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Schooling, dusk flight and dance: social organisations as amplifiersof indi7idual quality?

Iain Barber, Fish Biology Group, Inst. of Biomedical and Life Sciences, Uni7. of Glasgow, Glasgow, UK G12 8QQ(ibarber@udcf.gla.ac.uk) and I7ar Folstad, Inst. of Biology, Uni7. of Tromsø, Tromsø, Norway.

One striking aspect of certain types of animal assemblages, forexample fish schools or bird flocks, is the level of synchrony andspatial regularity that group members achieve. Although theevolutionary mechanisms leading to the formation of animalaggregations appear to be understood reasonably well, the evolu-tion of spatial regularity and the high levels of synchrony thattypify the groups in which certain animals move are less clear.Traditional explanations have generally focused on benefitsgained during interspecific interactions, particularly the improve-ment of antipredator responses, or have suggested aero- orhydrodynamic advantages during locomotion. However, since thelatter benefits of structural regularity may be largely rejected ontheoretical grounds, and because many examples of spatiallyregular, synchronous groupings – such as dusk-flying flocks ofsome birds – may occur in the absence of predators, we suggestthat these behaviours may not be explained solely in terms oflocomotory efficiency or performance in predator-prey interac-tions. Instead, we suggest that the maintenance of regular spatialpositions and the level of synchrony achieved within certainsocial groups may reveal honest information about an individu-al’s neurosensory or locomotory performance, and that thesebehaviours may have evolved as amplifiers of individual quality.The evolution of such behaviour therefore need not have occurredas a result of interspecific interactions, but could have happenedin the arena of conspecific evaluation.

The term amplifier, coined by Hasson (1989), has beenused to describe traits that are reliable because theirdesign improves the receiver’s perception of the sig-naller’s underlying quality. In contrast to traits likehandicaps, which are reliable because of costly trade-offs (Zahavi and Zahavi 1997), amplifiers have nocosts. An example may illustrate the difference: antlersize in cervids may be a signal of an individual’s surplusof calcium and potassium and, as these raw materialsare scarce minerals in the cervid’s ecosystem, antler sizemay be a costly handicap. However, for a given antlersize it need not be more costly, in terms of scarceresources, to produce a symmetric rather than an asym-

metric antler, only more ‘difficult’. As antler symmetrymay be influenced by an individual’s developmentalstability, it may improve a receiver’s perception of asignaller’s quality without costs to the latter (Lagesenand Folstad 1998). Antler symmetry could thus beregarded as an amplifier whereas antler size could beconsidered a handicap (see also Hasson 1991, 1997).

Amplifiers have usually been thought of as morpho-logical traits, but they can also be behavioural traits.For example, tail fanning as a behavioural courtshipritual among males in several species of birds may easea female’s evaluation of feather quality. This behaviourmay have evolved because high quality males had negli-gible costs of showing their good feather quality,thereby enforcing the behavioural dictate upon lowquality males with damaged feathers (Hasson 1991).Moreover, some forms of behavioural interaction mayhave evolved as cultural institutions for amplifyingdifferences between high and low quality individuals.The driving force in the formation and evolution ofthese entities are high quality individuals which, byinitiating (or ‘setting the stage’ for) these forms ofinteractions make it easier for evaluators to distinguishhigh from low quality individuals.

Ordered aggregations as amplifiers

Social organisations may take the form of highly syn-chronised dynamic groups, such as fish schools, birdflocks, song choruses or dance assemblages, which arecharacterised by the incorporation of individuals intorecognisable spatial and/or synchronously moving pat-terns. The ability to adopt and maintain accurate posi-tions within such spatially regular groups and perform

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synchronous movements with respect to other groupmembers, may demand a minimum threshold level ofbehavioural ability, or ‘finesse’, for spatio-temporal ad-justment, but need not be any more energetically costlythan occupying of incorrect positions. Because thisbehavioural finesse may be reduced by, for example,morphological defects caused by disease, injury or de-velopmental instability, an individual’s participationand performance in such groups potentially providesinformation regarding aspects of its quality. Such infor-mation could, of course, be used by heterospecificextra-group spectators to assess individual quality, butcould also be used by conspecific group members andconspecific extra-group spectators. Under this scenario,the signal conveyed by an individual’s ability for spatio-temporal adjustment would be a reliable indicator ofquality, but not because of differential costs to high andlow quality individuals during signalling. Instead, itwould be reliable because of individual differences inthe ability to incorporate into a spatio-temporal design,and would therefore have evolved as an amplifier (Has-son 1997), rather than as a handicap (Zahavi andZahavi 1997).

Behavioural, positional and synchronal odditywithin ordered groups

The term oddity has been used to describe the extent towhich individuals within groups differ from othergroup members, and usually applies to a discrepancybetween the size, or some other visible morphologicalcharacter such as colour or pattern, of the focal individ-ual and the rest of the group (e.g. Landeau and Ter-borgh 1986). The adoption of visibly differentbehaviours is another way in which individuals maydiffer, or be ‘odd’, within groups. In addition, the term‘spatial oddity’ has been used to describe lone individu-als that take up positions close to, but not within,groups (e.g. Milinski 1977). Individual spatial odditymay be accentuated in groups that are structurallyregular and need not relate solely to satellite individualsoutside groups. Individuals that take up deviant posi-tions within ordered, cohesive groups may be conspicu-ous because they do not conform to the regular patternor background created by other group members. Theymay therefore be described as exhibiting ‘positionaloddity’. Since spatial regularity probably facilitates syn-chrony within dynamic groups, individuals that assumeinaccurate positions are also likely to be unable tomatch the movements of the other regularly spacedgroup members, and positional oddity may translateinto ‘synchronal oddity’ during group manoeuvres.Synchronal oddity may further be accentuated by mor-phological traits like reflective body surfaces in fish,wing bands in birds and pelt coloration in mammals

(e.g. zebra stripes). These morphological charactersmay again have evolved as amplifiers of an individual’sability to perform behavioural synchrony.

Individuals may benefit from gaining informationabout the quality of their interactors (Hauser 1997).This is particularly evident in interspecific interactions,such as those between evaluating predators and theirprey. However, although high levels of spatial regular-ity and synchrony observed in such groups are impor-tant in predator-prey interactions, synchronised,spatially ordered organisations also occur in the ab-sence of heterospecific predators, suggesting that suchself-assemblages may also have importance for in-traspecific communication of individual quality. Suchinformation may be of importance when individuals areselecting mates or co-operators (as, for example, part-ners in predator inspection). Recently demonstrationsthat vertebrates have the ability to recognise familiarindividuals and that such recognition persists over time(Brown and Smith 1994, Griffiths and Magurran 1997,Smith 1997) means that it is conceivable that informa-tion gained from earlier experiences could be applied tocurrent relevant decisions. The fact that very largeaggregations (such as some oceanic fish schools) tend tobe composed of considerably smaller, cohesive sub-units (Pitcher and Parrish 1993: 369) probably facili-tates the development of individual-level recognition.Thus, predators do not need to be implicated in theevolution of synchrony and order within groups if suchability of individuals imparts useful information toconspecifics.

Fish schools – an example

Fish schools are dynamic swimming groups, distin-guishable from simple aggregations (‘shoals’) by theirhigh levels of structural regularity, polarity and syn-chrony (Pitcher 1983). The most commonly postulatedbenefit of synchrony and spatial order within schools,over and above those gained through simple shoaling,is the improved antipredator responses of the schoolresulting from increased predator confusion (Magurran1990, Pitcher and Parrish 1993). It is now thought thatpositive hydrodynamic advantages, once thought of asa major force in driving the evolution of synchrony andspatial organisation within fish schools, are unlikely toexist (Partridge and Pitcher 1979, Pitcher and Parrish1993).

The rapid, almost instantaneous adjustments toswimming direction and speed made whilst schoolingare made possible by detection, via the acoustico-later-alis system, of local water pressure changes resultingfrom the movements of adjacent fish (Gray and Denton1991) and may be facilitated by the silvery reflectivesurfaces typical of many schooling fish species (Rowe

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and Denton 1997). The occupancy of precise spatialpositions within schools that allow the detection ofboth pressure changes and visual cues from ‘flashing’neighbours is therefore likely to be an important pre-requisite for synchronised schooling behaviour infishes.

If the functioning of the sensory, motor or nervoussystems that allow fish to maintain accurate positionswithin schools varies between individuals dependingon some aspect of their condition, then the ability toparticipate, or the level of performance, in group ma-noeuvres is also likely to reflect individual quality.This idea is supported by experimental data. Individ-ual European minnows (Phoxinus phoxinus) infectedwith plerocercoids of the pseudophyllidean cestodeLigula intestinalis take up deviant spatial positions inschools of size-matched uninfected conspecifics, withinfected fish exhibiting significantly greater nearest-neighbour distances than uninfected school members(Barber and Huntingford 1996). The discrepancy inthe spatial positioning of infected school members,compared to uninfected fish, increases as schools be-come more dispersed, and following a simulated avianattack, infected fish do not reduce their nearest-neigh-bour distance (a typical response of schooling fish toa perceived predatory threat) as far as uninfected fish.The mechanism impairing schooling behaviour in in-fected minnows is unclear, but it is possible that theabdominal swelling associated with infection may in-terfere with the efficient functioning of the lateralissystem, which appears to be an important prerequisiteto ordered schooling. This has been demonstrated inmackerel (Scomber scombrus) which, when deprivedof their lateral line function, are unable to maintainregular spatial positions in schools (Partridge andPitcher 1980).

Presumably as a result of strict constraints imposedby the streamlined body plan and life in the openwater habitat, schooling oceanic species typically haveno sexually dimorphic ornamentation on which asses-sors may evaluate quality. The positions that individ-uals take up within the school, and their performanceduring group manoeuvres, may therefore be especiallyimportant indicators of quality in these species. Anymalfunctioning of sensory or motor systems could re-sult in individuals being unable to position themselvesaccurately within otherwise ordered groups, or partici-pate effectively in synchronous manoeuvres. Thus, in-teractors may gain honest information about anindividual’s infection status, or other aspect of qual-ity, from its schooling behaviour. Carefully controlledexperiments could be used to test our main predic-tion, namely that performance in synchronised socialbehaviour determines subsequent desirability as matesor as predator inspecting partners.

General considerations

Striking levels of spatial regularity and synchrony arenot only restricted to fish schools. Flocks of birds,ungulate herds and humans may all perform remark-able displays of synchronisation. Potts (1984) describeshow synchronous turns, initiated by a small number ofindividuals in flocks of dunlin (Calidris alpina), arepropagated through the flock at three times the rateexpected if signal transfer was solely based on visualcues. Birds initiating turns – which may be those of thehighest quality – therefore enforce the manoeuvre on‘followers’, which then attempt to move in synchronyand potentially reveal honestly their own quality.Moreover, social rules of etiquette and acceptable be-haviour in all human societies dictate how individualsshould behave in certain social circumstances. An indi-vidual’s particular behaviour under such circumstancesmay honestly reveal certain facets of their quality, anddeviations from these acceptable patterns of behaviourmay be expected to be associated with certain individ-ual conditions. Although participation within these as-semblages, which may be imagined along a continuumfrom formal social gatherings (such as cocktail parties)to dancing, may have a cost in terms of energy or otherresources, the adoption of correct behaviour patternswithin them may reveal honest information about theactor’s quality without being costly. For example, someforms of dancing may demand precise timing and co-ordination, but variation in the specific quality of thedance itself need not always be linked with variation inenergetic cost (e.g. Argentinian tango versus swing).However, the individual ability to adapt to the be-havioural design of the dance may still reveal individualqualities, such as a well-functioning nervous system,motor control or sensory capability. The behaviouralconformity is therefore probably not a handicap, sinceit has no cost. However, since only individuals above athreshold level of quality can conduct the necessarybehavioural adjustments, the ability to conform wouldbe an honest signal. In such cases high quality individu-als that impose a social dictate – the dance – on otherindividuals, set the stage.

Low initial costs to individuals dictating behaviouralpatterns could facilitate the evolution of social confor-mity, and generate spatial and synchronous regularityas a background against which individual quality isclearly shown. Imagine the effect of a few high qualityindividuals engaging in socially or spatially orderedactivities within eyesight of numerous conspecifics.From this point it is not necessary to invoke a highlevel of consciousness to explain the spread of thebehaviour, only an ability for individual recognition.Recognising odd individuals may be difficult for ahuman watching dusk flight in starlings (Sturnus 6ul-garis), but it is probably not difficult for a mate search-ing female starling. And if she only needs to identify

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whether or not an individual participates to assessquality, then the process becomes even more straight-forward.

Acknowledgements – We would like to thank Frode Skarstein(who has never been seen dancing) for valuable comments andOren Hasson for his stimulating ideas. IB thanks the FisheriesSociety of the British Isles for a travel grant to visit Tromsø.IB was in receipt of a Swedish Royal Academy of Sciences/Munkedals Research Fellowship and a TMR-Large Scale Fa-cility award, both held at the Kristineberg Marine ResearchStation, Sweden, during the writing of the paper.

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