Study on Gastrointestinal Parasitism of Wild Animals in Captivity at the Zoological Garden of Haramaya University, Ethiopia

Captivity of wild animals and restriction of their movement can lead to stress, resulting in suppressed immune response and reduced disease resistance ability. Wild animals in zoological gardens can predominately affected by various gastro-intestinal parasites. This study was therefore, conducted to determine occurrence, identify types and assess seasonal variation of gastrointestinal parasites in captive animals at the Zoological garden of Haramaya University. The study involved a retrospective investigation of zoo records and fecal examinations. Twenty two fecal samples were collected in December, 2013 from all the animals in the garden and examined using concentration and fecal culture techniques. Sampling was repeated after four months in April, 2014 to assess seasonal variations of the parasites. The result from the retrospective study showed death of 21 animals in the last five years. Fecal examination confirmed presence of gastrointestinal parasites with an overall mean prevalence rate of 73.8%. A total of 9 parasite taxa were identified of which 6 (66.67%) and 4 (33.33%) were helminths and protozoa respectively. No Cestode and Trematode species were recovered. Trichuris spp., Toxocara spp., Strongyloides spp., Toxascaris leonine, Passalurus ambiguous and Ascaridia spp. were the helminth parasites observed in the garden. Entamoeba spp., Isospora spp. and Eimeria spp. were the protozoan parasites encountered. No remarkable seasonal variation in parasitic infection was noticed in the garden. The study revealed occurrence of gastrointestinal parasites in the zoological garden, most of which are zoonotic and hence future studies are needed to determine risks of cross-transmission.


Introduction
Large populations of wild animals in captivity are affected by various diseases.
Parasite infections are one of the major problems in the wild animals in captivity. Gastrointestinal parasites are frequently reported to affect the health and the wellbeing of the animals in zoological gardens [1]. The species of the gastrointestinal parasites infecting wild animals in captivity might differ with the type of animals and the management practices [2] [3].
In captivity, animals appear to be less resistant to parasitic infections than under their natural habitats [4]. The changes in environment and living conditions from the natural habitat to captivity alter the life styles of animals, reduce disease resistance ability and increase their susceptibility to parasitic infections [5] [6] [7]. Vulnerability of captive wild animals to parasitic infections depends on factors, like feeding, keeping conditions, animal management and environmental conditions, such as temperature and humidity. Confining captive animals in cages accompanied with improper feeding systems and poor sanitation may lead to contamination of environment, which makes the animals more prone to different parasitic infections [4] [6] [8] [9]. Proximity and close contact of humans with captive animals provide opportunity for the transmission of new parasite species which would not normally come in contact with them in the natural habitat [10]. Most of the deaths of wild animals in controlled areas are amounted to parasitic diseases. Parasitism, especially endoparasitic infection produces ill effects like weakness, emaciation, inappetance in zoo animals that can cause immune suppression and potentially predispose the animals to other diseases [11].
Although many parasitological investigations are conducted in domestic animals for long period of time, it has been recently recognized that parasitic infections are also common and important in wild animals [12] [13]. Incidence of gastrointestinal parasites in wild and zoo animals has been reported from different parts of the world [9] [14]. Several studies have been carried out on gastro-intestinal parasites in non-human primates [15]  There are incidences that the health problems and death of the zoo animals is usually connected with infection of gastrointestinal parasites. However, the attention given to investigate and document the type of gastrointestinal parasites infecting zoo animals in the country in general and at Haramaya University in particular is minimal. This study was therefore conducted to determine the occurrence, identify species and assess seasonal variation of gastrointestinal parasites in captive animals at the Zoological garden of Haramaya University.

Description of the Study Area
The study was conducted at the Zoological garden of Haramaya University, In the garden, animals are housed in different cages individually and/or in small groups based on species and age of the animals.

Study Methodology
The study involved observation of the general management practices and retrospective investigation of zoo records, detection and identification of the parasites infecting the animals at the zoological garden. Fecal samples were analyzed for the presence and identification of nematodes, cestodes and protozoan oocysts. Samples from the East African Giant Tortoise (Geochelone sulcata) were excluded due to the failure to obtain fresh samples.

Fecal Sample Collection
Twenty two fresh fecal samples were collected from eight species, consisting of

Identification of Parasite Oocyst
Zinc sulphate centrifugal floatation technique was used for the identification of  scope slides and examined. The identification keys described in Soulsby [28] and van Wyk and Mayhew [31] were employed to identify the larvae.

Results and Discussion
The data from retrospective study indicated that most of the disease cases of wild animals at Zoological garden of Haramaya University were related to parasite infections. Records revealed the death of 21 animals over the last five years (

Occurrence of Gastrointestinal Parasites
Out

Identification of Species of Gastrointestinal Parasites
The species of gastrointestinal parasites detected in the zoological garden is shown in Table 3. A total of 9 parasite taxa were identified both in December and in April, of which 6 (66.67%) and 3 (33.33%) were helminthes and protozoa respectively ( Among the helminths in the zoological garden, Trichuris spp. had the highest prevalence (46.67%) followed by Toxocara spp. (20%) in December. Trichuris spp. had similar position in April (46.15%) followed by Strongyloides spp. (23.08%). On the other hand, Eimeria spp. (60%) were found predominant protozoan parasite in December while Entamoeba spp. (50%) took the lead in April (Table 3).
Mixed infections were noticed in some of the animals both in December (25%) and April (20%). Mixed cases of helminthes such as Trichuris spp. and Strongyloides spp. in Hamadryas baboons and Trichuris spp. and Toxocara spp. in kit foxes were observed in the garden. Similarly, combinations of helminths and protozoan infections including Trichuris spp. with Entamoeba spp. in Hamadryas baboons; Toxascaris leonine with Isospora spp. in lions; Passalurus ambiguus with Eimeria spp. in rabbit and Ascaridia spp. with Eimeria spp. in helmeted guinea fowl were also observed in some animals (Table 3). In agreement with this study, many previous works reported mixed infections in wild animals in captivity [7]. Otegbade and Morenikeji [26] reported that that mixed infections may consists of two or more parasites.
The present study revealed that nematodes take the entire share of infection  (100%) among the helminth parasites encountered. There were no cestodes and trematode species recovered from the fecal samples which agrees with the result of Bezjian et al. [34], who reported that no parasites eggs found by sedimentation from forest baboons at Kibale National Park, Uganda. Similarly, Singh et al. [22] reported that nematodes had the highest prevalence among the helminthes recovered in captive wild animals. The high percentages of helminths compared to protozoan parasites can also be supported by the report of Varadharajan and Kandasamy [2], who found about 58% helminth parasites and 6% protozoan infections in wild animals at V.O.C. Park and Mini Zoo, Coimbatore, India.
Most of the gastrointestinal parasites observed in this study had also been reported by several authors. The occurrence of Trichuris and Strongyloides spp. in captive wild animals were reported by Opara et al. [35]. Trichuris trichuira and Entamoeba spp. in non-human primates were reported to be more prevalent [10] [15] [19] [36]. The incidence of Toxocara cati and Toxascaris leonine in Lions in the current study was supported by Okulewicz et al. [37], Pawar et al. [38], Mukarati et al., [39]. In line with the present study Engh et al. [40] reported that Toxocara canis was infecting hyena in the Masai Mara national reserve of Kenya while Luty [41] recovered it in the feces of foxes in the University zoological garden of south western Nigeria. The presence of Passalurus ambiguous and Eimeria perforans from white rabbit was also reported by Okumu et al. [42]. Several reports revealed Ascaridia spp. to be more prevalent in birds, particularly in helmeted guinea fowl [26] [43] [44].

D. Dashe, A. Berhanu Open Journal of Veterinary Medicine
Overall, the high incidences of the same species of parasites among the animals in the garden indicated that there was a share the parasites between the animals in the garden. The introduction of large numbers of visitors to the animal habitats and the closeness of humans to the animals, particularly non-human primates in the zoological gardens might have caused the exchange of parasites between humans and animals. The presence of Trichuris, Strongyloides and Toxocara spp. in high numbers in the animals in the current study may be due to the contact with human beings as these species of helminthes are more likely to be transmitted from humans to animals. The spread of gastrointestinal parasites among zoo animals by zoo keepers were reported by several authors [16] [26] [35]. Arafa et al. [45] reported that unhygienic zoo keepers can potentially transmit parasites between the animals especially when the life cycle is direct.
Calvignac-Spencer et al. [46] stated that people who share the same habitat with nonhuman primates are considered as potential sources of transmission. Prevalence of zoonotic gastrointestinal parasites was reported in Papio anubis (baboon) and Cercopithecus aethiops (vervet) in Ethiopia [47]. Maske et al. [14] and Kashid et al. [9] reported that parasites can be transmitted from wild animals to domestic animals and man and vice-versa.

Seasonal Patterns of Gastrointestinal Parasites in the Garden
The pattern of parasitic infection in the garden was found nearly the same throughout a year. Examinations conducted on fecal samples during dry and wet seasons indicated that there were no marked differences in the infection rates of parasites. The number of animals infected in December (72.72%) were slightly lower than the number infected in April (75%). On the other hand, the species and number of the parasites found was almost similar both in December (dry season) and April (a wet season). This showed that the seasonal variation in parasitic infection among the zoo animals in the garden is not remarkable. The finding was in agreement with the report of Gillespie et al. [48], who reported that seasonal variation in parasite infections was minimum. This minimum variation in parasite loads between these seasons in the zoo may indicate that the animals are kept constantly in a contaminated environment with the parasites which was also stated by Atanaskova [4]. It can also be explained that in natural environments, wild animals live on large areas and have a low genetic resistance against parasitic infections because of low exposure. However, when the wild animals are kept in captivity in zoological gardens, the problem of parasitic infections can aggravate which agrees with the observation of Muoria et al. [49]. The study showed that most of the gastrointestinal parasites of wild animals examined may be zoonotic and hence future studies are needed to determine risks of cross-transmission.