Advertisement

Behavioral Ecology and Sociobiology

, Volume 68, Issue 10, pp 1649–1660 | Cite as

Intra-sexual variability in feeding behaviour of a mountain ungulate: size matters

  • Francesca Brivio
  • Stefano Grignolio
  • Alice Brambilla
  • Marco Apollonio
Original Paper

Abstract

Many studies comparing the behaviour of individuals of different genders or species showed that animal body mass and forage quality/quantity are key elements of the foraging ecology of herbivores. Since body mass could also influence the animal’s sensitivity to predation risk, its vigilance behaviour should consequently be affected. Alpine ibex (Capra ibex) is characterised by a strong dimorphism among males of different ages, thus representing an ideal case study for testing the Jarman-Bell principle, avoiding possibly misleading effects resulting from the comparison between different species or genders. We analysed the fine-scale foraging behaviour of male ibex in order to assess the effect of body mass and the effects of vegetation quality/quantity on both foraging and vigilance behaviour. Our results showed that smaller males were more selective than larger ones, on account of their lower capability of digesting plant. Smaller males scanned the environment more frequently than larger ones. Male ibex grazed more selectively in sites with high quality forage and their bite rate increased as forage biomass decreased. Vigilance frequency increased with increasing forage biomass as, under these circumstances, ibex are able to prolong anti-predator vigilance while chewing bites that have already been cropped. Our findings highlight the effects of body mass per se on both foraging and anti-predator behaviours in herbivores, thus supporting the Jarman-Bell principle. Foraging can arguably be considered a very flexible behaviour with high evolutionary relevance as it enables herbivores to optimally adjust their total energy intake under varying conditions of food resources.

Keywords

Alpine ibex Body mass Diet selection Forage quality Jarman-Bell principle Vigilance behaviour 

Notes

Acknowledgments

We wish to thank the Gran Paradiso National Park for their economic and logistical support. We are grateful to the rangers of the GPNP for the capture of animals and for their contribution in data collection. A special thank is due to B. Bassano and A. von Hardenberg for their scientific input during all steps of this research. We thank C. Fracastoro, V. Gerbo, A. Melotto and E. Piano for their invaluable help in the fieldwork. Finally, we thank the Regione Autonoma della Valle d’Aosta for meteorological data. FB post-doc grant and this project were also supported by the Italian Ministry of Education, University and Research (PRIN 2010–2011, 20108 TZKHC, J81J12000790001). SG had the support of the fund “P.O.R. F.S.E. 2007–2013—Obiettivo competitività regionale e occupazione. Asse IV Capitale umano—Linea di attività 1.3.1”. The English version was edited by G. Falceri.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

This study complies with all national and regional laws dealing with ethics and animal welfare. The capture and handling protocol was approved by the Italian Ministry of Environment (protoc. n. 25114/04).

Supplementary material

265_2014_1773_MOESM1_ESM.pdf (9.9 mb)
ESM 1 (PDF 10175 kb)

References

  1. Alados CL, Escos J (1987) Relationships between movements rate, agonistic displacements and forage availability in Spanish ibexes (Capra pyrenaica). Biol Behav 12:245–255Google Scholar
  2. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–265PubMedCrossRefGoogle Scholar
  3. Arnold GW (1975) Herbage intake and grazing behaviour in cows of four breeds at different physiological states. Aust J Agric Res 21:755–766Google Scholar
  4. Aublet JF, Festa-Bianchet M, Bergero D, Bassano B (2009) Temperature constraints on foraging behaviour of male alpine ibex (Capra ibex) in summer. Oecologia 159:237–247PubMedCrossRefGoogle Scholar
  5. Bailey DW, Gross JE, Laca EA, Rittenhouse LR, Coughenour MB, Swift DM, Sims PL (1996) Mechanisms that result in large herbivore grazing distribution patterns. J Range Manag 49:386–400CrossRefGoogle Scholar
  6. Barboza PS, Bowyer RT (2000) Sexual segregation in dimorphic deer: a new gastrocentric hypothesis. J Mammal 81:473–489CrossRefGoogle Scholar
  7. Bassano B, Bergero D, Peracino A (2003a) Accuracy of body weight prediction in alpine ibex (Capra ibex, L. 1758) using morphometry. J Anim Physiol Anim Nutr 87:79–85CrossRefGoogle Scholar
  8. Bassano B, von Hardenberg A, Pelletier F, Gobbi G (2003b) A method to weight free-ranging ungulates without handling. Wildl Soc B 31:1205–1209Google Scholar
  9. Bednekoff PA, Lima SL (2002) Why are scanning patterns so variable? An overlooked question in the study of anti-predator vigilance. J Avian Biol 33:143–149CrossRefGoogle Scholar
  10. Berger J, Cunningham C (1988) Size-related effects on search times in North American grassland female ungulates. Ecology 69:177–183CrossRefGoogle Scholar
  11. Bergeron P, Grignolio S, Apollonio M, Shipley B, Festa-Bianchet M (2010) Secondary sexual characters signal fighting ability and determine social rank in alpine ibex (Capra ibex). Behav Ecol Sociobiol 64:1299–1307CrossRefGoogle Scholar
  12. Bergman CM, Fryxell JM, Gates CC, Fortin D (2001) Ungulate foraging strategies: energy maximizing or time minimizing? J Anim Ecol 70:289–300CrossRefGoogle Scholar
  13. Bunnell FL, Gillingham MP (1985) Foraging behavior: dynamics of dining out. In: Hudson RJ, White RG (eds) Bioenergetics of wild herbivores. CRC, Boca Raton, pp 53–75Google Scholar
  14. Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer, New YorkGoogle Scholar
  15. Carranza J, Valencia J (1999) Red deer females collect on male clumps at mating areas. Behav Ecol 10:525–532CrossRefGoogle Scholar
  16. Carranza J, Alarcos S, Sánchez-Prieto CB, Valencia J, Mateos C (2004) Disposable-soma senescence mediated by sexual selection in an ungulate. Nature 432:215–218PubMedCrossRefGoogle Scholar
  17. Clauss M, Frey R, Kiefer B, Lechner-Doll M, Loehlein W, Polster C, Rössner GE, Streich WJ (2003) The maximum attainable body size of herbivorous mammals: morphophysiological constraints on foregut, and adaptations of hindgut fermenters. Oecologia 136:14–27PubMedCrossRefGoogle Scholar
  18. 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 Lond B 271:27–33CrossRefGoogle Scholar
  19. Demment MW, Van Soest PJ (1985) A nutritional explanation for body-size patterns of ruminant and nonruminant herbivores. Am Nat 125:641–672CrossRefGoogle Scholar
  20. R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/
  21. Dochtermann NA, Jenkins SH (2011) Developing multiple hypotheses in behavioral ecology. Behav Ecol Sociobiol 65:37–85CrossRefGoogle Scholar
  22. 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 68:1335–1344Google Scholar
  23. Festa-Bianchet M (1988) Seasonal range selection in bighorn sheep: conflicts between forage quality, forage quantity, and predator avoidance. Oecologia 75:580–586CrossRefGoogle Scholar
  24. Fortin D, Boyce MS, Merrill EH, Fryxell JM (2004) Foraging costs of vigilance in large mammalian herbivores. Oikos 107:172–180CrossRefGoogle Scholar
  25. 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 14:91–97CrossRefGoogle Scholar
  26. Fryxell JM, Wilmshurst JF, Sinclair RE (2004) Predictive models of movement by Serengeti grazers. Ecology 85:2429–2435CrossRefGoogle Scholar
  27. Geist V (1974) On the relationship of ecology and behaviour in the evolution of ungulates: theoretical considerations. In: Geist V, Walther F (eds) The behaviour of ungulates and its relation to management, vol 24. IUCN, Morges, pp 235–246Google Scholar
  28. Grignolio S, Parrini F, Bassano B, Luccarini S, Apollonio M (2003) Habitat selection in adult males of alpine ibex, Capra ibex ibex. Folia Zool 52:113–120Google Scholar
  29. Grignolio S, Rossi I, Bassano B, Apollonio M (2007) Predation risk as a factor affecting sexual segregation in alpine ibex. J Mammal 88:1488–1497CrossRefGoogle Scholar
  30. Gross JE, Shipley LA, Hobbs NT, Spalinger DE, Wunder BA (1993) Functional response of herbivores in food-concentrated patches: tests of a mechanistic model. Ecology 74:778–791CrossRefGoogle Scholar
  31. Gross JE, Alkon PU, Demment MW (1996) Nutritional ecology of dimorphic herbivores: digestion and passage rates in Nubian ibex. Oecologia 107:170–178CrossRefGoogle Scholar
  32. Hamr J (1984) Home range sizes of male chamois (Rupicapra rupicapra) in the Tyrolean Alps. Acta Zool Fenn 171:293–298Google Scholar
  33. Hebblewhite M, Merrill E, McDermid G (2008) A multi-scale test of the forage maturation hypothesis in a partially migratory ungulate population. Ecol Monogr 78:141–166CrossRefGoogle Scholar
  34. Illius AW (2006) Linking functional responses and foraging behaviour to population dynamics. In: Danell K, Bergström R, Duncan P, Pastor J (eds) Large herbivore ecology, ecosystem dynamics and conservation. Cambridge University Press, New York, pp 71–96CrossRefGoogle Scholar
  35. Illius AW, Fitzgibbon C (1994) Costs of vigilance in foraging ungulates. Anim Behav 47:481–484CrossRefGoogle Scholar
  36. Illius AW, Gordon IJ (1987) The allometry of food intake in grazing ruminants. J Anim Ecol 56:989–999CrossRefGoogle Scholar
  37. Illius AW, Gordon IJ (1992) Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89:428–434Google Scholar
  38. Komers PE, Messier F, Gates CC (1993) Group structure in wood bison: nutritional and reproductive determinants. Can J Zool 71:1367–1371CrossRefGoogle Scholar
  39. Laca EA, Ungar ED, Demment MW (1994) Mechanisms of handling time and intake rate of a large mammalian grazer. Appl Anim Behav Sci 39:3–19CrossRefGoogle Scholar
  40. Laundré JW, Hernández L, Altendorf KB (2001) Wolves, elk, bison: reestablishing the ‘landscape of fear’ in Yellowstone National Park, USA. Can J Zool 79:1401–1409CrossRefGoogle Scholar
  41. Lima SL (1988) Vigilance and diet selection: the classical diet model reconsidered. J Theor Biol 132:127–143CrossRefGoogle Scholar
  42. Lima SL (1995) Back to the basics of anti-predatory vigilance: the group size effect. Anim Behav 49:11–20CrossRefGoogle Scholar
  43. Lima SL, Zollner PA, Bednekoff PA (1999) Predation, scramble competition, and the vigilance group size effect in dark-eyed juncos (Junco hyemalis). Behav Ecol Sociobiol 46:110–116CrossRefGoogle Scholar
  44. 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 80:1437–1441CrossRefGoogle Scholar
  45. Oosenbrug SM, Theberge JB (1980) Altitudinal movements and summer habitat preferences of woodland caribou in the Kluane Ranges, Yukon territory. Arctic 33:59–72CrossRefGoogle Scholar
  46. Palmegiani I, Gazzola A, Apollonio M (2013) Wolf diet and its impact on the ungulates community in a new recolonized area of western alps: Gran Paradiso National Park. Folia Zool 62:59–66Google Scholar
  47. Parrini F, Grignolio S, Luccarini S, Bassano B, Apollonio M (2003) Spatial behaviour of adult male alpine ibex (Capra ibex ibex) in the Gran Paradiso National Park, Italy. Acta Theriol 48:411–423CrossRefGoogle Scholar
  48. Parsons AJ, Thornley JHM, Newman J, Penning PD (1994) A mechanistic model of some physical determinants of intake rate and diet selection in a two-species temperate grassland sward. Funct Ecol 8:187–204CrossRefGoogle Scholar
  49. Pelletier F, Festa-Bianchet M (2004) Effects of body mass, age, dominance and parasite load on foraging time of bighorns rams, Ovis canadensis. Behav Ecol Sociobiol 56:546–551CrossRefGoogle Scholar
  50. Pelletier F, Réale D, Garant D, Coltman DW, Festa-Bianchet M (2007) Selection on heritable seasonal plasticity of body mass. Evolution 61:1969–1979PubMedCrossRefGoogle Scholar
  51. Penning PD, Parsons AJ, Orr RJ, Treacher TT (1991) Intake and behaviour responses by sheep to changes in sward characteristics under continuous stocking. Grass Forage Sci 46:15–28CrossRefGoogle Scholar
  52. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New YorkCrossRefGoogle Scholar
  53. Pulliam HR, Caraco T (1984) Living in groups: is there an optimal group size? In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell, Cambridge, pp 122–147Google Scholar
  54. Risenhoover KL, Bailey JA (1985) Relationships between group size, feeding time, and agonistic behavior of mountain goats. Can J Zool 63:2501–2506CrossRefGoogle Scholar
  55. Roberts G (1996) Why individual vigilance declines as group size increases. Anim Behav 51:1077–1086CrossRefGoogle Scholar
  56. Ruckstuhl KE, Neuhaus P (2005) Sexual segregation in vertebrates: ecology of the two sexes. Cambridge University PressGoogle Scholar
  57. 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 54:167–173Google Scholar
  58. Saino N (1994) Time budget variation in relation to flock size in carrion crows, Corvus corone corone. Anim Behav 47:1189–1196CrossRefGoogle Scholar
  59. Senft RL, Coughenour MB, Bailey DW, Rittenhouse LR, Sala OE, Swift DM (1987) Large herbivore foraging and ecological hierarchies. Bioscience 37:789–799CrossRefGoogle Scholar
  60. Shipley LA, Spalinger DE (1995) Influence of size and density of browse patches on intake rates and foraging decisions of young moose and white-tailed deer. Oecologia 104:112–121CrossRefGoogle Scholar
  61. Shipley LA, Gross JE, Spalinger DE, Hobbs NT, Wunder BA (1994) The scaling of intake rate in mammalian herbivores. Am Nat 143:1055–1082CrossRefGoogle Scholar
  62. Spalinger DE, Hobbs NT (1992) Mechanism of foraging in mammalian herbivores: new models of functional response. Am Nat 140:325–348PubMedCrossRefGoogle Scholar
  63. St-Louis A, Côte SD (2012) Foraging behaviour at multiple temporal scales in a wild alpine equid. Oecologia 169:167–176PubMedCrossRefGoogle Scholar
  64. Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21CrossRefGoogle Scholar
  65. Treves A (2000) Theory and method in studies of vigilance and aggregation. Anim Behav 60:711–722PubMedCrossRefGoogle Scholar
  66. Trudell J, White RG (1981) The effect of forage structure and availability on food intake, biting rate, bite size and daily eating time of reindeer. J Appl Ecol 18:63–81CrossRefGoogle Scholar
  67. von Hardenberg A (2005) Sénescence, Sélection Sexuelle et Dynamique de Population du Bouquetin des Alpes (Capra ibex). PhD thesis, Université de Sherbrooke, Sherbrooke, CanadaGoogle Scholar
  68. von Hardenberg A, Shipley B, Festa-Bianchet M (2003) Another one bites the dust: does incisor-arcade size affect mass gain and survival in grazing ungulates? Can J Zool 81:1623–1629CrossRefGoogle Scholar
  69. von Hardenberg A, Bassano B, del P iZuArM, Bogliani G (2004) Horn growth but not asymmetry heralds the onset of senescence in male Alpine ibex (Capra ibex). J Zool 263:425–432Google Scholar
  70. Wilmshurst JF, Fryxell JM, Colucci PE (1999) What constrains daily intake in Thomson’s gazelles? Ecology 80:2338–2347Google Scholar
  71. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Francesca Brivio
    • 1
  • Stefano Grignolio
    • 1
  • Alice Brambilla
    • 2
  • Marco Apollonio
    • 1
  1. 1.Department of Science for Nature and Environmental ResourcesUniversity of SassariSassariItaly
  2. 2.Department of Earth and Environmental ScienceUniversity of PaviaPaviaItaly

Personalised recommendations