Parasitic Nematodes in the Chimpanzee Population on Rubondo Island, Tanzania

  • Klara J. Petrzelkova
  • Hideo Hasegawa
  • Liza R. Moscovice
  • Taranjit Kaur
  • Mwanahamissi Issa
  • Michael A. Huffman
Article

We identified 3 nematodes not previously reported in chimpanzees (Pan troglodytes) introduced on Rubondo Island, Tanzania: Protospirura muricola, Subulura sp., and Anatrichosoma sp. Vervet monkeys (Cercopithecus aethiops pygerythrus), rodents, and intermediate insect hosts might maintain Protospirura muricola and Subulura sp., and indigenous monkeys on the island might also maintain Anatrichosoma sp. Low prevalence of Subulura sp. and Anatrichosoma sp. suggests that chimpanzees acquired them from ingestion of contaminated food.

Key words

chimpanzee introduced population nematode new parasite record Rubondo Island 

INTRODUCTION

Researchers have studied extensively parasites of common chimpanzees (Pan troglodytes) in captivity and in the wild (Ashford et al., 2000; File et al., 1976; Huffman et al., 1997; Kabawata and Nishida, 1991; Landsoud-soukate et al., 1995; Lilly et al., 2002; McGrew et al., 1989; Murray et al., 2000). Meyers and Kuntz (1972) created a checklist of parasites and commensals for Pan.

Some intestinal protozoan species and probably all helminths can be pathogenic to their hosts, particularly in large numbers and if the host is not treated. Symptoms include acute diarrhea, gastric pain, anemia, and pulmonary problems. Hyperinfection can lead to death, especially when the host is immunocompromised (Beaver et al., 1984; Mehlhorn, 1988).

Only few publications are available on parasites of great apes released into the wild. Release into a novel environment can transmit new parasites not previously reported during studies in their natural habitats. In a comparative study of parasitism in captive, wild, and rehabilitated orangutans, Collet et al.(1986) reported a fatal outbreak of Mammomonogamus sp. (lung-worms) in rehabilitated orangutans introduced into a new environment. Researchers described the nematode in many wild and domestic animals, also incidentally in humans, but not in orangutans (Collet et al., 1986). Vanthomme (2004) compared parasite fauna between wild and reintroduced chimpanzees in Concouati-Douli, Congo. We found no published reports of studies on chimpanzees introduced into a nonnative habitat of chimpanzees, making ours the first report of its kind.

As part of an ongoing study into the behavioral ecology of chimpanzees introduced into a nonnative habitat of chimpanzees on Rubondo Island, Tanzania, we are investigating the parasitic fauna of the population. We detected 3 nematode species in feces of Rubondo chimpanzees not previously reported in other wild or captive chimpanzees.

MATERIALS AND METHODS

Study Population

Between 1966 and 1969, the Frankfurt Zoological Society (FZS) released 17 chimpanzees onto Rubondo Island, Tanzania, in Lake Victoria (2° 18′S, 31° 50′E). The chimpanzees were wild born and originated from several African countries including Sierra Leone and Guinea. Before release, the subjects spent 3.5 mo–9 yr in European zoos and circuses (Borner, 1985). Immediately before release, their health ranged from good to poor and their behavior from normal to abnormal. Staff provisioned chimpanzees for 2 mo, but conducted no rehabilitation or systematic monitoring in the years that followed (Borner, 1985; Grzimek, 1970). It is likely staff treated chimpanzees for gastrointestinal parasite infections via antihelminthics during captivity and before release (Borner et al., pers. comm.).

Chimpanzees rely entirely on the island's natural vegetation for subsistence and the population is thriving, having at least doubled over the last 30 yr (Huffman, 2000; Moscovice et al., 2004).

Study Site

The 240-km2 Rubondo Island is part of a 450-km2 area, including several smaller islands and a large portion of lake gazetted as a national park in 1977. The island is 1134 m above sea level, and contains a series of parallel ridges 200–300 m in elevation. Approximately 70% of the habitat comprises mixed evergreen and semideciduous forest, dominated by Croton sylvaticus, Synsepalum brevipes, and Pancovia turbinata. Forests also have high densities of lianas. Papyrus swamp habitat dominates near the lakeshores. Grassland areas also occur sporadically throughout the island and are more dominant in the far southern regions. Annual rainfall is ca. 1200 mm and annual temperature is 19–26°C. The only indigenous primate species is the vervet monkey (Cercopithecus aethiops pygerythrus). Several other mammals were introduced “by the Frankfurt Zoological Society” onto the island between 1964 and 1974, including black rhinoceros (Diceros bicornis), giraffes (Giraffa camelopardalis), sunni antelopes (Nesotragus moschatus), roan antelopes (Hippotragus equinus), elephants (Loxodonta africana), black-and-white colobus (Colobus abyssinicus), and porcupines (Borner, 1985; Kiwango, 2002).

Sample Collection

We collected fecal samples from the Rubondo chimpanzees between October 2002 and April 2004. Though chimpanzees were not fully habituated, we collected feces only when we directly observed subjects defecating, or when we found feces on the forest floor under night nests and at natural feeding sites. We collected fresh feces (12 h) only where we confirmed chimpanzee origin. We stored them in plastic bags and took them back to camp for processing. We divided all dung samples into 2-g portions, fixed them with commercial formaldehyde solution (37%), and placed them into screw-cap sealable vials. We later transported samples to the Department of Infectious Diseases (Biology), Faculty of Medicine, Oita University, Japan. We examined the samples microscopically via MGL (Ritchie, 1948). To recover adult worms, we washed fecal debris on strainers with aperture sizes of 5 mm, .5 mm, and .1 mm. We transferred the residues from strainers to a Petri dish and observed them via a stereomicroscope. We collected adult worms in feces, fixed them in formalin, cleared in glycerol-alcohol solution by evaporation, and observed the specimens via a light microscope with Nomarski interference contrast apparatus.

For comparison, we also observed Protospirura muricola Gedoelst, 1916 from Gabonese rodents (courtesy of Dr. M. Asakawa, Rakuno Gakuen University) and Subulura sp. from Cercopithecus mitis kolbi of Kenya (U.S. National Parasite Collection 54620).
Fig. 1.

Protospirura muricola (a) egg and (b, c) fragments of the posterior body of male. Scale bar = 50 μm for a, 0.5 mm for b, c.

RESULTS AND DISCUSSION

New Nematode Records

During an ecological parasitological investigation, we examined 124 fecal samples. We recorded 3 new nematodes for chimpanzees: Protospirura muricola, Subulura sp., and Anatrichosoma sp.

Protospirura muricola Gedoelst, 1916 (syn. Protospirura bonnei Ortlepp, 1924)

The eggs of Protospirura muricola occurred in 7 (5.4%) samples. They measured 50–56 × 37–42 (mean 52.4×38.9) μm (n=17); contained larvae; and were colorless, ellipsoidal, thick-shelled, and surrounded by a hyaline substance (Fig. 1a). One fecal sample contained both eggs and a fragment of the posterior body of an adult male. The posterior end had thick caudal alae and area rugosa ventrally (Figs. 1b, c). The genital papillae comprised 4 pairs of preanal papillae, 1 unpaired median papilla on the anterior anal lip, and 6 pairs of postanal papillae of which the posterior 3 were near the posterior end (Fig. 1c). The tail was 0.53 mm long. The spicules were dissimilar, with the right spicule thin, 0.40 mm long, and the left spicule thick, 0.47 mm long. The gubernaculum was robust.

The egg shape and size were identical to those in Baylis (1928; 50 × 37 μm) and Brumpt (1931; 55–60 × 40 μm). Brumpt (1931) also described the hyaline substance around the egg. The morphology of the male tail was identical with previous descriptions (Brumpt, 1931; Quentin, 1969) and that of specimens from the Gabonese rodents (cf. Asakawa and Nicolas, 2003).

Protospirura muricola is a relatively frequent parasite of exanthope and synanthrope rodents in Africa and Asia (Baylis, 1928; Gedoelst, 1916; Joyeux et al., 1928; Morel, 1959; Tubangui, 1931). Researchers have noted its presence in primates, e.g., in Perodicticus potto in Nigeria (Baylis, 1928), captive Aotus zonalis, Ateles dairensis, and Cebus capucinus in Panama (Foster and Johnson, 1939), captive Ateles ater in the Paris Botanical Garden (Dollfus and Chabaud, 1955), and Cercopithecus aethiops in Congo (Vuylsteke, 1956). Dermapterans and most probably also scarabeid beetles are intermediate hosts in the life cycle of the nematode (Anderson, 2000; Quentin, 1969; Scharff et al., 1993). The normal location of adults is in the stomach of the definitive host (Tenora et al., 2003).

Though Protospirura muricola in rodents seems to be a relatively nonpathogenic parasite, it causes severe, sometimes fatal, disease in captive primates, especially in capuchins (cf. Ruch, 1959). Foster and Johnson (1939) reported numerous deaths in a colony of Cebus caused by invasion of P. muricola. A typical postmortem picture, in case of a severe infection, was an enormous number of worms concentrated in the stomach and esophagus, with pressure effects on the entire mucosal surface, obvious mechanical blockage, rarely perforation, and with tissue invasion generally confined to the distal portion of the esophagus. The pathogenicity of the nematode in chimpanzees remains unknown.

Subulura sp.

We found the eggs of Subulura sp. in only 1 sample (.8% of samples) (Fig. 2a, b). The eggs were round, though their depth was much smaller than their diameter, and measured 40–43 × 30–37 (mean 41.6–34.5) μm (n=10). They were relatively thick shelled and contained larva that formed coils, often leaving a space in the center. The features coincide with those of Subulura sp. in Cercopithecus mitis kolbi from Kenya, though egg size was much smaller (64–77 × 54–61 μm in the latter species; U.S. National Parasite Collection 54620). According to Cameron (1930), the egg size of Subulura distans (Rudolphi, 1809), which inhabits mainly Cercopithecus spp., was 43–63 × 30–33 μm, nearly the same as that of eggs in Rubondo. Hence, we surmise that the present species is Subulura distans or a closely related species.
Fig. 2.

Subulura sp. eggs. (a) Frontal view. (b) Lateral view Scale bar = 50 μm.

Though Subulura includes many species, mostly parasites that inhabit the cecum of birds, researchers have also reported 9 species in primates (Yamashita, 1963). Yamashita (1963) reported Subulura distans from several species of Cercopithecus, Cercocebus, and Erythrocebus. Subulura spp. utilize coleopterans, dermapterans, and orthopterans as intermediate hosts (Anderson, 2000). Petter (1960) studied the development of Subulura distans in the cockroach (Blatella germanica). Though Subulura spp. do not cause serious problems in their hosts, Desportes and Roth (1943) isolated a large number of S. distans at necropsies of several primates in the Paris Zoo.

Anatrichosoma sp.

We found only 1 egg in 1 sample (.8% of samples) (Fig. 3). The egg measured 83 × 53 μm, was dark brown, barrel-shaped with polar plugs, thick-shelled, and contained larva. The eggs of Anatrichosoma spp. measure ca. 76 × 58 μm but may be larger or smaller depending on the species (Orihel and Ash, 1995).
Fig. 3.

Anatrichosoma sp. egg. Scale bar = 50 μm.

Anatrichosoma spp. are parasites of various mucosal epithelid in primates, marsupials, rodents, and tree shrews. Anderson (2000) described Anatrichosoma cutaneum and A. cynamolgi in 2 Asian primates (Macaca mulatta, M. fascicularis Philippinensis). Orihel (1970) reported Anatrichosoma spp. in African monkeys (Erythrocebus patas, Cercopithechus talapoin, C. aethiops, Cercocebus galeritus, and Papio sp.). Recently, Kilbourn et al. recorded Anatrichosoma sp. in 2 fecal samples of Govilla govilla (http://www.ecofac.org/Ebola/_DownloadBrazaville/Reed_GorillaHealth.pdf). Swift et al. (1922) reported a cutaneous form of Anatrichosoma that caused creeping eruptions in the palms and soles of rhesus monkeys. Dalgard (1980), Le-Van-Hoa et al.(1963), and Morishita and Tani (1960) also described it in lemurs, marmosets, langurs, macaques, siamangs, orangutans, and humans. Though the life cycle of Anatrichosoma spp. is unknown, Conrad and Wong (1973) and Remfry (1978) suggested direct transmission via swallowing infected mucosa.

Proposed Origin of Parasites of Chimpanzees on Rubondo Island

After introduction of a population to an isolated area that is nonnative to the introduced species, parasite fauna may arise from 2 sources: those already inhabiting the population at the time of introduction and those acquired in the new habitat. Chimpanzees seem to have acquired Protospirura muricola after their release onto Rubondo Island, though one cannot completely exclude the possibility that chimpanzees introduced the nematode. If acquisition of this parasite occurred after release, rodents or the indigenous vervets might naturally maintain it as final hosts and insects as intermediate hosts. Though researchers have not observed chimpanzees consuming reported intermediate hosts (e.g., beetles or dermapterans), Rubondo chimpanzees have eaten grasshoppers, Homorocoryphus nitidulus vicinus (Petrzelkova, pers. obs.). Grasshoppers are an intermediate host of Protospirura numidica Seurat, 1914, a parasite of the lower esophagus and stomach of palearctic and nearctic rodents and carnivores (Anderson, 2000). Thus, Protospirura muricola may also utilize grasshoppers as an intermediate host.

Nevertheless, one cannot exclude the possibility that Anatrichosoma sp. and Subulura sp. in the chimpanzee are examples of pseudoparasitism because we found egg(s) of each parasite in only 1 sample each. Consumption of known definitive hosts, vervets and rodents, could lead to deposition of their eggs in chimpanzee feces. Chimpanzees from the Mahale Mountains National Park, Tanzania, hunted vervets (Nishida and Uehara, 1983). There are also many records of rodent consumption by chimpanzees in Tanzania (cf. Goodall 1986; Nishida and Uehara, 1983). However, to date, researchers have not observed Rubondo chimpanzees hunting vervets or rodents.

Scientists have not extensively studied parasite transmission between chimpanzees and other wildlife species. It is important to identify parasites in the species of interest, as well as those of sympatric species and the indigenous human populations with whom they have contact. McGrew et al.(1989) and Murray et al.(2000) conducted parasite surveys in sympatric populations of chimpanzees and baboons and Landsoud-Soukate et al.(1995) in chimpanzees and gorillas. Lilly et al.(2002) examined parasites in local populations of chimpanzees, gorillas, agile mangabeys, and humans. More studies on parasite prevalence in sympatric populations and parasite transmission between populations are needed. as human encroachment onto wildlife habitats progresses, the data would serve as a baseline for comparative assessments of microfaunal changes. In this way, parasites can function as ecological indicator species of habitat degradation (Stuart et al., 1993). Considering the current results of our parasitological study of Rubondo chimpanzees, further research is required to investigate the parasite fauna of vervets and the human population on Rubondo and to assess the risk of transmission to chimpanzees.

Notes

ACKNOWLEDGMENTS

The authors thank the administration and staff of the Tanzania Commission for Science and Technology, Tanzanian Wildlife Research Institute and Tanzanian National Parks for permission to conduct the research and for their support and guidance. We express special thanks to the management and staff of Rubondo Island National Park for their assistance and technical help during the study. Flycatcher Safaris and the Frankfurt Zoological Society also provided technical and logistical support. We thank Giulia Grazziani, Alessia Gallastroni, and our many Tanzanian trackers for their participation in the collection of fecal samples and their help and wonderful companionship in the field. The Grant Agency of the Academy of Sciences of the Czech Republic supported the field work of K. J. Petrzelkova. Grants from the Leakey Foundation and Graduate Women in Science and a Research Assistantship at the Psychology Department, University of Wisconsin-Madison provided research funding for Liza R. Moscovice. JSPS grant 12640684 supported parasitological analyses by Hideo Hasegawa. Taranjit Kaur received financial support from the National Science Foundation, Award 0238069. Grants for field research from the Primate Research Institute, Kyoto University and the 21st Century COE Program of Kyoto University supported Michael A. Huffman. We are indebted to D. Modry, V. Barus, M. Ondrackova, and Jatinder Singh for their valuable comments during the preparation and writing of the manuscript. We also acknowledge and thank 2 anonymous reviewers for their time and comments.

REFERENCES

  1. Anderson, R. C. (2000). Nematode Parasites of Vertebrates: Their Development and Transmission, 2nd ed. C.A.B. International. Wallingford, Oxon, U.K.Google Scholar
  2. Asakawa, M. and Nicolas, V. (2003): A new host and locality records of a spirurid species, Protospirura muricola, from Gabonese wild murids. Biogeography 5: 67–70.Google Scholar
  3. Ashford, R. W., Reid, G. D. F., and Wrangham, R. W. (2000). Intestinal parasites of the chimpanzee Pan troglodytes in Kibale Forest, Uganda. Ann. Trop. Med. Parasitol. 94(2): 173–179.PubMedCrossRefGoogle Scholar
  4. Baylis, H. A. (1928). On a collection of nematodes from Nigerian mammals (chiefly rodents). Parasitology 20: 280–304.CrossRefGoogle Scholar
  5. Beaver, P. C., Jung, R. C., and Cupp, F. W. (1984). Clinical Parasitology. 9th ed. Lea & Febiger, Philadelphia.Google Scholar
  6. Borner, M. (1985). The rehabilitated chimpanzees of Rubondo Island. Oryx 19(3): 151–154.CrossRefGoogle Scholar
  7. Brumpt, E. (1931). Némathelminthes parasites des rats sauvages (Epimys norvegicus) de Caracas. 1. Protospirura bonnei. Infections expérimentales et spontanees. Formes adultes et larvaires. Ann. Parasit. Hum. Comp. 9: 344–358.Google Scholar
  8. Cameron, T. W. M. (1930). The species of Subulura Molin in primates. J. Helminthol. 8(1): 49–58.CrossRefGoogle Scholar
  9. Collet, J., Galdikas, B. M. F., Sugarjito, J., and Jojosudharmo, S. (1986). A coprological study of parasitism in orangutans (Pongo pygmaeus) in Indonesia. J. Med. Primatol. 15: 121–129.PubMedGoogle Scholar
  10. Conrad, H. D., and Wong, M. D. (1973). Studies of Anatrichosoma (Nematoda: Trichinellida) with description of Anatrichosoma rhina sp.n. and Anatrichosoma nacepobi sp.n. from nasal mucosa of Macaca mulatta. J. Helminthol. 47: 289–302.PubMedGoogle Scholar
  11. Dalgard, D. (1980). Note on Anatrichosoma in primates and request for information. Lab. Primate Newsl. 19(1): 7.Google Scholar
  12. Desportes, C., and Roth, P. (1943). Helminthes recoltes au cours d’autopsies pratiquees sur differents mammiferes morts a la menagerie du museum de Paris. Bull. Mus. Hist. Nat. 15(2): 108–114.Google Scholar
  13. Dollfus, R. P., and Chabaud, A. G. (1955). Cinq espèces de nématodes chez un atèle [Ateles ater (G. Cuvier 1823)] mort a la ménagerie du museum. Arch. Mus. Hist. Nat. 3: 27–40.Google Scholar
  14. File, S. K., McGrew, W. C., and Tutin, C. E. G. (1976). The intestinal parasites of a community of feral chimpanzees, Pan troglodytes sweinfurthii. J. Parasitol. 62(2): 259–261.PubMedCrossRefGoogle Scholar
  15. Foster, A. O., and Johnson, C. M. (1939). A preliminary note on identity, life cycle, and pathogenicity of an important parasite of captive monkeys. Am. J. Trop. Med. Hyg. 19(3): 265–277.Google Scholar
  16. Gedoelst, L. (1916). Notes sur la faune parasitaire du Congo Belge. Rev. Zool. Afr. 5: 1–90.Google Scholar
  17. Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior. Cambridge: Harvard University Press.Google Scholar
  18. Grzimek, B. (1970). Among Animals of Africa. Stein & Day, New York.Google Scholar
  19. Huffman, M. A. (2000). Evaluation of the Rubondo Island National Park Chimpanzee Habituation Project (unpublished report).Google Scholar
  20. Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M., and Yoshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale, Tanzania. Primates 38(2): 111–125.CrossRefGoogle Scholar
  21. Joyeux, C., Gendre, E., and Baer, J. G. (1928). Recherches sur les helminthes de l’Afrique occidentale francaise. Masson, Paris.Google Scholar
  22. Kabawata, M., and Nishida, T. (1991). A preliminary note on the intestinal parasites of wild chimpanzees in the Mahale Mountains, Tanzania. Primates 32(2): 275–278.CrossRefGoogle Scholar
  23. Kiwango, J. (2002). Ecological survey RINP (unpublished TANAPA report).Google Scholar
  24. Landsoud-Soukate, J., Tutin, C. E., and Fernandez, M. (1995). Intestinal parasites of sympatric gorillas and chimpanzees in the Lope Reserve, Gabon. Ann. Trop. Med. Parasitol. 89(1): 73–79.PubMedGoogle Scholar
  25. Le-Van-Hoa, Duong-Hong-Mo, and Nguen-Luu-Vien (1963). Premier cas de capillariose cutanee humaine. Bull. Soc. Path. Exot. 56: 121–126.Google Scholar
  26. Lilly, A. A., Mehlman, P. T., and Doran, D. (2002). Intestinal parasites in gorillas, chimpanzees, and humans at Mondika research site, Dzanga-Ndoki National Park, Central African Republic. Int. J. Primatol. 23(3): 555–573.CrossRefGoogle Scholar
  27. McGrew, W. C., Tutin, C. E. G., Collins, D. A., and File, S. K. (1989). Intestinal parasites of sympatric Pan troglodytes and Papio spp, at two sites—Gombe (Tanzania) and Mt. Assirik (Senegal). Am. J. Primatol. 17(2): 147–155.CrossRefGoogle Scholar
  28. Mehlhorn, H. (1988). Parasitology in Focus. Springer-Verlag Berlin Heidelberg. Berlin.Google Scholar
  29. Meyers, B. J., and Kuntz, R. E. (1972). A checklist of parasites and commensals reported for the chimpanzee (Pan). Primates 13(4): 433–471.CrossRefGoogle Scholar
  30. Morel, P. C. (1959). Les helminthes des animaux domestiques de l’Afrique occidentale. Rev. Elev. Med. Vet. Pays Trop. 12: 153–174.Google Scholar
  31. Morishita, K., and Tani, T. (1960). A case of Capillaria infection causing cutaneus creeping eruption in man. J. Parasitol. 4: 79–83.CrossRefGoogle Scholar
  32. Moscovice, L. R., Petrzelkova, K. J., Issa, M. H., Huffman, M. A., Snowdon, C. T., Mbago, F., Kaur, T., Singh, J., and Graziani, G. (2004). Role of lianas for introduced chimpanzees (Pan troglodytes) on Rubondo Island, Tanzania. Folia Primatol. 75 (Suppl 1): 308.Google Scholar
  33. Murray, S., Stem, C., Boudreau, B., and Goodall, J. (2000). Intestinal parasites of baboons (Papio cynocephalus anubis) and chimpanzees (Pan troglodytes) in Gombe National Park. J. Zoo Wild. Med. 31(2): 176–178.Google Scholar
  34. Nishida, T., and Uehara, S. (1983). Natural diet of chimpanzees (Pan troglodytes schweinfurthii): long-term records from the Mahale Mountains, Tanzania. African Study Monogr. 3: 109–130.Google Scholar
  35. Orihel, T. C. (1970). Anatrichosomiasis in African monkeys. J. Parasitol. 56(5): 982–985.PubMedCrossRefGoogle Scholar
  36. Orihel, T. C., and Ash, L. R. (1995). Parasites in Human Tissues. American Society of Clinical Pathologists, Chicago.Google Scholar
  37. Petter, A. J. (1960). Sur une larve de Subuluridae, parasite de la blatte germanique (Blatella germanica L.). C. R. Soc. Biol. 154: 300.Google Scholar
  38. Quentin, J. C. (1969). Cycle biologique de Protospirura muricola Gedoelst, 1916 Nematoda Spiruridae. Ann. Parasitol. Hum. Comp. 44: 485–504.PubMedGoogle Scholar
  39. Remfry, J. (1978). The incidence, pathogenesis and treatment of helmith infections in rhesus monkeys (Macaca mulatta). Lab. Anim. 12: 213–218.PubMedCrossRefGoogle Scholar
  40. Ritchie, L. S. (1948). An ether sedimentation technique for routine stool examination. Bull. U.S. Army Med. Dept. 8: 326.Google Scholar
  41. Ruch, T. C. (1959). Diseases of Laboratory Primates. W.B. Saunders, Philadelphia/London.Google Scholar
  42. Scharff, A., Burda, H., Tenora, F., Kawalika, M., and Barus, V. (1993). Parasites in social subterranean Zambian mole-rats (Cryptomys spp., Bathyergidae, Rodentia). J. Zool. Lond. 241: 571–577.CrossRefGoogle Scholar
  43. Stuart, M. D., Strier, K. B., and Pierberg, S. M. (1993). A coprological survey of parasites of wild muriquis, Brachyteles arachnoides, and brown howling monkeys, Alouatta fusca. J. Helmint. Soc. Wash. 60(1): 111–115.Google Scholar
  44. Swift, H. F., Boots, R. H. and Miller, C. P. (1922). A cutaneous nematode infection in monkeys. J. Exp. Med., 35: 599–620.Google Scholar
  45. Tenora, F., Barus, V., Prokes, M., Sumbera, R., and Koubkova, B. (2003). Helminths parasitizing the silvery mole-rat Heliophobius argenteocinereus (Rodentia: Bathyergidae) from Malawi. Helminthologia 40(3): 153–160.Google Scholar
  46. Tubangui, M. A. (1931). Worm parasites of the brown rat (Mus norvegicus) in the Philippine Islands with a special reference to those forms that may be transmitted to human beings. Philippine J. Sci. 46: 537–592.Google Scholar
  47. Vanthomme, H. (2004). Mise au point d’un protocole de suivi parasitaire de primates libres en foret tropicale et premiers resultats. These pour le diplome d’Etat Ecole de docteur veterinaire. Ecole Nationale Veterinaire de Nantes, France.Google Scholar
  48. Vuylsteke, A. (1956). Note sur quelques Nématodes parasites avec description de neuf espèces nouvelles. Rev. Zool. Bot. Afr. 53(3/4): 441–477.Google Scholar
  49. Yamashita, J. (1963). Ecological relationships between parasites and primates. I. Helminth parasites and primates. Primates 4(1): 1–96.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Klara J. Petrzelkova
    • 1
  • Hideo Hasegawa
    • 2
  • Liza R. Moscovice
    • 3
  • Taranjit Kaur
    • 4
  • Mwanahamissi Issa
    • 5
  • Michael A. Huffman
    • 6
  1. 1.Institute of Vertebrate BiologyAcademy of Sciences of the Czech RepublicBrnoCzech Republic
  2. 2.Department of Infectious Diseases (Biology), Faculty of MedicineOita University, HasamaOitaJapan
  3. 3.Department of PsychologyUniversity of Wisconsin-MadisonMadisonUSA
  4. 4.Department of Biomedical Sciences & PathobiologyVirginia Polytechnic Institute and State UniversityBlacksburgUSA
  5. 5.Rubondo Island National ParkGeita, MwanzaTanzania
  6. 6.Section of Ecology, Primate Research InstituteKyoto UniversityAichiJapan

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