Abstract
Macaques possess a repertoire of extractive foraging techniques that range from complex manipulation to tool-aided behaviors, to access food items that increase their foraging efficiency substantially. However, the complexity and composition of such techniques vary considerably between species and even between populations. In the present study, we report seven such complex manipulative behaviors that include six extractive foraging behaviors, and teeth flossing, in a population of Nicobar long-tailed macaques. The apparent purpose of these behaviors was an extraction of encased food, processing food, foraging hidden invertebrates, and dental flossing. Among these behaviors, three behaviors viz. wrapping, wiping, and teeth-flossing were tool-aided behaviors, where macaques used both natural and synthetic materials as tools. Occasionally macaques also modified those tools prior to their use. The substrate use patterns of leaf rubbing and teeth flossing were similar to that observed in other macaques. The spontaneous tool modification to perform wrapping was a first time observation. These observations suggest that Nicobar long-tailed macaques have a high level of sensorimotor intelligence which helps to evolve such innovative foraging solutions.
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References
Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–265
Bertrand M (1966) Training without reward: traditional training of pig-tailed macaques as coconut harvesters. Science 155:484–486
Carpenter A (1887) Monkeys opening oysters. Nature 36:53
Chiang M (1967) Use of tools by wild macaque monkeys in Singapore. Nature 214:1258–1259
Comins JA, Russ BE, Humbert KA, Hauser MD (2011) Innovative coconut-opening in a semi free-ranging rhesus monkey (Macaca mulatta): a case report on behavioral propensities. J Ethol 29:187–189
Dunba RIM (1977) Feeding ecology of gelada baboons: a preliminary report. In: Clutton-Brock TH (ed) Primate ecology. Academic, London, pp 251–273
Erwin JM, Southwik CH (1992) Population, habitat and conservation status of Macaca mourus, Macaca tonkeana and their putative hybrids. Trop Biodivers 1:31–48
Ewer RF (1968) Ethology of mammals. Plenum, New York
Goodall JVL, Goodall HVL (1966) Use of tools by the Egyptian vulture, Neophron percnopterus. Nature 212:1468–1469
Gumert M, 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. Am J Primatol 71:594–608
Gumert M, Hoong LK, Malaivijitnond S (2011) Sex differences in the stone tool-use behavior of a wild population of Burmese long-tailed macaques (Macaca fascicularis aurea). Am J Primatol 73:1239–1249
Hall KRL, Schaller GB (1964) Tool-using behavior of the California sea otter. J Mammal 45:287–298
Hauser MD, Marier P (1993) Food-associated calls in rhesus macaques (Macaca mulatta): I. Socioecological factors. Behav Ecol 4:194–205
Hohmann G (1988) A case of simple tool use in wild lion tailed macaques (Macaca silenus). Primates 29:565–567
Izawa K (1982) Nihonzaru no Seitai: Gousetsu no Hakusanni Yaseiwo Tou. [Ecology of Japanese Macaques: Considering the Wilderness in the Heavy-Snowing Hakusan Mountains], (In Japanese). Tokyo, Doubutsu-Sha
Jaman MF, Huffman MA (2013) The effect of urban and rural habitats and resource type an activity budgets of commensal rhesus macaques (Macaca radiata) in Bangladesh. Primates 54:49–59
Kawai M (1965) Newly-acquired pre-cultural behavior of the natural troop of Japanese monkeys on Koshima Islet. Primates 6:1–30
Kawamura S (1959) The process of sub-culture propagation among Japanese macaques. Primates 2:43–60
King BJ (1986) Extractive foraging and the evolution of primate intelligence. Hum Evol 1:361–372
Kuruvilla GP (1980) Ecology of the bonnet macaque (Macaca radiata) with special reference to feeding habits. J Bombay Nat Hist Soc 75:976–988
Leca JB, Gunst N, Huffman MA (2010) Indirect social influence in the maintenance of the stone-handling tradition in Japanese macaques, Macaca fuscata. Anim Behav 79:117–126
Malaivijitnond S, Lekprayoon C, Tandavanitj N, Panha S, Cheewatham C, Hamada Y (2007) Stone-tool usage by Thai long-tailed macaques (Macaca fascicularis). Am J Primatol 69:227–233
Melin AD, Young HC, Mosdossy KW, Fedigan LM (2014) Seasonality, extractive foraging and the evolution of primate sensorimotor intelligence. J Hum Evol 71:77–86
Menard N (2004) Do ecological factors explain variation in social organization. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, pp 237–266
Menzel EW, Wyers EJ (1981) Cognitive aspects of foraging behaviour. In: Kamil AC, Sargent TD (eds) Foraging behavior: ecological, ethological and psychological approaches. Garland STPM, New York, pp 355–377
Moura ADA, Lee PC (2004) Capuchin stone tool use in Caatinga dry forest. Science 306:1909
O’brien TG, Kinnaird MF (1997) Behavior, diet and movents of Sulawesi crested black macaques (Macaca nigra). Int J Primatol 18:321–351
Parker ST, Gibson KR (1977) Object manipulation, tool use, and sensorimotor intelligence as adaptations in Cebus monkeys and great apes. J Hum Evol 6:623–641
Sinha A (1997) Complex tool manufacture by a wild bonnet macaque. Folia Primatol 68:23–25
Sugiyama Y, Koman J (1979) Tool-using and -making behavior of wild chimpanzees at Bossou, Guinea. Primates 20:513–524
Supriatna J, Froehlich JW, Erwin JM, Southwick CH (1992) Population, habitat and conservation status of Macaca maurus, Macaca tonkena and their putative hybrids. Trop Biodivers 1:31–48
Suzuki A (1965) An ecological study of wild Japanese monkeys in snowy areas: focused on their food habits. Primates 6:31–72
Tan AWY (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. J Comp Psychol 131:89–114
Tan A, Tan SH, Vyas D, Malaivijitnond S, Gumert MD (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(2):e0124733. doi:10.1371/journal.pone.0124733
Tan AWY, Luncz L, Haslman M, Malaivijitnond S, Gumert M (2016) Complex processing of prickly pear cactus (Opuntia sp.) by free ranging long-tailed macaques: preliminary analysis for hierarchical organisation. Primates 57:141–147
Troscianko J, Bluff LA, Rutz C (2008) Grass-stem tool use in new Caledonian crows Corvus moneduloides. Ardea 96:283–285
Umapathy G, Singh M, Mohnot SM (2003) Status and distribution of Macaca fascicularis umbrosa in the Nicobar Islands, India. Int J Primatol 24:281–293
van Schaik CP, Deaner RO, Merrill MY (1999) The conditions for tool use in primates: implications for the evolution of material culture. J Hum Evol 36:719–741
Velankar AD, Kumara HN, Pal A, Mishra PS, 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. doi:10.1371/journal.pone.0148205
Visalberghi E, Fragaszy DM (1990) Do monkey ape? In: Parker ST, Gibson KR (eds) “Language” and intelligence in monkeys and apes: comparative developmental perspectives. Cambridge University Press, New York, pp 247–273
Watanabe K, Urasopon N, Malaivijitnond S (2007) Long-tailed macaques use human hair as dental floss. Am J Primatol 69:940–944
Watts DP (2008) Tool use by chimpanzees at Ngogo, Kibale national park, Uganda. Int J Primatol 29:83–94
Wheatley BP (1988) Cultural behavior and extractive foraging in Macaca fascicularis. Curr Anthropol 29:516–519
Yamakoshi G (2004) Evolution of complex feeding techniques in primates: is this the origin of great ape intelligence? In: Russon AE, Begun DR (eds) The evolution of thought: evolutionary origins of great ape intelligence. Cambridge University Press, Cambridge, pp 140–171
Acknowledgements
The present research was supported by the Department of Science and Technology, Government of India (Grant no. SR/SO/AS-49/2011) to HNK and INSPIRE fellowship, Department of Science and Technology, Government of India (Grant no. A.20020/11/97-IFD.DT.31.03.2010) to A. Pal. We thank Principal Chief Conservator of Forests, Port Blair, Andaman and Nicobar islands for permitting us to carry out the field work (Permit no. CWLW/WL/134/566). We thank the local people of Campbell Bay for being helpful throughout the study. MS and PSM thank SERB for the award of a J.C. Bose Fellowship during which this article was prepared. We also acknowledge the anonymous reviewers and the handling editor whose comments helped enhance the quality of this article.
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This study was approved by the Ethical Committee for Animal Research of Sálim Ali Centre for Ornithology and Natural History, Coimbatore. It also adhered to the guidelines and principles of the Ministry of Environment, Forest and Climate Change, Government of India. Further, permission to carry out this study was granted by the Andaman and Nicobar Forest Department (Permit no. CWLW/WL/134/566).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Video 1 An adult male performing coconut pounding to break outer shell of a dehusked coconut (MP4 15882 kb)
Video 2 A subadult male employing tool-aided food rubbing by rubbing dry leaves over a cashew nut to remove latex (MP4 47576 kb)
Video 3 A left-hand amputee adult male modifying a tool by detaching it from tree twigs and wrapping it over dehusked coconut shell (MP4 455270 kb)
Video 4 An adult female cleaning sand from food items by employing food rubbing by hand technique (MP4 27847 kb)
Video 5 A subadult male flossing teeth with a feather (MP4 16030 kb)
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Pal, A., Kumara, H.N., Mishra, P.S. et al. Extractive foraging and tool-aided behaviors in the wild Nicobar long-tailed macaque (Macaca fascicularis umbrosus). Primates 59, 173–183 (2018). https://doi.org/10.1007/s10329-017-0635-6
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DOI: https://doi.org/10.1007/s10329-017-0635-6