Gastrointestinal Parasites of Captive and Free-roaming Primates at the Afi mountain Primate Conservation Area in Calabar, Nigeria and their Zoonotic Implications

Mbaya, A.W.; Udendeye, U.J.

INTRODUCTION

Wild primate population, as members of biologically diverse arboreal or terrestrial habitats are regarded as major source of emerging infectious diseases and may hold valuable clues to the origins and evolutions of some important zoonosis (Wolfe et al., 1998). Primates over the years have been identified as reservoirs of human gastrointestinal parasites (Soulsby, 1982). The anthropoid primates and to a lesser degree simian primates share broadly similar physiologic and genetic characteristics and thus susceptible to gastrointestinal parasites (Wolfe et al., 1998). The ability of parasitic infections to cross primate-species boundary to affect man has been documented (Brack, 1987; Jin et al., 1994). Since primates live in game reserves or National parks in tropical rain forests, the degree of interactions between primates and humans occur in this high-risk interface (Meslin, 1992; Turner, 1996; Wolfe et al., 1998). Similarly, handling of primates in zoological gardens or through pet trade in new world monkeys could lead to the transfer of parasitic zoonosis. Although primates act as reservoir of common gastrointestinal parasites of man without manifesting obvert clinical signs (Nwosu, 1995; Mbaya et al., 2006b), severe outbreaks of clinical amoebiasis, trichurosis and balantidosis have been reported in a colony of captive chimpanzees (Pan troglodytes) in Sanda Kyarimi Park, Maiduguri Nigeria (Mbaya and Nwosu, 2006; Mbaya et al., 2006a). In view of the prospects of emerging infectious diseases from primates to man or vice-versa, the search for answers is usually turned to the non-human primate as a sentinel. This study was therefore, designed for the first time in Nigeria, to investigate the gastrointestinal parasitic infections of primates at the Afi Mountain Primate Conservation Area in Calabar, Nigeria and their possible zoonotic implication on one hand and the conservation of the primates on the other hand.

MATERIALS AND METHODS

Study area: The primate preserve, where this study was conducted is located in the Afi mountain Wildlife Conservation Area in Calabar, Nigeria, occupying 1.6 km square of the about 100 km square of the wildlife sanctuary. The area lies between Latitude 5’ N and longitude 8’ E in Boki local Government Area, North of Calabar, Nigeria. It contains a number of spatially separate captive or free-roaming primate colonies. Each colony consist of multiple primate species such as the chimpanzee (Pan troglodytes), mandrill (Mandrillus sphinx), drill (Mandrillus leucophaeus), mona monkeys (Cercopithecus mona), spot-nosed guenons (Cercopethicus nictitans), white-collared mangabey (Cercocebus torquatus) and Sclater’s white-nosed monkey (Cercopethicus erythrotis sclateri) in a very rich biodiversity of undisturbed ecosystem. The primates in captivity were fed on fruits and vegetables and water was provided ad-libitum while their free-roaming counterparts fed on twigs, fruits, vegetables, root barks and termites at specific periods of the year and drink water from rivers within the preserve. Non-governmental organizations (Cercopan) and (Pandrillus) were actively involved in the conservations of orphaned primates that were victims of habitat loss and the ever-increasing bush meat trade in Nigeria. They provide captive environment that mimic the primates natural habitat with a view of re-introducing them into the wild.

Sample collection and examination: The study involved 108 primates, with 49 under captivity and 59 under free-roam. No form of capture whatsoever was involved during the study. Similarly, the Ethical and Animal Welfare Committee for the use of animals for Biomedical Research of the Faculty of Veterinary Medicine University of Maiduguri, Nigeria and The Nigerian National Parks Service approved the research. The various captive primate groups were monitored daily and freshly passed faecal samples collected from their cages. Meanwhile, faecal samples from the free-roaming primates were randomly collected opportunistically as they were dropped. The samples were labeled, according to captive or free-roam status, species, sex and age. The samples were subjected to direct smear to establish the presence of gastrointestinal parasitic infections and transported to the Parasitology laboratory of the University of Maiduguri, Nigeria and subjected to concentration by floatation technique (Soulsby, 1982). Egg counts per gram of feces (epg) and oocyst counts per gram of faeces (opg) were determined by the modified McMaster technique using saturated sodium chloride solution as floating medium (Soulsby, 1982). Identification of helminth ova and oocysts were done by standard parasitological criteria (Soulsby, 1982; Smyth, 1994; Urquhart et al., 1996; Lynne and David, 2005). Modified Baerman’s technique for larval isolation and identification of helminthes and sporulation of oocysts of protozoa was carried out for identification of the species using standard parasitological criteria (Soulsby, 1982; Smyth, 1994; Urquhart et al., 1996; Lynne and David, 2005).

Statistical analysis: Data obtained were either summarized as Means±Standard deviation or percentages and the difference between means were determined using the t-test at the 5% level of significance (Mead and Curnow, 1983).

RESULTS

The prevalence of gastrointestinal parasites as well as the various species of parasites with their respective worm burdens in the various captive and free roaming primate colonies examined at the Afi Mountain Wildlife Sanctuary in Calabar, Nigeria, is presented in Table 1. Out of 108 primates examined, 75 (69.44%) were found to be shedding the ova and oocysts of at least one specie of gastrointestinal parasite in their faeces. Although the prevalence of infection was generally high irrespective of species, the mona monkeys (Cercopethicus mona) 16(80%) followed by the white-collared mangabey (Cercocebus torquatus) 7 (77.78%) had the highest prevalence of infection (p<0.05) but with few species of parasites among other primate groups. Meanwhile, the chimpanzees (Pan troglodytes) had the highest variety of gastrointestinal parasites such as Ascaris lumbricoides 5 (21.74%), Trichuris trichiura 6 (26.17%), Balantidium coli 2 (8.70%), Enterobius vermicularis 2 (8.70), Entamoeba histolytica 2 (8.70%), Strongyloides stercoralis 3 (13.04%), Blastocystis hominis 3 (13.04%), Hymenolepis nana 5 21.74%), Schistosoma mansoni 10 (43.48%), Ancylostoma duodenale 2 (8.70%) and Cryptosporidium species 5 (21.74%). This was followed by the drill (Mandrillus leucophaeus) which mainly had Ascaris lumbricoides 5 (55.56%), Ancylostoma duodenale 2 (22.22%) and Strongyloides stercoralis 2 (22.22%). The mandrill (Mandrillus sphinx) had Ascaris lumbricoides 6 (50%), Ancylostoma duodenale 6 (50%) so also did the spot-nosed guenons (Cercopethicus nictitans) which had Ascaris lumbricoides 5 (100%) and Ancylostoma duodenale 5 (100%) while the Sclater’s white-nosed monkey (Cercopethicus erythrotis sclateri) and the white-collared mangabey (Cercocebus torquatus) had only Ascaris lumbricoides with 3 (100%) and 7 (100%) prevalence rates, respectively.

Table 1:	Various species of gastrointestinal parasites of captive and semi-captive primates and their associated worm burden at the Afi Mountain Primate Conservation Area in Calabar, Nigeria

Values with different superscripted in columns differed significantly (p<0.05)

Table 2:	Comparative prevalence of gastro intestinal parasitic infections between captive and free-roaming primates examined at the Afi Mountain Primate Conservation Area Calabar, Nigeria

Values with different superscripted in rows differed significantly (p<0.05)

Table 3:	Prevalence of gastrointestinal parasitic infections of primates examined at the Afi Mountain Primate Conservation Area in Calabar, Nigeria according to sex

Values with different superscripted in rows differed significantly (p<0.05)

Similarly, egg or oocyst counts were significantly high (p<0.05) and ranged between 300.0±0.25 to 500.0±0.16 among the chimpanzees (Pan troglodytes) as compared to the other primate groups.

The comparative prevalence of infection between the captive and free-roaming primates is presented in Table 2. All captive primates irrespective of species had significantly (p<0.05) higher prevalence of infection as compared to those roaming freely in the sanctuary. The prevalence of infection between sex and age among the primates are presented in Table 3 and 4.

Table 4:	Prevalence of gastro intestinal parasitic infections of primates examined at the Afi Mountain Primate Conservation Area Calabar, Nigeria according to age

Values with different superscripted in rows differed significantly (p<0.05)

The females irrespective of species had higher prevalence (p<0.05) of infection than the males, similarly, the young primates (<12 months) of age had significantly (p<0.05) higher prevalence of infection than the adults (>12 months) of age.

DISCUSSION

The results of the study revealed that primates at the Afi Mountain Primate Conservation area, located in the rain forest region of eastern Nigeria, harboured a variety of potentially pathogenic gastrointestinal parasites of zoonotic importance (Soulsby, 1982; Lynne and David, 2005). Some of the parasites encountered in this study have been reported among primates elsewhere in the world (Looms and Wright, 1986; Brock-Utne et al., 1988). They have also been reported in a reservoir status among captive primates in the arid zone of northeastern, Nigeria (Nwosu, 1995; Mbaya et al., 2006b) or in the southwestern, Nigeria (Okon and Dipeolou, 1975; Bamidele and Ogunrinade, 1980) and in few fatal cases (Emikpe et al., 2002). However, Blastocystis hominis, Enterobius vermicularis, Schistosoma mansoni and Strongloides stercoralis encountered during this study are being reported for the first time among chimpanzees (Pan troglodytes) in Nigeria. Ascaris lumbricoides and Ancylostoma duodenale were however, the most common parasites encountered among the various primate species. Some of the parasites such as Balantidium coli, Entamoeba histolytica and Trichuris trichiura have been associated with severe outbreaks in a colony of captive chimpanzees (Pan troglodytes) in Sanda Kyarimi Park in the arid zone of northeastern Nigeria (Mbaya and Nwosu, 2006; Mbaya et al., 2006a, b). Similarly, Balantidium coli were reported concurrently with Ancylostoma species, Enterobius species and Strongyloides in a red pattas monkey (Erythrocebus pattas) in the University of Ibadan Zoological Garden in Western, Nigeria (Adedokun et al., 2002). The outbreak reported among the captive chimpanzees (Pan troglodytes) in Sanda Kyarimi Park, Maiduguri, Nigeria was however, traced to a human attendant who was found to be shedding trophozoites and oocyst of Entamoeba histolytica, Balantidium coli and ova of Trichuris trichiura in his faeces (Mbaya and Nwosu, 2006; Mbaya et al., 2006a). In this present study, however, human faecal samples could not be obtained from game wardens or attendants due to cultural reasons. It is therefore, clear from the findings of this study that the parasites encountered in this primate preserve are zoonotic and may be potential sources of human infections or of future outbreak among the primate colonies in the sanctuary. The public health importance of Trichuris species was extensively reviewed (Okon and Dipeolu, 1975; Chang and McClure, 1975). However, that the primates living in absolute captivity had higher prevalence of infection than their counterparts on free-roam may be a reflection of captivity on the host-parasite relationship (Soulsby, 1994). Many gastrointestinal parasites of primates occur sporadically and appear to exist in balance with the host. When this equilibrium is disrupted by diverse stress factors as obtained in captivity, clinical disease and mortality ensue. Previous studies have shown that animals ordinarily presumed to have specific resistance to parasites while on free-roam in the wild usually harbour higher prevalence and burdens of the same parasite when subjected to captivity (Nwosu, 1995; Mbaya et al., 2006b). Confinement predisposes to the build up of high concentrations of infective stages of gastrointestinal parasites within primate housing in contrast, large expanse of land available for roaming in conservation area often ensues a wider dispersal of infective parasite stages and hence a reduction of the primates roaming freely to infection (Nwosu, 1995). This may therefore, account for the lower prevalence among the free roaming primates than among their captive counterparts. Captive form of conservation (ex-situ) in wild animals is generally, accompanied with severe stress with resultant increased corticosteroid out put, which in turn compromises their innate resistance through immunosuppression (Mbaya, 2007). This may therefore, further explain why Cryptosporidium oocyst was encountered among the captive primates. Cryptosporidiosis has been reported to occur in immunosupressed or immuno deficient individuals (Lynne and David, 2005). This agrees with the occurrence of cryptosporidiosis among captive wild animals and birds in the arid region of northeastern Nigeria (Ibrahim et al., 2007). Similarly, it will be expected that those primates in free-roam, may have lower prevalence of infection because recent evidences have suggested that wild primates in their natural habitat, often self medicate themselves with medicinal plants in their environment (Clayton and Wolf, 1993; Robles et al., 1995). The effect of age on the prevalence of infection among the primates in the Afi Mountain Primate Conservation area, however, showed that the young primates (<12 months) had higher (p<0.05) prevalence of infection as compared to the adults (>12 months) of age in the conservation area. This could be due to age susceptibility and lack of premunity in the young (Soulsby, 1982). Comparison of the prevalence of gastrointestinal infection among different sex groups, also showed a significant statistical variation (p<0.05) with a higher prevalence of infection among the females as compared to the males. This might be associated with the fact that primates generally live in social groups, where the bond of social interaction and ‘social grooming’ exist more commonly between the young and females thereby facilitating cross transmission of infection between them as compared to the males which usually assumes a more solitary defensive role in the colony. In conclusion, therefore, this study is important in being the first to be undertaken among primates in the Afi Mountain Primate Conservation Area in Calabar, Nigeria. The results also showed that the primates harboured various gastrointestinal parasitic infections of zoonotic importance. However, Blastocystis hominis, Enterobius vermicularis, Schistosoma mansoni and Strongloides stercoralis encountered during this study are being reported for the first time among chimpanzees (Pan troglodytes) in Nigeria. This may therefore, provide valuable clues to the origins and evolutions of some important zoonosis in the area. Similarly, captive primates, females and the young were significantly more infected than their counterparts were. These may provide useful information towards more effective primate conservation goals. It was therefore, advised that strategic and sustained broad-spectrum anthelminthic therapy be routinely carried out among the captive primates before re-introduction in to the wild.

ACKNOWLEDGMENT

The effort and support of the management and staff of Cercopan and Pandrillus primate conservation groups in Calabar, Nigeria are highly appreciated. Grants from University of Maiduguri Central Research Committee supported this study.