Smith_ResC_71-75.indd INTRODUCTION Little data are available on the endoparasites car- ried by free-ranging African lions (Panthera leo) in the Kalahari Desert. What is available stems from East Africa (Müller-Graf 1995; Müller-Graf, Wool- house & Packer 1999; Bjork, Averbeck & Stromberg 2000) or are anecdotal records from dead lions (Le Roux 1958; Rodgers 1974) or institutions where they were held captive. Parasites are known to in- fluence fitness and, more recently, have also been shown to influence behaviour (Zimmer 2000). The endoparasitic taxa carried by each individual in the pride are influenced not only by how pride members associate, but also by the general health of the indi- vidual, the size of the parasite suprapopulation as well as ecological factors. Here we report on the endo parasites of a small pride of lions in the south- western Kalahari, Namibia, as determined by oppor- tunistic collection of faeces during field ob serva- tions. MATERIALS AND METHODS Research subjects A small pride of lions on the western fringe of the Kalahari Desert in southeastern Namibia was stud- ied. The pride was held in a 500 ha enclosure on a private reserve, Intu Afrika Kalahari Game Reserve (24°33’ S, 18°31’ E), situated approximately 60 km 71 Onderstepoort Journal of Veterinary Research, 73:71–75 (2006) RESEARCH COMMUNICATION Faecal helminth egg and oocyst counts of a small population of African lions (Panthera leo) in the southwestern Kalahari, Namibia Y. SMITH* and O.B. KOK Department of Zoology and Entomology, University of the Free State, P.O. Box 339 Bloemfontein, 9300 South Africa ABSTRACT SMITH, Y. & KOK, O.B. 2006. Faecal helminth egg and oocyst counts of a small population of African lions (Panthera leo) in the southwestern Kalahari, Namibia. Onderstepoort Journal of Veterinary Research, 73:71–75 An endoparasite survey of a small pride of African lions (Panthera leo) was conducted at Intu Afrika Kalahari Game Reserve, southwestern Namibia, during winter and summer of 2003 and 2004, re- spectively. Overall, 23 fresh lion scats were collected opportunistically during fieldwork trials. A flota- tion technique was employed for the diagnosis of parasites. Three nematodes, Ancylostoma brazili- ense, Gnathostoma spinigerum and Uncinaria stenocephala and two coccidians, Toxoplasma gondii and Isospora felis were recorded. By using the McMaster method for quantification, a maximum num- ber of 14 866 oocysts per gram of faeces was obtained for I. felis during winter 2003. Endoparasite taxa carried by the different individuals in the pride were found to be related to their levels of associa- tion. Rates of infection were relatively low as a result of the habitat, semi-captive conditions and ear- lier sporadic deworming. Keywords: Coccidians, endoparasites, Kalahari Desert, nematodes, Panthera leo ∗ Author to whom correspondence is to be directed. E-mail: liongirl@mweb.com.na Accepted for publication 1 August 2005—Editor 72 Faecal helminth egg and oocyst counts of African lions (Panthera leo) in Namibia north-east of Mariental. The pride consists of two adult males, an adult female and two cubs. The younger male and female are siblings and are close- ly bonded. The pride was being rehabilitated and was provided with a live animal once a week. Field- work trials on aspects of their behaviour were per- formed during winter (May to July 2003) and again during summer (February and March 2004). The cubs were born during November 2003 and were included in the summer trials. Faecal collection and preservation Intestinal parasite surveys were conducted by op- portunistic collection of scats during field observa- tions. A total of 23 fresh samples were collected from the adult lions during both summer and winter. During the summer, six samples of scat from the cubs were also obtained, four from the male and two from the female. Nematode eggs, cestode eggs and proglottids, and oocysts in the faeces were pre- served in 10 % formalin in 750 ml glass bottles with- in 12 h after collection. A standard operating procedure (SOP CVI/07/02/014 Faecal Examination: Diagnostic and Quantitative) obtained from ClinVet International (Pty) Limited was employed. Eggs of Taenia spp. could be identi- fied by using a flotation technique and expelled proglottids were located by washing over a sieve with 0.5 mm apertures. The resulting residues were suspended in a small amount of water and exam- ined under a stereoscopic microscope for the pres- ence of proglottids. A quantitative parasite egg and coccidian oocyst count was done according to the modified McMaster method described by Reinecke (1983). RESULTS The eggs of three nematodes, Ancylostoma brazili- ense, Gnathostoma spinigerum and Uncinaria steno- cephala, and the oocysts of two coccidians, Toxo- plasma gondii and Isospora felis, were recovered and identified following Soulsby (1982) and the ex- perience of the laboratory staff of ClinVet Inter- national. All these species, excluding Uncinaria, are listed by Boomker, Penzhorn & Horak (1997) as typical helminth and coccidian parasites of African lions. Table 1 indicates the seasonal occurrence of the parasite species recovered. Intact and frag- mented nematodes were also found in the scat dur- ing the summer trial. They were present in each flo t- a tion performed. A total of six samples, three from each season, were negative for any eggs, oocycts or worms when quantitative counts were done with the McMaster method. All of these were collected from the adult lions. As shown in Table 2, the inten- sity of eggs and oocysts of the endoparasites de- creased during the subsequent summer trial except for the hookworm, A. braziliense, which increased. Results differed during the flotation and the McMas- ter slide investigations. Two species of parasite, A. braziliense and T. gondii, were present in both the male lions. Flotation results for the older male indi- cated A. braziliense and the McMaster slide results showed only the presence of T. gondii. The younger male’s flotation results indicated only T. gondii, while the McMaster slide demonstrated the presence of A. braziliense. The female had the highest egg counts in both the flotation and the McMaster slide counts. Flotation showed that the female harboured the oocysts of I. felis, but they were not present in the McMaster slide. Results for the female cub’s flo- tation included A. braziliense and I. felis, whereas the former and T. gondii were present in the McMas- ter slide. In the case of the male cub, flotation indi- cated the presence of A. braziliense, T. gondii and G. spinigerum, while the McMaster slide showed only T. gondii. The female cub had a higher egg and oocyst count than the male cub. Uncinaria steno- cephala was not present during the summer trials. DISCUSSION Egg and oocyst counts during both the winter and summer trials indicate low rates of infection. Research in the Serengeti and Ngorongoro Crater (Müller-Graf 1995) indicated that median values per gram faeces may reach up to 5 700 for coelozoic helminths with no apparent ill-effects to the host. With the excep- tion of A. braziliense, all egg counts decreased from the winter to the summer trials (Table 2). The scope of the increase of the former is reduced by the in- crease in sample size since two cubs were included in the summer trials. The results, however, may be attributable to the high egg production of A. brazili- ense which permits a higher fecundity (Hinz 1988). Schmidt & Roberts (1985) state that some 25 000– 30 000 eggs may be produced per day by a female in the gastrointestinal tract. In respect of the histo- zoic coccidians and specifically I. felis, oocyst counts subside after initial infection which explains the sub- stantial decrease in oocyst count from winter to sum- mer. Cysts persist in the tissue, egg production all but ceases and immunity responses after the first infection is generally permanent (Schmidt & Roberts 73 Y. SMITH & O.B. KOK 1985). The high oocyst count for I. felis during the winter trials indicates a new infection for the female. Further to the former, the pride was dewormed one year prior to the inception of the fieldwork and the animals are fed, albeit live animals reducing expo- sure to some of the nematodes. The specific habitat experienced drought conditions for two years before the research and this would have assisted in reduc- tion of viable parasite eggs in the environment. The discrepancies between endoparasite presence in the flotation and McMaster slide can be explained in terms of the opportunistic nature of the scat col- lection and the random dispersion of endoparasite eggs and oocysts in faecal matter. When calculated in total, the female had the highest egg and oocyst counts using both the flotation and McMaster slide methods. Schmidt & Roberts (1985) call this phe- nomenon overdispersion and state that parasite in- frapopulations are not randomly dispersed, but that a minority of the hosts will harbour a majority of the parasites. A relative large number of intact and fragmented nematodes were found in the scat samples. In the case of both species of hookworms present, the eggs, after voiding, require warm and moist condi- tions to hatch into L1 or rhabditiform larvae (Schmidt & Roberts 1985). The majority of scats collected were in the form of diarrhoeic faeces. The lions were fed sporadically during the summer trials and en- gorged themselves when large ungulates were killed. The diarrhoeic faeces had to be left for a day or two to permit drying prior to being collected. Dur- ing this time, some of the nematode eggs could have hatched. Alternatively, nematode eggs also hatch in warm, moist soil and as a result of the rains some of the hatched larvae in the scat may also have been present in the environment (Schmidt & Roberts 1985). TABLE 1 Endoparasite suprapopulation in African lions during two contrasting periods of study at Intu Afrika Kalahari Game Reserve A. braziliense G. spinigerum U. stenocephala T. gondii I. felis Winter 2003 Older male Female Younger male Summer 2003 Older male Female Younger male Male cub Female cub TABLE 2 Egg and oocyst counts of endoparasites in the pride of African lions at Intu Afrika Kalahari Game Reserve Sample size Infected samples Infected hosts Mean intensity Maximum intensity Winter 2003 A. braziliense G. spinigerum T. gondii I. felis 11 11 11 11 4 1 4 7 3 1 2 3 133 666 233 3 320 200 666 400 14 866 Summer 2004 A. braziliense G. spinigerum T. gondii I. felis 17 17 17 17 4 1 7 1 3 1 4 1 173 66 173 66 600 66 200 66 74 Faecal helminth egg and oocyst counts of African lions (Panthera leo) in Namibia All of the helminth endoparasites found are trans- mitted either via the environment or by transplacen- tal transmission. According to Noble & Noble (1988) congenital transmission of hookworms has been demonstrated in domestic dogs, but not in domestic cats. However, this has not been investigated in li- ons and remains to be proved or disproved. The in- fection of the female cub with I. felis was most likely due to contact with the female. Curio (1988) reported that faecal egg counts matter correlate positively with dominance rank in the yel- low baboon (Papio cynocephalus). The data col- lected on the Kalahari lion in this investigation does not support this. Although feeding habits of the older male should support greater exposure to parasites, especially T. gondii which has the herbivore as an intermediate host, behaviour may play a more promi- nent role in terms of the parasite burden. The older male spent most of his time alone and did not allo- groom often and, as a result, his exposure to endo- parasite eggs and oocysts from other members of the pride was reduced. The younger male had the lowest egg and oocyst counts, which is contradictory to published data. The circumstances in which the lions were held were, how ever, unnatural and under more natural condi- tions the younger male would have left the pride for a nomadic lifestyle. All the behaviour of the younger male indicated that he was under considerable so- cial pressure. Dominance from the older male was constant and turned violent as the younger male grew older and began to resist. When an animal is under stress, adrenal glands become hyperactive and corticosteroids are released (H. Bertschinger, personal communication 2004). This impacts nega- tively on the animal in question and reduces its re- sistance to parasites (Esch, Whitfield Gibbons & Bourque 1975). Wilson (1976) makes mention of what Hans Seyle called the General Adaptation Syn drome in 1956, in which there is a sequence of three stages, namely the alarm stage when adrenal corticotropical hor- mones are released, a stage of resistance in which the adrenal glands enlarge due to a continuous in- creased demand for corticosteroids, and finally, a stage of exhaustion is reached when the body is not able to withstand the increased corticosteroid levels which increases the chances of infection. Aggressive interactions are named as the most potent of stres- sors. Exposure to infection in the younger male was also increased by the protracted periods spent with the female and later, the cubs. The positive response determined in the younger male in terms of resistance to the parasites could be as a result of his response to the pressure. In all our observations of the animals’ feeding, the younger male consumed the largest amounts of meat (on one occasion he fed for 4 h and 22 min) with an average consumption of 50 kg, and also drank wa- ter for 8.39 min, the longest time recorded. Although he was not weighed, he was obviously the most overweight of the lions and, as a result, he may have had the physiological resources to resist para- site infections. The relatively low egg and oocyst counts and cor- responding infection levels of the lion pride are as a result of a variety of factors. Firstly, the habitat was clean and parasites present in the environment would have been reduced by the two years of drought and the sporadic deworming prior to the inception of this study. Isolation of the lions from the greater reserve may also have been responsible for the fewer taxa present. Finally, the relative safety and lack of natu- ral pressure on the animals would have permitted a well-functioning immune system allowing for a strong defense response to endoparasites. ACKNOWLEDGEMENTS We thank Mr Howard Hebbard for permission to conduct research at Intu Afrika Kalahari Game Re- serve, the National Research Foundation of South Africa and the business community in Namibia, no- tably Siemens, Engen, Proforce, Sirkel Motors and the Windhoek Observer, for generous financial con- tributions towards the project, and the staff of ClinVet International for assistance with the laboratory work and the identification of parasites. REFERENCES BJORK, K.E., AVERBECK, G.A. & STROMBERG, B.E. 2000. Parasite and parasite stages of free-ranging wild lions (Pan- thera leo) of northern Tanzania. Journal of Zoo and Wild life Medicine, 31:56–61. BOOMKER, J., PENZHORN, B.L. & HORAK, I.G. 1997. Parasites of lions (Panthera leo) and leopards (Panthera pardus): A doc umentation. Proceedings of a Symposium on Lions and Leopards as Game Ranch Animals, Onderstepoort, Pre toria: 131–142. CURIO, E. 1988. Behaviour and parasitism, in Parasitology in focus, edited by H. Melhorn. Berlin: Springer-Verlag. ESCH, G.W., WHITFIELD GIBBONS, J. & BOURQUE, J.E. 1975. An analysis of the relationship between stress and parasit- ism. The American Midland Naturalist, 93:339–353. HINZ, E. 1988. Geomedical aspects of parasitology, in Para sitol- ogy in focus, edited by H. Melhorn. Berlin: Springer-Verlag. 75 Y. SMITH & O.B. KOK LE ROUX, P.L. 1958. Pharyngostomum cordatum (Dies, 1850), Galoncus perniciosus (v. Linstow, 1885) and Gnathostomum spinigerum (Owen, 1836) infections in a lion in northern Rho- desia. Transactions of the Royal Society of Tropical Med i- cine and Hygiene, 52:14. MÜLLER-GRAF, C.D.M. 1995. A coprological survey of intestinal parasites of wild lions (Panthera leo) in the Serengeti and Ngorongoro Crater, Tanzania, East Africa. 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