Skip to main content

Advertisement

SpringerLink
Log in

Prevalence and climatic associated factors of Cryptosporidium sp. infections in savanna chimpanzees from Ugalla, Western Tanzania

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Studies about parasitization by Cryptosporidium in great apes have been scarce and mostly conducted in captivity. The present study reports the presence of Cryptosporidium sp. in wild chimpanzees (Pan troglodytes) from Ugalla, western Tanzania. Ugalla is one of the driest, most open, and seasonal habitats inhabited by chimpanzees. Cryptosporidium sp. was found in 8.9 % of the samples. The presence of the parasite was determined by preserving fecal samples in chemical conventional fixatives (MIF and alcohol absolute) staining them using a modified Zielh-Neelsen technique, and examining them with a light microscope. The number of fecal samples positive for Cryptosporidium was significantly higher during the rainy than during the dry season (p < 0.005). The results showed that feces collected in the rainy season were almost three times more likely to be positive for Cryptosporidium than those collected in the dry season (OR = 2.81). Cryptosporidium detection was significantly negatively affected by highest temperatures (>28.7 °C, p < 0.001). Cryptosporidiosis can cause serious health problems in humans and its potential effect on Ugalla chimpanzees is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alves M, Xiao L, Lemos V, Zhou L, Cama V, Barao da Cunha M, Matos O, Antunes F (2005) Occurrence and molecular characterization of Cryptosporidium spp. in mammals and reptiles at the Lisbon Zoo. Parasitol Res 97:108–112

    Article  PubMed  Google Scholar 

  • Anderson JR (1998) Sleep, sleeping sites, and sleep-related activities: awakening to their significance. Am J Primatol 46:63–75

    Article  PubMed  CAS  Google Scholar 

  • Bazuka JS, Nkwengulila G (2009) Variation over time in parasite prevalence among free-ranging chimpanzees at Gombe National Park, Tanzania. Int J Primatol 30:43–53

    Article  Google Scholar 

  • Chalmers RM, Davies AP (2010) Minireview: clinical cryptosporidiosis. Exp Parasitol 124:138–146

    Article  PubMed  Google Scholar 

  • Da Silva AJ, Caccio S, Williams C, Won KY, Nace EK, Whittier C, Pieniazek NJ, Eberhard ML (2003) Molecular and morphologic characterization of a Cryptosporidium genotype identified in lemurs. Vet Parasitol 111:297–307

    Article  PubMed  Google Scholar 

  • Dupain J, Van Elsacker L, Nell C, Garcia P, Ponce F, Huffman MA (2002) New evidence for leaf swallowing and Oesophagostomum infection in Bonobos (Pan paniscus). Int J Primatol 23:1053–1062

    Article  Google Scholar 

  • Ekanayake DK, Welch DM, Kieft R, Hajduk S, Dittus WPJ (2007) Transmission dynamics of Cryptosporidium infection in a natural population of non-human primates at Polonnaruwa, Sri Lanka. AmJTrop Med Hyg 77:818–822

    CAS  Google Scholar 

  • Fayer R, Spear CA, Dubey JP (1997) General biology of Cryptosporidium and cryptosporidiosis. In: Fayer R (ed) Cryptosporidium and cryptosporidiosis. CRC, Boca Raton, pp 1–49

    Google Scholar 

  • Fayer R, Trout JM, Jenkins MC (1998) Infectivity of Cryptosporidium oocysts stored in water at environmental temperatures. J Parasitol 84:1165–1169

    Article  PubMed  CAS  Google Scholar 

  • Fayer R, Morgan U, Upton SJ (2000) Epidemiology of Cryptosporidium: transmission, detection and identification. Int J Primatol 30:1305–1322

    CAS  Google Scholar 

  • Freeland WJ (1980) Mangabey (Cercocebus albigena) movement patterns in relation to food availability and fecal contamination. Ecology 61:1297–1303

    Article  Google Scholar 

  • Golvan YJ, Drouhet E, Segretain G, Mariat F (1972) Les examens de laboratoire. Techniques en parasitologie et en mycologie. Flammarion Medicine-Sciences, Paris

    Google Scholar 

  • Gomez MS, Gracenea M, Gonsalbez P, Feliu C, Enseñat C, Hidalgo R (1992) Detection of oocysts of Cryptosporidium in several species of monkeys and in one prosimian species at the Barcelona Zoo. Parasitol Res 78:619–620

    Article  PubMed  CAS  Google Scholar 

  • Gomez MS, Torres J, Gracenea M, Fernández-Morán J, González-Moreno O (2000) Further report on Cryptosporidium in Barcelona Zoo mammals. Parasitol Res 86:318–323

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Moreno O, Gracenea M, Hernandez-Aguilar RA, Perez A (2004) Cryptosporidium sp. in wild chimpanzees (Pan troglodytes) from Ugalla, Tanzania. In: IX European multicolloquium of parasitology, symposium on opportunistic and emerging parasitoses and mycoses, Valencia, Spain

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge

    Google Scholar 

  • Gracenea M, Gomez MS, Torres J, Carné E, Fernández-Morán J (2002) Transmission dynamics of Cryptosporidium in primates and herbivores at the Barcelona zoo: a long-term study. Vet Parasitol 104:19–26

    Article  PubMed  CAS  Google Scholar 

  • Graczyk TK, DaSilva AJ, Cranfield MR, Nizeyi JB, Kalema GRN, Pieniazek NJ (2001) Cryptosporidium parvum genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda. Parasitol Res 87:368–370

    Article  PubMed  CAS  Google Scholar 

  • Hausfater G, Meade BJ (1982) Alternation of sleeping groves by yellow baboons Papio cynocephalus as a strategy for parasite avoidance. Primates 23:287–297

    Article  Google Scholar 

  • Hernandez-Aguilar RA (2006) Ecology and nesting patterns of chimpanzees (Pan troglodytes) in Issa, Ugalla, Western Tanzania. Dissertation, University of Southern California

  • Hernandez-Aguilar RA (2008) Diet of chimpanzees (Pan troglodytes schweinfurthii) in a dry habitat: Ugalla, western Tanzania In: XXII Congress of the International Primatological Society. Edinburgh, United Kingdom, pp 155

  • Hernandez-Aguilar RA (2009) Chimpanzee nest distribution and site re-use in a dry habitat: implications for early hominin ranging. J Hum Evol 57:350–364

    Article  PubMed  Google Scholar 

  • Hernandez-Aguilar RA, Moore J, Stewart F, Piel A, Ogawa HA, Pintea L (2006) Surveys of Ugalla and Masito. In: Moyer D, Plumptre AJ, Pintea L, Hernandez-Aguilar RA, Moore J, Stewart F, Davenport TRB, Piel A, Kamenya S, Mugabe H, Mpunga N and Mwangoka M (eds) Surveys of chimpanzees and other biodiversity in Western Tanzania, wildlife conservation society, the Jane Goodall Institute and the United States Fish and Wildlife Service, pp 24–31

  • Hope K, Goldsmith ML, Graczyk T (2004) Parasitic health of olive baboons in Bwindi Impenetrable National Park, Uganda. Vet Parasitol 22:165–170

    Article  Google Scholar 

  • Huffman MA, Caton JM (2001) Self-induced increase of gut motility and the control of parasitic infections in wild chimpanzees. Int J Primatol 22:329–345

    Article  Google Scholar 

  • Huffman MA, Page JE, Sukhdeo MVK, Gotoh S, Kalunde MS, Chandrasiri T, Towers GHN (1996) Leaf-swallowing by chimpanzees: a behavioral adaptation for the control of strongyle nematode infections. Int J Primatol 17:475–503

    Article  Google Scholar 

  • Huffman MA, Gotoh S, Turner LA, Hamai M, Yoshida K (1997) Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates 38:111–125

    Article  Google Scholar 

  • Itani J (1979) Distribution and adaptation of chimpanzees in an arid area. In: Hamburg DA, McCown ER (eds) The great apes. Benjamin/Cummings, Menlo Park, pp 55–71

    Google Scholar 

  • Kano T (1972) Distribution and adaptation of the chimpanzees on the Eastern shore of Lake Tanganyka. Kyoto Univ Afr Stud 7:37–129

    Google Scholar 

  • Kawabata M, Nishida T (1991) A preliminary note on the intestinal parasites of wild chimpanzees in the Mahale Mountains, Tanzania. Primates 32:275–278

    Article  Google Scholar 

  • Legesse M, Erko B (2004) Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia. Acta Trop 90:231–236

    Article  PubMed  Google Scholar 

  • Lim YAL, Ngui R, Shukri J, Rohela M, Mat Naim HR (2008) Intestinal parasites in various animals at a zoo in Malaysia. Vet Parasitol 157:154–159

    Article  PubMed  CAS  Google Scholar 

  • Lonsdorf E, Travis DA, Rudicell RS, Gillespie TR, Salzer J, O’Donnell C, Lantz E, Nadler Y, Raphael JM, Hahn B, Pussey AE (2009) Observational health assessments of the Gombe chimpanzees: correlating clinical signs with diagnosed infections. 32nd Conference of the American Society of Primatologists, San Diego, California

  • McGrew WC, Baldwin PJ, Tutin CEG (1981) Chimpanzees in a hot, dry, and open habitat: Mt Assirik, Senegal, West Africa. J Hum Evol 10:227–244

    Article  Google Scholar 

  • McGrew WC, Tutin CEG, File SK (1989) Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal). Am J Primatol 17:147–155

    Article  Google Scholar 

  • Moore J (1992) “Savanna” chimpanzees. In: Nishida T, McGrew WC, Marler P, Pickford MP, De Waal FBM (eds) Topics in primatology vol. I: human origins. University of Tokyo Press, Tokyo, pp 99–118

    Google Scholar 

  • Moore J (1994) Plants of the Tongwe East Forest Reserve (Ugalla), Tanzania. Tropics 3:333–340

    Article  Google Scholar 

  • Moore J (1996) Savanna chimpanzees, referential models and the last common ancestor. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 275–292

    Chapter  Google Scholar 

  • Muriuki SMK, Farah IO, Kagwiria RM, Chai DC, Njamunge G, Suleman M, Olobo JO (1997) The presence of Cryptosporidium oocysts in stools of clinically diarroheic and normal nonhuman primates in Kenya. Vet Parasitol 72:141–147

    Article  PubMed  CAS  Google Scholar 

  • Nishida T (1989) A note on the chimpanzee ecology of the Ugalla area, Tanzania. Primates 30:129–138

    Article  Google Scholar 

  • Nizeyi JB, Mwebe R, Nanteza A, Cranfield MR, Kalema GR, Graczyk TK (1999) Cryptosporidium sp. and Giardia sp. infections in mountain gorillas (Gorilla gorilla berengei) of the Bwindi Impenetrable National Park, Uganda. J Parasitol 85:1084–1088

    Article  PubMed  CAS  Google Scholar 

  • Nizeyi JB, Cranfield MR, Graczyk TK (2002a) Cattle near the Bwindi Impenetrable National Park, Uganda, as a reservoir of Cryptosporidium parvum and Giardia duodenalis for local community and free-ranging gorillas. Parasitol Res 88:380–385

    Article  PubMed  CAS  Google Scholar 

  • Nizeyi JB, Sebunya D, da Silva A, Cranfield MR, Pieniazek NJ, Graczyk TK (2002b) Cryptosporidiosis in people sharing habitats with free-ranging mountain gorillas (Gorilla gorilla beringei), Uganda. AmJTrop Med Hyg 66:442–444

    Google Scholar 

  • Ogawa H, Idani G, Moore J, Pintea L, Hernandez-Aguilar RA (2007) Sleeping parties and nest distribution of chimpanzees in the savanna woodland, Ugalla, Tanzania. Int J Primatol 28:1397–1412

    Article  Google Scholar 

  • Petrzelkova KJ, Hasegawa H, Appleton CC, Huffman MA, Archer CE, Moscovice LR, Mapua MI, Singh J, Kaur T (2010) Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania. Am J Primatol 72:307–316

    PubMed  Google Scholar 

  • Pusey AE, Oehlert GW, Williams JM, Goodall J (2005) Influence of ecological and social factors on body mass of wild chimpanzees. Int J Primatol 26:3–31

    Article  Google Scholar 

  • Rudicell RS, Piel AK, Stewart F, Moore DL, Learn GH, Li Y, Takehisa J, Pintea L, Shaw GM, Moore J, Sharp PM, Hahn BH (2011) High prevalence of Simian Immunodeficiency Virus Infection in a community of savanna chimpanzees. J Virol 85:9918–9928

    Article  PubMed  CAS  Google Scholar 

  • Salzer JS, Rwego IB, Goldberg TL, Kuhlenschmidt MS, Gillespie TR (2007) Giardia sp. and Cryptosporidium sp. infections in primates in fragmented and undisturbed forest in Western Uganda. J Parasitol 93:439–440

    Article  PubMed  Google Scholar 

  • Xiao L (2010) Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 124:80–89

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Tano Ahmadi, Busoti Juma, Mzee Katandasha, Shedrack Lucas, Alejandro Perez, Moshi Rajabu, Abdalla Said, Ndai Sammwely, and Are Thune for their help in the field. We thank the Government of Tanzania, the Commission for Science and Technology (COSTECH), and the Tanzania Wildlife Research Institute (TAWIRI) for permission to work at Ugalla and to export chimpanzee fecal samples. We thank the University of Barcelona and Labco Analysis, Barcelona, for technical support. We are grateful to the L.S.B. Leakey Foundation, National Science Foundation, Jane Goodall Center at the University of Southern California, Ugalla Lab at UCSD, Wenner-Gren Foundation, International Primatological Society, Carnegie Trust for Universities of Scotland, Harold Hyam Wingate Foundation, Royal Anthropological Institute, and UCSD Committee on Research for financial support.

Author information

Authors and Affiliations

  1. Laboratory of Parasitology, Faculty of Pharmacy, University of Barcelona, Av. Joan XXIII s/n E-08028, Barcelona, Catalonia, Spain

    Olga Gonzalez-Moreno

  2. Laboratory of Parasitology, Labco Analysis, C/Londres, 28, Barcelona, Spain

    Olga Gonzalez-Moreno

  3. Centre for Ecological and Evolutionary Synthesis, Department of Biology, University of Oslo, P.O. Box 1066, Blindern, 0316, Oslo, Norway

    R. Adriana Hernandez-Aguilar

  4. Department of Anthropology, University of California at San Diego, La Jolla, CA, 92093-0532, USA

    Alex K. Piel

  5. Department of Biological Anthropology, University of Cambridge, Fitzwilliam Street, Cambridge, CB2 1QH, UK

    Fiona A. Stewart

  6. Laboratory of Parasitology, Faculty of Pharmacy, University of Barcelona, Av. Joan XXIII s/n E-08028, Barcelona, Catalonia, Spain

    Mercedes Gracenea

  7. Department of Anthropology, University of California at San Diego, La Jolla, CA, 92093-0532, USA

    Jim Moore

Authors
  1. Olga Gonzalez-Moreno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Adriana Hernandez-Aguilar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alex K. Piel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fiona A. Stewart
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mercedes Gracenea
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jim Moore
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olga Gonzalez-Moreno.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gonzalez-Moreno, O., Hernandez-Aguilar, R.A., Piel, A.K. et al. Prevalence and climatic associated factors of Cryptosporidium sp. infections in savanna chimpanzees from Ugalla, Western Tanzania. Parasitol Res 112, 393–399 (2013). https://doi.org/10.1007/s00436-012-3147-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-012-3147-8

Keywords

Search

Navigation