Research on population structure and behavior of musk deer has been conducted on defined areas within Sikhote-Alin Reserve (Russian Far East) since 1974 using a combination of techniques (snowtracking, visual observation, and radiotracking since 2012). We have acquired previously unknown data on the structure of the overall population and sub-groups, home range size, sex and age-related differences in habitat use, inheritance of home ranges and territories between generations, mechanisms regulating distribution of individuals and population structure. This knowledge is extremely valuable in understanding recent population declines of musk deer associated with habitat destruction, unregulated hunting and natural cycles in population size.
Musk deer; Moschus moschiferus; Sikhote-Alin Reserve; Home range; Population structure
The main habitats of musk deer (Moschus moschiferus) are confined to mountain taiga forests with notable presence of dark coniferous species. Musk deer feeds on over 150 species of plants; however a significant part of its diet consists of epiphytic foliose lichen of Parmeliceae family (Usnea, Evernia, Bryoria etc.) which influences the distribution of the population ( Zaitsev, 1991 and Zaitsev, 2006). Musk deer is of great importance in the functioning of ecological relationships with predators (lynx Lynx lynx, yellow-throated marten Martes flavigula), endo- and ectoparasites, and scavengers.
Ecological relationship with mountain taiga determines the decline of musk deer population due to reduction and transformation of coniferous forests by man and also due to extensive fires. Unregulated hunting and illegal trade in derivatives with the Asia–Pacific region countries which intensified since 1990-s have led to a significant downsizing of population (up to 6–10 times) in many hunting grounds. Decrease in number occurs in nature reserves as well (Zaitsev, 2006). The study of the ecology of musk deer was started in the Sikhote-Alin Reserve in 1930-s by Salmin (Salmin, 1972), and continues from 1974 to the present time, providing the basis for the implementation of measures for the preservation of species (Zaitsev, 2006, Zaitsev et al., 2013a, Maksimova et al., 2014b and Slaght et al., 2012). During this time, a number of properties of the population structure and the position of musk deer in the ecosystem were identified, and population density counting methods were developed (Zaitsev, 1991, Zaitsev, 2006, Zaitsev et al., 2013b and Maksimova et al., 2015). Nevertheless, musk deer still cannot be attributes to species with well-known ecology. Since the beginning of the study we used a complex technique, and a number of significant results of using this technique are presented in this paper.
Since 1970-s a system for keeping track of the size and structure of musk deer population using multiple methods of observation was shaped in the nature reserve. This system involves the study: a) at few key areas, including two main areas (Zimoveinyi — over 10 km2 in the basin of Serebryanka River; Nechet — over 10 km2 in the basin of Tayozhnaya River); b) a comprehensive study of different areas using one of the counting methods developed. A promising way to study the population structure and behavior of musk deer at stations involves a combination of techniques including snowtracking (since 1974), radiotracking (since 2012), photo and video observation of individual animals accustomed to the observer (since 1975), registration with trail cameras (since 2011), and counting of hoofprints and abundance of food plants (lichens) at the test areas. Topographical maps, aerial and satellite images, and GPS-navigators are used.
The studies are conducted at controlled home ranges where the routes form a network with the distance between the routes from 200 to 500 m. Prior to the use of GPS-navigators 10 km of regular routes were labeled at the main station at 20 m intervals. Permanent areas of lichen count (30 × 30 m or 20 × 20 m) were labeled.
During multi-day tracking the daily route of an individual musk deer was tracked (from contact to contact), and a part of the daily route was tracked with fragmentary tracking. The paths of animal movement were plotted on the topographic base; and the outlines of habitats and activity centers were laid out at the outermost animal movement paths. Several tracking techniques were used differing in the precision of recording the route of an animal using different measurement tools and devices (Zaitsev, 1991, Zaitsev, 2000 and Zaitsev, 2002). The method of accustoming musk deer (21 individuals in total) to close presence of an observer (up to 1.5–6 m) based on a sort of “breaking” of the defensive range expanded the research opportunities.
During tracking and visual observation 1749 objects were labeled with bright-colored tags, which made it possible to determine the amount of time that passed after marking. These objects were: caudal gland excreta marks, excrement piles, urinary points, and complex marks near beds. In 628 cases (35.8%) these sites were re-visited by musk deer. For this purpose trail cameras were used. More than 10 musk deer behavior reactions to labeling were observed.
Since 2012 radiotracking is used in addition to snowtracking. Musk deer were caught using modified box traps (Shcherbakov, 1953) or by approaching accustomed individuals and immobilizing them. In 2012–2014 six musk deer were captured and tagged with Telonics transmitters, USA (150–152 MHz), of which five animals were males. They were monitored from several months to several years along with tracking and visual observations. Radiotracking allowed the researchers to obtain information on changes in home ranges during snowless period and throughout the year (Maksimova et al., 2014a and Maksimova et al., 2014b). To determine the size of home range the minimum convex polygon method and kernel density estimation method (Powell, 2000 and Worton, 1987) were applied. The latter method is based on a statistical model that allows localizing the movement of individuals to contours with 95% (home range) or 50% (core zone or the center of activity of the range) probability of frequency of visits. We have obtained up to date data for comparison of the results of radiotracking and snowtracking for choosing the optimal option to calculate the parameters of animals' home range.
Up until 1970-s the information on spatial and social structure of the population of musk deer was missing (home range was described by Ustinov (1967)) or was contradicting in nature. A difference in the size of home ranges used by musk deer during the same time interval between males (up to 70–380 ha), and females and juveniles (10–60 ha) (Zaitsev, 1978 and Zaitsev, 1982) was observed in Sikhote-Alin. During the lifetime (up to 7–8 years, rarely more) some males claimed areas of 3.5–6 km2. Home ranges of females and juveniles are “contained” within vast ranges of adult males (starting from the age class of 2–3 years and older). The sizes of home ranges correlate with the distance of the daily route of musk deer (from 0.9 to 4–5 km for males starting with the second year of life; 0.56–1.5 km and rarely more for females and juveniles); for males — r = 0.949, p < 0.001. A home range has one or more centers of activity (cores) united by passages. Under various conditions in different seasons the centers of activity reached for males, according to snowtracking data, 20–53% of the size of the range, and the areas with day-time beds — from 1.5 to 15%. According to radio tracking, the home range core (50% probability) where a male was usually resting during the day-time, occupied 3.1–21.2% of the range area.
Overlap areas between home ranges are important in providing contacts between neighboring individuals. Under stable conditions for males ≥ 2 years old, according to tracking data, these areas covered not more than 10–15% of home range, but in destabilized groups they reached 40–63%, and for males of 1–2 years age group they sometimes reached 90%. The overlap of home ranges of neighboring males, and visits to the same place by different individuals were detected by radiotracking and trail cameras. Under conditions of high population density and limited home range sizes neighboring females had the smallest contact zones.
After a few days of using a home range (7–10 days or more for males) it stabilizes in size; then an abrupt change of the area size and location occurs, which is again followed by a brief stabilization period, etc. (Zaitsev, 2014). During the season, the year and the lifetime of an individual these changes reach significant values up to dislocation of the center of activity by a kilometer or more. As individuals of both sexes settle in the area, a system of home range separated by hundreds of meters or kilometers is formed (Zaitsev, 1991 and Zaitsev, 2006). According to radiotracking, in case of a stable connection of musk deer to an area, home range sizes for each male changed throughout the year: for one of adult males it changed from 0.57 km2 in July–August to 1.81 km2 in September–October; for a young male — from 0.47 km2 in January–March to 1.12 km2 in the April–June (Maksimova et al., 2014a and Maksimova et al., 2014b). In general, snowtracking and radiotracking revealed that the sizes of home ranges of males, as well as the levels of physical activity decrease from September–December (pre-rutting and rutting periods) to the end of the winter, and increase with the start of snowless period, and then decrease in summer during mass emergence of bloodsucking insects, subcutaneous parasite (Booponus inexspectatus). The most notable changes in the size of a home range are more likely to occur during snowless period, especially before the rut. Throughout several years (up to 7–8 years of life of a male) one can observe general expansion of the home range and its gradual shift into the community center of the group where a male may take a dominating position, and then a rapid decrease of home range size until the death of the male ( Zaitsev, 1991 and Zaitsev, 2006).
Uneven distribution of musk deer connected to life conditions is reflected in formation of associations of different ranks of geographical structure, ranging from ones completely or partially isolated from each other, sub- or metapopulations distributed on the slopes of major watersheds to small parcel-type groups consisting of several neighboring species. The latter are of chorologic (parcels of several types) and reproductive character. In the period when the number of musk deer in Sikhote-Alin was high (1970-s–1980-s) these groups were composed of up to 7–16 individuals, including 1–2 adult males (≥ 3 years), up to 4–5 younger males, up to 3–8 females and 3 or more current years young animals of both sexes. In the basic reproductive groups females often outnumbered males of reproductive age (from 2 years), but the predominant emigration of young males was consistent with the sex ratio in the population which was close to 1:1. The number of current years young animals reached 20–34%. Dominant males contributed the most to the reproduction of the population in accordance with their reproductive strategy (Zaitsev, 1991). After many years of decrease in numbers, in 2000-s the sex ratio in these groups became even or dominated by males: 1:1–1:0.75 (Zaitsev, 2006), reflecting the overall decline in the reproductive potential of the population.
Each group has a central part corresponding to good living conditions. This center is populated by the dominant male, who with aging shifts its home range here. Home ranges of many females are located in the vicinity of the center. The distribution of females is usually aggregated, and philopatry is traced. Home range of an adult female often (11 of 18 cases, 61%) neighbors on home range of a young (1–2 years old) female. However, 75% of females changed home ranges, successively using adjacent forest areas, often not going beyond the home range of a single male. During the decrease of the number of animals in 2000-s 21% of females left the males home range after the rutting period. At a high population density typically there are aggregations of several females at adult males home range (harem aggregation), in which each female has a range with most favorable feeding conditions. The reduction of the rate of females in the period of low abundance was accompanied by a decrease in the number of harem aggregations.
Stable conditions in taiga forests contribute to conservatism in populating home ranges and vacant-type stocking of habitats with animals in successive generations, when individuals of different sex and age class occupy special “vacant cells”. As a result, the group has a stable structure throughout many years and decades, based on year-round territoriality in relation to the individuals of the same sex with a limited number of contacts at short distances (Zaitsev, 1991 and Zaitsev, 2006). The relationships between individuals do not possess the traits of the opposing social alliances. The major role in maintaining the structure of the groups belongs to olfactory communication that provides more than 99% of contacts between males. Adult males organize mutual relationship in such a way as to maintain stable ties at different population density. All types of excreted marks influence the distribution of individuals in relation to each other; however caudal gland excreta marks on elevated objects, and excrements are of particular importance for distribution of males in home ranges. Distribution of these marks forms the zones functioning for many years. The larger the size of the males home range and the longer its daily route, the greater number of caudal gland excreta (r2 = 0.578, p < 0.0001) and excrements (r2 = 0.253, p = 0.02) it produces. Males begin to mark the territory with caudal gland excreta after 10 months of life, gradually increasing the frequency of marking until 3–5 years, and reducing the frequency after 6–7 years of age. Marking with excreta is a flexible means of adjusting the structure of groups.
We assume that further studies of the structure of the population will be aimed at clarifying its adaptive capacity to varying habitat conditions due to climate changes, and will identify different variants of the structure and regulatory mechanisms. The research results allowed identifying musk deer as an indicator species in the planning of the system of protected areas of old-growth coniferous forests within the framework of a joint program with the Amur branch of WWF (Slaght et al., 2012).
We would like to express our gratitude to the staff and administration of the Sikhote-Alin Nature Reserve, Wildlife Conservation Society, and the Amur branch of World Wide Fund for Nature, who participated in the field work and provided the necessary tools and equipment.