, Volume 57, Issue 2, pp 221–230 | Cite as

Performing monkeys of Bangladesh: characterizing their source and genetic variation

  • M. Kamrul HasanEmail author
  • M. Mostafa Feeroz
  • Lisa Jones-Engel
  • Gregory A. Engel
  • Sharmin Akhtar
  • Sree Kanthaswamy
  • David Glenn Smith
Original Article


The acquisition and training of monkeys to perform is a centuries-old tradition in South Asia, resulting in a large number of rhesus macaques kept in captivity for this purpose. The performing monkeys are reportedly collected from free-ranging populations, and may escape from their owners or may be released into other populations. In order to determine whether this tradition involving the acquisition and movement of animals has influenced the population structure of free-ranging rhesus macaques in Bangladesh, we first characterized the source of these monkeys. Biological samples from 65 performing macaques collected between January 2010 and August 2013 were analyzed for genetic variation using 716 base pairs of mitochondrial DNA. Performing monkey sequences were compared with those of free-ranging rhesus macaque populations in Bangladesh, India and Myanmar. Forty-five haplotypes with 116 (16 %) polymorphic nucleotide sites were detected among the performing monkeys. As for the free-ranging rhesus population, most of the substitutions (89 %) were transitions, and no indels (insertion/deletion) were observed. The estimate of the mean number of pair-wise differences for the performing monkey population was 10.1264 ± 4.686, compared to 14.076 ± 6.363 for the free-ranging population. Fifteen free-ranging rhesus macaque populations were identified as the source of performing monkeys in Bangladesh; several of these populations were from areas where active provisioning has resulted in a large number of macaques. The collection of performing monkeys from India was also evident.


Performing monkey Rhesus macaque Performer Bedey Bangladesh 



This research was supported by a base grant to the California National Primate Research Center from the National Center for Research Resources at the National Institutes of Health (RR000169-48 to DGS; RR005090 and RR025781 to DGS) and the National Institute of Allergy and Infectious Diseases (R01 AI078229; R01AI078229-03S1; R03 AI064865 to LJE). We are thankful to the Forest Department of Bangladesh for their permission and constant support during fieldwork and to the authority of Wildlife Rescue Center (WRC) of the Department of Zoology, Jahangirnagar University for their assistance with logistics during sample collection.

Supplementary material

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Supplementary material 1 (PDF 127 kb)
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Supplementary material 4 (PDF 24 kb)


  1. Akhtar S (2014) Monkey performers in Bangladesh: monkey population, health care, human-monkey interaction and socio-economic condition of the monkey owners (M. Phil dissertation). Department of Zoology, Jahangirnagar University, Savar, Dhaka, BangladeshGoogle Scholar
  2. Bensasson D, Zhang D-X, Hartle DL, Hewitt GM (2001) Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends Ecol Evol 16:314–321CrossRefPubMedGoogle Scholar
  3. Brown WM, George M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci USA 76:1967–1971CrossRefPubMedPubMedCentralGoogle Scholar
  4. Collura RV, Stewart CB (1995) Insertions and duplications of mtDNA in the nuclear genomes of Old World monkeys and hominoids. Nature 378:485–489CrossRefPubMedGoogle Scholar
  5. Engel GA, Small CT, Soliven K, Soliven K, Feeroz MM, Wang X, Hasan MK, Oh G, Alam SMR, Craig KL, Jackson DL, Matsen FA IV, Linial ML, Jones-Engel L (2013) Zoonotic simian foamy virus in Bangladesh reflects diverse patterns of transmission and co-infection. Emerg Microbes Infect 2:e58CrossRefPubMedPubMedCentralGoogle Scholar
  6. Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol Res 10(3):564–567CrossRefGoogle Scholar
  7. Feeroz MM (2001) Species diversity and population density of non-human primates in north-east and south-east of Bangladesh. Ecoprint 8:53–57Google Scholar
  8. Feeroz MM, Hasan MK, Khan MMH (2011) Biodiversity of protected areas of Bangladesh, vol I. Rema-Kalenga Wildlife Sanctuary, Bangladesh. BioTrack. Arannayk FoundationGoogle Scholar
  9. Feeroz MM, Soliven K, Small CT, Engel GA, Pacheco MA, Yee JL, Wang X, Hasan MK, Oh G, Levine KL, Alam SMR, Craig KL, Jackson DL, Lee EG, Barry PA, Larche NW, Escalante AA, Matsen FA IV, Linial ML, Jones-Engel L (2013) Population dynamics of Rhesus macaques and associated foamy virus in Bangladesh. Emerg Microbes Infect 2:e29CrossRefPubMedPubMedCentralGoogle Scholar
  10. Forster P, Harding R, Torroni A, Bandelt HJ (1996) Origin and evolution of Native American mtDNA variation: a reappraisal. A J Hum Gen 59:935Google Scholar
  11. Giles RE, Blanc H, Cann HM, Wallace DC (1980) Maternal inheritance of human mitochondrial DNA. Proc Natl Acad Sci USA 77:6715–6719CrossRefPubMedPubMedCentralGoogle Scholar
  12. Hasan MK, Aziz MA, Alam SR, Kawamoto Y, Jones-Engel L, Kyes RC, Akhtar S, Begum S, Feeroz MM (2013) Distribution of rhesus macaques (Macaca mulatta) in Bangladesh: inter-population variation in group size and composition. Primate Conserv 26:125–132CrossRefGoogle Scholar
  13. Hasan MK, Feeroz MM, Jones-Engel L, Engel GA, Smith DG (2014) Diversity and molecular phylogeny of Rhesus macaques (Macaca mulatta) of Bangladesh. Am J Primatol 76:1074–1104CrossRefGoogle Scholar
  14. Hutchinson CA III, Newbold JE, Potter SS, Edgell EH (1974) Maternal inheritance of mammalian mitochondrial DNA. Nature 251:536–538CrossRefGoogle Scholar
  15. Islam M, Ameen M, Nishat A (2000) Red book of threatened mammals of Bangladesh. IUCN, DhakaGoogle Scholar
  16. Islam N, Jamal AA, Chowdhury AM (2003) Banglapedia: national encyclopedia of Bangladesh. Asiatic Society of Bangladesh, RamnaGoogle Scholar
  17. Jones-Engel L, Engel GA, Heidrich J, Chalise M, Poudel N, Barry PA, Allan JS, Grant R, Kyes R (2006) Temple monkeys and health implications of commensalism, Kathmandu, Nepal. Emerg Microbes Infect 12:900–906CrossRefGoogle Scholar
  18. Khan MAR (1982) Wildlife of Bangladesh: a checklist. University of Dhaka, DhakaGoogle Scholar
  19. Kyes RC, Jones-Engel L, Chalise MK, Engel G, Heidrich J, Grant R, Bajimaya SS, McDonough J, Smith DG, Ferguson B (2006) Genetic characterization of rhesus macaques (Macaca mulatta) in Nepal. Am J Primatol 68:445–455CrossRefPubMedGoogle Scholar
  20. Maksud AKM, Rasul I (2006) The Nomadic Bede community and their mobile school program. In: International conference on what works for the poorest: knowledge, policies and practices. BRAC Gazipur, Centre for Development Management, BangladeshGoogle Scholar
  21. Matsen FA IV, Small CT, Soliven K, Engel GA, Feeroz MM, Wang X, Craig KL, Hasan MK, Emerman M, Linial ML, Jones-Engel L (2014) A Novel Bayesian method for detection of APOBEC3-mediated hypermutation and its application to zoonotic transmission of simian foamy viruses. PLoS Comput Biol 10:e1003493. doi: 10.1371/journal.pcbi.1003493 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Pusey AE, Packer C (1987) Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, ChicagoGoogle Scholar
  23. Sade D (1972) A longitudinal study of the social behavior of Rhesus monkeys. In: Tuttle RH (ed) The functional and evolutionary biology of primates. Aldine, ChicagoGoogle Scholar
  24. Smith DG, McDonough JW (2005) Mitochondrial DNA variation in Chinese and Indian Rhesus macaques (Macaca mulatta). Am J Primatol 65:1–25CrossRefPubMedGoogle Scholar
  25. Smith DG, Mcdonough JW, George DA (2007) Mitochondrial DNA variation within and among regional populations of longtail macaques (Macaca fascicularis) in relation to other species of the fascicularis group of macaques. Am J Primatol 69:182–198CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2016

Authors and Affiliations

  • M. Kamrul Hasan
    • 1
    • 2
    Email author
  • M. Mostafa Feeroz
    • 2
  • Lisa Jones-Engel
    • 3
  • Gregory A. Engel
    • 3
  • Sharmin Akhtar
    • 2
  • Sree Kanthaswamy
    • 1
    • 4
  • David Glenn Smith
    • 1
  1. 1.Molecular Anthropology Laboratory, Department of AnthropologyUniversity of California, Davis (UC Davis)DavisUSA
  2. 2.Department of ZoologyJahangirnagar UniversitySavar, DhakaBangladesh
  3. 3.National Primate Research CenterUniversity of WashingtonSeattleUSA
  4. 4.Department of Environmental ToxicologyUniversity of California DavisDavisUSA

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