To ensure that captive breeding programs are more robust and sustainable, it is important to ethically and legally ensure optimum animal welfare [1
]. The rapid developmental processes of humans are affecting the natural habitats of wildlife. Thus, wildlife reservoirs, zoos, and enclosures must be adapted to minimize the effect of these changes [2
]. Today, captive breeding is one of the most important conservation tools [3
], providing an opportunity to the rare endangered species to produce stable populations for eventual release into the wild [4
In the meantime, enclosures and other facilities for wild animals are under severe pressure to limit animals to small areas [5
]. Thus, animal welfare subjects, particularly those related to the captive wild species, are rapidly recognized [6
]. It is important to ensure the optimum levels of animal welfare of captive animals for the production and maintenance of healthy, viable populations [8
]. To make captive breeding more robust, it is important to determine the main factors of species welfare and, most importantly, the welfare of every individual of a particular group [9
Animal welfare assessment protocols can be designed by gathering information through simple inspections, animal observations, and visiting animal facilities and enclosures [10
]. Animal welfare assessment protocols for livestock (poultry, cattle, and pigs) have already been developed under the auspices of the Welfare Quality®
project. These protocols are mainly based on animal-based indicators, in addition to also having resource or environmental measures [11
]. Animal-based measures can be directly recorded by observing animals, including their physical appearance, health, and behavior. Unlike animal-based measures, environmental measures assess the available resources for these animals in captivity, and the animal itself is not taken into account.
(urial) is a wild sheep that closely resembles Marco Polo sheep in general body appearance [12
]. In Pakistan, the urial is represented by three subspecies: Ovis vignei vigeni
(Ladakh urial), which is restricted to northern areas (Gilgit-Baltistan) of Pakistan; Ovis vignei punjabiensis
(Punjab urial) found in the Salt Range (Punjab) and the northwestern province of Khyber Pakhtunkhwa (formerly known as the North-West Frontier Province); and Ovis vignei blanfordi
(Baluchi urial), which is found in the southwestern province of Balochistan [13
]. The Punjab urial is a gregarious ungulate, and most big herds include females, lambs, and immature males. It has been observed that the urial generally prefers grasses, but can also be found foraging on shrubs [14
The species has been declared as vulnerable globally, with a declining population trend, according to the International Union for Conservation (IUCN) list of threatened species [15
], and is endangered in Pakistan [16
]. In Pakistan, wild ungulates are reared in captivity, but there are no standardized methods and protocols to measure the welfare of these captive ungulates. Therefore, this current study aimed to (i) design and develop a baseline welfare assessment protocol for captive Punjab urial based on the livestock welfare assessment protocol from the Welfare Quality®
project, (ii) implement this welfare assessment protocol in facilities hosting Punjab urial, and (iii) suggest recommendations for better captive breeding and management.
2. Materials and Methods
For this study, we selected the subspecies Ovis orientalis punjabiensis
because of its availability in captivity. The current study was conducted in two steps. In the first step, the welfare assessment protocol was developed, and, in the second step, the newly established protocol was implemented at captive facilities housing Punjab urial. We developed the welfare assessment protocol by combining results from other studies on the biology and behavior of the species and the sheep welfare assessment protocol [19
], as both domestic sheep and Punjab urial belong to the family Bovidae.
To obtain information on the general biology and behavior of the species, we used Google Scholar and Web of Science search engines using “Ovis vignei” as keywords. Limited scientific published information is available regarding the biology of this species in natural habitats. Moreover, no work has been conducted to investigate the problems faced by this species in captivity. More than 31 scientific published papers were reviewed. Most of these published work focused on population status, population dynamics, diet ecology, and habitat, of which two papers [12
] provided useful detailed information on the behavior and general biology of the species that was utilized for the welfare assessment protocol.
For developing the Punjab urial welfare assessment protocol, four basic principles were taken into account: good feeding, good housing, good health, and suitable behavior [10
]. These principles led to twelve criteria (see Section 3
), which in turn allowed the development of welfare assessment indicators [21
]. After combining information from [19
], we developed an extensive set of 31 welfare indicators for Punjab urial (see Section 3
The final version of the welfare assessment protocol was then applied to three different groups of captive Punjab urial at two different facilities—Cherat Wildlife Park (CWP) in Nowshera and Manglot Wildlife Park (MWP) in Nizampur—in the month of August 2019. Both of these parks are located in the Nowshera District of Khyber Pakhtunkhwa Province, Pakistan. The captive breeding program was launched in 2008 at CWP with a single pair of founder animals, while in 2012 it was initiated at MWP, also with a single pair. The groups of both programs were mixed herds, including adult males, sub adult males, adult females, sub adult females, and lambs. CWP had one group consisting of 23 individuals (n = 23) with a mean age of 3.21 ± 2.21 years. At MWP, two groups were present (n = 6 and n = 8), with mean ages of 3.16 ± 1.57 and 3.33 ± 1.69 years, respectively. Groups were represented by coding their facilities (centers) as captive Punjab urial-1 (CU1) at CWP, and captive Punjab urial-2 (CU2) and captive Punjab urial-3 (CU3) at MWP. The protocol was applied by the same person.
In the current protocol, the observation time for social behavior was 120 min per herd in six 20-min sessions. Continuous focal sampling was used because these behaviors may be of short duration and elusive nature [10
]. We performed the Shapiro–Wilk test with our datasets to check for normality. Later, data recorded for social behavior (n
= number of occurrences of an event) for all three groups in the current protocol were analyzed using the nonparametric Kruskal–Wallis test to determine the significance of observed variables. All the statistical analyses were performed using SPSS version 23.0 (IBM Corp., Armonk, NY, USA).
The current project was designed to develop, for the first time in Pakistan, a baseline protocol to assess the welfare of wild ungulates in captivity. The assessment of resources, management, and animal-based measures are collectively termed as animal welfare assessments. In order to have a clear idea about the welfare of a group of animals in captivity, it is difficult to achieve the goals by having a single indicator or very few indicators. Thus, to have a complete and appropriate welfare assessment for a particular species, it is important to have a combination of several indicators according to the biology and ecology of that species [21
]. The protocol proposed in this study is based on the welfare protocol for domestic sheep. This protocol differs from the domestic sheep welfare protocol in terms of the number of indicators, consisting of an extended list of 31 different animal- and resource-based indicators. In this newly developed protocol, we found that some indicators are difficult to assess with accurate results, especially in wild animals, when they are kept in large enclosures with dense vegetation. Although we used binoculars to assess integument and skin deformities (indicator 7.1), it was difficult to determine if there were any small lesions or patches on the body. According to [46
], there is a high possibility of high levels of aggression and fights in wild ungulates in captivity. Detailed observations of skin and other integuments are thus very important. We do not encourage excluding this indicator; rather, we suggest the use of more powerful binoculars or a high-resolution camera to obtain clear pictures of the animals.
Our protocol is based on the welfare protocol for domestic sheep, but we excluded the criteria ‘positive emotional state’. There is a lack of information relative to this subject in captive ungulates [10
]. This state includes pleasure, comfort, confidence, and interest. The aim of animal welfare assessment is to determine positive emotional states, or reduce undesirable experiences and increase opportunities for animals to have more healthy and positive states [47
]. We suggest that these criteria should be included in developing welfare assessment protocols for any wild species in captivity.
An emerging trend in establishing zoos and enclosures is to provide large and more natural environments for captive animals [48
]. The current protocol found the area requirements for captive Punjab urial very true-to-life and acceptable in each of the three enclosures examined. All three enclosures offered vast areas to the animals, with natural habitats utilizing natural vegetation and uneven ground. All the animals could easily experience grazing, browsing, and athletic activities. With the exception of CU1, where animals were observed to be moving back and forth and the enclosure is located in close proximity to local settlements and roads, so stereotypic behavior was recorded during the application of the current protocol. According to [49
], eye contact of visitors and wild animals in captivity can result in stress and stereotypic behavior. Following [34
], fences at CUI should be covered with raffia in order to avoid frequent eye contact between the animals and the public.
Interspecific aggression has been mostly documented in carnivores [50
], while such information for wild ungulates is scarce [51
]. Interspecific aggression can possibly increase intraspecific aggression. In our study, we found that animals in CU3 showed the highest aggression (66.59%), followed by CU1 (43.64%) and CU2 (37.75%). We assumed that the higher aggression in CU3 was due to the presence of other species [52
]. Punjab urial males were frequently observed chasing chinkara, showing comparatively less aggression toward mouflon sheep. We also recorded counter aggression from chinkara males toward Punjab urial and mouflon sheep. According to [36
], interspecific aggression is usually greater between distantly related species than closely related species, and it is recommended to separate the species with aggressive males. Our results suggested isolating chinkara from Punjab urial. Regarding stereotypic behavior, it was observed only in three animals (two adult females and one subadult male) at CU1. This facility had less natural vegetation as compared to the other two facilities, where the animals did not show any stereotypic behavior. According to [45
], captive ungulates have a high tendency to produce oral stereotypies when they have limited opportunities for natural foraging; those findings are in agreement with results produced from the current study.
Recently, medical training programs and training techniques have been practiced and understood in modern zoos and facilities. These methodologies are frequently used and applied in different species, including big cats, elephants, giraffes, and apes. There is a lack of implementation of such programs in ungulates [10
]. We consider it important to add a medical training program (12.2) because, if properly practiced, it is a promising means of reducing the stress caused by veterinary techniques. For capture of animals, every facility must have the right material (capture enclosure, net, handling crush, and dart gun), coupled with an experienced team, in order to avoid trauma and other serious injuries [34
]. During application of the proposed protocol, it was found that several animals had expired during capture and translocation. These results make the medical training program a top priority in Punjab urial and other associated captive ungulates.
The development of this welfare assessment protocol is a leading documented work in developing a scientific and standard tool for the measurement of welfare in Punjab urial (Ovis vignei punjabiensis
). Using the Welfare Quality®
protocol for farm animals as a reference, welfare assessment protocols for several wild species have been developed, including those for mink (Neovison vison
), foxes (Vulpes
], dorcas gazelles (Gazella dorcas
], and bottlenose dolphins (Tursiops truncatus
Welfare assessment protocols are developed with the aim of assessing the welfare level in captive animals, to discover limitations in captive breeding, and to ensure optimal welfare through recommendations. Protocols that are practical and easy to be applied are considered successful protocols. Protocols developed for different species differ in terms of time for their implementation. In the case of mink and foxes [47
], the developed welfare assessment protocol needs three visits to each farm. In the case of bottlenose dolphins [53
], the protocol requires two days for a complete welfare assessment of a dolphin pod including up to 10 individuals. Our protocol includes an extensive set of 31 indicators, and thus has some practical challenges. According to [10
], protocols for dorcas gazelles require less than 6 h per herd. During the application of the proposed protocol, the largest herd of Punjab urial (n
= 23) was assessed at CU1, and all the indicators were assessed in 5 h per herd. Our protocol is in early-stage development for assessing the welfare in captive Punjab urial and endorsement is still needed; however, its application to the three different herds and the results obtained allowed to identify some areas in all the facilities which need to be improved.
Using the welfare assessment protocol for farm animals (sheep) as the base, we developed a welfare protocol for welfare assessment in captive Punjab urial (Ovis vignei punjabiensis). This first specific protocol developed for Punjab urial comprised 4 basic principles, 12 criteria, and 31 animal- and environmental-based indicators. Although this protocol still needs validation, its first application and subsequent results obtained from three different herds of captive Punjab urial at CU1, CU2, and CU3 highlight some areas where improvements are essential. According to the results obtained from this protocol, handling, capturing, and translocation were found to be the most important areas for necessary action as most of the mortalities happened in capturing and translocation. Another important area which needs to be improved on an urgent basis is the availability of veterinary facilities. Furthermore, we recommend the shifting of breeding animals between different populations. Based on the results, we recommend covering the fence at CU1 in order to prevent frequent human–animal eye contact. On the basis of this study results, we believe that this protocol can be a promising tool for welfare assessment at facilities that hold Punjab urial. The current protocol has the best combination of welfare indicators for the target species and is a leading step in captive breeding research in Pakistan. In addition, this protocol can be used as a base for developing similar welfare protocols for other captive mountain ungulates in Pakistan and globally.