Abstract
Time is a limited resource and how well it is allocated to competing behaviours can profoundly affect Darwinian fitness. Life history theory predicts that the amount of time allocated to vital behaviours will change with life history stage, resulting in trade-offs between competing behaviours. Moreover, a range of environmental factors can also affect activity budgets. We studied diurnal time allocation by migratory plains zebras (Equus quagga) in the Serengeti ecosystem, Tanzania, and investigated the effect of life history stage, social environment, habitat structure, and day time on time allocation to five behavioural categories (grazing, resting, vigilance, movement, other). We expected (1) increased vulnerability to predation and impeded predator detection to increase vigilance and decrease resting and grazing; (2) energetically costly life stages to increase grazing and decrease resting; and (3) increasing age in young to result in increased vigilance and grazing and decreased resting. Our findings revealed that in young zebras, resting decreased and grazing increased from the youngest to the oldest age class. Band stallions spent more time grazing and less time resting and moving than bachelors. Lactating mares devoted more time to grazing but less to resting and vigilance than other mares. Mares spent most time vigilant in the last third and stallions in the first third of the day. Adult zebras moved more, and mares were more vigilant in the woodland boundary than on short grass plains. Taken together, our study identifies intrinsic and extrinsic factors shaping time allocation decisions and trade-offs between competing behaviours in plains zebra.
Significance statement
How well animals allocate their limited time to competing behaviours will affect their survival and reproduction. For example, energetically costly life history stages often require an increase in foraging whereas when predators threaten survival, more time should be allocated to vigilance. Increased investment of time in one behaviour requires decreased investment in another or other behaviours; thus, trade-offs in time are expected. Life history theory predicts substantial changes in the time allocated to vital behaviours between life stages. We investigated the effect of life history stage and environmental factors on the behavioural time budgets of migratory plains zebras in the Serengeti ecosystem. Our results showed that life history stage, juvenile age and environmental factors determine how time is invested in vital behaviours, and the behavioural trade-offs this entails.
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The datasets produced and/or analysed during the current study available from the corresponding author on reasonable request.
References
Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Barnier F, Duncan P, Fritz H, Blanchard P, Rubenstein D, Pays O (2016) Between-gender differences in vigilance do not necessarily lead to differences in foraging-vigilance tradeoffs. Oecologia 181:757–768. https://doi.org/10.1007/s00442-016-3614-5
Beauchamp G (2009) Sleeping gulls monitor the vigilance behaviour of their neighbours. Biol Lett 5:9–11. https://doi.org/10.1098/rsbl.2008.0490
Beauchamp G (2013) Social foragers adopt a riskier foraging mode in the centre of their groups. Biol Lett 9:20130528. https://doi.org/10.1098/rsbl.2013.0528
Beauchamp G, Ruxton GD (2008) Disentangling risk dilution and collective detection in the antipredator vigilance of semipalmated sandpipers in flocks. Anim Behav 75:1837–1842. https://doi.org/10.1016/j.anbehav.2007.12.016
Becker CD, Ginsberg JR (1990) Mother-infant behaviour of wild Grevy’s zebra: adaptations for survival in semidesert East Africa. Anim Behav 40:1111–1118. https://doi.org/10.1016/S0003-3472(05)80177-0
Bednekoff PA (1997) Mutualism among safe, selfish sentinels: a dynamic game. Am Nat 150:373–392. https://doi.org/10.1086/286070
Bednekoff PA, Blumstein DT (2009) Peripheral obstructions influence marmot vigilance: integrating observational and experimental results. Behav Ecol 20:1111–1117. https://doi.org/10.1093/beheco/arp104
Bednekoff PA, Lima SL (2005) Testing for peripheral vigilance: do birds value what they see when not overtly vigilant? Anim Behav 69:1165–1171. https://doi.org/10.1016/j.anbehav.2004.07.020
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. RJournal 9:378–400. https://doi.org/10.32614/RJ-2017-066
Burger J, Gochfeld M (1994) Vigilance in African mammals: differences among mothers, other females, and males. Behaviour 131:153–169. https://doi.org/10.1163/156853994X00415
Byers JA, Hogg JT (1995) Environmental effects on prenatal growth rate in pronghorn and bighorn: further evidence for energy constraint on sex-biased maternal expenditure. Behav Ecol 6:451–457. https://doi.org/10.1093/beheco/6.4.451
Cameron E, Stafford K, Linklater W, Veltman C (1999) Suckling behaviour does not measure milk intake in horses, Equus caballus. Anim Behav 57:673–678. https://doi.org/10.1006/anbe.1998.0997
Childress MJ, Lung MA (2003) Predation risk, gender and the group size effect: does elk vigilance depend upon the behaviour of conspecifics? Anim Behav 66:389–398. https://doi.org/10.1006/anbe.2003.2217
Clutton-Brock TH, Iason GR, Albon SD, Guinness FE (2009) Effects of lactation on feeding behaviour and habitat use in wild red deer hinds. J Zool 198:227–236. https://doi.org/10.1111/j.1469-7998.1982.tb02072.x
Corlatti L, Béthaz S, von Hardenberg A, Bassano B, Palme R, Lovari S (2012) Hormones, parasites and male mating tactics in alpine chamois: identifying the mechanisms of life history trade-offs. Anim Behav 84:1061–1070. https://doi.org/10.1016/j.anbehav.2012.08.005
Costa DP, Le Boeuf BJ, Huntley AC, Ortiz CL (1986) The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J Zool 209:21–33. https://doi.org/10.1111/j.1469-7998.1986.tb03563.x
Côté SD, Schaefer JA, Messier F (1997) Time budgets and synchrony of activities in muskoxen: the influence of sex, age, and season. Can J Zool 75:1628–1635. https://doi.org/10.1139/z97-789
Creel S, Schuette P, Christianson D (2014) Effects of predation risk on group size, vigilance, and foraging behavior in an African ungulate community. Behav Ecol 25:773–784. https://doi.org/10.1093/beheco/aru050
Dias PAD, Rangel-Negrín A, Canales-Espinosa D (2011) Effects of lactation on the time-budgets and foraging patterns of female black howlers (Alouatta pigra). Am J Phys Anthropol 145:137–146. https://doi.org/10.1002/ajpa.21481
Dunbar RIM (1992) Time: a hidden constraint on the behavioural ecology of baboons. Behav Ecol Sociobiol 31:35–49. https://doi.org/10.1007/BF00167814
Duncan P, Foose TJ, Gordon IJ, Gakahu CG, Lloyd M (1990) Comparative nutrient extraction from forages by grazing bovids and equids: a test of the nutritional model of equid/bovid competition and coexistence. Oecologia 84(3):411–418. https://doi.org/10.1007/BF00329768
Duncan P (1992) Horses and grasses. Springer New York, New York
East ML, Otto E, Helms J, Thierer D, Cable J, Hofer H (2015) Does lactation lead to resource allocation trade-offs in the spotted hyaena? Behav Ecol Sociobiol 69:805–814. https://doi.org/10.1007/s00265-015-1897-x
Elgar MM (1989) Predator vigilance and group size in mammals and birds: a critical review of the empirical evidence. Biol Rev 64:13–33. https://doi.org/10.1111/j.1469-185X.1989.tb00636.x
Favreau F-RR, Goldizen AW, Pays O (2010) Interactions among social monitoring, anti-predator vigilance and group size in eastern grey kangaroos. Proc R Soc Lond B 277:2089–2095. https://doi.org/10.1098/rspb.2009.2337
Fernández-Juricic E, Beauchamp G, Bastain B (2007) Group-size and distance-to-neighbour effects on feeding and vigilance in brown-headed cowbirds. Anim Behav 73:771–778. https://doi.org/10.1016/j.anbehav.2006.09.014
Fischhoff IR, Sundaresan SR, Cordingley J, Rubenstein D (2007) Habitat use and movements of plains zebra (Equus burchelli) in response to predation danger from lions. Behav Ecol 18:725–729. https://doi.org/10.1093/beheco/arm036
Fisher DO, Blomberg SP, Owens IPF (2002) Convergent maternal care strategies in ungulates and macropods. Evolution 56:167–176. https://doi.org/10.1111/j.0014-3820.2002.tb00858.x
Fitzgibbon C, Lazarus J (1995) Antipredator behavior of Serengeti ungulates: individual differences and population consequences. In: Sinclair ARE, Arcese P (eds) Serengeti II: dynamics, management and conservation of an ecosystem. University of Chicago Press, Chicago, pp 274–296
Forsyth DM, Duncan RP, Tustin KG, Gaillard J-M (2005) A substantial energetic cost to male reproduction in a sexually dimorphic ungulate. Ecology 86:2154–2163. https://doi.org/10.1890/03-0738
Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Animal Behaviour 67(3):591–602. https://doi.org/10.1016/j.anbehav.2003.08.007
Grange S, Duncan P, Gaillard J-M, Sinclair A, Gogan P, Packer C, Hofer H, East M (2004) What limits the Serengeti zebra population? Oecologia 140:523–532. https://doi.org/10.1007/s00442-004-1567-6
Hamel S, Côté SD (2008) Trade-offs in activity budget in an alpine ungulate: contrasting lactating and nonlactating females. Anim Behav 75:217–227. https://doi.org/10.1016/j.anbehav.2007.04.028
Hofer H, East ML (1993) The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. II. Intrusion pressure and commuters’ space use. Anim Behav 46:559–574. https://doi.org/10.1006/anbe.1993.1223
Hofer H, East ML (1995) Population dynamics, population size, and the commuting system of Serengeti spotted hyenas. In: Sinclair ARE, Arcese P (eds) Serengeti II: dynamics, management, and conservation of an ecosystem. University of Chicago Press, Chicago, pp 332–363
Höner OP, Wachter B, East ML, Hofer H (2002) The response of spotted hyaenas to long-term changes in prey populations: functional response and interspecific kleptoparasitism. J Anim Ecol 71:236–246. https://doi.org/10.1046/j.1365-2656.2002.00596.x
Hopcraft G, Sinclair ARE, Packer C (2005) Planning for success: Serengeti lions seek prey accessibility rather than abundance. J Anim Ecol 74:559–566. https://doi.org/10.1111/j.1365-2656.2005.00955.x
King SR, Asa CS, Pluhácek J, Houpt K, Ransom J (2016) Behavior of horses, zebras, and asses. In: Ransom JI, Kaczensky P (eds) Wild equids: ecology, management and conservation. Johns Hopkins University Press, Baltimore, pp 23–40
Klingel H (1969a) The social organisation and population ecology of the plains zebra (Equus quagga). Zool Afr 4:249–263. https://doi.org/10.1080/00445096.1969.11447374
Klingel H (1969b) Reproduction in the plains zebra, Equus burchelli boehmi, behaviour and ecological factors. J Reprod Fertil 6:339–345
Klingel H (1974) A comparison of the social behaviour of the Equidae. In: Geist V, Walther F (eds) The behavior ungulates and its relation to management. IUCN Publ. 24, Morges, pp 124–132. https://doi.org/10.1016/0304-3762(75)90090-5
Landete-Castillejos T, Garcia A, Gómez JA, Laborda J (2002) Effects of nutritional stress during lactation on immunity costs and indices of future reproduction in Iberian red deer (Cervus elaphus hispanicus). Biol Reprod 67:1613–1620. https://doi.org/10.1095/biolreprod.102.004507
Li Z, Jiang Z (2008) Group size effect on vigilance: evidence from Tibetan gazelle in Upper Buha River, Qinghai-Tibet Plateau. Behav Process 78:25–28. https://doi.org/10.1016/j.beproc.2007.11.011
Liley S, Creel S (2008) What best explains vigilance in elk: characteristics of prey, predators, or the environment? Behav Ecol 19:245–254. https://doi.org/10.1093/beheco/arm116
Maddock L (1979) The migration and grazing succession. In: Sinclair A, Norton-Griffiths M (eds) Serengeti: dynamics of an ecosystem. The University of Chicago Press, Chicago, pp 104–129
McDougall PL, Ruckstuhl KE (2018a) Vigilance behaviour is more contagious when chewing stops: examining the characteristics of contagious vigilance in bighorn sheep. Behav Ecol Sociobiol 72:143. https://doi.org/10.1007/s00265-018-2536-0
McDougall PL, Ruckstuhl KE (2018b) Doing what your neighbor does: neighbor proximity, familiarity, and postural similarity increases behavioral contagion. Anim Behav 135:177–185. https://doi.org/10.1016/j.anbehav.2017.11.009
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Hormones and Behavior 43(1):2–15. https://doi.org/10.1016/S0018-506X(02)00024-7
McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 55:259–294. https://doi.org/10.2307/1942578
McNaughton SJ (1990) Mineral nutrition and seasonal movements of African migratory ungulates. Nature 345:613–615. https://doi.org/10.1016/0021-9797(80)90501-9
McNaughton SJ, Banyikwa FF (1995) Plant communities and herbivory. In: Sinclair ARE, Arcese P (eds) Serengeti II: dynamics, management and conservation of an ecosystem. The University of Chicago Press, Chicago, pp 49–70
Michelena P, Pillot M-H, Henrion C, Toulet S, Boissy A, Bon R (2012) Group size elicits specific physiological response in herbivores. Biol Lett 8:537–539. https://doi.org/10.1098/rsbl.2012.0197
Mousseau T (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407. https://doi.org/10.1016/S0169-5347(98)01472-4
Mysterud A, Solberg E, Yoccoz N (2005) Ageing and reproductive effort in male moose under variable levels of intrasexual competition. J Anim Ecol 74:742–754. https://doi.org/10.1111/j.1365-2656.2005.00965.x
Neuhaus P, Ruckstuhl KE (2002) The link between sexual dimorphism, activity budgets, and group cohesion: the case of the plains zebra (Equus burchelli). Can J Zool 80:1437–1441. https://doi.org/10.1139/Z02-126
Nuñez C, Asa C, Rubenstein D (2011) Zebra reproduction: plains zebra (Equus burchelli), mountain zebra (Equus zebra), and Grevy’s zebra (Equus grevyi). In: McKinnon A, Squires E, Vaala W, Varner D (eds) Equine reproduction. Wiley-Blackwell, Ames, pp 2851–2865
Oftedal O (1984) Milk composition, milk yield and energy output at peak lactation: a comparative review. Sym Zool Soc 51:33–85
Oftedal OT, Hintz HF, Schryver HF (1983) Lactation in the horse: milk composition and intake by foals. J Nutr 113:2096–2106
Owen-Smith N, Goodall V (2014) Coping with savanna seasonality: comparative daily activity patterns of African ungulates as revealed by GPS telemetry. 293(3):181–191. https://doi.org/10.1111/jzo.12132
Pays O, Jarman PJ, Loisel P, Gerard J-F (2007) Coordination, independence or synchronization of individual vigilance in the eastern grey kangaroo? Anim Behav 73:595–604. https://doi.org/10.1016/J.ANBEHAV.2006.06.007
R Development Core Team (2016) R: a language and environment for statistical computing. Austria, Vienna http://www.R-project.org
Radford AN, Fawcett TW (2012) Negotiating a stable solution for vigilance behaviour. Proc R Soc Lond B 279:3633–3634. https://doi.org/10.1098/rspb.2012.1210
Radford AN, Ridley AR (2007) Individuals in foraging groups may use vocal cues when assessing their need for anti-predator vigilance. Biol Lett 3:249–252. https://doi.org/10.1098/rsbl.2007.0110
Ransom JI, Cade BS (2009) Quantifying equid behavior — a research ethogram for free-roaming feral horses. US Geol Surv Tech Methods 2:1–23. https://doi.org/10.1017/CBO9781107415324.004
Ransom JI, Kaczensky P (eds) (2016) Wild equids: ecology, management, and conservation. Johns Hopkins University Press, Baltimore
Riek A (2008) Relationship between milk energy intake and growth rate in suckling mammalian young at peak lactation: an updated meta-analysis. J Zool 274:160–170. https://doi.org/10.1111/j.1469-7998.2007.00369.x
Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086. https://doi.org/10.1006/anbe.1996.0109
Roff DA (1992) The evolution of life histories: theory and analysis. Chapman & Hall, New York
Rubenstein DI (1978) On predation, competition, and the advantages of group living. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology, vol 3. Springer US, Boston, pp 205–231
Rubenstein DI (1986) Ecology and sociality in horses and zebras. In: Rubenstein D, Wrangham R (eds) Ecological aspects of social evolution. Princeton University Press, Princeton, pp 282–302
Ruckstuhl KE, Neuhaus P (2009) Activity budgets and sociality in a monomorphic ungulate: the African oryx (Oryx gazella). Can J Zool 87:165–174. https://doi.org/10.1139/z08-148
Ruckstuhl K, Festa-Bianchet M, Jorgenson JT (2003) Bite rates in Rocky Mountain bighorn sheep (Ovis canadensis): effects of season, age, sex and reproductive status. Behav Ecol Sociobiol 54:167–173. https://doi.org/10.1007/s00265-003-0615-2
Seeber PA, Franz M, Dehnhard M, Ganswindt A, Greenwood AD, East ML (2018) Plains zebra (Equus quagga) adrenocortical activity increases during times of large aggregations in the Serengeti ecosystem. Horm Behav 102:1–9. https://doi.org/10.1016/j.yhbeh.2018.04.005
Sirot E (2012) Negotiation may lead selfish individuals to cooperate: the example of the collective vigilance game. Proc R Soc Lond B 279:2862–2867. https://doi.org/10.1098/rspb.2012.0097
Souris A-C, Kaczensky P, Julliard R, Walzer C (2007) Time budget-, behavioral synchrony- and body score development of a newly released Przewalski’s horse group Equus ferus przewalskii, in the Great Gobi B strictly protected area in SW Mongolia. Appl Anim Behav Sci 107:307–321. https://doi.org/10.1016/j.applanim.2006.09.023
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Tambling CJ, Minnie L, Meyer J, Freeman EW, Santymire RM, Adendorff J, Kerley GIH (2015) Temporal shifts in activity of prey following large predator reintroductions. Behav Ecol Sociobiol 69:1153–1161. doi: https://doi.org/10.1007/s00265-015-1929-6
Tchabovsky AV, Krasnov B, Khokhlova IS, Shenbrot GI (2001) The effect of vegetation cover on vigilance and foraging tactics in the fat sand rat Psammomys obesus. J Ethol 19:105–113. https://doi.org/10.1007/s101640170006
Twine W (2002) Feeding time budgets of selected African ruminant and non-ruminant grazers. Afr J Ecol 40:410–412. https://doi.org/10.1111/j.1365-2028.1990.tb01139.x
Watts DP (1988) Environmental influences on mountain gorilla time budgets. Am J Primatol 15:195–211. https://doi.org/10.1002/ajp.1350150303
Welch RJ, le Roux A, Petelle MB, Périquet S (2018) The influence of environmental and social factors on high- and low-cost vigilance in bat-eared foxes. Behav Ecol Sociobiol 72:29. https://doi.org/10.1007/s00265-017-2433-y
Willisch CS, Ingold P (2007) Feeding or resting? The strategy of rutting male alpine chamois. Ethology 113:97–104. https://doi.org/10.1111/j.1439-0310.2006.01301.x
Xia C, Liu W, Xu W, Yang W, Xu F, Blank D (2013) Diurnal time budgets and activity rhythm of the Asiatic wild ass Equus hemionus in Xinjiang, Western China. Pak J Zool 45:1241–1248
Acknowledgments
We thank the Tanzania Commission of Science and Technology, Tanzania National Parks and the Tanzania Wildlife Research Institute for their support of this study. We thank H. Hofer for statistical advice and the reviewer and the editor K.E. Ruckstuhl for providing valuable comments and constructive critique.
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This study was funded by a grant from the Leibniz Gemeinschaft (SAW-2015-IZW-1 440) and the Leibniz Institute for Zoo and Wildlife Research.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Permission to conduct research in Tanzania was granted by the Tanzania Commission for Science and Technology (permit no. 2015-168-NA-90-130). All procedures performed were in accordance with the ethical standards of the Leibniz Institute for Zoo and Wildlife Research, and approved by the Internal Ethics Committee, Approval No. 2015-09-03.
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Seeber, P.A., Franz, M., Greenwood, A.D. et al. Life history stage and extrinsic factors affect behavioural time allocation in plains zebras (Equus quagga) in the Serengeti ecosystem. Behav Ecol Sociobiol 73, 126 (2019). https://doi.org/10.1007/s00265-019-2738-0
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DOI: https://doi.org/10.1007/s00265-019-2738-0