Distribution pattern of endangered bird species in China
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1 Integrative Zoology 2006; 1: doi: /j x ORIGINAL ARTICLE Distribution pattern of endangered bird species in China Fumin LEI, 1 Hongfeng ZHAO 1,2 and Zuohua YIN 1 1 Institute of Zoology, Chinese Academy of Sciences, Beijing, China and 2 College of Life Sciences, Shaanxi Normal University, Xi an, China Abstract In this study, we determined six hotspots for avian biodiversity conservation in China. We analyzed the distribution patterns of 183 threatened bird species in China in conjunction with geographical data to produce a distribution map that shows the concentrations of threatened species. The six biodiversity hotspots are: the western Tianshan Mountains; the Qilian and Hengduan mountains; southern Anhui, southern Jiangsu, and the Zhejiang Hills; the Songliao Plain and the northern region of the North China Plain; the island of Taiwan; and the island of Hainan. Based on our analysis of a species habitat matrix, species were determined to be distributed mainly in broadleaved forest, grassland and meadows, urban and agricultural areas, wetlands, and bush. Most species were commonly found to have a range of three to five different habitat types. Apart from the six biodiversity hotspots, six ecological clusters were determined. Protection strategies indicating different levels of habitat priority among the biodiversity hotspots were also recommended. Key words: China, distribution pattern, endangered birds, habitat, species richness. Correspondence: Fumin Lei, Institute of Zoology, Chinese Academy of Sciences, Beisihuan Xilu 25, Beijing , China. leifm@ioz.ac.cn INTRODUCTION Biodiversity loss has increased exponentially in recent years. Currently, 1186 species of birds are threatened with extinction worldwide (Birdlife International 2000). This phenomenon of biodiversity loss affects some habitats more than others, which results in an uneven distribution of threatened species. This uneven distribution of threatened bird populations has encouraged conservationists to determine key sites for species distribution ( biodiversity hotspots ) and to take action to protect (Myers 1988; Dobson et al. 1997). Biodiversity hotspots are regions that are home to a large number of threatened species. These regions should be given a high priority for biodiversity conservation (Reid 1998). The basis for determining the status of these hotspots may be overall species richness, rare species (Myers 1988; Prendergast et al. 1993; Chen & Peterson 2002), endemic species (Balmford & Long 1994; Kerr 1997; Lei et al. 2003a,b), or it may be determined on the basis of two measures combined with some assessment of urgency for conservation action (Williams et al. 1996). Lei et al. (2003 a,b) have suggested biodiversity hotspots in China based on avian endemism. We, on the other hand, have focused on the distribution patterns of threatened birds species found in the China Red Data Book of Endangered Animals: Aves (Zheng & Wang 1998) in order to identify alternative biodiversity hotspots. Identification of biodiversity hotspots based on the distribution patterns of threatened species will give us new insights for improving biodiversity conservation in China. It is hoped that this study will be useful for conservation and land management leaders as well as politicians in their efforts to
2 Distribution of endangered birds in China expand support for biodiversity conservation, and in developing policies, regulations, and legislation regarding biodiversity conservation. MATERIALS AND METHODS Mapping distribution patterns We studied the distribution patterns of all 183 threatened bird species listed in the China Red Data Book of Endangered Animals: Aves (Zheng & Wang 1998). The endangered species criteria in this book do not follow the criteria of the IUCN (2001); however, the criteria in the China Red Data Book of Endangered Animals: Aves are useful for managing local habitat and for creating species protection plans for threatened wildlife in China. Although the threatened species list in the China Red Data Book of Endangered Animals: Aves (Zheng & Wang 1998) has no official legal function, it may serve as the basis for setting priorities for conservation action plans (Zheng & Wang 1998). Species taxonomic status in the present paper follows that used by Cheng (2000). A geographical distribution database was set up, and it is kept with the Ornithological Research Group, Museum of Zoology, Chinese Academy of Sciences. The method used for setting up the database follows that used by Lei et al. (2003a). Distribution patterns of threatened and endangered bird species were mapped using a geographic information system (GIS; Arc View 3.2; Environmental Systems Research Institute, Redlands, CA, USA). We then digitized a map of China (with a scale of 1: ), and used it in conjunction with the GIS in order to produce a geographic-units map based on provinces and zoogeographical regions. From this, we produced a 20 km 20 km grid map with statistics of species richness in each grid. In determining distribution patterns we did not weight the value of each species. Rather, we considered each species to be of equal importance with respect to biodiversity conservation. Species habitat relationship A total of 17 different types of habitats were classified using habitat authority files from the Chinese Academy of Sciences (1998). The 17 habitats are as follows: desert (DT); grassland and prairie (GL(PR)); bush (BR); steppe (ST); marsh (ML); tundra (TU); coniferous forest (PF); broadleaf forest (BF); mixed coniferous and broadleaf forest (MF); rainforest and tropical monsoon rainforest (RF); bamboo forest (BB); sparse forest (SF); mountainous (RH); urban and agricultural (HH); garden and park (GD); lake, river, and bottomland (LA); and sea and costal areas (SC). Table 1 Species richness of different taxa in the 6 regions Orders/species/regions I II III IV V VI Galliformes Falconiformes Passeriformes Gruiformes Columbiformes Ciconiiformes Strigiformes Anseriformes Charadriiformes Pelecaniformes Psittaciformes Coraciiformes Lariformes Cuculiformes Trogoniformes Procellariiformes Piciformes Caprimulgiforms Total Resident Breeding Wintering Passaging Habitat data came from collection records, publications, and field exploration (e.g. Wu et al. 1986; Cheng 1987; Yang et al. 1995; Tang et al. 1996). A species-habitat matrix (SHM) was produced using data on the relationship between the 183 threatened and endangered bird species and the 17 different habitat types. The SHM was used to indicate whether or not a particular species exists in a particular habitat. In the SHM, 1 indicates that a species is present in a habitat, and 0 indicates that a species is not known to be distributed in a particular habitat. The information from the SHM was analyzed using a Jaccard similarity index to produce a dendrogram. The dendrogram was used to compare the numbers of species within the habitats. We then produced a histogram to show the scale of habitat occupation by the various taxa. All distribution data and habitat records for these species were not completely known at the time of the study, but we assume that the knowledge gaps are too small to affect the overall analysis of habitat biodiversity.
3 F. Lei et al. RESULTS Species composition There are currently 1253 bird species recognized in China (Cheng 2000), of which 183 species (14.6% of the total bird species in China) are listed in the China Red Data Book of Endangered Animals: Aves (Zheng & Wang 1998). These 183 species belong to 18 orders, 39 families, and 105 genera. The 105 genera consist of: Galliformes (44 species in 20 genera), Falconiformes (30 species in 18 genera), Passeriformes (17 species in 9 genera), Gruiformes (16 species in 6 genera), Columbiformes (15 species in 8 genera), etc. A total of 133 bird species are protected by the National Wildlife Protection Law. Of these 133 species, 42 are ranked as class I protected and 91 are ranked as class II protected. Among the 183 bird species, two species (1. 1% of the total threatened bird species in China) have become extinct, 25 species (13.7%) are endangered, 49 species (26.8%) are vulnerable, 74 species (40.4%) are classified as rare, and 33 species (18%) are undetermined. Distribution areas and species richness We have identified six regions (hotspots) with the highest numbers of threatened species in China (Fig. 1). We have also analyzed the species composition in each region (Table 1) and the species richness in different habitats of the region (Fig. 2). The regions with the highest species richness are: the western Tianshan Mountains; the Qilian and the Hengduan Mountains; southern Anhui, southern Jiangsu, and the Zhejiang Hills; the Songliao Plain and the northern region of the North China Plain; the island of Taiwan; and the island of Hainan. The western Tianshan Mountains are located in western Xinjiang Province, the northwestern-most region of China (Cheng 1987, 1997). There are 36 bird species recorded here, of which 11 are class I protected, and 21 are class II. This region s many scattered lakes are home to several species of waterfowl. However, the majority of birds Figure 1 The six distribution centers of endangered birds in China.
4 Distribution of endangered birds in China Species richness DT GL BR ST ML TU PF BF MF RF BB SF RH HH GD LA SC Figure 2 Species richness in different habitats and different distribution centers. I: the western Tianshan Mountains; II: the Qilian and the Hengduan Mountains; III: southern Anhui, southern Jiangsu, and the Zhejiang Hills; IV: the Songliao Plain and the northern region of the North China Plain; V: the island of Taiwan; VI: the island of Hainan. Species richness coast of mainland China. It is a typical island habitat. There are 54 bird species there, of which 10 species are class I protected, and 25 are class II. This region contains 23 species of waterfowl and 16 species of raptor. The island of Hainan is located off the southern coast of China. In this region there are 44 bird species, of which 2 are class I protected, and 23 are class II. There are 12 DT GL BR ST ML TU PF BF MF RF BB SF RH HH GD LA SC Habitat (18 species) in this region are raptors; they dominate this area because of the easy access to prey in the region s open grasslands. The Qilian and Hengduan Mountains are located on the eastern Tibetan Plateau. This region includes areas of southeastern Qinghai, western Yunnan, and northwestern Sichuan. There are 120 bird species living in this region, of which 23 species are class I protected, and 67 are class II. This region has the highest species richness among the six biodiversity hotspots. A total of 33 terrestrial bird species and 33 raptor species inhabit this region. Diverse climatic and geomorphological features make this region a hotbed of biodiversity. The region that includes southern Anhui, southern Jiangsu, and the Zhejiang Hills is located in southeastern China. There are 39 bird species in this region, of which nine species are class I protected, and 21 are class II. Two of the largest freshwater lakes in China, the Poyanghu and the Taihu, are in this region; for this reason, the majority of birds here are waterfowl. The Songliao Plain and the northern region of the North China Plain are located in northeastern China near the Bohai Sea. There are 43 bird species in this region, of which 12 are class I protected, and 22 are class II. Of this region s 43 bird species, 22 are waterfowl, and 17 are raptors. Many wetlands, which are essential for sustaining local ecosystems, are located in this region. The island of Taiwan is located off the southeastern
5 F. Lei et al Number of species Figure 3 Habitat requirements shared by species. BF PR L A BR HH ML MF PF SC BB DT SF ST RH RF GD TU Habitat type species of raptors and 11 species of waterfowl in Hainan. From Table[xy2] 3, we can see that in every region the protected, and 25 are class II. This region contains 23 species of waterfowl and 16 species of raptor. The island of Hainan is located off the southern coast of China. In this region there are 44 bird species, of which 2 are class I protected, and 23 are class II. There are 12 species of raptors and 11 species of waterfowl in Hainan. From Table 1, we can see that in every region the number of waterfowl species is relatively high. They are widely distributed among the six regions, but are sensitive to environmental changes, especially changes in water quality, and waterfowl populations can decline quickly if environmental changes are severe. Although raptors are also relatively abundant in these six hotspots, they also face threats in these regions, mostly due to hunting and trade. Ecological assemblage of taxa We determined habitat sharing patterns (Fig. 3) by analyzing the distribution patterns of 183 endangered bird species among 17 different habitats based on the SHM. The habitat sharing patterns reveal the scale of habitat selection by individual species. We found that most endangered bird species in China are distributed in the BF, PR, LA, BR, and HH habitats (Fig. 3), and that the range of most species encompasses three to five different habitats (Fig. 4). Based on the SHM database, we also analyzed the relationship between the 17 habitat types. A dendrogram was produced with six obvious clusters showing habitats with similar species distribution (Fig. 5). Figure 5 shows that the following groups of habitat types have similar species distributions: ML, LA, SC, and HH in branch 1; DT, PR, and RH in branch 2; ST and TU in branch 3; PF, MF, BF, BR, and BB in branch 4; and RF and SF in branch 5. Type GD is located in a cluster by itself to form branch 6, and does not share species distribution with any other region. DISCUSSION Avian diversity conservation based on threatened species distribution patterns Historically, China has been extremely rich in biodiversity; however, in the push for modernity, China has become a place where biodiversity has suffered greatly (State Environmental Protection Administration 1998). The preservation of regions with a high concentration of rare species is a key consideration in the preservation of biodiversity in China (May 1992; Miller & Allen 1994). Though it is ideal, it is not practical to protect every region containing threatened or endangered species. Therefore, we suggest that conservation management be focused on the aforementioned six biodiversity hotspots. These hotspots help highlight distribution areas with high numbers of threatened species independent of overall species richness or endemism (Dobson et al. 1997). Focusing on changes in patterns of threatened species within these
6 Distribution of endangered birds in China Number of species biodiversity hotspots may serve as an indicator of broader trends in overall species distribution because many threatened avian taxa are well studied and can act as surrogates for understanding the regional distribution of other poorly known taxa (Bibby et al. 1992; Pearson & Cassola 1992; Dobson et al. 1997). ML LA SC HH DT PR RH ST TU PF MF BF BR BB RF SF GD Habitat type Figure 4 Histogram showing habitat sharing by the species. X- axis represents how many species are distributed in the habitat, while Y-axis represents how many habitats are occupied by these species. eg. in the first left bar, it means there are 18 species are distributed in only one habitat. Figure 5 Habitat assemblage by hierarchical cluster analysis, using Jaccard similarities of species distributions Conservation priorities for habitats in biodiversity hotspots Even after narrowing the focus to these six biodiversity hotspots it is a difficult task to spread conservation efforts evenly across all taxa and all habitats within them. Considering ecological assemblages for wintering, breeding, and resident taxa, it may be more important to focus conservation efforts on certain types of habitats; likewise, some species may be more important than others with respect to conservation priority. Below we have listed which habitats should have priority for conservation in each of the six biodiversity hotspots. In the western Tianshan Mountains, GL, LA, DT, ML, and HH should have priority for conservation (Fig. 2), especially for residents and breeding birds. In the Qilian and Hengduan Mountains, BF, BR, GL, and HH should have priority for conservation (Fig. 2), especially for resident species. In southern Anhui, southern Jiangsu, and the Zhejiang Hills, LA, ML, and GL should have priority for conservation (Fig. 2), especially for resident species and wintering birds. On the Songliao Plain and in the northern region of the North China Plain, LA, GL, ML, and SC should have priority for conservation (Fig. 2), especially for breeding and wintering birds. On the island of Taiwan, LA, ML, HH, SC, and BF should have priority for conservation (Fig. 2), especially for resident species and wintering birds. On the island of Hainan, BF, HH, LA, and BR should have priority for conservation (Fig. 2), especially for resident species. Conservation suggestions regarding endemism Of the six biodiversity hotspots indicated by this survey, the Qilian and Hengduan Mountains and the island of Taiwan are also the endemism centers (Lei et al. 2003a,b). These regions should be given higher biodiversity conservation priority based on the high numbers of endangered endemic species within them. Challenge of human activity in biodiversity conservation Human activity, both directly and indirectly, has played a leading role in the reduction of biodiversity throughout the world. Biodiversity hotspot analysis by Dobson et al. (1997) indicated that hotspots in the US with high numbers of threatened species tend to overlap significantly with areas of high agricultural output. Harcourt and Woodroffe (2002) also suggested that regions of high human population density are likely to wipe out entire species in Africa. Other abundant evidence of the adverse
7 F. Lei et al. effects of high human population density on the survival of species as well as on the survival of their habitat indicates that human influence must be taken into serious consideration in developing strong conservation practice (Olson 1989; Veach et al. 2003). China s biodiversity continues to suffer from an explosion of human activity (Liu et al. 2003; Yang & Xu 2003). Of these six hotspots, four are located in areas of high human population density. This indicates that human activity is possibly the main factor in biodiversity loss in these regions; furthermore, with human population and urban development continuing to grow, biodiversity loss is likely to continue in these hotspots unless appropriate measures are developed and implemented (Cincotta et al. 2000). Understanding the cause-and-effect relationship in regions with high human activity is important for developing strong habitat management policy and effective conservation action plans. National significance and current conservation status In the China Red Data Book of Endangered Animals: Aves (Zheng & Wang 1998), there are 49 bird species that are cross-listed by the IUCN (2001), accounting for 26.8% of all threatened bird species in China. Of these, two species (1.1%) are listed as critical, eight species (4.4%) are endangered, 23 species (12.6%) are vulnerable, and 16 species (8.7%) are near threatened globally. In comparing the lists of the IUCN (2001), we find that more than one-quarter of threatened species in China are threatened globally. Although three-quarters of China s bird species are not listed by the IUCN, they still face many threats in China. The criteria for endangered or threatened species to be listed by the IUCN (2001) may be very useful for biodiversity conservation globally. However, in determining hotspots based on threatened species distribution, we focused solely on species from the China Red Data Book of Endangered Animals: Aves (Zheng & Wang 1998) in order to make this paper more relevant to China s current environmental situation. In doing so, we hope to not only determine the immediate biodiversity problems at hand, but also to encourage the nation s top leaders to put forward relevant action plans and to take the appropriate measures to step up biodiversity conservation on a national level. ACKNOWLEDGMENTS We would like to thank Mr. G.A. Wei, Ms. S.J. Yang, and Ms. J.L. Lu for helping with the preparation of this manuscript. This paper was supported by the CAS President Grant and IOZ Innovation Program and the National Natural Science Foundation of China REFERENCES Balmford A, Long A (1994). Avian endemism and forest loss. Nature 372, Bibby CJ, Collar NJ, Crosby MJ et al. (1992). Putting Biodiversity on the Map: Global Priorities for Conservation. ICBP, Cambridge. Birdlife International (2000). Threatened Birds of the World. Lynx Edicions and Birdlife International, Barcelona and Cambridge. Chen GJ, Peterson AT (2002). Prioritization of areas in China for the conservation of endangered birds using modeled geographical distributions. Bird Conservation International 12, Cheng TH (1987). A Synopsis of the Avifauna of China. Science Press, Beijing. Cheng TH (1997). Fauna Sinica: Aves Vol Science Press, Beijing (In Chinese.) Cheng TH (2000). A Complete Checklist of Species and Subspecies of the Chinese Birds. Science Press, Beijing. Cincotta RP, Wisnewki J, Engelman R (2000). Human population in the biodiversity hotspots. Nature 404, Dobson AP, Rodriguez JP, Roberts WM, Wilcove DS (1997). Geographic distribution of endangered species in the United States. Science 275, Harcourt AH, Woodroffe R (2002). Human density as an influence on species/area relationships: double jeopardy for small African reserves? Biodiversity and Conservation 10, IUCN (2001). IUCN Red List Categories and Criteria: Version 3.1. [Cited Sept. 2006] Available from URL: html. Kerr JT (1997). Species, richness, endemism, and the choice of areas for conservation. Conservation Biology 11, Lei FM, Qu YH, Lu JL, Yin ZH (2003a). Conservation on diversity and distribution patterns of endemic birds in China. Biodiversity and Conservation 12, Lei FM, Qu YH, Tang QQ, An SC (2003b). Priorities for the conservation of avian biodiversity in China based on the distribution patterns of endemic bird genera. Biodiversity and Conservation 12, Liu JG, Ouyang ZY, Pimm SL et al. (2003). Protecting China s biodiversity. Science 300,
8 Distribution of endangered birds in China May RM (1992). The Calculus of Biodiversity. Presentation at the Systematics and Conservation Evolution symposium. Natural History Museum, London, pp Miller RI, Allen JH (1994). Mapping the elements of biodiversity: the rare species of Madagascar. In: Miller RI, ed. Mapping the Diversity of Nature. Chapman and Hall, London, pp Myers N (1988). Threatened biotas: hot-spots in tropical forests. Environmentalist 8, Olson SL (1989). Extinction on islands: Man as catastrophe. In: Pearl M, Western D, eds. Conservation Biology for the Twenty-first Century. Oxford University Press, Oxford, pp Pearson DL, Cassola F (1992). World-wide species richness patterns of tiger beetles (Coleoptera: Cicindelidae): indicator taxon for biodiversity and conservation studies. Conservation Biology 6, Prendergast JR, Quinn RM, Lawton JH, Eversham BC, Gibbons DW (1993). Rare species, the coincidence of diversity hotspots and conservation strategies. Nature 365, Reid WV (1998). Biodiversity hotspots. Trends in Ecology and Evolution 13, State Environmental Protection Administration (1998). China s Biodiversity: A Country Study. China Environmental Sciences Press, Beijing. Tang CZ, Xu YG, Yang L (1996). [Birds of the Hengduan Mountains Region.] Science Press, Beijing. (In Chinese). Veach R, Lee D, Philippi T (2003). Human disturbance and forest diversity in the Tansa Valley, India. Biodiversity and Conservation 12, Williams P, Gibbons D, Margules C, Rebelo A, Humphries C, Pressey R (1996). A comparison of richness hotspots, rarity hotspots, and complementary areas for conserving diversity of British birds. Conservation Biology 10, Wu ZK, Lin QW, Yang JL, Liu JC, Wu L (1986). [The Avifauna of Guizhou Province.] Guizhou People s Publishing House, Guiyang. (In Chinese.) Yang L, Wen XJ, Han LX (1995). [The Avifauna of Yunnan, China. Vol. I: Non-Passeriformes.] Yunnan Science and Technology Press, Kunming, China. (In Chinese). Yang X, Xu M (2003). Biodiversity conservation in Changbai Mountain Biosphere Reserve, northeastern China: status, problem, and strategy. Biodiversity and Conservation 12, Zheng GM, Wang QS (1998). [China Red Data Book of Endangered Animals: Aves.] Science Press, Beijing. (In Chinese.)
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