A zoological garden is a form of ex situ conservation, which primarily involves keeping wild animals alive outside their natural environment for aesthetic, educa-tional, research and recreational purposes (Varadharajan and Pythal, 1999).

Nigeria is blessed with abundant wildlife species which need to be properly managed on a sustainable basis to prevent depletion (Opara et al., 2010), hence the need to adopt strict management of these resources. Repopulation of endangered species and conservation of wild animals in wildlife parks and zoological gardens are management strategies (Ajibade et al., 2010). Parasites play a major role in the lives of animals, with effects ranging from negative impacts on host population size to the evolution of host behaviours to combat parasites. Parasitic diseases constitute one of the major challenges in wild animals in captivity (Adedokun et al., 2002; Emikpe et al.,  2002;  Singh  et  al.,  2006;  Emikpe  et  al.  2007).

In the wild, animals might have a natural resistance against parasitic infections or live mutually with their parasites (Borkovcova and Kopriva , 2005).  Change in environment and living conditions from freedom to cap-tivity influences the animals’ ecology and might increase the susceptibility to parasitic infections (Goossensa et al., 2005; Singh et al., 2006).  Many of these animals are exotic to the geographical location of the parks and zoo gardens where they are kept.  So also, keeping animals in captivity aggregates a number of species of animals in close proximity. Proximity provides opportunity for the transmission of diseases or parasites to species which would not normally come in contact with such pathogens (Moudgil and Singla, 2013). Severe parasitoses can lead to blood loss, tissue damage, spontaneous abortion, congenital malformations and death (Adedokun et al., 2002; Emikpe et al., 2002; Despommier, 2003; Emikpe et al., 2007).

Another possibility of parasite transmission is when ani-mals are moved from one enclosure to another, without proper parasite treatment. Mixing different species brings additional risks of parasitic infections (Goossensa et al., 2005). Zoological garden staff members have also been reported to play an important role in the transmission of parasites amongst animals in zoos, through their shoes, clothes, hands, food or with working tools (Adetunji, 2014; Otegbade and Morenikeji, 2014).  Most of these parasites are zoonotic and pose a serious threat to human health (Kashid et al., 2003).

Carnivorous animals act as definitive hosts for many intestinal parasites, some of which are responsible for several zoonotic diseases like ancylostomosis, echinococcosis, gnathostomosis and toxocarosis (Schantz and Kramer, 1995; Eslami and Hosseini, 1998).  Overgaauw (1997), further suggested close interaction between humans and carnivores as reasons for endemicity of these zoonotic parasites.

Inadequate information on diseases and parasites of zoo animals is a major limiting factor in the management of zoological gardens. Investigations into prevalence, geographical distribution, systematic and biology of parasites of zoo animals are important for planning and control of parasitoses. Hence, the need for a regular program of gastrointestinal parasite surveillance and measures of control based on correct diagnosis, effective treatment and proper prophylaxis to ensure sound health of zoo animals (Ajibade et al., 2010;  Moudgil et al., 2014). This study aims to establish the profile of gastro-intestinal parasites in carnivores in three zoos in Nigeria.

Study area

This study was carried out in the zoological gardens of three Southwestern Universities in Nigeria: the University of Ibadan Zoological Garden (UI Zoo), Ibadan which lies on latitude 7°26´ N and longitude 3°53´ E; Obafemi Awolowo University Biological gardens (OAU Zoo), Ile Ife (7.4667°N, 4.5667°E) and University of Ilorin Zoological Garden (UNILORIN Zoo), Ilorin (latitude 8°30 and longitude 4°35´ E). The zoological gardens have several different sections and the animals are put in sections by species. Indoor and outdoor enclosures are cleaned on a routine basis with necessary prophylaxis. Animals are regularly dewormed in some zoos to curb parasitic infections. Natural features, such as branches, climbing structures, and platforms are used for enrichment of enclosures to promote animal well-being. Carnivore species, such as lions, are housed in large closed circuit enclosures for the safety of visitors and tourists (Table 1).

Collection of samples and coprologic examination

Fresh faecal samples were collected in triplicates from the carnivores between March, 2012 and May, 2012 to examine for gastrointestinal parasites. Samples were collected in plastic vials, which were clearly marked with the time and date of collection, species of the animal, and the animal’s cage number. All samples were transported to the laboratory, and examined within 48 h. The faeces were examined macroscopically for consistency, presence of blood, mucus, tapeworm proglottids and larval nematodes. Examination for parasite eggs and larvae was by standard methods. Qualitative egg identification was done by floatation technique using a saturated solution of zinc sulfate (703 g/l, specific gravity 1.18) as the floating solution, McMaster Egg Counting Technique for quantitative ova examination while larva culture was done using the petri dish- filter paper slant culture technique (modified Harada- Mori Technique) as described by Garcia (2001). Some quantity of each faecal sample was cultured for 10 days to harvest and identify helminth larvae (Soulsby, 1982). Larvae that emerged were subsequently recovered for identification using typical morphological features (Sloss et al., 1994

Statistical analysis of data

Descriptive statistical analysis was used to summarize the results as percentage, means and standard deviations and differences between the means were determined using the analysis of variance (ANOVA) at the 5% level of significance. 

Study population

A total of 35 carnivorous animals of two families, Canidae and  Felidae  were  present  in  the  three

zoological gardens (Table 1).

Prevalence of helminth parasites in the zoological gardens

Of all the faecal samples collected (108), 53 (49.1%) were found infected. The prevalence of gastrointestinal parasites in the samples examined comprises UI - 23.7%, OAU - 54.8%, UNILORIN - 69.2% (Table 2). Ascaris sp. was found in 12 (22.6%), Ancylostoma sp. in 11 (20.8%), Baylisascaris sp. in 7 (13.2%), Toxascaris sp. in 9 (17%), Toxocara sp. in 5 (9.4%), and Strongyloides sp. in 7 (13.2%). None was found infected with tapeworms.

Distribution of parasites in the zoo animals

In UI Zoo, not all the animals sampled were infected. Infections were found only in some samples collected from hyaenas and jackal and these were infected with Ancylostoma sp. and Baylisascaris sp. respectively (Table 3). In OAU Zoo, parasites were identified in most samples, with Fox having the highest prevalence rate of 100%. The foxes were infected with Toxocara  sp. were infected with more types of parasites (Ascaris sp, Toxascaris sp and Strongyloides sp) even though their prevalence was not  as  high  as that of the foxes.

In University of Ilorin Zoo, infections were found in some samples collected from all the animals except the fox. All the stripped and spotted Hyenas, and Civet sampled were 100% infected, but the lions were infected with more types of parasites (Table 3).

Intensity of gastrointestinal parasites in the carnivorous animals

There was no significant difference in the intensity of Ancylostoma sp (100.0 ± 0.50) and Baylisascaris sp (83.0 ± 0.33) discovered in UI (P>0.05), also, no significant difference in the intensity of the different parasites (Ascaris sp 90.0 ± 0.19, Toxascaris sp 66.7 ± 0.17; Strongyloides sp 100.0 ± 0.50) found in OAU zoo. The number of Toxacara sp (25.0 ± 0.25) found in OAU was significantly lower than other parasites discovered (P<0.05).

This study showed the types, prevalence and intensity of gastrointestinal parasites in carnivo-rous animals in three strategic zoos in South West Nigeria.  Ascaris sp, Toxascaris sp, Strongyloides sp, Baylisascaris sp, Ancylostoma sp, Toxacara sp  and Entamoeba sp were the parasites identified in different carnivores. All the parasites recovered from the various species of carnivores were also earlier reported in Nigerian captive animals (Parsani et al., 2001; Ajibade et al., 2010; Opara et al., 2010).

The observed total prevalence of 49.1% is in agreement with the studies of Atanaskova et al. (2011) in Skopje, Macedonia and Lalosevic et al. (2007) in Palic Zoo in Serbia. However, pre-valence observed in the present study was lower than that reported by Ajibade et al. (2010) and Opara et al. (2010) with prevalence rates of 62.5 and 61.5% respectively. Among individual parasi-tic infections, the study revealed infection of 22.6% for Ascaris sp, 13.2% for Strongyloides sp, 20.8% for Ancylostoma sp and 3.8% for Entamoeba sp. The observation was in agree-ment with the findings of Opara et al. (2010) who recorded a higher prevalence of helminthes (82.2%) and protozoan (17.8%) (Entamoeba and Giardia species) parasites in zoo captive animals.

This study also showed that parasitic diseases are common to zoo carnivores in countries of warm and tropical climates due to the factors that favor the development of parasites such as light, temperature and humidity (Magona and Musisi, 1999; Opara et al., 2010).  Attendants cleaning the cages and enclosures of these animals could act as a vehicle (formite) for cross transmission. Also, the animals serve as potential reservoirs that could transmit gastrointestinal protozoans and helminths to zoo keepers and possibly to visitors.

This study further shows the need for a well-adjusted anthelmintic program, such as early season treatments to prevent infection in wildlife species under captivity, regular passive surveillance for parasitic infections and effective treatment programs.

The authors declare that they have no conflicts of interest.