Skip to main content

The Role of Landscape Structure in Primate Crop Feeding: Insights from Rhesus Macaques (Macaca mulatta) in Northern India

Abstract

Human-modified landscapes play an important role in supporting the survival of primate populations, but they may also facilitate human–primate interactions, possibly leading to negative outcomes. We conducted a scalar investigation of the role of landscape structure in shaping the intensity of crop feeding by a generalist primate species, the rhesus macaque (Macaca mulatta) in northern India. At the species level, we used behavioral sampling techniques to assess habitat selection by two groups of rhesus macaques. At the landscape level, we used GIS-based analyses to quantify landscape structure in terms of class-level and patch-level metrics and correlated it with macaque crop feeding intensities. We found that, on average, both study groups spent only 15% of their total feeding time on cultivars. However, they spent a large proportion of their feeding (BH: 75% and CH: 36%) and ranging (BH: 72% and CH: 39%) time in agroecosystem habitats. Landscape level analysis showed that crop feeding intensity was not related to total area under cultivation. Instead, macaque crop feeding intensity was positively correlated to the arrangement of deciduous forest patches beside cultivated area patches. Our findings call for careful appraisal of landscape management practices as a potential mitigation strategy for primate crop-depredation in such human-modified landscapes.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. Agetsuma, N. (2007). Ecological function losses caused by monotonous land use induce crop raiding by wildlife on the island of Yakushima, southern Japan. Ecological Research, 22, 390–402. https://doi.org/10.1007/978-4-431-73238-9_4.

    Article  Google Scholar 

  2. Ahsan, M. F., & Uddin, M. M. (2014). Human-rhesus monkey conflict at Rampur Village under Monohardi Upazila in Narsingdi District of Bangladesh. Journal of Threatened Taxa, 6(6), 5905–5908.

    Article  Google Scholar 

  3. Altieri, M. A., & Koohafkan, P. (n.d.). Globally Important Ingenious Agricultural Heritage Systems (GIAHS): Extent, significance, and implications for development. http://www.fao.org/docrep/015/ap021e/ap021e.pdf

  4. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49(3/4), 227–267.

    CAS  Article  Google Scholar 

  5. Anand, S., Binoy, V. V., & Radhakrishna, S. (2018). The monkey is not always a god: Attitudinal differences toward crop-raiding macaques and why it matters for conflict mitigation. Ambio, 47(6), 711–720. https://doi.org/10.1007/s13280-017-1008-5.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Anderson, J., Rowcliffe, J. M., & Cowlishaw, G. (2007). Does the matrix matter? A forest primate in a complex agricultural landscape. Biological Conservation, 135(2), 212–222. https://doi.org/10.1016/j.biocon.2006.10.022.

    Article  Google Scholar 

  7. Boulton, A. M., Horrocks, J. A., & Baulu, J. (1996). The Barbados vervet monkey (Cercopithecus aethiops sabaeus): Changes in population size and crop damage, 1980–1994. International Journal of Primatology, 17(5), 831–844. https://doi.org/10.1007/BF02735267.

    Article  Google Scholar 

  8. Chauhan, A., & Pirta, R. S. (2010). Agonistic interactions between humans and two Species of Monkeys (rhesus monkey Macaca mulatta and Hanuman langur Semnopithecus entellus) in Shimla, Himachal Pradesh. Journal of Psychology, 1(1), 9–14.

    Article  Google Scholar 

  9. Dhiman, S. P., & Mohan, L. (2014). Prospects of managing human-rhesus monkey conflict in Himachal Pradesh, India. In Human-wildlife conflict in the mountains of SAARC region: Compilation of successful management strategies and practices (pp. 48–60). SAARC Forestry Centre.

  10. Engeman, R. M., Laborde, J. E., Constantin, B. U., Shwiff, S. A., Hall, P., Duffiney, A., & Luciano, F. (2010). The economic impacts to commercial farms from invasive monkeys in Puerto Rico. Crop Protection, 29(4), 401–405. https://doi.org/10.1016/j.cropro.2009.10.021.

    Article  Google Scholar 

  11. Estrada, A. (2006). Human and non-human primate co-existence in the Neotropics: A preliminary view of some agricultural practices as a complement for primate conservation. Ecological and Environmental Anthropology, 2(2), 17–29 http://digitalcommons.unl.edu/icwdmeea/3/.

    Google Scholar 

  12. Estrada, A., & Coates-Estrada, R. (1996). Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. International Journal of Primatology, 17(5), 759–783. https://doi.org/10.1007/BF02735263.

    Article  Google Scholar 

  13. Estrada, A., Raboy, B. E., & Oliveira, L. C. (2012). Agroecosystems and primate conservation in the tropics: A review. American Journal of Primatology, 74(8), 696–711. https://doi.org/10.1002/ajp.22033.

    Article  PubMed  Google Scholar 

  14. Fashing, P. J. (2001). Activity and ranging patterns of guerezas in the Kakamega Forest: Intergroup variation and implications for intragroup feeding competition. International Journal of Primatology, 22(4), 549–577. https://doi.org/10.1023/A:1010785517852.

    Article  Google Scholar 

  15. Goldman, A., Hartter, J., Southworth, J., & Binford, M. (2008). The human landscape around the Island Park: Impacts and responses to Kibale National Park. In R. Wrangham & E. Ross (Eds.), Science and conservation in African forests: The benefits of long-term research (pp. 129–144). Cambridge University Press. https://doi.org/10.1017/CBO9780511754920.014

  16. Gupta, A. K. (2001). Status of the primates in Tripura. In ENVIS bulletin: Wildlife and protected areas, non-human primates of India (pp. 127–135). Wildlife Institute of India.

  17. Hill, C. M. (1997). Crop-raiding by wild vertebrates: The farmer’s perspective in an agricultural community in western Uganda. International Journal of Pest Management, 43(1), 77–84. https://doi.org/10.1080/096708797229022.

    Article  Google Scholar 

  18. Hill, C. M. (2005). People, crops and primates: A conflict of interests. In J. Paterson & J. Wallis (Eds.), Commensalism and conflict: The human-primate interface (pp. 40–59). American Society of Primatologists.

  19. Hill, C. M. (2017). Crop raiding. In The International Encyclopedia of Primatology, 1–5. https://doi.org/10.1002/9781119179313.wbprim0109

  20. Hockings, K. J. (2016). Mitigating human-nonhuman primate conflict. In The International Encyclopaedia of Primatology, 1–8. https://doi.org/10.1002/9781119179313.wbprim0053

  21. Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2009). Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: Feeding dynamics in a human-influenced environment. American Journal of Primatology, 71(8), 636–646. https://doi.org/10.1002/ajp.20698.

    Article  PubMed  Google Scholar 

  22. Hockings, K. J., & McLennan, M. R. (2012). From forest to farm: Systematic review of cultivar feeding by chimpanzees—management implications for wildlife in anthropogenic landscapes. PLoS ONE, 7(4). https://doi.org/10.1371/journal.pone.0033391.

  23. Hockings, K. J., McLennan, M. R., Carvalho, S., Ancrenaz, M., Bobe, R., Byrne, R. W., Dunbar, R. I. M., Matsuzawa, T., McGrew, W. C., Williamson, E. A., Wilson, M. L., Wood, B., Wrangham, R. W., & Hill, C. M. (2015). Apes in the Anthropocene: Flexibility and survival. Trends in Ecology and Evolution. https://doi.org/10.1016/j.tree.2015.02.002

  24. Holzner, A., Ruppert, N., Swat, F., Schmidt, M., Weiß, B.M., Villa, G., Mansor, A., Sah, S.A.M., Engelhardt, A., Kühl, H. and Widdig, A. (2019). Macaques can contribute to greener practices in oil palm plantations when used as biological pest control. Current Biology, 29(5), R1066-R1067. https://doi.org/10.1016/j.cub.2019.09.011.

  25. Huang, C., Li, X. Y., Shi, L. J., & Jiang, X. L. (2018). Patterns of human-wildlife conflict and compensation practices around Daxueshan Nature Reserve, China. Zoological Research, 39(6), 406–412. https://doi.org/10.24272/j.issn.2095-8137.2018.056.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Imaki, H., Koganezawa, M., & Maruyama, N. (1994). Habitat selection and forest edge use by Japanese monkeys in the Nikko and Imaichi Area, Central Honshu, Japan. Biosphere Conservation, 7(2), 87–96.

    Google Scholar 

  27. Imam, E., Yahya, H. S. A., & Malik, I. (2002). A successful mass translocation of commensal rhesus monkeys Macaca mulatta in Vrindaban, India. Oryx, 36(1), 87–39. https://doi.org/10.1017/S0030605301000011.

    Article  Google Scholar 

  28. Jaman, M. F., & Huffman, M. A. (2013). The effect of urban and rural habitats and resource type on activity budgets of commensal rhesus macaques (Macaca mulatta) in Bangladesh. Primates, 54(1), 49–59. https://doi.org/10.1007/s10329-012-0330-6.

    Article  PubMed  Google Scholar 

  29. Kansky, R., & Knight, A. T. (2014). Key factors driving attitudes towards large mammals in conflict with humans. Biological Conservation, 179, 93–105.

    Article  Google Scholar 

  30. Knight, J. (2000). Natural enemies: People-wildlife conflicts in anthropological perspective. Routledge.

  31. Lafleur, M., & Gould, L. (2009). Feeding outside the forest: The importance of crop raiding and an invasive weed in the diet of gallery forest ring-tailed lemurs (Lemur catta) following a cyclone at the Beza Mahafaly Special Reserve, Madagascar. Folia Primatologica, 80(3), 233–246. https://doi.org/10.1159/000240968.

    CAS  Article  Google Scholar 

  32. Lemessa, D., Hylander, K., & Hambäck, P. (2013). Composition of crops and land-use types in relation to crop raiding pattern at different distances from forests. Agriculture, Ecosystems and Environment, 167, 71–78. https://doi.org/10.1016/j.agee.2012.12.014.

    Article  Google Scholar 

  33. Li, W., & Essen, E. V. (2020). Guarding crops from monkey troops: farmer-monkey interaction near a nature reserve in Guangxi, China. Environmental Sociology, 7(1), 12–24. https://doi.org/10.1080/23251042.2020.1811004.

  34. Linkie, M., Dinata, Y., Nofrianto, A., & Leader-Williams, N. (2007). Patterns and perceptions of wildlife crop raiding in and around Kerinci Seblat National Park, Sumatra. Animal Conservation, 10(1), 127–135. https://doi.org/10.1111/j.1469-1795.2006.00083.x.

    Article  Google Scholar 

  35. Manly, B.F.J., McDonald, L.L., Thomas, D.L., McDonald, T.L., Erickson, W.P., (2002). Resource Selection by Animals: Statistical Design and Analysis for Field Studies (2nd ed). Kluwer Academic Publishers.

  36. McGarigal, K. (2015). FRAGSTATS help. http://www.umass.edu/landeco/research/fragstats/documents/fragstats.help.4.2.pdf

  37. Meijaard, E., Buchori, D., Hadiprakarsa, Y., Utami-Atmoko, S. S., Nurcahyo, A., Tjiu, A., Prasetyo, D., Nardiyono, Christie, L., Ancrenaz, M., Abadi, F., Antoni, I. N. G., Armayadi, D., Dinato, A., Ella, Gumelar, P., Indrawan, T. P., Kussaritano, Munajat, C., Priyono, C. W. P., et al. (2011). Quantifying killing of orangutans and human-orangutan conflict in Kalimantan, Indonesia. PLoS ONE, 6(11), 1–10. https://doi.org/10.1371/journal.pone.0027491

  38. Mekonnen, A., Fashing, P. J., Bekele, A., Hernandez-Aguilar, R. A., Rueness, E. K., Nguyen, N., & Stenseth, N. C. (2017). Impacts of habitat loss and fragmentation on the activity budget, ranging ecology and habitat use of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian Highlands. American Journal of Primatology, 79(7), 1–13. https://doi.org/10.1002/ajp.22644.

    Article  Google Scholar 

  39. Mekonnen, A., Fashing, P. J., Bekele, A., & Stenseth, N. C. (2020). Use of cultivated foods and matrix habitat by Bale monkeys in forest fragments: Assessing local human attitudes and perceptions. American Journal of Primatology, 82(4), 1–12. https://doi.org/10.1002/ajp.23074.

    Article  Google Scholar 

  40. Mikich, S. B., & Liebsch, D. (2014). Assessment of food supplementation and surveillance as techniques to reduce damage caused by black capuchin monkeys Sapajus nigritus to forest plantations. Current Zoology, 60(5), 581–590. https://doi.org/10.1093/czoolo/60.5.581.

    Article  Google Scholar 

  41. Ministry of Environment Forest and Climate Change. (2017). Notification for declaration of rhesus macaque as a vermin species. http://hpforest.nic.in/upload/contents/File-148.pdf

  42. Mishra, C. (1997). Livestock depredation by large carnivores in the Indian trans-Himalaya: conflict perceptions and conservation prospects. Environmental Conservation, 24, 338–343. https://doi.org/10.1017/S0376892997000441.

  43. Mochizuki, S., & Murakami, T. (2011a). Change in habitat selection by Japanese macaques (Macaca fuscata) and habitat fragmentation analysis using temporal remotely sensed data in Niigata Prefecture, Japan. International Journal of Applied Earth Observation and Geoinformation, 13(4), 562–571. https://doi.org/10.1016/j.jag.2011.02.006.

    Article  Google Scholar 

  44. Mochizuki, S., & Murakami, T. (2011b). The influence of forest boundary shape and environmental variables on farmland invasion by wild Japanese macaques. Journal of Forest Planning, 16, 223–231.

    Article  Google Scholar 

  45. Mochizuki, S., & Murakami, T. (2013). Scale dependent effects in resource selection by crop-raiding Japanese macaques in Niigata Prefecture, Japan. Applied Geography, 42, 13–22. https://doi.org/10.1016/j.apgeog.2013.04.016.

    Article  Google Scholar 

  46. Naughton-Treves, L., & Treves, A. (2005) Socio-ecological factors shaping local support for wildlife: Crop-raiding by elephants and other wildlife in Africa. In R. Woodroffe, S. Thirgood, & A. Rabinowitz (Eds.), People and wildlife: Conflict or coexistence? (pp. 253–277). Cambridge University Press.

  47. Nekaris, K. A. I., Boulton, A., & Nijman, V. (2013). An ethnoprimatological approach to assessing levels of tolerance between human and commensal non-human primates in Sri Lanka. Journal of Anthropological Sciences, 91, 219–231. https://doi.org/10.4436/JASS.91008.

    Article  PubMed  Google Scholar 

  48. Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: The primates of Kibale National Park, Uganda. International Journal of Primatology, 21(4), 587–611. https://doi.org/10.1023/A:1005509119693.

    Article  Google Scholar 

  49. Pebsworth, P., & Radhakrishna, S. (2020). Using conditioned taste aversion to reduce human-nonhuman primate conflict: A comparison of four potentially illness-inducing drugs. Applied Animal Behaviour Science, 225(May 2019), 104948. https://doi.org/10.1016/j.applanim.2020.104948.

    Article  Google Scholar 

  50. Pozo-Montuy, G., Serio-Silva, J. C., Chapman, C. A., & Bonilla-Sánchez, Y. M. (2013). Resource use in a landscape matrix by an arboreal primate: Evidence of supplementation in black howlers (Alouatta pigra). International Journal of Primatology, 34(4), 714–731. https://doi.org/10.1007/s10764-013-9691-y.

    Article  Google Scholar 

  51. Priston, N. E. C., & McLennan, M. R. (2013). Managing humans, managing macaques: Human–macaque conflict in Asia and Africa. In S. Radhakrishna, M. A. Huffman, & A. Sinha (Eds.), The macaque connection: Cooperation and conflict between humans and macaques (pp. 225–250). Developments in Primatology: Progress and Prospects. Springer Science+Business Media.

  52. Raboy, B. E., Christman, M. C., & Dietz, J. M. (2004). The use of degraded and shade cocoa forests by Endangered golden-headed lion tamarins Leontopithecuschrysomelas. Oryx, 38(1), 75–83. https://doi.org/10.1017/S0030605304000122.

    Article  Google Scholar 

  53. Radhakrishna, S., Huffman, M. A., & Sinha, A., Eds. (2013). The macaque connection: Cooperation and conflict between humans and macaques. Developments in Primatology: Progress and Prospects. Springer Science+Business Media.

  54. Regmi, G. R., Nekaris, K. A. I., Kandel, K., & Nijman, V. (2013). Crop-raiding macaques: Predictions, patterns and perceptions from Langtang National Park, Nepal. Endangered Species Research, 20(3), 217–226. https://doi.org/10.3354/esr00502.

    Article  Google Scholar 

  55. Riley, E. P. (2007). The human–macaque interface: Conservation implications of current and future overlap and conflict in Lore Lindu National Park, Sulawesi, Indonesia. American Anthropologist, 109(3), 473–484. https://doi.org/10.1525/AA.2007.109.3.473.474.

    Article  Google Scholar 

  56. Riley, E. P., & Wade, T. W. (2016). Adapting to Florida’s riverine woodlands: The population status and feeding ecology of the silver river rhesus macaques and their interface with humans. Primates, 57(2), 195–210. https://doi.org/10.1007/s10329-016-0517-3.

    Article  PubMed  Google Scholar 

  57. Ruppert, N., Holzner, A., See, K. W., Gisbrecht, A., & Beck, A. (2018). Activity budgets and habitat use of wild southern pig-tailed macaques (Macaca nemestrina) in oil palm plantation and forest. International Journal of Primatology, 39, 237–251. https://doi.org/10.1007/s10764-018-0032-z.

    Article  Google Scholar 

  58. Sahoo, S. K., & Mohnot, S. M. (2004). A survey of crop damage by rhesus monkeys and Hanuman langur in Himachal Pradesh, India. Tiger Paper, 31, 1–5. https://doi.org/10.1017/CBO9781107415324.004.

    Article  Google Scholar 

  59. Saj, T. L., Sicotte, P., & Paterson, J. D. (2001). The conflict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda. African Journal of Ecology, 39(2), 195–199. https://doi.org/10.1046/j.0141-6707.2000.00299.x.

    Article  Google Scholar 

  60. Sambyal, P., Kumar, S., & Sahi, D. N. (2009). Translocation of urban rhesus monkeys (Macaca mulatta) of Mubarak Mandi Jammu to forest areas of Nagrot. Tiger Paper, 36(2), 11–13.

    Google Scholar 

  61. Saraswat, R., Sinha, A., & Radhakrishna, S. (2015). A god becomes a pest? Human-rhesus macaque interactions in Himachal Pradesh, northern India. European Journal of Wildlife Research, 61, 435–443. https://doi.org/10.1007/s10344-015-0913-9.

    Article  Google Scholar 

  62. Sengupta, A., McConkey, K. R., & Radhakrishna, S. (2015). Primates, provisioning and plants: Impacts of human cultural behaviours on primate ecological functions. PLoS ONE, 10(11). https://doi.org/10.1371/journal.pone.0140961.

  63. Sengupta, A., & Radhakrishna, S. (2016). Influence of fruit availability on fruit consumption in a generalist primate, the rhesus macaque Macaca mulatta. International Journal of Primatology, 37(6), 703–717. https://doi.org/10.1007/s10764-016-9933-x.

    Article  Google Scholar 

  64. Sillero-Zubiri, C., & Switzer, D. (2001). Crop raiding primates: searching for alternative, humane ways to resolve conflict with farmers in Africa. People and Wildlife Initiative. Wildlife Conservation Research Unit, Oxford University.www.peopleandwildlife.org.uk/crmanuals/CropRaidingPrimatesP&WManual

  65. Singh, V., & Thakur, M. (2012). Rhesus macaque and associated problems in Himachal Pradesh-India. TAPROBANICA, 4(2), 112–116 http://www.sljol.info/index.php/TAPRO/article/viewFile/5066/4045.

    CAS  Article  Google Scholar 

  66. Treves, A., Wallace, R. B., Naughton-Treves, L., & Morales, A. (2006). Co-managing human-wildlife conflicts: A review. Human Dimensions of Wildlife, 11, 383–396.

    Article  Google Scholar 

  67. Turner, M.G. & Gardner, R. H. (2015). Landscape Ecology in Theory and Practice. Springer-Verlag.

  68. Vandermeer, J. H., Ed. (2003). Tropical agroecosystems. CRC Press.

  69. Warren, Y. (2008). Crop-raiding baboons (Papio anubis) and defensive farmers: A West African perspective. West African Journal of Applied Ecology, 14, 1–11. https://doi.org/10.4314/wajae.v14i1.44705.

    Article  Google Scholar 

  70. Weibull, A. C., Östman, Ö., & Granqvist, Å. (2003). Species richness in agroecosystems: The effect of landscape, habitat and farm management. Biodiversity and Conservation, 12(7), 1335–1355. https://doi.org/10.1023/A:1023617117780.

    Article  Google Scholar 

  71. Williams-Guillén, K., McCann, C., Martínez Sánchez, J. C., & Koontz, F. (2006). Resource availability and habitat use by mantled howling monkeys in a Nicaraguan coffee plantation: Can agroforests serve as core habitat for a forest mammal? Animal Conservation, 9(3), 331–338. https://doi.org/10.1111/j.1469-1795.2006.00042.x.

    Article  Google Scholar 

  72. Yamada, A., & Muroyama, Y. (2010). Effects of vegetation type on habitat use by crop-raiding Japanese macaques during a food-scarce season. Primates, 51(2), 159–166. https://doi.org/10.1007/s10329-009-0183-9.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to express our sincere thanks to Vijay Raput and Jagdish Chand for their assistance in fieldwork. We are also extremely thankful for the support provided by all the villagers in our study area during the period of field data collection. SA was supported by an institutional fellowship from National Institute of Advanced Studies during the period of this study.

Author information

Affiliations

Authors

Contributions

SA and SR conceived the study and developed methodology. SA conducted field work and performed statistical analyses. SV collaborated in data analysis. SA and SR wrote the manuscript.

Corresponding author

Correspondence to Shaurabh Anand.

Additional information

Handling Editor: Joanna M. Setchell.

Supplementary Information

ESM 1

(DOCX 16 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Anand, S., Vaidyanathan, S. & Radhakrishna, S. The Role of Landscape Structure in Primate Crop Feeding: Insights from Rhesus Macaques (Macaca mulatta) in Northern India. Int J Primatol 42, 764–780 (2021). https://doi.org/10.1007/s10764-021-00238-y

Download citation

Keywords

  • Agroecosystems
  • Deciduous vegetation
  • Human-primate interaction
  • Land use management
  • Rhesus macaque (Macaca mulatta)