Skip to main content

Advertisement

Log in

Prevalence of enteric bacterial parasites with respect to anthropogenic factors among commensal rhesus macaques in Dehradun, India

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

There has been a recent surge in research on primate infectious disease ecology. Two major areas remain relatively unaddressed to date—the prevalence of enteric bacterial parasites and the role of anthropogenic environmental factors in parasite acquisition in commensally living primate populations. In this preliminary assessment, we address both these gaps by assessing the prevalence, and the role of anthropogenic factors in shaping this prevalence, of three enteric bacterial parasites—E . coli O157:H7, Salmonella sp., Shigella sp.—across populations of rhesus macaques (M. mulatta) that live commensally with humans in Dehradun, northern India. Across 10-week study period, we collected data on (1) human-macaque behavioral interactions, (2) macaque and human demographic and activity scans, and (3) macaque fecal samples from the environment at four different locations in Dehradun. Biochemical tests and morphology-based confirmations clearly established the presence of all three enteric bacterial parasites in rhesus macaques. Overall prevalence ranged from 2 to 5 %, with Shigella sp. being the most prevalent. Regression analyses linking anthropogenic factors to bacterial prevalence showed a positive association between rates of macaques eating human garbage and E. coli O157:H7 (β = 0.23, p = 0.083), but a negative association with Salmonella sp. (β = −0.17, p = 0.026). Rather, the prevalence of Salmonella sp. was positively linked to rates of macaque eating provisioned food (β = 0.0012, p = 0.058). Finally, we found no relationship between anthropogenic factors and the prevalence of Shigella sp. Our findings establish the prevalence of enteric bacterial parasites in commensal populations of primates and suggest that although anthropogenic factors are linked to bacterial prevalence, the nature of the relationships may depend on the socioecological/foraging strategies of macaques and the food sources that facilitate the environmental survival of particular types of enteric bacteria over others.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abegg C, Thierry B (2002) Macaque evolution and dispersal in insular south-east Asia. Biol J Linn Soc 75:555–576

    Article  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266

    Article  CAS  PubMed  Google Scholar 

  • Beisner BA, Heagerty A, Seil SK, Balasubramaniam KN, Atwill ER, Gupta BK, Tyagi PC, Chauhan NPS, Bonal BS, Sinha PR et al (2015) Human–wildlife conflict: proximate predictors of aggression between humans and rhesus macaques in India. Am J Phys Anthropol 156:286–294

    Article  PubMed  Google Scholar 

  • Benjamin L, Atwill ER, Jay-Russell MT, Cooley M, Carychao D, Gorski L, Mandrell RE (2013) Occurrence of generic E. coli, E. coli O157:H7 and Salmonella spp. in water and sediment from leafy green produce farms and streams on the Central California coast. Int J Food Microbiol 165:65–76

    Article  PubMed  Google Scholar 

  • Bhan MK, Bhandari N, Sazawal S, Clemens JD, Raj P, Levine MM, Kaper JB (1989) Descriptive epidemiology of persistent diarrhoea among young children in rural northern India. Bull WHO 67:281–288

    CAS  PubMed  PubMed Central  Google Scholar 

  • Carpenter KP, Cooke ERN (1965) An attempt to find shigellae in wild primates. J Comp Pathol 75:201–204

    Article  CAS  PubMed  Google Scholar 

  • Chauhan A, Pirta RS (2010a) Agonistic interactions between humans and two species of monkeys (rhesus monkey Macaca mulatta and Hanuman langur Semnopithecus entellus) in Shimla, Himachal Pradesh. J Psychol 1:9–14

    Article  Google Scholar 

  • Chauhan A, Pirta RS (2010b) Socio-ecology of two species of non-human primates, rhesus monkey (Macaca mulatta) and Hanuman langur (Semnopithecus entellus), in Shimla, Himachal Pradesh. J Hum Ecol 30:171–177

    Google Scholar 

  • de Vos V, van Niekerk Gawj, McConnell EE (1973) A survey of selected bacteriological infections of the Chacma Baboon Papio ursinus from the Kruger National Park. Koedoe Monogr 16:1–10

    Google Scholar 

  • Drewe JA, O’Riain MJ, Beamish E, Currie H, Parsons S (2012) Survey of infections transmissible between baboons and humans, Cape Town, South Africa. Emerging Infect Dis 18:298–301

    Article  PubMed  PubMed Central  Google Scholar 

  • Ejercito CLA, Cai L, Htwe KK, Taki M, Inoshima Y, Kondo T, Kano C, Abe S, Shirota K, Sugimoto T et al (1993) Serological evidence of Coxiella burnetii infection in wild animals in Japan. J Wildl Dis 29:481–484

    Article  CAS  PubMed  Google Scholar 

  • Ekanayake DK, Arulkanthan A, Horadagoda NU, Sanjeevani GKM, Kieft R, Gunatilake S, Dittus WPJ (2006) Prevalence of Cryptosporidium and other enteric parasites among wild non-human primates in Polonnaruwa, Sri Lanka. Am J Trop Med Hyg 74:322–329

    PubMed  Google Scholar 

  • Eley RM, Strum SC, Muchemi G, Reid GDF (2005) Nutrition, body condition, activity patterns, and parasitism of free-ranging troops of olive baboons (Papio anubis) in Kenya. Am J Phys Anthropol 18:209–219

    Google Scholar 

  • Engel G, Jones-Engel L (2011) The role of Macaca fascicularis in infectious disease transmission. In: Gumert MD, Fuentes A, Jones-Engel L (eds) Monkeys on the edge: ecology and management of long-tailed macaques and their interface with humans. Cambridge University Press, Cambridge, pp 183–203

    Chapter  Google Scholar 

  • Engel GA, Pizarro M, Shaw E, Cortes J, Fuentes A, Barry P, Lerche NW, Grant R, Cohn D, Jones-Engel L (2008) Unique pattern of enzootic primate viruses in Gibraltar macaques. Emerging Infect Dis 14:1112–1115

    Article  PubMed  PubMed Central  Google Scholar 

  • Fuentes A, Rompis ALT, Putra IGA, Soma IG, Wandia IN, Putra IDKH, Stephenson R, Selamet W (2011) Macaque behavior at the human-monkey interface: the activity and demography of semi-free ranging Macaca fascicularis at Padangtegal, Bali, Indonesia. In: Gumert MD, Fuentes A, Jones-Engel L (eds) Monkeys on the edge: ecology and management of long-tailed macaques and their interface with humans. Cambridge University Press, Cambridge

    Google Scholar 

  • Fujita S, Ogasawara A, Kageyama T (2009) Prevalence of Clostridium perfringens in intestinal microflora of non-human primates. In: Huffman MA, Chapman CA (eds) Primate parasite ecology. Cambridge University Press, Cambridge, pp 271–281

    Google Scholar 

  • Ghandour AM, Zahid NZ, Banaja AA, Kamal KB, Bouq AI (1995) Zoonotic intestinal parasites of hamadryas baboons Papio hamadryas in the western and northern regions of Saudi Arabia. J Trop Med Hyg 98:431–439

    CAS  PubMed  Google Scholar 

  • Goldberg TL, Gillespie TR, Rwego IB, Wheeler E, Estoff EL, Chapman CA (2007) Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biol Conserv 135:511–517

    Article  Google Scholar 

  • Good RC, May BD, Kawatomari T (1969) Enteric pathogens in monkeys. J Bacteriol 97:1048–1055

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gorski L, Parker CT, Liang A, Cooley MB, Jay-Russell MT, Gordus AG, Atwill ER, Mandrell RE (2011) Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl Environ Microbiol 77:2734–2748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gotoh S, Takenaka O, Watanabe K, Hamada Y, Kawamoto Y, Watanabe T, Suryobroto B, Sajuthi D (2001) Hematological values and parasite fauna in free-ranging Macaca hecki and the M. hecki/M. tonkeana hybrid group of Sulawesi Island, Indonesia. Primates 42:27–34

    Article  Google Scholar 

  • Griffin RH, Nunn CL (2012) Community structure and the spread of infectious disease in primate social networks. Evol Ecol 26:779–800

    Article  Google Scholar 

  • Gumert MD (2011) A common monkey of Southeast Asia: longtailed macaque populations, ethnophoresy, and their occurrence in human environments. In: Gumert MD, Fuentes A, Jones-Engel L (eds) Monkeys on the edge: ecology and management of long-tailed macaques and their interface with humans. Cambridge University Press, Cambridge, pp 3–43

    Chapter  Google Scholar 

  • Harper KN, Fyumagwa RD, Hoare R, Wambura PN, Coppenhaver DH, Sapolsky RM, Alberts SC, Tung J, Rogers J, Kilewo M et al (2012) Treponema pallidum infection in the wild baboons of east Africa: distribution and genetic characterization of the strains responsible. PLoS ONE 7:e50882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasegawa M, Kishino H, Yano TA (1985) Dating of the human ape splitting by a molecular clock of mitochondrial-DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Herikstad H, Motarjemi Y, Tauxe RV (2002) Salmonella surveillance: a global survey of public health serotyping. Epidemiol Infect 129:1–8

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffman TS, O’Riain MJ (2011) The spatial ecology of chacma baboons (Papio ursinus) in a human-modified environment. Int J Primatol 32:308–328

    Article  Google Scholar 

  • Huffman MA, Chapman CA (2009) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge

    Google Scholar 

  • Interagency Food Safety Analytics Collaboration (IFSAC) Project (2015). Foodborne illness source attribution estimates for Salmonella, Escherichia coli O157 (E. coli O157), Listeria monocytogenes (Lm), and Campylobacter using outbreak surveillance data. Centers for Disease Control and Prevention, the U.S. Food and Drug Administration, the US Department of Agriculture

  • Jones-Engel L, Engel GA, Schillaci MA, Babo R, Froehlich J (2001) Detection of antibodies to selected human pathogens among wild and pet macaques (Macaca tonkeana) in Sulawesi, Indonesia. Am J Primatol 54:171–178

    Article  CAS  PubMed  Google Scholar 

  • Jones-Engel L, Steinkraus KA, Murray SM, Engel GA, Grant R, Aggimarangsee N, Lee BPYH, May C, Schillaci MA, Somgrid C et al (2007) Sensitive assays for simian foamy viruses reveal a high prevalence of infection in commensal, free-ranging Asian monkeys. J Virol 81:7330–7337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kalter SS, Kuntz RE, Myers BJ, Eugster AK, Rodriguez AR, Benke M, Kalter GV (1968) The collection of biomedical specimens from baboons (Papio sp.) Kenya, 1966. Primates 9:123–139

    Article  Google Scholar 

  • Kaur T, Singh J (2009) Primate-parasitic zoonoses and anthropozoonoses: a literature review. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 199–230

    Google Scholar 

  • Kilonzo C, Li X, Vivas E, Jay-Russell MT, Fernandez K, Atwill ER (2013) Prevalence of and risk factors associated with fecal shedding of zoonotic food-borne pathogens by wild rodents inhabiting a major agricultural region of central California. Appl Environ Microbiol 79:6337

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kotloff KL, Winickoff JP, Ivanoff B, Clemens JD, Swerdlow DL, Sansonetti PJ, Adak GK, Levine MM (1999) Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull WHO 77:651–666

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lane KE, Holley C, Hollocher H, Fuentes A (2011) The anthropogenic environment lessens the intensity and prevalence of gastrointestinal parasites in Balinese long-tailed macaques (Macaca fascicularis). Primates 52:117–128

    Article  PubMed  Google Scholar 

  • Lee K-S, Divis PCS, Zakaria SK, Matusop A, Julin RA, Conway DJ, Cox-Singh J, Singh B (2011) Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Path 7:e1002015

    Article  CAS  Google Scholar 

  • MacIntosh AJJ, Jacobs A, Garcia C, Shimizu K, Mouri K, Huffman MA, Hernandez AD (2012) Monkeys in the middle: parasite transmission through the social network of a wild primate. PLoS ONE 7:e51144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malik I, Seth PK, Southwick CH (1984) Population growth of free-ranging rhesus monkeys at Tughlaqabad. Am J Primatol 7:311–321

    Article  Google Scholar 

  • Matsubayashi K, Gotoh S, Kawamoto Y, Watanabe T, Nozawa K, Takasaka M, Narita T, Griffiths O, Stanley M-A (1992) Clinical examinations on crab-eating macaques in Mauritius. Primates 33:281–288

    Article  Google Scholar 

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

    Google Scholar 

  • Nunn CL (2012) Primate disease ecology in comparative and theoretical perspective. Am J Primatol 74:497–509

    Article  PubMed  Google Scholar 

  • Nunn CL, Altizer SM (2006) Infectious diseases in primates: behavior, ecology and evolution. Oxford University Press, Oxford

    Book  Google Scholar 

  • Pedersen A, Poss M, Nunn CL, Altizer SM (2005) Patterns of host specificity and transmission among parasites of free-living primates. Int J Parasitol 35:647–657

    Article  PubMed  Google Scholar 

  • Radhakrishna S (2013) The gulf between men and monkeys. In: Radhakrishna S, Huffman MA, Sinha A (eds) The macaque connection: cooperation and conflict between humans and macaques. Springer, New York, pp 3–18

    Chapter  Google Scholar 

  • Radhakrishna S, Huffman MA, Sinha A (2013) The macaque connection: cooperation and conflict between humans and macaques. Springer, New York

    Book  Google Scholar 

  • Rwego IB, Isabirye-Basuta G, Gillespie TR, Goldberg TL (2008) Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv Biol 22:1600–1607

    Article  PubMed  Google Scholar 

  • Sapolsky RM, Else JG (1987) Bovine tuberculosis in a wild baboon population—epidemiologic aspects. J Med Primatol 16:229–235

    CAS  PubMed  Google Scholar 

  • Southwick CH, Siddiqi MF (1994) Population status of nonhuman primates in Asia, with emphasis on rhesus macaques in India. Am J Primatol 34:51–59

    Article  Google Scholar 

  • Southwick CH, Siddiqi F (2011) India’s rhesus population: protection versus conservation management. In: Gumert MD, Fuentes A, Jones-Engel L (eds) Monkeys on the edge: ecology and management of long-tailed macaques and their interface with humans. Cambridge University Press, Cambridge, pp 275–292

    Chapter  Google Scholar 

  • Sterck EHM (1998) Female dispersal, social organization, and infanticide in langurs: are they linked to human disturbance? Am J Primatol 44:235–254

    Article  CAS  PubMed  Google Scholar 

  • Takasaka M, Honjo S, Fujiwara T, Hagiwara T, Ogawa H, Imaizumi K (1964) Shigellosis in cynomologous monkeys (Macaca irus). Jpn J Med Sci Biol 17:259–265

    Article  CAS  PubMed  Google Scholar 

  • Taylor LH, Latham SM, Woolhouse MEJ (2001) Risk factors for human disease emergence. Philos Trans R Soc B Biol Sci 356:983–989

    Article  CAS  Google Scholar 

  • VanderWaal KL, Atwill ER, Hooper S, Buckle K, McCowan B (2013) Network structure and prevalence of Cryptosporidium in Belding’s ground squirrels. Behav Ecol Sociobiol 67:1951–1959

    Article  Google Scholar 

  • VanderWaal KL, Atwill ER, Isbell LA, McCowan B (2014a) Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis). J Anim Ecol 83:406–414

    Article  PubMed  Google Scholar 

  • VanderWaal KL, Wang H, McCowan B, Fushing H, Isbell LA (2014b) Multilevel social organization and space use in reticulated giraffe (Giraffa camelopardalis). Behav Ecol 25:17–26

    Article  Google Scholar 

Download references

Acknowledgments

We thank the Wildlife Institute of India, the Central Zoo Authority of India and the Ministry of Environment, Forest and Climate Change in India for permission to conduct this research. We also thank Drs. S. P. Goyal and K. Sankar for their time and use of laboratory space and Mr. Sen for his patience in coordinating in-country logistics. This pilot study was made possible by funds received through University of California Davis UOIP Seed Grant and International Primatological Society Conservation Grant. The research was approved by the Wildlife Institute of India and India’s Central Zoo Authority and conducted in accordance with terms drawn up in the Memorandum of Understanding (MOU) signed by all participating institutions: the University of California Davis, the Central Zoo Authority, and the Wildlife Institute of India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Brianne A. Beisner.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Beisner, B.A., Balasubramaniam, K.N., Fernandez, K. et al. Prevalence of enteric bacterial parasites with respect to anthropogenic factors among commensal rhesus macaques in Dehradun, India. Primates 57, 459–469 (2016). https://doi.org/10.1007/s10329-016-0534-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-016-0534-2

Keywords

Navigation