Abstract
Object manipulation and tool use by nonhuman primates have received considerable attention from primatologists and anthropologists, because of their broad implications for understanding the evolution of tool use in humans. To date, however, most of the studies on this topic have focused on apes, given their close evolutionary relationship with humans. In contrast, fewer studies on tool use and object manipulation have been conducted on monkeys. Documenting and studying object manipulation and tool use in species that are more distantly related to humans can provide a broader perspective on the evolutionary origins of this behavior. We present a detailed description of tool-aided behaviors and object manipulation by Nicobar long-tailed macaques (Macaca fascicularis umbrosus) living along the coastlines of Great Nicobar Island. We made observations from December 2018 to March 2019, using ad libitum and focal sampling methods. We observed behaviors related to object manipulation and tool use in six different behavioral contexts (foraging, hygiene, communication, play, self-directed and self-hygiene behavior) involving eight different types of objects: resonance rod, play object, rolling platform, scraping tool, dental groom, pounding substrate, leaves as grip pads and wipers, and stimulation tool. We observed that males were involved in tool use and object manipulation more frequently than females. Our results add to existing records of object manipulation, tool-use behavior, and tool variants displayed by nonhuman primates, showing that Nicobar macaques perform multiple and diverse tool-aided behaviors.
Similar content being viewed by others
Change history
12 August 2020
The original version of this article unfortunately contained mistakes in Methods and Acknowledgements sections.
References
Allritz, M., Tennie, C., & Call, J. (2013). Food washing and placer mining in captive great apes. Primates, 54(4), 361–370. https://doi.org/10.1007/s10329-013-0355-5.
Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 9(3/4), 227–267.
Arroyo, A., Hirata, S., Matsuzawa, T., & de la Torre, I. (2016). Nut cracking tools used by captive chimpanzees (Pan troglodytes) and their comparison with Early Stone Age percussive artefacts from Olduvai Gorge. PLoS One, 11(11), e0166788. https://doi.org/10.1371/journal.pone.0166788.
Barrett, B. J., Monteza-Moreno, C. M., Dogandžić, T., Zwyns, N., Ibáñez, A., & Crofoot, M. C. (2018). Habitual stone-tool-aided extractive foraging in white-faced capuchins, Cebus capucinus. Royal Society Open Science, 5(8), 181002. https://doi.org/10.1098/rsos.181002.
Beck, B. B. (1980). Animal tool behavior: The use and manufacture of tools by animals. New York: Garland STPM Press.
Boyd, R., & Silk, J. B. (2009). How humans evolved, 5th ed. New York: W. W. Norton.
Breuer, T., Ndoundou-Hockemba, M., & Fishlock, V. (2005). First observation of tool use in wild gorillas. PLoS Biology, 3(11), e380. https://doi.org/10.1371/journal.pbio.0030380.
Call, J., & Tomasello, M. (1994). The social learning of tool use by orangutans (Pongo pygmaeus). Human Evolution, 9(4), 297–313. https://doi.org/10.1007/BF02435516.
Carpenter, A. (1887). Monkeys opening oysters. Nature, 36(916), 53–53. https://doi.org/10.1038/036053d0.
Estienne, V., Cohen, H., Wittig, R. M., & Boesch, C. (2019). Maternal influence on the development of nut-cracking skills in the chimpanzees of the Taï forest, Côte d’Ivoire (Pan troglodytes verus). American Journal of Primatology, 81(7), e23022. https://doi.org/10.1002/ajp.23022.
Falótico, T., & Ottoni, E. B. (2014). Sexual bias in probe tool manufacture and use by wild bearded capuchin monkeys. Behavioural Processes, 108, 117–122. https://doi.org/10.1016/j.beproc.2014.09.036.
Falótico, T., Spagnoletti, N., Haslam, M., Luncz, L. V., Malaivijitnond, S., & Gumert, M. (2017). Analysis of sea almond (Terminalia catappa) cracking sites used by wild Burmese long-tailed macaques (Macaca fascicularis aurea). American Journal of Primatology, 79(5), e22629. https://doi.org/10.1002/ajp.22629.
Fontaine, B., Moisson, P. Y., & Wickings, E. J. (1995). Observations of spontaneous tool making and tool use in a captive group of western lowland gorillas (Gorilla gorilla gorilla). Folia Primatologica, 65(4), 219–223. https://doi.org/10.1159/000156892.
Gross, L. (2005). Wild gorillas handy with a stick. PLoS Biology, 3(11), 1841–1842. https://doi.org/10.1371/journal.pbio.0030385.
Gruber, T., Clay, Z., & Zuberbühler, K. (2010). A comparison of bonobo and chimpanzee tool use: Evidence for a female bias in the Pan lineage. Animal Behaviour, 80(6), 1023–1033. https://doi.org/10.1016/j.anbehav.2010.09.005.
Gumert, M. D., Kluck, M., & Malaivijitnond, S. (2009). The physical characteristics and usage patterns of stone axe and pounding hammers used by long-tailed macaques in the Andaman Sea region of Thailand. American Journal of Primatology, 71(7), 594–608. https://doi.org/10.1002/ajp.20694.
Gumert, M. D., Hoong, L K., Malaivijitnond, S. (2011). Sex differences in the stone tool-use behavior of a wild population of burmese long-tailed macaques (Macaca fascicularis aurea). American Journal of Primatology 73(12), 1239–1249. https://doi.org/10.1002/ajp.2099.
Haslam, M. (2018). Food hardness and stone tool weight in wild primate nut-cracking. bioRxiv. https://doi.org/10.1101/267542.
Haslam, M., Hernandez-Aguilar, A., Ling, V., Carvalho, S., de la Torre, I., et al (2009). Primate archaeology. Nature, 460(7253), 339–344. https://doi.org/10.1038/nature08188.
Haslam, M., Hernandez-Aguilar, R. A., Proffitt, T., Arroyo, A., Falótico, T., et al (2017). Primate archaeology evolves. Nature Ecology & Evolution, 1(10), 1431–1437. https://doi.org/10.1038/s41559-017-0286-4.
Haslam, M., Fujii, J., Espinosa, S., Mayer, K., Ralls, K., Tinker, M. T., Uomini, N. (2019). Wild sea otter mussel pounding leaves archaeological traces. Scientific Reports 9(1). https://doi.org/10.1038/s41598-019-39902-y.
Hohmann, G. (1988). A case of simple tool use in wild liontailed macaques (Macaca silenus). Primates, 29(4), 565–567. https://doi.org/10.1007/BF02381143.
Huffman, M. A., & Quiatt, D. (1986). Stone handling by Japanese macaques (Macaca fuscata): Implications for tool use of stone. Primates, 27(4), 413–423. https://doi.org/10.1007/BF02381887.
Kahlenberg, S. M., & Wrangham, R. W. (2010). Sex differences in chimpanzees’ use of sticks as play objects resemble those of children. Current Biology, 20(24), R1067–R1068. https://doi.org/10.1016/j.cub.2010.11.024.
Kaplan, M. (2009). Orangutans kiss leaves to sound bigger and badder? National Geographic News. Reporting your world daily. http://news.nationalgeographic.com/news/2009/08/090804orangutanskissleaves.html(Accessed 3 Jan 2017).
King, B. J. (1986). Extractive foraging and the evolution of primate intelligence. Human Evolution, 1(4), 361–372. https://doi.org/10.1007/BF02436709.
Luncz, L. V., Svensson, M. S., Haslam, M., Malaivijitnond, S., Proffitt, T., & Gumert, M. (2017a). Technological response of wild macaques (Macaca fascicularis) to anthropogenic change. International Journal of Primatology, 38(5), 872–880. https://doi.org/10.1007/s10764-017-9985-6.
Luncz, L. V., Tan, A., Haslam, M., Kulik, L., Proffitt, T., et al. (2017b). Resource depletion through primate stone technology. eLife, 6. https://doi.org/10.7554/eLife.23647
Malaivijitnond, S., Lekprayoon, C., Tandavanittj, N., Panha, S., Cheewatham, C., & Hamada, Y. (2007). Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis). American Journal of Primatology, 69(2), 227–233. https://doi.org/10.1002/ajp.20342.
Mallapur, A., Sinha, A., & Waran, N. (2005). Influence of visitor presence on the behaviour of captive lion-tailed macaques (Macaca silenus) housed in Indian zoos. Applied Animal Behaviour Science, 94(3–4), 341–352. https://doi.org/10.1016/j.applanim.2005.02.012.
Mangalam, M., Singh, M., & Addessi, E. (2013). Flexibility in food extraction techniques in urban free-ranging bonnet macaques, Macaca radiata. PLoS One, 8(12), e85497. https://doi.org/10.1371/journal.pone.0085497.
Menzel Jr., E. W., Davenport, R. K., & Rogers, C. M. (1970). The development of tool using in wild-born and restriction-reared chimpanzees. Folia Primatologica, 12(4), 273–283. https://doi.org/10.1159/000155297.
Meulman, E. J. M., & Van Schaik, C. P. (2013). Orangutan tool use and the evolution of technology. Cambridge: Cambridge University Press. https://doi.org/10.5167/uzh-92534.
Milich, K. M., & Maestripieri, D. (2016). Sex or power? The function of male displays in rhesus macaques. Behaviour, 153(3), 245–261. https://doi.org/10.1163/1568539X-00003340.
Ottoni, E. B., & Izar, P. (2008). Capuchin monkey tool use: Overview and implications. Evolutionary Anthropology: Issues, News, and Reviews, 17(4), 171–178. https://doi.org/10.1002/evan.20185.
Pal, A., Kumara, H. N., Mishra, P. S., Velankar, A. D., & Singh, M. (2017). Extractive foraging and tool-aided behaviors in the wild Nicobar long-tailed macaque (Macaca fascicularis umbrosus). Primates. https://doi.org/10.1007/s10329-017-0635-6.
Pascual-Garrido, A. (2019). Cultural variation between neighbouring communities of chimpanzees at Gombe, Tanzania. Scientific Reports, 9(1). https://doi.org/10.1038/s41598-019-44703-4.
Proffitt, T., Luncz, V. L., Malaivijitnond, S., Gumert, M., Svensson, M. S., & Haslam, M. (2018). Analysis of wild macaque stone tools used to crack oil palm nuts. Royal Society Open Science, 5(3), 171904. https://doi.org/10.1098/rsos.171904.
Sanz, C. M., Call, J., & Boesch, C. (Eds.) (2013). Tool use in animals: Cognition and ecology. Cambridge: Cambridge University Press.
Shumaker, R. W., Walkup, K. R., Beck, B. B., & Burghardt, G. M. (2011). Animal tool behavior: The use and manufacture of tools by animals. Baltimore: The Johns Hopkins University Press.
Sinha, A. (1997). Complex tool manufacture by a wild bonnet macaque, Macaca radiata. Folia Primatologica, 68(1), 23–25. https://doi.org/10.1159/000157227.
Sivakumar, K. (2010). Impact of the tsunami (December, 2004) on the long tailed macaque of Nicobar Islands, India. Hystrix, (1). https://doi.org/10.4404/hystrix-21.1-4484
Spagnoletti, N., Visalberghi, E., Ottoni, E., Izar, P., & Fragaszy, D. (2011). Stone tool use by adult wild bearded capuchin monkeys (Cebus libidinosus): Frequency, efficiency and tool selectivity. Journal of Human Evolution, 61(1), 97–107. https://doi.org/10.1016/j.jhevol.2011.02.010.
St Amant, R., & Horton, T. E. (2008). Revisiting the definition of animal tool use. Animal Behaviour, 75(4), 1199–1208. https://doi.org/10.1016/j.anbehav.2007.09.028.
Tan, A. W. Y. (2017). From play to proficiency: The ontogeny of stone-tool use in coastal-foraging long-tailed macaques (Macaca fascicularis) from a comparative perception-action perspective. Journal of Comparative Psychology, 131(2), 89–114. https://doi.org/10.1037/com0000068.
Tan, A., Tan, S. H., Vyas, D., Malaivijitnond, S., & Gumert, M. D. (2015). There is more than one way to crack an oyster: Identifying variation in Burmese long-tailed macaque (Macaca fascicularis aurea) stone-tool use. PLoS One, 10(5), e0124733. https://doi.org/10.1371/journal.pone.0124733.
Tan, A., Luncz, L., Haslam, M., Malaivijitnond, S., Gumert, M. D. (2016). Complex processing of prickly pear cactus (Opuntia sp.) by free-ranging long-tailed macaques: preliminary analysis for hierarchical organisation. Primates 57(2), 141–147. https://doi.org/10.1007/s10329-016-0525-3.
Thierry, B., Singh, M., & Kaumanns, W. (Eds.) (2004). Macaque societies: A model for the study of social organization, Vol. 41. Cambridge: Cambridge University Press.
van Schaik, C. P., Deaner, R. O., & Merrill, M. Y. (1999). The conditions for tool use in primates: Implications for the evolution of material culture. Journal of Human Evolution, 36(6), 719–741.
van Schaik, C. P., Pradhan, G. R. (2003). A model for tool-use traditions in primates: implications for the coevolution of culture and cognition. Journal of Human Evolution 44(6), 645–664. https://doi.org/10.1016/S0047-2484(03)00041-1.
Velankar, A. D., Kumara, H. N., Pal, A., Mishra, P. S., & Singh, M. (2016). Population recovery of Nicobar long-tailed macaque Macaca fascicularis umbrosus following a tsunami in the Nicobar Islands, India. PLoS One, 11(2), e0148205. https://doi.org/10.1371/journal.pone.0148205.
Visalberghi, E., & Fragaszy, D. (1990). Do monkeys ape? In S. T. Parker & K. R. Gibson (Eds.), “Language” and intelligence in monkeys and apes: Comparative developmental perspectives, 1st ed. (pp. 247–273). New York: Cambridge University Press.
Watanabe, K., Urasopon, N., & Malaivijitnond, S. (2007). Long-tailed macaques use human hair as dental floss. American Journal of Primatology, 69(8), 940–944. https://doi.org/10.1002/ajp.20403.
Westergaard, G. C., Lundquist, A. L., Haynie, M. K., Kuhn, H. E., & Suomi, S. J. (1998). Why some capuchin monkeys (Cebus apella) use probing tools (and others do not). Journal of Comparative Psychology, 112(2), 207–211. https://doi.org/10.1037/0735-7036.112.2.207.
Wheatley, B. P. (1988). Cultural behavior and extractive foraging in Macaca fascicularis. Current Anthropology, 29(3), 516–519.
Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., et al (1999). Cultures in chimpanzees. Nature, 399(6737), 682–685. https://doi.org/10.1038/21415.
Acknowledgments
We want to thank the Chief Secretary, Andaman & Nicobar Administration, Forest Department of Andaman and Nicobar Island, Andaman and Nicobar Tribal Welfare Department for permitting us to conduct the work. The present study was financially supported by the International Primatological Society (Research Grant) and Indian Institute of Science Education and Research, Mohali awarded to Jayashree Mazumder (PhD student, IISER Mohali). We would also like to thank Pondicherry University (Port Blair Campus), the local people of Port Blair and Campbell Bay, Mr Amit Kerketta, Mr Paparao, Mr Srinu and his family, and forest rangers Dakhmi and Vinod Singh for their support and help during the study. We thank Parth R. Chauhan for his guidance and support during the study and article preparation. We also thank the reviewers and the editor-in-chief Dr. Joanna Setchell for their constructive comments that helped enhance the quality of the article.
Author information
Authors and Affiliations
Contributions
JM designed the study and collected the data; JM and SSKK developed the methodology, performed data analyses and wrote the manuscript.
Corresponding author
Additional information
Handling Editor: Joanna M. Setchell
Electronic supplementary material
(MP4 301079 kb)
Rights and permissions
About this article
Cite this article
Mazumder, J., Kaburu, S.S.K. Object Manipulation and Tool Use in Nicobar Long-Tailed Macaques (Macaca fascicularis umbrosus). Int J Primatol 41, 141–159 (2020). https://doi.org/10.1007/s10764-020-00141-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-020-00141-y