Plateau Wetlands, an Indispensible Habitat for the Black-Necked Crane (Grus Nigricollis) - a Review

Wetlands (2014) 34:629–639 DOI 10.1007/s13157-014-0559-5

REVIEW

Plateau Wetlands, an Indispensible Habitat for the Black-Necked Crane (Grus nigricollis) - A Review

Hongtao Song & Yinsheng Zhang & Haifeng Gao & Yanhong Guo & Shengnan Li

Received: 24 November 2013 /Accepted: 19 June 2014 /Published online: 6 July 2014 # Society of Wetland Scientists 2014

Abstract As a highly productive and sensitive ecosystem, wetlands (BirdLife International 2001). The existence of plateau wetlands provide indispensable habitats for Grus Grus nigricollis was unknown until 1876 due to the high nigricollis, an endangered species of crane. However, the altitude and low temperature of its habitat. In the 1980s and destruction and degeneration of plateau wetlands caused by 1990s, surveys of Grus nigricollis mainly focused on the climate change and human disturbance have influenced the birds’ overwintering sites and population counts and included habitats and biological behaviors of Grus nigricollis. Previous preliminary research into the ecology of these overwintering studies have ignored the importance of particular habitats to sites (Wang et al. 1989; Zhang and Luo 1991;LiandMa the continued existence of Grus nigricollis,especiallywith 1992;Yuetal.1993;Chen1994, 1997;Lietal.1997). Since regard to extremely fragile plateau wetland systems. In this 2000, studies have been carried out into the cranes’ individual review, the importance of plateau wetlands for the breeding, behaviors, foraging habits, reproductive behaviors and migra- overwintering and foraging of Grus nigricollis is summarized; tory routes (Li and Ma 2000;BishopandLi2002;Yangetal. the impact of human activities and climate change on Grus 2006; Gao et al. 2007;Yangetal.2007). nigricollis and on plateau wetland habitats is also presented. However, previous studies and related species conservation Further monitoring and research is required to produce sub- management attached importance only to population numbers stantive suggestions vis-à-vis future, and better, conservation and to the biological behavior of this species; they ignored the of Grus nigricollis and its habitats. significance of particular habitats to Grus nigricollis,especially the extremely fragile plateau wetland system as impact- Keywords Grus nigricollis . Habitat change . Plateau ed by climate change and increasing human disturbance. wetlands . Climate change . Human activity Habitat change can destroy the living space of wildlife and lead to reductions in populations or even species extinction (Didham et al. 1998). This review intends to summarize related data and research results from previously-published Introduction literature to emphasize the importance, and initiate the better conservation, of wetland habitats indispensable to the black- The black-necked crane (Grus nigricollis), an endangered necked crane. This is designed not only to enhance research species, is a large wader with the largest body size of the into the populations and behavioral ecology of this species, world’s 15 crane species. It is the only crane that inhabits and but also to facilitate an improvement in the management of reproduces in high plateau (2500–5000 m asl) freshwater regional nature reserves.

H. Song (*) : Y. Zh an g : H. Gao : Y. Guo Institute of Tibetan Plateau Research, Chinese Academy of Sciences, No. 16 Lincui Road, Chaoyang District, Beijing 100101, People’s The Importance of Plateau Wetlands for the Breeding Republic of China of Grus nigricollis e-mail: [email protected] The breeding areas of Grus nigricollis are located prin- S. Li Institute of Wetland Research, Chinese Academy of Forestry, cipally in the northeastern sector of the Qinghai-Tibet Beijing 100091, China Plateau (TP) (Li 2005). More than 33 breeding sites 630 Wetlands (2014) 34:629–639 have been identified in Tibet, Xinjiang, Western Qinghai The Importance of Plateau Wetlands as Wintering Areas and Northern Sichuan (Fig. 1); breeding altitudes range for Grus nigricollis from 3400 m asl (this being the lowest, located in Ruo’ergai County, Sichuan) to 4,850 m asl (this being Overwintering sites of Grus nigricollis are mainly distributed the highest, identified at Ngari, Tibet) (Kuang et al. in the midstream river valley of the Yarlung Zangbo River in 2010;Wangetal.2013). the TP, the Lhasa River and the Nianchu River (a tributary of As indicated by many studies, the breeding sites of Yarlung Zangbo River) (Fig. 1), as well as on the southern Grus nigricollis are concentrated in plateau meadows, slopes of the Himalaya and the Yunnan-Guizhou Plateau (Li swampy meadows and marshes, where herbaceous 1997, 2005). Over 4200 Grus nigricollis overwinter in plants are abundant (Zhang and Luo 1991; Kuang Tibetan wetlands, accounting for about 80 % of the total et al. 2010). Grus nigricollis prefers to nest in mounds global overwintering population (Bishop and Drolma 2007). (or small islands) in shallow-water wetlands with low Populations at Dashanbao and Napahai in Yunnan Province vegetation, and uses the deep mud layers near its nest and Caohai in Guizhou Province constitute the bulk of Grus to escape from predators or to prevent the nest from nigricollis wintering outside Tibet in China. being flooded (Dwyer et al. 1991;LiandLi2005; The size of overwintering populations and the behavior Kuang et al. 2010;Wangetal.2013). Research on displayed by colonies of Grus nigricollis are closely associat- Grus nigricollis breeding in northern Tibet revealed that ed with the environment found in their habitats. The all nests were built close to uncovered water surfaces on overwintering environment is a key factor affecting the birds’ island-shaped highlands with a water depth of 15±2 cm; adaptive instincts, and changes in overwintering population shallow-water peat bogs and Carex meadows were es- size reflect the adaptability or otherwise of Grus nigricollis to pecially preferred by Grus nigricollis (Kuang et al. environmental disturbance. Factors that directly influence the 2010). It has also been reported that the breeding overwintering of Grus nigricollis include the geography of, Grus nigricollis populations of different districts tend and food supply found in, their habitats (Wang et al. 2007). to select different types of habitats. For instance, the Lei et al. (2012) studied 11 night-time overwintering resting Tebo breeding population prefers shallow-water peat sites in Tibet and found that Grus nigricollis prefers shoals, bog, whereas the Caohai population prefers sedge mead- open warm rivers and leeward wetlands. Li (1999, 2005) ow (Li 1999), and the overwintering population of further determined that Grus nigricollis prefers marshes con- Napahai Lake and the breeding population of Xiaman taining Juncus leucomelas and Chenopodium prostratum as prefer marshes (Zhao et al. 2008; Ran et al. 1999). All its overwintering sites. At Napahai Lake in Yunnan Province, of these habitats are closely related to wetlands, these the Grus nigricollis population displays the highest utilization being the perfect sites for food, energy and shelter for rate of marshes over the entire overwintering period—here, breeding colonies of Grus nigricollis. about 60 % of individuals prefer marshes as their main Overexploitation of plateau marshes, mudflats and lakes in overwintering habitat (Zhao et al. 2008). This finding high- the northeastern TP since the 1960s has severely affected the lights the critical importance of marshes for overwintering breeding patterns of Grus nigricollis and has thus caused colonies of Grus nigricollis. Yu et al. (1993) studied 38 fluctuations in their population numbers. Ruo’ergai County, overwintering populations in the upper Lhasa River and re- Qinghai Lake Basin, Longbaohu County, the TP, East Kunlun vealed that Grus nigricollis distributions over lakeshore Mountains and Altun Mountains, the main breeding sites of meadows, river shoals, and wetlands/wet river shoals Grus nigricollis, have, over the past decades, suffered great accounted for 34.2 %, 26.4 % and 26 % of the total, respec- wetland loss at an average rate of 1.22 % per annum (Table 1). tively. At Kuang et al. (2008) found that Grus nigricollis chose Qinghai Lake and Eling Lake used to be major breeding sites swampy meadows as their principal overwintering sites, with of Grus nigricollis; however, due to the construction of fish their annual utilization second only to that of farmlands. farms and roads, these breeding habitats have been destroyed, Moreover, wetlands also provide shelter from predators of leading to a drastic decrease in numbers (Yao 1982). Wetland Grus nigricollis. Liu et al. (2008) discovered that the shrinkage in the TP at a rate of almost 0.14 % per annum from overwintering Grus nigricollis population of Napahai Lake 1990–2006 has posed the main threat to breeding habitats, this mostly preferred their night-time resting sites to be on lakesides being equivalent to 186 km2 of possible habitats disappearing or at the confluence of ravine streams, these being shallow-water every year (Table 1). The Ruo’ergai wetland, a vital breeding areas with water depths over 10 cm that are not easily traversed and stopover site along Grus nigricollis’ migratory pathway, by land-based predators. lost near 40 % of its breeding habitat from 1975–2006, suf- Wetland loss and degeneration in China pose major fering a shrinkage rate of 1.23 % per annum (Table 1). Plateau threats to populations of overwintering Grus nigricollis. wetland conservation is thus critical for the normal breeding Human activities such as irrigation projects, dam con- and sustainable growth of the Grus nigricollis population. struction, drainage and reclamation, transformation of Wetlands (2014) 34:629–639 631

Fig. 1 Overwintering and breeding sites and nature reserve distribution of Grus nigricollis in China as recorded by previous studies uncultivated land to farmland, river canalization, (6,560 km2, accounting for 0.17 % of the total area) (Fig. 1). overgrazing, sedimentation and influxes of industrialized As revealed by many studies, Caohai, Napaihai, Dashanbao populations pose serious threats to the birds’ and Huize, the four most important wintering sites in China, overwintering sites (Bishop 1996;LiandLi2005). have all suffered great wetland loss during the past few de- The Kazi Reservoir in Tibet, which used to be a big cades, with an average per annum loss of 3.07 %, much overwintering site for Grus nigricollis, is shrinking due greater than for the breeding regions (1.22 %) (Table 1). to lake exploitation, fish farm construction, marsh rec- Although the overall population of Grus nigricollis has ap- lamation and expansion of pastureland (Lei et al. 2012). peared to increase in recent years (Table 1), the specific year- In the Napahai wetland in Yunnan, water coverage has to-year population size has shown unstable development declined repeatedly and sharply over the past 40 years trends vis-à-vis historical loss of wetland habitats. For in- from the mid-point of the period hosting the overwintering stance, the population of Grus nigricollis in Caohai from Grus nigricollis population, leading to serious drought by the 1975 to 1984 increased, then decreased continuously until end of the period. Combined with the damaging effects of 1991; the overwintering population in Napahai suffered a overgrazing, such changes in the area of water coverage dramatic decline from 2002 (292 individuals) to 2004 constitute a significant threat to the overwintering Grus (245 individuals), with a reduction rate of 16 %. nigricollis population of the region (Tian et al. 2004). Constant shrinkage of overwintering sites not only cre- Heqing County in Yunnan Province was once an important ates interspecific competition, but also intensifies the overwintering site for Grus nigricollis, but the shallow-water conflicts between Grus nigricollis and local residents marshes in the region have now disappeared in tandem with (Bishop and Li 2002). Therefore, in addition to ongoing the appearance of more farmland and fish ponds, making this research, further studies of the use of lakes, rivers and region no longer suitable for overwintering (Wei 1994). marshes as stopover sites along migratory routes and as China has established different categories of nature re- pre-wintering sites of Grus nigricollis need to be con- servesbasedonthenaturalhabitatsofGrus nigricollis. ducted. Furthermore, changes in the environment of However, of the 18 conservation zones covering a total area such stopover sites in the early and later stages of the of more than 383,000 km2, only six are overwintering sites overwintering period should also be addressed. 632 Wetlands (2014) 34:629–639

The Importance of Plateau Wetlands for Foraging 2013 by Grus nigricollis

Grus nigricollis feeds on plant seeds, roots and stems of aquatic 2008 ;Douetal.

2012 or semi-aquatic plants, small-sized fish, small-sized mammals

1991 and reptiles, insects and other invertebrates (Table 2) (Hu et al. 1985 2012 2000 2002;Lietal.1997, 2005;HeandHu2000;Lietal.1997;He 2009 2004 2006 ;Chenetal. ;Qietal. and Hu 2000;Liuetal.2006; Zhang 2010;Luetal.1980). 1982

2012 Wetlands are major sources of food in that they provide abun- 2011 dant water resources and animal/vegetative food for popula- Zhang et al. tions of Grus nigricollis. The major foraging grounds for Grus nigricollis, namely farmlands, mudflats, shallow-water marshes andswampymeadows,areusually located away from sites of human aggregation (Han 1995;LiandLi2005). Furthermore,

Average loss ratio distance to any water resource is the most important factor influencing foraging crane flocks (Liu et al. 2006). In overwintering regions, Grus nigricollis spend more than 20 % of the day-time foraging along the river (Bishop et al.

Annual loss ratio 1998), and aquatic or semi-aquatic plants provide a great variety of vegetative food for Grus nigricollis (Table 2). Of these,

habitats in China wetland sedge (Cyperaceae) plants account for a significant 2006) 0.14 % Xing et al. – 1999) 1.08 % Zhang et al. 2006) 6.89 %proportion Li (approximately 76.54 %) of all the vegetative food – – 2006) 1.23 % 1.22 % Yang and Wang ) 2 – 2001) 4.33 %species; Tian et al. underground plant tubers provide the bulk of food 2000) 2.37 % Yao – 2012) 0.46 % 3.07 % Liu – 2006) 2.57 % Liu et al. – – foraged by Grus nigricollis, followed by stalk-like stems, 2008) 1.14 % Li and Zhou – flowers, fruits/seeds and leaves (Li et al. 1997). Li et al. (1997) Grus nigricollis 131894 (1990 0.0548 (1965 0.0041 (1992 – – 22.46 (1975 analyzed the food sources of the Grus nigricollis populations in – 847 (1977 – 0.376 (1981 – 192 (1992 – 50 (1985 23.25 (1958 – Caohai, Guizhou Province, and found that of all 47 plants – – 1860 0.0864 ––– (Period) Wetland changeArea Variation (km Reference foraged by Grus nigricollis,12weresubmergedandsixwere floating-leaved plants, including Scirpus triqueter L., S. yagara, S. validus and S. triangulates (Table 2). Wu et al. (1985) dissect- 2007) 134864 – 2010) 300 ed deceased Grus nigricollis in Caohai for two consecutive years 2012) 35.89 2010) 31 – 2011) 70 – 2011) – 2009) 2.82 2009) 0.1179 – – – – and found mostly tubers of the dominant marsh species (Sparganium stoloniferum) in the stomachs of four cranes. This

6490 (1990 confirmed that the wetland is a major food source for the – 287 (1991 1062 (1989 144 (1985 – 260 (1991 1000 (1975 334 (1984 287 (1986 – – – – – – overwintering Grus nigricollis. In addition, wetlands contain – – (Period) large quantities of soil invertebrates, snails and fish, which provide a major animal food source for overwintering Grus ypical breeding and overwintering regions of nigricollis (Li et al. 2009;Li2011). Liu et al. (2008)andZhao et al. (2008) suggested that fish, Misgurnus anguillicaudatus and Corbicula aurea in shallow-water areas during the early overwintering period also provide a certain amount of food for Grus nigricollis. In some overwintering sites in northeastern Yunnan Province, Tabanus sp., Delia sp ., Metabolus flavescens, Carassius auratus and Pseudorasbora parva are also foraged by ergai 239 ’ Grus nigricollis (Hu et al. 2002;HeandHu2000). Longbaohu 22 Qinghai-Tibet Plateau 3041 Qinghai lake basin East Kunlun and Altun Mountains 12 Napaihai 53 Dashanbao 116 Changhai of Huize 26 Lalu In breeding regions, Grus nigricollis prefer to forage in water bodies near their nests; families and flocks like to forage near water bodies 100–500 m distant, especially in swamp- land (Lu et al. 1980; Kuang et al. 2010). Relatively significant proportions of plant seeds, roots and stems of aquatic or semi- Population number changes and wetland loss in t aquatic plants are also foraged by Grus nigricollis:sucha diverse food supply has, in turn, been demonstrated to boost Breeding regions Ruo Overwintering regions Caohai 35 Habitat type Region Population change Table 1 significantly the sizes of the foraging flocks and breeding Wetlands (2014) 34:629–639 633

Table 2 Typical vegetative food resources found in breeding and overwintering regions of Grus nigricollis wetland habitats

Habitat type Family Name Species Name Root Stem Leaf References

Characeae Chara spp . Li et al., 1997; He and Hu, 2000 Halorrhagaceae Myriopyllum spicatum Callitrichaceae Callitriche stagnalis Ceratophyllaceae Ceratophylum demersum Hydrocharis dubia, Hydrilla verticillata, Hydrocharitaceae Vallisneria gigantean Potamogeton distinctus Potamogetonaceae Potamogeton perfoliatus, Potamogeton crispus, Potamogeton Overwintering He and Hu, 2000 malainus, Potamogeton pectinatus, Potamogeton pusillus, regions Juncus allioides, Juncus castaneus, Juncus concinnus, Juncaceae Juncus setchuensis, Zizania caduciflora Araceae Acorus gramineus Lemnaceae Spirodela polyrrhiza Polygonaceae Polygonum orientale, Polygonum amphibium Cyperus niveus, Cyperus duclouxii, Eleocharis quinqueflora, Li et al., 1997; He and Hu, 2000; Cyperaceae Scirpus validus, Juncellus seretinu, Pycreus sanguinolentus Liu et al., 2006; Zhang, 2010 Potamogetonaceae Potamogeton pectinatus Zhang 2010 Breeding Ranunculaceae Batrachium bungei Kuang et al., 2010 regions Rosaceae Potentilla anserina Lu et al., 1980 (○-inedible, -edible, ●-preferred) season populations (Hu et al. 2002; Li et al. 2005). Grus Plateau wetlands are gradually shrinking and deteriorating nigricollis feed on more wetland plant species in breeding because of furrowing, drainage, swamp reconstruction, high- regions than in overwintering regions; for instance, radix intensity grazing and tillage. In the meantime, meadow and rubiae (Potamogeton petinatus), Batrachium bungei and marsh degeneration continues to occur and wetland vegetation Potentilla anserine are also found to be a food source in the is being either destroyed or transformed in the process, caus- breeding regions of northern Tibet and Qinghai (Table 2) ing significant reductions in the vegetative food reserves that (Kuang et al. 2010). Further, Grus nigricollis in wetland can be utilized by Grus nigricollis (Wu and Li 1985; Ran et al. breeding regions tend to forage for more small-sized fish, 1999). In addition, the animal food source of Grus nigricollis small-sized mammals and reptiles, insects and other inverte- is also endangered as wetlands favorable for the survival of brates than they do in wetland overwintering regions (Kuang insect larvae are being lost through desertification (Hu et al. et al. 2010;Luetal.1980). In Bange County, Tibet, even bar- 2002; Gao et al. 2012). For instance, the number of Corbicula headed goose (Anser indicus) and ruddy shelduck (Tadorna fluminea, one of the most important animal foods for Grus ferruginea) fledglings were found to be foraged by Grus nigricollis, has proven to have sharply decreased along with nigricollis during the breeding season (Lu et al. 1980;Liand the degeneration of the Napahai wetland (Table 3)(Tian Li 2005; Kuang et al. 2007). This phenomenon indicates that, 2004). When natural food sources are insufficient to meet when breeding, Grus nigricollis tend to forage for more demand, farmlands on the periphery of wetlands become the animal food than vegetative food, perhaps related to the phys- new food sources for overwintering Grus nigricollis.In iological characteristics concomitant with frequent excretion Huize, Yunnan Province, extensive loss of wetland and mead- and hunger intolerance (Zhang and Xiao 2000), and the great- ow has led Grus nigricollis to forage for seeds, radish and er energy requirements of the breeding period. potato from farmland, causing significant economic loss Thus, the primary reason why Grus nigricollis chooses to the local farmers and an escalation in the competition wetlands as its foraging habitat source is that the wetland for land between human and cranes (Li et al. 2009). provides abundant vegetative and other energy-rich foods Grus nigricollis in Guizhou Province also forage for such as aquatic animals (Han 1995;LiandLi2005). food in farmland, and, as a countermeasure, local Moreover, the loose wetland soil makes it easier for farmers use dogs to drive them away (Han 1995). Grus nigricollis to forage in deeper layers of the soil. Thus, the destruction and degeneration of wetlands di- The third reason is that wetlands are usually far from rectly impacts the survival of Grus nigricollis and fur- human interference and are thus the safest place for ther aggravates the conflict between humans and cranes. foraging (Kuang et al. 2010). This can also lead to increased interspecific and 634 Wetlands (2014) 34:629–639

Table 3 Number of Corbicula fluminea fed on by Grus nigricollis in behaviors and even survival of Grus nigricollis (Zhao et al. different habitats, Napahai (Tian 1989) 2008). Due to wetland overexploitation and pollution, the Number Primary Swampy Meadow Reclaimed number of overwintering sites for Grus nigricollis in Yunnan swamp meadow wetland Province decreased from 20 in the 1990s (Li 1996)to12in 2002; today the remaining overwintering sites, which now Alive 100 48 2 0 number 10 or fewer, are ecologically unstable (Li and Yang Dead 1.5 24 28 0 2003; Liu et al. 2010). Similarly, Caohai County in Guizhou Province implemented a wetland drainage and reclamation project starting in the late 1950s, and the wetland area de- intraspecific competition in the environs of habitats or creased sharply until 1982, when the water surface was rein- even the abandoning of its habitat by Grus nigricollis. stated. As a result of this recovery, the number of Grus nigricollis intheregionrosefrom35in1975to305in1984 (Wu and Li 1985). Related research in Bhutan has also revealed Human Influence on Wetlands Inhabited by Grus that residential expansion, expansioninlanduseandtillage nigricollis modes have had a decisive impact on Grus nigricollis habitats (Bishop 1996; Meine and Archibald 1996; BirdLife Wetlands are highly productive ecosystems intermediate be- International 2001; International Crane Foundation 2004). At tween water and land with a rich biodiversity and ecology. least three typical overwintering sites in that region were grad- They provide a major habitat for the overwintering, resting ually abandoned by Grus nigricollis due to changes in land use and breeding of birds (Samraoui and Samraoui 2008). The and intensifying human activity (Lhendup and Webb 2009). availability of an ample water supply near wetlands makes Another major overwintering region for waterfowl, the them centres of human aggregation, which in turn displaces Lhasa River Basin, together with the adjacent Yamdrok the resident wildlife population. Historically, human activity Lake, provides sites for at least 115 rare bird species including in wetland regions has been closely related to reductions in Grus nigricollis, Tadorna ferruginea and Anser indicus Grus nigricollis populations, although their numbers have (Fig. 1). A recent study showed that overwintering selection been increasing in China over the past decades (Harris 1994; intensity for Grus nigricollis in the marshes along the Lhasa Bishop 1996; Meine and Archibald 1996;BirdLife River Basin is as high as 85.52 % (Tsering et al. 2009). During International 2001). The habitats of Grus nigricollis are the past thirty years, natural wetlands in the drainage basins disappearing or deteriorating because of changes in con- near Lhasa City and the major neighboring counties have ventional tillage modes, extensive reclamation and utili- shrunk and deteriorated due to human activity (Liu et al. zation of wetlands, riverside tree plantations, dam con- 2006;Langetal.2007; Pan et al. 2007). Heavy loss of natural struction, farmland expansion and water body pollution wetlands and farmland has caused a significant destruction of (Li 2005;Qianetal.2005). the overwintering habitats, and a decline in the populations, of In overwintering regions, such negative activities have had wading birds such as Grus nigricollis and Anser indicus.For a particularly significant effects on the Grus nigricollis habi- example, a program of conversion of farmland to forest has tats. For instance, large areas of marsh in Huize were sub- been implemented in the Lhasa River Basin since 1998; Salix merged by the elevation of the water level in a nearby reser- L., Populus L., and Hippophae rhamnoides have been planted voir in 2005, leading to a reduction in night-time resting sites extensively in this region. As a result, the area of marshland for Grus nigricollis (Li et al. 2009). Haizi and Dashanbao in has been declining year after year, seriously affecting the Xundian County suffered slope erosion along their reservoir night-time resting environment of Grus nigricollis (Bishop banks and serious water and soil loss due to wetland destruc- and Li 2002). In addition, some wetlands in the Basin that tion, which in turn led to a shrinkage in Grus nigricollis are natural habitats for Grus nigricollis have been converted to habitats (Chou et al. 1995). In Heqing County, a large portion farmland (Cangjue et al. 2008), and water conservancy efforts of wetland was reclaimed as farmland and fish ponds, and coupled with the artificial diversion of river courses for irri- shallow-water areas and marshes could no longer be inhabited gation and flood control have disrupted the original wetland by Grusnigricollis. In the Dashanbao Conservation Zone, the landscape pattern, reducing the number of night-time resting grass layer and peat were dug up from the bogs to be used as sites for Grus nigricollis (Bishop et al. 1998). Likewise, Grus fuel, directly resulting in water and soil loss and serious wet- nigricollis overwintering sites in the Kazi Reservoir area of land sedimentation; as a result, the number of overwintering Linzhou County have been shrinking due to lake exploitation, sites available for Grus nigricollis in this area has been fish farm construction, marsh reclamation and an expansion in declining every year (Rank 1994). In the Napahai Lake pastureland (Lei et al. 2012). Notably, some studies also region, the wetland is shrinking and deteriorating because suggest that other seemingly innocuous human activities over of trampling by tourists, thus greatly affecting the normal the past 20 years such as the construction of extensive Wetlands (2014) 34:629–639 635 networks of power transmission lines along the drainage basin has been predicted that by 2100, the land surface temperature (Bishop and Tsamchu 2005) may have had significant impact will have risen by 3.5°C, resulting in the extinction of 600– on Grus nigricollis habitats (Lang et al. 2007). 900 bird species (Sekercioğlu et al. 2012). Average tempera- Similarly, the human impact in the breeding regions of tures on the TP have been 0.74°C higher than the global Grus nigricollis has been significant. For instance, more than average over the last hundred years (Du et al. 2004;IPCC 0.09 km2 of the Balikun wetland in Xinjiang has been blighted 2007). This poses a significant threat to the diversity of species by coal ash deposition contamination due to the construction that rely on plateau wetlands for survival. of a power station; the human population settling around The Ruo’ergai wetland is a major breeding for Grus wetland areas in the Qinghai Lake Basin has increased by nigricollis in China. Six out of 17 lakes in this wetland totally 15 % from 1982 to 2005, whereas the livestock number is now dried up during 1985–2000, and the wetland area shrank by more than threefold that of 50 years ago (Qi 2012). These about 6.6hm2;thishashadagreatimpactontheGrus increases in human influence have dramatically damaged nigricollis population (Harris and Mirande 2013); The wet- wetland areas and thus reduced Grus nigricollis habitats. lands in the eastern Kunlun and Altun Mountains of Xinjiang The Three Rivers Source region, an important breeding and that are suitable breeding habitats for Grus nigricollis are stopover site for Grus nigricollis, has experienced gold mining, constantly shrinking due to changes in temperature and pre- excavation of medicinal materials and slashing and burning of cipitation distribution (Zhang et al. 2012). Meteorological data shrubland since the 1980s, leading directly to water loss and from 1961 to 2000 indicates that rising temperatures and soil erosion in the upstream wetland habitats of Grus nigricollis increased evaporation in the Qinghai Lake Basin are princi- (Huang 2005). The Ruo’ergai Wetland in Sichuan Province pally responsible for the significant shrinkage in seasonal and was also artificially drained in the mid-1960s to create grass- permanent river wetland (Chen et al. 2008), indirectly land, resulting in the dual effect of marsh shrinkage and grass- influencing the breeding habitats of Grus nigricollis in this land degeneration. Consequently, the marshy area suitable as a region. Climate change has also had an impact: the glaciers in breeding site for Grus nigricollis declined dramatically (Harris the Lhasa River Valley are retreating due to higher tempera- 1994). Construction of the S204 Expressway along the Yarlung tures, and vegetation composition has changed accordingly, River in Xietongmen County in Tibet has led to the disappear- significantly impacting the overwintering habitats of Grus ance of small Grus nigricollis populations living within 100 m nigricollis in this region (Lang et al. 2007). of the expressway (Bishop et al. 2012). Climate change increases the risk of extinction for species Diverse human activities have been expanding at the ex- dependent upon a narrow range of habitats or that exhibit poor pense of wetlands inhabited by Grus nigricollis, which are adaptation to climate. For many bird species throughout the becoming increasingly fragmented. The distances between world, populations are declining and/or habitats are habitat patches are increasing, whilst the number of habitats disappearing (Baral 2002; Wormworth and Mallon 2006). available to Grus nigricollis is declining. In addition, growth However, it remains unclear which specific parameter of in tourism in India and China has had negative impact on the climate change reduces the habitats of plateau birds biodiversity of wetlands (Tian et al. 2004; Ranade 2008). (Doswald et al. 2009). By taking Grus nigricollis as a typical Even though the reasonable use of wetlands has been advo- narrow-habitat-range species, the influence of climate change cated for many years (Baral and Bhandari 2011), the gap on the population size and habitats of this bird can be system- between theoretical proposition and practice remains huge. atically studied on various temporal-spatial scales in breeding Furthermore, finding a balance between economic develop- and overwintering regions. Here, understanding the ability of ment and habitat conservation is an important part of Grus nigricollis to adapt to changes in climate and habitat protecting Grus nigricollis and its habitats. structure, and identifying specific strategies adopted to cope with these changes, is crucial for maintaining long-term survival of this species in climate-sensitive regions. The Influence of Climate Change on Grus nigricollis and Its Wetland Habitats Discussion Against the backdrop of global climate change, rising temperatures, the melting of glaciers, reduced rainfall and increased The choice of natural habitats by wild animals depends on evapotranspiration, there have been significant changes in maximum energy use efficiency, nutrient balance and mini- water distribution patterns in high-altitude regions (Ye et al. mum predation risk (Kie and Bowyer 1999;McSheaetal. 2007; Zhang et al. 2011). Consequently, the wetland land- 2001). The dependence of Grus nigricollis on water and scape pattern has been modified, resulting in a persistent plateau wetlands is a reflection of its instinctive needs for reduction in narrow-habitat-range species that depend on wet- energy, nutrients and security. Unfortunately, plateau wetlands lands for breeding and resting (Harris and Mirande 2013). It in China have been seriously endangered, and most wetlands 636 Wetlands (2014) 34:629–639

Fig. 2 Propaganda and education notice in Yarlung Tsangpo Black- Necked Crane National Nature Reserve. (a Billboard in Yarlung Tsangpo Black-Necked Crane National Nature Reserve in Linzhou County, Lhasa; b Damaged billboard about plateau wetland conservation. Photograph taken by author, 2013)

have been either transformed or lost because of climate environments away from possible human interruption: breed- change and human activity (Want et al. 2007; Bai et al. ing sites in China are located in sparsely-populated regions, 2005;Lietal.2003). With respect to breeding and but breeding area shrinkage and wetland degeneration have overwintering habitats for Grus nigricollis, plateau wetlands also led to a wider variety of animal and plant species being are equally important. Overwintering sites in China are almost foraged by Grus nigricollis. all located within tourist destination areas, especially in Yunnan, Guizhou and the Lhasa River Basin. Frequent human disturbance, together with climate change, has resulted in Research and Monitoring Needs greater wetland habitat loss and damage in overwintering areas than in breeding regions, especially vis-à-vis major Being the main habitat of Grus nigricollis, an accurate and climate events, such as the droughts and seasonal extenuation dynamic assessment of the current situation in plateau wet- experienced in Yunnan Province. Habitat shrinkage combined lands accompanied by an analysis of the causes of change are with food shortages during the overwintering season have led important for identifying the underlying reasons for the de- directly to conflict between humans and Grus nigricollis and cline in number and the endangered status of this rare species. consequent unstable population fluctuations. In breeding re- Previous research on Grus nigricollis habitats has mainly gions, wetland habitats have suffered less destruction or de- focused on qualitative or quantitative descriptions over short generation, perhaps explaining the instinctive reaction implied timescales. The influence of changes in wetland landscapes on in the selection by populations of Grus nigricollis of safer the populations and biological responses of Grus nigricollis Wetlands (2014) 34:629–639 637 using a variety of spatial-temporal scales has never been use in conserving and rebuilding Grus nigricollis habitats. attempted. Furthermore, temperature-precipitation patterns Every year, the Pengbo District of Linzhou County, the and the water landscape in the Tibetan Plateau have been Lhasa River and other tributaries suffer from seasonal found to have dynamically and significantly changed during flooding. Effective management of this problem is impor- the past few decades (Zhang et al. 2011; Yao et al. 2012). It is tant for protecting the natural habitats of Grus nigricollis. not known whether the population size and the habitat selection of Grus nigricollis have altered along with long-term changes in the region’s water and wetland landscapes. Future Focus Behaviors and biological characteristics, such as breeding site selection, reproduction numbers, sex ratio, and adaptive The chances of survival for young Grus nigricollis migrating foraging and wintering mechanisms, may well have changed from their breeding to their overwintering sites along the over large temporal and/or spatial scales, and future studies Lhasa River are rather low. Whether this is related to human should address these topics. In addition, the stopover sites activity or to changes in wetland landscape remains to be found along the migratory route of Grus nigricollis are mostly investigated. Some Grus nigricollis populations are now wetlands. Gao et al. (2007) found that the 13 Grus nigricollis found on dry land in the Lhasa River Basin, where they prefer migratory route stopover sites in Dabaoshan, Yunnan the leeward slope of the valley or cultivated land and/or Province were all located in mudflats, alpine lakes, alpine farmland for night-time resting. Can such changes in their swampy meadows and alpine meadows. As shown by a study habits be attributed to the destruction of their habitats? What of the migratory route of Grus nigricollis in 2005–2007 by are the potential driving factors behind changes in their inter- Qian et al. (2009), 14 out of the 20 stopover sites located in 12 action with the environment and with habitat selection? Do counties were typical wetlands (70 %) and two were located in such adaptive changes affect the biological responses and lake areas (10 %). The migration of Grus nigricollis provides healthy development of the population? These questions need an important link between breeding and overwintering, and to be addressed in future studies in order to develop an the environment of its stopover sites largely determines the effective program of intervention. success rate of its migration. Changes to wetlands that serve as sites for breeding, overwintering, and resting during migra- Acknowledgments Thanks to our group from the Institute of Tibetan tion, and the impact of such changes upon the population size Plateau Research, Chinese Academy of Sciences, especially to Dr. and biological responses of Grus nigricollis therefore need to Haifeng Gao and Yanhong Guo for support conducting wetland field surveys and investigations. This study was funded by the Major State be systematically studied. Basic Research Development Program of China (973 Program) (Grant No. 2010CB951701). The research was also supported by the Strategic Priority Research Program (B) of the Chinese Academy of Sciences Improvements in Conservation (Grant No. XDB01030300).

The measures that have been adopted for the protection and management of Grus nigricollis habitats are far from perfect. References Firstly, scientific and local communities should both be in- volved in the regional strategy for Grus nigricollis conserva- Bai JH, Ouyang H, Yang ZF, Cui BS, Cui LJ, Wang QG (2005) Changes tion. In particular, local communities urgently need help in in wetland landscape patterns: a review. Progress in Geography 4:005 Baral HS (2002) Impact of climate change on Nepal’s birds. Danphe 11:6 becoming better informed about the comprehensive conser- Baral HS, Bhandari BB (2011) Importance of high altitude wetlands for vation of this species; their cooperation with a scientifically- protection of avian diversity in the Hindu Kush Himalayas. The based, effective and expanding program of conservation is Initiation 4:96–102 essential. In northern Yunnan and the middle reaches of the BirdLife International (2001) Threatened birds of Asia: The bird life Yarlung Tsangpo Valley, local Tibetans do not hurt wild international red data book. BirdLife International, Cambridge Bishop MA (1996) Black-necked crane (Grus nigricollis). In: Meine CD, animals in tune with their religious beliefs, but, in contrast, Archibald GW (eds) The cranes: Status survey and conservation they have no real grasp of how the expansion of farmland and action plan. IUCN, Gland, Switzerland, pp 174–179 the drainage of wetlands is endangering the Grus nigricollis Bishop MA, Drolma T (2007) Tibet autonomous region January 2007 population (See Fig. 2). Secondly, nature reserve manage- survey for black-necked crane, common crane, and Bar-headed goose. China Crane News 11:24–25 ment methodology should fit the ecological needs of Grus Bishop MA, Feng-Shan L (2002) Effects of farming practices in Tibet on nigricollis. For instance, the wetland area of the Dashanbao wintering black necked crane (Grus nigricollis)dietandfoodavail- Black-Necked Crane National Nature Reserve in Yunnan ability. Biodiversity Science 10:393–398 increased from 300 ha in the 1990s to 3,150 ha in 2004, but Bishop MA, Can JZ, Song YL, Jim H, Gu BY (1998) Winter habitat use by black-necked cranes (Grus nigricollis) in Tibet. Wildfow l49:228–241 a huge increase in water area unaccompanied by a growth Bishop MA, Tsamchu D (2005) History and influence of a nature reserve in aquatic vegetation and few stopover sites is of little on a local population of wintering Black-necked Cranes in Tibet. Pp. 638 Wetlands (2014) 34:629–639

30–35 in Wang QS and Li FS, eds. Crane research in China. IPCC (2007) Climate Change 2007: The Physical Sciences Basis. In Kunming: Yunnan Nationalities Publishing House Summary for Policy Makers, IPCC: 21. Geneva:IPCC Bishop MA, Tsamchu D, Li FX (2012) Number and distribution of black- Kie JG, Bowyer RT (1999) Sexual segregation in white-tailed deer: necked cranes wintering in Zhigatse prefecture, Tibet. Chinese Birds density-dependent changes in use of space, habitat selection, and 3:191–198 dietary niche. Journal of Mammalogy 80:1004–1020 Canjue ZM, Yang L, Li JC (2008) Time budget in daytime of black- Kuang FL, Liu N, Cangjue ZM, Li JC, Yang L, Li FX (2007) Diurnal necked cranes in wintering period in Tibet. Chinese Journal of time-activity budgets of Grus nigricollis for the pre-laying phase in Wildlife 29:15–20 northern Tibet. Journal of Zhejiang Forestry College 24:686–691 Chen XP (1994) Black-necked cranes and overwintering places investi- Kuang FL, Cangjue ZM, Li JC, Yang L, Liu N (2010) Nest site charac- gation on the Yunnan and Guizhou plateau. Yunnan Geographic teristics and foraging habitat selection of breeding black-necked Environment Research 6:84–87 cranes in bange, Tibet Autonomous Region, China. Journal of Chen ZD (1997) Wintering ecology and environmental effect observa- Northeast Forestry University 38:89–92 tion. Biosphere Reserve of China 4:1–17 Kuang FL, Zhong XY, Dao MB, Ji YS, Liu N (2008) Initial observation Chen KL, Li SC, Zhou QF, Duo HR, Chen Q (2008) Analyzing dynamics of on selection for forage location of Grus nigricollis in Dashanbao. ecosystem service values based on variations of landscape patterns in Forest Inventory and Planning 33:75–77 Qinghai lake area in recent 25 years. Resources Science 30:274–280 Lang A, Bishop MA, Sueur AL (2007) An annotated list of birds Chou GX, Huang GZ, Liu FL (1995) Overwintering ecology research wintering in the Lhasa river watershed and Yamzho Yumco, Tibet and conservation of black-necked cranes in east- and northeast Autonomous Region, China. Forktail 23:1–11 Yunnan. Yunnan Environmental Science 14:40–43 Lei GL, Sang J, Zheng Z (2012) Site and behavior of sleep of Grus Didham RK, Hammond PM, Lawton JH, Eggleton P, Stork NE (1998) nigricollis in Kazi water reserve of Linzhou, Tibet. Journal of West Beetle species responses to tropical forest fragmentation. Ecological China Forestry Science 4:93–97 Monographs 6:295–323 Lhendup P, Webb EL (2009) Black-necked cranes Grus nigricollis in Dou L, Li H, Li FS, Zhang M, Zheng ZR, Ran JH (2013) Survey on the Bhutan: migration routes, threats and conservation prospects. Black-necked Cranes during the Breeding Period at Sichuan Forktail 25:125–129 Ruoergai Wetland National Nature Reserve. Sichuan Journal of Li C (1996) Distribution, population and conservation of the black- Zoology 32:770–773 necked crane (Grus nigricollis) in Yunnan province. Chinese Doswald N, Willis SG, Collingham YC, Pain DJ, Green RE, Huntley B Wildlife 17:14–15 (2009) Potential impacts of climatic change on the breeding and Li LX (1997) Population ecology and endangered categories evaluation non‐breeding ranges and migration distance of European Sylvia of the Black-necked crane (Grus nigricollus). Chinese Biodiversity warblers. Journal of Biogeography 36:1194–1208 5:84–89 Du MY, Kawashima S, Yonemura S, Zhang XZ, Chen SB (2004) Mutual Li FS (1999) Foraging habitat selection of the wintering black-necked influence between human activities and climate change in the Cranes in Caohai, Guizhou, China. Chinese Biodiversity 7:257–262 Tibetan plateau during recent years. In Global and Planetary Li FS (2005) Status and conservation of black-necked cranes. In: Li FS, Change 41:241–249 Yang XJ, Yang F (eds) Status and conservation of black-necked Dwyer NC, Bishop MA, Harkness JS, Zhong ZY (1991) Black-necked cranes on the Yunnan and Guizhou plateau, People’ Republic of Cranes nesting in Tibet Autonomous Region, China. In Proceedings China. Yannan Nationalities Publishing House, Kunming, pp 44–56 of the Sixth North American Crane Workshop, Regina, Li GG (2011) The wintering behaviors of black-necked cranes at Mashu. Saskatchewan, Canada (pp. 3–5) Qinghai Normal University, Yunnan Gao LB, Qian FW, Yang XJ, Wu HQ, Li FS (2007) Satellite tracking on Li DH, Zhou ZJ (1985) Nursery population behaviors of Black-necked the migratory routes of wintering black-necked cranes at Dashanbao Cranes in Longbao Beach. Wild Animal 6:4–9 in Yunnan. Zoological Research 28:353–361 Li FS, Ma JZ (1992) Wintering time budget and benefit study between Gao XG, Wang L, Sang ZL, Tian H, Wang SM, Liu JJ (2012) family and group black-necked cranes. Chinese Wildlife 3(36–41):29 Relationship between the population dynamics and their habitat Li FS, Ma JZ (2000) Behavioral ecology of black-necked crane during change of the wintering black-necked crane in Dashanbao. winter at Caohai, Guizhou, China. Acta Ecologica Sinica 20:293–298 Journal of Natural Science of Hunan Normal University 35: Li FS, Yang F (2003) Population numbers and distribution of black- 70–73 necked cranes (Grus nigricollis) in the Yunnan-Guizhou Plateau. Han L (1995) The current status of habitats for cranes and their Chinese Journal of Zoology 38:43–46 consevation. In: Chen Y (ed) Study on wetlands in China. Jilin Li ZM, Li FS (2005) Research on the black-necked crane. Shanghai Science and Technique Press, Changchun, pp 256–261 Scientific and Technological Education Publishing House, Shanghai Harris J (1994) Cranes, people and nature: preserving the balance. The Li FS, Nie H, Ye CH (1997) Microscopic analysis on herbivorous diets of future of cranes and wetlands: 1–14 wintering black-necked Cranes (Grus nigricollis)atCaohai,China. Harris J, Mirande C (2013) A global overview of cranes: status, threats Zoological Research 18:51–57 and conservation priorities. Chinese Birds 4:189–209 Li YN, Zhao XQ, Zhao L, Wang QJ, Shen ZX (2003) Analysis of vegetation He XR, Wu JL (2000) A studies on winter diet of black-necked crane succession and climate change in Haibei alpine marsh in the Qilian (Grus nigricollis) at northeast of Yunnan, China. Journal of Yunnan Mountains. Journal of Glaciology and Geocryology 25:243–249 University 22:460–464 Li WJ, Zhang KX, Wu ZL, Jiang P (2009) A study on the available food Hu JS, Wu JL, Dang CL, Zhong XY,Dao MB (2002) Study on the animal for the wintering black- necked crane (Grus nigricollis) in Huize foods of wintering black-necked cranes (Grus nigricollis)at nature reserve, Yunnan. Journal of Yunnan University 31:644–648 Dashanbao reserve, Zhaotong, Yunnan. Journal of Yunnan Liu J (2012) Studies on ecological security assessment of the Caohai University 24:459–461 plateau lake wetland, Chongqing Normal University Huang GL (2005) Status Quo and protection countermeasures of the Liu N, Kuang FL, Xia F, Zhong XY (2006) A primary study on feeding wetlands in the three rivers. Source region in Qinghai. Forest habitat use of black-necked crane during winter. Journal of West Resources Management 4:35–39 China Forestry Science 35:25–32 International Crane Foundation (2004) Black-necked Crane. Available Liu Q, Yang XJ, Zhu JG, Zhao JL, Yu HZ (2008) Flock of black-necked online: http://www.savingcranes.org/blackneckedcrane. html. crane wintering at Napahai nature reserve, China. Zoological Accessed 8 June 2009 Research 29(5):553–560 Wetlands (2014) 34:629–639 639

Liu Q, Yang JX, Zhao JL, Yu HZ (2010) Foraging habitats and utilization Wei TH, Wu JL, Huang GZ et al (1994) Research of the wintering black- distributions of black-necked cranes wintering at the Napahai necked cranes in Yunnan. Waterbird group of China Ornithological Wetland, China. Journal of Field Ornithology 81:21–30 Society. Research on Chinese birds. East China Normal University Lu ZB, Yao JC, Liao YF (1980) Breeding ecology observation of black- Press, Shanghai, pp 43–48 necked cranes. Chinese Journal of Zoology 1:19–24 Wormworth J, Mallon K (2006) Bird species and climate change. World Mcshea WJ, Aung M, Poszig D, Wemmer C, Monfort S (2001) Forage, Wide Fund for Nature Australia, Sydney habitat use, and sexual segregation by a tropical deer in a dipterocarp Wu ZK, Li RX (1985) A preliminary study on the overwintering ecology forest. Journal of Mammalogy 82:848–857 of black-necked cranes (grus nigricollis). Acta Ecologica Sinica 5: Meine CD, Archibald G (1996) The cranes: Status survey and conserva- 71–76 tion action plan. IUCN, Gland Xing Y, Jiang QG et al (2009) Landscape spatial patterns changes of the Pan JH, Wang J, Wang JH (2007) Dynamic change of frigid wetlands in wetland in Qinghai-Tibet Plateau. Ecology and Environmental source region of the Yangtze and yellow rivers. Wetland Science 5: Sciences 18:1010–1015 298–304 Yang XJ, Qian FW, Li FS, Gao LB, Wu HQ (2006) First satellite tracking Qi YF (2012) The dynamics changes of Qinghai Lake basin wetland in of black-necked cranes in China. Zoological Research 26:657–658 the past 20 years. Qinghai Normal University Yang XY, Wang SY (1991) Survey of Black-necked Crane in Ruoergai Qi JW, Li KM et al (2012) Restoration strategies of Caohai Wetland in swamp of Sichuan province. Journal of Sichuan Forestry Science Guizhou province. Central south forest inventory and planning 31:39–40 and Technology 12:60–63 Qian FW, Chu GJ, Jiang HX (2005) Distribution and conservation status Yang R, Wu HQ, Yang XJ, Jiang WG, Zuo L, Xiang ZR (2007) Diurnal of Chinese cranes. In: Li FS, Yang XJ, Yang F (eds) Status and time budget of the black-necked crane during the breeding season. conservation of black-necked cranes on the Yunnan and Guizhou Waterbirds 30:80–85 Plateau, People’ Republic of China. Yannan Nationalities Yao JC (1982) Quantity distribution of black-necked crane (Grus Publishing House, Kunming, pp 14–43 nigricollis) in Qinghai province. Wild Life 1:20–22 Qian FW, Wu HQ, Gao LB, Zhang HG, Li FS, Zhong XY, Yang XJ, Yao TD, Thompson J, Yang W, Yu WS, Gao Y, Guo XJ, Yang XX, Duan Zheng GM (2009) Migration routes and stopover sites of black- KQ, Zhao HB, Xu BQ, Pu JC, Lu AX, Xiang Y, Kattel DB, Joswiak necked cranes determined by satellite tracking. Journal of Field D (2012) Different glacier status with atmospheric circula- Ornithology 80:19–26 tions in Tibetan Plateau and surroundings. Nature Climate Ran JH, Liu SY, Lin Q, Zheng ZY, Shao KQ, Zhang M (1999) The Change 2:663–667 population and distribution of black-necked cranes (grus nigricollis) Ye QH, Zhu LP, Zheng HX, Naruse RJ, Zhang XQ, Kang SC (2007) in Xiaman nature reserve in Sichuan. Chinese Journal of Applied Glacier and lake variations in the Yamzhog Yumco Basin in the last and Environmental Biology 5:40–44 two decades using remote sensing and GIS technologies. Journal of Ranade P S (2008) Managing Lake Tourism: Challenges Ahead. Glaciology 53:673–676 Conference on Tourism in India - Challenges Ahead 15–17 May Yu YQ, Liu WL, Sang J (1993) A preminary study on the overwintering 2008, IIMK, 543–554 ecology of black-necked crane (Grus nigricollis) in The Upper Rank M (1994) New Chinese black-necked crane population discovered. Lhasa River. Zoological Research 14:250–251 Oriental Bird Club Bulletin 19:18–19 Zhang KX (2010) Wintering habitat changes and available food research Samraoui B, Samraoui F (2008) An ornithological survey of Algerian of black-necked cranes in Huize Nature Reserve, Yunnan province. wetlands: important bird areas, Ramsar sites and threatened species. Yunnan University, Yunnan Wildfowl 58:71–98 ZhangJJ,LuoJ(1991)Numberanddistribution of black-necked Sekercioğlu CH, Primack RB, Wormworth J (2012) The effects of crane on Ruoergai Plateau Marsh. Sichuan Journal of climate change on tropical birds. Biological Conservation 148:1–18 Zoology 10:37–38 Tian K, Mo JF, Lu M, Chang FL, Yang YX (2004) Human disturbances Zhang ZH, Xiao F (2000) Preliminary studies on the histology of the on the ecological environment degradation of Napahai wetland in digestive tract of a female Grus nigricollus. Journal of Capital the upstream of Yangtze river. Resources and Environment in the Normal University 21:48–50 Yangtze Basin 13:293–296 Zhang YL, Li XB et al (2000) Urban land use change in Lhasa. Acta Tsering, Benba D, Lagdor, Basang, Pubu (2009) Relationship between Geographica Sinica 55:395–405 Wintering Habitat Protection of the Black-necked Crane and Local Zhang YS, Yao TD, Ma YZ (2011) Climatic changes lead significant Agricultural Activities. Journal of Tibet University: 1–7 expansion of Endorheic Lakes in Xizang (Tibet) Since 1995. Wang YH, Wu ZK, Li ZM, Jiang YM (1989) Black-necked crane and Sciences in Cold and Arid Regions 3:463–467 study of China. Zoological Research 24:35–39 Zhang T, Ma M, Zhang X, Zhang HB, Liu M, Ding P, Xu F (2012) Wang D, Zhao YH, Zhang CG, Zhou J (2007) Species diversity of wild Distribution and population size of black-necked cranes in autumn freshwater fishes and sustainable utilization of the fish resource in in East Kunlun and Altun Mountains, Xinjiang. Chinese Journal of Guangxi, china. Acta Zootaxonomica Sinica 32:160–173 Zoology 47:31–35 Wang N, Zhu PF, Wan M, Ye YX, Qu S (2013) Size and distribution of Zhao JL, Han LX, Feng Li WZR, Yu HZ (2008) Wintering behav- the breeding population of Black-necked crane in Haizishan, iors and habitat using of black-necked crane in Napahai nature Sichuan province. Journal of Ecology and Rural Environment: reserve, Yunnan province. Sichuan Journal of Zoology 27:78– 265–268 91