Time is a valuable but limited resource, and animals’ survival depends on their ability to carefully manage the amount of time they allocate to each daily activity. While existing research has examined the ecological factors affecting animals’ activity budgets, the impact of anthropogenic factors on urban-dwelling animals’ time budgets remains understudied. Here we collected data through focal animal sampling from three groups of rhesus macaques in Northern India to examine whether interactions with humans decrease macaques’ resting and social time (time constraints hypothesis), or whether, by contrast, foraging on anthropogenic food, that is potentially high in calories, leads macaques to spend more time resting and in social interactions (free time hypothesis). We found that macaques who interacted more frequently with people spent significantly less time resting and grooming, supporting the time constraints hypothesis. We argue that these time constraints are likely caused by the unpredictability of human behaviour.
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Altmann, J. (1974). Observational study of behavior: sampling methods. — Behaviour 49: 227-266.
Aublet, J.-F., Festa-Bianchet, M., Bergero, D. & Bassano, B. (2009). Temperature constraints on foraging behaviour of male Alpine ibex (Capra ibex) in summer. — Oecologia 159: 237-247.
Backwell, P.R. & Passmore, N.I. (1996). Time constraints and multiple choice criteria in the sampling behaviour and mate choice of the fiddler crab, Uca annulipes. — Behav. Ecol. Sociobiol. 38: 407-416.
Balasubramaniam, K.N. & Berman, C.M. (2017). Grooming interchange for resource tolerance: biological markets principles within a group of free-ranging rhesus macaques. — Behaviour 154: 1145-1176.
Beisner, B.A., Heagerty, A., Seil, S.K., Balasubramaniam, K.N., Atwill, E.R., Gupta, B.K., Tyagi, P.C., Chauhan, N.P., Bonal, B., Sinha, P. & McCowan, B. (2015). Human–wildlife conflict: proximate predictors of aggression between humans and rhesus macaques in India. — Am. J. Phys. Anthropol. 156: 286-294.
Beisner, B.A., Jackson, M.E., Cameron, A.N. & McCowan, B. (2011). Detecting instability in animal social networks: genetic fragmentation is associated with social instability in rhesus macaques. — PLoS ONE 6: e16365.
Black, J.M., Carbone, C., Wells, R. & Owen, M. (1992). Foraging dynamics in goose flocks: the cost of living on the edge. — Anim. Behav. 44: 41-50.
Brotcorne, F., Giraud, G., Gunst, N., Fuentes, A., Wandia, I.N., Beudels-Jamar, R.C., Poncin, P., Huynen, M.-C. & Leca, J.-B. (2017). Intergroup variation in robbing and bartering by long-tailed macaques at Uluwatu Temple (Bali, Indonesia). — Primates 58: 1-12.
Burnham, K.P., Anderson, D.R. & Huyvaert, K.P. (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. — Behav. Ecol. Sociobiol. 65: 23-35.
Carne, C., Wiper, S. & Semple, S. (2011). Reciprocation and interchange of grooming, agonistic support, feeding tolerance, and aggression in semi-free-ranging Barbary macaques. — Am. J. Primatol. 73: 1127-1133.
Chapman, C.A., Chapman, L.J. & Wrangham, R. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. — Behav. Ecol. Sociobiol. 36: 59-70.
Chauhan, A. & Pirta, R. (2010a). Agonistic interactions between humans and two species of monkeys (rhesus monkey Macaca mulatta and hanuman langur Semnopithecus entellus) in Shimla, Himachal Pradesh. — J. Psychol. 1: 9-14.
Chauhan, A. & Pirta, R. (2010b). Socio-ecology of two species of non-human primates, rhesus monkey (Macaca mulatta) and Hanuman langur (Semnopithecus entellus), in Shimla, Himachal Pradesh. — J. Hum. Ecol. 30: 171-177.
Clutton-Brock, T. (2002). Breeding together: kin selection and mutualism in cooperative vertebrates. — Science 296: 69-72.
Cords, M. (2012). The behavior, ecology, and social evolution of cercopithecine monkeys. — In: The evolution of primate societies (Mitani, J.C., Call, J., Kappeler, P.M., Ryne, A.P. & Silk, J.B., eds). University of Chicago Press, Chicago, IL, p. 91-112.
Duchesne, M., Côté, S.D. & Barrette, C. (2000). Responses of woodland caribou to winter ecotourism in the Charlevoix Biosphere Reserve, Canada. — Biol. Conserv. 96: 311-317.
Dunbar, R.I.M. (1988). Primate social systems. — Cornell University Press, Ithaca, NY.
Dunbar, R.I.M. (1991). Functional significance of social grooming in primates. — Folia Primatol. 57: 121-131.
Dunbar, R.I.M. (1992). Time: a hidden constraint on the behavioural ecology of baboons. — Behav. Ecol. Sociobiol. 31: 35-49.
Dunbar, R.I.M. (1996). Determinants of group size in primates: a general model. — Proc. Br. Acad. 88: 33-57.
Dunbar, R.I.M. (2010). The social role of touch in humans and primates: behavioural function and neurobiological mechanisms. — Neurosci. Biobehav. Rev. 34: 260-268.
Dunbar, R.I.M. & Dunbar, P. (1988). Maternal time budgets of gelada baboons. — Anim. Behav. 36: 970-980.
Dunbar, R.I.M., Hannah-Stewart, L. & Dunbar, P. (2002). Forage quality and the costs of lactation for female gelada baboons. — Anim. Behav. 64: 801-805.
Dunbar, R.I.M. & Shi, J. (2013). Time as a constraint on the distribution of feral goats at high latitudes. — Oikos 122: 403-410.
Dunbar, R.I.M., Korstjens, A.H. & Lehmann, J. (2009). Time as an ecological constraint. — Biol. Rev. 84: 413-429.
El Alami, A., Van Lavieren, E., Rachida, A. & Chait, A. (2012). Differences in activity budgets and diet between semiprovisioned and wild-feeding groups of the endangered Barbary Macaque (Macaca sylvanus) in the Central High Atlas Mountains, Morocco. — Am. J. Primatol. 74: 210-216.
Fooden, J. (2000). Systematic review of rhesus macaque, Macaca mulatta (Zimmermann, 1780). — Fieldiana Zool. 96: 1-180.
Formica, V.A., Wood, C., Larsen, W., Butterfield, R., Augat, M., Hougen, H. & Brodie III, E. (2012). Fitness consequences of social network position in a wild population of forked fungus beetles (Bolitotherus cornutus). — J. Evol. Biol. 25: 130-137.
Forthman-Quick, D. (1988). Dynamics of exploitation: differential energetic adaptations of two troops of baboons to recent human contact. — In: Ecology and behavior of food enhanced primate groups (Fa, J.E. & Southwick, C.H., eds). Alan R. Liss, New York, NY, p. 25-51.
Frère, C.H., Krützen, M., Mann, J., Connor, R.C., Bejder, L. & Sherwin, W.B. (2010). Social and genetic interactions drive fitness variation in a free-living dolphin population. — Proc. Natl. Acad. Sci. USA 107: 19949-19954.
Fuentes, A. (2012). Ethnoprimatology and the anthropology of the human-primate interface. — Annu. Rev. Anthropol. 41: 101-117.
Fujii, K., Jin, J., Shev, A., Beisner, B., McCowan, B. & Fushing, H. (2015). Perc: using percolation and conductance to find information flow certainty in a direct network. — R Package Version 0.1. R Foundation for Statistical Computing, Vienna.
Fushing, H., McAssey, M.P., Beisner, B. & McCowan, B. (2011). Ranking network of a captive rhesus macaque society: a sophisticated corporative kingdom. — PLoS ONE 6: e17817.
Gelman, A. (2008). Scaling regression inputs by dividing by two standard deviations. — Stat. Med. 27: 2865-2873.
Grover, K.E. & Thompson, M.J. (1986). Factors influencing spring feeding site selection by elk in the Elkhorn Mountains, Montana. — J. Wildl. Manage. 50: 466-470.
Gumert, M.D. & Ho, M.-H.R. (2008). The trade balance of grooming and its coordination of reciprocation and tolerance in Indonesian long-tailed macaques (Macaca fascicularis). — Primates 49: 176-185.
Hemelrijk, C.K. (1994). Support for being groomed in long-tailed macaques, Macaca fascicularis. — Anim. Behav. 48: 479-481.
Henzi, S.P. & Barrett, L. (1999). The value of grooming to female primates. — Primates 40: 47-59.
Herbers, J.M. (1981). Time resources and laziness in animals. — Oecologia 49: 252-262.
Hodgson, A.J., Marsh, H. & Corkeron, P.J. (2004). Provisioning by tourists affects the behaviour but not the body condition of Mareeba rock-wallabies (Petrogale mareeba). — Wildlife Res. 31: 451-456.
Hoebel, B.G., Avena, N.M., Bocarsly, M.E. & Rada, P. (2009). A behavioral and circuit model based on sugar addiction in rats. — J. Addict. Med. 3: 33-41.
Hsu, M.J., Kao, C. & Agoramoorthy, G. (2008). Interactions between visitors and Formosan macaques (Macaca cyclopis) at Shou-Shan Nature Park, Taiwan. — Am. J. Primatol 71: 214-222.
Ilham, K., Nurdin, J. & Tsuji, Y. (2018). Effect of provisioning on the temporal variation in the activity budget of urban long-tailed macaques (Macaca fascicularis) in West Sumatra, Indonesia. — Folia Primatol. 89: 347-356.
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: 49-59.
Johansson, F. & Rowe, L. (1999). Life history and behavioral responses to time constraints in a damselfly. — Ecology 80: 1242-1252.
Johansson, F., Stoks, R., Rowe, L. & De Block, M. (2001). Life history plasticity in a damselfly: effects of combined time and biotic constraints. — Ecology 82: 1857-1869.
Kaburu, S.S.K. & Newton-Fisher, N.E. (2015). Egalitarian despots: hierarchy steepness, reciprocity and the grooming-trade model in wild chimpanzees, Pan troglodytes. — Anim. Behav. 99: 61-71.
Kaburu, S.S.K., Marty, P., Beisner, B., Balasubramanian, K., Bliss-Moreau, E., Kawaljit, K., Mohan, L. & McCowan, B. (2019). Rates of human–macaque interactions affect grooming behavior among urban-dwelling rhesus macaques (Macaca mulatta). — Am. J Physic. Anthropol. 168: 92-103.
Kappeler, P.M., Cremer, S. & Nunn, C.L. (2015). Sociality and health: impacts of sociality on disease susceptibility and transmission in animal and human societies. — Philos. Trans. Roy. Soc. Lond. B: Biol. Sci. 370: 20140116.
Kapsalis, E. (2004). Matrilineal kinship and primate behavior. — In: Kinship and behavior in primates (Chapais, B. & Berman, C., eds). Oxford University Press, Oxford, p. 153-176.
Keys, G.C. & Dugatkin, L.A. (1990). Flock size and position effects on vigilance, aggression, and prey capture in the European starling. — Condor 92: 151-159.
Koirala, S., Chalise, M.K., Katuwal, H.B., Gaire, R., Pandey, B. & Ogawa, H. (2017). Diet and activity of Macaca assamensis in wild and semi-provisioned groups in Shivapuri Nagarjun National Park, Nepal. — Folia Primatol. 88: 57-74.
Korstjens, A.H., Verhoeckx, I.L. & Dunbar, R.I.M. (2006). Time as a constraint on group size in spider monkeys. — Behav. Ecol. Sociobiol. 60: 683-694.
Korstjens, A.H., Lehmann, J. & Dunbar, R.I.M. (2010). Resting time as an ecological constraint on primate biogeography. — Anim. Behav. 79: 361-374.
Korstjens, A.H., Lehmann, J. & Dunbar, R.I.M. (2018). Time constraints do not limit group size in arboreal guenons but do explain community size and distribution patterns. — Int. J. Primatol. 39: 511-531.
Lehmann, J., Korstjens, A.H. & Dunbar, R.I.M. (2010). Apes in a changing world — the effects of global warming on the behaviour and distribution of African apes. — J. Biogeogr. 37: 2217-2231.
Lewis, S., Schreiber, E.A., Daunt, F., Schenk, G., Wanless, S. & Hamer, K. (2004). Flexible foraging patterns under different time constraints in tropical boobies. — Anim. Behav. 68: 1331-1337.
Lipetz, V.E. & Bekoff, M. (1982). Group size and vigilance in pronghorns. — Z. Tierpsychol. 58: 203-216.
Lott, D.F. & McCoy, M. (1995). Asian rhinos Rhinoceros unicornis on the run? Impact of tourist visits on one population. — Biol. Conserv. 73: 23-26.
Majolo, B., van Lavieren, E., Maréchal, L., MacLarnon, A., Marvin, G., Qarro, M. & Semple, S. (2013). Out of Asia: the singular case of the Barbary macaque. — In: The macaque connection (Radhakrishna, S., Huffman, M.A. & Sinha, A., eds). Springer, New York, p. 167-183.
Maréchal, L., MacLarnon, A., Majolo, B. & Semple, S. (2016). Primates’ behavioural responses to tourists: evidence for a trade-off between potential risks and benefits. — Sci. Rep. 6: 32465.
Marty, P., Beisner, B., Kaburu, S.S.K., Balasubramaniam, K., Bliss-Moreau, E., Ruppert, N., Sah, S., Ahmad, I., Arlet, M., Atwill, E. & McCowan, B. (2019). Time constraints and stress imposed by human presence alter social behaviour in urban long-tailed macaques. — Anim. Behav. 150: 157-165.
McCarthy, M.S., Matheson, M.D., Lester, J.D., Sheeran, L.K., Li, J.H. & Wagner, R.S. (2009). Sequences of Tibetan macaque (Macaca thibetana) and tourist behaviors at Mt. Huangshan, China. — Primate Conserv. 24: 145-152.
McCowan, B., Beisner, B. & Hannibal, D. (2018). Social management of laboratory rhesus macaques housed in large groups using a network approach: a review. — Behav Processes 156: 77-82.
McFarland, R., Barrett, L., Boner, R., Freeman, N.J. & Henzi, S.P. (2014). Behavioral flexibility of vervet monkeys in response to climatic and social variability. — Am. J. Phys. Anthropol. 154: 357-364.
McLennan, M.R. & Ganzhorn, J.U. (2017). Nutritional characteristics of wild and cultivated foods for chimpanzees (Pan troglodytes) in agricultural landscapes. — Int. J. Primatol. 38: 122-150.
Menon, S. & Poirier, F.E. (1996). Lion-tailed macaques (Macaca silenus) in a disturbed forest fragment: activity patterns and time budget. — Int. J. Primatol. 17: 969-985.
Murton, R., Isaacson, A. & Westwood, N. (1971). The significance of gregarious feeding behaviour and adrenal stress in a population of wood-pigeons Columba palumbus. — J. Zool. 165: 53-84.
Owen-Smith, N. (1998). How high ambient temperature affects the daily activity and foraging time of a subtropical ungulate, the greater kudu (Tragelaphus strepsiceros). — J. Zool. 246: 183-192.
Petit, D.R. & Bildstein, K.L. (1987). Effect of group size and location within the group on the foraging behavior of white ibises. — Condor 89: 602-609.
Pollard, K.A. & Blumstein, D.T. (2008). Time allocation and the evolution of group size. — Anim. Behav. 76: 1683-1699.
Priston, N.E. & McLennan, M.R. (2013). Managing humans, managing macaques: human–macaque conflict in Asia and Africa. — In: The macaque connection: cooperation and conflict between humans and macaques (Radhakrishna, S., Huffman, M.A. & Sinha, A., eds). Springer, New York, NY, p. 225-250.
Pusey, A. & Packer, C. (1987). Dispersal and philopatry. — In: Primate societies (Smuts, B.B., Cheney, D.L., Seyfarth, R.M., Wrangham, R.W. & Struhsaker, T.T., eds). Chicago University Press, Chicago, IL, p. 250-266.
Rhine, R.J., Cox, R.L. & Costello, M.B. (1989). A twenty-year study of long-term and temporary dominance relations among stumptailed macaques (Macaca arctoides). — Am. J. Primatol. 19: 69-82.
Richards, S.A., Whittingham, M.J. & Stephens, P.A. (2011). Model selection and model averaging in behavioural ecology: the utility of the IT-AIC framework. — Behav. Ecol. Sociobiol. 65: 77-89.
Riley, E.P. (2007). Flexibility in diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration. — Int. J. Primatol. 28: 107-133.
Riley, E.P., Tolbert, B. & Farida, W.R. (2013). Nutritional content explains the attractiveness of cacao to crop raiding Tonkean macaques. — Curr. Zool. 59: 160-169.
Rode, K.D., Chiyo, P.I., Chapman, C.A. & McDowell, L.R. (2006). Nutritional ecology of elephants in Kibale National Park, Uganda, and its relationship with crop-raiding behaviour. — J. Trop. Ecol. 22: 441-449.
Roser, M. & Ortiz-Ospina, E. (2018). World Population Growth. — Available online at https://ourworldindata.org/world-population-growth.
Saj, T.L. (1998). The ecology and behavior of vervet monkeys in a human-modified environment. MA thesis, University of Calgary, Calgary, AB.
Saj, T.L., Sicotte, P. & Paterson, J.D. (1999). Influence of human food consumption on the time budget of vervets. — Int. J. Primatol. 20: 977-994.
Schino, G., di Sorrentino, E.P. & Tiddi, B. (2007). Grooming and coalitions in Japanese macaques (Macaca fuscata): partner choice and the time frame reciprocation. — J. Comp. Psychol. 121: 181.
Siikamäki, P. (1998). Limitation of reproductive success by food availability and breeding time in pied flycatchers. — Ecology 79: 1789-1796.
Silk, J.B., Alberts, S.C. & Altmann, J. (2003). Social bonds of female baboons enhance infant survival. — Science 302: 1231-1234.
Snyder-Mackler, N., Kohn, J.N., Barreiro, L.B., Johnson, Z.P., Wilson, M.E. & Tung, J. (2016). Social status drives social relationships in groups of unrelated female rhesus macaques. — Anim. Behav. 111: 307-317.
Southwick, C.H. & Siddiqi, F. (2011). India’s rhesus population: protection versus conservation management. — In: Monkeys on the edge: ecology and management of long-tailed macaques and their interface with humans (Gumert, D., Fuentes, A. & Jones-Engel, L., eds). Cambridge University Press, Cambridge, p. 275-292.
Szott, I.D., Pretorius, Y. & Koyama, N.F. (in press). Behavioural changes in African elephants in response to wildlife tourism. — J. Zool.
Thatcher, H.R., Downs, C.T. & Koyama, N.F. (2019). Anthropogenic influences on the time budgets of urban vervet monkeys. — Landsc. Urban Plan 181: 38-44.
Tiddi, B., Aureli, F., Polizzi di Sorrentino, E., Janson, C.H. & Schino, G. (2011). Grooming for tolerance? Two mechanisms of exchange in wild tufted capuchin monkeys. — Behav. Ecol. 22: 663-669.
Ventura, R., Majolo, B., Koyama, N.F., Hardie, S. & Schino, G. (2006). Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support. — Am. J. Primatol. 68: 1138-1149.
Vitousek, P.M., Mooney, H.A., Lubchenco, J. & Melillo, J.M. (1997). Human domination of Earth’s ecosystems. — Science 277: 494-499.
Xia, D.P., Li, J., Garber, P.A., Sun, L., Zhu, Y. & Sun, B. (2012). Grooming reciprocity in female Tibetan macaques Macaca thibetana. — Am. J. Primatol. 74: 569-579.
Xia, D.P., Li, J.H., Garber, P.A., Matheson, M.D., Sun, B.H. & Zhu, Y. (2013). Grooming reciprocity in male Tibetan macaques. — Am. J. Primatol. 75: 1009-1020.
Young, C., Majolo, B., Heistermann, M., Schülke, O. & Ostner, J. (2014). Responses to social and environmental stress are attenuated by strong male bonds in wild macaques. — Proc. Natl. Acad. Sci. USA 111: 18195-18200.
Kaburu, S.S.K., Marty, P., Beisner, B., Balasubramanian, K., Bliss-Moreau, E., Kawaljit, K., Mohan, L. & McCowan, B. (2019). Rates of human–macaque interactions affect grooming behaviour among urban-dwelling rhesus macaques (Macaca mulatta). — Am. J. Phys. Anthropol. 168: 92-103.
de Waal, F.B. & Luttrell, L.M. (1985). The formal hierarchy of rhesus macaques: an investigation of the bared-teeth display. — Am. J. Primatol. 9: 73-85.
All Time | Past 365 days | Past 30 Days | |
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Time is a valuable but limited resource, and animals’ survival depends on their ability to carefully manage the amount of time they allocate to each daily activity. While existing research has examined the ecological factors affecting animals’ activity budgets, the impact of anthropogenic factors on urban-dwelling animals’ time budgets remains understudied. Here we collected data through focal animal sampling from three groups of rhesus macaques in Northern India to examine whether interactions with humans decrease macaques’ resting and social time (time constraints hypothesis), or whether, by contrast, foraging on anthropogenic food, that is potentially high in calories, leads macaques to spend more time resting and in social interactions (free time hypothesis). We found that macaques who interacted more frequently with people spent significantly less time resting and grooming, supporting the time constraints hypothesis. We argue that these time constraints are likely caused by the unpredictability of human behaviour.
All Time | Past 365 days | Past 30 Days | |
---|---|---|---|
Abstract Views | 1420 | 272 | 32 |
Full Text Views | 255 | 14 | 1 |
PDF Views & Downloads | 260 | 25 | 2 |