July1999] ShortCommunications 847

tics,version 6.12. SAS Institute Inc., Cary, North sonal patternsof time and energy allocationby Carolina. .Physiological Zoology 66:511-536. SEARLE,S. R. 1971. Linear models.John Wiley and WEBSTER,g. D., AND W. W. WEATHERS.1989. Vali- Sons, New York. dation of single-sampledoubly labeled water WALSBERG, G. E., AND W. W. WEATHERS. 1986. A sim- method.American Journal of PhysiologyR 256: ple techniquefor estimatingoperative environ- 572-576. mentaltemperature. Journal of ThermalBiology WOOD, R. A., K. A. NAGY, $. MACDONALD, $. T. 11:67-72. WAKAKUWA,R. J. BECKMAN,AND H. KAAZ. 1975. WEATHERS, W. W., AND K. A. SULLIVAN. 1989. Juve- Determinationof oxygen-18in water contained in biologicalsamples by chargedparticle acti- nile foraging proficiency,parental effort, and vation.Analytical Chemistry 47:646-650. avian reproductive success.Ecological Mono- graphs59:223-246. Received29 May 1998, accepted27 January1999. WEATHERS, W. W., AND K. A. SULLIVAN. 1993. Sea- AssociateEditor: J. S. Sedinger

The Auk 116(3):847-851, 1999

Confirmation of Infanticide in the Communally Breeding Guira

REGINA H. F. MACEDO 1,3AND CELINE MELO 2 lDepartamentode Zoologia, Universidade de Brast'lia, 70910-900 Brast'lia, DF, ; and 2DepartamentodeBioci•ncias, Curso de Ci•ncias Bioldgicas, Universidade Federal de Uberlgndia, CampusUmuarama, 38405-320 Uberlgndia, MG, Brazil

The killing of conspecificinfants may be common namics.For example,despite the appearanceof so- (Hrdy 1979, Sherman 1981, Hrdy and Hausfater cial monogamy,the Guira Cuckoomating system in- 1984,Parmigiani and VomSaal 1994) but is reported cludespolyandry and polygyny (Quinn et al. 1994). infrequentlybecause the behavioroccurs rapidly. In Additionally,breeding opportunities may be limited several speciesof mammals, infanticide has been becausesome group members are excludedfrom re- linked with mate takeover or cases where a new production.Circumstantial evidence has suggested dominant male comes into contact with infants sired that the killing of newlyhatched chicks is a common by the harem'sprevious male (Hausfateret al. 1982, occurrenceand that high chickmortality probably Sommer1994). In birds,infanticide usually has been resultsfrom infanticideby conspecifics(Macedo and reportedin the contextof siblingrivalry (Mock1984, Bianchi1997b). In this paper,we confirmthat infan- Fujioka 1985, Drummond et al. 1986, Mock and ticide is indeed an important causeof mortality for Forbes1994), althoughevidence suggests that the Guira Cuckoonestlings, and we speculateabout its killing of infantsalso may increasethe perpetrator's function as a reproductivestrategy. fitness by decreasing a competitor's reproductive Methods.--Thestudy was conducted in a suburban successor enhancingaccess to a potentialmate (Trail area of Brasilia, Brazil (15ø47'S,47ø56'W; elevation = et al. 1981,Stephens 1982, Stacey and Edwards1983, 1,158m), from September1995 to March 1996and Fujioka 1986). September1997 to February1998; these periods co- Guira (Guira guira) occur in groupsof as incidewith the rainy seasonin this region.Further many as26 individuals(Gallardo 1984) and are clas- descriptionof the study site and vegetationcan be sifiedby Brown (1987)as plural breederswith joint found in Macedo(1992). Each active nest was visited nests. During reproductive periods, groups are dailyto checkfor neweggs, and the groundbeneath smallerbut still may includeas many as 13 adults. thenesting tree was searched for vestigesof anyeggs Throughoutthe egg-layingand incubationperiods, or chicksnot in the nest.On the first or seconddays eggsare commonlytossed out of the nestby group posthatching,each chick received temporary colored members(Macedo 1992). After chickshatch, group legbands made out of plasticdrinking straws, or col- membersdo not participate equitably in nestling ored dye marks. Continuousperiods of nest obser- feedingor nestguarding (Macedo 1994). DNA anal- vationswere conductedprimarily during the first ysishas shedlight on severalaspects of groupdy- week after chickshatched (the periodwhen nestling disappearanceis mostprevalent). Group sizewas es- E-mail: [email protected] timatedby countingthe adultsaround the nestat 848 ShortCommunications [Auk, Vol. 116

TABLE1. Fatesof eggsand chicksin 15 communalnests of Guira Cuckoosduring two nestingseasons. Rangesare in parentheses.

Variable 1995-96 1996-97 g +_ SD

No. nests monitored 7 8 -- Total eggslaid 65 85 -- Total eggslost 11 41 -- Totaleggs hatched 41 53 -- Total chicks lost 24 30 -- No. eggslaid per nest 9.3 (6 to 13) 10.6 (6 to 21) 10.0 _+3.8 No. eggslost per nesta 1.6 (1 to 4) 1.5 (0 to 9) 1.5 _+2.3 No. eggshatched per nest 6.8 (4 to 12) 6.6 (2 to 10) 6.7 _+2.7 No. nests with chick losses 6 7 -- No. chickslost per nest 4.0 (1 to 7) 3.8 (0 to 7) 3.9 _+2.5 No. observed infanticides 2 4 -- Overall chickslost (%) 58.5 56.6 57.5 Egg lossfrom tossingby cuckoosor disappearancewith causeunknown. eachvisit andduring observation periods; three con- Infanticide3, nestC16.2.--0n 13 November 1995, sistent maximum counts were needed before an es- we observedan adult approachthe nestat 1235,pick timate was consideredadequate. Adult group mem- up a live four-day-oldnestling, and carry it to the berswere capturedand colorbanded whenever pos- groundabout 35 m from the nesttree. It peckedthe sible. nestlingrepeatedly for about1 min andthen left. The Results.--We monitored 15 successfulnests (i.e. at chick was examined immediately afterwards and least one chickhatching) from egg laying until at wasdead, although without visible external wounds. leastthe eighth day after hatching.The numberof Group size at this nestwas five adults. eggslaid per nestin bothyears averaged 10.0 _+ SD Infanticides4 and 5, nestFlbl.--The infanticide of 3.8; egg lossper nest averaged1.5 _+2.3 (Table1). events at this nest occurred on 28 December 1995, Additionally,chicks disappeared from 13 nests(g = when the nestlingswere six daysold. Our evidence 3.9 -+ 2.5), with more than half of the hatchedchicks was circumstantial in one case: we found a dead nes- dyingwithin the first week.Group size averaged 6.4 tling on the ground,about 10 m from the nest,with adults(range 4 to 8) for the sevengroups observed. hematomasaround its eyes.We founda live nestling We observedeight infanticidesduring the studype- on the groundat 1530,but we did not seeit being riod and had circumstantial evidence for an addi- evictedfrom the nest.For about30 min, a groupof tional two cases.Below, we detail these10 cases(nest sevenadults vocalized near the nesttree. Gradually, codingmatches other published work), two of which four of them approachedthe nestlingand peckedit are not includedin Table1 owing to lack of nesting violentlyfor a shortperiod of time.At 1800,when the data (nest Flbl). observationperiod ended, the nestlingwas alive but Infanticide1, nestA8.2.--On 31 October 1995, at motionless.Group size was sevenadults. 1115,an adultwent to the nest,picked up a two-day- Infanticide6, nestB9.1.--At 1025on 2 October1997, old nestlingwith its beak, and flew to the ground an adult went to the nest,picked up a three-day-old some 30 m away from the nest tree. Three other chick,and carriedit to a perchon a fenceabout 10 m adults approached,and for approximately1 min, from the nesttree. The chickwas alive and moving. theyall peckedand pulled on the chick.The nestling Anotheradult flew from the nesttree andjoined the was still alive at 1500, at which time it showed no ex- first one. The first adult dropped the chick to the ternal woundsbut was barely moving.The adults ground,and after about1 min, both adultsflew away did not approachthe chick after the initial attack. from the area. When the chickwas inspectedabout Groupsize at this nestwas eight adults. 5 min later, it was dead and showed no external Infanticide2, nestA8.2.--A secondcase of infanti- wounds.Group size at this nestwas eight adults. cide occurredat nestA8.2 at 1205on the sameday, Infanticide7, nestC16.1.--This episode occurred at 31 October1995, when an adult approachedthe nest, 1619 on 8 October 1997. An adult flew to the nest, pickedup a secondnestling, and tossedit overthe pickedup a one-day-oldnestling, and flew to the nestrim. This adult, alongwith two others,pecked groundabout 10 m from the nesttree. It peckedthe and pulled on the nestlingfor about 1 min before chick repeatedly,then picked it up and flew away abandoningit. Upon examination10 min after the from the area.Group size at thisnest was four adults. event, the chick was dead and exhibited two abdom- Infanticides8 and 9, nestB8.2.--At 1250 on 16 No- inal punctures.At 1415,an adult took food to the re- vember 1997, an adult picked up a live one-day-old maining nestlingsand then approachedthe dead nestlingand flew to a tree approximately40 m from chick,pecked it repeatedly,and tossedit in the air. the nest. We were unable to determine whether it July1999] ShortCommunications 849 droppedthe nestlingor flew awaywith it. Laterthat at leastone other adult was in closeproximity to the day, a dead nestlingwith severalhead woundswas one that evictedthe chick,or helpedto attackthe found at the baseof the nest tree. Group size was chickafter it had been evicted.We observedno ag- eight adults. gressionamong adults, and it is very unlikelythat a Infanticide10, nestD3.2.--On 9 December1997, a groupof nonresidentindividuals could approach the marked adult group memberpicked up a one-day- nestand evict chickswithout beingattacked by the old nestlingand carriedit to a fenceabout 20 m from residentgroup members.In usinghand-reared lure the nest.It droppedthe chick,retrieved it, and then birdsto captureadult groupmembers (Macedo 1992, pecked it occasionallywhile walking around the 1994),resident birds quickly attacked the strangein- area. This adult belongedto a group that nested dividual, frequently using alarm vocalizationsand threetimes during the rainy season.It wascaptured aggressivedisplays. One additional piece of evi- and markedduring the secondnesting event (being dence that infanticidal adults are acceptedgroup describedhere), when group size was five adults. members comes from observations at nest D3.2. In This adult activelyparticipated in group activities this nest, the infanticidal adult was marked, and it during this nestingbout, suchas feedingnestlings participatedin incubationand chickfeeding before and remainingnear the nest tree, as well as in the and after the infanticidetook place. Also, this adult subsequentnesting event. In the nestingbout pre- belongedto the group during the nestingbout fol- vious to the one describedhere (C16.1;group size lowing the one described.However, we do not ex- not estimated),five nestlingsvanished within the cludethe possibilitythat infanticideis alsoused by first weekafter hatching, and we witnessedone case non-groupmembers. Because chicks are not canni- of infanticide(described above). During the nesting balizedafter being killed, it is likely that infanticide bout following this one (D3.3; group size of five alsofunctions as a reproductivestrategy, perhaps to adults, but otherwise not describedhere), we found provokea nestingfailure and force a renestingat- one nestlingdead inside the nest,without external tempt by the group,wherein the infanticidaladult wounds. couldgain a matingopportunity. Discussion.--Our observations indicate that infan- In some of the cases(nos. 1, 2 and 5), multiple ticide is a commonoccurrence during reproduction adults attacked chicks that had been removed from in Guira Cuckoos. More than half of the 54 chicks the nest. One possibleinterpretation is that all of that hatcheddied within the followingweek. These these adults were infanticidal, and their behavior deathsoccurred in a sequentialfashion at eachnest, wasdue to a lackof breedingopportunity dependent and the dead nestlingsdid not exhibit evidenceof upongroup size. However, we do not think that this predation.At least11% of thesedeaths occurred as a is a likely explanation.Although nesting attempts direct result of adult intervention at nests. This value may occurwith asmany as 13 adults,none of the at- almostcertainly is an underestimate,and we suspect temptswe observedinvolved groups exceeding eight that infanticide is the cause of death for most nes- individuals.It is dubiousthat in smallergroups the tlings. involvementof up to four adultskilling a chickqual- Our observationssuggest that infanticidein Guira ifies all of them as infanticidalin the specificsense Cuckoos occurs in a context somewhat different discussedhere. Rather, we believethat attackingnes- from that suggestedfor othergroup-breeding birds. tlingsthat havebeen removed from the nestmay in- Most recorded casesof avian infanticide implicate dicate that recognitionof a chick as one of the the arrivalof an immigrant,for whom the killing of group'soffspring does not occurdirectly, but maybe nestlingsmay result in a breeding opportunity. For based, instead, on nest-associationcues (Sherman example, Stacey and Edwards (1983) reported cir- 1981).Although this behavior can be considereddif- cumstantial evidence whereby immigrant female ferentfrom the actionof evictinga chickfrom a nest, Acorn Woodpeckers(Melanerpes formicivorus) killed this situationclearly demonstratesthe capacityof nestlingsto obtaina reproductiveopportunity with- group membersto act togetherduring aggressive in the groupand raisetheir ownyoung. In non-com- acts. munal species,such as egrets (Fujioka 1986), jacanas Socialityis the resultof many conflictingelements (Stephens1982), and sparrows(Veiga 1993), the be- through which a point of equilibrium is reached havioralrepertoire also includes egg destruction and (Emlen 1991). Guira Cuckoogroups fall into the chickkilling duringmate-takeover events. "egalitarian" categoryproposed by Vehrencamp In some(or perhapsall) cases,infanticide in Guira (1983),whereby all individualspotentially can attain Cuckoosmay be perpetrated by acceptedgroup reproductivestatus. However, the occurrenceof in- members. Unfortunately, the infanticidal adults, fanticidein Guira Cuckoogroups suggests that the with but oneexception, were not markedat the time objectivesof individuals in the group sometimes of their chick-killingbehavior. Despite little direct conflict,and that fitnessbenefits are not alwaysequal proof, however,several general factors point to the for all individuals during a single reproductive likelihood that infanticidal adults were members of event.In many studies,parental behavior has been the nestinggroup. In four of the episodesdescribed, associatedwith gamete contribution(Vehrencamp 850 ShortCommunications [Auk, Vol. 116

1977,Joste et al. 1982,Craig andJamieson 1985). The CRAIG,J. L., AND I. G. JAMIESON.1985. The relation- lack of a geneticcontribution in the broodcan result ship of presumedgamete contribution and pa- in the absenceof parentalinvestment. In the caseof rental investment in a communally breeding Guira Cuckoos,data indicate that somegroup mem- . BehavioralEcology and Sociobiology17: bersare completelyexcluded from a breedingevent 207-211. (Quinn et al. 1994).This couldoccur for a numberof DRUMMOND, H., E. GONZALEZ, AND J. L. OSORNO. reasons(e.g. sexual immaturity, lack of copulation 1986. Parent-offspringcooperation in the Blue- opportunities).An adult also couldhave a low fit- footed Booby (Sula nebouxii):Social roles in in- nesspayoff in a particular nestingbout (e.g. a sub- fanticidalbrood reduction.Behavioral Ecology ordinategroup member may have all of its earlyeggs and Sociobiology19:365-372. tossedfrom the nest). EMLEN,$. t. 1991.Evolution of cooperativebreeding Given theseobservations, we hypothesizethat in- in birdsand mammals.Pages 301-337 in Behav- fanticide in Guira Cuckoosis an alternative repro- ioural ecology:An evolutionaryapproach (J. R. ductive strategythat could benefitseveral types of Krebs and N. B. Davies, Eds.). Blackwell Scien- individuals:(1) group memberswho fail to repro- tific Publications, London. duce, and for whom a new breeding opportunity FUJIOKA,M. 1985. Food delivery and sibling com- mayarise if infanticidedecreases the time until a re- petition in experimentallyeven-aged broods of nesting attempt is made; (2) non-group members the Cattle Egret.Behavioral Ecology and Socio- that may gain membershipin the nextbreeding bout biology 17:67-74. by eliminatingthe communally produced brood; and FUJIOKA,M. 1986. Infanticide by a male parent and (3) group membersfor whom fitnessgains poten- by a new female mate in colonial egrets. Auk tially are greaterin a future nestingattempt than in 103:619-621. the currentattempt. GALLARDO,J. M. 1984. Observacionessobre el com- An intriguing questionraised by theseobserva- portamientodel Pirincho(Guira guira) Aves: Cu- tions concernsthe benefitsof socialitythat would culiformes.Revista Museo Argentino de Cien- offsetthe very high reproductivecosts represented cias Naturales Bernardino Rivadavia 13:167- by egg and chickelimination. The habitat occupied 170. by the studypopulation is not saturatedwith breed- HAUSFATER,G., S. AREF, AND S. J. CAIRNS. 1982. In- ing territories, so sociality probably is not main- fanticide as an alternative male reproductive tained by ecologicalconstraints (Macedo 1992, Ma- strategyin langurs:A mathematicalmodel. Jour- cedo and Bianchi 1997a). Potential benefitsof soci- nal of TheoreticalBiology 22:19-58. ality in Guira Cuckoosinclude: (1) increaseddetec- HRD¾,S. 1979. Infanticideamong : A review, tion of and defenseagainst predators; (2) improved classification,and examinationof the implica- foraging efficiencythrough enhanceddetection of tionsfor the reproductivestrategies of females. prey items; (3) increaseddefense of resources(nest- Ethologyand Sociobiology1:13-40. ing sites, food, etc.) against conspecifics;(4) better HRDY,S., ANDG. HAUSFATER.1984. Comparative and careof nestlingsthrough increased levels of per ca- evolutionaryperspectives on infanticide:Intro- pita feeding;and (5) higher long-term survival for duction and overview.Pages xiii-xxxv in Infan- individualsin groups.Further studies are required ticide: Comparativeand evolutionaryperspec- to enhanceour understandingof the selectivepres- tives(G. Hausfaterand S. B. Hrdy, Eds.).Aldine suresthat resultedin cooperativeas well as conten- Press, New York. tious behaviors in Guira Cuckoos. JOSTE,N. E., W. D. KOENIG, R. L. MUMME, AND F. A. Acknowledgments.--Wethank R. Oliveira, M. Si- PITELKA.1982. Intra-group dynamics of a co- mon,A. Polejack,C. Ara6jo, M. Cariello,and B. Fon- operative breeder:An analysisof reproductive secafor help with field work and M. Marini, G. Colli, rolesin the AcornWookpecker. Behavioral Ecol- T. C. Edwards,and an anonymousreviewer for com- ogy and Sociobiology11:195-201. mentson the manuscript.RHM is a ResearchFellow MACEDO,R. H. 1992.Reproductive patterns and so- of the Conselho Nacional de Desenvolvimento Cien- cial organizationof the communalGuira Cuck- ffficoe Tecno16gico(CNPq). The studywas support- oo (Guira guira) in central Brazil. Auk 109:786- ed by grantsfrom Fundo Nacionaldo Meio Ambien- 799. te (FNMA), BehaviorSociety (Developing MACEDO,R. H. 1994.Inequities in parentaleffort and NationsResearch Grant), and Fundode Apoioa Pes- costsof communalbreeding in the Guira Cuck- quisa do D.E (FAP-DF). oo. OrnitologiaNeotropical 5:79-90. MACEDO, R. H., AND C. g. BIANCHI. 1997a. Com- LITERATURE CITED munalbreeding in tropicalGuira CuckoosGuira guira:Sociality in theabsence of a saturatedhab- BROWN,J. L. 1987. Helping and communalbreeding itat. Journalof Avian Biology 28:207-215. in birds. PrincetonUniversity Press, Princeton, MACEDO, R. H., AND C. A. BIANCHI. 1997b. When New Jersey. birds go bad: Circumstantialevidence for infan- July1999] ShortCommunications 851

ticide in the communal South American Guira ticide and parentalcare (S. Parmigianiand ES. Cuckoo.Ethology, Ecology and Evolution9:45- Saal, Eds.). Harwood Academic Publishers, 54. Chur, Switzerland. MOCK, D. W. 1984. Infanticide, siblicide, and avian STACEY,P. g., AND t. C. EDWARDS,Jr. 1983. Possible nestling mortality. Pages 3-30 in Infanticide: casesof infanticide by immigrant females in a Comparativeand evolutionaryperspectives (G. group-breedingbird. Auk 100:731-733. Hausfater and S. B. Hrdy, Eds.). Aldine Press, STEPHENS,M. L. 1982.Mate takeoverand possiblein- New York. fanticideby a femaleNorthern Jacana (Jacana spi- MOCK, D. W., AND L. S. FORBES.1994. Life-history nosa).Animal Behaviour30:1253-1254. consequencesof avian brood reduction. Auk TRAIL, P. W., S. D. STRAHL, AND J. L. BROWN. 1981. 111:115-123. Infanticide in relation to individual and flock PARMIGIANI,S., AND E S. VOM SAAL. 1994. Infanti- historiesin a communallybreeding bird, the cide and parentalcare. Harwood AcademicPub- MexicanJay (Aphelocoma ultramarina). American lishers, Chur, Switzerland. Naturalist 118:72-82. QUINN, J. S., R. H. MACEDO, AND B. N. WHITE. 1994. VEHRENCAMP,S. L. 1977.Relative fecundity and pa- Genetic relatednessof communally breeding rental effort in communallynesting anis, Croto- Guira Cuckoos. Animal Behaviour 47:515-529. phagasulcirostris. Science 197:403-405. SHERMAN,P. 1981.Reproductive competition and in- VEHRENCAMP,S. L. 1983. A model for the evolution fanticidein Belding'sground squirrels and other of despoticversus egalitarian societies. Animal animals. Pages311-331 in Natural selectionand Behaviour 31:667-682. socialbehavior: Recent research and new theory VEIGA,J.P. 1993. Prospectiveinfanticide and ovula- (R. Alexander and D. Tinkle, Eds.). Chiron Press, tion retardationin free-livingsparrows. Animal New York. Behaviour 45:43-46. SOMMER,V. 1994.Infanticide among the langursof Jodhpur:Testing the sexualselection hypothesis Received23 March 1998, accepted29 January1999. with a long-termrecord. Pages 155-198 in Infan- AssociateEditor: J. Ekman

TheAuk 116(3):851-854, 1999

ConsistentMale-biased Seabird Mortality in the PatagonianToothfish Longline Fishery

PETER G. RYAN • AND CHRISTIAN BOIX-HINZEN PercyFitzPatrick Institute of AfricanOrnithology, University of CapeTown, Rondebosch 7701, SouthAfrica

Seabirdby-catch from longlinefisheries is a global noides),in waters to the south of the area exploited conservationconcern. Many thousandsof birds are by the tuna fishery(Cherel et al. 1996,Moreno et al. killed eachyear when they seizebait from longlines 1996).Mortality from thesefisheries is placingad- and are drowned (Brothers 1991, Alexander et al. ditional pressureon seabirdsin the SouthernOcean 1997). Most of these birds are procellariiforms, (Alexander et al. 1997). which are long-livedspecies with low reproductive Procellariiformsare monogamous(Warham 1990). rates and high susceptibilityto even small changes Consequently,the demographic implications of long- in survival rate, especiallyin adults (Croxall et al. line by-catchare exacerbatedwhen mortality is sex 1990).The estimatedeffect of the tuna longlinefish- biased.Female-biased mortality from longlinefish- ery in the SouthernOcean during the last30 yearsis erieshas been reportedfor WanderingAlbatrosses sufficient to account for observed decreases in breed- (Diomedeaexulans; Weimerskirch and Jouventin 1987, ing numbersof many albatrossesand other procel- Croxall and Prince1990) and Grey Petrels(Procellaria lariiforms (Weimerskirchand Jouventin1987, Crox- cinerea;Bartie 1990, Murray et al. 1993).These biases all et al. 1990, Gales 1993). More recently,longline have been attributed to differences between the sexes fisheries have commenced in the Southern Ocean, in foragingranges, with femalesforaging farther notably for Patagoniantoothfish (Dissostichuselegi- north thanmales and thus spending more time in the waterswhere tuna longlinevessels operate. Here, we report consistentmale-biased mortality from the E-mail: [email protected] longlinefishery for Patagoniantoothfish that oper-