfaces of individuals from both species were vaguely spotted and the lower parts of the limps were white Fig.

Previous studies related to habitat and ecology of musk deer from the southern part of the high Himalayas in Nepal, India, and Pakistan 8 , 11 , 12 , 25 , 26 , 27 , 28 , 29 have misidentified the Kashmir musk deer as alpine musk deer. All of the studies previously conducted in ACA have also considered the species of study to be alpine musk deer 8 , 30 , The potential misidentification of musk deer is directly partially due to its behavior.

Musk deer are extremely shy and nocturnal and therefore, are hard to detect directly 2. However, observing musk deer in daylight is difficult because they hide in shrub understory during the day When musk deer are encountered in the forest, they are generally only seen for a few seconds, or only the sound of leaps or escape through bushes can be heard.

Green et al. Sathyakumar and Vinod and Sathyakumar sighted musk deer 92 and 65 times respectively during their three year study of musk deer in India. Taxonomic classification of Moschus has remained controversial throughout the range of musk deer and until now unresolved for four decades because these highly cryptic species are extremely difficult to identify reliably using only morphological characters 33 , 34 , 35 , Even under the best conditions, alpine musk deer, Siberian musk deer, and forest musk deer cannot be distinguished by morphology, biogeography or ecological criteria Three species; Anhui musk deer, forest musk deer and black musk deer can easily be confused with each other because of their similar morphology and pelage color.

Often, these species are considered sub-species either of alpine musk deer, Siberian musk deer or forest musk deer 35 , 38 , Recent genetic studies have confirmed that these species are different species of musk deer 15 , Guo et al. Before genetic study, Anhui musk deer was considered as sub-species of Siberian musk deer Pelage color may or may not vary among different species. Pelage may even be different within individuals of any species of musk deer throughout different seasons 23 , Investigation of the images captured during this study also showed that different pelage colors in different individuals of HMD and KMD.

The reason that earlier researchers misidentified musk deer species in Nepal including in ACA was that they were able to rely on observations of pelage color and morphology. Although, molecular studies on musk deer have been conducted from their distribution ranges in China 15 , 22 , 23 , 24 , 38 , 40 this is the first molecular study of musk deer from the southern parts of Himalayas. This study established KMD as a new species recorded in Nepal from Mustang as well as genetically validating it as a distinct species.

The Mustang area within the Kaligandaki river gorge and the Annapurna -Dhaulagiri Himalayan range within ACA have likely isolated population of musk deer species in the southern slopes of the Himalaya Fig. The Mustang valley lies on the southern margin of the Tibetan Plateau and on the leeward side of the high Himalayas.

To the north, dry habitat in the rain shadow area on the north side of the valley may have prevented the dispersion of musk deer in Tibet. Geographical barriers; such as mountains, rivers, and gorges obstruct gene flow and lead to genetic differentiation of naturally isolated populations 43 , 44 , The southern Himalaya, west of Mustang receive active winter precipitation from the Mediterranean while summer precipitation dominates east of Mustang 46 , This different precipitation pattern may have resulted in adaptation to different vegetation and climate conditions resulting in the evolution of two distinct species; KMD to the west and HMD to the east of the Annapurna Himalayas and Kaligandaki gorge.

The map was plotted using ArcGIS The western distribution of KMD is up to Nuristan, northeast Afghanistan 9 while the eastern distribution was assumed to be the Kashmir region in India. It suggests that the species of musk deer found in between the two extreme limits in the northern Himalayas of India, Pakistan, and western Nepal must be KMD, though previously they have been identified as alpine musk deer.

A recent genetic study by Guo et al.