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Habitat dynamics and its influence on the genetic diversity of Tarim red deer (Cervus elaphus yarkandensis) Xayar population of Xinjiang, China
Quaternary International 311 (2013) 140e145
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Habitat dynamics and its influence on the genetic diversity of Tarim red deer (Cervus elaphus yarkandensis) Xayar population of Xinjiang, China Anwar Tumur, Dilshat Abliz, Mahmut Halik* College of Life Sciences and Technology, Xinjiang University, No 14, Shengli Road, Urumqi 830046, Xinjiang, China
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 3 August 2013
The Tarim red deer (Cervus elaphus yarkandensis) is an endangered and endemic animal, with three populations isolated in the regions around Xayar, Lopnur, and Qarqan counties of Xinjiang, China. The Xayar populations of Tarim red deer are mainly distributed in the southern parts of Xayar and Kuqa County. In order to better understand the habitat dynamics and its influence on genetic diversity of Tarim red deer Xayar population, we interpreted LANDSAT TM/ETMþ satellite images of the habitat area of Tarim red deer during the period from 1972 to 2006 using RS and GIS technologies. The land covers within the habitat of Tarim red deer are classified into seven classes: farmland, high-cover vegetation, middle-cover vegetation, low-cover vegetation, water area, desertified area, and sandy land. Our results show that the land covers of Tarim red deer habitat have changed significantly during the 34-year period (1972e2006). Specifically, the areal extents of farmland, middle-cover vegetation and low-cover vegetation increased greatly, while the areal extents of high-cover vegetation and water area decreased dramatically. The detected decrease in the habitat areal extents suitable for of Tarim red deer and the associated habitat fragmentation are interpreted to be contributing factors to the observed decrease in the genetic diversity. Ó 2013 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction Cervidae appeared early in the Miocene Ephoch and evolved in the Northern Hemisphere during a period characterized by cold climate and seasonal food availability (Geist, 1998). The red deer (Cervus elaphus) is considered to have evolved during the Pleistocene in the Himalayan foothills from a sika deer-like ancestor before expanding from China to Europe (Geist, 1971, 1983; Groves and Grubb, 1987; Ohtaishi, 1992, 1995) and was classified into 22 subspecies according to coat colors, and morphological features of cranium and antlers (Ohtaishi and Gao, 1990; Ohtaishi, 1992, 1995). These species are widely distributed from the Arctic Circle to the Tropic and have adapted to a variety of landscapes ranging from fully-covered forests to sparsely-vegetated prairies (Janis and Jarman, 1984). Red deer species are abundantly found in China, an important center of the evolution and the dispersal (Sheng and Ohtaishi, 1993) and Xinjiang is an important distribution area of the red deer in China. Totally, 22 subspecies of red deer are found in the northern hemisphere and eight of them are in China. Three of the eight * Corresponding author. E-mail address: [email protected] (M. Halik). 1040-6182/$ e see front matter Ó 2013 Elsevier Ltd and INQUA. All rights reserved. http://dx.doi.org/10.1016/j.quaint.2013.07.007
Chinese subspecies inhabit in Xinjiang and they are Tarim red deer (Cervus elaphus yarkandensis Blanford, 1892), Tianshan red deer (Cervus elaphus songaricus Severzov, 1872), and Altai red deer (Cervus elaphus sibiricus Severzov, 1873). These three subspecies are characterized by distinct distributions and were reported to have stable populations (Gao and Gu, 1985; Gao, 1993). Tarim red deer is the only subspecies of red deer in Central Asia that exhibits unique adjustment to a dry climate (Gu et al., 1987; Luo and Gu, 1993) and is normally associated with large river channels in the deserts of the Tarim Basin (Gao and Gu, 1985; Gu et al., 1987; Luo and Gu, 1993). Tarim red deer are concentrated in riparian poplar forests, reed meadows, and some agricultural lands with tamarisk shrub (Tamarix spp.) (Wen, 1994; Yan et al., 1997). Their habitat selection depends on food availability. For example, reed meadows are preferred in summers and poplar (Populus diversifolia) meadows and tamarisk shrubs are favored in winters (Luo and Gu, 1993; Qiao et al., 2006). The Tarim red deer is well documented to inhabit the valleys of the Tarim, Konqi, and Qarqan rivers in Xinjiang. It was reported to inhabit the valleys of Hotan and Yarkan rivers and probably also in Keriya and Niya areas (Gao and Hu, 1993). Field studies conducted in 2000 recorded the Tarim red deer in Alar, Xaya, Bugur, Lopnur,
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Tikanlik, and Aktaz (all in Tarim Basin). The lack of references to this red deer in historical documents of the 19th and early 20th centuries suggests that the red deer was rare then. Some works (Allen, 1940; Ellerman and Morrison-Scott, 1951) proposed that the Tarim red deer was nearly extinct by the 1920s. Due to its limited distribution and small population, this deer has been included on the Red List (2000) of the International Union for the Conservation of Nature and Natural Resources (IUCN) under “endangered species” (ED) and has been designated as a Category II protected animal in China (Gao and Gu, 1985; Mahmut, 2002; Mahmut et al., 2004). The Tarim red deer population has decreased dramatically from about 15 000 in 1970s to about 450 in 2006, and is reported to be on the verge of extinction (Mahmut, 2002; Mahmut et al., 2002). The habitation areas of the Tarim red deer are also the areas where human activities have been intensive and the humaninduced disappearance or fragmentation of the riparian forests along river channels have resulted in isolation of local populations of the red deer. Consequently, only three populations are documented in Xaya, Lopnur and Qarqan (Mahmut et al., 2001, 2012) (Fig. 1). The endangered situation of the Tarim red deer is thought to result from farmland expansion, overgrazing, oil exploitation, and fawn catching (Gao and Gu,1985; Sheng,1992; Wang,1998). Integrity and diversity of habitat are essential for preserving endangered species and for maintaining ecosystem balance in this area. There have been numerous studies of Xinjiang red deer, but most have focused on the distribution of subspecies and estimation of population size (Mahmut et al., 2002). Recently, some studies have started to focus on genetic diversity, molecular ecology, phylogenetics and diet analysis and food habitat selection (Mahmut et al., 2001, 2002, 2005, 2012; Qiao et al., 2006) and some studies have started to investigate the habitat dynamics and the factors that affect the habitat change of Lopnur and Qarqan populations (Anwar and Mahmut, 2007, 2008a, 2008b, 2009a, 2009b; Anwar et al., 2008; Mahmut et al., 2012). The first population census, using the line transect method, was conducted in 1997 by Anwar et al. (1998), and another census was conducted in 2000 (Mahmut et al., 2001). Although other estimates are very rough, some data, e.g., those obtained by Gao and Gu (1985) and by Luo and Gu (1993) are useful to trace the general trends in the population dynamics. Habitat loss and fragmentation are the most serious threats to biological diversity and are the primary causes of the present extinction crisis (Heywood, 1995). In investigating changes in habitats of wildlife, Geographic Information Systems (GIS) and Remote Sensing (RS) (Jin et al., 2005) have increasingly been used to quantify landscape patterns, dynamics, and ecological processes underlying habitat change (Lewis, 1995; Ross et al., 2001; Tobias, 2006; Cao and Liu, 2008). In this paper, we investigate the dynamics of habitat of the Tarim red deer by using images from 1972, 1989, 2001, and 2006, and discuss the factors affecting the changes of genetic diversity of the Tarim red deer Xayar population.
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2. Study area The study area, covering an area of about 572 563.24 hm2, is located on the southern edge of the forested area of Xayar and Kuqa Counties in northern part of the Taklimakan Desert in the middle reach of the Tarim River (40 400 e41 170 N and 82 050 e84160 E, 950e1020 m asl) (Fig. 2). The northern part of the area is occupied by the Tarim River plain extending along the river area, and the southern part is in the Taklimakan Desert. This regional climate is continental with a mean annual precipitation of only 47 mm/y. The mean annual potential evaporation of 2000 mm is 45.8 times more than the precipitation. Summers are hot with an average temperature of 32.7 C in July and winters are cold with an average temperature 14.80 C in January (annual frost-free period is 215 days). The mean annual daylight hours are 3029 h. Principal vegetation in the area includes P. diversifolia, Tamarix ramosissima, Apocynum venetum, Nitraria tangutorum, Alhagi sparsifolia, Acorusgr amineus Soland, Carex phacota and Anabasis brevifolia. 3. Methods 3.1. Data source We made field observations on four occasions (February 2007, June 2008, October and April 2009) to establish location point data for land-cover vegetation classification and to record the GPS locations of signs from the Tarim red deer. Human activities such as farming and grazing were also investigated. The MSS image of 25th August 1972 and TM/ETMþ images of 8th August 1989 and 30th June 2001 were obtained from the Global Land Cover Facility website (http://www.glcf.umiacs.umd.edu/). ETMþ image of 30th July 2006 was from the US Geological Survey website (http://edcsns17. cr. usgs. gov/Earth Explorer/). The spatial resolution is 60 m 60 m for 1972 images, and 30 m 30 m for 1989, 2001 and 2006 images. 3.2. Image processing and classification We processed the images using ERDAS IMAGINE 9.0 software. We first made a composite of bands of 5, 4, and 3, which were geometrically corrected according to topographic maps of the study area. We then applied a variety of image enhancement processes (e.g., convolution and histogram equalization) to eliminate the effects of cloud cover. The radiometric correction was made for different time periods so that the images are comparable for the entire study area. We processed GPS data recorded from the field observation using ArcView GIS 3.2 to generate corresponding image layers and the final images were interpreted using visual interpretation and computer classification methods. Seven classes for the final images were formulated and confirmed through the use of location point data. Table 1 presents the land cover types applied for image classification.
Table 1 Classification system used in this research.
Fig. 1. Present and historical distribution areas of the Tarim red deer in Xinjiang.
No.
Land-cover types
Characteristics
1 2 3 4 5 6
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water bodies Desertified area
7 8
Sandy land Outside area
Cultivated land Coverage over 50e75% Coverage between 25 and 50% Coverage lower than 5e25% River or lake Coverage between 0 and 5% and distribute rare plant species Sand dune without vegetation Unclassified area
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Fig. 2. Location of the study area.
3.3. Analysis of dynamic land-cover change
of the Tarim red deer from 1972 to 2006. Table 3 shows that in the period of 1972e1989, the area of farmland, middle-cover vegetation, low-cover vegetation, water area, and sandy land in the study area increased, while high-cover vegetation and desertified area decreased (see Table 3).
In order to describe the rate at which the land cover types changed during various time periods, we used the following models of land cover change which detect the changes in raw area, proportional change, and annual proportional change of each one of the seven land-cover types (Xu, 2008):
F ¼ Ub Ua=Ua
Table 3 Land cover change of study area (hm2) from 1972 to 2006.
K ¼ F=T 100%
where Ua and Ub represent the initial and final land areas of a certain land cover type, respectively. F is the proportional change of a specific land-cover types; T is the duration length of the study period and K is the annual change rate of a certain land type in a period of time. 4. Results 4.1. Classification of habitat types The land covers that best represent change in habitat of Tarim red deer are classified into seven classes: farmland, high-cover vegetation, middle-cover vegetation, low-cover vegetation, water area, desertified area, and sandy land (see Table 1). Table 2 and Fig. 3 presents the area under different land cover types and the proportion of the total area in 1972, 1989, 2001, and 2006, respectively.
Land-cover types
Changed area (hm2) 1972e1989
1989e2001
2001e2006
1972e2006
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water area Desertified area Sandy land
4695.02 12710.91
1946.72 12367.36
10019.86 9046.5
12768.16 34124.77
1145.12
2576.53
11222.24
9790.83
3549.89
8073.14
5897.4
17520.43
2519.28 1030.62 1946.72
5267.58 2003.98 1545.92
23215.45 3149.09 1030.61
14428.59 4122.45 4523.25
High-cover vegetation was the land-cover type that decreased the most dramatically in terms of the areal extent (12 710.91 hm2) in the period of 1972e1989. In the period of 1989e2001, farmland and middle-cover vegetation decreased and high-cover vegetation decreased the most dramatically in terms of the areal extent
Table 2 Areas of different land cover types (hm2) and their proportions to the total area (%). Land-cover types
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water area Desertified area Sandy land
1972
1989
2001
2006
Area (hm2)
Proportion (%)
Area (hm2)
Proportion (%)
Area (hm2)
Proportion (%)
Area (hm2)
Proportion (%)
14 314.08 56741.02 56912.79 46950.19 54164.48 59374.81 35785.20
2.50 9.91 9.94 8.20 9.46 10.37 6.25
19009.10 44030.11 58057.91 50500.08 56683.76 58344.19 37731.92
3.32 7.69 10.14 8.82 9.90 10.19 6.59
17062.38 31662.75 55481.38 58573.22 61951.34 60348.17 39277.84
2.98 5.53 9.69 10.23 10.82 10.54 6.86
27082.24 22616.25 66703.62 64470.62 39735.89 63497.26 40308.45
4.73 3.95 11.65 11.26 6.94 11.09 7.04
4.2. Dynamic change of habitat Analysis models of land cover change were applied to analyze the temporal and spatial characteristics of dynamic habitat changes
(12 367.36 hm2). In the period of 2001e2006, the areas of farmland, middle-cover vegetation and low-cover vegetation had increased substantially (10 019.86 hm2 and 11 222.24 hm2 respectively) whereas water area decreased by 23 215.45 hm2 and the area of
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Fig. 3. Classified land cover change maps of study area in 1972, 1989, 2001 and 2006.
high cover vegetation continued to decrease. For the entire period of 1972e2006, the areas of farmland, middle-cover vegetation and low-cover vegetation increased by 12 768.16 hm2, 9790.83 hm2, 17 520.43 hm2 respectively. Desertified area and sandy land also increased. In contrast, the areas of high-cover vegetation and water decreased by 34 124.77 hm2 and 14 428.59 hm2, respectively. Table 4 summarizes the proportional changes and the annual rates of change for the time periods 1972e1989, 1989e2001, 2001e2006, and 1972e2006.
land. For the entire period of 1972e2006, farmland changed at the highest rate (2.62% annually) and the high-cover vegetation was the second highest (1.77% annually). 4.3. Habitat fragmentation and its influence on genetic diversity Recent studies showed that the habitat fragmentation in the Tarim Basin has adversely influenced the population size and genetic diversity of the Tarim red deer Xayar population. Mahmut
Table 4 Proportional change and annual rate of change in land cover types of study area, from 1972 to 2006. Land-cover types
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water area Desertified area Sandy land
1972e1989
1989e2001
2001e2006
1972e2006
Proportional change
Annual rate of change
Proportional change
Annual rate of change
Proportional change
Annual rate of change
Proportional change
Annual rate of change
0.3280 0.2240 0.0201 0.0756 0.0465 0.0173 0.0544
1.929% 1.318% 0.118% 0.445% 0.274% 0.102% 0.320%
0.1024 0.2808 0.0444 0.1598 0.0929 0.0343 0.0409
0.853% 2.341% 0.369% 1.332% 0.774% 0.286% 0.341%
0.5872 0.2857 0.2023 0.1006 0.3586 0.0522 0.0262
11.745% 5.714% 4.045% 2.014% 7.172% 1.044% 0.525%
0.8920 0.6014 0.1720 0.3731 0.2664 0.0694 0.1264
2.624% 1.769% 0.506% 1.098% 0.784% 0.204% 0.372%
Specifically, farmland increased the most in the period of 1972e 1989 (almost 33%). Low-cover vegetation, sandy land, water area and middle-cover vegetation increased by 7.6%, 5.4%, 4.6%, and 2.0%, respectively. High-cover vegetation and desertified area decreased by 22.4% and 17.3% respectively. From 1989 to 2001, farmland and high-cover vegetation decreased by 10.2% and 28.1% respectively, while low-cover vegetation increased by 16%. In the period of 2001e2006, farmland increased by 58.7% while water area decreased by 35.9%. For the entire period of 1972e2006, farmland increased by 89.2%; low-cover vegetation, middle-cover vegetation and sandy land also increased but by lesser amounts. High-cover vegetation showed the greatest reduction (60.1%) and the second greatest reduction was water area (26.6%). Farmland also showed the fastest rate of increase from 1972 to 1989, 1.93% yearly. High-cover vegetation increased at a rate of 1.32% yearly, while low-cover vegetation increased at a rate of 0.44% yearly. In the period of 1989e2001, high-cover vegetation was reduced at a rate of 2.34% yearly, while low-cover vegetation increased at a rate of 1.33%. In the period of 2001e2006, the fastest change was farmland and the slowest rate of change was sandy
et al. (2001) investigated the genetic variations of the Tarim red deer Xayar population using microsatellite DNA method and found that the average observed multilocus heterozygosity Ho was 0.08 0.04. The observed heterozygosities were significantly lower than the expected values. By contrast, the North American red deer have a higher observed mean heterozygosity with Ho ¼ 0.552 0.039 (Talbot et al., 1996). This greatly reduced heterozygosity (Ho ¼ 0.08 0.04) suggests that the population of Tarim red deer in Xayar might have resulted from the observed inbreeding under conditions of suitable habitat decrease that led to population decrease and associated habitat fragmentation that led to inbreeding (Mahmut et al., 2001). Dong et al. (2010) investigated genetic diversity and gene flow in the Tarim red deer population by analyzing 342 base pairs of the mitochondrial DNA controlled region in 34 individuals sample from Xayar, Lopnur and Qarqan. Their results show that the haplotype diversity of Xayar population was 0.893 0.080 and the nucleotide diversity was very low (0.01446 0.000182). Overall, an increasing human population and the related activities of livestock production, uncontrolled agricultural development, harvest of trees and the extraction of mineral
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resources all have contributed to decreasing water resources and reduction and fragmentation of deer habitats in Xayar. Therefore, under the harsh natural environments combined with severe human disturbances, the increased isolation the Tarim red deer population in Xayar promoted the deer for in-breeding and demoted the deer for out-breeding, thus leading and the genetic deterioration of the Tarim red deer. 5. Discussion and conclusions Land cover changes we detected can be attributed to the ecological vulnerability of this region. Plant growth in this area depends mainly on groundwater. Groundwater in turn depends on surface water. If surface water decreases, groundwater level will decline, leading to soil drying and thus plant dying (Hao et al., 2006; Pan et al., 2007). The reported increases in precipitation and in ice-melt water in the Tarim Basin ensure that the total amount of surface water resources has not been reduced during the study period. However, undeniable facts are: (1) river flow in the middle and lower reaches of the Tarim Basin has been dramatically reduced and the groundwater levels at two sides of the rivers in the middle and lower reaches have been declining during the same time (Chen et al., 2010). Apparently, the growth of human population and the associated economic expansion have been the reasons for the observed reductions in the surface runoff and in groundwater levels (Zhang et al., 2003; Ye et al., 2006; Li, 2008). Specifically, agriculture is the primary human activity in this region and water used for irrigation accounts for more than 85% of total withdrawals (Xu et al., 2005). Since the mid-1980’s, with increasing domestic demand for cotton, land has been increasingly exploited, leading to a sharp increase in water consumption (Guo, 2005). This, coupled with petroleum exploitation, has resulted in a serious water shortage in the soil and also a decline in the groundwater level (Wang et al., 2006). Since the 1950s, the human population in the Tarim Basin has expanded rapidly, inevitably exacerbating deforestation and overcultivation in this area, leading to fragmentation of wildlife habitats (Wang et al., 2006). Total human population of Xayar County was 115 000 in 1970 and nearly doubled to 207 000 in 2003. The agricultural population increased by 54% from 108 000 in 1970 to the 166 000 at the end of 2003 (Statistical Yearbook of Xayar, 2004). Our results show that expansion of agricultural activities was mainly associated with conversion of high-cover vegetation to other forms of land covers. Field interviews with local farmers and observations substantiated that most woodland and shrub lands were cleared for agriculture. Reclamation and subsequent abandonment of cultivated land in some areas have not only destroyed natural grasslands and shrub lands but also loosened the ground surface and undermined the protective layer, further exacerbating desertification and sandstorm generation. The Tarim red deer prefers habitats with high-covered vegetation and rich food resources near water bodies but far from human disturbances (Anwar et al., 2008). We found that high-cover vegetation decreased in the period of 1972e2006. We attribute most of these changes to human activity. We also observed that red deer signs (or imprints) were frequently found on farmlands where human disturbance is common. This suggests that the Tarim red deer has begun to search for food and water around farmlands although the human threat is imminent. We conclude that the Tarim red deer habitat in the Xayar and Kuqa area has declined because of the expansion of human activities and the decline has resulted in the decrease in their population. The human-induced fragmentation of the habitat seems to be a major contributing factor to the observed genetic deterioration of the Tarim red deer. Management interventions are needed to reverse these trends.
Local authorities should take appropriate measures to prohibit excessive development in the existing Tarim red deer habitat and should reinforce protection and management of vegetation and wildlife habitat. Acknowledgements This research was supported by the National Natural Science Foundation of China (30660025, 31060152), Natural Science Foundation of Xinjiang Uygur Autonomous Region, China (2010211A02), The Key discipline of Animal Science of Xinjiang University. The authors would like to thank Masters students Arzigul Sattar，Aysajan Tohti and Askar Mamat for their assistance during the field work in Xayar. We would like to thank Dr. Zhaodong Feng for his critical comments that led us to improve the quality of the paper. References Allen, G.M., 1940. The Mammals of China and Mongolia. In: Natural History of Central Asia. American Museum of Natural History, New York 11, pp. 1126e1261. Anwar, T., Mahmut, H., Sultan, M., 1998. The Preliminary Study on the Structure of Populations of the Tarim Red Deer in Qarqan Xinjiang (in Chinese). Collections of Scientific Papers of the Higher Education. Chinese Three-Strait Publishing House, pp. 131e132. Anwar, T., Mahmut, H., 2007. Study on dynamic habitat characteristics of Red deer Tarim subspecies in popular natural reservation in Xinjiang (in Chinese). Ecological Sciences 26, 63e68. Anwar, T., Mahmut, H., 2008a. Preliminary analysis on the habitat selection of red deer Tarim species (Cervus elaphus yarkandensis) in middle reaches of Tarim river (in Chinese). Xinjiang Agricultural Sciences 45, 847e853. Anwar, T., Mahmut, H., 2008b. Preliminary study of the current population density and habitat characteristics of Tarim red deer in middle reaches of Tarim river (in Chinese). Xinjiang Agriculture Sciences 45, 743e749. Anwar, T., Yan, S.X., Mahmut, H., 2008. Habitat suitability assessment on the Tarim subspecies of red deer (Cervus elaphus yarkandensis) in the lower reaches of Cherchen River, Xinjiang, China (in Chinese). Journal of Arid Land Resources and Environment 22, 196e200. Anwar, T., Mahmut, H., 2009a. Current situation and conservation of isolated population of Tarim red deer (Cervus elaphus yarkandensis) in lower reaches of Charchen River in Xinjiang (in Chinese). Journal of Arid Land Resources and Environment 23, 195e200. Anwar, T., Mahmut, H., 2009b. Preliminary study of the habitat selection of red deer Tarim species (Cervus elaphus yarkandensis) in lower reaches of Cherchen River (in Chinese). Arid Zone Research 26, 228e233. Chen, Y.N., Xu, C.C., Hao, X.M., Li, W.H., Chen, Y.P., Zhu, Ye, Z.X., 2010. Fifty-year climate change and its effect on annual runoff in the Tarim River Basin, China. Quaternary International 208, 53e61. Cao, M.C., Liu, G.H., 2008. Habitat suitability change of red-crowned crane in Yellow River Delta Nature Reserve (in Chinese). Journal of Forestry Research 19, 141e147. Dong, X.Y., Shan, W.J., Yu, L.J., Mahmut, H., 2010. Structure of mitochondrial DNA control region and population genetic diversity analysis of Tarim red deer (Cervus elaphus yarkandensis). Biotechnology 20, 16e20. Ellerman, J.R.Q., Morrison-Scott, T.C.S., 1951. Checklist of Palaearctic and Indian Mammals 1758 to 1946. Trustees of the British Museum, London, pp. 1e810. Gao, X.Y., Gu, J.H., 1985. Red deer in Xinjiang (in Chinese). Chinese Wildlife 2, 24e26. Gao, X.Y., 1993. Status and rear of red deer in Xinjiang (in Chinese). Chinese Wildlife 2, 6e8. Gao, X., Hu, D., 1993. Status of wild and farmed red deer in Xinjiang. In: Ohtaishi, Sheng, H.L. (Eds.), Deer of China: Biology and Management. Elsevier Science Publisher, Amsterdam, pp. 159e164. Geist, V., 1971. The relation of social evolution and dispersal in ungulates during the Pleistocene, with emphasis on the old world deer and genus Bison. Quaternary Research 1, 283e315. Geist, V., 1983. On the evolution of ice age mammals and its significance to an understanding of speciations. Association of Southeastern Biologists Bulletin 30, 109e133. Geist, V., 1998. Deer of the World: Their Evolution, Behaviour and Ecology. Stackpole Books, Mechanicsburg, pp. 170e223. Groves, C.P., Grubb, P., 1987. Relationships of living deer. In: Wemmer, C.M. (Ed.), Biology and Management of the Cervidae. Smithsonian Institute Press, Washington, DC, pp. 21e59. Guo, J., 2005. Analysis on variation of soil utilization covering and its influences to eco-environment in the plain area of Tarim river basin in Xinjiang Municipality. Ground Water 27, 493e496. Gu, J., Gao, X., Xiang, L., 1987. Red Deer in Western Lopnor District-Scientific Survey and Research in Lopnor (in Chinese). Science Press, Beijing, pp. 226e234.
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Habitat dynamics and its influence on the genetic diversity of Tarim red deer (Cervus elaphus yarkandensis) Xayar population of Xinjiang, China Anwar Tumur, Dilshat Abliz, Mahmut Halik* College of Life Sciences and Technology, Xinjiang University, No 14, Shengli Road, Urumqi 830046, Xinjiang, China
a r t i c l e i n f o
a b s t r a c t
Article history: Available online 3 August 2013
The Tarim red deer (Cervus elaphus yarkandensis) is an endangered and endemic animal, with three populations isolated in the regions around Xayar, Lopnur, and Qarqan counties of Xinjiang, China. The Xayar populations of Tarim red deer are mainly distributed in the southern parts of Xayar and Kuqa County. In order to better understand the habitat dynamics and its influence on genetic diversity of Tarim red deer Xayar population, we interpreted LANDSAT TM/ETMþ satellite images of the habitat area of Tarim red deer during the period from 1972 to 2006 using RS and GIS technologies. The land covers within the habitat of Tarim red deer are classified into seven classes: farmland, high-cover vegetation, middle-cover vegetation, low-cover vegetation, water area, desertified area, and sandy land. Our results show that the land covers of Tarim red deer habitat have changed significantly during the 34-year period (1972e2006). Specifically, the areal extents of farmland, middle-cover vegetation and low-cover vegetation increased greatly, while the areal extents of high-cover vegetation and water area decreased dramatically. The detected decrease in the habitat areal extents suitable for of Tarim red deer and the associated habitat fragmentation are interpreted to be contributing factors to the observed decrease in the genetic diversity. Ó 2013 Elsevier Ltd and INQUA. All rights reserved.
1. Introduction Cervidae appeared early in the Miocene Ephoch and evolved in the Northern Hemisphere during a period characterized by cold climate and seasonal food availability (Geist, 1998). The red deer (Cervus elaphus) is considered to have evolved during the Pleistocene in the Himalayan foothills from a sika deer-like ancestor before expanding from China to Europe (Geist, 1971, 1983; Groves and Grubb, 1987; Ohtaishi, 1992, 1995) and was classified into 22 subspecies according to coat colors, and morphological features of cranium and antlers (Ohtaishi and Gao, 1990; Ohtaishi, 1992, 1995). These species are widely distributed from the Arctic Circle to the Tropic and have adapted to a variety of landscapes ranging from fully-covered forests to sparsely-vegetated prairies (Janis and Jarman, 1984). Red deer species are abundantly found in China, an important center of the evolution and the dispersal (Sheng and Ohtaishi, 1993) and Xinjiang is an important distribution area of the red deer in China. Totally, 22 subspecies of red deer are found in the northern hemisphere and eight of them are in China. Three of the eight * Corresponding author. E-mail address: [email protected] (M. Halik). 1040-6182/$ e see front matter Ó 2013 Elsevier Ltd and INQUA. All rights reserved. http://dx.doi.org/10.1016/j.quaint.2013.07.007
Chinese subspecies inhabit in Xinjiang and they are Tarim red deer (Cervus elaphus yarkandensis Blanford, 1892), Tianshan red deer (Cervus elaphus songaricus Severzov, 1872), and Altai red deer (Cervus elaphus sibiricus Severzov, 1873). These three subspecies are characterized by distinct distributions and were reported to have stable populations (Gao and Gu, 1985; Gao, 1993). Tarim red deer is the only subspecies of red deer in Central Asia that exhibits unique adjustment to a dry climate (Gu et al., 1987; Luo and Gu, 1993) and is normally associated with large river channels in the deserts of the Tarim Basin (Gao and Gu, 1985; Gu et al., 1987; Luo and Gu, 1993). Tarim red deer are concentrated in riparian poplar forests, reed meadows, and some agricultural lands with tamarisk shrub (Tamarix spp.) (Wen, 1994; Yan et al., 1997). Their habitat selection depends on food availability. For example, reed meadows are preferred in summers and poplar (Populus diversifolia) meadows and tamarisk shrubs are favored in winters (Luo and Gu, 1993; Qiao et al., 2006). The Tarim red deer is well documented to inhabit the valleys of the Tarim, Konqi, and Qarqan rivers in Xinjiang. It was reported to inhabit the valleys of Hotan and Yarkan rivers and probably also in Keriya and Niya areas (Gao and Hu, 1993). Field studies conducted in 2000 recorded the Tarim red deer in Alar, Xaya, Bugur, Lopnur,
A. Tumur et al. / Quaternary International 311 (2013) 140e145
Tikanlik, and Aktaz (all in Tarim Basin). The lack of references to this red deer in historical documents of the 19th and early 20th centuries suggests that the red deer was rare then. Some works (Allen, 1940; Ellerman and Morrison-Scott, 1951) proposed that the Tarim red deer was nearly extinct by the 1920s. Due to its limited distribution and small population, this deer has been included on the Red List (2000) of the International Union for the Conservation of Nature and Natural Resources (IUCN) under “endangered species” (ED) and has been designated as a Category II protected animal in China (Gao and Gu, 1985; Mahmut, 2002; Mahmut et al., 2004). The Tarim red deer population has decreased dramatically from about 15 000 in 1970s to about 450 in 2006, and is reported to be on the verge of extinction (Mahmut, 2002; Mahmut et al., 2002). The habitation areas of the Tarim red deer are also the areas where human activities have been intensive and the humaninduced disappearance or fragmentation of the riparian forests along river channels have resulted in isolation of local populations of the red deer. Consequently, only three populations are documented in Xaya, Lopnur and Qarqan (Mahmut et al., 2001, 2012) (Fig. 1). The endangered situation of the Tarim red deer is thought to result from farmland expansion, overgrazing, oil exploitation, and fawn catching (Gao and Gu,1985; Sheng,1992; Wang,1998). Integrity and diversity of habitat are essential for preserving endangered species and for maintaining ecosystem balance in this area. There have been numerous studies of Xinjiang red deer, but most have focused on the distribution of subspecies and estimation of population size (Mahmut et al., 2002). Recently, some studies have started to focus on genetic diversity, molecular ecology, phylogenetics and diet analysis and food habitat selection (Mahmut et al., 2001, 2002, 2005, 2012; Qiao et al., 2006) and some studies have started to investigate the habitat dynamics and the factors that affect the habitat change of Lopnur and Qarqan populations (Anwar and Mahmut, 2007, 2008a, 2008b, 2009a, 2009b; Anwar et al., 2008; Mahmut et al., 2012). The first population census, using the line transect method, was conducted in 1997 by Anwar et al. (1998), and another census was conducted in 2000 (Mahmut et al., 2001). Although other estimates are very rough, some data, e.g., those obtained by Gao and Gu (1985) and by Luo and Gu (1993) are useful to trace the general trends in the population dynamics. Habitat loss and fragmentation are the most serious threats to biological diversity and are the primary causes of the present extinction crisis (Heywood, 1995). In investigating changes in habitats of wildlife, Geographic Information Systems (GIS) and Remote Sensing (RS) (Jin et al., 2005) have increasingly been used to quantify landscape patterns, dynamics, and ecological processes underlying habitat change (Lewis, 1995; Ross et al., 2001; Tobias, 2006; Cao and Liu, 2008). In this paper, we investigate the dynamics of habitat of the Tarim red deer by using images from 1972, 1989, 2001, and 2006, and discuss the factors affecting the changes of genetic diversity of the Tarim red deer Xayar population.
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2. Study area The study area, covering an area of about 572 563.24 hm2, is located on the southern edge of the forested area of Xayar and Kuqa Counties in northern part of the Taklimakan Desert in the middle reach of the Tarim River (40 400 e41 170 N and 82 050 e84160 E, 950e1020 m asl) (Fig. 2). The northern part of the area is occupied by the Tarim River plain extending along the river area, and the southern part is in the Taklimakan Desert. This regional climate is continental with a mean annual precipitation of only 47 mm/y. The mean annual potential evaporation of 2000 mm is 45.8 times more than the precipitation. Summers are hot with an average temperature of 32.7 C in July and winters are cold with an average temperature 14.80 C in January (annual frost-free period is 215 days). The mean annual daylight hours are 3029 h. Principal vegetation in the area includes P. diversifolia, Tamarix ramosissima, Apocynum venetum, Nitraria tangutorum, Alhagi sparsifolia, Acorusgr amineus Soland, Carex phacota and Anabasis brevifolia. 3. Methods 3.1. Data source We made field observations on four occasions (February 2007, June 2008, October and April 2009) to establish location point data for land-cover vegetation classification and to record the GPS locations of signs from the Tarim red deer. Human activities such as farming and grazing were also investigated. The MSS image of 25th August 1972 and TM/ETMþ images of 8th August 1989 and 30th June 2001 were obtained from the Global Land Cover Facility website (http://www.glcf.umiacs.umd.edu/). ETMþ image of 30th July 2006 was from the US Geological Survey website (http://edcsns17. cr. usgs. gov/Earth Explorer/). The spatial resolution is 60 m 60 m for 1972 images, and 30 m 30 m for 1989, 2001 and 2006 images. 3.2. Image processing and classification We processed the images using ERDAS IMAGINE 9.0 software. We first made a composite of bands of 5, 4, and 3, which were geometrically corrected according to topographic maps of the study area. We then applied a variety of image enhancement processes (e.g., convolution and histogram equalization) to eliminate the effects of cloud cover. The radiometric correction was made for different time periods so that the images are comparable for the entire study area. We processed GPS data recorded from the field observation using ArcView GIS 3.2 to generate corresponding image layers and the final images were interpreted using visual interpretation and computer classification methods. Seven classes for the final images were formulated and confirmed through the use of location point data. Table 1 presents the land cover types applied for image classification.
Table 1 Classification system used in this research.
Fig. 1. Present and historical distribution areas of the Tarim red deer in Xinjiang.
No.
Land-cover types
Characteristics
1 2 3 4 5 6
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water bodies Desertified area
7 8
Sandy land Outside area
Cultivated land Coverage over 50e75% Coverage between 25 and 50% Coverage lower than 5e25% River or lake Coverage between 0 and 5% and distribute rare plant species Sand dune without vegetation Unclassified area
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Fig. 2. Location of the study area.
3.3. Analysis of dynamic land-cover change
of the Tarim red deer from 1972 to 2006. Table 3 shows that in the period of 1972e1989, the area of farmland, middle-cover vegetation, low-cover vegetation, water area, and sandy land in the study area increased, while high-cover vegetation and desertified area decreased (see Table 3).
In order to describe the rate at which the land cover types changed during various time periods, we used the following models of land cover change which detect the changes in raw area, proportional change, and annual proportional change of each one of the seven land-cover types (Xu, 2008):
F ¼ Ub Ua=Ua
Table 3 Land cover change of study area (hm2) from 1972 to 2006.
K ¼ F=T 100%
where Ua and Ub represent the initial and final land areas of a certain land cover type, respectively. F is the proportional change of a specific land-cover types; T is the duration length of the study period and K is the annual change rate of a certain land type in a period of time. 4. Results 4.1. Classification of habitat types The land covers that best represent change in habitat of Tarim red deer are classified into seven classes: farmland, high-cover vegetation, middle-cover vegetation, low-cover vegetation, water area, desertified area, and sandy land (see Table 1). Table 2 and Fig. 3 presents the area under different land cover types and the proportion of the total area in 1972, 1989, 2001, and 2006, respectively.
Land-cover types
Changed area (hm2) 1972e1989
1989e2001
2001e2006
1972e2006
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water area Desertified area Sandy land
4695.02 12710.91
1946.72 12367.36
10019.86 9046.5
12768.16 34124.77
1145.12
2576.53
11222.24
9790.83
3549.89
8073.14
5897.4
17520.43
2519.28 1030.62 1946.72
5267.58 2003.98 1545.92
23215.45 3149.09 1030.61
14428.59 4122.45 4523.25
High-cover vegetation was the land-cover type that decreased the most dramatically in terms of the areal extent (12 710.91 hm2) in the period of 1972e1989. In the period of 1989e2001, farmland and middle-cover vegetation decreased and high-cover vegetation decreased the most dramatically in terms of the areal extent
Table 2 Areas of different land cover types (hm2) and their proportions to the total area (%). Land-cover types
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water area Desertified area Sandy land
1972
1989
2001
2006
Area (hm2)
Proportion (%)
Area (hm2)
Proportion (%)
Area (hm2)
Proportion (%)
Area (hm2)
Proportion (%)
14 314.08 56741.02 56912.79 46950.19 54164.48 59374.81 35785.20
2.50 9.91 9.94 8.20 9.46 10.37 6.25
19009.10 44030.11 58057.91 50500.08 56683.76 58344.19 37731.92
3.32 7.69 10.14 8.82 9.90 10.19 6.59
17062.38 31662.75 55481.38 58573.22 61951.34 60348.17 39277.84
2.98 5.53 9.69 10.23 10.82 10.54 6.86
27082.24 22616.25 66703.62 64470.62 39735.89 63497.26 40308.45
4.73 3.95 11.65 11.26 6.94 11.09 7.04
4.2. Dynamic change of habitat Analysis models of land cover change were applied to analyze the temporal and spatial characteristics of dynamic habitat changes
(12 367.36 hm2). In the period of 2001e2006, the areas of farmland, middle-cover vegetation and low-cover vegetation had increased substantially (10 019.86 hm2 and 11 222.24 hm2 respectively) whereas water area decreased by 23 215.45 hm2 and the area of
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Fig. 3. Classified land cover change maps of study area in 1972, 1989, 2001 and 2006.
high cover vegetation continued to decrease. For the entire period of 1972e2006, the areas of farmland, middle-cover vegetation and low-cover vegetation increased by 12 768.16 hm2, 9790.83 hm2, 17 520.43 hm2 respectively. Desertified area and sandy land also increased. In contrast, the areas of high-cover vegetation and water decreased by 34 124.77 hm2 and 14 428.59 hm2, respectively. Table 4 summarizes the proportional changes and the annual rates of change for the time periods 1972e1989, 1989e2001, 2001e2006, and 1972e2006.
land. For the entire period of 1972e2006, farmland changed at the highest rate (2.62% annually) and the high-cover vegetation was the second highest (1.77% annually). 4.3. Habitat fragmentation and its influence on genetic diversity Recent studies showed that the habitat fragmentation in the Tarim Basin has adversely influenced the population size and genetic diversity of the Tarim red deer Xayar population. Mahmut
Table 4 Proportional change and annual rate of change in land cover types of study area, from 1972 to 2006. Land-cover types
Farmland High cover vegetation Middle cover vegetation Low cover vegetation Water area Desertified area Sandy land
1972e1989
1989e2001
2001e2006
1972e2006
Proportional change
Annual rate of change
Proportional change
Annual rate of change
Proportional change
Annual rate of change
Proportional change
Annual rate of change
0.3280 0.2240 0.0201 0.0756 0.0465 0.0173 0.0544
1.929% 1.318% 0.118% 0.445% 0.274% 0.102% 0.320%
0.1024 0.2808 0.0444 0.1598 0.0929 0.0343 0.0409
0.853% 2.341% 0.369% 1.332% 0.774% 0.286% 0.341%
0.5872 0.2857 0.2023 0.1006 0.3586 0.0522 0.0262
11.745% 5.714% 4.045% 2.014% 7.172% 1.044% 0.525%
0.8920 0.6014 0.1720 0.3731 0.2664 0.0694 0.1264
2.624% 1.769% 0.506% 1.098% 0.784% 0.204% 0.372%
Specifically, farmland increased the most in the period of 1972e 1989 (almost 33%). Low-cover vegetation, sandy land, water area and middle-cover vegetation increased by 7.6%, 5.4%, 4.6%, and 2.0%, respectively. High-cover vegetation and desertified area decreased by 22.4% and 17.3% respectively. From 1989 to 2001, farmland and high-cover vegetation decreased by 10.2% and 28.1% respectively, while low-cover vegetation increased by 16%. In the period of 2001e2006, farmland increased by 58.7% while water area decreased by 35.9%. For the entire period of 1972e2006, farmland increased by 89.2%; low-cover vegetation, middle-cover vegetation and sandy land also increased but by lesser amounts. High-cover vegetation showed the greatest reduction (60.1%) and the second greatest reduction was water area (26.6%). Farmland also showed the fastest rate of increase from 1972 to 1989, 1.93% yearly. High-cover vegetation increased at a rate of 1.32% yearly, while low-cover vegetation increased at a rate of 0.44% yearly. In the period of 1989e2001, high-cover vegetation was reduced at a rate of 2.34% yearly, while low-cover vegetation increased at a rate of 1.33%. In the period of 2001e2006, the fastest change was farmland and the slowest rate of change was sandy
et al. (2001) investigated the genetic variations of the Tarim red deer Xayar population using microsatellite DNA method and found that the average observed multilocus heterozygosity Ho was 0.08 0.04. The observed heterozygosities were significantly lower than the expected values. By contrast, the North American red deer have a higher observed mean heterozygosity with Ho ¼ 0.552 0.039 (Talbot et al., 1996). This greatly reduced heterozygosity (Ho ¼ 0.08 0.04) suggests that the population of Tarim red deer in Xayar might have resulted from the observed inbreeding under conditions of suitable habitat decrease that led to population decrease and associated habitat fragmentation that led to inbreeding (Mahmut et al., 2001). Dong et al. (2010) investigated genetic diversity and gene flow in the Tarim red deer population by analyzing 342 base pairs of the mitochondrial DNA controlled region in 34 individuals sample from Xayar, Lopnur and Qarqan. Their results show that the haplotype diversity of Xayar population was 0.893 0.080 and the nucleotide diversity was very low (0.01446 0.000182). Overall, an increasing human population and the related activities of livestock production, uncontrolled agricultural development, harvest of trees and the extraction of mineral
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resources all have contributed to decreasing water resources and reduction and fragmentation of deer habitats in Xayar. Therefore, under the harsh natural environments combined with severe human disturbances, the increased isolation the Tarim red deer population in Xayar promoted the deer for in-breeding and demoted the deer for out-breeding, thus leading and the genetic deterioration of the Tarim red deer. 5. Discussion and conclusions Land cover changes we detected can be attributed to the ecological vulnerability of this region. Plant growth in this area depends mainly on groundwater. Groundwater in turn depends on surface water. If surface water decreases, groundwater level will decline, leading to soil drying and thus plant dying (Hao et al., 2006; Pan et al., 2007). The reported increases in precipitation and in ice-melt water in the Tarim Basin ensure that the total amount of surface water resources has not been reduced during the study period. However, undeniable facts are: (1) river flow in the middle and lower reaches of the Tarim Basin has been dramatically reduced and the groundwater levels at two sides of the rivers in the middle and lower reaches have been declining during the same time (Chen et al., 2010). Apparently, the growth of human population and the associated economic expansion have been the reasons for the observed reductions in the surface runoff and in groundwater levels (Zhang et al., 2003; Ye et al., 2006; Li, 2008). Specifically, agriculture is the primary human activity in this region and water used for irrigation accounts for more than 85% of total withdrawals (Xu et al., 2005). Since the mid-1980’s, with increasing domestic demand for cotton, land has been increasingly exploited, leading to a sharp increase in water consumption (Guo, 2005). This, coupled with petroleum exploitation, has resulted in a serious water shortage in the soil and also a decline in the groundwater level (Wang et al., 2006). Since the 1950s, the human population in the Tarim Basin has expanded rapidly, inevitably exacerbating deforestation and overcultivation in this area, leading to fragmentation of wildlife habitats (Wang et al., 2006). Total human population of Xayar County was 115 000 in 1970 and nearly doubled to 207 000 in 2003. The agricultural population increased by 54% from 108 000 in 1970 to the 166 000 at the end of 2003 (Statistical Yearbook of Xayar, 2004). Our results show that expansion of agricultural activities was mainly associated with conversion of high-cover vegetation to other forms of land covers. Field interviews with local farmers and observations substantiated that most woodland and shrub lands were cleared for agriculture. Reclamation and subsequent abandonment of cultivated land in some areas have not only destroyed natural grasslands and shrub lands but also loosened the ground surface and undermined the protective layer, further exacerbating desertification and sandstorm generation. The Tarim red deer prefers habitats with high-covered vegetation and rich food resources near water bodies but far from human disturbances (Anwar et al., 2008). We found that high-cover vegetation decreased in the period of 1972e2006. We attribute most of these changes to human activity. We also observed that red deer signs (or imprints) were frequently found on farmlands where human disturbance is common. This suggests that the Tarim red deer has begun to search for food and water around farmlands although the human threat is imminent. We conclude that the Tarim red deer habitat in the Xayar and Kuqa area has declined because of the expansion of human activities and the decline has resulted in the decrease in their population. The human-induced fragmentation of the habitat seems to be a major contributing factor to the observed genetic deterioration of the Tarim red deer. Management interventions are needed to reverse these trends.
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