heterogeneous structure in mixed-species corvid flocks in ... · and jackdaws are an ideal system...

Problem: Studies of collective behaviour seldom consider the impact of heterogeneity on collective behaviour and fail to account for individual characteristics and social relationships among group members

Objective: To investigate how heterogeneity (specifically species differences and social relationships) can affect flock structure and dynamics. Mixed-corvid flocks of rooks and jackdaws are an ideal system to investigate this as (1) they spent a large portion of the year together in large groups; (2) both species’ social system centres around long-term monogamous pair bonds; (3) rooks are larger and often dominant in foraging interactions and access to roosting sites.

Figure 1. (a) Proportion of rooks in the front, middle and back of flocks. The horizontal line indicates the average proportion of rooks across all flocks. (b) Relationship between flock size and neighbour distances.

Positional Differences by Species

Rooks made up only 21.8 ! 0.03% of flocks on average, but weredisproportionately likely to be positioned at the front of flocks(Fig. 1a, Appendix Table A2). The first bird at the leading edge wasa rook in 19 out of 44 flocks (¼ 43.2%), more than twice as often asexpected by chance (binomial test: P ¼ 0.001). Species distributionswithin flocks were not significantly affected by flock size, month ortime to sunset (Appendix Table A2).

Proximity and Alignment between Neighbours

Neighbours flew more closely together in larger flocks (Fig. 1b,Appendix Table A3) and in the middle of flocks relative to the frontand back (Fig. 1c, Appendix Table A3). Jackdaw dyads flew sig-nificantly closer together than rook dyads or mixed dyads (Fig. 2a,Appendix Table A3), and the directional alignment of same-speciesdyads was greater than that of mixed dyads (Fig. 2b, AppendixTable A4).

Do Birds Fly in Discrete Dyads?

An average of 41 ! 5% of jackdaws (range 22e63%) and 46 ! 4%(range 37e67%) of rooks in the illustrative selection of photographs

flew in clearly identifiable, discrete dyads (Fig. 2c, Table 1). Histo-grams of neighbour distances commonly showed a bimodal char-acter with a peak before the average nearest-neighbour distance foreach species (Figure A2), suggestive of discrete dyads of birds flyingin close proximity.

DISCUSSION

Contrary to the assumptions of many mathematical models ofsingle-species aggregations, which treat individuals as equivalentand interchangeable, our results suggest that the structure ofmixed-species flocks may be critically influenced by species dif-ferences and social systems. The larger and socially dominantrooks were disproportionately likely to be located in the front offlocks. This effect is unlikely to result from the influence of par-ticular individual rooks, as our data set contained photographs ofnumerous flocks of differing size, but rather seems to representa general property of mixed rookejackdaw flocks. Nor is thepattern readily explicable by species differences in flight velocityas rooks tend to be found towards the front of flocks despiteobservational evidence suggesting that jackdaws can fly faster(Coombs 1961). Previous work on fish schools (Krause et al.2000), zebra herds (Fischhoff et al. 2007) and small pigeonflocks (Nagy et al. 2010) suggests that individuals located at the

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Figure 1. (a) Proportion of rooks in the front, middle and back of flocks. The horizontal line indicates the average proportion of rooks across all flocks. (b) Relationship between flocksize and neighbour distances. (c) Distance between neighbours in the front, middle and back of flocks. Bars show means ! SE. Asterisks indicate significance levels betweencategories in post hoc analyses: *P < 0.05; **P < 0.001.

J. W. Jolles et al. / Animal Behaviour xxx (2013) 1e84

Please cite this article in press as: Jolles, J. W., et al., Heterogeneous structure in mixed-species corvid flocks in flight, Animal Behaviour (2013),http://dx.doi.org/10.1016/j.anbehav.2013.01.015








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Heterogeneous structure in mixed-species corvid flocks in flight

Jolle W. Jollesa, Andrew J. Kingb, Andrea Manicaa , Alex Thorntonc a Department of Zoology, University of Cambridge, Cambridge, UK; b College of Science, Swansea University,

Swansea, UK; c Centre for Ecology and Conservation, University of Exeter, Penryn, UK

Background: Flocks of birds in flight represent a striking example of collective behaviour. Models of self-organization suggest that repeated interactions among individuals following simple rules can generate the complex patterns and coordinated movements exhibited by flocks. Such models are often based on the assumption that individuals are identical and interchangeable. However, group members often mix associatively according to a variety of morphological and physiological factors such as sex and size as well as species’ social systems.

Models of self-organisation propose the simple rules of attraction, short-range repulsion and alignment among neighbours determine collective behaviour. We show that these simple rules were affected by the size of and position within flocks, the relationships between group members and birds’ distribution across flocks. Birds typically flew near conspecifics and in discrete dyads which may potentially reflect the monogamous pair-bonds in both species; rooks may have a dominant influence on the collective movements of the flocks. Thus, characteristics of individuals and their social systems likely result in preferential associations that critically influence flock structure. Future studies must consider the modulating effect of heterogeneity on the simple rules individuals use in collective movements.

This work is published in the journal Animal Behaviour: Jolles, Jolle W., King, A.J., Manica, A., Thornton, A. (2013) Heterogeneous structure in mixed-‐species corvid flocks in flight. Animal Behaviour. Published online 1 March 2013

Beauchamp, G. 2012. Animal Behaviour 83, 1125-1129; Conradt, L. & Roper, T. J. 2005. Trends in Ecology & Evolution 20, 449-456; Coombs, C. J. F. 1961. Bird Study 8, 55-70; Couzin, I. D. & Krause, J. 2003. Advances in the Study of Behavior 32, 1-75; Krause, J. & Ruxton, G. D. 2002. Oxford: Oxford University Press; Sumpter, D. J. T. 2006. Philosophical Transactions of the Royal Society B 361, 5-22; Vicsek, T. & Zafeiris, A. 2012. Physics Reports 517, 71-140.

Flock analyses based on photos of mixed-species corvid flocks What: front, middle and back thirds of corvid flocks (see picture ) How: Canon EOS 7D with Canon EF 100-400mm f/4.5-5.6 L IS lens (8fps) When: sunset ± 45min between 19 Oct 2011 - 8 Feb 2012 Where: in and around the village of Madingley, Cambridgeshire Photo selection: 115/1211 photos of 44 flocks (no duplicates, flock < 20 birds)

Analysis •  Species identification >95% certainty •  Randomly 4 focal birds selected in each flock section •  Determined species of focal and 7 nearest neighbours •  Measured distance to and relative alignment with neighbours

expected to emerge from morphological or aerodynam

ic con-

straints alone and is likely to result from social partners flying

together, although further studies with identifiableindividuals

would be needed to confirm this. Second, the alignment of neig

h-

bours was significantly higher if they were of the same species,

with jackdaw dyads showing near perfect parallel alignment

(a mean differenceof only 3.8!). Both species form lifelong,

monogamous pair bonds characteriz

ed by high levels of affiliative

behaviourand close proximity (Emery et al. 2007)

, and our results

suggest thepossibility

that these relationship

s are reflected in flock

structure.

Together, our results s

uggest thatthe theoret

ical convenience of

treating group members as identical and interchang

eable does not

adequatelyreflect biolo

gical realityin mixed-specie

s flocks. Indeed,

wewould argue thatthis assumption is similarly unlikely to

hold in

single-species flocks in which individuals

vary and have social

relationships. Differences

between individualscan give rise to

leadershiproles, which may be particularly

pronounced in mixed-

species aggregations in which larger and more dominant speci

es

may commonly take the lead (King et al. 2009). Moreover, stu

dies

of both single-species and mixed-specie

s flocks must consider how

the relationships between individuals

may modulate the degree of

attraction,separation

and alignment between group members.

Thus, flockstructure cannot be fully understood

without taking

species’ characteristic

s, their social systems and individuals’ re-

lationshipsinto account. Fu

ture work incorporating information on

themovements of known individuals

will provide further empirical

data that can be integratedinto mathematical models to better

understandthe influences

of within-groupheterogene

ity on col-

lective movements.

Acknowledgments

We thank Neeltje Boogert forher friends

hip, help and valuable

comments. Thiswork was funded by a British Ecological

Society

grant and a BBSRC David Phillips Fellowship to A.T. (BB/H0

21817/1).

A.J.K was supported by a NERC Fellowship.

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Appendix

Coefficientestimates in all tables represent t

he change in the

dependentvariable relative to the baseline category and can thus

be interpretedas measures of

effect size.

Figure A1. Map of Madingley and surroundings. Photogr

aphs were taken within the

large shaded area. To avoid pseudoreplication, photograph

s taken within a given

evening were shot from different locations within this area. The hatched area shows

the roost, where flocks would combine into a single large flock and spend the night.

J. W. Jolles et al. / Animal Behaviou

r xxx (2013) 1e8

6

Please cite this articlein press as: Jo

lles, J. W., et al., Heterogeneous s

tructure in mixed-species corvid flocks in flight, Anim

al Behaviour (2013),

http://dx.doi.org/10.101

6/j.anbehav.2013.01.015

Introduction

Material & Methods

Figure 3. (left) Alignment between neighbours in jackdaw, rook and mixed dyads. (right) Distance between neighbours in the front, middle and back of flocks. Bars show means ± SE.

front of groups tend to assume leadership roles, initiatingchanges in direction or pace of movement that are followed bygroup members. Similarly, rooks may play a dominant role ininfluencing collective movements of mixed-species corvid flocks.It is possible that rooks’ preference for the front of flocks maysimply reflect their motivation to reach the roost first and obtainfavoured positions (Coombs 1961). If this was the case, one mightexpect rooks to move to the front as sunset approaches, but wefound no such effect. Moreover, roosting flocks form spectacular,swirling displays similar to starling murmurations (King &Sumpter 2012) before settling, so individuals at the front ofpreroosting flocks may not necessarily land first at the roost.

Thus, it remains unclear whether rooks derive benefits frompositioning themselves towards the front of flocks, whether jack-daws preferentially follow rooks or whether species’ relative posi-tions reflect aerodynamic considerations Futurework incorporatingGPS technology to track flock members (Nagy et al. 2010) couldassist in discriminating between these possibilities.

The general rules of attraction, short-range repulsion andalignment among neighbours proposed by models of self-organization provide a valuable framework for understandingflocking (Bajec & Heppner 2009; Petit & Bon 2010), but our resultsindicate that their specific manifestations may be influenced by thecharacteristics of social systems. Our measurements of neighbourdistances and alignments are somewhat crude and, given the noisein the data, they are likely to underestimate the true extent ofspatial structure within flocks. Nevertheless, a number of impor-tant patterns were apparent. First, the extent of attraction andrepulsion may vary depending on the position within a flock, thesize of the flock (see Beauchamp 2012 for similar results in semi-palmated sandpipers, Calidris pusilla) and the relationships be-tween group members. Critically, corvids were not evenlydistributed across the flock but typically flew near conspecifics,with jackdaws being particularly closely attracted to same-speciesneighbours, and birds of both species often appeared to fly in dis-crete dyads. The occurrence of discrete dyads of birds would not be

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Figure 2. (a) Distance and (b) alignment between neighbours in jackdaw, rook and mixed dyads. Bars show means ! SE. Asterisks indicate significance levels between categories inpost hoc analyses: **P < 0.001. (c) Jackdaws flying in clearly identifiable, discrete dyads.

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Please cite this article in press as: Jolles, J. W., et al., Heterogeneous structure in mixed-species corvid flocks in flight, Animal Behaviour (2013),http://dx.doi.org/10.1016/j.anbehav.2013.01.015Selected literature

Results

Discussion

Back Middle Front

Spectacular collective behaviour can be found in a large range of animal

species. Our research highlights that heterogeneity plays an important

role in these striking displays of group behaviour.

“

” Jolle Jolles

Figure 2. Jackdaws flying in clearly identifiable, discrete dyads.

Birds were closer together in larger flocks (p=0.02; Fig. 1b) and in the middle of flocks (p<0.001; Fig 3R), which did not affect the species distribution within flocks (p=0.28).

1

Rooks were were more likely to be at the front (Fig. 1a) and leading edge of the flock (both: p<0.001).

2

Birds preferentially associated with same species neighbours (p<0.001) and birds were often observed to fly in same-species dyads (Fig 2).

3

Same-species neighbours were more aligned than mixed-species dyads (p<0.001; Fig. 3L).

4

heterogeneous structure in mixed-species corvid flocks in ... · and jackdaws are an ideal system...

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