Next Article in Journal
Effects of Strategic Supplementation with Lupinus angustifolius and Avena sativa Grains on Colostrum Quality and Passive Immunological Transfer to Newborn Lambs
Next Article in Special Issue
Laissez-Faire Stallions? Males’ Fecal Cortisol Metabolite Concentrations Do Not Vary with Increased Female Turnover in Feral Horses (Equus caballus)
Previous Article in Journal
Identification and Antimicrobial Resistance in Klebsiella spp. Isolates from Turkeys in Poland between 2019 and 2022
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 12
Issue 22
10.3390/ani12223158
animals-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

An Update on Status and Conservation of the Przewalski’s Horse (Equus ferus przewalskii): Captive Breeding and Reintroduction Projects

by
Mardan Aghabey Turghan
1,2,*,
Zhigang Jiang
2,3,* and
Zhongze Niu
4
1
State Key Laboratory of Oasis and Desert Ecology, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, China
2
Graduate School, University of Chinese Academy of Sciences, Beijing 100049, China
3
Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
4
College of Biology and Geography Sciences, Yili Normal University, Yining 835000, China
*
Authors to whom correspondence should be addressed.
Animals 2022, 12(22), 3158; https://doi.org/10.3390/ani12223158
Submission received: 17 October 2022 / Revised: 6 November 2022 / Accepted: 10 November 2022 / Published: 15 November 2022
(This article belongs to the Special Issue Wild and Feral Equids—Biology, Conservation and Management)
Review Reports Versions Notes

Abstract

:

Simple Summary

The Przewalski’s horse (Equus ferus przewalskii), the only extant species of wild horse, was extinct in the wild in 1960s. The wild horse has been successfully saved from extinction by captive breeding projects outside the historic range. Although multiple studies were conducted, the main problems such as loss of founder genes, inbreeding depression, hybridization with domestic horses, high morbidity and mortality, and a lack of reliable prevention strategies and treatment limitations of these problems are still unresolved and require further scientific effort. This review aims to increase understanding of the scientific attributes that make the survival of the species possible and how these attributes can be useful for appropriate design of conservation and management strategies oriented to improve the viability of the existing population of the species.

Abstract

This review summarizes studies on Przewalski’s horse since its extinction in the wild in the 1960s, with a focus on the reintroduction projects in Mongolia and China, with current population status. Historical and present distribution, population trends, ecology and habitats, genetics, behaviors, conservation measures, actual and potential threats are also reviewed. Captive breeding and reintroduction projects have already been implemented, but many others are still under considerations. The review may help to understand the complexity of problem and show the directions for effective practice in the future.

1. Introduction

Przewalski’s horse (Equus ferus przewalskii), also known as Przewalski’s wild horse, the Asian wild horse, Mongolian wild horse, Takhi or Junggar Horses, is classified by the IUCN as Extinct in the Wild (EW) as no Przewalski’s horse has been seen in the wild since 1969, despite efforts to find them in Mongolia or China [1,2,3,4,5,6,7]. Among the seven extant equid species, the Przewalski’s horse is the only true wild horse in the world [4,8,9,10,11,12,13]. As a species the Przewalski’s horse has been successfully saved from extinction by breeding in captivity [14,15,16,17,18,19] based on a carefully managed founder population [20,21,22]. All Przewalski’s horses alive today are descendants of only 12 wild-caught horses and possibly up to four domesticated individuals [6,7,21,22,23,24,25]. These founders reproduced successfully through captive and reintroduction programs worldwide, and as of 2014 there was an estimated free-ranging population of over 1988 Przewalski’s horses [26,27]. At present, 2500 Przewalski’s horses live in about 112 breeding centers and zoos around the world [6,28]. Reintroduction projects of the species started in 1985 and 1992 in China and Mongolia respectively with a goal to return the horses to their former habitat from captive breeding stock [4,6,25,29,30,31].
Despite extensive studies on captive breeding and reintroduction over the half past century, the long term conservation of the Przewalski’s horses still poses many problems [6,7]. This paper presents an overview of the history and current status of Przewalski’s horses. The main problems which need to be overcome in establishing a wild population are identifying a suitable area and selecting appropriate sources of animals for re-wilding as well as effective conservation management strategies. The consequences of interspecific interaction with other species of equids and ungulates in the release area, including hybridization with domestic horses need to be taken into account.

2. Historic Distribution and Extinction

The 55-million-year history of equine phylogeny has been well-documented from the fossil record. The first visual account of Przewalski’s wild horse-type dates back more than 20,000 years ago [32,33]. Guthrie [34] describes the Przewalski’s wild horse as belonging to the four top grazing herbivores of the Pleistocene Mammoth Steppe, along with the steppe bison (Bison priscus), the wooly rhino (Coelodonta antiquitatis), and the mammoth (Mammuthus primigenius). The Przewalski’s horses were regarded to be a typical representative of the Eurasian steppe fauna [9,10,35,36], although its distribution in prehistoric times was difficult to trace [10].
The Eurasian steppe, with higher solar radiation and richer soil fertility, was considered to be the ideal habitat of equids [34,37,38]. Consequently, the Przewalski’s horses were widely distributed over central Asia and Western Europe in prehistoric times [39]. However, in recorded history, it has only been found in the Gobi Desert of Xinjiang, China and Mongolia (85–95° E, 44–50° N), where all Przewalski’s horses were captured around the turn of the 19th and 20th centuries [6,33,40]. The last wild horse was also seen in Mongolia in 1969 [10].
There was no description of Przewalski’s horses in Linnaeus’s classic studies [41]. The horses remained unknown in the scientific world until John Bell, a Scottish doctor, sighted the horse in his trip to Peking in 1719–1722 [33]. Colonel Nikolai Przewalski, a Russian explorer collected specimens of a wild horse during his expedition in Xinjiang China in 1880 [42]. Poliakov scientifically documented this species as wild horses for the first time, and he named the specimen Equus przewalskii. Later the wild horse was taken as a subspecies of Equus ferus [3,43,44,45].
The numbers of Przewalski’s horses in the wild appeared to decline dramatically after World War II. The last wild horse was seen in the Dzungarian Gobi in 1969 [4,10,44]. It is likely that Przewalski’s horses were already quite rare in the wild in the first half of the 20th Century, with only occasional sightings of small groups of horses being reported [10]. Investigations have consistently failed to find the wild populations of the species [4,40,45,46]. The horse was extinct in its original range, and was categorized as Extinct in the Wild by the IUCN [6,7,10,47].
Almost all endangered species are threatened because their ecological needs are affected negatively by human interference [18]. However, insight into the extinction of the Przewalski’s horses may also be better understood by studying a variety of information on the historic distribution, taxonomy and ethology of the horse and its relatives [19,48]. Factors such as competition with livestock, hunting, capture of foals for zoological collections, climate change, inbreeding and hybridization, predation and infanticide, restricted access to natural water source have been cited for the extinction of Przewalski’s horses in the wild [4,6,9,10,19,37,49,50,51,52,53,54,55]. Another reason might be a series of harsh winters, for example, recorded in 1945, 1948 and 1956 [10,19].

3. Captive Breeding and Population Trends

Conservation of endangered species in captive breeding (in zoos and other protected areas) so far has saved several species from extinction [56]. The Przewalski’s horse is an example [10,15,19]. Since the discovery of the Przewalski’s horses, there has been interest in the collection of the species, especially in Western Europe [14,15,16]. At first, six Przewalski’s horses were captured in 1899–1890 and transported to Europe [6,57,58]. It is obvious that an increasing demand for captive breeding of the western world was one of the important factors which caused the extinction of the Przewalski’s horse in the wild [6,10,19]. Thirty-four foals had been transported alive to the west before 1930s. Since then, the numbers of horses captured in the wild reduced drastically [19].
After the Second World War the captive Przewalski’s horse population went through another bottleneck, and there remained only 31 horses in western zoos and wild animal parks, of which only nine were capable to breed [4,49], which apparently descended from the wild stock, but had a slight contribution from domestic horses [4,59]. Horses were exchanged between zoos in order to reduce the level of inbreeding since the 1970s [6,10]. More than 1500 Przewalski’s horses in captivity had been recorded in the studbook by the 1990s [4,19,60], and the number reached 5000 in 2012 [61]. At present, the worldwide population of the living Przewalski’s horses has reached nearly 2500 individuals [28]. Among them, approximately 1360 horses live in the wild in China and Mongolia, 900 were distributed in zoos in Europe, and 120 in wildlife parks in the US [6,28,61].

4. Reintroduction Projects of the Przewalski’s Horse

Reintroduction projects in China and Mongolia were proved to be successful in the restoration of the Przewalski horses which disappeared from their former habitats [18]. Semi-reserves were created by the European Conservation Project for preparation for returning wild horse to their original habitat [4,6,29,30,50,62,63,64,65,66]. The Hustai National Park in Mongolia has established which is large enough to maintain groups of Przewalski horses throughout all seasons of the year without any supplemental provisioning. As far as possible, those wild horses are kept totally isolated from external influences, except for necessary interventions such as veterinary care [6,66]. All the reintroduction projects begin with an adaption period in semi-reserves [67]. As early as the 1980s, Przewalski’s horses have been released into large enclosed (semi) reserves in Canada, The Netherlands, Germany, France, Holland, England, Hungary, Ukraine, Uzbekistan and China as a pre-adaption phase before their release to the wild [10,18,68]. By 1990, at least four projects in China and Mongolia have reached the stage of adaptation at the release site [4,10,19]. However, there was a poor coordination of these different reintroduction projects [6].

4.1. Reintroduction Projects in Mongolia

Reintroduction project of the Przewalski’s horses into Mongolia was initiated by an expert consolation in 1986 [4,6,19]. Two sites were selected for the reintroduction of Przewalski’s horses to the wild in their former range in Mongolia: Takhin Tal (45.3219° N, 93.3905° E), in the Gobi Strictly Protected Area, an International Biosphere Reserve in the south western part of Mongolia where Przewalski’s horses were last seen in the wild; and Hustain Nuruu National Park, a smaller protected area north of the centre of Mongolia, about 130 km west of Ulaan Baatar [4,19]. The two projects were initiated and supported by different organizations: the former was initiated by the Ministry of Nature and Environment of Mongolia and supported by the Christian Oswald Foundation, Germany and the Mongolian government, subsequently being run by the International Takhi Group with the support of various international sponsors. In 1999 the International Takhi Group (ITG) was established to continue and extend this project in accordance with the IUCN reintroduction guidelines [69,70,71]. The latter was mainly initiated and supported by the Dutch Ministry of Development Aid [4,6,62,72,73,74].
The reintroduction site of Przewalski’s horses in Takhin Tal is a typical semi desert area located in the western part of the Gobi National Park [4,6,19,70]. Five adult Przewalski’s horses including two males and three females were transported from Ukraine in 1992, and released to the wild after a period of adaptation in enclosures, from which the first foal was born in 1992. Another transportation of eight individuals from Ukraine was taken place in 1993 [6]. Sixty horses in ten groups were transported, and 25 foals had been born by the new millennium, of which 14 survived [4,6,29]. In June 2000, seven foals had been born in the free-ranging harem group [70,71,73].
The reintroduction of Przewalski’s horse in Hustain Nuruu is set within the context of the broader goals of the restoration and protection of biodiversity within the reserve [4,16,73,74,75]. In June 1992, first group of 16 captive born Przewalski’s horses were transported to the Hustai National Park, where they were held in adaptation enclosures in view of a possible future reintroduction [74]. A second group of 16 Przewalski’s horses was sent in July 1994 to the same site [4,6,76]. In total, 89 Przewalski’s horses were transported to the park in the next eight years [69,70,71,72,77,78]. In 1997 the first harem group was released from the adaptation enclosures, and in 1999 the first foals were successfully raised in the wild [76,77]. The total number of the wild horses in the Hustai National Park reached 122 individuals belonging to nine groups by the new millennium, and became an important vehicle for national park development [71,78].
In 2004, 12 captive-born and carefully-selected horses were brought to Khomii Tal, buffer zone of Khar Us Nuur National Park, where they are being held in adaptation enclosures for possible future reintroduction. A second group of horses was shipped in the following year [6,62].
The return of the Przewalski’s horses to their native steppes of Mongolia is proven to be successful as the species population has grown steadily in these semi-reserves [17,71,79]. The IUCN Red List of Threatened Species Working Group downgraded the Przewalski’s horse to the status of Endangered in 2011, mainly based on the status of wild horses in Mongolia, for free ranging Przewalski’s horses roaming these sites has reached approximately 350 [29,30]. Today, the number of Przewalski’s horses in the wild in Mongolia has already exceeded 900 [28,80].

4.2. Reintroduction Projects in China

The current populations of the Przewalski’s horses in China are distributed in three different localities. Among them, the population bred in the wild horse breeding center in Xinjiang Provence is the largest. The other two are the Wuwei–Dunhuang population in Gansu Provence and Beijing–Anxi population in Beijing City respectively [6,7,30,81,82].

4.2.1. The Xinjiang Population

The reintroduction projects in China has been carried out since 1985, immediately after a conservation action plan for the restoring re-wild population of the Przewalski’s horses was proposed by the Chinese government [4,6,7,30,50]. From 1985 to 2005, 14 males and 10 females captive Przewalski’s horses in five groups from captive facilities in Germany, the United Kingdom, and the United States were transferred to the wild horse breeding center which was established in the semi-desert region of the Junggar Basin in Xinjaing. [6,20,30]. In 2006, a group of six Przewalski’s horses was brought to the center with the aim of improving genetic diversity of the captive individuals [6]. The first foal was born in 1988. Between 1988 and 2013, 339 foals were born and 285 survived at the Centre [50]. In the following year, 11 males and 16 females Przewalski’s horses were released to the wild as a beginning of the restoration program of the species within its former ranges in China [6,30]. Thirteen more groups of Przewalski’s horses have been released since 2013 [6].
In total 89 captive-born Przewalski’s horses (32 males and 57 females) were transported to the Mt. Kalamaili Wild Ungulate Nature Reserve between August 2001 and December 2013 [6]. The first foal was born in 2003 in Mt. Kalamaili Wild Ungulate Nature Reserve by the group released in 2001, and by 2013, a total of 107 foals had been born, of which 88 survived their first year. In 2013, the total population of the released Przewalski’s horses reached 127 individuals divided into 16 groups (13 breeding and 3 bachelor groups) [6,29,50,83]. A preliminary success of restoring the wild population of the Przewalski’s horses has been achieved [30,50,82,83]. The numbers of captive and free-ranging populations in Xinjiang has reached 413 by the end of 2018, but the Przewalski’s horse in China is still listed as Extinct in the Wild because their wild populations still depend on supplemental feeding for their winter survival [6,30,82].

4.2.2. The Wuwei–Dunhuang Population

The distribution sites of the Wuwei–Dunhuang population includes the Wuwei Endangered Animal Breeding Centre and the Dunhuang West Lake Nature Reserve [6]. Since 1990, 18 Przewalski’s horses were brought to the Wuwei Endangered Animal Breeding Centre from the US and Germany as a part of the reintroduction project initiated by the former Ministry of Forestry of the Peoples Republic of China [6,81]. Two releases of wild horses were carried out on 25 September 2010 and 06 September 2012 respectively. Seven and 21 wild horses bred in captivity at the center were kept in enclosures of the west lake national nature reserve to allow them to adapt to the local environment, then they were released. Sixteen foals were born by the re-wildering horses [6]. By the end of 2018, the Wuwei–Dunhuang population increased to 60 as 41 foals were produced. However, the horses were driven into the paddocks to allow for supplemental feeding to increase winter survival, and to reduce competition with domestic horses of local herdsmen [6,81].

4.2.3. The Beijing-Anxi Population

The distribution sites of the Beijing–Anxi population includes the David’s Deer Park in Beijing City and the extreme-arid desert national nature reserve in Anxi County, Gansu Provence [4,6]. Ten Przewalski’s horses brought to the reserve from the United Kingdom in 1985 were kept in the David’s Deer Park for a better acclimatization. In 1997, seven males and three females were translocated to the reserve, which is one of their original areas [6], the David’s Deer Park retained two Przewalski’s horses in the park. By 2018, the number of wild horses in the park increased to five [6], but decreased to one in 2021.
In 1999, the first foal was born in the translocated population in the reserve, and the 2nd, 3rd and 4th generations were born in 2004, 2008 and 2012 respectively. All the individuals introduced in 1997 bred and died before 2012. The number current population of the Beijing–Anxi Przewalski’s horses has reached 23, which still depend on supplemental feeding as the other reintroduced populations do [6].

5. Research Activities on the Reintroduced Przewalski’s Horse

The Przewalski’s horse was never studied in the wild before its extinction, so only anecdotal accounts of its habitat, genetics, social structure and behaviour before its extinction were available [33]. Nevertheless, all knowledge available on the development of their ethology and ecology in the reintroduction projects is critically important for the understanding of their ecological requirements, as the goal of the research activities on the reintroduced Przewalski’s Horse is to establish a basic reference dataset as well as to provide the scientists with reliable methods for the long-term monitoring of the reintroduction projects worldwide.

5.1. Habitat Controversy

The Przewalski’s horse is a typical grazer within the sub-optimal ranges in arid landscape in central Asia [6,84], as the more favourable steppe region was colonized by nomadic pastoralists over several millennia [19]. The ever-growing human and livestock pressure on the diminishing steppe range forced the Przewalski’s horse to suboptimal ranges, as the last Przewalski’s horse range was located within arid area in the vicinity of water holes, which is not not necessarily its optimal habitat [4,9,19,85]. Of all the wild horse species, the Przewalski’s horse was the one with the most eastern distribution and was most likely well adapted to the arid steppe of the Dzungarian Gobi [64]. However, it is still debated whether these areas represent a mere refuge or were the typical Przewalski’s horse habitat for the living conditions in the Gobi regions are much harsher than in the mountain steppe zone of Hustain Nuuru, where water and forage is more plentiful [4,18,19,49,79,82]. In addition, the adaptation enclosures in the Gobi do not provide enough forage; the wild horses need supplementary feeding year-round [11]. Consequently, the most critical step in the release process is seen in the actual release from the adaptation enclosure [86]. The arid Gobi, in which the Przewalski’s horse can survive as a steppe herbivore, is probably a marginal habitat rather than part of their optimal habitat, and rarity of waterholes in their last refuge should has been considered as a significant factor contributing to their extinction [4,18,19,87,88].
The steppe was also considered as optimal habitat of Przewalski’s horse by biological arguments that feral and free ranging horses thrive best on steppe-like grasslands [68,89,90], implying that availability of critical resources may affect the habitat use of the horses [91]. Several studies also suggested that feral horses, including Przewalski’s horses, preferred proximity to rivers, forest and simple plant communities with the preferred species, flatter and lowland areas where they could more easily notice the movement of predators [62,91,92,93]. They use the shade of trees for temperature regulation during summer [94,95], and they climb to windy hillsides located close to such forests to avoid attack from flies [96], as reported previously in feral horses [62,91,92,94,97]. In summary, the view that the Przewalski’s horses are primarily a steppe herbivore has received growing support in the captive breeding as well as reintroduction projects [6,9,11,19,85,86,87,88]. Captive breeding and reintroduction efforts reviewed by Black et al. [88] also indicated that Przewalski’s horses survive and reproduce more successfully when they are dispersed to optimal habitats such grassy semi-desert than they stay at the reintroduction sites which were parts of the arid Gobi.

5.2. Genetic Diversity

Understanding the genetic relationship between domestic and Przewalski’s horses is critical for formulating conservation and breeding strategies for the species [12,98,99,100,101]. The Przewalski’s horse was recently identified as a descendant of wild horses domesticated in today’s Kazakhstan [98], and significantly different from other horses in morphological traits [1,100,101,102,103]. Genotypical differences also strongly identify the Przewalski’s horse as being more different from other equids [15,104,105,106,107,108,109]. Although genetic studies have yet to identify when and where horse domestication first took place, a recent archaeozoological report indicated the presence of domesticated horses 5500 years ago in Kazakhstan [102,110,111,112]. It is clear from genetic studies that Przewalski’s and domestic horses are also distinct in chromosomal number [101,113,114], but interbreeding between Przewalski’s horses and domestic horses produces fertile offspring [109,110,115,116]. Interspecies embryo transfer has also been successful [23,49,51,117,118].
Przewalski’s horse is the first species to return to its native habitat after living in captivity in small and isolated groups in zoos and parks for generations [4,6,19]. Because of the long and unnatural selection in captivity, it is necessary to map an accurate genetic diversity of Przewalski’s horses to ensure their successful reintroduction to the wild [10,12]. Early studies on the genetics of the species have mainly focused on phylogenetic relationship using a variety of markers, including protein polymorphisms [23,119], chromosomal variation [99,105,108,115,120,121], blood group and allozyme loci [23]. With the widespread use of molecular tools such as mtDNA, immune genes, microsatellite genotyping and genome-wide markers in endangered species [114,118,122,123,124,125,126], more attention has been paid on the evaluation of the level of inbreeding in the Przewalski’s horses, which is critically important for the implementation of long term conservation strategies [12,13,81,101,127,128,129,130].
Przewalski’s horses went through large bottlenecks even in pre-historic times [13]. Genetic diversity of the founder population of the Przewalski’s horses was lost significantly due to the genetic drift and bottlenecks of the horse population bred in captivity [4,131]. Only 12 horses have contributed to the gene pool of living wild horse [132], explaining the inbreeding depression in the captive population which results in high mortality, abnormalities in reproduction, and shorter lifespans [15,52,53,54,81,126,128,129,130,133,134,135]. One of the effective ways to minimize inbreeding is to select most distantly related horses to produce offspring [4,15,136], but such a practice has long been debated [137]. Empirical and simulated data [81] showed that the loss of genetic diversity decreases with increasing size of the founder population [81,138,139,140], and this is consistent with the considerable reduction in inbreeding in the reintroduced population in Mt. Kalamaili Wild Ungulate Nature Reserve China since 2001, when the number of the released horses exceeded 100 individuals [81]. The above result is also in consistent with the study of Taylor and Jamieson [141] that differentiation inevitably will occur by genetic drift in small population [142].
Another problem is the adaptation to captive environments which impedes the successful implementation of reintroduction [139]. Reducing the number of generations a species spends is considered to be the best approach to minimize genetic adaptation in captivity [143]. Ecological and ethological adaptation mainly happens in the early 5–10 generations, which the Chinese and Mongolian populations have already surpassed [144,145]. It was also suggested that genetic adaptation in captivity poses no threat to the survival of the Przewalski’s horses as they have already spent 16 generations in captivity globally [81].

5.3. Social Structure and Ethology

Social structure in Przewalski’s horses resembles feral horses (Equus ferus caballus) in many aspects [4,62,68]. They are both highly socialized within a harem with strong social bounds [146,147,148,149]. There are two types of social groups in Przewalski’s horses: harem groups, including a stallion, mares, and foals, are the breeding units of horses; bachelor groups are the combination of young males [150]. In a harem group, the stallion takes the responsibility of defending females from stallions of other harem groups [151]. Home ranges of harems are commonly separated, but slightly overlapping in some cases [28,30,151,152]. The same phenomenon has also been observed in 2001 in the Pentezug Reserve in Eastern Hungary at the beginning of the reintroduction project with 22 Przewalski’s horses. It is proven that harem groups do not overlap when the home ranges are relatively small [28]. However, overlapping rate became relatively high in 2014 (almost 70%) as the horse population and the number of harem groups continuously grew over the years in the area [28], and this is consistent with the reintroduced horses in China and Mongolia [28,30,151]. Similar social structures and demographic changed were found in domestic horses [68,90] and plain zebras in Africa [152,153].
Almost all information on the ecology and ethology of the Przewalski’s horses is from zoos, wild parks and semi-reserves [79], which is important for the understanding of their ecological requirements and ethology. Most scientists assume that the ecology and ethology of the Przewalski’s horses in the wild do not differ greatly from that of feral horses while some predict a more aggressive role of the stallions, based on observations in semi-reserves and zoos [154,155,156]. In captivity, male Przewalski’s horses are more active than females [7] in which solitary males and bachelors move more per hour than harem males [24]. Males devote more time to harem acquisition and defense in the wild, which would maximize male reproductive success while females devote more energy to foraging which influences their reproductive success [24,90,157,158,159]. These gender differences are in consistent with the speculations that, in equids, as in other polygynous mammals, males commonly invest more time and resources in intrasexual competition for access to mates than do females [92] while females typically provide the most parental investment in offspring [160].
The type of enclosure also has significant effects on the time budgets of Przewalski’s horse. Horses in small enclosures spend less time stand-resting and change behavior states frequently than horses in larger enclosures [24]. Enclosures with lower density of horses approximate the natural conditions [161], and it is evident that density or space can regulate the conditions of the captive populations of the Przewalski’s horses [162,163].
Stress resulting from poor captivity conditions is also known to affect growth, reproduction and resistance to disease in caged animals [143,164] while optimum captivity conditions will result in more natural behavior and greater reproductive success [157]. It was advised that enclosures allow the normal feeding patterns to maintain a healthy herd and to minimize aggressive interactions [154]. Some individual horses may have problems due to lack of experience, lack of acclimatisation or unsuitable physiological or morphological characteristics, and stress associated with increased aggression may have even predisposed colts to disease [79]. In such a case, individuals that are found unable to cope with natural conditions should be identified and excluded in order to protect horses from unnecessary suffering [56].

6. Conclusions

Przewalski’s horse was extinct in the wild in 1960s, and has been successfully saved from extinction by captive breeding [20,21,22]. Breeding centers for the Przewalski’s horse have been established, and nature reserves have been founded in China and Mongolia [6,30]. With a considerable increase in the number of living horses roaming in the wild, the IUCN Red List of Threatened Species downgraded the Przewalski’s horse to “Endangered” from “Critically Endangered” in 2011 [6,29,30].
Although the Przewalski’s horses have successfully been saved from extinction, they still face actual and potential threats such as habitat deterioration, loss of founder genes, inbreeding, predation by wolves, parasitic diseases, crossbreeding with domestic horses, and so on. We suggest that the real conservation issue for the horses at present, especially in China, is related to intensifying human-wildlife conflicts resulting in increasing human presence and movements in key wildlife habitats along with increasing livestock numbers. We recommend that threats such as over-grazing, road construction and mining activities should be closely monitored to avoid further degradation of the horse’s original habitats.
The long-term threat to the retention of heritable variation in the Przewalski’s horses is loss of founder genes [4]. Further losses of founder genes must be minimized through scientific management. Furthermore, Przewalski’s horses reintroduced into the wild are at risk of crossbreeding with domestic horses. Przewalski’s horses most be isolated during the breeding season [6,15].
Predation by wolves is one of the significant mortality causes in Przewalski’s horses. In the Anxi Nature Reserve, China, for example, 12 wild horses were preyed on by wolves, accounting for more than 30% of the total deaths [165]. Careful monitoring of Przewalski’s horse population dynamics, ecology and ethology in all current and future projects should be carried out to prevent wolf predation and male infanticide in Przewalski’s horses.
Finally, we stress that hybridisation with domestic horses and thus introgression of domestic genes into the reintroduced population is the critical problem to be addressed in the future, in order to secure free-ranging populations of Przewalski’s horses in the wild.

Author Contributions

Conceptualization: M.A.T.; writing—original draft preparation: M.A.T. and Z.J.; editing—language correction: Z.N. All authors have read and agreed to the published version of the manuscript.

Funding

Chinese Academy of Sciences (XDA19050204).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We would like to thank Chughluhk Mardan, a student from the Zhejiang University China, who participated in the language correction of the manuscript. We also thank Kawsar Aman for her attention during our research.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Groves, C.P. The taxonomy, distribution and adaptations of recent equids. In Equids in the Ancient World; Meadow, R.H., Uepermann, H.P., Eds.; Dr Ludwig Reichert Verlag: Wiesbaden, Germany, 1986; Volume 421, pp. 11–65. [Google Scholar]
  2. Groves, C. Morphology, Habitat and Taxonomy. In Przewalski’s Horse: The History and Biology of an Endangered Species; Boyd, L., Houpt, D.A., Eds.; State University of New York Press: Albany, NY, USA, 1994; pp. 39–60. [Google Scholar]
  3. Poliakov, I.S. Przewalski’s horse (Equus przewalskii n. sp.). Isvestia Rus. Geogr. Obs. -Va St Petersburg 1881, 17, 1–20. [Google Scholar]
  4. Wakefield, S.; Knowles, J.; Zimmermann, W.; Van Dierendonck, M.C. Status and action plan for the Przewalski’s horse (Equus ferus przewalskii). In Equids: Zebras, Asses and Horses; Moehlman, P., Ed.; IUCN/SSC Equid Specialist Group; IUCN Publications Services Unit: Cambridge, UK, 2002; pp. 82–92. [Google Scholar]
  5. Paige, W. The Remarkable Comeback of Przewalski’s Horse. In Smithsonian Magazine; Smithsonian Institution: Washington, DC, USA, 2016. [Google Scholar]
  6. Jiang, Z.G.; Zong, H. Rentroduction of the Przewalsk’s horse in China: Status Quo and Outlook. Nat. Conserv. Res. 2019, 4 (Suppl. S2), 15–22. [Google Scholar] [CrossRef]
  7. Lu, V.; Xu, F.; Turghan, M.A. Przewalski’s Horses (Equus ferus przewalskii) Responses to Unmanned Aerial Vehicles Flights under Semireserve Conditions: Conservation Implication. Int. J. Zool. 2021, 2021, 6687505. [Google Scholar] [CrossRef]
  8. Sokolov, V.E.; Orlov, V.N. The Przewalski horse and restoration to its natural habitat in Mongolia. In Animal Production and Health Division; FAO: Rome, Italy, 1986; pp. 77–88. ISBN 92-5-102441-3. [Google Scholar]
  9. Sokolov, V.E.; Amarsanaa, G.; Paklina, M.W.; Posdnjakowa, M.K.; Ratschkowskaja, E.I.; Chotoluu, N. Das Letzte Przewalskipferd areal und seine Geobotanische Characteristik. In International Symposium on the Preservation of the Przewalski Horse; Seifert, S., Ed.; Zoologischer Garten Leipzig: Leipzig, Germany, 1992; pp. 213–218. [Google Scholar]
  10. Bouman, D.T.; Bouman, J.G. The history of Przewalski’s Horse. In Przewalski’s Horse: The History and Biology of an Endangered Species; Boyd, L., Houpt, D.A., Eds.; State University of New York Press: Albany, NY, USA, 1994; pp. 5–38. [Google Scholar]
  11. Souris, A.C.; Kaczensky, P.; Julliard, R.; Walzer, C. Time budget, behavioral synchrony and body score development of a newly released przewalski’s horse group Equus ferus przewalskii, in the Great Gobi b Strictly Protected Area in SW Mongolia. Appl. Anim. Behav. Sci. 2007, 107, 307–321. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Goto, H.; Ryder, O.A.; Fisher, A.R.; Schultz, B.; Pond, S.L.K.; Nekrutenko, A.; Makova, K.D. A massively parallel sequencing approach uncovers ancient origins and high genetic variability of endangered Przewalski’s horses. Genome Biol. Evol. 2011, 3, 1096–1106. [Google Scholar] [CrossRef] [Green Version]
  13. Orlando, L.; Ginolhac, A.; Zhang, G.; Froese, D.; Albrechtsen, A.; Stiller, M.; Schubert, M.; Cappellini, E.; Petersen, B.; Moltke, I. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse. Nature 2013, 499, 74–78. [Google Scholar] [CrossRef] [PubMed]
  14. Bouman, J.; Bouman, I.; Groeneveld, A. (Eds.) Semi-reserves for Przewalski’s horse. In Breeding Przewalski Horses in Captivity for Release into the Wild; Foundation for the Preservation and Protection of the Przewalski Horse: Rotterdam, The Netherlands, 1982; pp. 221–240. [Google Scholar]
  15. Ryder, O.A. Genetic studies of Przewalski’s horses and their impact on conservation. In Przewalski’s Horse: The History and Biology of an Endangered Species; Boyd, L., Houpt, K.A., Eds.; The State University of New York Press: Albany, NY, USA, 1994; pp. 75–92. [Google Scholar]
  16. Volf, J. The studbook. In Przewalski’s Horse: The History and Biology of an Endangered Species; Boyd, L.E., Houpt, K.A., Eds.; State University of New York Press: Albany, NY, USA, 1994; p. 313. [Google Scholar]
  17. Wallis de Vries, M.F.; Manibazar, N.; Wgerlham, S. The vegetation of the forest steppe region of Hustain Nuruu, Mongolia. Vegetatio 1996, 122, 11l–127. [Google Scholar] [CrossRef]
  18. Van Dierendonck, M.C.; Wallis De Vries, H.; Schilder, M.B.H. An analysis of dominance, its behavioural parameters and possible determinants in a herd of Icelandic horses in captivity. Neth. J. Zool. 1995, 45, 362–385. [Google Scholar]
  19. Van Dierendonck, M.C.; Wallis de Vries, M.F. Ungulate reintroductions: Experiences with the Takhi or Pnewalski Horse (Equus ferus przewalskii) in Mongolia. Conserv. Biol. 1996, 10, 728–740. [Google Scholar] [CrossRef]
  20. Mohr, E. Das Urwildpferd. In Die Neue Brehm-Bucherei. Wittenberg (Lutherstadt): A. Ziemsen Verlag; WittenbergLutherstadt: Halle, Germany, 1959; p. 144. (In German) [Google Scholar]
  21. Mohr, E.; Volf, J. Das Urwildpferd. In Die Neue Brehm-Bücherei. A. Ziemsen Verlag; WittenbergLutherstadt: Halle, Germany, 1984; p. 128. (In German) [Google Scholar]
  22. Volf, J. Das Urwildpferd. In Die Neue Brehm-Bücherei; Westarp Wissenschaften: Magdeburg, Germany, 1996; Volume 249, p. 147. (In German) [Google Scholar]
  23. Bowling, A.T.; Ryder, O.A. Genetic studies of blood markers in Przewalski’s horses. J. Hered. 1987, 78, 75–80. [Google Scholar] [CrossRef] [PubMed]
  24. Boyd, L.E.; Carbonaro, D.A.; Houpt, K.A. The 24-hour time budget of Przewalski horses. Appl. Anim. Behav. Sci. 1988, 21, 5–17. [Google Scholar] [CrossRef]
  25. Der Sarkissian, C.; Ermini, L.; Schubert, M.; Yang, M.A.; Librado, P.; Fumagalli, M.; Jónsson, H.; Bar-Gal, G.K.; Albrechtsen, A.; Vieira, F.G.; et al. Evolutionary genomics and conservation of the endangered Przewalski’s horse. Curr. Biol. 2015, 25, 2577–2583. [Google Scholar] [CrossRef] [PubMed]
  26. King, S.R.B.; Boyd, L.; Zimmermann, W.; Kendall, B.E. Equus ferus ssp. przewalskii. In The IUCN Red List of Threatened Species; IUCN: Gland, Switzerland, 2015. [Google Scholar]
  27. Li, Y.; Zhang, K.; Liu, Y.; Li, K.; Wronski, T. Community composition and diversity of intestinal microbiota in captive and reintroduced przewalski’s horse (Equus ferus przewalskii). Front. Microbiol. 2019, 10, 1821. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Kerekes, V.; Sándor, I.; Nagy, D.; Ozogány, K.; Barta, Z. Trends in demography, genetics, and social structure of Przewalski’s horses in the Hortobagy National Park, Hungary over the last 22 years. Glob. Ecol. Conserv. 2021, 25 (Suppl. S2), e01407. [Google Scholar] [CrossRef]
  29. Walzer, C.; Kaczensky, P.; Zimmermann, W.; Staufer, C. Przewalski’s horse reintroduction to Mongolia: Status and outlook. WAZA Mag. 2012, 13, 3–6. [Google Scholar]
  30. Xia, C.; Cao, J.; Zhang, H.; Gao, X.; Yang, W.K.; Blank, D. Reintroduction of Przewalski’s horse (Equus ferus przewalskii) in Xinjiang, China: The status and experience. Biol. Conserv. 2014, 177, 142–147. [Google Scholar] [CrossRef]
  31. Bourjade, M. Sociogeny and Manifestation of Individual and Collective Behaviours in Horses. Ph.D. Dissertation, University of Strasbourg, Strasbourg, France, 2007. [Google Scholar]
  32. May-Davis, S.; Vermeulen, Z.; Brown, W.Y. A primitive trait in two breeds of Equus caballus revealed by comparative anatomy of the distal limb. Animals 2019, 9, 6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Mohr, E. The Asiatic Wild Horse, 2nd ed.; J. A. Allen & Co., Ltd.: London, UK, 1971. [Google Scholar]
  34. Guthrie, R.D. Frozen Fauna of the Mammoth Steppe; University of Chicago Press: Chicago, IL, USA, 1990. [Google Scholar]
  35. Leroi-Gourhan, A. Préhistoire de l’ar Occidental; Éditions D’art Lucien Mazenod: Paris, France, 1971; p. 482. [Google Scholar]
  36. Ryder, O.A. Putting the wild horse back to the wild. In International Symposium on the Preservation of the Przewalski Horse; Seifert, S., Ed.; Zoologische Garten Leipzig: Leipzig, Germany, 1992; pp. 328–331. [Google Scholar]
  37. Ryder, O.A. Przewalski’s horse: Prospects for reintroduction into the wild. Conserv. Biol. 1993, 7, 13–15. [Google Scholar] [CrossRef]
  38. MTSPWG (Mongolia Takhi Strategy and Plan Work Group). Recommendations for Mongolia’s Takhi: Strategy and Plan; Mongolian Government, Ministry of Nature and Environment: Ulaan Baatar, Mongolia, 1993.
  39. Ryder, O. Putting the wild horse back into the wild. In Przewalski’s Horse Global Conservation Plan; Zoological Society of San Diego, Center for Reproduction of Endangered Species: San Diego, CA, USA, 1990. [Google Scholar]
  40. Gao, X. Preliminary report of Przewalski horse. Arid. Zone Res. 1984, 1, 71–72. [Google Scholar]
  41. Linnaeus, C. Systema Naturae Fundamenta Botanica. Lomolino, M.V. and Channell, R. 1995. Splendid Isolation: Patterns of Geographic Range Collapse in Endangered Mammals. J. Mammal. 1758, 76, 335–347. [Google Scholar]
  42. Przewalski, N. Reisen in Tibet Und am Oberen Lauf des Gelben Flusses in Den Jahren 1879 bis 1880; Stein Nordheim: Jena, Germany, 1884; p. 269. [Google Scholar]
  43. Allen, G.M. The Mammals of China and Mongolia; American Museum (Natural History): New York, NY, USA, 1938; Volume 4, pp. 1280–1287. [Google Scholar]
  44. Paklina, N.; Pozdnyakova, M.K. Why the Przewlaski horses of Mongolia died out. Przewalski Horse 1989, 24, 30–34. [Google Scholar]
  45. Jiang, Z. Wild Horse (Equus przewalskii). Chin. J. Zool. 2004, 39, 100–101. (In Chinese) [Google Scholar]
  46. Gao, X.; Gu, J. The distribution and status of the Equidae in China. Acta Theriol. Sin. 1989, 9, 269–274. (In Chinese) [Google Scholar]
  47. IUCN. From Extinction to Free Ranging by Successful Reintroduction. 2017. Available online: https://www.iucn.org/news/commission-ecosystem-management/201803/extinction-free-ranging-successful-reintroduction (accessed on 1 September 2022).
  48. Saltz, D.; Rubenstein, D.I. Population dynamics of a reintroduced Asiatic wild ass (Equus hemionus) herd. Ecol. Appl. 1995, 5, 327–335. [Google Scholar] [CrossRef]
  49. Boyd, L.; Houpt, K.A. (Eds.) Przewalski’s Horse: The History and Biology of an Endangered Species; State University of New York Press: New York, NY, USA, 1994; p. 313. [Google Scholar]
  50. Zhao, T.; Liang, G. On returning to its native place and conservating of the Przewalski horse. In International Symposium on the Preservation of the Przewalski Horse; Seifert, S., Ed.; Zoologischer Garten Leipzig: Leipzig, Germany, 1992; pp. 227–231. [Google Scholar]
  51. Chen, J.L.; Hu, D.F.; Li, K.; Cao, J.; Meng, Y.P.; Cui, Y.Y. The diurnal feeding behavior comparison between the released and captive adult female Przewalski’ s horse (Equus przewalskii) in summer. Acta Ecol. Sin. 2008, 28, 1105–1108. [Google Scholar]
  52. Kaiser, J. Inbreeding’s kiss of death. Science 1998, 280, 35. [Google Scholar] [CrossRef]
  53. Westemeier, R.L.; Brawn, J.D.; Simpson, S.A.; Terry, L.E.; Jansen, R.W.; Walk, J.W.; Kershner, E.L.; Bouzat, J.L.; Paige, K.N. Tracking the long-term decline and recovery of an isolated population. Science 1998, 282, 1695–1698. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Bouman, J.; Bos, H. wo symptoms of inbreeding depression in Przewalski horses living in captivity. In Genetics and Hereditary Diseases of the Przewalski Horse; Foundation for the Preservation and Protection of the Przewalski Horse: Rotterdam, The Netherlands, 1979; pp. 165–168. [Google Scholar]
  55. Bannikov, A.G. Der Bestand des Przewalskipferdes in der freien Natur. Equus 1967, 1, 243–245. [Google Scholar]
  56. Berger, A.; Scheibe, K.M.; Eichhorn, K.; Scheibe, A.; Streich, J. Diurnal and ultradian rhythms of behaviour in a mare group of Przewalski horse (Equus ferus przewalskii), measured through one year under semi-reserve conditions. Appl. Anim. Behav. Sci. 1999, 64, 1–17. [Google Scholar] [CrossRef]
  57. Grum-Grzimailo, G.E. The wild horse (Equus przewalskii). From the diary of a travel to China in 1889–1890 (translated by Aleinikov, P). 1892; Volume 17. pp. 374–382. (In Russian) [Google Scholar]
  58. Grum-Grzimailo, G.E. Description of the Expedition to the West China; Russian Geographical Society: St. Petersburg, Russia, 1896. [Google Scholar]
  59. Seal, U.S.; Foose, T.; Lacy, R.C.; Zimmermann, W.; Ryder, O.; Prince, F. Przewalski’s Horse Global Conservation Plan (Draft); Captive Breeding Specialist Group, IUCN: Gland, Switzerland, 1990. [Google Scholar]
  60. Geyer, C.; Thompson, E.; Ryder, O. Gene survival in the Asiatic wild horse (Equus przewalskii): II. Gene survival in the whole population, in subgroups, and through history. Zoo Biol. 1989, 8, 313–329. [Google Scholar] [CrossRef]
  61. Bakirova, R.T.; Zharkikh, T.L. Programme on establishing a semi-free population of Przewalski’s horse in Orenburg State Nature Reserve: The first successful project on the reintroduction of the species in Russia. Nat. Conser. Res. 2019, 4 (Suppl. S2), 57–64. [Google Scholar] [CrossRef]
  62. King, S.R.B. Extinct in the Wild to Endangered: The history of Przewalski’s horse (Equus ferus przewalskii) and its future conservation. Mong. J. Biol. Sci. 2005, 3, 37–41. [Google Scholar]
  63. Bouman, J. The return of the Takhi. In The Tale of the Przewalski’s Horse; Wit, P., Bouoman, I., Eds.; KNNV Publishers: Utrecht, The Netherlands, 2006; pp. 82–161. [Google Scholar]
  64. Zimmermann, W. Feasibility study, Site Selection and Development of a Reintroduction Project of the Przewalski’s Horse (Equus ferus przewalskii) in the Dzungarian Gobi in Mongolia. Proc. Int. Symp. Neuhaus/Solling, 21–23.4.1998: Natural and Man-Made Landscape-History, Models and Perspectives for the Development of European Landscapes with Large Herbivores, Gerken, B., Meyer, C., Eds.; 1999. [Google Scholar]
  65. Zimmermann, W. Przewalski’s horses on the track to reintroduction -various projects compared. Z. Des Kölner Zoo 2005, 48, 183–209. [Google Scholar]
  66. Zimmermann, W. Das Erhaltungszuchtprogramm Przewalskipferd, eine 10-jährige Zusammenarbeit in Europa. In Populationsgenetik im Artenschutz; Schreiber, A., Lehmann, J., Eds.; Landwirtschaftsverlag: Münster, Germany, 1997; pp. 189–200. [Google Scholar]
  67. Pereladova, O.B.; Sempéré, A.J.; Soldatova, N.V.; Dutov, V.; Fisenko, G.; Flint, V.E. Przewalski’s horse—Adaptation to semi-wild life in desert conditions. Oryx 1999, 1, 12. [Google Scholar]
  68. Duncan, P.B. Zebras, Asses and Horses. An Action Plan for the Conservation of Wild Equids; IUCN/SSC Equid Specialist Group: Gland, Switzerland, 1992. [Google Scholar]
  69. Kaczensky, P.; Walzer, C. Przewalski Horses, Wolves and Khulans in Mongolia—ITG Research Report 2002; Annual Research Report; International Takhi Group: Salzburg, Austria, 2002; p. 12. [Google Scholar]
  70. Kaczensky, P.; Walzer, C. Monitoring of free-ranging Przewalski’s horses with satellite telemetry in Takhin Tal. Mong. J. Biol. Sci. 2004, 2, 59–60. [Google Scholar]
  71. Kaczensky, P.; Ganbaatar, O.; Wehrden, H.V.; Enksaikhan, N.; Lkhagvasuren, D.; Walzer, C. Przewalski horse reintroduction in the Great Gobi B Strictly Protected area from species to ecosystem conservation. Mong. J. Biol. Sci. 2007, 5, 13–18. [Google Scholar]
  72. Boyd, L.; Bandi, N. Reintroduction of takhi to Hustai National Park, Mongolia: Time budget and synchrony of activity pre- and post-release. Appl. Anim. Behav. Sci. 2002, 78, 87–102. [Google Scholar] [CrossRef]
  73. Germeraad, P. Towards an effective management and strategy of nature reserves in Mongolia. In Seminar on Naturschutz Und Okotourismus in Der Mongolei; World Wildlife Fund: Ulaan Baatar, Mongolia, 1993. [Google Scholar]
  74. Germeraad, P.; Van Dierendonck, M.C.; Wallis de Vries, M.F. Standard rapport Hustain Nuruu Steppe Reserve Mongolia. In Directorate for International Co-Operation from the Dutch Ministry of Development Aid; Den Haag The Netherlands/Foundation Reserves Przewalski’s Horse (FRPH): Rotterdam, The Netherland, 1993. [Google Scholar]
  75. Bouman, I. The Reintroduction of Przewalski Horses in the Hustain Nuruu Mountain Forest Steppe Reserve in Mongolia: An integrated conservation development project.Mededelingen van de Nederlandsche Commissie voor Internationale Natuurbescherming. Commun. Dutch Comm. Int. Nat. Preserv. 1998, 32, 1–50. [Google Scholar]
  76. Walzer, C.; Kaczensky, P.; Ganbaatar, O.; Lengger, J.; Enkhsaikhan, N.; Lkhagvasuren, D. Capture and anaesthesia of wild Mongolian equids-the Przewalski’s horse (E. ferus przewalskii) and khulan (E. hemionus). Mong. J. Biol. Sci. 2007, 4, 19–28. [Google Scholar]
  77. Walzer, C.; Kaczensky, P.; Ganbataar, O.; Enkhsaikhan, N.; Stauffer, C. Coming home: The return of the Przewalski’s horse to the Mongolian Gobi. In Building a Future for Wildlife -Zoos and Aquariums Committed to Biodiversity Conservation; Dick Gusset, M., Ed.; World Association of Zoos and Aquariums (WAZA): Gland, Switzerland, 2010; pp. 123–128. [Google Scholar]
  78. Bouman, I. Reintroduction of Przewalski’s Horses in the Mountain Steppe of Hustain Nuruu in Mongolia; Foundation Reserves Przewalski Horse: Rotterdam, The Netherlands, 1996; p. 7. [Google Scholar]
  79. Van Dierendonck, M.C.; Bandi, N.; Batdorj, D.; Dugerlham, S.; Munkhtsog, B. Behavioural observations of reintroduced Takhi or Przewalski horses Equus ferus przewalskii in Mongolia. Appl. Anim. Behav. Sci. 1996, 50, 95–114. [Google Scholar] [CrossRef]
  80. Huang, H.; Zhang, K.; Zhang, B.; Liu, S.; Chu, H.; Qiu, Y. Analysis on the relationship between winter precipitation and the annual variation of horse stomach fly community in arid desert steppe, northwest china (2007-2019). Integr. Zool. 2022, 17, 128–138. [Google Scholar] [CrossRef] [PubMed]
  81. Liu, G.; Shafer, A.B.; Zimmermann, W.; Hu, D.; Wang, W.; Chu, H. Evaluating the reintroduction project of Przewalski’s horse in China using genetic and pedigree data. Conserv. Biol. 2014, 171, 288–298. [Google Scholar] [CrossRef]
  82. Hu, D.; Chao, Y.; Zhang, B.; Wang, C.; Qi, Y.; Ente, M.; Zhang, D.; Li, K.; Mok, M.K. Effects of Gasterophilus pecorum infestation on the intestinal microbiota of the rewilded Przewalski’s horses in China. PLoS ONE 2021, 16, e0251512. [Google Scholar] [CrossRef] [PubMed]
  83. Wang, H.; He, Z.Q.; Wang, H.J.; Niu, Y.X. Study on Survival status of reintroduced equus przewalskii in dunhuang west lake national nature reserve. J. Gansu For. Sci. Technol. 2012, 37, 44–46. (In Chinese) [Google Scholar]
  84. Kaczensky, P.; Burnik Šturm, M.; Sablin, M.V.; Voigt, C.C.; Smith, S.; Ganbaatar, O. Stable isotopes reveal diet shift from pre-extinction to reintroduced Przewalski’s horses. Sci. Rep. 2017, 7, 5950. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Ryder, O.A.; Wedemeyer, E.A. A cooperative breeding program for the Mongolian wild horse, Equus przewalskii, in the United States. Biol Conserv. 1982, 22, 259–271. [Google Scholar] [CrossRef]
  86. Ganbaatar, O. Takhi’s (Equus przewalskii Polj., 1883) Home Range and Water Point Use. Master’s Thesis, National University of Mongolia, Ulaanbaatar, Mongolia, 2003. Available online: www.takhi.org (accessed on 1 September 2022).
  87. Arzdord, W. Stand, Moglichkeiten und Grenzen von Zucht und Auswilderung bedrohter Tierarten als beitrag zum Artenschutz. In Gefordertes Forschungs-und Entwicklingsvorhaben des Bundesministeriums fur Umwelt; Naturschutz und Reaktorsicherheit: Koln, Deutschland, 1990. [Google Scholar]
  88. Black, J.; Marshall, M.A.P.; Gilburn, A. Survival, Movements and Reproductive Success of Released Hawaiian geese: An Assessment After Thirty-three Years. In Conjunction with the Nene Recovery Team’s Field Biologists; A report to the Nene Recovery Team; Number 14; U.S. Fish and Wildlife Service: Honolulu, HI, USA, 1993. [Google Scholar]
  89. Waring, G.H. Horse Behavior: Behavioral Traits and Adaptations of Domestic and Wild Horses, Including Ponies; Noyes Publications: Berkshire, UK, 1983. [Google Scholar]
  90. Berger, J. Wild Horses of the Great Basin; The University of Chicago Press: Chicago, IL, USA, 1986. [Google Scholar]
  91. Kajiwara, I.; Yoshihara, Y.; Sato, S. A preliminarily assessment of landscape factors affecting habitat use by Przewalski horses and habitat evaluation in Hustai National Park, Mongolia. Mamm. Biol. 2016, 81, 340–344. [Google Scholar] [CrossRef]
  92. Kaczensky, P.; Ganbaatar, O.; Von Wehrden, H.; Walzer, C. Resource selection by sympatric wild equids in the Mongolian Gobi. J. Appl. Ecol. 2008, 45, 1762–1769. [Google Scholar] [CrossRef]
  93. Stevens, E.F. Contests between bands of feral horses for access to fresh water: The resident wins. Anim. Behav. 1988, 36, 1851–1853. [Google Scholar] [CrossRef]
  94. Mysterud, A.; Østbye, E. Cover as a habitat element for temperate ungulates: Effects on habitat selection and demography. Wildl. Soc. Bull. 1999, 27, 385–394. [Google Scholar]
  95. Ganskopp, D.; Vavra, M. Slope use by cattle, feral horses, deer, and bighorn sheep. Northwest Sci. 1987, 61, 74–81. [Google Scholar]
  96. King, S.R.B.; Gurnell, J. Effects of fly disturbance on the behaviour of a population of reintroduced Przewalski horses (Equus ferus przewalskii) in Mongolia. Appl. Anim. Behav. Sci. 2010, 125, 22–29. [Google Scholar] [CrossRef]
  97. Girard, T.L.; Bork, E.W.; Neilsen, S.E.; Alexander, M.J. Landscape-scale factors affecting feral horse habitat use during summer within the rocky mountain foothills. Environ. Manag. 2013, 51, 435–447. [Google Scholar] [CrossRef]
  98. Volf, J.; Kus, E.; Prokopova’, L. General Studbook of the Przewalski Horse (Zoological Garden Prague, Prague, Czech Republic). 1991. Available online: http://przwhorse.pikeelectronic.com/ (accessed on 1 September 2022).
  99. Oakenfull, E.; Ryder, O.A. Mitochondrial control region and 12S rRNA variation in Przewalski’s horse (Equus przewalskii). Anim. Genet. 1998, 29, 456–459. [Google Scholar] [CrossRef] [Green Version]
  100. Sasaki, M.; Endo, H.; Yamagiwa, D.; Yamamoto, M.; Arishima, K.; Hayashi, Y. Morphological character of the shoulder and leg skeleton in Przewalski’s horse (Equus przewalskii). Ann. Anat. 1999, 181, 403–407. [Google Scholar] [CrossRef]
  101. Shimodaira, H.; Hasegawa, M. Multiple comparisons of Loglikelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 1999, 16, 1114–1116. [Google Scholar] [CrossRef] [Green Version]
  102. Gaunitz, C.; Fages, A.; Kristian, H.; Albrechtsen, A.; Khan, N.; Schubert, M.; Seguin-Orlando, A.; Owens, I.J.; Felkel, S.; Bignon-Lau, O.; et al. Ancient genomes revisit the ancestry of domestic and Przewalski’s horses. Science 2018, 360, 111–114. [Google Scholar] [CrossRef] [Green Version]
  103. Benirschke, K.; Malouf, N.; Low, R.J.; Heck, H. Chromosome complement: Differences between Equus caballus and Equus przewalskii, poliakoff. Science 1965, 148, 382–383. [Google Scholar] [CrossRef] [PubMed]
  104. Oosterhout, C.; Hutchinson, W.F.; Wills, D.P.; Shipley, P. Micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 2004, 4, 535–538. [Google Scholar] [CrossRef]
  105. Ahrens, E.; Stranzinger, G. Comparative chromosomal studies of E. caballus (ECA) and E. przewalskii (EPR) in a female F1 hybrid. J. Anim. Breed Genet. 2005, 122 (Suppl. S1), 97–102. [Google Scholar] [CrossRef]
  106. Myka, J.L.; Lear, T.L.; Houck, M.L.; Ryder, O.A.; Bailey, E. FISH analysis comparing genome organization in the domestic horse (Equus caballus) to that of the Mongolian wild horse (E. przewalskii). Cytogenet. Genome Res. 2003, 102, 222–225. [Google Scholar] [CrossRef]
  107. Bowling, A.T.; Ruvinsky, A. Genetic aspects of domestication breeds and their origin. In The Genetics of the Horse; Bowling, A.T., Ruvinsky, A., Eds.; CAB International: Wallingford, UK, 2000. [Google Scholar]
  108. Yang, F.; Fu, B.; O’Brian, P.C.M.; Robinson, T.J.; Ryder, O.A.; Ferguson-Smith, M.A. Karyotypic relationships of horses and zebras: Results of cross-species chromosome painting. Cytogenet. Genome Res. 2003, 102, 235–243. [Google Scholar] [CrossRef] [PubMed]
  109. Trommerhansen-Smith, A.; Ryder, O.A.; Suzuki, Y. Bloodtyping studies of twelve przewalskii’s horses. Intl. Zoo Yrbk. 1979, 9, 224–227. [Google Scholar] [CrossRef]
  110. Short, R.V.; Chandley, A.C.; Jones, R.C.; Allen, W.R. Meiosis in interspecific equine hybrids II. The Przewalski horse/domestic horse hybrid (Equus przewalskii X E. caballus). Cytogenet. Cell Genet. 1974, 13, 465–478. [Google Scholar] [CrossRef] [PubMed]
  111. Outram, A.K.; Stear, N.A.; Bendrey, R.; Olsen, S.; Kasparov, A.; Zaibert, V.; Thorpe, N.; Evershed, R.P. The earliest horse harnessing and milking. Science 2009, 323, 1332–1335. [Google Scholar] [CrossRef] [PubMed]
  112. George, M.; Ryder, O.A. Mitochondrial DNA evolution in the genus Equus. Mol. Bit1 Evol. 1986, 3, 535–546. [Google Scholar]
  113. Ishida, N.; Oyunsuren, T.; Mashima, S.; Mukoyama, H.; Saitou, N. Mitochondrial DNA sequences of various species of the genus Equus with special reference to the phylogenetic relationship between Przewalskii’s wild horse and domestic horse. J. Mol. Evol. 1995, 41, 180–188. [Google Scholar] [CrossRef] [PubMed]
  114. Oakenfull, E.A.; Lim, H.N.; Ryder, O.A. Survey of equid mitochondrial DNA: Implications for the evolution, genetic diversity and conservation of Equus. Cons. Gen. 2000, 1, 341–355. [Google Scholar] [CrossRef]
  115. Short, R.V. The evolution of the horse. J. Reprod. Fertil. 1975, 23, 1–6. [Google Scholar]
  116. Ryder, O.A.; Epel, N.C.; Benirschke, K. Chromosome banding studies of the Equidae. Cytogenet. Cell Genet. 1978, 20, 323–350. [Google Scholar] [CrossRef]
  117. Bandi, N. Reproduction status of takhi being reintroduced in Hustai National Park. Mong. J. Biol. Sci. 2004, 2, 57. [Google Scholar]
  118. Maudet, C.; Miller, C.; Bassano, B.; Breitenmoser-Würsten, C.; Gauthier, D.; ObexerRuff, G.; Michallet, J.; Taberlet, P.; Luikart, G. Microsatellite DNA and recent statistical methods in wildlife conservation management: Applications in Alpine ibex (Capra ibex). Mol. Ecol. 2002, 11, 421–436. [Google Scholar] [CrossRef] [PubMed]
  119. Hedrick, P.W.; Parker, K.M.; Miller, E.L.; Miller, P.S. Major histocompatibility complex variation in the endangered Przewalski’s horse. Genetics 1999, 152, 1701–1710. [Google Scholar] [CrossRef]
  120. Lau, A.N.; Peng, L.; Goto, H.; Chemnick, L.; Ryder, O.A.; Makova, K.D. Horse domestication and conservation genetics of Przewalski’s horse inferred from sex chromosomal and autosomal sequences. Mol. Biol. Evol. 2009, 26, 199–208. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  121. Wallner, B.; Brem, G.; Muller, M.; Achmann, R. Fixed nucleotide differences on the Y chromosome indicate clear divergence between Equus przewalskii and Equus caballus. Anim. Genet. 2003, 34, 453–456. [Google Scholar] [CrossRef] [Green Version]
  122. Ivy, J.A.; Miller, A.; Lacy, R.C.; DeWoody, J.A. Methods and prospects for using molecular data in captive breeding programs: An empirical example using parma wallabies (Macropus parma). J. Hered. 2009, 100, 441–454. [Google Scholar] [CrossRef] [Green Version]
  123. Alqamy, E.H.; Senn, H.; Roberts, M.F.; McEwing, R.; Ogden, R. Genetic assessment of the Arabian oryx founder population in the Emirate of Abu Dhabi, UAE: An example of evaluating unmanaged captive stocks for reintroduction. Conserv. Genet. 2012, 13, 79–88. [Google Scholar] [CrossRef]
  124. Barba, D.M.; Waits, L.; Garton, E.; Genovesi, P.; Randi, E.; Mustoni, A.; Groff, C. The power of genetic monitoring for studying demography, ecology and genetics of a reintroduced brown bear population. Mol. Ecol. 2010, 19, 3938–3951. [Google Scholar] [CrossRef] [PubMed]
  125. Henkel, J.R.; Jones, K.L.; Hereford, S.G.; Savoie, M.L.; Leibo, S.; Howard, J.J. Integrating microsatellite and pedigree analyses to facilitate the captive management of the endangered Mississippi sandhill crane (Grus canadensis pulla). Zoo Biol. 2012, 31, 322–335. [Google Scholar] [CrossRef] [PubMed]
  126. Townsend, S.; Jamieson, I. Molecular and pedigree measures of relatedness provide similar estimates of inbreeding depression in a bottlenecked population. J. Evol. Biol. 2013, 26, 889–899. [Google Scholar] [CrossRef]
  127. Robert, A. Captive breeding genetics and reintroduction success. Biol. Conserv. 2009, 142, 2915–2922. [Google Scholar] [CrossRef]
  128. Armbruster, P.; Reed, D. Inbreeding depression in benign and stressful environments. Heredity 2005, 95, 235–242. [Google Scholar] [CrossRef] [PubMed]
  129. Charlesworth, D. Effects of inbreeding on the genetic diversity of populations. Pyilos. Trans. R. Soc. B Biol. Sci. 2003, 358, 1051–1070. [Google Scholar] [CrossRef]
  130. Kalinowski, S.T.; Hedrick, P.W.; Miller, P.S. Inbreeding depression in the Speake’s gazelle captive breeding program. Conserv. Biol. 2000, 14, 1375–1384. [Google Scholar] [CrossRef]
  131. Świsłocka, M.; Czajkowska, M.; Duda, N.; Ratkiewicz, M. Admixture promotes genetic variation in bottlenecked moose populations in eastern poland. Mammal Res. 2015, 60, 169–179. [Google Scholar] [CrossRef] [Green Version]
  132. Bowling, A.T.; Zimmermann, W.; Ryder, O.; Penado, C.; Peto, S.; Chemnick, L.; Yasinetskaya, N.; Zharkikh, T. Genetic variation in Przewalski’s horses, with special focus on the last wild caught mare, 231 Orlitza III. Cytogenet. Genome Res. 2003, 102, 226–234. [Google Scholar] [CrossRef]
  133. Wade, C.M.; Giulotto, E.; Sigurdsson, S.; Zoli, M.; Gnerre, S.; Imsland, F.; Lear, T.L.; Adelson, D.L.; Bailey, E.; Bellone, R.R.; et al. Genome sequence, comparative analysis, and population genetics of the domestic horse. Science 2009, 326, 865–867. [Google Scholar] [CrossRef] [Green Version]
  134. White, J.M. Inbreeding effects upon growth and maternal ability in laboratory mice. Genetics 1972, 70, 307–317. [Google Scholar] [CrossRef] [PubMed]
  135. Breen, M.; Downs, P.; Irvin, Z.; Bell, K. Intrageneric amplification of horse microsatellite markers with emphasis on the Przewalski’s horse (E. przewalskii). Anim. Genet. 1994, 25, 401–405. [Google Scholar] [CrossRef] [PubMed]
  136. Jones, K.L.; Glenn, T.C.; Lacy, R.C.; Pierce, J.R.; Unruh, N.; Mirande, C.M.; Chavez-Ramirez, F. Refining the Whooping Crane studbook by incorporating microsatellite DNA and leg-banding analyses. Conserv. Biol. 2002, 16, 789–799. [Google Scholar] [CrossRef]
  137. Tracy, L.N.; Wallis, G.P.; Efford, M.G.; Jamieson, I.G. Preserving genetic diversity in threatened species reintroductions: How many individuals should be released? Anim. Conserv. 2011, 14, 439–446. [Google Scholar] [CrossRef]
  138. Witzenberger, K.A.; Hochkirch, A. Ex situ conservation genetics: A review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv. 2011, 20, 1843–1861. [Google Scholar] [CrossRef]
  139. Williams, S.E.; Hoffman, E.A. Minimizing genetic adaptation in captive breeding programs: A review. Biol. Conserv. 2009, 142, 2388–2400. [Google Scholar] [CrossRef]
  140. Slotta-Bachmayr, L.; Boegel, R.; Kaczensky, P.; Stauffer, C.; Walzer, C. Use of population viability analysis to identify management priorities and success in reintroducing Przewalski’s horses to Southwestern Mongolia. J. Wildl. Manag. 2004, 68, 790–798. [Google Scholar] [CrossRef]
  141. Taylor, S.S.; Jamieson, I.G. No evidence for loss of genetic variation following sequential translocations in extant populations of a genetically depauperate species. Mol. Ecol. 2008, 17, 545–556. [Google Scholar] [CrossRef] [PubMed]
  142. Willi, Y.; Van Buskirk, J.; Schmid, B.; Fischer, M. Genetic isolation of fragmented populations is exacerbated by drift and selection. J. Evol. Biol. 2007, 20, 534–542. [Google Scholar] [CrossRef] [PubMed]
  143. Snyder, N.F.; Derrickson, S.R.; Beissinger, S.R.; Wiley, J.W.; Smith, T.B.; Toone, W.D.; Miller, B. Limitations of captive breeding in endangered species recovery. Conserv. Biol. 1996, 10, 338–348. [Google Scholar] [CrossRef] [Green Version]
  144. Gilligan, D.M.; Frankham, R. Dynamics of genetic adaptation to captivity. Conserv. Genet. 2003, 4, 189–197. [Google Scholar] [CrossRef]
  145. Frankham, R. Challenges and opportunities of genetic approaches to biological conservation. Biol. Conserv. 2010, 143, 1919–1927. [Google Scholar] [CrossRef]
  146. Boyd, L. The 24 h time budget of a takhi harem stallion (Equus ferus przewalskii) pre- and post-reintroduction. Appl. Anim. Behav. Sci. 1998, 60, 291–299. [Google Scholar] [CrossRef]
  147. Boyd, L.; Kasman, L. The marking behavior of male Przewalski’s horses. In Chemical Signals in Vertebrates; Duvall, D., Muller-Schwarze, D., Silverstein, R.M., Eds.; Springer: New York, NY, USA, 1986; Volume 4, pp. 623–626. [Google Scholar]
  148. Klingel, H. Soziale organisation und Verhalten freilebender Steppenzebras. Z. Tierpsychol. 1967, 24, 580–624. [Google Scholar] [CrossRef] [PubMed]
  149. Klingel, H. Soziale Organisation und Verhaltensweisen von Haltmann und Bergzebras. Z. Tierpsychol. 1968, 25, 76–88. [Google Scholar] [CrossRef]
  150. Klimov, V.V. Space-ethological organisation of Przewalski horses (Equus przewalskii) herds in Askania Nova. In The Przewalski Horse and Its Restoration in Nature in Mongolia; FAO/UNEP: Moscow, Russia, 1986; pp. 160–179. (In Russian) [Google Scholar]
  151. King, S.R.B. Home range and habitat use of free-ranging Przewalski horses at Hustai National Park, Mongolia. Appl. Anim. Behav. Sci. 2002, 78, 103–113. [Google Scholar] [CrossRef]
  152. Rubenstein, D.I.; Hack, M.A.C.E. Natural and Sexual Selection and the Evolution of Multi-Level Societies: Insights from Zebras with Comparisons to Primates. In Sexual Selection in Primates: New and Comparative Perspectives; Cambridge University Press: Cambridge, UK, 2004; pp. 266–279. [Google Scholar]
  153. Klingel, H. The social organisation and population ecology of the plains zebra (Equus quagga). Afr. Zool. 1969, 4, 249–263. [Google Scholar] [CrossRef] [Green Version]
  154. Hogan, E.S.; Houpt, K.A.; Sweeney, K. The effect of enclosure size on social interactions and daily activity patterns of the captive Asiatic Wild Horse (Equus przewalskii). Appl. Anim. Behav. Sci. 1998, 21, 147–168. [Google Scholar] [CrossRef]
  155. Kolter, L.; Zimmermann, W. Social behaviour of Przewalski horses (Equus p. przewalskii) in the Cologne Zoo and its consequence for management and housing. Appl. Anim. Behav. Sci. 1988, 21, 117–145. [Google Scholar] [CrossRef]
  156. Boyd, L. The behaviour of Przewalski’s horses and its importance to their management. Appl. Anim. Behav. Sci. 1991, 29, 301–318. [Google Scholar] [CrossRef]
  157. Hediger, H. Wild Animals in Captivity: An Outline of the Biology of Zoological Gardens; Dover Pubns: New York, NY, USA, 1964. [Google Scholar]
  158. Mackler, S.F.; Dolan, J.M. Social structure and herd behavior of Equus przewalskii Poliakov, 1881 at the San Diego Wild Animal Park. Equus 1980, 2, 55–69. [Google Scholar]
  159. Pollock, J.I. Behavioural Ecology and Body Condition Changes in New Forest Ponies; R.S.P.C.A. Scientific Publications, Horsham: Gt. Britain, UK, 1881. [Google Scholar]
  160. Trivers, R.L. Parental investment and sexual selection. In Sexual Selection and the Descent of Man 1871–1971; Campbell, B.G., Ed.; Aldine: Chicago, IL, USA, 1972; pp. 136–179. [Google Scholar]
  161. Dallaire, A. Rest behavior. In The Veterinary Clinics of North America: Equine Practice 2 (3); Crowell-Davis, S.L., Houpt, K.A., Eds.; Saunders: Philadelphia, PA, USA, 1986; pp. 591–607. [Google Scholar]
  162. Tatin, L.; King, S.R.B.; Munkhtuya, B.; Hewison, A.J.M.; Feh, C. Demography of a socially natural herd of Przewalski’s horses: An example of a small, closed population. J. Zool. 2009, 277, 134–140. [Google Scholar] [CrossRef]
  163. Gaillard, J.M.; Festa-Bianchet, M.; Yoccoz, N.G.; Loison, A.; Toigo, C. Temporal variation in fitness components and population dynamics of large herbivores. Ann. Rev. Ecol. Syst. 2000, 31, 367–393. [Google Scholar] [CrossRef]
  164. Górecka-Bruzda, A.; Fureix, C.; Ouvrard, A.; Bourjade, M.; Hausberger, M. Investigating determinants of yawning in the domestic (Equus caballus) and przewalski (Equus ferus przewalskii) horses. Die Nat. 2016, 9, 72. [Google Scholar] [CrossRef] [PubMed]
  165. Pei, P.; Wang, L.; Shao, Y.; Shi, C.; Yang, Y.; Bai, X. Reintrodued Przewalski’s horse’s breeding success and population viability analyses in Anxi National Nature Reserve. Acta Theriol. Sin. 2018, 38, 128–139. (In Chinese) [Google Scholar]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Turghan, M.A.; Jiang, Z.; Niu, Z. An Update on Status and Conservation of the Przewalski’s Horse (Equus ferus przewalskii): Captive Breeding and Reintroduction Projects. Animals 2022, 12, 3158. https://doi.org/10.3390/ani12223158

AMA Style

Turghan MA, Jiang Z, Niu Z. An Update on Status and Conservation of the Przewalski’s Horse (Equus ferus przewalskii): Captive Breeding and Reintroduction Projects. Animals. 2022; 12(22):3158. https://doi.org/10.3390/ani12223158

Chicago/Turabian Style

Turghan, Mardan Aghabey, Zhigang Jiang, and Zhongze Niu. 2022. "An Update on Status and Conservation of the Przewalski’s Horse (Equus ferus przewalskii): Captive Breeding and Reintroduction Projects" Animals 12, no. 22: 3158. https://doi.org/10.3390/ani12223158

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop