Skip to main content
Log in

Vegetation structure and inter-individual distance affect intake rate and foraging efficiency in a granivorous forager, the Eurasian Skylark Alauda arvensis

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

Animals gain benefits from group living through increased probability of predator detection, dilution of individual risk and confusion of predators during attack. A further benefit involves larger groups in which individuals may further decrease the amount of time spent being vigilant, while maintaining the probability of predator detection by allocation of this extra time to foraging activities. Living in groups or flocks, however, also incurs costs, e.g., by increasing inter-group competition, with negative impacts on intake rates. Our aim was to investigate the trade-offs between the costs of competition and the benefits of group living in contrasted habitats. For prey species that rely on sight for detecting predators, vegetation structure may influence the perceived predation risk. Hence, we experimentally examined the combined effects of vegetation height and inter-individual distance on foraging time, intake rate and foraging efficiency in a granivorous species, the Eurasian Skylark (Alauda arvensis). Our experimental results based on temporally captive birds indicate that time devoted to foraging decreased with increasing inter-individual distance, but was unrelated to cover height. Conversely, increasing both vegetation height and distance with other group members did translate into a foraging disadvantage, i.e. reduced intake rate as well as foraging efficiency. Overall, our results show that both vegetation structure and inter-individual distances modify patch profitability, and therefore provide another example of how flock dynamics can influence the trade-off between vigilance and foraging.

Zusammenfassung

Art der Vegetation und Abstände zwischen Einzeltieren beeinflussen Häufigkeit und Effizienz der Nahrungsaufnahme eines Körnerfressers, der Eurasischen Feldlerche ( Alauda arvensis )

Ein Leben in größeren Gruppen ist für Tiere vorteilhaft, weil dadurch Feinde eher entdeckt werden, das Risiko für jedes einzelne Tier geringer ist und Räuber bei einem Angriff verwirrt werden. Ein weiterer Vorteil liegt darin, dass einerseits jedes Einzeltier weniger Zeit in Wachsamkeit und Aufpassen investieren muss, während andererseits die Wahrscheinlichkeit, Feinde zu entdecken, durch die Gruppe weiterhin hoch bleibt. Dadurch gewinnt jedes einzelne Tier zusätzliche Zeit, die für die Nahrungsaufnahme genutzt werden kann. Das Leben in Gruppen, oder Schwärmen, hat jedoch auch seine Kosten: eine erhöhte Konkurrenz zwischen den einzelnen Tieren innerhalb der Gruppe mit entsprechend negativen Auswirkungen auf die Nahrungsaufnahme. Ziel unserer Studie war, in unterschiedlichen Lebensräumen die Vorteile des Gruppenlebens gegen die Nachteile der intensiveren Konkurrenzsituation abzuwägen. Bei Tieren von Beutearten, die davon abhängen, Räuber so rasch wie möglich zu entdecken, beeinflusst die Struktur der Vegetation vermutlich das empfundene Risiko, erbeutet zu werden. Deshalb überprüften wir für eine körnerfressende Art, die Eurasische Feldlerche (Alauda arvensis), experimentell den kombinierten Effekt von Vegetationshöhe und Abständen zwischen den Einzeltieren auf die Dauer, Häufigkeit und Effizienz der Nahrungsaufnahme. Die Ergebnisse unserer Experimente mit zeitweise gekäfigten Vögeln zeigen, dass die für die Nahrungsaufnahme verwendete Zeit mit wachsenden Abständen zwischen den Einzeltieren abnahm, es aber keinen Zusammenhang mit der Vegetationshöhe gab. Wurde jedoch beides, die Vegetationshöhe und die Abstände zu anderen Gruppenmitgliedern, erhöht, ergab sich daraus ein Nachteil für die Ernährung: eine Verminderung sowohl der Häufigkeit als auch der Effizienz der Nahrungsaufnahme. Unsere Ergebnisse zeigen, dass beides, die Vegetationsstruktur und die Abstände zwischen Einzeltieren, Auswirkungen auf den Nahrungs-Ertrag haben können und liefern so ein weiteres Beispiel dafür, wie die Schwarmdynamik den trade-off, das Ausbalancieren der Vor- und Nachteile, von Nahrungsaufnahme und Wachsamkeit beeinflussen kann.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J, Chapman CA, Connor R, Di Fiore A, Dunbar RIM, Henzi SP, Holekamp K, Korstjens AH, Layton R, Lee P, Lehmann J, Manson JH, Ramos-Fernandez G, Strier KB, Van Schaik CP (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654

    Article  Google Scholar 

  • Beauchamp G (1998) The effect of group size on mean food intake rate in birds. Biol Rev 73:449–472

    Article  Google Scholar 

  • Beauchamp G (2009) How does food density influence vigilance in birds and mammals? Anim Behav 78:223–231

    Article  Google Scholar 

  • Beauchamp G (2013) Social foragers adopt a riskier foraging mode in the center of their groups. Biol Lett 9:05–28. http://dx.doi.org/10.1098/rsbl.2013.0528

  • Brown JS, Kotler BP, Mitchell WA (1997) Competition between birds and mammals: a comparison of giving-up densities between crested larks and gerbils. Evol Ecol 11:757–771

    Article  Google Scholar 

  • Butler SJ, Whittingham MJ, Quinn JL, Cresswell W (2005a) Quantifying the interaction between food density and habitat structure in determining patch selection. Anim Behav 69:337–343

    Article  Google Scholar 

  • Butler SJ, Bradbury RB, Whittingham MJ (2005b) Stubble height affects the use of stubble fields by farmland birds. J App Ecol 42:469–476

    Article  Google Scholar 

  • Caraco T, Martindale S, Pulliam HR (1980) Avian time budgets and distance to cover. Auk 97:872–875

    Google Scholar 

  • Chapman CA, Chapman LJ (2000) Determinants of group size in social primates: the importance of travel costs. In: Boinski S, Garber P (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 24–42

    Google Scholar 

  • Clark CW, Mangel M (1986) The evolutionary advantages of group foraging. Theor Pop Biol 30:45–75

    Article  Google Scholar 

  • Cowlishaw G (1998) The role of vigilance in the survival and reproductive strategies of desert baboons. Behaviour 135:431–452

    Article  Google Scholar 

  • Cramp S (1988) The birds of the Western Palearctic, vol 5. Oxford University Press, Oxford

    Google Scholar 

  • Cresswell W (1994) Song as a pursuit-deterrent signal, and its occurrence relative to other anti-predator behaviours of sky- lark (Alauda arvensis) on attack by merlins (Falco columbarius). Behav Ecol Sociobiol 34:217–223

    Article  Google Scholar 

  • Cresswell W (1998) Variation in the strength of interference competition with resource density in blackbirds, Turdus merula. Oikos 81:152–160

    Article  Google Scholar 

  • Desrochers A, Hannon SJ, Nordin KE (1988) Winter survival and territory acquisition in a northern population of Black-capped Chikadees. Auk 105:727–736

    Google Scholar 

  • Donald PF, Buckingham DL, Moorcroft D, Muirhead LB, Evans AD, Kirby WB (2001) Habitat use and diet of skylarks Alauda arvensis wintering on lowland farmland in southern Britain. J App Ecol 38:536–547

    Article  Google Scholar 

  • Ekman J (1987) Exposure and time use in willow tit flocks: the cost of subordination. Anim Behav 35:445–452

    Article  Google Scholar 

  • Eraud C, Lallemand J, Lormee H (2006) Sex-ratio of skylark Alauda arvensis in relation to timing of breeding: capsule earlier broods tend to be more male biased than later broods. Bird Study 53:319–322

    Article  Google Scholar 

  • Fernandez-Juricic E, Kacelnik A (2004) Information transfer and gain in flocks: the effects of quality and quantity of social information at different neighbour distances. Behav Ecol Sociobiol 55:502–511

    Article  Google Scholar 

  • Fernandez-Juricic E, Erichsen JT, Kacelnik A (2004) Visual perception and social foraging in birds. Trends Ecol Evol 19:25–31

    Article  PubMed  Google Scholar 

  • Fernandez-Juricic E, Beauchamp G, Bastain B (2007) Group-size and distance to neighbours effects on feeding and vigilance in brown-headed cowbirds. Anim Behav 73:771–778

    Article  Google Scholar 

  • Foster WA, Treherne JE (1981) Evidence for the dilution effect and the selfish herd from fish predation on a marine insect. Nature 293:466–467

    Article  Google Scholar 

  • Geiger F, Hegemann A, Gleichman M, Flinks H, de Snoo GR, Prinz S, Tieleman BI, Berendse F (2014) Habitat use and diet of skylarks (Alauda arvensis) wintering in an intensive agricultural landscape of the Netherlands. J Ornithol 155:507–518

    Article  Google Scholar 

  • Gillings S, Fuller R (2001) Habitat selection by skylarks Alauda arvensis wintering in Britain in 1997/98. Bird Study 48:293–307

    Article  Google Scholar 

  • Goulson D, Peat J, Stout J, Tuckers J, Darvill B, Derwent L, Hughes WHO (2002) Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency ? Anim Behav 64:123–130

    Article  Google Scholar 

  • Hilton GM, Cresswell W, Ruxton GD (1999) Intraflock variation in the speed of escape—flight response on attack by an avian predator. Behav Ecol 10:391–395

    Article  Google Scholar 

  • Högstad O (1988) Social rank and antipredator behaviour of willow tits Parus montanus in winter flocks. Ibis 130:45–56

    Article  Google Scholar 

  • Janson CH (1988) Intra-specific food competition and primate social structure: a synthesis. Behaviour 105:1–17

    Article  Google Scholar 

  • Kiltie RA (2000) Scaling of visual acuity with body size in mammals and birds. Funct Ecol 14:226–234

    Article  Google Scholar 

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

    Google Scholar 

  • Krebs J, MacRoberts M, Cullen J (1972) Flocking and feeding in the great tit Parus major: an experimental study. Ibis 114:507–530

    Article  Google Scholar 

  • Lima SL (1995) Back to the basics of anti-predatory vigilance: the group-size effect. Anim Behav 49:11–20

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Back to the basics of antipredatory vigilance: can non-vigilant animals detect attack? Anim Behav 58:537–543

    Article  PubMed  Google Scholar 

  • Lima L, Dill LM (1990) Behavioral decisions made under the risk of predation. A review and prospectus. Can J Zool 68:619–640

    Article  Google Scholar 

  • 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 46:110–116

    Article  Google Scholar 

  • Metcalfe NB (1984) The effects of habitat on the vigilance of shorebirds: is visibility important? Anim Behav 32:981–985

    Article  Google Scholar 

  • Moorcroft D, Whittingham MJ, Bradbury RB, Wilson JD (2002) The selection of stubble fields by wintering granivorous birds reflects vegetation cover and food abundance. J App Ecol 39:535–547

    Article  Google Scholar 

  • Ottoni EB (1996) Etholog 1.0: ethological transcription tool for Windows. Behavior Research Methods, Instruments and Computers 28:472–473

    Article  Google Scholar 

  • Palombit RA, Cheney DL, Seyfarth RM (1999) Male grunts as mediators of social interaction with females in wild chacma baboons (Papio cynocephalus ursinus). Behaviour 136:221–242

    Article  Google Scholar 

  • Pelletier F, Festa-Bianchet M (2004) Effects of body mass, age, dominance and parasite load on foraging time of bighorn rams, Ovis canadensis. Behav Ecol Sociobiol 56:546–551

    Article  Google Scholar 

  • Powolny T (2012) Faire face à l’hiver—Quelles réponses à l’hétérogénéité de la ressource en agro-écosystème ? L’exemple de l’alouette des champs (Alauda arvensis). Université de Poitiers, France

    Google Scholar 

  • Powolny T, Eraud C, Bretagnolle V (2012) Group size modulates time budget and foraging efficiency in captive skylarks Alauda arvensis. J Ornithol 153:485–490

    Article  Google Scholar 

  • Powolny T, Bretagnolle V, Aguilar A, Eraud C (2014) Sex-Related Differences in the trade-off between foraging and vigilance in a granivorous forager. PLoS ONE 9(7):e101598. doi:10.1371/journal.pone.0101598

    Article  PubMed Central  PubMed  Google Scholar 

  • Roberts G (1996) Why individual’s vigilance declines as group size increases. Anim Behav 51:1077–1086

    Article  Google Scholar 

  • Robinson RA, Sutherland WJ (1999) The winter distribution of seed-eating birds: habitat structure, seed density and seasonal depletion. Ecography 22:447–454

    Article  Google Scholar 

  • Rohner C, Krebs CJ (1996) Owl predation on snowshoe hares: consequences of antipredator behaviour. Oecologia 108:303–310

    Article  Google Scholar 

  • Rolando A, Caldoni R, De Sanctis A, Laiolo P (2001) Vigilance and neighbour distance in foraging flocks of red-billed choughs, Pyrrhocorax pyrrhocorax. J Zool Lond 253:225–232

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Schellinck J, White T (2011) A review of attraction and repulsion models of aggregation: methods, findings and a discussion of model validation. Ecol Model 222:1897–1911

    Article  Google Scholar 

  • Steenbeck R, Piek RC, Van Buul M, Van Hoff JARAM (1999) Vigilance in wild Thomas’s langurs (Presbytis thomasi): the importance of infanticide risk. Behav Ecol Sociobiol 45:137–150

    Article  Google Scholar 

  • Teichroeb JA, Sicotte P (2012) Cost-free vigilance during feeding in folivorous primates? Examining the effects of predation risk, scramble competition, and infanticide threat on vigilance in ursine colobus monkeys (Colobus vellerosus). Behav Ecol Sociobiol 66:453–466

    Article  Google Scholar 

  • Templeton JJ, Giraldeau LA (1995) Public information cues affect the scrounging decisions of starlings. Anim Behav 49:1617–1626

    Article  Google Scholar 

  • Tisdale V, Fernandez-Juricic E (2009) Vigilance and predator detection vary between avian species with different visual acuity and coverage. Behav Ecol 20:936–945

    Article  Google Scholar 

  • Treves A (1998) The influence of group size and neighbours on vigilance in two species of arboreal monkeys. Behaviour 135:453–481

    Article  Google Scholar 

  • Treves A (2000) Theory and method in studies of vigilance and aggregation. Anim Behav 60:711–722

    Article  PubMed  Google Scholar 

  • Valone TJ (1993) Patch information and estimation—a cost of group foraging. Oikos 68:258–266

    Article  Google Scholar 

  • Valone TJ, Templeton JJ (2002) Public information for the assessment of quality: a widespread social phenomenon. Philos Trans R Soc Lond B 357:1549–1557

    Article  Google Scholar 

  • Verdolin JL (2006) Meta-analasis of foraging and predation risk trade-offs in terrestrials systems. Behav Ecol Sociobiol 60:457–464

    Article  Google Scholar 

  • Whittingham MJ, Markland HM (2002) The influence of substrate on the functional response of an avian granivore and its implications for farmland bird conservation. Oecologia 130:637–644

    Article  Google Scholar 

  • Whittingham MJ, Devereux CL, Evans AD, Bradbury RB (2006) Altering perceived predation risk and food availability: management prescriptions to benefit farmland birds on stubble fields. J Appl Ecol 43:640–650

    Article  Google Scholar 

  • Wilson JD, Evans J, Browne SJ, King JR (1997) Territory distribution and breeding success of skylarks Alauda arvensis on organic and intensive farmland in southern England. J Appl Ecol 34:1462–1478

    Article  Google Scholar 

  • Wrangham RW (1980) An ecological model of female bonded primate groups. Behaviour 75:262–300

    Article  Google Scholar 

  • Zimmer C, Boos M, Poulin N, Gosler A, Petit O, Robin JP (2011) Evidence of the trade-off between starvation and predation risks in ducks. PLoS ONE 6:e22352

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank V. Rocheteau for assistance during fieldwork, N. Guillon, and X. Duchemin for caring for the birds while in captivity and two anonymous reviewers whose comments greatly improved the manuscript. This work was performed with governmental authorizations from the Préfecture des Deux-Sèvres (Niort, France, No. 10.79-219). All experiments were carried out in compliance with French legal requirements. The protocol was approved by the Committee on the Ethics of Animal Experiments of the National Conservation Authority (Permit No. 79349). Bird captures were performed under permit from the National Hunting and Wildlife Agency to TP (No. 2009-014). T.P. was funded by a PhD grant from ONCFS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thibaut Powolny.

Additional information

Communicated by F. Bairlein.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Powolny, T., Eraud, C., Masson, JD. et al. Vegetation structure and inter-individual distance affect intake rate and foraging efficiency in a granivorous forager, the Eurasian Skylark Alauda arvensis . J Ornithol 156, 569–578 (2015). https://doi.org/10.1007/s10336-015-1161-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-015-1161-1

Keywords

Navigation