Abstract
Research suggests that wild animals in urban areas exhibit heightened behavioral flexibility when they encounter novel human-made objects, but most such studies compared responses in urban populations with those from disjunct populations in less disturbed environments. We therefore know little about intrapopulation variation in cognitive or behavioral flexibility under different conditions of anthropogenic exposure. Here, we investigate object exploration and behavioral flexibility in a single group of samango monkeys (Cercopithecus mitis) in an environment in which individuals forage in both gardens and natural forest. Over 2 months, we presented monkeys with novel, human-made objects in both natural and disturbed areas, varying the position of objects in trees to represent exposed or safer foraging zones. We video-recorded and analyzed interactions with these novel objects, assessing interaction times (an indicator of persistence), exploratory diversity (or motor diversity), and the occurrence of foraging innovations. Results from 67 interactions (29 in natural habitats and 38 in disturbed) indicate that samango monkeys exhibited a spatially complex response to novel objects: in contrast to that in other species, exploration diversity decreased significantly in anthropogenic environments, even as persistence remained largely static across contexts. Monkeys also exhibited foraging innovations by pulling on strings to bring objects closer. This may reduce exposure to danger, as string-pulling was most prevalent in the highest risk condition (ground level in human gardens). Significant intrapopulation variation in behavioral flexibility suggests that samango monkeys adjust the expression of problem-solving behaviors in relation to the degree of human disturbance in their immediate environment.
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References
Audet, J.-N., & Lefebvre, L. (2017). What’s flexible in behavioral flexibility? Behavioral Ecology, 28(4), 943–947.
Benson-Amram, S., Weldele, M. L., & Holekamp, K. E. (2013). A comparison of innovative problem-solving abilities between wild and captive spotted hyaenas, Crocuta crocuta. Animal Behaviour, 85(2), 349–356.
Bergman, T. J., & Kitchen, D. M. (2009). Comparing responses to novel objects in wild baboons (Papio ursinus) and geladas (Theropithecus gelada). Animal Cognition, 12(1), 63–73.
Bleicher, S. S. (2017). The landscape of fear conceptual framework: Definition and review of current applications and misuses. PeerJ, 5, e3772.
Carter, A. J., Feeney, W. E., Marshall, H. H., Cowlishaw, G., & Heinsohn, R. (2013). Animal personality: What are behavioural ecologists measuring? Biological Reviews, 88, 465–475.
Carter, A. J., Marshall, H. H., Heinsohn, R., & Cowlishaw, G. (2012). How not to measure boldness: Novel object and antipredator responses are not the same in wild baboons. Animal Behaviour, 84, 603–609.
Emerson, S. E., & Brown, J. S. (2013). Identifying preferred habitats of samango monkeys (Cercopithecus (nictitans) mitis erythrarchus) through patch use. Behavioural Processes, 100, 214–221.
Fehlmann, G., O’Riain, M. J., Kerr-Smith, C., Hailes, S., Luckman, A., et al (2017). Extreme behavioural shifts by baboons exploiting risky, resource-rich, human-modified environments. Scientific Reports, 7(1), 15057.
Greggor, A. L., Clayton, N. S., Fulford, A. J. C., & Thornton, A. (2016a). Street smart: Faster approach towards litter in urban areas by highly neophobic corvids and less fearful birds. Animal Behaviour, 117, 123–133.
Greggor, A. L., McIvor, G. E., Clayton, N. S., & Thornton, A. (2016b). Contagious risk taking: Social information and context influence wild jackdaws’ responses to novelty and risk. Scientific Reports, 6(1), 27764.
Griffin, A., & Guez, D. (2014). Innovation and problem solving: A review of common mechanisms. Behavioural Processes, 109, 121–134.
Griffin, A. S., Netto, K., & Peneaux, C. (2017). Neophilia, innovation and learning in an urbanized world: A critical evaluation of mixed findings. Current Opinion in Behavioral Sciences, 16, 15–22.
Kühl, H. S., Boesch, C., Kulik, L., Haas, F., & Arandjelovic, M. (2019). Human impact erodes chimpanzee behavioral diversity. Science, eaau4532.
Lowry, H., Lill, A., & Wong, B. B. M. (2013). Behavioural responses of wildlife to urban environments. Biological Reviews, 88(3), 537–549.
Mangalam, M., & Singh, M. (2013). Flexibility in food extraction techniques in urban free-ranging bonnet macaques, Macaca radiata. PLoS ONE, 8(12), e85497.
McLennan, M. R., Spagnoletti, N., & Hockings, K. J. (2017). The implications of primate behavioral flexibility for sustainable human–primate coexistence in anthropogenic habitats. International Journal of Primatology, 38, 105–121.
Nowak, K., Hill, R. A., Wimberger, K., & le Roux, A. (2016a). Risk-taking in samango monkeys in relation to humans at two sites in South Africa. In M. Waller (Ed.), Ethnoprimatology: Primate conservation in the 21st century, Developments in Primatology: Progress and Prospects (pp. 301–314). Cham, Switzerland: Springer.
Nowak, K., le Roux, A., Richards, S. A., Scheijen, C. P. J., & Hill, R. A. (2014). Human observers impact habituated samango monkeys’ perceived landscape of fear. Behavioral Ecology, 25(5), 1199–1204.
Nowak, K., Richards, S. A., le Roux, A., & Hill, R. A. (2016b). Influence of live-capture on risk perceptions of habituated samango monkeys. Journal of Mammalogy, 97(5), 1461–1468.
Nowak, K., Wimberger, K., Richards, S. A., Hill, R. A., & le Roux, A. (2017). Samango monkeys (Cercopithecus albogularis labiatus) manage risk in a highly seasonal, human-modified landscape in Amathole mountains, South Africa. International Journal of Primatology, 38(2), 194–206.
R Core Team (2016). R: A language and environment for statistical computing. Vienna, Austria. https://www.R-project.org/
Reader, S. M., & Laland, K. N. (2003). Animal innovation: An introduction. In S. M. Reader & K. N. Laland (Eds.), Animal innovation (pp. 3–35). Oxford: Oxford University Press.
Sapolsky, R. M. (2004). Stress and cognition. In M. S. Gazzaniga (Ed.), Cognitive Neurosciences, 3rd ed. (pp. 1031–1042). Cambridge: MIT Press.
Wimberger, K., Nowak, K., & Hill, R. A. (2017). Reliance on exotic plants by two groups of threatened Samango monkeys, Cercopithecus albogularis labiatus, at their southern range limit. International Journal of Primatology, 38(2), 151–171.
Acknowledgments
K. Nowak was funded by a Durham University COFUND research fellowship and the R. W. Primate Fund while A. le Roux was supported, in part, by a grant from the Afromontane Research Unit. The National Research Foundation granted a bursary to N. Mathibane. We are grateful to S. Boyes, A. Midgley, and K. Wimberger for logistical support and assistance in the field. H. Stander and C. Lehloenya provided invaluable assistance in the analysis of video data. We thank the community of Hogsback for allowing us to run experiments in their gardens. We are grateful to Phyllis C. Lee for her valuable comments and insights into behavioral flexibility, which improved our manuscript meaningfully. We also wish to thank our anonymous reviewers for their constructive contributions.
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ALR designed the study, contributed to funding, executed final data analysis, and wrote the manuscript. NM conducted field work, data extraction, and exploratory analyses and provided significant editorial advice. KN contributed to funding, data collection, and analysis and provided significant editorial advice.
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le Roux, A., Mathibane, N. & Nowak, K. Wild Samango Monkeys, Cercopithecus mitis, Balance Risk and Opportunity to Interact with Novel Objects in Village Gardens. Int J Primatol 40, 661–670 (2019). https://doi.org/10.1007/s10764-019-00113-x
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DOI: https://doi.org/10.1007/s10764-019-00113-x