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Between-gender differences in vigilance do not necessarily lead to differences in foraging-vigilance tradeoffs

Abstract

When prey are time limited in their access to food, any trade-off involving time should ultimately affect their intake rate. In many herbivores, males and females experience different ecological pressures affecting their survival and reproduction because of differences in morphology, physiology and energy/nutrient requirements. If males and females have different vigilance strategies that affect their intake rates differently, they will suffer different foraging costs. This is particularly relevant in sexually monomorphic herbivores, where the two sexes have similar basal energy/nutrient requirements and risk of predation. We investigated how gender, reproductive status, age, group size, predation risk, and food biomass affected vigilance, intake rate, and their trade-off in a monomorphic species, the plains zebra (Equus quagga). Males were more vigilant than females, and lactating females were less vigilant than other females; the levels of vigilance were low (ca. 10 % of feeding time). The effects on time spent feeding, bite rates and intake rates were small and statistically not significant. Reproductive status did not affect the strength of the relationship between vigilance and intake rate, but intake rates increased with group size and, for adult females, were higher in tall grass. While gender and reproductive status were major drivers of vigilance, and group size and food biomass of the rate of food intake, males and females adjust their bite rates and food intake with vigilance in similar ways. Our results support the hypothesis that in monomorphic animals, males and females seem to make similar trade-offs (i.e. adjustments) between vigilance and intake rate.

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References

  1. Ale SB, Brown JS (2007) The contingencies of group size and vigilance. Evol Ecol Res 9:1263–1276

  2. Baker DJ, Stillman RA, Smart SL, Bullock JM, Norris KJ (2011) Are the costs of routine vigilance avoided by granivorous foragers? Funct Ecol 25:617–627

  3. Baldellou M, Henzi SP (1992) Vigilance, predator detection and the presence of supernumerary males in vervet monkey troops. Anim Behav 43:451–461. doi:10.1016/S0003-3472(05)80104-6

  4. Barnier F, Valeix M, Duncan P, Chamaillé-Jammes S, Barre P, Loveridge AJ, Macdonald DW, Fritz H (2014) Diet quality in a wild grazer declines under the threat of an ambush predator. Proc R Soc B Biol Sci 218:20140446. doi:10.1098/rspb.2014.0446

  5. Beauchamp G (2009) How does food density influence vigilance in birds and mammals? Anim Behav 78:223–231. doi:10.1016/j.anbehav.2009.04.029

  6. Blanchard P, Fritz H (2007) Induced or routine vigilance while foraging. Oikos 116:1603–1608. doi:10.1111/j.2007.0030-1299.15799.x

  7. Blanchard P, Sabatier R, Fritz H (2008) Within-group spatial position and vigilance: a role also for competition? The case of impalas (Aepyceros melampus) with a controlled food supply. Behav Ecol Sociobiol 62:1863–1868. doi:10.1007/s00265-008-0615-3

  8. Blumstein DT, Daniel JC, Sims RA (2003) Group size but not distance to cover influences agile wallaby (Macropus agilis) time allocation. J Mammal 84:197–204. doi:10.1644/1545-1542(2003)084<0197:GSBNDT>2.0.CO;2

  9. Brown JS, Laundre JW, Gurung M (1999) The ecology of fear: optimal foraging, game theory, and trophic interactions. J Mammal 80:385–399. doi:10.2307/1383287

  10. Burger J, Gochfeld M (1994) Vigilance in African mammals: differences among mothers, other females, and males. Behaviour 131:153–169

  11. Burger J, Safina C, Gochfeld M (2000) Factors affecting vigilance in springbok: importance of vegetative cover, location in herd, and herd size. Acta Ethol 2:97–104. doi:10.1007/s102119900013

  12. Burkepile DE, Burns CE, Tambling CJ, Amendola E, Buis GM, Govender N, Nelson V, Thompson DI, Zinn AD, Smith MD (2013) Habitat selection by large herbivores in a southern African savanna: the relative roles of bottom-up and top-down forces. Ecosphere 4:139. doi:10.1890/ES13-00078.1

  13. Carrascal LM, Alonso CL (2006) Habitat use under latent predation risk. A case study with wintering forest birds. Oikos 112:51–62. doi:10.1111/j.0030-1299.2006.13787.x

  14. Chamaillé-Jammes S, Fritz H, Murindagomo F (2007) Detecting climate changes of concern in highly variable environments: quantile regressions reveal that droughts worsen in Hwange National Park, Zimbabwe. J Arid Environ 71:321–326. doi:10.1016/j.jaridenv.2007.05.005

  15. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, Chicago

  16. Courant S, Fortin D (2012) Search efficiency of free-ranging plains bison for optimal food items. Anim Behav 84:1039–1049. doi:10.1016/j.anbehav.2012.08.003

  17. Cowlishaw G, Lawes MJ, Lightbody M, Martin A, Pettifor R, Rowcliffe JM (2004) A simple rule for the costs of vigilance: empirical evidence from a social forager. Proc R Soc B Biol Sci 271:27–33

  18. Cripps JK, Wilson ME, Elgar MA, Coulson G (2011) Experimental manipulation of fertility reveals potential lactation costs in a free-ranging marsupial. Biol Lett 7:859–862. doi:10.1098/rsbl.2011.0526

  19. Drouet-Hoguet N (2007) Influence of anthropogenic activities on feeding habits and numerical response of spotted hyaena in a dystrophic woodland savanna dominated by elephants. PhD dissertation, University of Lyon, France

  20. Duncan P (1985) Time-budgets of Camargue horses. III. Environmental influences. Behaviour 92:188–208

  21. Duncan P, Foose T, Gordon I, Gakahu C (1990) Comparative nutrient extraction from forages by grazing bovids and equids: a test of the nutritional model of equid/bovid competition and coexistence. Oecologia 84:411–418. doi:10.1007/BF00329768

  22. Ebensperger LA, Hurtado MJ, Ramos-Jiliberto R (2006) Vigilance and collective detection of predators in degus (Octodon degus). Ethology 112:879–887. doi:10.1111/j.1439-0310.2006.01242.x

  23. Favreau F-R, Goldizen AW, Pays O (2010) Interactions among social monitoring, anti-predator vigilance and group size in eastern grey kangaroos. Proc R Soc B Biol Sci 277:2089–2095. doi:10.1098/rspb.2009.2337

  24. Ferretti F, Costa A, Corazza M, Pietrocini V, Cesaretti G, Lovari S (2014) Males are faster foragers than females: intersexual differences of foraging behaviour in the Apennine chamois. Behav Ecol Sociobiol 68:1335–1344. doi:10.1007/s00265-014-1744-5

  25. Fischhoff IR, Sundaresan SR, Cordingley J, Rubenstein DI (2007) Habitat use and movements of plains zebra (Equus burchelli) in response to predation danger from lions. Behav Ecol 18:725–729. doi:10.1093/beheco/arm036

  26. Fleurance G, Fritz H, Duncan P, Gordon I, Edouard N, Vial C (2009) Instantaneous intake rate in horses of different body sizes: influence of sward biomass and fibrousness. Appl Anim Behav Sci 117:84–92. doi:10.1016/j.applanim.2008.11.006

  27. Fortin D, Boyce MS, Merrill EH, Fryxell JM (2004) Foraging costs of vigilance in large mammalian herbivores. Oikos 107:172–180. doi:10.1111/j.0030-1299.2004.12976.x

  28. Frid A (1997) Vigilance by female Dall’s sheep: interactions between predation risk factors. Anim Behav 53:799–808. doi:10.1006/anbe.1996.0345

  29. Fritz H, Guillemain M, Durant D (2002) The cost of vigilance for intake rate in the mallard (Anas platyrhynchos): an approach through foraging experiments. Ethol Ecol Evol 14:91–97

  30. Gakahu C (1982) Feeding strategies of the plains zebras, Equus quagga burchelli, in the Ambolesi ecosystem. PhD dissertation, University of Nairobi, Kenya

  31. Gaylard A, Owen-Smith N, Redfern J (2003) Surface water availability: implications for heterogeneity and ecosystem processes. In: Du Toit JT, Rogers KH, Biggs HC (eds) The Kruger experience. Ecology and management of savanna heterogeneity. Island Press, Washington, pp 171–188

  32. Gélin U, Wilson ME, Coulson GM, Festa-Bianchet M (2013) Offspring sex, current and previous reproduction affect feeding behaviour in wild eastern grey kangaroos. Anim Behav 86:885–891. doi:10.1016/j.anbehav.2013.08.016

  33. Grange S, Duncan P (2006) Bottom-up and top-down processes in African ungulate communities: resources and predation acting on the relative abundance of zebra and grazing bovids. Ecography 29:899–907. doi:10.1111/j.2006.0906-7590.04684.x

  34. Grange S, Barnier F, Duncan P, Gaillard JM, Valeix M, Ncube H, Fritz H (2015) Demography of plains zebras (Equus quagga) under heavy predation. Popul Ecol 57:201–214

  35. Guillemain M, Duncan P, Fritz H (2001) Switching to a feeding method that obstructs vision increases head-up vigilance in dabbling ducks. J Avian Biol 32:345–350. doi:10.1111/j.0908-8857.2001.320409.x

  36. Hamel S, Côté SD (2008) Trade-offs in activity budget in an alpine ungulate: contrasting lactating and nonlactating females. Anim Behav 75:217–227. doi:10.1016/j.anbehav.2007.04.028

  37. Hayward MW, Kerley GIH (2005) Prey preferences of the lion (Panthera leo). J Zool 267:309. doi:10.1017/S0952836905007508

  38. Illius A, Fitzgibbon CD (1994) Costs of vigilance in foraging ungulates. Anim Behav 47:481–484. doi:10.1006/anbe.1994.1067

  39. Jönsson K (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78:57–66

  40. Klingel H (1969) The social organisation and population ecology of the plains zebra (Equus quagga). Zool Afr 4:249–263

  41. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford

  42. Lima SL (1990) Protective cover and the use of space: different strategies in finches. Oikos 58:151–158. doi:10.2307/3545422

  43. Loveridge AJ, Davidson Z, Hunt JE, Valeix M, Elliot N, Stapelkamp B (2007) Hwange Lion Project annual report 2007. Harare, Zimbabwe

  44. McNamara JM, Houston AI (1992) Risk-sensitive foraging: a review of the theory. Bull Math Biol 54:355–378

  45. 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. doi:10.1139/z02-126

  46. Owen-Smith N (1988) Megaherbivores. The influence of very large body size on ecology. Cambridge University Press, Cambridge

  47. Owen-Smith N (2002) Adaptive herbivore ecology. From resources to populations in variable environments. Cambridge University Press, Cambridge

  48. Pappano DJ, Snyder-Mackler N, Bergman TJ, Beehner JC (2012) Social ‘predators’ within a multilevel primate society. Anim Behav 84:653–658

  49. Pays O, Jarman PJ (2008) Does sex affect both individual and collective vigilance in social mammalian herbivores? The case of the eastern grey kangaroo Behav Ecol Sociobiol 62:757–767. doi:10.1007/s00265-007-0501-4

  50. Pays O, Blanchard P, Valeix M, Chamaillé-Jammes S, Duncan P, Périquet S, Lombard M, Ncube G, Tarakini T, Makuwe E, Fritz H (2012) Detecting predators and locating competitors while foraging: an experimental study of a medium-sized herbivore in an African savanna. Oecologia 169:419–430. doi:10.1007/s00442-011-2218-3

  51. Pays O, Beauchamp G, Carter AJ, Goldizen AW (2013) Foraging in groups allows collective predator detection in a mammal species without alarm calls. Behav Ecol 24:1229–1236. doi:10.1093/beheco/art057

  52. Penning PD, Parsons AJ, Orr RJ, Harvey A, Champion RA (1995) Intake and behaviour responses by sheep, in different physiological states, when grazing monocultures of grass or white clover. Appl Anim Behav Sci 45:63–78. doi:10.1016/0168-1591(95)00602-O

  53. Périquet S, Todd-Jones L, Valeix M, Stapelkamp B, Elliot N, Wijers M, Pays O, Fortin D, Madzikanda H, Fritz H, Macdonald DW, Loveridge AJ (2012) Influence of immediate predation risk by lions on the vigilance of prey of different body size. Behav Ecol 23:970–976. doi:10.1093/beheco/ars060

  54. Prins H, Iason GRG (1989) Dangerous lions and nonchalant buffalo. Behaviour 108:262–296

  55. R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/

  56. Rogers CML (1993) A woody vegetation survey of Hwange National Park. Harare, Zimbabwe

  57. Rubenstein DI (1986) Ecology and sociality in horses and zebras. In: Rubenstein DI, Wrangham RW (eds) Ecological aspects of social evolution. Princeton University Press, Princeton, pp 282–302

  58. Rubenstein DI (2010) Ecology, social behavior, and conservation in zebras. In: Macedo R (ed) Advances in the study of behavior: behavioral ecology of tropical animals, vol 42, Elsevier, Oxford, pp 231–258

  59. Rubenstein DI, Hack M (2004) Natural and sexual selection and the evolution of multi-level societies: insights from zebras with comparisons to primates. In: Van Schaik CP, Kappeler PM (eds) New and comparative perspectives. Sexual selection in primates. Cambridge University Press, Cambridge, pp 266–279

  60. Ruckstuhl KE, Neuhaus P (2009) Activity budgets and sociality in a monomorphic ungulate: the African oryx (Oryx gazella). Can J Zool 87:165–174. doi:10.1139/Z08-148

  61. Ruckstuhl KE, 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. doi:10.1007/s00265-003-0615-2

  62. Sansom A, Cresswell W, Minderman J, Lind J (2008) Vigilance benefits and competition costs in groups: do individual redshanks gain an overall foraging benefit? Anim Behav 75:1869–1875. doi:10.1016/j.anbehav.2007.11.005

  63. Simpson HI, Rands SA, Nicol CJ (2012) Social structure, vigilance and behaviour of plains zebra (Equus burchellii): a 5-year case study of individuals living on a managed wildlife reserve. Acta Theriol 57:111–120. doi:10.1007/s13364-011-0061-x

  64. Smith AC, Kelez S, Buchanan-Smith HM (2004) Factors affecting vigilance within wild mixed-species troops of saddleback (Saguinus fuscicollis) and moustached tamarins (S. mystax). Behav Ecol Sociobiol 56:18–25

  65. Spalinger DE, Hobbs NT (1992) Mechanisms of foraging in mammalian herbivores: new models of functional response. Am Nat 140:325–348

  66. Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R Soc B 363:375–398

  67. Thaker M, Vanak AT, Owen CR, Ogden MB, Slotow R (2010) Group dynamics of zebra and wildebeest in a woodland savanna: effects of predation risk and habitat density. Plos One 5:6

  68. Unck CE, Waterman JM, Verburgt L, Bateman PW (2009) Quantity versus quality: how does level of predation threat affect Cape ground squirrel vigilance? Anim Behav 78:625–632. doi:10.1016/j.anbehav.2009.05.028

  69. Valeix M, Loveridge AJ, Chamaillé-Jammes S, Davidson Z, Murindagomo F, Fritz H, Macdonald DW (2009) Behavioral adjustments of African herbivores to predation risk by lions: spatiotemporal variations influence habitat use. Ecology 90:23–30. doi:10.1890/08-0606.1

  70. Venter F, Scholes R, Eckhardt H (2003) The abiotic template and its associated vegetation pattern. In: Du Toit JT, Rogers KH, Biggs HC (eds) The Kruger experience. Ecology and management of savanna heterogeneity. Island Press, Washington, pp 83–129

  71. Whittingham MJ, Butler SJ, Quinn JL, Cresswell W (2004) The effect of limited visibility on vigilance behaviour and speed of predator detection: implications for the conservation of granivorous passerines. Oikos 106:377–385

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Acknowledgments

This work was funded by the CNRS Institut Ecologie et Environnement, the Zones Ateliers Network Long-term Ecological Research (LTER) France; the Agence Nationale de la Recherche (FEAR project ANR-08-BLAN-0022), CIRAD, the French Ministère des Affaires Etrangères and the Ambassade de France au Zimbabwe. Pierrick Blanchard is at the Laboratory Evolution et Diversité Biologique, part of the Laboratoire d’Excellence TULIP (ANR-10-LABX-41). The Director General of the Zimbabwe Parks and Wildlife Management Authority is acknowledged for providing the opportunity to carry out this research: we are particularly grateful to Dr H. Madzikanda for his long-term support and friendship and our warm thanks also go to Mr A. Musakwa, the then area manager, for his support, as well as to the then senior ecologist in HNP, Mr G. Mtare. This study is part of the Hwange Environmental Research Development (HERD) program, now Hwange LTER (Zone Atelier Hwange): we would like to thank the whole HERD team for making this study possible, Dr G. Fleurance for providing the data on horses, and finally Dr K.E. Ruckstuhl, Dr F. Ferretti and one anonymous referee for their helpful suggestions.

Author contribution statement

O. P. and H. F. conceived and designed the experiments. O. P., P. B., F. B. and P. D. conducted the fieldwork. F. B. and O. P. analysed the data. F. B., O. P. and P. D. wrote the manuscript. Other authors provided crucial editorial advice.

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Correspondence to Olivier Pays.

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The authors declare that they have no conflict of interest.

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Our work complied with the current laws of Zimbabwe. It was conducted under permits from the Director General of the Zimbabwe Parks and approved by the Wildlife Management Authority [reference D/M/Gen/(T), permit 23(l)(c)(ii) 01/2010]. The long-term individual-based study on zebra population dynamics started in 2004 is supervised by Dr P. Duncan and is part of the programme of the CNRS ZA/LTER Hwange directed by Dr H. Fritz under permits from the authorities cited above.

Communicated by Peter Banks.

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Barnier, F., Duncan, P., Fritz, H. et al. Between-gender differences in vigilance do not necessarily lead to differences in foraging-vigilance tradeoffs. Oecologia 181, 757–768 (2016). https://doi.org/10.1007/s00442-016-3614-5

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Keywords

  • Anti-predator behaviour
  • Gender effect
  • Herbivores
  • Intake rate
  • Zebra