J. Parasitol., 91(3), 2005, pp. 569±573 q American Society of Parasitologists 2005 GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF UGANDA Thomas R. Gillespie*², Ellis C. Greiner³, and Colin A. Chapman²§ Department of Zoology, University of Florida, Gainesville, Florida 32611. e-mail: [email protected] ABSTRACT: From August 1997 to July 2003, we collected 2,103 fecal samples from free-ranging individuals of the 3 colobus monkey species of UgandaÐthe endangered red colobus (Piliocolobus tephrosceles), the eastern black-and-white colobus (Co- lobus guereza), and the Angolan black-and-white colobus (C. angolensis)Ðto identify and determine the prevalence of gastro- intestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate ¯otation and fecal sedimentation. Coprocultures facilitated identi®cation of helminths. Seven nematodes (Strongyloides fulleborni, S. stercoralis, Oesophagostomum sp., an unidenti®ed strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicro- coeliidae), and 3 protozoans (Entamoeba coli, E. histolytica, and Giardia lamblia) were detected. Seasonal patterns of infection were not apparent for any parasite species infecting colobus monkeys. Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus, but prevalence did not differ for any other shared parasite species between age and sex classes. Colobinae is a large subfamily of leaf-eating, Old World 19 from Angolan black-and-white colobus. Red colobus are sexually monkeys represented in Africa by species of 3 genera, Colobus, dimorphic, with males averaging 10.5 kg and females 7.0 kg (Oates et al., 1994); they display a multimale±multifemale social structure and Procolobus, and Piliocolobus (Grubb et al., 2002). These foli- live in groups of 20 to more than 100 within home ranges that average vorous monkeys live in groups of highly variable size (5±300 35.3 ha (Struhsaker, 1975; Gillespie and Chapman, 2001). Eastern individuals) and often form mixed-species associations with black-and-white colobus are sexually dimorphic, with males averaging other primates (Struhsaker, 1981; Oates, 1994; Chapman and 13.5 kg and females 8.6 kg (Oates et al., 1994); they display variable Chapman, 2000). Colobines are forest-dependent and, conse- social structure (1 male±multifemale or multimale±multifemale), and live in groups of 7±11 within home ranges that average 15 ha (Oates, quently, are acutely threatened by human activities that reduce 1974; Onderdonk and Chapman, 2000). Angolan black-and-white co- forest cover. More than two-thirds of sub-Saharan Africa's orig- lobus are sexually dimorphic, with males averaging 9.7 kg and females inal forest cover has been lost because of anthropogenic dis- 7.4 kg (Napier, 1985); they display a variable social structure (1 male± turbance (World Resources Institute, 1998), and forest cover multifemale or multimale±multifemale) and live in groups of 5 to more than 300 within home ranges from 1 to more than 400 ha (Oates et al., continues to decline at a rate of 0.7% annually (Food and Ag- 1994; T. Gillespie, pers. obs.). riculture Organization, 1999). Largely because of this habitat Red colobus and eastern black-and-white colobus samples were col- loss, 50% of African colobine species are endangered, and an lected from individuals inhabiting a 50 km2 area in western Uganda additional 20% are rare (Grubb et al., 2002). Within this con- consisting of a matrix of protected primary and secondary forest, forest text, baseline data regarding patterns of parasitic infections in fragments, and agricultural plots (Gillespie, 2004). Sampling effort fo- cused on Kanyawara, a 1,034-ha area characterized by logged and un- wild colobine populations are critical to providing an index of logged forest within Kibale National Park (766 km2;08139±08419N, population health and beginning to assess and manage disease 308199±308329E) (Struhsaker, 1997) and 21 forest fragments ranging risks. from 1 to 10 ha (total area 82 ha) located within 6.5 km of Kanyawara Although many studies have documented the gastrointestinal (Chapman et al., 2003). Red colobus density in this area ranged from parasites of wild populations of African apes (Huffman et al., 1 to 8 individuals/ha and averaged 2.3 individuals/ha (Gillespie, 2004). Eastern black-and-white colobus density in this area ranged from 0.2 to 1997; Graczyk et al., 1999; Nizeyi et al., 1999; Ashford et al., 5 individuals/ha and averaged 0.8 individuals/ha (Gillespie, 2004). 2000; Lilly et al., 2002) and baboons (Appleton et al., 1986; Mean annual rainfall (1990±2001) was 1,749 mm (Chapman et al., Eley et al., 1989; MuÈller-Graf et al., 1997; Hahn et al., 2003), 2002). Daily temperature minima and maxima averaged 14.9 and 20.2 the gastrointestinal parasites of other African primate taxa re- C, respectively, from 1990 to 2001. Angolan black-and-white colobus main poorly known (see, however, Gillespie et al., 2004). The samples were collected from 3 forest fragments ranging from 1 to 10 ha (total area 15 ha) adjacent to Lake Nabugabo in southeastern Uganda present study identi®es and quanti®es the prevalence of gastro- (08209±08259S, 318509±318569E). Angolan black-and-white colobus den- intestinal helminth and protozoan parasites for the 3 colobine sity in this area ranged from 0.5 to 3 individuals/ha and averaged 1.5 species of Uganda: the endangered red colobus (Piliocolobus individuals/ha (Gillespie, 2004). Annual rainfall ranges from 520 to tephrosceles), the eastern black-and-white colobus (Colobus 1,970 mm (E®tre et al., 2001), and daily temperature minima and max- guereza), and the Angolan black-and-white colobus (C. ango- ima average 15.2 and 27.2 C, respectively (Meteorology Department, Masaka, Uganda). All survey sites experience a bimodal pattern of sea- lensis). When data are suf®cient, we also examine the effect of sonal rainfall, with peaks occurring in March±May and August±Novem- season and host sex on parasite prevalence. ber. Samples were collected from habituated and semihabituated adult and MATERIALS AND METHODS subadult males and females of each primate species. Every attempt was From August 1997 to July 2003, we collected 2,103 fecal samples: made to sample as widely as possible within each primate population; 1,608 from red colobus, 476 from eastern black-and-white colobus, and however, because individual recognition was not always possible, some individuals may have been sampled more than once. Samples were col- lected immediately after defecation to avoid contamination and exam- Received 16 July 2004; revised 11 October 2004; accepted 12 October ined macroscopically for adult nematodes and tapeworm proglottids. 2004. Samples were stored individually in 5.0-ml vials in 10% formalin so- * Current address: Department of Veterinary Pathobiology, University lution. Preserved samples were transported to the University of Florida, of Illinois, Urbana, Illinois 61802. where they were examined for helminth eggs and larvae as well as ² Department of Zoology, University of Florida, Gainesville, Florida. protozoan cysts using concentration by sodium nitrate ¯otation and fecal ³ Department of Pathobiology, College of Veterinary Medicine, Uni- sedimentation (Sloss et al., 1994). Parasites were identi®ed on the basis versity of Florida, Gainesville, Florida 32611. of egg or cyst color, shape, contents, and size. Iodine was used to fa- § Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, New cilitate protozoan identi®cation. Measurements were made to the nearest York 10460. 0.1 m6SD using an ocular micrometer ®tted to a compound micro- 569 570 THE JOURNAL OF PARASITOLOGY, VOL. 91, NO. 3, JUNE 2005 TABLE I. The prevalence (%) of gastrointestinal parasite infections in colobus species (measuring 70.0 6 1.4 3 41.8 6 1.6 mm for colobus monkeys of Uganda (sample size is in parentheses following red colobus and 70.2 6 1.8 3 41.6 6 1.6 mm[n5 2] for species name). eastern black-and-white colobus). Cultured third-stage larvae of Oesophagostomum sp. did not differ in length (U 5 36.50, Piliocolobus Colobus Colobus P 5 0.334) between red colobus (905.0 6 4.7 mm) and eastern tephrosceles guereza angolensis 6 m Parasite species (1.608) (476) (19) black-and-white colobus (904.5 3.6 m). Prevalence of Oe- sophagostomum sp. was higher in eastern black-and-white co- Strongyloides fulleborni 3.54 4.20 5.26 lobus than in red colobus (x2 5 11.40, df 5 1, P , 0.001) Strongyloides stericalis 0.44 0.00 0.00 (Table I). Oesophagostomum sp. 2.80 6.09 0.00 Unidenti®ed strongyle eggs were found in feces of all colo- Unidenti®ed Strongyle 1.55 1.05 10.53 bus species and differed in length (H 5 6.6, P 5 0.037) and Ascaris sp. 0.12 1.26 0.00 5 5 Trichuris sp. 37.75 78.99 100.00 width (H 6.678, P 0.035) among colobus species (mea- Colobenterobius sp. 0.44 0.63 0.00 suring 59.6 6 5.6 3 38.2 6 4.1 mm for red colobus, 63.7 6 Bertiella sp 0.06 0.21 0.00 4.8 3 40.1 6 4.5 mm[n5 5] for eastern black-and-white co- Dicrocoeliidae sp. 0.06 0.63 0.00 lobus, and 68.4 6 2.0 3 40.3 6 2.3 mm[n5 2] for Angolan Entamoeba coli 4.35 7.77 15.79 black-and-white colobus). These strongyles may represent Ne- Entamoeba histolytica 3.48 7.56 10.53 cator sp., Ancylostoma sp., and/or Oesophagostomum sp.; how- Giardia lamblia 0.81 0.00 0.00 ever, coprocultures were not performed, limiting our ability to Overall 37.75 78.99 100.00 identify these parasites to the genus level.