Matching times of leading and following suggest cooperation through direct reciprocity during V-formation flight in ibis

Bernhard Voelkl; Steven J. Portugal; Markus Unsöld; James R. Usherwood; Alan M. Wilson; Johannes Fritz

doi:10.1073/pnas.1413589112

New Research In

Edited by Raghavendra Gadagkar, Indian Institute of Science, Bangalore, India, and approved January 13, 2015 (received for review July 17, 2014)

Significance

Cooperation in animals is an enigma because it contravenes the basic notion that evolution favors selfish genes that promote only their own well-being. Bird migration in organized V-shaped or echelon formations constitutes such a cooperation dilemma. We show that juvenile Northern bald ibis (Geronticus eremita) cooperate by taking turns and precisely matching times they spend in the advantageous trailing position and in the disadvantageous front position. This time matching is done on a pairwise level. Furthermore, we found evidence that the animals' propensity to reciprocate in leading has a substantial influence on the size and cohesion of the flight formations. This study shows that direct reciprocation can enable cooperation between animals in a natural context.

Abstract

One conspicuous feature of several larger bird species is their annual migration in V-shaped or echelon formation. When birds are flying in these formations, energy savings can be achieved by using the aerodynamic up-wash produced by the preceding bird. As the leading bird in a formation cannot profit from this up-wash, a social dilemma arises around the question of who is going to fly in front? To investigate how this dilemma is solved, we studied the flight behavior of a flock of juvenile Northern bald ibis (Geronticus eremita) during a human-guided autumn migration. We could show that the amount of time a bird is leading a formation is strongly correlated with the time it can itself profit from flying in the wake of another bird. On the dyadic level, birds match the time they spend in the wake of each other by frequent pairwise switches of the leading position. Taken together, these results suggest that bald ibis cooperate by directly taking turns in leading a formation. On the proximate level, we propose that it is mainly the high number of iterations and the immediacy of reciprocation opportunities that favor direct reciprocation. Finally, we found evidence that the animals' propensity to reciprocate in leading has a substantial influence on the size and cohesion of the flight formations.

Footnotes

↵¹To whom correspondence should be addressed. Email: bernhard.voelkl{at}zoo.ox.ac.uk.
↵²Present address: School of Biological Sciences, Royal Holloway, University of London, Surrey TW20 0EX, United Kingdom.

Author contributions: B.V., A.M.W., and J.F. designed research; B.V., S.J.P., M.U., and J.F. performed research; B.V. and S.J.P. analyzed data; and B.V., S.J.P., M.U., J.R.U., A.M.W., and J.F. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: Complete raw data are provided as Dataset S1.
*As it is possible that the frequency of bout-switches changes in the course of the migration due to experience, energetic demands, or varying weather and flight conditions, we cannot give a more precise estimate.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1413589112/-/DCSupplemental.

Freely available online through the PNAS open access option.