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Richard Wagner’s fascination withthe natural world goes back as faras he can remember. As a childgrowing up in Long Island, USA hestarted by collecting insects in hisback garden and by the age of tenhe had acquired his first petsnake. His unusually tolerantparents encouraged his hobbyand in his teens his snakecollection reached a peak ofseven (augmented by manylizards, turtles and so on, allhoused in terrariums he builthimself). His great idol at the timewas Raymond Ditmars, who as ayouth had a collection of over 100snakes in his home and went on tobecome the founding father ofAmerican herpetology. Wagnersecretly nursed the ambition tolook after a similar collection. Atthe age of 19, however, he finallygrew tired of the jibes from hisbirdwatching friends, who pointedout (correctly) that, while he spentmost of his time looking forsnakes rather than watching them,they could find birds whereverthey went. He thus switched thefocus of his attentions to birds.

A college summer trip to Israelintroduced Wagner to deserts. Theresult was a revelation. “It waswonderful: for the first time in mylife I saw how easy it is to watchanimals in open habitats.” Hedecided to interrupt hisundergraduate studies and spendsome time in Israel. There he wasoffered a job as field assistant toAmotz Zahavi, who was studyingthe breeding system of the Arabianbabbler Turdoides squamiceps.Under Zahavi’s supervision,Wagner learned the importance ofcareful observations of behaviourand grew to appreciate thesubtleties of birds’ interactionswith one another.

A chance event in Israel (onemorning he found and caught a

huge horned viper Cerastescornutus) brought him to theattention of Ariel Ulmann, whowas in charge of the reptilecollection at Haifa Zoo. WhenUlmann was drafted into theIsraeli army, he insisted thatWagner be appointed to take careof the Haifa snakes. Thus it wasthat – for six months at least –Wagner achieved his ambition oflooking after as many snakes asDitmars.

Work on further behaviouralprojects followed: on the commontern Sterna hirundo on LongIsland, on the white-fronted bee-eater Merops bullockoides inKenya and on the acornwoodpecker Melanerpesformicivorus in New Mexico, USA.Wagner’s field experience wasgrowing rapidly but he wasstarting to become frustrated atworking on other people’sprojects rather than his own. Herealized that a PhD would helphim in obtaining funding forindependent research, so took upa doctoral position at OxfordUniversity under ChristopherPerrins.

His work focussed on therazorbill Alca torda, a coloniallybreeding seabird, and addressedthe particular issue of why thespecies elected to breed incolonies. Razorbills were knownto lay their eggs under boulders oron small ledges, so their coloniesare much smaller and looser thanthose of several closely relatedspecies. During his intensive fieldobservations Wagner noticed thatextra-pair copulations, neverpreviously recorded in thespecies, were very common.Intriguingly, these took place notat the nest sites but on large,open ledges away from thenesting territories. It seemed thatmale razorbills congregated on

such ledges, which were visitedby females for the explicit purposeof securing extra-pair copulations.

This finding was extremelysignificant. Extra-pair copulationswere known from many speciesbut it was generally assumed thatthese were forced upon unwillingfemales by males who hoped tofather more offspring. Recentworks from other groups hadshown that competition forfertilization — and thus paternity— can take place after copulation,adding an important mode ofsexual selection to that ofmale–male competition describedby Darwin. Wagner’sdemonstration that femaleschoose to visit the ‘mating arenas’proved that they are activelypursuing matings with multiplemales and suggested for the firsttime that females are far more incontrol of mating than had beensupposed.

These serendipitousobservations had very importantconsequences for Wagner’ssubsequent career. Wagner notes,“We started out trying to studycoloniality, got distracted bysomething we noticed and endedup being led back to coloniality.”Before Wagner’s work onrazorbills, the accepted theory toaccount for social behaviour incolonial species of animals andbirds was that certain behaviourpatterns were a consequence ofthe need to breed in colonies. Theaggregation of male razorbills onledges, however, may arisebecause females visit the ledgesfor extra-pair matings. Razorbillstherefore show a type of socialbehaviour that is distinct from theircolonial breeding. The situation isanalogous to a ‘lek’, or displayground, where males ofpromiscuous species congregateto display to females, who visit leksto select from potential mates.Leks are widely used in the animalkingdom, not only by birds such asgrouse but also by animals asdiverse as flies, fish and antelopes.Wagner speculated that colonies in

Features

Insights into the mating gamesA paper published earlier this year in Proceedings of the Royal Societyhas caught the attention of science journalists throughout Europe. Thepaper’s author, Richard H. Wagner, describes to Graham Tebb how aninterest in snakes led to a study of colonial breeding in birds and tofundamental insights into female control of sexual behaviour.

other species might form aroundplaces that females visit for thepurpose of mating. According tothis notion, protection frompredation and increased food-finding abilities are by-products ofcolony formation rather thanreasons for it. Wagner’s work onrazorbills had shown that‘monogamous’ species can showsome of the behavioural traitsthought to be peculiar topromiscuous species. Themechanisms that produceaggregations of displaying males inpromiscuous species maytherefore act to produce coloniesin monogamous species whenfemales pursue matings withmultiple males. Wagner termed thisiconoclastic idea the ‘hidden lekhypothesis’ and it has been hotlydebated in the literature ever since.

Following completion of hisdoctorate, Wagner returned to theUS and spent three years withEugene Morton at the SmithsonianInstitute studying the breeding ofthe purple martin Progne subis.These birds breed in colonies in‘martin houses’, which are easilyaccessible and thus offer readymaterial for genetic analysis. DNAfingerprinting studies had shownthat older males in the coloniesfather almost all offspring, withyoung males being cuckolded to avery large extent. An obviousquestion was why young males,which return to the breedingterritories significantly later thanolder males, should choose tosettle near older males and run the(high) risk of helping to raiseoffspring that they have notfathered.

Wagner showed that femalebirds choose to take up residencenear old males, so young malesare forced to settle nearby to haveany chance of obtaining mates.Once again, then, it is the femalesthat are in control of extra-paircopulations. And once again acolonially breeding species hadbeen shown to operate a kind of‘hidden lek’: colonies form aroundplaces that females visit formating.

Wagner’s next position was atYork University in Toronto. Whilethere his work came to theattention of Etienne Danchin atthe CNRS in Paris. Danchin hadbeen studying the kittiwake Rissatridactyla, a colonially breedingseabird, in France for over fifteenyears in the hope of coming upwith a generally applicable theoryto account for colony formation.He had suggested that animalscopy the habitat choices taken bysuccessful conspecifics, thusproducing colonies. His theory,though, did not seem fully able toaccount for the behaviour heobserved: something wasmissing. As Wagner says, “Habitatselection isn’t everything and —alas — sex isn’t everythingeither.”

Danchin and Wagner decided tocombine their ideas and thusbegan a cooperation that hascontinued to the present day.After his initial surprise (“Whyshould the French have to importan American to help them thinkabout sex?”) Wagner realized thebenefits of collaboration, as bothhe and Danchin believed thatcolonies resulted from otheraspects of behaviour rather thanbeing ends in themselves. Theyfelt that colony formation shouldbe seen as the result of selectionfor ‘commodities’, both habitat(Danchin) and partners (Wagner).According to this notion,attempting to identify possiblebenefits of coloniality would nothelp explain how or why coloniesare formed.

In 2000, after six years at YorkUniversity, Wagner was offeredthe position of senior scientist atthe Austrian Academy ofSciences’ Konrad Lorenz Institutefor Comparative Behaviour(KLIVV) in Vienna, Austria. His

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Richard Wagner: Careful observation of colonial breeding birds has producedrevealing insights into female behaviour.

connections with this institute goback to 1993, when he was invitedto give a talk at a symposium onfemale control of paternity, and hehad cooperated loosely with staffat the institute ever since. He hadno hesitation in accepting theoffer: as he says, “KLIVV is a topinstitute specializing inbehavioural ecology and myposition gives me independenceand allows me to attract third-party funding to build up myresearch programme.” Althoughthe institute itself may appearsomewhat isolated, all of the staffhave good internationalconnections. Wagner has receiveda research grant to study thebreeding of lapwing Vanellusvanellus in Sweden and hascontinued and intensified hiscooperation with Danchin. Awelcome by-product of hisfieldwork in France was a meetingwith his girlfriend Nelly, whorecently moved to Austria.

Meanwhile, his study ofcommodity selection in kittiwakeshas continued. Wagner still relieslargely on close observation inthe field. He feels strongly thatthe area of behavioural ecologyhas been tending to move in thewrong direction. In his words,“The problem is that people nolonger spend enough timewatching behaviour but relyinstead on indirect information,e.g. from DNA studies, which theyhope will tell them what hashappened. Genetics andphysiology are clearly importantbut there are some things thatyou can only learn by watching.”While watching kittiwakes,Wagner happened to notice thatfemales frequently eject thesperm of their mates aftercopulation. Sperm ejection hadpreviously been recorded inseveral other species but thekittiwake differs from all of thesein that it is strictly monogamous.The explanation seems to be thatthe females do not wish to storesperm in their bodies, as eggsfertilized with ‘old’ sperm aremore subject to hatching failureand the chicks that result areoften in poor condition. Femalekittiwakes are thus activelyselecting the quality of spermbased on its age rather than on

any properties of the donor male.The findings represent the firstexample of intra-male spermselection and demonstrate furtherthat females — at least in birds —are far more in control offertilization of their eggs thangenerally believed.

In twenty years of “watchingcopulations”, Wagner has madeseveral highly significantcontributions to ourunderstanding of colonialbreeding systems in birds. Hehopes now to assess whether themechanisms he has uncoveredare generally applicable across

different taxons and to this endplans to study the formation ofcolonies in fish, using KLIVV’sextensive aquarium facilities toobserve colony formation underpseudo-natural conditions in thelab. He will continue with fieldobservations – on lapwings,kittiwakes and possibly again onpurple martins – as an integralpart of his research. But as headmits, “Even behaviouralecologists should be prepared totest their ideas under controlledconditions sometimes. And somethings really are easier to study inthe lab than in the field.”

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While a growing number ofmodelling studies attempt toaddress the potential impacts ofglobal warming on a variety ofspecies, scenarios are necessarilyspeculative given the complexinteraction of many factors overand above changes in averagetemperatures. What is becomingincreasingly valuable is historicaldata that can be used to analysechanges in species abundance inpast years, that may be linked towell-documented changes intemperatures in many regions.

There are two main hypothesesconcerning how populations andtherefore communities change inresponse to climate. Onesuggests that changes in speciesdistributions and abundancedepend on the physiology ofindividuals. Under this scenario,changing climate should directlyinfluence survivorship, dispersal,fecundity and behaviour ofindividuals, and these will directlytransfer to species-level changesin abundance and distribution. Analternative viewpoint suggeststhat interspecific interactions maybe important under climatechange and will cascade throughto population and community levelresponses, both directly andindirectly. Under this scenario itmight be expected that differentpopulations of a particular species

might have different outcomesunder warming events.

A new paper reports resultsfrom two surveys of marineenvironments that are separatedbut have undergone the sameclimate fluctuations over the pastcentury. One is based on a regulartrawl of the English Channel thatbegan in 1913, and the other, ananalysis of species recoveredsince 1981 at the filter for coolingwater to a nuclear power station inthe Bristol Channel, around 350kms away.

The species data have beencompared with sea-surfacetemperatures calculated as meanmonthly temperatures for units of1 degree of longitude and 1degree of latitude since 1870.Both regions have been subject toclimatic shifts with mean annualsea-surface temperaturefluctuating within a range of 1.8oC— trends that are consistent withlarger-scale patterns intemperatures in the northernhemisphere over the past century,namely a warming in the 1950sand in the 1990s to the presentday, following relatively coolperiods in the early 1900s and1970s.

The results suggest that theinfluence of temperature changesmay have a more dramatic effecton the structure of marine

The heat is onResearchers tackling the potential impact of global warming on speciesaround the world may need to look more carefully at the situation of eachpopulation. Nigel Williams reports.