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A bird's view of new conservation hotspots in China

⁎ MARK Ruocheng Hua,b,1, Cheng Wena,b, ,1, Yiyun Gub, Hao Wanga, Lei Gub,c, Xiangying Shib, Jia Zhongd, Ming Weid, Fenqi Hee, Zhi Lua a Center for Nature and Society, School of Life Sciences, Peking University, Beijing 100871, China b Shan Shui Conservation Center, Beijing 100871, China c School of Life Sciences, Capital Normal University, Beijing 100871, China d Chinese Bird Watching Societies Network, Kunming, Yunnan 650224, China e Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

ARTICLE INFO ABSTRACT

Keywords: Blooming citizen science in China creates opportunities to update distribution maps of threatened and Citizen science contributes to decision making for conservation. 46,073 records submitted by over 7000 bird watchers from Threatened bird species 1998 to 2013 in China cover 1195 of 1371 species and all provincial administrative districts in the country. We Conservation hotspots extracted 13,181 occurrence localities for 95 threatened species defined by the IUCN Red List and 239 national Species distribution model protected species in China. By applying these data in MaxEnt model, we identified new conservation hotspots for Gap analysis threatened birds in China in coastal regions of the Bohai Gulf and the Yellow Sea, the south of the North China Plain, and the lower reach of the Yangtze River. These new conservation hotpots are not included in the global biodiversity hotspots, and not all represented in the priority regions in National Biodiversity Strategy and Action Plan (NBSAP). These newly identified conservation hotspots are seriously under-protected: only less than 2% of them are in national nature reserves. There is a long way to go to meet the Aichi targets, a plan to halt the loss of biodiversity by 2020.

1. Introduction 2009, Birdlife International published Directory of Important Bird Areas in China (Mainland), Key Sites for Conservation, which listed 512 Birds have been widely accepted as flagship taxa for conservation Important Bird Areas (IBAs). 75% (384/512) of IBAs are protected hotspot identification and conservation GAP analysis (Scott et al., 1993; areas, and 62.5% (320/512) of IBAs are nature reserves (Chan, 2009). Balmford, 1998; Reid, 1998; Lei et al., 2003a; Chape et al., 2005; However, the clear boundary of each IBA has not been offered (Chan, Jenkins et al., 2013). China is home to 1371 bird species (Zheng, 2011), 2009). accounting for about 15% of the world's total bird species (del Hoyo Recently, the global richness pattern and hotspots of birds have et al., 2014), while it also holds the greatest human population and the been drawn according to breeding ranges (Jenkins et al., 2013). While second largest economy in the world. Over a decade ago, the Mountains in China, the umbrella protective effect of the Giant Panda Ailuropoda of Southwest China, the Qinling Mountains, and the Dabashan Moun- melanoleuca to endemic and sympatric species including birds in China's tain Region were identified as China's priority regions for bird southwest forests has been assessed and new conservation hotspots conservation based on the distribution of endemic species (Lei et al., have been identified based on endemic species distributions (Li and 2003a; Lei et al., 2003b; Lei et al., 2006; Chen and Townsend Peterson, Pimm, 2016). Biodiversity hotspots of endemic and non-endemic avian 2002). At the same time, six bird conservation hotspots were identified diversity in the mountains of Southwest China have been identified (Wu based on the distribution of 183 threatened species from China Red Data et al., 2016). Endemic species of China need to be in a higher-threat Book of Endangered : Aves (Lei et al., 2006; Zheng and Wang, category than the current IUCN Red List, and more attention need to be 1998), namely the west of Tianshan Mountains, the Qilian and payed to these endemic species (Li et al., 2016; Ocampo-Peñuela et al., Hengduan Mountains, southern Anhui Province-southern Jiangsu Pro- 2016). However, the hotspots of endemic species and threatened vince-the Zhejiang Hills, the Songliao Plain and the north of the North species do not necessarily overlap with each other (Orme et al., China Plain, and islands of Taiwan Province and Hainan Province. In 2005). The blooming economy in China heavily affected the key

⁎ Corresponding author at: Shan Shui Conservation Center, Beijing 100871, China. E-mail address: [email protected] (C. Wen). 1 These authors contributed equally to this work. http://dx.doi.org/10.1016/j.biocon.2017.03.033 Received 22 September 2016; Received in revised form 27 March 2017; Accepted 31 March 2017 0006-3207/ © 2017 Published by Elsevier Ltd. R. Hu et al. Biological Conservation 211 (2017) 47–55 stopover habitats of birds (Ma et al., 2014; Kamp et al., 2015), and this selected 33,174 bird records of 273 species, 13,181 independent caused a notable decline of migratory bird population (Runge et al., localities from all 46,073 records collected by birdwatchers, which 2015). Therefore, the analysis of conservation hotspots for birds, were checked by experienced birders on Bird Report to reduce errors especially for the threatened migratory birds, should take into con- (Kelling et al., 2015) and examined via spatial autocorrelation in sideration the stopover sites along migrating routes. MATLAB software (2009a, Mathworks, Natick, Massachusetts); 2) All The GAP analysis of China's nature reserves also needs to be peer-reviewed papers published since 2004 concerning the 288 species. updated. In past decades, China's rapid economic growth and large- These papers offered 295 different occurrence localities of 187 species. scale urbanization resulted in significant habitat loss of a large array of We verified the accurate coordinates of those points manually accord- species (Brooks et al., 2002; Güneralp et al., 2015), especially birds (Li ing to the place names using Google Maps (https://www.google.com/ and Wilcove, 2005). This is one of the main reasons why 23 species of maps). bird including 13 migrants have been upgraded to “threatened” by To reduce statistical errors associated with small sample size, we IUCN Red list in the last ten years (Baillie et al., 2004; IUCN, 2015). excluded species with fewer than 5 independent localities (Hernandez This may lead to a change of spatial patterns of conservation hotspots. et al., 2006; Wisz et al., 2008). The remaining 158 species and 12,951 Furthermore, this rapid change has not been taken into consideration independent localities were applied to simulate species distribution by China's Wildlife Protection Law, in which the National Protected maps, including 3 CR, 14 EN, 26 VU, 23 NPS-Class I and 120 NPS-Class Species (NPS) List has not been systematically updated since the law II species; 230 localities of 115 species were used to make scatter plots; went into effect in 1988 (Ministry of Forestry in the People's Republic of and 15 of the 288 species have no occurrence data. China and Ministry of Agriculture of the People's Republic of China, 1988), leaving many threatened species out of legal protection, 2.2. Environmental variables and bioclimatic variables including those critically endangered and endangered ones. The GAP analysis of protected areas has been performed at global level We compiled a total of 22 environmental and bioclimatic variables (Rodrigues et al., 2004; Alexander and Armitage, 2015) as well as for projection (Zhao et al., 2017): 19 bioclimatic variables (ESRI grids, national level, e.g. in the United States (Jenkins et al., 2015), and in bio 10 m) were downloaded from the WorldClim 1.4 (current condi- Southeast Asia including Yunnan Province, China (Li et al., 2016; tions) database (Hijmans et al., 2005), distance to water from the IGRR Hughes, 2017). However, the national or regional analysis in China (Institute of Geography and Resource Research, Chinese Academy of needs to be done. Such analysis is important for guiding conservation Sciences) by inter-agency letter of agreement, land cover type (Global- plans and actions on the ground through strategies and investment. All Land 30) from the National Geomatics Centre of China (National these plans and actions require more accuracy and need to be updated Geomatics Center of China, 2013), and digital elevation model (G- from time to time. TOPO30) from the United States Geological Survey (USGS) (USGS, In China, historical occurrence data of birds are mostly from 1996). specimen collection sites (Zheng and Wang, 1998). From 1998 to All bioclimatic variables were downscaled to a resolution of 30 arc- 2001 and from 2012 onwards, the State Forestry Administration seconds (0.8421 km per pixel) using the Abdus Salam International organized two National Terrestrial Wildlife Resources Surveys. How- Centre for Theoretical Physics (ICTP) Regional Climate Model version 3 ever, the occurrence data from the surveys is not publically available. (RegCM3) (Gao et al., 2012) and spline interpolation, and we used On the other hand, the number of birdwatchers and bird reports has nearest neighbor for resampling land cover type (GlobalLand 30) to grown rapidly since birdwatchers established the first online bird match the spatial resolution of other sets of data in ArcMap 10.2 (2010, record database, Bird Report, in 2002 (http://birdreport.cn/bird/). ESRI, Red Land, California). Up to 2013, the database covers 1195 of 1371 species and all provincial administrative districts, complementing the basic knowledge of bird 2.3. Ecological Niche Modeling distribution (Li et al., 2013). Citizen scientists can provide timely and expansive information for addressing fast-changing threats and prior- We created the Ecological Niche Modeling (ENM) of the selected itizing conservation (Todd et al., 2016). species in the software MaxEnt 3.3.3k (Phillips et al., 2006). MaxEnt is In this paper, we chose to model 160 bird species of interest in a machine-learning method using a maximum entropy approach to MaxEnt 3.3.3k, including 43 threatened species, using the occurrence estimate the most uniform distribution of a particular species across the data accumulated over 16 years (from 1998 to 2013), the majority of study area, constrained by the provided environmental correlations which collected from Bird Report. We conducted the GAP analysis to represented by training presence-only data (Phillips et al., 2006; Elith identify new conservation hotspots and addressed the following ques- et al., 2011). The number of occurrence localities collected for each tions: where are the conservation hotspots and critical regions for species is usually small and highly variable (the average is 81.9, the threatened bird species in China? To what extent are they protected median is 32.5, the mode is 9, and the standard deviation is 193.8,see legally, and how to improve the situation? Appendix S1). To reduce the influence of small sample size on forecasted accuracy (Stockwell and Peterson, 2002; Bean et al., 2. Methods 2012), we chose MaxEnt because it has been proven to work better than other approaches with limited presence-only occurrence data 2.1. Species checklist and occurrence data (Phillips and Dudík, 2008; Wisz et al., 2008; Merow and Silander, 2014; P Anderson et al., 2006). For each species, the model was run by We selected 288 species from 1371 bird species in China according 5 bootstrap replicates with randomly assigned 80% of the presence to two criteria: 1) Threatened bird species - Critically Endangered (CR, records as training data and the other 20% as testing data. We used the 10 species), Endangered (EN, 25 species) and Vulnerable (VU, 60 default settings of the software and logistic output format ranging from species) defined by the most recent IUCN Red List (IUCN, 2012, 2015); 0 to 1. The Area Under the Curve (AUC) was used to assess the accuracy 2) NPS listed under the List of Key Protected Wildlife of the China of predict results (Lobo et al., 2008), and the average AUC value of 158 Wildlife Protection Law (Ministry of Forestry in the People's Republic of species is 0.956 (Appendix S1). China and Ministry of Agriculture of the People's Republic of China, 1988), including Class I (43 species) and Class II (196 species). The 2.4. Distribution mapping and GAP analysis checklist of these species is in the Supporting information Appendix S1. The sources of occurrence point data of the 288 species include: 1) For each species, the logistic outputs of models for forecasted Bird Report (http://birdreport.cn/bird/, from 1998 to 2013). We distribution (FD) were converted to “presence/absence” binary maps

48 R. Hu et al. Biological Conservation 211 (2017) 47–55

Fig. 1. The distribution range and habitat area of threatened species in China.The first column (A–D) shows the distribution range, the second column (E–H) shows the pattern of the habitat area. The first row (A and E) shows the CR species, the second row (B and F) shows the EN species, the third row (C and G) shows the VU species, and the forth row (D and H) shows all the threatened species. Most of all groups of threatened species high richness areas are in East China.

49 R. Hu et al. Biological Conservation 211 (2017) 47–55 using variable thresholds. We independently tested the thresholds 3.2. Richness pattern and hotspots of threatened species and the coverage of meeting the equal training sensitivity and specificity (ETSS) criterion, the hotspots by NNRs the maximum training sensitivity plus specificity (MTSS) criterion, and the balanced training omission, predicted area and threshold value The richness patterns of CR, EN, and VU species derived from (BTOPT) criterion, which have been proven to be rational (Hernandez BFDMs are generally consistent with each other, while the richness et al., 2006; Jiménez-Valverde and Lobo, 2007; Liu et al., 2005; Liu patterns derived from BFHMs differ (Fig. 1). The richness patterns et al., 2016). Then we selected the most optimal “presence/absence” derived from BFDMs of CR, EN, and VU species all weigh more in East map with the largest threshold that made the presence area include all China (Fig. 1A–C). High richness areas of CR species derived from the known occurrence localities as the binary FD map (BFDM) (thresh- BFHMs only locate in a series of scattered and highly restricted patches olds of each species see Appendix S1). We defined the area of each in lakes and coastal tidal flats (Fig. 1E). 3 CR species historically species' BFDM as “the distribution range” of the species. occurring in Yunnan Province (White-rumped Vulture Gyps bengalensis, For each selected species, the BFDM was masked by land cover types Red-headed Vulture Sarcogyps calvus and White-shouldered Ibis Pseudi- to obtain a binary forecasted habitat map (BFHM). The habitat types of bis davisoni) might have gone extinct in China. The majority of surviving each species were obtained from existing data (Mackinnon et al., 2000; CR species distributes in the North China Plain, coastal areas of the Zhao, 2001) (see Appendix S1). We defined the area of each species' Bohai Gulf and the Yellow Sea, as well as the lower and middle reaches BFHM as “the habitat area” of the species. Different populations of the of the Yangtze River (Fig. 1A, Fig. 1E). The richness patterns of EN and same bird species in China may have different residence types, but the VU species resemble that of CR species, but also concentrate in full-year-round occurrence data of many species are limited, so we only mountains and coastal areas in West and South China (EN: Fig. 1B, made one distribution map for each species, regardless of the seasonal Fig. 1F; VU: Fig. 1C, Fig. 1G), including the east of the Tianshan changes of habitats. Mountains, the Qilian Mountains, the north of the Hengduan Moun- We used the map of national nature reserves 2014 (NNRs-2014) in tains, Shennongjia, the Luoxiao Mountains. High richness areas of EN China (from the Nanjing Institute of Environmental Science, Ministry of species derived from BFHMs weigh more in West China, while those Environment Protection of China by inter-agency letter of agreement) from VU species weigh more in Southeast China (Fig. 1F, Fig. 1G). The to calculate the percentages of the distribution range and the habitat distribution range and habitat area of all threatened species is similar to area of all threatened birds covered by NNRs (see Appendix S1). that of VU species (Fig. 1D, Fig. 1H). This is because VU species consist Identical analyses were applied for NPS. most of the modelled threatened species (26/41). Appendix S2 reveals We overlaid the BFDMs of Critically Endangered (CR), Endangered the richness and habitat pattern of NPS-Class I and NPS-Class II. The (EN), and Vulnerable (VU) species respectively to draw the richness richness also concentrates in east China. Besides, the high richness of pattern of each group. Then, we overlaid all threatened species' BFDMs NPS-Class I also occurs in: the Altai Mountains, the Qinling-Daba to infer overall richness pattern and hotspots of threatened species. The Mountains, the Hengduan Mountains, and south Tibet. The high BFHMs were treated similarly. We identified the top 5% richest areas of richness of NPS-Class II also occurs the south Gaoligong Mountains, EN or VU species as the hotspot of the group (Myers, 1988; Jenkins the west Sichuan Basin, as well as Guangdong and Guangxi. The habitat et al., 2013). Extinction risks that all the CR species in East China are pattern of NPS is differentiated from that of threatened species by high facing are so high that we cannot afford any loss of their habitats. In this concentration of NPS-Class I at the Tianshan-Altai region, the Qilian case, II occurrence sites and full BFHMs of CR species were identified as Mountain, the Hengduan Mountains, and high concentration of NPS- hotspots. Identical analyses were applied for NPS. Class II in the Taihang and Lvliang Mountains, as well as all the All the spatial analyses were conducted in ArcMap 10.2. mountains and forests in south China, except for the Sichuan Basin and central Yunnan-Guizhou Plateau. 2.5. Statistical analysis Since the habitat area of the CR species is only 5147 km2 according to the top 5% richest criteria, the hotspots for EN and CR species are put We conducted one-way ANOVA analyses to test the statistical together for further analysis. The hotspots for CR and EN species, with a differences between the percentages of the distribution range and 67,967 km2 area, include: ① the delta of the Liao River; ② the western habitat area of NPS-Class I species and CR/EN species covered by coast of the Bohai Gulf; ③ the coast of the Yellow Sea; ④ wetlands and NNRs. The p-value, F-value, intra-group variance and group variance lakes in the south of the North China Plain, wetlands and lakes in the were calculated to measure these differences. All statistical analyses lower reaches of the Huai River and the Yangtze River; and ⑤ wetlands were conducted in Excel 2013 (2013, Microsoft, Redmond, and lakes in the middle reaches of the Yangtze River, especially the Washington). Dongting Lake and the Poyang Lake (Fig. 2A. Detailed maps see Fig. 2B–D). The western coast of the Bohai Gulf, the North China Plain, 3. Results the southern Liaoning Peninsula, the Shandong Peninsula, the middle and lower reaches of the Yangtze River comprise the hotspots for VU 3.1. Mismatch between IUCN threatened species and NPS list species with a 303,974 km2 area (Fig. 2E). The hotspots for all IUCN threatened species are also similar to those of VU species (Fig. 2F). There is a mismatch between species on the NPS List and those that Appendix S3 shows the hotspots for NPS-Class I and NPS-Class II in IUCN Red List threatened categories. There are 95 threatened bird species, concentrating in the coastal regions of the Bohai Gulf, the lower species identified by IUCN Red List (10 CR, 25 EN and 60 VU), and 239 reaches of the Yangtze River, and southwest Yunnan. The hotspots for bird species listed as NPS (43 Class I and 196 Class II) in China. Among the IUCN threatened species that are not listed as NPS locate in the the 10 CR species, there are 3 NPS-Class I species, 3 NPS-Class II lower reaches of the Huai River and the middle and lower reaches of the species, and 4 species not listed as NPS (Baer's Pochard Aythya baeri, Yangtze River. Spoon-billed Sandpiper Eurynorhynchus pygmeus, Blue-crowned Laughingthrush Garrulax courtoisi, Sociable Plover Vanellus gregarius). 3.3. Percentages of distribution range, habitat area and hotspots covered by At EN level, there are 6 NPS-Class I species, 8 NPS-Class II species, and NNRs of IUCN threatened species and NPS 11 species not listed as NPS. At VU level, there are 16 NPS-Class I species, 10 NPS-Class II species, and 34 species not listed as NPS. On the Results of distribution range and habitat area in each category are other hand, 34 Class I (79%) and 179 (91%) Class II NPS species are shown in Table 1. The distribution ranges of CR, EN, and VU, NPS-Class non-threatened species according to IUCN Red List (details see I, and NPS-Class II species are all far larger than the habitat areas, Appendix S1). especially those of the CR species (see Table 1). The modelled habitat

50 R. Hu et al. Biological Conservation 211 (2017) 47–55

Fig. 2. The hotspots of threatened species in China.A shows the hotspots of CR & EN species, B–D shows the detailed hotspot maps for CR & EN species, E shows the hotspot of VU species, and F shows the hotspot of all IUCN threatened (CR, EN and VU) species. The hotspots concentrate along the coast of the Bohai Gulf and the Yellow Sea, as well as in the middle and lower reaches of the Yangtze River. area of all three CR birds is less than 5% of their distribution range. For (Aichi Target, Convention on Biological Diversity, 2011). There is only other species except the CR birds, the mean modelled habitat area of one species (Black-necked Crane Grus nigricollis) whose percentage of each category is from 20% to 33% of the mean modelled distribution distribution range covered by NNRs is more than 17%. As for most range. species, the percentages of either distribution range or habitat area There are only 5 threatened species (0 CR, 2 EN, 3 VU; 0 NPS-Class covered by NNRs are lower than 5% (see Fig. 3). I, 2 NPS-Class II) with more than 17% of habitat area covered by NNRs The top 10 of threatened species with lowest percentage of

51 R. Hu et al. Biological Conservation 211 (2017) 47–55 The coverage of theby hot spots NRs (%) 13.7) 1.26 19.6) 4.49 28.1) 1.37 28.1) 1.42 17.0) 0.74 34.2) 1.79 34.2) 1.88 – – – – – – –

Fig. 3. Histogram of coverages by national nature reserves on distribution range (orange) and habitat area (blue) of threatened birds.The coverages of most modelled species' Mean coverage of thespecies habitat by for each NRs (%) distribution ranges (orange bars) are not higher than 5%, while the coverages of most modelled species' habitat areas (blue bars) are not higher than 9%. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

distribution range covered by NNRs are Baer's Pochard Aythya baeri, Great Knot Calidris tenuirostris, Grey-sided Thrush Turdus feae, Lesser White-fronted Goose Anser erythropus, Reeve's Pheasant Syrmaticus reevesii, Saunder's Gull Chroicocephalus saundersi, Scaly-sided Merganser Mergus squamatus, Siberian Crane Grus leucogeranus, 2.53) 9.06 (5.57 11.3) 9.57 (1.23 19.6) 7.07 (0.68 19.6) 8.18 (0.68 19.6) 7.64 (0.97 16.7) 5.81 (0.98 19.6) 6.08 (0.97 – – – – – – – Spoon-billed Sandpiper Eurynorhynchus pygmeus and Yellow Emberiza sulphurata. All of them, including 3 CR, 1 EN, and 6 VU species, distribute in East China, especially the coastal area and the species by NRs (%) 4.35 (2.19 5.89 (2.19 lower reaches of the Yangtze River. Only 2 of them are listed as NPS- Class I and 1 as NPS-Class II. ) Mean coverage of the distribution for each 2 The top 10 of threatened species with lowest percentage of habitat area covered by NNRs are Cabot's Tragopan Tragopan caboti, Elliot's 1,716,357) 4.48 (2.29 – 1,634,962) 4.68 (2.19 4,224,838) 6.39 (2.19 – – Pheasant Syrmaticus ellioti, Great Bustard Otis tarda, Lesser White- 4,958,566) 5.81 (2.45 – fronted Goose, Reeves's Pheasant Syrmaticus reevesii, Swan Goose Anser cygnoides, White-eared Night Heron Gorsachius magnificus, White-naped Crane Grus vipio, Yellow-Breasted Bunting Emberiza aureola, Yellow Bunting. Yellow Bunting only marginally distributes in Southeast China and Great Bustard mainly distributes in North ) Mean habitat area (km

2 China. The rest mainly distribute in East and South China. There are 2 EN, and 8 VU species, including 3 NPS-Class I and 3 NPS-Class II 4,883,180) 447,173 (1927 5,315,119) 339,222 (11,240 4,426,667) 410,482 (7010 – – – species. 6,704,911) 744,182 (56 – We calculated the percentage of the hotspots for threatened species covered by NNRs. The results reveal that the percentages of the hotspots covered by NNRs for all groups are below 2%, except for the EN species with a coverage of 4.49%. Even the hotspots of NPS-Class I and NPS–Class II are poorly covered by NNRs, with a coverage less than Mean distribution area (km 2% (Table 1). The one-way ANOVA analysis shows that the percentage of distribution range covered by NNRs of CR and EN species is signifi- cantly lower (F-value = −5.22; p-value = 0.02) than that of NPS-Class I species. The percentage of habitat areas shows similar trend (F-

species value = −4.37; p-value = 0.04).

4. Discussion

4.1. Urgency of updating NPS list

The mismatch between IUCN threatened species and the NPS list may indicate that the fast development in the past 30 years in China has Type Number of CR 3 1,562,639; 860,148; 1,273,947 51,814; 2822; 56,933 2.38 (2.29 EN 14 1,385,378 (100,113 VU 26 1,727,435 (376,008 All IUCN threatenedspecies 43 NPS Class I 23 1,349,099 (162,681 NPS Class II 120 2,226,451 (27,284 All NPS 143 fi Table 1 The distribution and habitat area coverage data of all threatened and national protected species. imposed signi cant threats to many species, which consequently

52 R. Hu et al. Biological Conservation 211 (2017) 47–55 became endangered. This change of bird species is better reflected by them mainly distribute in East China. Our finding suggests a geogra- the IUCN Red List, which is evaluated and updated every 5 years or so. phical overlap between one of the most important engines of the world's For example, although 2 CR species (White-rumped Vulture and economy and the conservation hotspots of world's threatened species. Siberian Crane) and 7 EN species (Sichuan Partridge, Green Peafowl It is not surprising that the percentage of these new conservation Pavo muticus, Hainan Peacock Pheasant Polyplectron katsumatae, Scaly- hotspots covered by NNRs in East China is low, compared with the sided Merganser, Oriental White Stork Ciconia boyciana, Crested Ibis hotspots in Southwest China (Joppa and Pfaff, 2010; Cantú-Salazar and Nipponia nippon and Red-crowned Crane Grus japonensis) are included Gaston, 2010). The mean percentage of distribution range covered by as strictly protected under NPS-Class I category, still 12 of the CR and NNRs of all 41 modelled threatened species is 4.35%, far below the EN species (Baer's Pochard, Spoon-billed Sandpiper, Blue-crowned Aichi target (Table 1). The NNR coverage of the habitat area of Spoon- Laughingtrush, Sociable Plover Vanellus gregarius, White headed Duck billed Sandpiper, one of the most famous CR birds in the world, is only Oxyura leucocephala, Japanese Night Heron Gorsachius goisagi, Silver 13.7% in China, far from adequate for the conservation of the last Oriole Oriolus mellianus, Streaked Reed Warbler sorghophi- 210–228 breeding pairs of the species (Clark et al., 2016). It is urgent to lus, Giant Sitta magna, Rufous-headed Robin Larvivora ruficeps, increase the protection coverage of conservation hotspots in East China Jankowski's Bunting Emberiza jankowskii, Yellow-breasted Bunting) are in order to achieve the Aichi Target of halting species extinction. not nationally protected at all. While celebrating the conservation achievements of panda as a In addition, our work revealed that the habitat areas of 7 threatened flagship species in China (Lu et al., 2000), we need to pay more species are below 20,000 km2. All of them (Great Knot, Spoon-billed attention to the large habitats of the numerous threatened birds, which Sandpiper, Manchurian Reed Warbler Acrocephalus agricola, Chinese are declining dramatically due to unprecedented economic develop- Egret Egretta eulophotes, Far Eastern Curlew Numenius madagascariensis, ment. Given the dense human population and high economic land value Nordmann's Greenshank Tringa guttifer) are migrants with key breeding in East China, it is difficult to designate many new large protected or stopover sites in China. Except for Manchurian Reed Warbler which areas. Conservation of the rich but fragmented biodiversity in the depends on large reed-beds, all of the species depend on tidal flats. highly developed East China poses a real challenge for the government Considering the importance and fast loss of tidal flat habitats (Ma et al., and people of China in the 21st century. Small and local community- 2014), of these species needs careful re-evaluation. based protected areas may be an effective approach and there are The status of Great Knot and Far-eastern Curlew has just been upgraded examples feasible. The management of these protected areas may also to “EN” in November 2015 (IUCN, 2015). involve more contribution from NGOs and enterprises in future. There are two Chinese versions of Red Lists, China Red Data Book of Endangered Animals: Aves (Zheng and Wang, 1998) and Red List of China's Vertebrates (Jiang et al., 2016), yet the lists have not been 4.3. New data source for biological conservation research in China reflected in the China Wildlife Protection Law. The threatened species are classified by scientists based on threatened species assessment, Recently, the number of birdwatchers in China has been growing while the NPS are classified by national authorities, taking the rapidly. The occurrence records from birdwatchers could provide a new scientific, socio-economic and management attributes into account data source for large-scale researches in conservation biology (Chandler (Jiang, 2016). The national authorities are trying to change the et al., 2016). This paper makes an attempt in this direction, as situation. A new version of the China Wildlife Protection Law has been researchers in the U.S. did recently (e.g. La Sorte et al., 2016), mapping launched in China since July 1st, 2016, proposing that the NPS list the distributions of 160 birds of concern. For those birds without needs to be updated every 5 years, and stipulating the habitat con- enough points for modeling, the lack of witness in the past 16 years servation in explicit terms (The National People's Congress of the reveals that we cannot be optimistic about the status of these People's Republic of China, 2015). However, the assessment on the threatened birds. Besides the localities adopted in this paper, the timing status and trends of the species' populations and habitat areas is highly of records and individual counts of each species can be applied to data-driven, and will become a major challenge considering the limited further researches, e.g. analysis of migration strategies and population data availability and difficulties in collecting sufficient information in fluctuations (Supp et al., 2015). Moreover, the butterfly lovers and China. To lower the expense on updating NPS list, we suggest that all plant lovers can also provide citizen science data for ecological and the species higher than “VU” should be enlisted as NPS and strictly phenological monitoring. All these citizen science researches and data protected by the China Wildlife Protection Law. can contribute to conservation planning by government and other stakeholders. We appeal that the government should create policy 4.2. New conservation hotspots for threatened birds identified and convenience for conservation actions by all kinds of stakeholders and significant conservation gaps existing in China increase investment in the environmental education. This will enhance the environmental awareness of the public, and promote the citizen Taking the IUCN threatened bird species checklist into considera- science in biodiversity conservation in return. However, occurrence tion, this paper used a new citizen science bird record database to data from citizen scientific researchers has its own limitations. For reveal new conservation hotspots in East China at a much finer example, bird watchers are not evenly distributed across the country, resolution (0.8421 km × 0.8421 km) than previous studies. They are leading to potential bias in the distribution of the occurrence data. coastal areas of the Bohai Gulf and the Yellow Sea, the south of the In this paper, the use of bird-watching data may introduce some North China Plain, neighboring wetlands of the Huai River, and the errors. For example, the sample size of each species is still relatively middle and lower reaches of the Yangtze River. It is worth mentioning small; the localities of the observation sites might deviate from the true that the hotspots in the Bohai Gulf and the Yellow Sea identified in this occurrences of the birds (similar to the dataset in http://ebird.org, paper coincide with the endangered tidal flats habitats strongly Sullivan et al., 2014); the coordinate conversion might induce errors. advocated (Ma et al., 2014; Kamp et al., 2015; Larson, 2015). All these can result in offsets which are difficult to quantify in the The identified hotspots coincide with China's fast developing species distribution maps and the hotspots maps. Therefore, some regions in the past three decades. Since the enactment of the NPS list results in this paper need to be treated with caution, and more accurate in 1988, the human population has grown by 35.7% (from 1.01 to 1.36 data and new methods are needed in the following studies. billion) in China (National Bureau of Statistics of the People's Republic Supplementary data to this article can be found online at http://dx. of China, 2015). The growth speed is even faster in East and South doi.org/10.1016/j.biocon.2017.03.033. China. In the last 10 years, 23 birds in China were upgraded by IUCN Red List as “threatened” (Baillie et al., 2004; IUCN, 2015) and 15 of

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