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The Globally Threatened in Mongolia: A Review

Onolragchaa Ganbold, Munkhbaatar Munkhbayar, In-Hwan Paik, Gi-Chang Bing, Ariunbold Jargalsaikhan, Erdenetushig Purevee, Woon Kee Peak

PII: S2287-884X(17)30101-2 DOI: 10.1016/j.japb.2017.08.009 Reference: JAPB 253

To appear in: Journal of Asia-Pacific Biodiversity

Received Date: 27 June 2017 Revised Date: 17 August 2017 Accepted Date: 25 August 2017

Please cite this article as: Ganbold O, Munkhbayar M, Paik I-H, Bing G-C, Jargalsaikhan A, Purevee E, Peak WK, The Globally Threatened Birds in Mongolia: A Review, Journal of Asia-Pacific Biodiversity (2017), doi: 10.1016/j.japb.2017.08.009.

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The Globally Threatened Birds in Mongolia: A Review

Onolragchaa Ganbold a,b , Munkhbaatar Munkhbayar c, In-Hwan Paik b, Gi-Chang Bing b, Ariunbold Jargalsaikhan c , Erdenetushig Purevee c, and Woon Kee Peak b*

a Department of Science, Chungnam National University, Daejeon 305-764 Korea b Division of Research and Promotion, National Science Museum of Korea, Daejeon 305-705, Korea c Departments of Biology, Mongolian National University of Education, Ulaanbaatar-210648, Mongolia

ABSTRACT This paper reviews status of globally threatened birds (GTBs) in Mongolia. Here we reviewed 26 GTBs from eight orders. In addition, we summarized here recorded ten GTBs during our 2016 field surveys. geese were most numerous and most frequently sighted of the GTBs with mean 33.8±54.1 counted . The Mongolian Avifauna assessed with 476 of 19 different orders. Twenty-six species (5.1%) out of 476 species had listed in the International Union for Conservation of Nature (IUCN) Red list as GTBs. In addition, there is still huge lack of investigation for GTBs (indeed, whole avifaMANUSCRIPTuna) of Mongolia.

Keywords: Globally threatened birds (GTBs), IUCN, Red list

INTRODUCTION

Mongolia is a vast country with diverse natural zones and landscapes, harboring rich and unique assemblages of birds (Gombobaatar et al, 2011). The country is located at the junction of three migratory flyways, i.e. Australian, Central Asian and East Africa-West Asia flyways. Over the past decades, Mongolia has undergone significant social and economic changes, and during that time, many groups of birds, including cranes, breeding shorebirds, raptors and some passerines, have experienced rapid declines (Gombobaatar et al, 2011). Categories in theACCEPTED IUCN Red list, i.e. Vulnerable (VU), Endangered (EN), and Critically Endangered (CR) were considered as Globally Threatened species in the IUCN Red List, whereas Near Threatened were not included in GTB.

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Foreign scientists have previously studied the Mongolian Avifauna, especially the Russian scientists (including those from the former Soviet Union) conducted basic studies on Mongolian Avifauna during the 19 th and 20 th Centuries (Adiya & Suran, 2008). The previous work included research into the avifauna along the Mongolian-Soviet border area (focusing on Mongol Daguur) which conducted by the Soviet Union’s Institute of Geography. Historical biological expeditions by Mongolia and Germany (between 1962 and 1964) and Mongolia and (since 1970) explored most of the Mongolian avifauna (Adiya & Suran, 2008). Since the second half of the 20 th Century, Mongolian researchers’ roles rapidly increased to study the country’s fauna (Adiya & Suran, 2008) especially in the case of Globally Threatened species. Currently, some surveys on Globally Threatened Birds (GTBs) are being conducted by a joint expedition of Mongolian and foreign scientists in Mongolia. Particularly, migration ecology-flyway, conservation management, and other ecological and biological surveys are being conducted for several GTBs, i.e. Swan ( cygniod ), White-napped Crane (Grus vipio ), Steppe Eagle ( Aquila nepalensis ), Great Bustard ( Otis tarda ), and Saker Falcon (Falco cherrug ). The Wildlife Science & Conservation Center of Mongolia (WSCCM) and the Mongolian Ornithological Society (MOS) are MANUSCRIPT participating with major roles for GTBs studies. Further, two major conservation documents for Mongolian birds were titled as: (a) “Directory of Important Bird Areas in Mongolia: KEY SITES FOR CONSERVATION” and (b) “MONGOLIAN RED LIST OF BIRDS” performed by these two organization, respectively. In addition, Ornithological Laboratory of the Mongolian Academy of Science and Department of Biology of Mongolian National University of Education (MNUE) had been playing a significant part for study on GTBs. Furthermore, here we reported ten GTBs belong to four orders which were observed in 2016 Important Bird Area (IBA) survey, performed by research team of MNUE and National Science Museum of Korea (NSMK). In addition, the most part of Mongolian avifauna remain as very poor investigated. As meintioned above,ACCEPTED earlier studies conducted by foriegn scientists and since 1980s by themselves which were focused on some GTBs. Further, there is still a need to expand the birds survyes in Mongolian avifauna to improve understanding their avifauna importance. Our

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objective for this paper is to introduce wide opportunities and territory of Mongolian avifauna to the international organizations, individual reseachers as well.

STATUS OF MONGOLIAN BIRDS

In recent years, international nature conservation organizations are paying attention to the highly diverse Mongolian avifauna. Mongolia is one of the top-priority countries for bird research and conservation as it is located at the junction of three different migratory flyways and contains globally significant breeding grounds for threatened species (Gombobaatar et al, 2011). The main bird habitats in Mongolia comprise of grassland steppe, semi-desert and desert, mountain steppe, high mountains, forested mountains, and riparian areas (Batbayar et al, 2009). Currently, 476 species of birds had recorded in Mongolia, belonging to 60 families and 19 orders. There are 81 species of resident birds and 395 species of migratory birds. In addition, 310 species of migratory birds breed in Mongolia, ten species are winter visitors from , nine species are summer visitors and 66 species MANUSCRIPT are vagrants (Bold et al, 2007). The 435 species listed as of Least Concern (LC) in the IUCN Red List, whereas, 14 species listed as Near Threatened (NT), 14 species as Vulnerable (VU), 9 species as Endangered (EN), and three species listed as Critically Endangered (CR) (Figure 1) (Gombobaatar et al, 2011). Twenty-six species GTBs (VU, EN, CR) are belonging to eight different orders (42%) of 19 orders of Mongolia (Figure 2). Population trend of these 26 GTBs is considering still rapidly decreasing across in their global ragnes.

Status summaries for GTBs

Here we reviewed the 26 GTBs that distributed in Mongolia using historical literature sources (time ranged fromACCEPTED 1930s to 2016). The most part of Mongolian avifauna, especially GTBs and Near Threatened species (NT) are poor investigated through its valuable Mongolian breeding range in the past. Just since 1990s, the investigation of GTBs had been increased at the regional and international research levels. As a result, three (12%) of 26 species became well

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studied species in their Mongolian range. Unfortunately, other 23 GTBs (88%) are considered as very poor studied species in their Mongolian range (indeed Eastern and Central Asia). Most of the previous studies were conducted for Raptors (six species) (also known as the birds of prey), especially for their distribution, number, , breeding, mortality and diet composition. In particularly, Endangered Saker falcon is the most investigated GTB in Mongolia, and this species historically studied by several expeditions such as: Przewalskii (1876); Bianki (1915); Dementiev & Shagdarsuren (1964); Kozlova (1975); Shagdarsuren (1983); Bold et al. (1996); Ellis et al. (1996; 1997); Sumiya & Batsaikhan (1999); Sumiya et al. (2001); Shagdarsuren et al. (2001); and Gombobaatar et al. (1999, 2000a, b, 2001, 2003). In Mongolia, the breeding Saker uses utility poles (n=10 nests), bridges (n=2), old buildings (n=3), track tires (n=1) and rock cliffs, slopes, top of stone pillars and short elms (n= 64 combined) for its nesting site in central and southeast Mongolia (Ellis et al .1997). Further, mortality of GT raptors, i.e. Saker Falcon and the Steppe Eagle (with other raptors) was investigated by several research teams (Harness et al, 2008; Amartuvshin et al, 2012; Batbayat et al, 2017) in eastern and southeast Mongolian steppes where shortage of nesting site. They reported that electrocution could considered as one of the dominant threat for raptors in Mongolia (indeed in their Global RanMANUSCRIPTge IUCN, 2016). During our survey in 2016, we observed seven individuals from seven different localities (Table 2) and we found four electrocuted (dead) birds just in our 10km drive in Bogd soum (village) of Ovorkhangai aimag (province: N44.81- 44.90; E101.92 – 102.00). The Steppe Eagle’s population, especially, its European population is rapidly decreasing since the past few decades due to strong factors such as the conversion of steppes to agricultural land and electrocution (Table 1). This species known from several studies in Mongolia: Gombobaatar et al. (2012) showed that high mortality occurred in their young nestlings ( and young chick) (average fledging success was 42.2%) during the early breeding time. Since the Steppe Eagle often selects the ground surface (22 of 49 nests) as its breeding site, foxes and wolves easily hunt on the nestlings (Ellis etACCEPTED al, 2003; Gombobaatar et al, 2012). The Pallas’s Fish Eagle (VU) is known from only one study (Gilbert et al, 2014) but no breeding pair has been observed so far. During our IBA survey in 2016, we observed 16 Steppe Eagle and single individual Pallas’s Fish Eagle respectively (table 2). For the other three raptors, i.e. the Greater Spotted Eagle

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(VU), the Imperial Eagle (VU) and the Egyptian Vulture (EN), the available studies were mostly conducted in South Asia (Cuthbert et al, 2006) and Europe (Katzner et al, 2005; Demerdzhiev et al, 2011), while no reports were available in Mongolia. Notably, the eastern Mongolian, especially the Mongol Daurian and a numerous small lakes host all six species of cranes in Mongolia (Batbayar et al, 2009). Four out of six cranes had been listed by the IUCN as globally threatened, including Siberian Crane (Grus leucogeranus ), Red-crowned Crane ( Grus japonensis ), Hooded Crane ( Grus monacha ) and White-napped Crane ( Grus vipio ) (Table 1). Among these species, White-napped Crane (WNC) is moderately studied, and known from three studies (Bradter et al, 2005; Gilbert et al, 2016; WSCCM) in eastern Mongolia, while no studies available for other three cranes (only individual registration available; all available studies performed in and Higuchi et al, 1998; Zou et al, 2004; Wang et al, 2009). WNC’s surveys conducted in the Ulz River basin where is considered as a most valuable breeding site for all cranes (17 breeding pairs of WNC were recorded by Gilbert et al, 2016) in eastern Mongolia. The WSCCM and the Arizona State University joint project performed poaching, nest destruction, migration flyway and land-use change observation surveys for the Great Bustard in eastern Mongolia (Kessler et al, 2013). In addition, the Eurasian Bustard Alliance MANUSCRIPTis performing key conservation studies on the Great Bustard in central Asia, including Mongolia (Kessler et al, 2014). We observed all four globally threatened cranes and great bustard: 22 WNCs, five hooded cranes, one Siberian and Red-crowned crane respectively, as well as five great bustards only from eastern Mongolia (Table 2) during our IBA survey in 2016. No studies available for other species Gruiformes such as, Houbara bustard (Chlamydotis undulata) and Swinhoe’s Rail (Coturnicops exquisitus ) in Mongolia. Four species of waterfowls (Table 1) are recognized as globally threatened in Mongolia. Among these species, only Swan Goose studied by several studies in Mongolia (Goroshko 2003, 2004; Batbayar et al, 2006, 2011). The eastern Mongolian lakes Buir Lake, Khukh Lake, and Mongol DaurianACCEPTED Lakes are supporting a major population of the Swan Goose by their nesting and molting sites (Goroshko, 2003, 2004; Batbayar et al, 2006). Moreover, Swan Goose was most numerous and most frequently sighted of the GTBs in our IBA survey, with over than 500 counted birds in eastern Mongolian lakes. Unfortunately, no reports are

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available for other three species of waterfowls. Moreover, Lesser White-fronted Geese is only known from two observations in Kherlen Ulz River valleys and Buir Lake-Khalkh River- Khyangan Region in small groups during their migration (Formin & Bold, 1991; Tseveenmyadag et al, 2005). Baer’s Pochard is a very rare summer visitor recorded at Mongol Daguur and Khalkh-Buir Lake Region (Formin & Bold, 1991). Only one pair of the White- headed Duck’s was found in Khar Us Lake, and this species occurred only in the western Mongolian lakes and rivers including Dorgon Lake, Khyargas Lake, Khovd River, and the Zavkhan River basin (Fomin & Bold, 1991; Dawaa et al, 1994; Boldbaatar, 2005). Three species of Passeriformes are recognizing as GTBs in Mongolia, including the White-throated Bushchat (WTB), the Yellow-breasted Bunting (YBB) and Jankowski’s Bunting. Only the WTB is known from a single study, which conducted by WSCCM in southwest Mongolia. In addition, Mongolia (Mongol Altai) is considered as only one of the breeding sites for WTB in the world. There are no studies available for the Yellow-breasted Bunting and Jankowski’s Bunting. However, several expeditions reported that the YBB is breeding in the valleys of big rivers and lakes, and in the Khangai, Altai, Khuvsgul and Khentii Mountains (Kozlova, 1930; Fomin & Bold, 1991; Dawaa et al, 1994). The only one record available for Jankowski’s Bunting in the MANUSCRIPT Khalkh and Numrug Rivers in eastern Mongolia (Mauersberger, 1979). Dalmatian Pelican is classified as Vulnerable, and this species is known from only one study in western Mongolia (Batbayar et al, 2007), and is regionally distributed in western Mongolian lakes, i.e. Khar Us Lake, Uvs Lake and Khotont Lake, and these sites were recognized as historical breeding sites for the species. Batbayar et al. (2007) reported that there are two important breeding sites for Pelican in Mongolia such as, Khar Us and Airag Lake, and shooting them for bill and high disturbance of nomadic herders are the most crucial threats to the species in western Mongolia. They counted 14 Pelicans at Khar-Us Lake, but no nestlings and active nests were observed that time. In addition, they assessed breeding habitat of Pelican in westernACCEPTED Mongolia, and constructed Pelican nest platform at an island of Khar Us lake for supporting new breeding site. Unfortunately, no studies are available for three species of Charadriiformes, such as, Relict Gull, Far Eastern Curlew and Sociable Lapwing; however, several records are available

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for them. According to historical review, two individuals of Sociable Lapwing were observed with the Northern Lapwing group at Ogii Lake in 1998 (Boldbaatar, 2002a). Far Eastern Curlew is not breeder in Mongolia and during the course of migration several individuals were observed at Ogii Lake, Orkhon-Tuul, Selenge and Onon Rivers (Dawaa et al, 1994; Tseveenmyadag & Bold, 2005). Moreover, Relict Gull has been recorded from many different localities through Mongolia, with breeding records from two sites, i.e. Khar-Us Lake and Taatsiin Tsagaan Lake (Tseveenmyadag & Bold, 2005) in western Mongolia. The Oriental Stork (Ciconiiformes) is a rare summer visitor or passage migrant, and this species known from only three records at Ulz River valley, Buir Lake, and Khalkh River, respectively (Tseveenmyadag, 1998; Formin & Bold, 1991; Dawaa et al, 1994). No more study is available for this species in Mongolia. The Yellow-eyed Pigeon (Columbiformes) is a vagrant in Mongolia, also known from only two records, such as, at Telmen Lake and Bulgan River Basin (Bold & Mainjargal, 2006). This species’ global distribution is in central and southwest Asia (Birdlife International 2016). There are six status changes in the IUCN Red List between 2011 and 2016 in Mongolian Avifauna, including Baikal Teal formosa and Lesser Kestrel Falco naumanni that were down-listed to Least Concern from vulnerable. FurthMANUSCRIPTermore, five upgrades were recorded, including the Steppe Eagle (Least Concern-EN), Baer’s Pochard (EN-CR), the Saker Falcon (VU-EN), Yellow-breasted Bunting (VU-EN) and Far Eastern Curlew (VU-EN) so far.

Threats for GTBs Although Mongolia has one of the lowest human population densities in the world, its population growth rate is one of the highest in East Asia (Batbayar et al, 2009). Following high growth rate of human settlements, livestock overgrazing, degradation and desertification of steppe and wetland ecosystem, steppe and forest fire and mining actions are rightly considering as crucial threats for GTB. Furthermore, other researchers previously reported for threats: ACCEPTED

(i) Steppe fires, which mostly originated by artificial have become a real threat to biodiversity, even to humans, contributing to mortality. They also considered steppe

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fires to be natural disasters that frequently occur in every dry season (Elbegjargal et al, 2016). The greatest threat to biodiversity at the eastern Mongolian IBA is the steppe fires, which mainly originate from Russia. Steppe fires occur every year and cover very large areas in Eastern and Northern Mongolia (Batbayar et al, 2009). Goroshko (2003; 2004) shows that steppe fires directly affect to high rate mortality of some GTBs, especially Swan Goose in eastern Mongolia. (ii) Fourteen (53.8%) of 26 GTBs live in the lake and wetland in Mongolia. Unfortunately, the water levels of many steppe lakes have fallen in recent decades, with some wetlands completely disappearing. In some cases, this has been due to the damming or diversion of rivers and streams, to divert water for irrigation and livestock (Batbayar et al, 2009). The Ministry of Environment and Green Development (2016) reported a rapid drying out of lakes all over Mongolia during the past 16 years (1996-2011). In our 2016 IBA survey we found that seven lakes out of 41 lakes completely drought in Mongol Daguur IBA because of both natural phenomena and uncontrolled human usage. (iii) Batbayar et al. (2009) also suggested that the main land use is for livestock husbandry in the most Important Bird Area (IBAs) sites MANUSCRIPT throughout Mongolia, and most of the wetland degradation (steppes as well) is caused by uncontrolled high-density livestock.

DISCUSSION & CONCLUSION Gombobaatar et al. (2011) reported that Mongolia has undergone significant social and economic changes, and during that time, many groups of birds, including cranes, breeding shorebirds, raptors and some passerines, have experienced rapid declines in over last decades. Whereas, authors consider it as Mongolian avifauna, in particularly GTB did not face with any dangerous threats in Mongolian range. Furthermore, there are could be some threats to the avifauna in some parts of Mongolia, but these threats risk are not as hish as those found in other part of theirACCEPTED global ranges, i.e. large group of Whooper Swan poisoned in Northeast China in 2016 and vultures poisoned in India, Russian waterfowl hunting culture, and limited distribution range in countries which have high human density. Whereas, Mongolia is

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considered as lowest human density in the world, do not have any waterfowl hunting culture and do not poisoning birds (indeed other wildlife). Mongolia is considering as the main breeding site for ten (38.5%) of 26 GTBs. The breeding site, occurrence, and distribution range varied among these species. In particular, the major breeding population of the Saker Falcon, the White-throated Bushchat, the Swan Goose, the Great Bustard and several species of cranes that breed in Mongolia. Unfortunately, only a few studies have been addressed to the few of the GTBs, i.e. the Saker Falcon, the Swan Goose, the Steppe Eagle, the White-napped Crane, and the Great Bustard. Otherwise, the Mongolian GTBs are very poor studied in their Mongolian range. It could be due to lack of budget-funds/management of researchers, as well as their limited distributions and densities in Mongolia. Approximately nine (34.6%) GTBs are known from only one up to three times observations in some parts of Mongolia. And, seven (27.0%) GTBs are frequently observing in the country, but no regular breeding sites were detected. Definitely, the lack of investigation of GTBs is badly affect for their future conservation trend. In addition, many species birds became Globally Threatened Bird in the world (Steppe Eagle in Mongolia in 2015) due to population decline, which caused by poor knowledge, habitat degradation and other dominant threats. For closing this gap, at least basic studi esMANUSCRIPT needed for future conservation of these GTBs.,

Conflict of interest

The authors declare no conflict of interest.

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Table 1. Summary of status for the 26 species GTB (Birdlife International.2016)

Species Name IUCN Estimated global Current Globally Major Threats status population trend Swan Goose VU 60,000-90,000 Decreasing Uncontrolled Hunt Anser cygnoides Lesser white-fronted Goose VU 28,000-33,000 Decreasing Illegal spring hunt Anser erythropus Creater spotted Eagle VU 5,000-13,200 Decreasing Electrocution and Aquila clanga Imperial Eagle VU 3,500-15,000 Decreasing Intensive forestry Aquila heliaca Steppe Eagle EN ~62,700 Decreasing Conversion of steppes to agricultural Aquila nipalensis land/ Electrocution Baer’s Pochard CR 150-700 Decreasing Poorly understood Aythya baeri Haubara bustard VU 13,000-33,000 Decreasing Illegal Hunt Chlamydotis undulata Oriental Stork EN 1,000-2,499 Decreasing Deforestation and drainage of wetlands Ciconia boyciana Yellow-eyed Pigeon VU 15,000-30,000 Decreasing Illegal Hunt Columba eversmanni Swinhoe’s Rail VU 2,500-9,999 Decreasing Destruction and modification of Coturnicops exquisitus wetlands Yellow-breasted Bunting EN 20,000-100,000 MANUSCRIPT Decreasing Excessive trapping Emberiza aureola Jankowski’s Bunting EN 375-1,499 Decreasing Increase of agricultural land Emberiza jankowskii Saker Falcon EN 12,800-30,800 Decreasing Degradation of steppes/ Electrocution Falco cherrug Red-Crowed Crane EN 3,050 Decreasing Degradation of wetlands Grus japonensis Siberian Crane CR 3,500-4,000 Decreasing Degradation of wetlands Grus leucogeranus Hooded Crane VU 11,600 Decreasing Wetland loss and degradation Grus monacha White-naped Crane VU 6,250-6,750 Decreasing Loss of wetlands to agricultural Grus vipio expansion Pallas’s Fish Eagle VU 3,500-15,000 Decreasing Habitat degradation and disturbance Haliaeetus leucoryphus Relict Gull ACCEPTEDVU 12,000 Decreasing Loss of ephemeral wetland Larus relictus Egyptian Vulture EN 12,000-38,000 Decreasing Direct and secondary poisoning Neophron percnopterus Far Eastern Curlew EN 38,000 Decreasing Wetland degradation in the Yellow Sea Numenius madagascariensis

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White-headed Duck EN 7,500-15,900 Decreasing Introgressive hybridization Oxyura leucocephala Great Bustard VU 44,000-57,000 Decreasing acclimated to agricultural landscapes Otis tarda Dalmatian Pelican VU 6,700-9,300 Decreasing Wetland drainage Pelecanus crispus White-throated Bushchat VU 3,500-15,000 Decreasing Loss and modification of grasslands Saxicola insignis Sociable Lapwing CR 6,000-8,000 Decreasing Poorly understood Vanellus gregarius Estimated Global population retrieved from official website of International Bird Life; IUCN Red List categories include Critically Endangered (CR), Endangered (EN) and Vulnerable (VU)

Table 2. Observed Globally Threatened Bird during our 2016 IBA survey

Scientific name English name OF Counted bird IUCN Global status Observed Areas Mean (±SD) IUCN Redlist Anser cygnoides Swan Goose 19 33.8±54.1 Vulnerable Mongol Dagur, Buir, Khukh Lake Haliaeetus leucoryphus Pallas's Fish-Eagle 1 1±0.0 Vulnerable Khukh lake Aquila nipalensis Steppe Eagle 11 1.5±1.2 Endangered Hustai NP, Eastern Mongolia Falco cherrug Saker Falcon 7 1±0.0 Endangered Eastern Mongolia, Khan MANUSCRIPTKhenty, Hustai NP, Ikh Nart Larus relictus Relict Gull 5 1.8±0.5 Vulnerable Khukh, Buir lake Lake Grus vipio White-naped Crane 7 3.1±1.5 Vulnerable Eastern Mongolia, Khan Khenty Grus monacha Hooded Crane 3 1.3±0.5 Vulnerable Mongol Dagur Grus leucogeranus Siberian Crane 1 1±0.0 Critically Ugtam Mountain (Nogoon lake) endangered Grus japonensis Red-Crowed Crane 1 1±0.0 Endangered Mongol Dagur Otis tarda Great Bustard 2 1.5±0.7 Vulnerable Khukh Lake, Eastern Mongolia OF=Observed frequency; NP = National Park; IUCN - International Union for Conservation of Nature . All of these threatened species have listed in Conservation for Migratory Species (CMS).

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List of figure.

Figure 1. IUCN Red List status of all birds (a) and IUCN Red List status of globally

threatened birds (GTBs) (Gombobaatar et al, 2011; Birdlife International 2017)

Figure 2. IUCN Red List status by orders (8) of Mongolian Avifauna. NS= No Species listed;

VU= Vulnerable; EN= Endangered; CR= Critically Endangered

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