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Journal of Resources and Ecology >

2022 , Vol. 13 >Issue 1: 41 - 50

DOI: https://doi.org/10.5814/j.issn.1674-764x.2022.01.005

Biodiversity Conservation and Use

Père David’s Deer (Elaphurus davidianus) in China: Population Dynamics and Challenges

  • XUE Dayuan , 1, † ,
  • ZHANG Yuanyuan , 2, 3, †, * ,
  • CHENG Zhibin 2, 3 ,
  • ZHONG Zhenyu 2, 3 ,
  • CAO Ming 4 ,
  • FU Mengdi 5 ,
  • BAI Jiade 2, 3 ,
  • YUAN Xuejiao 1
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  • 1. School of Life and Environmental Sciences, Minzu University of China, Beijing 100081, China
  • 2. Beijing Milu Ecological Research Center, Beijing 100076, China
  • 3. Beijing Biodiversity Conservation Research Center, Beijing 100076, China
  • 4. Institute of Environmental Governance and Big Data Application, Environmental Development Center of the Ministry of Ecology and Environment, Beijing 100029, China
  • 5. Key Laboratory of Regional Eco-Process and Function Assessment and State Environment Protection, Chinese Research Academy of Environmental Sciences, Beijing 100012, China
* ZHANG Yuanyuan, E-mail:

† means that they have the same contribution to this paper.

XUE Dayuan, E-mail:

ZHANG Yuanyuan, E-mail:

Received date: 2021-08-03

  Accepted date: 2021-11-02

  Online published: 2022-01-08

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Abstract

The reintroduction of rare and endangered species is one of the most important approaches to conservation and ecosystem restoration, but it has still proven to be an adventurous undertaking and most reintroduction programmes fail, so successful demonstrations are needed. Père David’s deer (Elaphurus davidianus, Milu in Chinese) could be considered one of conservation’s great success stories, as this species’ path on the road to extinction has been reversed by a combination of ex-situ conservation and successful re-introduction in China. The species had been consigned to an imperial hunting ground when the last Chinese herds were exterminated during the fall of the Qing Dynasty (1644-1912). Fortunately, a few of the last remaining individuals were sent to European zoos. From these animals, a herd was bred on the 14th Duke of Bedford’s estate, Woburn Abbey, and between 1985 and 1987, and 38 Milu were donated back to China for re-introduction in Beijing Milu Park (BMP), the former imperial hunting ground. An additional 39 deer were released at Dafeng National Nature Reserve (DFNNR), Jiangsu Province in 1986. In both of these safe and protected locations, the Milu thrived allowing for over 700 Milu to be sent to a further 82 sites throughout the species’ original Chinese range over the last 36 years. As a result, the Milu population totaled 9136 by 2021, with 2855 individuals now living back in the wild; while another 5681 individuals inhabit the DFNNR, and 186 reside in BMP. Wild Milu, however, still face significant conservation challenges. The population lacks genetic diversity, leading to severe inbreeding depression and carrying multiple risks, such as high miscarriage rates, a reduced lifespan, and susceptibility to disease. Environmental constraints such as pollution and habitat fragmentation further result in small, fragmented wild populations. Moreover, the species currently lacks a national level conservation master plan, the associated coordinated monitoring platforms, and breeding plans for China’s captive populations. Finally, there is now a lack of international cooperation in the conservation of this species. We therefore call for both a national-level conservation master plan in China and international cooperation to develop a shared database and germplasm databank covering Milu across all countries with ex-situ populations, as crucial steps for securing the long-term conservation of Milu and preventing it from ever becoming “extinct in the wild” again.

Key words： Elaphurus davidianus; Milu; reintroduction; ex-situ conservation; population dynamics

Cite this article

XUE Dayuan , ZHANG Yuanyuan , CHENG Zhibin , ZHONG Zhenyu , CAO Ming , FU Mengdi , BAI Jiade , YUAN Xuejiao . Père David’s Deer (Elaphurus davidianus) in China: Population Dynamics and Challenges[J]. Journal of Resources and Ecology, 2022 , 13(1) : 41 -50 . DOI: 10.5814/j.issn.1674-764x.2022.01.005

1 Introduction

The reintroduction of rare and endangered species is one of the most important approaches to conservation and ecosystem restoration (IUCN, 2013). Hundreds of reintroduction projects have been implemented around the world since a group of captive-bred American bison were reintroduced into a newly established reserve in Oklahoma, USA in 1907 (Kleiman, 1989; Seddon et al., 2012). From 2008 to 2018, 290 reintroduction programmes have been implemented globally for various species of invertebrates, amphibians, reptiles, birds and mammals (Soorae, 2010, 2011, 2013, 2016, 2018 and 2021). Nowadays, populations of some endangered species, such as Eurasian lynx (Lynx lynx), Eurasian beaver (Castor fiber) (Marr et al., 2018), wolf (Canis lupus) (Bartnick et al., 2013), etc., have increased and their wild populations have been reestablished.
However, reintroduction has still proven to be only sporadically successful and most reintroduction programmes fail (Oded and David, 2014). Due to a lack of monitoring, in many instances the causes of the failures are unknown (Seddon et al., 2007). Poorly conceived reintroduction project success rates have been very low (Griffith et al., 1989; Wolf et al., 1996). Reviews of reintroduction projects have generally reported success rates of lower than 20% (Osborne and Seddon, 2012). According to the IUCN Global Re-introduction Perspectives Bulletin, the rates of successful reintroduction projects in 2008, 2010, 2011, 2013, 2016 and 2018 were 54%, 58%, 56%, 61.2%, 64.8% and 79.7%, respectively (Soorae, 2008, 2010, 2011, 2013, 2016, 2018). Thus, global reintroduction programmes desperately need successful examples for demonstration purposes (Cheng et al., 2021).
Milu (Père David’s deer, Elaphurus davidianus) is endemic to China and listed on the IUCN Red List as Extinct in the Wild (IUCN, 2016). It was once widely distributed in the wetlands of the Yangtze River and Yellow River basins (Cao, 1985). Its historical wild distribution in China ranged from 18°N to 45°N and east of 110°E. As a result of climate change and human disturbances, it was believed that Milu may have been extinct in the wild 1500 years before the last captive population disappeared from Nanhaizi in Beijing in 1900 due to flood and war (Cao, 1985; Jiang and Harris, 2016). All Milu today are descendants of 18 individuals that were the nucleus for the 14th Duke of Bedford’s captive breeding project at Woburn Abbey, England (Cao, 1985). At the end of World War II, the size of the Woburn Abbey herd reached 250 individuals. To better protect them, the Duke of Bedford relocated some to other zoos, first to other sites in the UK and then to other countries (Maddison et al., 2012). In order to support Milu recovery in China, a total of 38 individuals were reintroduced into Beijing Milu Park (BMP) from Woburn Abbey in 1985 and 1987. To establish another founder population, 39 individuals were reintroduced to Dafeng Milu National Nature Reserve in Jiangsu Province from zoos of England in 1986 (Jiang and Harris, 2016; Cheng, 2021).
The reintroduction of this species is considered one of the most successful stories in the world. It provides a watershed example of biodiversity conservation best practices for the upcoming UN Decade on Ecosystem Restoration, and China’s wisdom in wildlife conservation (Zhang et al., 2021). This review investigates the population dynamics of this species before and after reintroduction, the achievements of the practices of reintroduction and ex-situ conservation, and the challenges faced by species development, and it also provides suggestions for the long-term conservation of this species in China.

2 Data collection and methods

Historical data were generated from the literature, including books and research and review papers on Milu.
After the reintroduction of Milu in 1985, we have been recording population dynamics in major distribution sites, including Beijing Milu Park (BMP), Dafeng Milu National Nature Reserve, Jiangsu Province (DFNNR), Yancheng Wetland and Rare Birds National Nature Reserve, Jiangsu Province (YCWNNR), East Dongting Lake National Nature Reserve, Hunan Province (DTLNNR), and Shishou Milu National Nature Reserve, Hubei Province (SSNNR).
Since 2013, in order to obtain a general picture of the Milu population and distribution in China, we have conducted dozens of field surveys, telephone surveys and literature reviews. Through those surveys, we have recorded Milu populations at 82 wildlife protection sites in China, including zoos, nature reserves, wetland parks, and wildlife rescue centers.
The distribution map was drawn using ArcGIS 10.6.

3 Population dynamics

3.1 Extinction and reintroduction of Milu in China

3.1.1 Phase 1: Extinct in the wild, preserved in the imperial hunting park

Milu are native to the swamp areas of the middle and lower reaches of the Yangtze and Yellow rivers in China. Fossil sites of wild Milu and the number of unearthed fossils indicate that Milu originated 2 million years ago, and the population peaked at about 10000 individuals around 3000 years ago (Bai, 2014). As of 1978, 64 fossil sites were reported, most of them in Jiangsu Province (Cao, 1978).
At the end of the Han Dynasty, the population of Milu declined sharply due to habitat loss and increased hunting. During the Yuan Dynasty, Mongolian soldiers transported the remaining wild Milu from the Yellow Sea coast to Dadu (Beijing) for the descendants of the royal family to shoot on horseback. Thus, the wild population of Milu disappeared. In the early Qing Dynasty, the last remaining herd of Milu in China was maintained in Nanhaizi Imperial Hunting Park in Beijing (Bai, 2014).
In 1865, the French missionary Jean Pierre Armand David went to the southern suburbs of Beijing and discovered the Milu for western science. He obtained a specimen of the Milu and sent it to the Natural History Museum in Paris, France. After inspection, it was determined that it was not only a new species, but also a distinct genus. At this point, the Chinese Milu was first described to the world.

3.1.2 Phase 2: The population survived abroad

After 1866, ministers and churchmen from Britain, France, Germany, Belgium and other countries sent dozens of Milu from Nanhaizi Imperial Hunting Park in Beijing to zoos around the world. In 1894, when the Yongding River flooded, the walls of Nanyuan collapsed and the Milu that escaped were fed by the hungry people. In 1900, when the Eight-power allied forces invaded Beijing, the remaining Milu were either killed or shipped to Europe by the Western powers. Thus, the Milu became extinct in China.
Over time, the population of Milu kept in zoos in Europe gradually decreased due to insufficient environmental adaptation. In 1898, the Duke of Bedford bought all 18 Milu from the zoos around the world and set them free on his 3000-acre Woburn Abbey estate. During World War Ⅱ, the population number reached 255. In order to avoid the risks posed by the war, Woburn Abbey began to transfer the Milu to zoos around the world. By the end of 1983, the total number of Milu reached 1320 (Bai, 2014).

3.1.3 Phase 3: Reintroduction of Milu to China

The ultimate goal of reintroduction is to establish long-term self-sustaining wild populations, and the reintroduction of Milu has two objectives. The first is to bring the Milu from foreign parks back to China and to keep them in captivity for ex-situ conservation. The second is to return the captive Milu population to its original wild habitat, in order to restore the lost wild characteristics of behavior and physiology and to allow the species to fulfill its ecological role in the wild.
In 1985, China launched the Milu reintroduction programme. A total of 38 Milu (5♂, 33♀) were transported from Woburn Abbey in the UK to BMP in 1985 and 1987, and the Beijing Milu Ecological Research Center dedicated to Milu and biodiversity conservation was established. In 1986, another 39 Milu (13♂, 26♀) were introduced from London Zoo to Dafeng National Nature Reserve (DFNNR), Jiangsu Province, and DFNNR was established for the purpose of Milu conservation (Cao, 1978; Cao, 1985; Wang, 2020).

3.2 Population development in China

3.2.1 Phase 1: Breeding and population expansion

BMP and DFNNR were responsible for the initial breeding, rejuvenation and population expansion of the introduced Milu population.
In 1991, BMP reached the first goal of Milu reintroduction by restoring the basic population to 60-80 Milu. By 1996, 250 Milu had been born in BMP (Zhang et al., 1998). In order to balance the relationship between the Milu population and the environmental carrying capacity, the Milu population has been maintained at about 150 through export. As of June 2021, the population of Milu in BMP was 186.
DFNNR is located in the southeastern corner of Dafeng City, Jiangsu Province, on the shore of the Yellow Sea. It has a total area of 2667 ha, of which the core area is 1657 ha, the buffer area is 288 ha, and the experimental area is 722 ha. The average elevation is 2-4 m, and there are 199 species of edible plants in the area, providing suitable habitat for Milu (Xu, 2019; Wang, 2020). In 1986, 39 Milu from London Zoo and other collections arrived at DFNNR. After breeding, the birth rate was maintained at 20%-30%, and the Milu population was expanding year by year. The basic population reached 78 in 1990 and 468 in 2000 (Su, 2003). In order to relieve the pressure of rapid population growth on the environment and promote the sustainable development of the population, the Milu population was adjusted according to a fixed age ratio, and the population size was kept in the appropriate range by transferring some Milu out every year (Yu, 1996). By the end of 2021, the population had grown to 5681.

3.2.2 Phase 2: ex-situ conservation

In order to achieve the second-phase goal of the introduction of Milu, namely restoring the natural population, BMP formulated and initiated the ex-situ conservation plan of transporting some Milu to Tian-e-zhou wetland of the Yangtze River in Shishou City, Hubei Province, and establishing Shishou Milu National Nature Reserve (SSNNR). A total of 64 Milu were exported from BMP to SSNNR in two batches in 1993 and 1994 (Zhang, 1998). Since then, BMP has exported Milu to other parts of the country, and a total of 546 Milu had been exported from BMP by the end of 2020 (Bai, 2021).
DFNNR began exporting Milu to other parts of the country in 1995, and it had exported a total of 164 Milu by the end of 2020.

3.2.3 Phase 3: Release into the wild to form a wild population

In 1998, the Yangtze River burst its banks and the habitat of the free-range Milu in SSNNR was flooded. According to statistics, a total of 34 Milu fled the area, including 11 that fled to Yangbotan wetland in Shishou County, and 23 that swam across the Yangtze River to Sanheyuan wetland in Shishou City. Five others drifted to Dongting Lake in Hunan province, where several Milu later settled. Of the population that fled to Yangbotan Wetland, due to the reclamation of this area, most of the Milu were transferred to Tuerzhou, Jianli County, where the number increased to more than 200. The Milu entering the wetland of Sanheyuan gradually formed a population of about 200. About 220 Milu have entered the East Dongting Lake National Nature Reserve, Hunan Province.
On November 5, 1998, DFNNR was chosen to carry out the rewilding plan, and eight Milu were selected to be released into the wild. The released Milu quickly adapted to the wild and successfully reproduced. After the initial release, in order to optimize the population structure of wild Milu, five additional wild reintroduction campaigns were conducted in 2002, 2003, 2006, 2016 and 2020, during which 108 Milu were released into the wild. In 2018 and 2019, some Milu were released from the reserve in two batches. According to field observations, these releases have led to a wild population of 1820 Milu by 2020.
Table 1 Main distribution sites of Milu in China
Site BMP DFNNR YCWNNR DTLNNR SSNNR
Geographic coordinates 39°07'N, 116°03'E 33°05'N, 120°49'E 33°37°N, 120°30°E 29°21°N, 112°55°E 29°49'N, 112°33'E
Area (ha) 60 2667 247260 156900 1567
Annual average temperature (℃) 13.1 14.1 14.2 17 16.5
Average temperature in January (℃) -3.4 0.9 1.1 2.1 2.4
Average temperature in July (℃) 26.4 22.4 22.1 22.9 23.8
Average precipitation (mm) 600 1068 1040 1250 1200
Population number 185 5681 230 210 1560
Vegetation Eleusine indica; Eragrostis cilianensis; Digitaria sanguinalis and Setaria viridis Cogongrass (Imperata cylindrica); Reed; Locust false-indigo (Amopha fruticosa); Robinia pseudoacacia Reed; Locust false-indigo (Amopha fruticosa); Locust (Robinia pseudoacacia) L. japonicum Thunb; E. debile Roxb; E. ramosissimum Desf; L. japonicum Thunb. Sw.; D. dichotoma (Thunb) Bernh Populus nigra var. italica; Phragmites communis; Salix matsudana; Phragmites communis; Miscanthus floridulus; Cynodon dactylon, etc.

Note: BMP: Beijing Milu Park, Beijing; DFNNR: Jiangsu Dafeng Milu National Nature Reserve, Jiangsu Province; YCWNNR: Jiangsu Yancheng Wetland National Nature Reserve, Rare Birds, Jiangsu Province; DTLNNR: East Dongting Lake National Nature Reserve, Hunan Province; SSNNR: Shishou Milu National Nature Reserve, Hubei Province.

Fig. 1 Population and distribution status of Milu in China
On 3 April, 2018, 30 Milu from BMP and 17 Milu from Poyang Lake National Wetland Park were released into the Poyang Lake area. In March 2019, a survey of the wild Milu at Poyang Lake revealed that their number had reached more than 50, and showed that they had spread from Poyang County to the wetlands in surrounding counties and cities.

4 Discussion

4.1 Achievements in population re-development

From prosperity to local extinction, and then reintroduction to successful recovery of the wild population, China’s Milu conservation work has been recognized worldwide. According to the “Guide to Species Introduction” published by the International Union for Conservation of Nature (IUCN) in 2012, China’s Milu reintroduction project is one of the 15 most successful species reintroduction projects worldwide among 138 projects which were assessed (Du, 2018).

4.1.1 Demonstrating a “Three-step model” for rebuilding the world’s endangered wildlife populations

After the reintroduction of Milu in China, the species went through the process of captive breeding, semi-free-range breeding, and rewilding training in nature reserves, before being gradually naturalized into the wild. From 1985 to 1993, the reintroduced Milu population in BMP was rejuvenated and expanded; from 1993 to 1998, rewilding training was carried out in SSNNR; and from 1998 to 2002, natural populations were formed in Yangbotan, Sanheyuan and East Dongting Lake. This successful experience can be summarized as the “Three-step model”. According to this model, BMP established an ex-situ Milu population in Poyang Lake Wetland Park in 2013. In April 2018, 47 Milu were successfully released into the wild, and by 2020, the number in the wild reached more than 60. At DFNNR, from 1986 to 1988 the population of Milu was rejuvenated and expanded; the domestication experiment was conducted from 1998 to 2003, and a wild population has been established since 2003. The successful experiences of BMP and DFNNR have proven that the “three-step model” (Fig. 2) of Milu wild population redevelopment is an effective method of ex-situ conservation.
Fig. 2 Sketch of “Three-step model” of Milu conservation

4.1.2 The population increased quickly, and the distribution expanded

At DFNNR, 39 Milu were introduced in 1986, and the number reached 5016 in 2019, a 129-fold increase. At SSNNR, 64 Milu were introduced in 1993 and 1994, and an additional 30 were introduced in 2002. At present, there are 1000 Milu in the semi-wild area and 800 outside the protected area, an overall 19-fold increase. In Jiangsu Yancheng Wetland National Nature Reserve, Rare Birds, 10 Milu were introduced in 1998, and by 2019, the number had reached 230, a 23-fold increase. If the base number of Milu established in 1985 and 1986 was 77, the current number of Milu in China has exceeded 9136 (Table 2), an increase of more than 100-fold.
Table 2 Population and living status of Milu in China
Code Site Population Living status
1 Beijing 1. Beijing Milu Park 186 Semi-free
2. Beijing Daxing Wildlife Zoo 20 Captive
3. Beijing Zoo 8 Captive
2 Jiangsu Province 4. Dafeng Milu Nature Reserve 3861 Free/captive
1820 Free
5. Yacheng Nature Reserve 230 Free
6. Qinhu Wetland Park 110 Captive
7. Suzhou Lyuguang Farm 75 Captive
8. Siyang Ecological Park 17 Captive
9. Taizhou Zoo 15 Captive
10. Suzhou Shangfangshan Forest Park 15 Captive
11. Wuxi Zoo 11 Captive
12. Yancheng Wildlife Zoo 9 Captive
13. Suqian Zoo 5 Captive
14. Yancheng Zoo 4 Captive
15. Yangzhou Zoo 4 Captive
16. Xuzhou Zoo 3 Captive
17. Changshu Shanghu Park 3 Captive
18. Nantong Wenfeng Zoo 1 Captive
19. Jiangshu Taizhouwang Wildlife Zoo 1 Captive
3 Hubei Province 20. Shishou Nature Reserve 1560 Free
21. Wuhan Zoo 18 Captive
25. Jinzhou Zoo 4 Captive
4 Hunan Province 22. Dongting Lake Nature Reserve 210 Free
23. Yueyang Rescue Center 15 Semi-free
24. Yangsha Lake Wetland Park 13 Semi-free
5 Jiangxi Province 26. Poyang Wetland Park 60 Free
27. Jingdezhen Zoo 5 Captive
28. Nanchang Zoo 3 Captive
6 Hebei Province 29. Luanhe Nature Reserve 29 Semi-free
30. Qinhuangdao Zoo 25 Captive
31. Baoding Zoo 14 Captive
32. Cangzhou Zoo 7 Captive
7 Tianjin 33. Tianjin Qilihai Wetland Park 22 Semi-free
34. Tianjin Zoo 22 Captive
35. Tianjin Fude Zoo 4 Captive
8 Zhejiang Province 36. Qingshanhu Wildlife Co, Ltd 125 Captive
37. Cixi Wetland Park 28 Semi-free
9 Liaoning Province 38. Liaoyang Qianshan deer center 122 Captive
39. Jinshan Deer Farm 27 Semi-free
40. Shenyang Zoo 21 Captive
41. Liaoyang Zoo 9 Captive
42. Dalian Zoo 5 Captive
10 Fujian Province 43. Yongtai Baiyun Park 43 Semi-free
44. Xiamen Wildlife Zoo 40 Captive
11 Shanghai 45. Shanghai Zoo 9 Captive
46. Chongming Xincun County 2 Semi-free
12 Shandong Province 47. Jinan Zoo 36 Captive
48. Rizhao Forest Park 31 Captive
49. Jinan Wildlife Zoo 21 Captive
50. Jining Zoo 13 Captive
51. Liugong Island Forest Park 7 Captive
52. Dezhou Zoo 4 Captive
53. Linyi Zoo 4 Captive
54. Qingdao Zoo 3 Captive
55. Xixiakou Wildlife Zoo 3 Captive
56. Jixi Zoo 3 Captive
57. Yantai Zoo 2 Captive
13 Hainan Province 58. Tropical Wildlife Park 32 Captive
59. Puyang Wildlife Zoo 6 Captive
60. Hainan Fengmu Deer Farm 1 Captive
14 Jilin Province 61. Changchun Zoo 20 Captive
62. Changchun Northeast Tiger Park 7 Captive
63. Jilin Jiangnan Park 2 Captive
15 Anhui Province 64. Yingshang Balihe Zoo 8 Captive
65. Hefei Wildlife Zoo 4 Captive
66. Bengbu Zoo 3 Captive
16 Yunnan Province 67. Kunming Zoo 4 Captive
68. Yunnan Wildlife Zoo 14 Captive
17 Sichuan Province 69. Chengdu Zoo 10 Captive
70. Yaan Bifengxia Wildlife Zoo 10 Captive
18 Heilongjiang Province 71. Qiqihaer Zoo 9 Captive
72. Jiamusi Shuiyuanshan Park 7 Captive
73. Haerbin Zoo 5 Captive
19 Guangdong Province 74. Dongguan Zoo 7 Captive
20 Henan Province 75. Zhengzhou Zoo 5 Captive
76. Xinxiang Zoo 2 Captive
77. Anyang Zoo 2 Captive
78. Luoyang Zoo 2 Captive
21 Guizhou Province 79. Guizhou Forest Wildlife Zoo 5 Captive
22 Shanxi Province 80. Taiyuan Zoo 2 Captive
23 Qinghai Province 81. Xining Zoo 2 Captive
24 Chongqing 82. Chongqing Zoo 2 Captive
Total 9136
The distribution sites of Milu have grown from the original two, namely BMP and DFNNR, to 82 by 2020, covering almost half of the original habitat of Milu before extinction. The wild population is distributed in six areas, with 1820 at the Yellow Sea tidal area, Dafeng, 220 at east Dongting Lake, Hunan, 500 in Shishou (including Yangpotan and Sanheyuan), Hubei, 60 at Poyang Lake, Jiangxi, 230 at Yancheng, Jiangsu, and 25 in the Mulan Enclosure, Hebei. By the end of 2020, the country’s wild Milu population totaled 2855 individuals (Bai, 2021).

4.1.3 Research outcomes of Milu are abundant, and the rearing standard and management technology of Milu are well-formed

Over the past 36 years, many achievements have been made in Milu research. Publications on the representative outcomes include China’s David’s Deer, Research on China’s Milu, Milu Research, Dafeng Milu and Biodiversity and Biological research of Milu (Bai, 2014), which systematically describe the origin and evolution of the Milu, its biological characteristics, behavioral mechanisms, population development, breeding management, etc. (Bai et al., 2021).
In terms of Milu breeding standards and management technology, BMP compiled the standard on Milu artificial breeding and release guidelines, which stipulates the standards for sites and enclosures for Milu artificial breeding and release.

4.1.4 Milu conservation promotes the public awareness of biodiversity conservation

BMP took the lead in raising the public awareness of Milu and biodiversity conservation. More than 500000 people visit Milu Park every year, while DFNNR receives more than 200000 tourists annually. At the same time, the relevant knowledge of Milu and biodiversity conservation is being incorporated into the school curriculum. Milu-related events have been broadcast by radio, television, newspapers and other media, and have been well received by the general public.

4.2 Challenges

4.2.1 Lack of a unified national plan for Milu monitoring and conservation

Although great achievements have been made in Milu conservation, the 100-fold increase in the Milu population over the past 36 years has posed new challenges. Nowadays, for the captive populations, BMP, DFNNR and SSNNR have their own respective master plans, monitoring methods and management regulations and standards, but do not coordinate with one another, and their data are not shared. For the wild population of Milu, management depends mainly on local forestry departments of all levels, and the standards and methods employed vary.

4.2.2 Low genetic diversity and potential risk of diseases

First, Milu suffers from a serious, sometimes disastrous, inbreeding problem, having experienced some periods of genetic bottlenecks (Beck and Wemmer, 1983). All existing Milu are descendants of 11 out of the 18 individuals that were kept at Woburn Abbey in England during the period of 1894-1904 (Bedford, 1951, 1952; Beck and Wemmer, 1983). Furthermore, all individuals living in China are the descendants of 77 individuals from two founder populations in BMP and DFNNR during the period of 1985-1987. All individuals in SSNNR are the offspring of 94 individuals from BMP, introduced in 1993, 1994 and 2002; and all individuals in YCWNNR are the descendants of 10 individuals from BMP, introduced in 1998. Studies have revealed that their low level of genetic variation (Zeng et al., 2013) puts Milu at risk of increased susceptibility to infectious pathogens. Second, there is a potential risk of diseases. Due to their weak ability to resist diseases, every few years malignant catarrhal fever breaks out in the populations in Europe or New Zealand (Reid, 1992; Orr et al., 2011). In China, hemorrhagic enteritis has caused a large number of Milu deaths (Zhong et al., 2013). For example, an epidemic of hemorrhagic enteritis in December 1999 caused the deaths of 28 individuals in seven days, with a death rate among infected animals of 18.4% (Zhong et al., 2013). A similar epidemic of hemorrhagic enteritis took place from April to May 2010 in SSNNR, causing the deaths of 316 individuals in one month, including all of the pregnant females. In May 2015, an epidemic of hemorrhagic enteritis caused the deaths of 15 out of 20 individuals in Luanhe Shangyou National Nature Reserve. Other phenomena such as offspring abandonment, abortion and dystocia also impact the population health of Milu every year.

4.2.3 More captive populations, fewer wild groups and less gene flow

In the present study, the captive populations were located at 69 sites, representing 84.1% of all sites, with only four pure wild populations at DFNNR, SSNNR, YCWNNR, and DTLNNR, and one released population in the wild at Poyang Lake Wetland National Nature Reserve, with the total number living in the wild being about 2855 (Bai, 2021). Among the captive populations, there were fewer than 10 individuals at 48 sites, and 5 sites have only 1 individual. Thus, the 48 small herds face the problems of effective population size and genetic health, since these herds are isolated with no gene exchange (Jiang and Harris, 2016). For example, Hainan Fengmu Deer Farm, into which 8 Milu were reintroduced from BMP in 1991, has seen its population decline from a peak of 19 in 2001 (Yang et al., 2003) to just 1 female due to a lack of gene exchange. The 3 subgroups of Milu at Sanheyuan, Yangbotan and HDLNR are isolated by landscape fragmentation and no longer have genetic exchange. Similarly, there can be no genetic exchange of the Milu between DFNNR and JYNR, due to the Dafeng Port. Moreover, it is unclear how much natural habitat remains on which Milu can exist in a free-ranging state (Jiang and Harris, 2016).

4.2.4 Human interference and conflict with humans

Human disturbance may be one of the most important factors in reintroduction projects (Xia et al., 2014). For example, humans were the direct cause of death in over 50% of all fatalities in the reintroduction of carnivores (Jule et al., 2008) and human-caused mortality could be the main factor limiting the increase in newly established and recovering wolf populations (Wabakken et al., 2001; Cheng et al., 2021). Despite being rare, human activities (e.g., entanglement in abandoned fishing nets, hit by cars) have led to the deaths of some Milu in the wild at DFNNR and Poyang Lake wetland. Moreover, the release project in Luanhe Shangyou National Nature Reserve failed due to the conflict between Milu and human beings; the wetlands in Sanheyuan and Yangbotan were not protected in a reserve and part of the habitat has been changed in recent years to fish ponds, croplands and stands of Populus euramericana. Furthermore, species reintroductions can increase conflict between people and wildlife, creating a problem for wildlife conservation (O’Rourke, 2014). Although Milu is under Class І protection in China, when the flood season comes, most parts of the habitat at Poyang Lake wetland and Dongting Lake are covered by floodwater, and the Milu in these areas are forced to move to farmland. At these times, conflicts in Sanheyuan, Yangbotan, and SSNNR frequently occur (Maddison et al., 2012). With the dispersal of Milu in DFNNR, the conflicts between Milu and local farmers have gradually increased and the local government in Dafeng City has built fences around farms to keep the Milu away from crops. These results resemble those found by Kidjo et al. (2007), who discovered that the reintroduction of Corsican red deer Cervus elaphus corsicanus caused damage to meadows and crops.

5 Conclusions

The Chinese Milu has experienced a process of extinction in the wild, introduction of captive populations to foreign countries, reintroduction from foreign countries to China, revitalization and expansion of the native population, ex-situ conservation, release into the wild and gradual reestablishment of the wild population. The recovery of China’s Milu population is a microcosm of China’s biodiversity conservation campaign, demonstrating China’s wisdom in biodiversity conservation and providing a useful case study for the international community in wildlife conservation.
However, as the Milu population expands, there are challenges ahead, including the lack of a unified national plan for Milu monitoring and conservation, and low genetic diversity, which make the population susceptible to disease with no quick solution in sight. A great majority of the Milu population is in captivity, with a limited ratio of free-range and semi-free-range animals. As the population grows, conflicts with human beings are emerging as a major problem. Effective international cooperation is also lacking.
Therefore, it is necessary to develop a top-level master plan, laying out unified monitoring standards and methods, and to set up a shared database for research and publicity purposes. National and international cooperation should be strengthened. The Milu was fist extinct in China, then reintroduced from England; and cooperation should be reestablished for the purpose of improving gene exchange among the existing Milu populations.

We appreciate the support of project “Population expansion and ex-situ conservation of Père David’s Deer and Equus ferus”, National Forestry and Grassland Administration (2020).

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