Abstract
Urbanisation is an important factor driving species and biodiversity decline. Although habitat alterations can be detrimental for species, studies have shown that many diurnal primates are able to adapt to novel environments. Little is known about the ability of nocturnal primates to survive within an urban environment. To increase our understanding on this topic, we present ad libitum observations on group movement and sociality from urban and rural populations of the African lesser bushbaby (Galago moholi) in South Africa from 2014–2018. Our data show considerable changes in the social dynamics within urban bushbaby populations. In contrast to rural individuals, which spent the majority of their activity period solitarily or in pairs, urban individuals displayed a larger degree of sociality throughout their active period, forming groups of up to ten individuals. Furthermore, urban individuals spent less time moving around, while increasing social (communication/pair-grooming), foraging and feeding behaviour. Urban individuals fed on a range of different anthropogenic and natural food sources (insects/tree gum/nectar) compared to their rural counterparts. In summary, urban bushbabies showed a large degree of behavioural plasticity, with changes in social dynamics and structure frequently observed. Such alterations in sociality, along with the ability to utilise different feeding resources, may explain the ability of the species to survive within a highly altered environment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altmann J (1974) Observational study of behavior: sampling methods. Behavior 49:227–267
Altmann J, Muruthi P (1988) Differences in daily life between semiprovisioned and wild-feeding baboons. Am J Primatol 15:213–221. https://doi.org/10.1002/ajp.1350150304
Alvey AA (2006) Promoting and preserving biodiversity in the urban forest. Urban Forestry & Urban Greening 5:195–201
Atwell JW, Cardoso GC, Whittaker DJ, Campbell-Nelson S, Robertson KW, Ketterson ED (2012) Boldness behavior and stress physiology in a novel urban environment suggest rapid correlated evolutionary adaptation. Behav Ecol 23:960–969. https://doi.org/10.1093/beheco/ars059
Bearder S (1999) Physical and social diversity among nocturnal primates: a new view based on long term research. Primates 40:267–282. https://doi.org/10.1007/BF02557715
Bearder SK, Martin RD (1979) The social organization of a nocturnal primate revealed by radio tracking. In: Amlaner CJ, MacDonald W (eds) A Handbook on biotelemetry and radio tracking. Pergamon, Oxford, pp 633–648
Boyle SA, Smith AT (2010) Behavioral modifications in northern bearded saki monkeys (Chiropotes satanas chiropotes) in forest fragments of central Amazonia. Primates 51:43
Brennan EJ, Else JG, Altmann J (1985) Ecology and behaviour of a pest primate: vervet monkeys in a tourist-lodge habitat. Afr J Ecol 23:35–44. https://doi.org/10.1111/j.1365-2028.1985.tb00710.x
Core Team R (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Crook JH, Gartlan JS (1966) Evolution of primate societies. Nature 210(5042):1200–1203
Cunha AA, Vieira MV, Grelle CE (2006) Preliminary observations on habitat, support use and diet in two non-native primates in an urban Atlantic forest fragment: the capuchin monkey (Cebus sp.) and the common marmoset (Callithrix jacchus) in the Tijuca forest, Rio de Janeiro. Urb Ecosyst 9:351–359
Dammhahn M, Kappeler PM (2005) Social system of Microcebus berthae, the World’s smallest primate. Int J Primatol 26:407–435. https://doi.org/10.1007/s10764-005-2931-z
Ditchkoff S, Saalfeld S, Gibson C (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12. https://doi.org/10.1007/s11252-006-3262-3
Doyle GA, Pelletier A, Bekker T (1967) Reproduction in the lesser bushbaby (Galago senegalensis moholi) under semi natural conditions. Folia Primatol 14:15–22
Dunbar RIM (1996) Determinants of group size in primates: a general model. In: Runciman WG, Smith JM, DRI M (eds) Evolution of social behaviour patterns in primates and man. Proceedings of The British Academy, vol 88. Oxford University Press, New York, pp 33–57
Engelbrecht D (2016) Galagos as avian nest predators in South Africa. Primates 57:455–458
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. https://doi.org/10.2307/30033784
Génin F (2010) Who sleeps with whom? Sleeping association and socio-territoriality in Microcebus griseorufus. J Mamm 91:942–951. https://doi.org/10.1644/09-MAMM-A-239.1
Gursky SL (2000) Sociality in the spectral tarsiers, Tarsius spectrum. Am J Primatol 51:89–101. https://doi.org/10.1002/(SICI)1098-2345(200005)51:1%3c89:AID-AJP7%3e3.0.CO;2-7
Gursky S (2002) Determinants of gregariousness in the spectral tarsier (Prosimina: Tarsius spectrum). J Zool 256:402–410
Hoffman TS, O'Riain MJ (2010) The spatial ecology of chacma baboons (Papio ursinus) in a human-modified environment. Int J Primatol. https://doi.org/10.1007/s10764-010-9467-6
Jaman MF, Huffman MA (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. https://doi.org/10.1007/s10329-012-0330-6
Janson CH (2017) Evolutionary ecology of primate social structure. In: Smith EA (ed) Evolutionary ecology and human behavior. Routledge, New York, pp 95–130
Kappeler PM (1991) Patterns of sexual dimorphism in body weight among prosimian primates. Folia Primatol 57:132–146
Kok P, Collinson M (2006) Migration and urbanisation in South Africa. Statistics South Africa, Pretoria
Li Y (2005) Effects of annual change in group size, human disturbances and weather on daily travel distance of a group in Sichuan snub-nosed monkey (Rhinopithecus roxellana) in Shennongjia Nature Reserve, China. Biodiv Sci 13:432–438
Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev 88:537–549. https://doi.org/10.1111/brv.12012
Martin RD (1990) Primate origins and evolution: a phylogenetic reconstruction. Princeton University Press, Princeton, p 804
McKinney T (2011) The effects of provisioning and crop-raiding on the diet and foraging activities of human-commensal white-faced Capuchins (Cebus capucinus). Am J Primatol 73:439–448. https://doi.org/10.1002/ajp.20919
Miranda AC, Schielzeth H, Sonntag T, Partecke J (2013) Urbanization and its effects on personality traits: a result of microevolution or phenotypic plasticity? Glob Change Biol 19:2634–2644. https://doi.org/10.1111/gcb.12258
Møller AP (2009) Successful city dwellers: a comparative study of the ecological characteristics of urban birds in the Western Palearctic. Oecologia 159:849–858. https://doi.org/10.2307/40309951
Møller AP (2010) Interspecific variation in fear responses predicts urbanization in birds. Behav Ecol 21:365–371
Müller AE, Soligo C (2005) Primate sociality in evolutionary context. Am J Phys Anthropol 128:399–414. https://doi.org/10.1002/ajpa.20086
Müller AE, Thalmann URS (2000) Origin and evolution of primate social organisation: a reconstruction. Biol Rev 75:405–435. https://doi.org/10.1111/j.1469-185X.2000.tb00050.x
Nowack J, Wippich M, Mzilikazi N, Dausmann KH (2013) Surviving the cold, dry period in Africa: behavioral adjustments as an alternative to heterothermy in the African lesser bushbaby (Galago moholi). Int J Primatol 34:49–64
Ostrov JM, Hart E (2014) Observational methods. In: Little TT (ed) The Oxford handbook of quantitative methods in psychology: foundations, vol 1. Oxford University Press, Oxford, p 286
Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecol 87:1945–1952. https://doi.org/10.1890/0012-9658(2006)87[1945:SATCUA]2.0.CO;2
Pinto LPS, Costa CMR, Strier KB, da Fonseca GAB (1993) Habitat, density and group size of primates in a Brazilian tropical forest. Folia Primatol 61:135–143
Poveda K, Sánchez-Palomino P (2004) Habitat use by the white-footed tamarin, Saguinus leucopus: a comparison between a forest-dwelling group and an urban group in Mariquita, Colombia. Neotrop Primates 12:6–9
Pullen SL, Bearder SK, Dixson AF (2000) Preliminary observations on sexual behavior and the mating system in free-ranging lesser galagos (Galago moholi). Am J Primatol 51:79–88
Radespiel U (2000) Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol 51:21–40
Ray I, Wren BT, Bowers EJ (2016) Documentation of plant consumption by Galago moholi in South Africa. Afr Primates 11:45–48
Robb GN, McDonald RA, Chamberlain DE, Bearhop S (2008) Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front Ecol Environ 6:476–484. https://doi.org/10.1890/060152
Saj T, Sicotte P, Paterson JD (1999) Influence of human food consumption on the time budget of vervets. Int J Primatol 20:977–994. https://doi.org/10.1023/A:1020886820759
Saj TL, Sicotte P, Paterson JD (2001) The conflict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda. Afr J Ecol 39:195–199
Scheun J, Bennett N, Ganswindt A, Nowack J (2014) Spicing up the menu: evidence of fruit feeding in Galago moholi. Primates 55:359–363. https://doi.org/10.1007/s10329-014-0420-8
Scheun J, Bennett N, Ganswindt A, Nowack J (2015) The hustle and bustle of city life: monitoring the effects of urbanisation in the African lesser bushbaby. Sci Nat 102:1–11
Scheun J, Nowack J, Bennett N, Ganswindt A (2016) Female reproductive activity and its endocrine correlates in the African lesser bushbaby, Galago moholi. J Comp Physiol B 186:255–264. https://doi.org/10.1007/s00360-015-0947-z
Scheun J, Bennett NC, Nowack J, Ganswindt A (2017) Reproductive behaviour, testis size and faecal androgen metabolite concentrations in the African lesser bushbaby. J Zool 301:263–270. https://doi.org/10.1111/jzo.12420
Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D (2006) From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol 21:186–191. https://doi.org/10.1016/j.tree.2005.11.019
Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4:367–387. https://doi.org/10.1111/j.1752-4571.2010.00166.x
Sol D, Lapiedra O, González-Lagos C (2013) Behavioural adjustments for a life in the city. Anim Behav 85:1101–1112. https://doi.org/10.1016/j.anbehav.2013.01.023
Sterling EJ, Richard AF (1995) Social organization in the Aye-Aye (Daubentonia Madagascariensis) and the perceived distinctiveness of nocturnal primates. In: Alterman L, Doyle GA, Izard MK (eds) Creatures of the dark: the nocturnal prosimians. Springer, Boston, pp 439–451 10.1007/978-1-4757-2405-9_26
Teixeira B, Hirsch A, Goulart VDLR, Passos L, Teixeira CP, James P, Young R (2015) Good neighbours: distribution of black-tufted marmoset (Callithrix penicillata) in an urban environment. Wildl Res 42:579–589. https://doi.org/10.1071/WR14148
Tuomainen U, Candolin U (2011) Behavioural responses to human-induced environmental change. Biol Rev Camb Philos Soc 86:640–657. https://doi.org/10.1111/j.1469-185X.2010.00164.x
van Doorn AC, O'Riain MJ, Swedell L (2010) The effects of extreme seasonality of climate and day length on the activity budget and diet of semi-commensal chacma baboons (Papio ursinus) in the Cape Peninsula of South Africa. Am J Primatol 72:104–112. https://doi.org/10.1002/ajp.20759
van Schaik CP (2013) The costs and benefits of flexibility as an expression of behavioural plasticity: a primate perspective. Philos Trans R Soc B Biol Sci. https://doi.org/10.1098/rstb.2012.0339
Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York
Wich SA, Geurts ML, Mitra T (2006) Influence of fruit availability on Sumatran orangutan sociality and reproduction. Feed Ecol Apes Other Primates 48:337
Wieczkowski J (2005) Examination of increased annual range of a Tana mangabey (Cercocebus galeritus) group. Am J Phys Anthropol 128:381–388
Acknowledgements
We would like to thank Jamey Gulson and Duodane Kindler for their assistance in conducting field observations.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Scheun, J., Greeff, D. & Nowack, J. Urbanisation as an important driver of nocturnal primate sociality. Primates 60, 375–381 (2019). https://doi.org/10.1007/s10329-019-00725-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-019-00725-0