How White-Throated Magpie-Jay Helpers Contribute During Breeding

The Auk 116(1):131-140, 1999

HOW WHITE-THROATED MAGPIE-JAY HELPERS CONTRIBUTE DURING BREEDING

TOM A. LANGEN • AND SANDRA L. VEHRENCAMP Departmentof Biology,University of CaliforniaSan Diego, 9500 GilmanDrive, La Jolla, California 90013, USA

ABSTRACT.--Weinvestigated the mechanismsby whichhelpers contribute to breederre- productionin a CostaRican population of White-throatedMagpie-Jays (Calocitta formosa). Helpersprovided a substantialproportion of all feedingsto femalebreeders and their offspring,proportionately more than mostspecies of cooperativelybreeding New Worldjays. Breedingmales typically fed breedingfemales and offspringless frequently than expected, however.There was little evidenceof brooddivision in the senseof individualprovisioners (breedersor helpers)preferentially feeding particular fledglings within a brood.The rate of provisioningper recipientincreased as a functionof group size only during the pre-incubationperiod (provisioningof the laying female).Provisioning rates per nestlingand per fledglingwere not correlatedwith groupsize, and the number of offspringfledged per successfulnest did not increasewith groupsize. Helpers did reducethe provisioningburden onbreeders, however, and occasionally were the primary care-providers of fledglings,which allowedbreeders to renest.More successful nests were produced in groupswith manyhelpers than few, resultingin more fledgedyoung per year.Mechanisms contributing to this "helper-effect"included more nesting attempts per yearand a higherlikelihood of renesting after a successfulattempt. We concludethat the contributionsof magpie-jay helpersin- creasedbreeder fitness, and the indirectand directbenefits gained by helpingprobably fa- voredits expressionby nonbreedinggroup members. Received 30 October1997, accepted 18 June 1998.

FORA FEWcarefully studied speciesof co- ing (e.g. Brown and Brown 1981, Rowley and operativelybreeding birds, evidencesuggests Russell 1990, Komdeur 1994). thathelpers (individuals that feed and perform Groupsof White-throatedMagpie-Jays (Cal- otherparental-care activities for offspringthat ocittaformosa)typically are composedof a pri- are not their own; Skutch 1961, Brown 1987) mary breedingpair and three to four helpers have no effect on, or may evenreduce, the fit- (rangeone to nine; Innes and Johnston1996, ness of breederswhose offspringthey help Langen1996a, Langen and Vehrencamp1998). (Leonard et al. 1989, Marzluff and Balda 1992, Most femalesremain on their natal territory as Komdeur1994, Magrath and Yezerinac1997). helpers,but malesdisperse at aboutone year of Formany other cooperatively breeding species, ageand become floaters (Langen 1996a, b). The however,helpers do indeedappear to increase primary breeding pair attemptsto reproduce the survivorshipand reproductivesuccess of repeatedlyduring the long breeding season thebreeders they help through a varietyof spe- (greaterthan 200 days), and somefemale help- cificmechanisms (Brown 1987, Stacey and Koe- ers alsobreed on occasion(Langen 1996a). Off- nig 1990,Emlen 1991). For example, helpers can springare fed by helpersduring the nestling increasethe numberor viability of offspringin period and after fledging until nutritional in- eachbrood by decreasingthe risk of starvation dependence(Langen 1996b). Group members and predation(e.g. Rabenold 1984, Strahl and associatewhile foragingand give a varietyof Schmitz1990, Emlen and Wrege 1992, Hein- visualand auditorysignals that alert othersto sohn1992, Mumme 1992),or they can reduce the presenceof food,predators, and conspecific the time and energythat the breeders devote to intruders (Langen 1996b,c, unpubl. data). eachbout of reproduction,resulting in higher In a recentpaper (Langenand Vehrencamp breedersurvivorship or morefrequent renest- 1998), we analyzed the effects of group size and territory size on the reproductivesuccess • Presentaddress: Department of Biology,Univer- of magpie-jaygroups. In our sampleof 14 ter- sity of California,405 Hilgard Drive, Los Angeles, ritories, the number of offspringfledged per California 90095,USA. E-mail: [email protected] successfulnest did not vary with group size,

131 132 LANGENAND VEHRENCAMP [Auk, Vol. 116 but a significantpositive association existed be- nestlingswas recorded(although we were not able tweengroup size and the numberof successful to determinethe distributionof feedingsamong nestsper year. As a result, large groups (i.e. nestlings).We also monitoredthe provisioningof groupswith manyhelpers) fledged significant- each fledged offspringuntil nutritionalindepen- dencevia timedsamples during which we recorded ly more youngper year than did small groups. the numberof feedingsreceived and the identityof This putative"helper effect"was independent provisioners (see Langen 1996b). Samples were of territory quality. Here, we examinein more madeonce per week or morefrequently (8 to 14 sam- detail how helperscontribute during breeding. ple daysper fledgling),each sample lasting 30 to 60 We ask whether: (1) helpersincrease nesting min (timedonly when the animal was in sight).Mag- successby reducingthe likelihoodof nestfail- pie-jaysare relativelytolerant of humans,so most ure or increasingthe number of nesting at- observations could be made at distances of 10 to 25 tempts,(2) helpersreduce the rate of foodpro- m. We could not reliably quantify the quality and visioningby thebreeders or increasethe rateof load size of the foodbrought by provisionersat any food delivery to recipients, and (3) breeders stageof breeding,however. Classificationof group members.--Groupmembers and helpers divide reproductivetasks to in- comprised all individuals that repeatedly were creaseefficiency during breeding. foundassociated while foraging or restingand who rangedwithin the boundariesof a singleterritory METHODS (Langenand Vehrencamp 1998). The female that incubated the clutch and the male that consorted and Monitoringof breeding groups.--We collected data at copulatedwith her duringthe pre-incubation period Santa Rosa National Park, Guanacaste Conservation are designatedas the breeders during a nestingat- Area, Guanacaste Province, Costa Rica (10ø50'N, tempt;other birds that fed the incubatingfemale or 85ø37'W)during 1992 and 1993.A detailedsite de- the offspringare calledhelpers. Within groups,the scriptioncan be foundin Langenand Vehrencamp samefemale incubated during most of thenesting at- (1998).The membersof six groupscontaining indi- tempts;we referto thesebirds as primary breeding vidually marked birds were the primary focusof females.A few femalehelpers also infrequently es- study,and an additionaleight groupswere moni- tablishedtheir own nests in thegroup territory (19% tored lessintensively during the breedingseason of helpersand 17% of nestingattempts). The nests of (detailson markingand censusingin Langen1996a, thesesecondary breeders are analyzedseparately b). We include data from theseadditional groups from thoseof the primary breedersbecause the for- where appropriate. mer generallyreceived much less help from other We visited all focalterritories and nearbyhabitat group members(see Results). at leastweekly during the breeding season (January The helpercategory of groupmembers includes to August).Nests were detected by listeningfor the secondarybreeding females because they helped at loud food-solicitation calls that are broadcast with mostof thenests of primarybreeders. Young helpers monotonousregularity during the pre-incubation are birds that were participatingin their first full periodby breedingfemales in the vicinity of their breedingseason (under 19 monthsof age; 16% of nest(Langen 1996a). Once a breedingepisode had helpers).Older helpersare thosethat had partici- begun, we initiated intensive monitoring of the patedin at leastone full breedingseason. When com- group (seebelow). In addition,group members were paring among species,we refer to nonbreeding talliedduring visits. Because the absenceof a female group memberscollectively as auxiliaries,because mightindicate nesting, we carefullysearched terri- helpingbehavior is not observedin all speciesin toriesfor additionalnests after detectingthat a fe- which nonbreedersare present during nesting male was absent.Most nests(83%) were locateddur- (Brown 1987). ing the pre-incubationperiod; the remainderwere Statisticalanalysis.--To analyze the associationbe- discoveredshortly after the onsetof incubation. tweengroup size and provisioningrate, we calculat- Feedingof thebreeding female or offspringby oth- ed the medianprovisioning rate (feedingvisits per er group memberswas quantifiedduring eachof hour) duringeach breeding stage for eachgroup three nestingstages: (1) pre-incubation,when the year.Nestling and fledglingprovisioning rates used breedingfemale was laying but not yet incubating; to calculatethe median are adjusted for the age of the (2) incubation,when the breedingfemale brooded offspring(residuals of theregression of provisioning the eggs;and (3) the nestlingperiod. Nests were ob- rate on age)because preliminary analysesindicated servedthrough spotting scopes at a distanceof 20to a significanteffect of this variableon feedingrate 75m (dependingon the tolerance of groupmembers) (Langen1996b). We analyzedprovisioning rate from for 90 min per morningthroughout each monitored the perspectiveof a recipientand a donor.The recip- breedingattempt such that every instance that an in- ient provisioningrate is definedas the numberof dividual broughtfood to the incubatingfemale or feedingvisits per hourto the female(pre-incubation J.anuary 1999] ContributionsofMagpie-Jay Helpers 133

and incubationstages), a nestling(nestling stage), or ¸ ¸ a focalfledgling (fledgling stage). The rate per nest- • 5 ling is estimatedby dividingthe numberof feeding visitsto the nestper hourby the numberof nestlings presentat banding(around 10 daysposthatching). We calculatedthe donorprovisioning rate by divid- ing the total rate of feedingto all recipientsby the number of group members(i.e. feedingvisits per hourper provisioner).We estimatedthe totalrate of provisioningduring the fledglingstage by multiply- ing the numberof feedingvisits per hour to a focal fledglingby the numberof fledglingsin the brood. Helper Number We present analysesusing total helper number FIG1. Relationshipbetween the numberof nest- (groupsize - 2);the conclusionsdid notdiffer when ing attemptsby White-throatedMagpie-Jays per the sameanalyses were performedwhile excluding year and numberof helpersduring the two yearsof younghelpers, presumably because the two mea- this study.Each circle represents one group year; all suresof groupsize are highly correlated(r = 0.86). groupsfrom 1992were alsopresent in 1993. Forall comparisonsbetween helper number and a dependentvariable, we use group year as the unit of replication.We initially performed ANCOVA that in- borusplancus; one nest), and black iguanas cludedyear as a factor,because helper effects may be (Ctenosaursimilis; one nest); severalother in- limited to particularyears. If the interactionterm was not near significance(P > 0.1) it was removed stancesof nestpredation may have been caused from the model, and if year was subsequentlynot by nocturnalmammals. near significance,it was also removed.Before mak- The total number of nesting attempts in- ing testsof linearassociations, we examinedplots for creasedwith helper number and differed be- evidenceof nonlineareffects. For parametrictests, tweenyears (helper number, F = 5.2, P = 0.05; variables were transformed as needed. All statistical year, F = 12.2,P = 0.007;Fig. 1). The number probabilitiesare two-tailed. of nestingattempts per year by the primary breedingfemale was predictedby year only RESULTS (helpernumber, F = 0.8, P = 0.4;year, F = 15.4, P = 0.004; 1992, œ = 4.2 + 0.37 nesting at- Nestingsuccess and group size.--The number tempts,1993, œ = 2.7 + 0.18).The time between of successfulnests per year, and hence the the termination of one failed nest and the start number of young fledged, increasedwith of thenext was not predictedby helpernumber group size (Langenand Vehrencamp1998). (œ= 12.0 - 2.08 days, n = 9, F = 0.2, P = 0.7), Large groupsmay have had more successful perhapsbecause the breedingpair performed neststhan smallgroups because: (1) the prob- most of the nest constructionwithin groups abilityof successper nesting attempt was high- (e.g.delivered 94.7% of the nestingmaterial, n er, (2) primary breedersattempted more nests, = 133 deliveriesamong four breeding pairs). or (3) more femalesbred. However,primary breeders with manyhelpers We were confident that we detected all of the weremore likely to renestafter having fledged nestingattempts in a total of 12 group years offspring than breeders with few helpers duringthe study.The proportionof nestingat- (Mann-Whitney U = 27, n• = 4, n2 = 7, P = temptsthat failed covariedwith the numberof 0.02).Renesting typically began before fledg- helpersdifferently between years (helper num- lings had attainednutritional independence; ber x year interaction,slope = 0.197, F = 6.6, two instanceswere 16 and 31 days after off- P = 0.03) and varied significantlybetween springhad fledged.This correspondedwith years(1992, œ = 0.82 -+ SEof 0.046nests failed; the periodof peak offspringprovisioning (Lan- 1993, œ= 0.76 -+ 0.063; F = 6.2, P = 0.04). Nest gen 1996b:figure 1). predationwas implicatedin virtually all fail- The numberof nestingattempts per year by ures whose cause could be determined, but secondarybreeding females was not associated wind damagemay have causeda few of the with helpernumber (F = 2.5, P = 0.1; œ= 0.5 failures. Confirmed diurnal nest predatorsin- + 0.20 nests).The failure rate of nests of sec- cludedwhite-faced capuchin monkeys (Cebus ondarybreeders was not significantlyhigher capucinus;six nests),Crested Caracaras(Poly- than that of primary breeders(Langen 1996a), 134 LANGENAND VEHRENCAMP [Auk,Vol. 116

12 13 Female Offspring

[] Preincubation 0.8

ßE 6 [] Incubation 18 [] Nestling ß• 4 ß Fledgling 0.6

2 0.4

5 20 23 71 Duration 0.2 (Days) F•G. 2. Total rate of provisioning(number of feedingvisits per hour)to femaleor all offspring • HelpersAll • ,•LI HelpersAll White-throatedMagpie-Jays combined during each stage of breeding (F = 41.1, df = 3 and 61, P < F•G. 3. Proportionof feeding visits made by 0.0001;Scheff6 post-hoc test, pre-incubation: in- breedingmale White-throated Magpie-Jays and all cubation< nestling< fledgling).Each sample is a helpersto the female,and by thebreeding female, mean rate per groupyear; aboveeach bar is the num- breedingmale, and all helpersto offspring(n = nine ber of groupyears sampled among 10 groups.The groupyears from five groups). mean durationin days of eachbreeding stage is shownbelow the bar.The fledglingstage only in- cludesfeedings through the meanage of nutritional independence. visioningrates were higher (helper number x year interaction,slope = 0.043, F = 3.7, P = 0.09;helper number, slope = -0.043, F = 3.8, but becausethese nesting attempts were infre- P = 0.08;year, slope = -0.270, F = 4.0, P = quent,only I of 10 successfulnests was by a 0.08;per recipienthelper number, F = 0.4, n = secondarybreeder. 13, P = 0.5; n = 13). Samplesizes were too Rateofprovisioning.--The rateof provisioning small to performthe same analyses for second- variedgreatly among the differentstages of ary breeders. breeding,with thehighest levels occurring af- Provisioningand group membership class.--A ter offspringhad fledged(Fig. 2). Primary majorityof all feedingvisits to thebreeding fe- breedingfemales were fed at significantly maleor offspringwere made by helpers(Fig. higherrates than were secondary females in the 3).Half of the young helpers made significantly pre-incubationand incubationstages (mean fewervisits than othergroup members, how- provisioningrate comparedwith t-testssepa- ever(25 _+ 11.5% fewer feeding visits than older ratelyfor each group; trend among groups test- groupmembers, n = 7 younghelpers; see Lan- edusing Fisher's combined probability; pre-in- gen 1996b).Slight differences existed in pro- cubation,X2 = 13.9,n = 2 groups,P < 0.01,sec- visioningeffort amongolder helpers within a ondaryrates 61 _+11.3% lower; incubation, X 2 group(CV of olderhelper feeding visits = 0.36 = 24.6,n = 5, P < 0.01,secondary rates 66 -+ --z-0.053, n = 7 groupyears). Breeding females 12.7%lower; nestling, X 2 = 3.9, n = 2, P > 0.1). made relatively smaller contributionsto off- Fornests of primarybreeders, the rate of pro- springfeeding in groupswith manyhelpers visioningincreased significantly with helper (Fig.4), buttheir efforts typically were not dif- numberduring pre-incubation from the point ferentfrom those of the averageolder helpers of view of therecipient and possibly of the do- (Table1). Breedingmales, however, made fewer nor (per recipient,F = 8.8, P = 0.02,slope = feedingvisits than expected(Table 1); five of 0.046;per donor,F = 3.9, P = 0.07, slope= six malesprovisioned less than expecteddur- 0.006,n = 14).There was no significanteffect ing some period. Surprisingly,one of these of helpernumber on eitherdonor or recipient males (group Comedor)made significantly provisioningrates during the incubationand morefeeding visits to offspringthan expected nestlingstages (incubation, Fs < 0.03, n = 14, duringone year and significantlyfewer the fol- Ps > 0.8;nestling, Fs < 0.1, n = 12, Ps > 0.7). lowingyear. Apparently, both the breeding fe- Duringthe fledglingstage, there was a trend maleand helpers compensated for a group's for provisioningper donor to declinewith breedingmale. helpernumber, particularly in 1993when pro- Division of fledged broods.--Weexamined January1999] ContributionsofMagpie-Jay Helpers 135

0.25-

c3 t• + I + 0.20. +

• + I +

Helper Number Fic. 4. Effectof total helpernumber on the proportion of White-throated Magpie-Jay offspring feedings (including nestling and fledgling stages) provided by the primary breeding female (rs = -0.82, P < 0.02). The line representsthe expected proportionof feedingsif all individualscontributed equally (n = nine group-yearsamong five groups).

whether eachprovisioner randomly distribut- ed feedingswithin a fledgling cohort.The al- locationof feedingsto fledglingswas significantly nonrandomduring one groupyear out of seven(plus one trend; Table2). In the one significant group year (Comedor 92), the +++ breedingmale fed onefledgling disproportion- ately,and onehelper fed a secondfledgling dis- proportionately,but the other groupmembers displayedno biasamong the three fledglings. Survivorshipof offspring.--Clutchsize was significantlyhigher in large groups than in small groups(Langen 1996a), but the number of nestlingsat the dayof banding(10 days post- hatching)did not covarywith groupsize (rs = -0.07, n = 27, P > 0.5;œ = 3.2 _+0.18 nestlings). Althoughin larger groupsa lower proportion of eggs producednestlings at day 10, as ex- pectedfrom the previousresults, the relation- ship was not significant(rs = -0.11, n = 17, P > 0.5; • = 0.61 _+0.061). For neststhat fledged young, nestling survival from banding to fledging did not differ significantlybetween small groups (1 to 3 helpers, 38.1% disappeared,n = 21) and largegroups (4 to 7 helpers, 45.5% disappeared,n = 11; Fisher'sexact test, P = 0.5). Disappearancesbetween fledging and six monthsof age,which is the period of transition to nutritional independence(Lan- gen 1996b),did not differ significantlybetween small groups(37.5%, n = 8) and large groups (11.7%, n = 17; Fisher'sexact test, P = 0.3). 136 LANGENAND VEHRENCAMP [Auk, Vol. 116

TABLE2. Resultsof contingencytests examining whether individual White-throated Magpie-Jays prefer- entiallyprovision particular fledglings within a brood.

Group X2 (df) No. of fledglingsa Provisionersb Aviary 92 6.1 5 2 (56, 62) M, F, 4H Caja 92 3.5 3 2 (45, 52) M, F, 2H Caja 93 3.6 6 3 (30, 34, 49) E 3H Casona92 8.6* 4 2 (62, 66) M, F, 3H Casona 93 4.5 5 2 (63, 89) M, E 4H Comedor 92 22.3** 8 3 (83, 109, 115) M, F, 3H Comedor 93 9.3 12 5 (38, 32, 39, 23, 27) F, 3H

*, P < 0.10; *% P < 0.01. Numberof observedfeedings for eachfledgling in parentheses. Groupmembers that provisioned fledglings frequently enough to be includedin statisticaltests. M = breedingmale; F = breedingfemale; = helper.

DISCUSSION visionedat leastas frequentlyas eachbreeder. However, as observedin a number of cooper- Effectsof helpers on breeding success.--Magpie- atively breeding species(Brown et al. 1978, jay helpersengaged in muchprovisioning of Brown and Brown 1981, Raitt et al. 1984, Rus- breeding females and offspring. Compared sell and Rowley 1988,Woolfenden and Fitzpat- with other New World jays (a monophyletic rick 1990),the rate of provisioningdid not ap- group within which cooperativebreeding is pear to increasesignificantly with the number widespread;Edwards and Naeem 1993, Espi- of helpers,nor did the numberof offspring nosade los Monterosand Cracraft1997), mag- fledgedper successfulnest increase with group pie-jaysprovided a higherproportion of feed- size.It is possible,however, that the quality or ingsto nestlingsthan 12 of 13 speciesthat have quantity of food broughtduring feedingvisits auxiliaries(Table 3). The large contributionby varied with membershipclass, as is true of nonbreederswas a consequenceof four factors: some other species(Stallcup and Woolfenden (1) a large number of auxiliariesper breeding 1978,Hunter 1987).We couldnot estimateload group;(2) eachauxiliary was a helper;(3) most size accurately,but for the subsetof feeding of the helperswere older, experiencedgroup visitsin which food itemswere visible,young members;and (4) the averageolder helper pro- helpersdid not provide qualitativelydifferent

TABLE3. Proportionof feedingvisits to nestlingsmade by groupmembers other than the presumed parents for speciesof New Worldjays. Only groupswith potentialhelpers are included;n is the numberof group years.Expected is theproportion of feedingvisits provided by auxiliariesif all groupmembers provisioned equally. Group Feedings Species size ObservedExpected n Source Aphelocomacalifornica 4.0 0.01 0.50 1 Burt and Peterson1993 Aphelocomacoerulescens 3.7 0.44 0.46 10 Stallcupand Woolfenden1978 Aphelocomaultramarina 13.3a 0.58 0.85 7 Brown 1972 Aphelocomaunicolor 4.0 0.77 0.50 2 Webber and Brown 1994 Calocitta colliei 5.7 0.49 0.65 12 Winterstein 1985 Calocittaformosa 5.6b 0.61 0.64 9 This study Cyanocoraxbeecheii 4.5 0.47 0.56 8 Raitt et al. 1984 Cyanocoraxmelanocyaneus 11.0 0.60 0.82 1 Hardy 1976 Cyanocoraxmorio 5.3 0.54 0.62 3 Skutch1960 Cyanocoraxsanblasianus nelsoni 6.0 0.45 0.67 1 Hardy 1976 Cyanocoraxs. sanblasianus 20.5a 0.40 0.90 8 Hardy et al. 1981 Cyanocoraxyncas cyanodorsalis 4.0 0.43 0.50 2 Alvarez 1975 Cyanocoraxyncas glaucescens 4.7 0.00 0.57 9? Gayou1986 Gymnorhinuscyanocephalus 3.0 0.26 0.33 4 Marzluff and Balda 1990 Pluralbreeders in whichbreeders also help at othernests; group size includesall territorymembers. Primarybreeders' nests only; includes young helpers. January1999] ContributionsofMagpie-Jay Helpers 137 food than did older group members(Langen Brown1980), or principallyby the parentsand 1996b). somemale helpers(Marzluff and Balda1992). Althoughnot affectingthe numberof off- Similar to anotherstudy of a cooperatively spring fledgedper nest, groupswith many breedingjay (McGowanand Woolfenden1990), helpershad moresuccessful nests per breeding brood division appearsto be rare in magpie- season.This was not a resultof higherrates of jays. A relativelyhigh risk of attractingCol- successfulnesting or increasednumbers of sec- lared Forest-Falcons(Micrastur torquatus)be- ondary nestsin larger groups, but arose be- causeof offspringbegging (Langen 1996b) may causebreeders attempted more nests.Helpers selectfor flexible responsesto offspring de- provideda type of "load-lightening"(sensu mand by provisioners,as has beensuggested Brown 1987)such that after producingfledg- for related species(Caraco and Brown 1986, lings,primary breederswere more likely to re- Marzluff and Balda 1992). nestin large than smallgroups while helpers In somepair-breeding birds, a reproductive continuedto carefor offspringof the previous divisionof laborexists after fledgingin which brood.Renesting even coincided with thepeak malescontinue to carefor the offspringwhile period of offspringprovisioning. Load-light- femalesprepare to renest(e.g. Zaias and Breit- eningthat facilitatesrenesting by breedersor wisch 1989, With and Balda 1990,Weatherhead increasesbreeder survivorship is the mostfre- and McRae 1990, Verhulst and Hut 1996). A quentlydocumented benefit provided by help- similar division of labor occurs between breeders (Crick 1992). ing magpie-jaysand helpers:breeders renest Usingdata from this studyand from previ- and leavethe helpersto continuefeeding the ous publications(Langen 1996a, Langen and fledglingsuntil the latter reachnutritional in- Vehrencamp1998), we estimatedthe directand dependence.This division of laborhas been ob- inclusivefitness of primary breedingfemales in servedin other cooperativelybreeding birds groupshaving one and six helpers(the range (e.g.Brown and Brown 1981,Carlisle and Za- in our data).We assumethat the only resultof havi 1986,Rowley and Russell1990) and may the helpers' contributionsis to increasethe significantlyincrease both the reproductive number of successfulnests, and we have esti- rate of breedersand the durationof offspring mated the proportionof successfulnests that care,which is typicallylonger than in species result from secondarybreeders. We also as- that lack helpers(McGowan and Woolfenden sumethat the numberof offspringthat result 1990, Heinsohn 1991). from egg dumping by nonbreedersis negligi- Conclusionsabout helper contributions.--Many ble,and that secondarybreeders are full sisters uncertainties remain about the form and extent or daughtersof theprimary breeder (coefficient of helper contributionsto breeder fitnessin of relatedness= 0.5). We estimatedthe differ- White-throatedMagpie-Jays. The small sample encein offspringproduction by primary breed- of groupsand the few yearsof studymake it ersin groupswith oneversus six helpers to be unlikelythat we wouldhave detected relatively 4.91fledglings. Thus, each helper augments the small contributionsby helpers,or contribu- offspringproduction of theprimary breeder by tions that were limited to exceptionalyears. 0.98offspring within this range.Including the The experienceof breederswas unknownand indirect componentowing to secondarybreed- conceivablymay have been correlated with the ers changesthis estimateslightly: the differ- numberof helpers.Our study was conducted ence in production of offspring equivalentsis in a nationalpark in whichthe densityof jays 5.08,or 1.02per helper andnest predators appeared to bemuch higher Brooddivision.--After fledging, male and fe- than is typical elsewherewithin the species' male parentscare for a differentsubset of the currentrange (pers. obs.). Habitat and predator brood in some pair- breeding birds (e.g. Mo- densitiesin the park were undergoingrapid reno 1984, Edwards 1985, McLaughlin and changes(e.g. nesting habitat was declining be- Montgomerie 1985, Byle 1990). Offspring of causeof successionafter fire suppression[Jan- different broodsjoin after fledgingin two co- zen1988], and the population of capuchinmon- operativelybreeding, plural-nesting jays, and keyshad grownby 33%in a decade[Fedigan et begging offspring are fed almost indiscrimi- al. 1996]).Finally, we observedan unmanipu- nately by all group members (Brown and lated range of group sizes;only a subsetof 138 LANGENAND VEHRENCAMP [Auk, Vol. 116 groupshad few helpers,and no grouplacked a ences in status and experiencebetween pri- helper.It is possiblethat the presence of helpers mary and secondarybreeders. had a positiveeffect on someundetected as- We conclude that the main contribution of pectsof breeding relative to an unaided pair, magpie-jayhelpers during our study was to but a ceilingwas reachedat a smallerhelper lightenthe burdenof offspringcare on breed- numberthan existedin mostgroups (such ceil- ers, resulting in rapid renestingafter a brood ing effectsare common;Emlen 1991). had fledged.Although we probablyfailed to Two aspectsof helperbehavior could modify documentsome of the helper contributions the conclusionsthat we present.First, we have duringbreeding, our datasuggest that helpers assumedthat helper reproductionwas negli- provide a substantialreproductive benefit to gible except via secondarynesting attempts. breeders, a conclusion similar to that of Innes However,helpers occasionally attempted to lay and Johnston(1996). Helpers probably benefit, eggsin the nestsof primarybreeders (Langen too,because they are closelyrelated to the off- 1996a). If such attempts were regularly suc- spring that are producedbecause of their ef- cessful,then our estimateof helper contribu- forts. However,some putative "helping" actu- tionsto breederfitness is too high. Second,by ally maybe offspringcare that results from egg associatingwith helpersduring the transition dumping by the putative "helper." In part, helpingmay allow nonbreedersto gain access to nutritional independence,offspring may to nestsand alsomay make it easierto become haveacquired foraging and otherskills more a breederon thenatal territory (Langen 1996a). quickly and reliably, potentially resulting in Thus,it appearsthat helpingbehavior is selec- lifelongbenefits (Langen 1996b). Skill acquisi- tively favoredfrom the point of view of both tion may have improvedbecause exploratory the breedersand the helpers. behaviorand practiceof skills were facilitated by supplementalfeeding and vigilanceagainst ACKNOWLEDGMENTS predatorsprovided by helpers, or because helperswere exploitedas sourcesof informa- We thank the staff of the Area de Conservacion tion about predators,appropriate food items,' Guanacastein CostaRica, especially R. Tiffer and R. or foraging tactics(Langen 1996b,c). Indeed, Blanco,for permissionto work in the park and for youngbirds (i.e. less than 500 days of age)were the many courtesiesthey performed during our stay. more successfulat harvestingarthropods in G. Barker, W. Fonseca,G. Birch, S. Villarino, D. Hoff- mann, K. Schoonmaker,K. Ward, and J. Schalley groupswith manyhelpers than in groupswith worked extremelyhard to help gatherthese data. few helpers(Langen and Vehrencamp1998). Commentsby three reviewersimproved the paper. Innes and Johnston(1996), who studied Financialsupport was provided by an NIH Genetics White-throatedMagpie-Jays at the sameloca- TrainingGrant, the TinkerFoundation, Sigma Xi, the tion 10 yearsbefore us, cameto somewhatdif- T.C. SchneirlaComparative Psychology Award, the ferent conclusionsabout the mechanismsby AmericanOrnithologists' Union, and NSF Research whichhelpers contribute during breeding. The GrantIBN 9120789to S.L.V.This paper was prepared main differencebetween the two studiesap- while T.A.L. wassupported by an NIH NationalSer- vice ResearchFellowship. pearsto lie in the socialclassification of jays. For example,Innes and Johnston(1996) includ- LITERATURE CITED ed amonggroup members a classcalled "part- time helpers"that appearsanalogous to some ALVAREZ,H. 1975.The socialsystem of theGreen Jay of the birds that we called"floaters" (i.e. males in Colombia.Living Bird 14:5-44. in the processof natal dispersal;Langen 1996a, BROWN,J. L. 1972.Communal feeding of nestlingsin b). More important,Innes and Johnston(1996) the MexicanJay Aphelocoma ultramarina. Animal includedall femalesthat attemptednests when Behaviour 20:395-402. investigatingthe effectsof helperson repro- BROWN,J. L. 1987.Helping and communalbreeding in birds. Princeton University Press,Princeton, ductivesuccess. Their data appearto havein- New Jersey. cluded females that we would have classified as BROWN,J. L., ANDE. R. BROWN.1980. Reciprocal aid- secondarybreeders. If so, the variationin re- giving in a communalbird. Zeitschriftftir Tier- productivesuccess that they associatewith the psychologie53:313-324. numberof helpersmay be the result of differ- BROWN,J. L., AND E. R. BROWN.1981. Kin selection January1999] ContributionsofMagpie-Jay Helpers 139

and individual selectionin babblers.Pages 244- BiasJay. Bulletin of theFlorida State Museum Bi- 256 in Natural selectionand social behavior (R. ologicalScience 26:203-264. D. Alexander and D. W. Tinkle, Eds.). Chiron HEINSOHN,R. G. 1991. Slow learning of foraging Press, New York. skills and extended parental care in coopera- BROWN, J. L., D. D. Dow, E. R. BROWN, AND S. D. tivelybreeding White-winged Choughs. Amer- BROWN.1978. Effectsof helperson feeding of ican Naturalist 137:864-881. nestlingsin the Grey-crownedBabbler (Pomato- HEINSOHN,R. G. 1992. Cooperativeenhancement stomustemporalis). Behavioral Ecology and So- of reproductive success in White-winged ciobiology4:43-59. Choughs.Evolutionary Ecology 6:97-114. BURT,D. B., ANDA. t. PETERSON.1993. Biology of co- HUNTER,L. A. 1987.Cooperative breeding in Purple operative-breedingScrub Jays (Aphelocoma coe- Gallinules,the role of helpersin feedingchicks. rulescens)of Oaxaca,Mexico. Auk 110:207-214. BehavioralEcology and Sociobiology20:171- B¾1•E,P. A. 1990.Brood division and parentalcare in 177. the periodbetween fledging and independence INNES,K. E., AND R. E. JOHNSTON.1996. Cooperative in the Dunnock (Prunellamodularis). Behaviour breeding in the White-throatedMagpie-Jay. 111:1-19. How do auxiliaries influence nesting success? CARACO,T., ANDJ. L. BROWN.1986. A gamebetween Animal Behaviour 51:519-533. communalbreeders: When is food- sharingsta- JANZEN,D. H. 1988. Managementof habitat frag- ble?Journal of TheoreticalBiology 118:379-393. mentsin a tropical dry forest:Growth. Annals CARLISLE,g.t., ANDA. ZAHAVI.1986. Helping at the of the Missouri Botanical Gardens 75:105-116. nest, allofeedingand socialstatus in immature KOMDEUR,J. 1994.Experimental evidence for help- Arabian Babblers.Behavioral Ecology and So- ing andhindering by previousoffspring in the ciobiology18:339-351. cooperative-breedingSeychelles Warbler Acro- CRI½•c,H. Q. E 1992. Load-lighteningin coopera- cephalussechellensis. Behavioral Ecology and So- tivelybreeding birds and the costof reproduc- ciobiology34:175-186. tion. Ibis 134:56-61. LANGEN,t. A. 1996a. The mating systemof the EDWARDS,P. J. 1985. Brood division and transition to White-throatedMagpie-Jay Calocittaformosa and independencein Blackbirds,Turdus merula. Ibis Greenwood'shypothesis for sex-biaseddispers- 127:42- 59. al. Ibis 138:506-513. EDWARDS,S. V., ANDS. NAEEM.1993. The phyloge- LANGEN,t. A. 1996b.Skill acquisitionand the timing netic component of cooperative breeding in of nataldispersal in theWhite-throated Magpie- perchingbirds. AmericanNaturalist 141:754- Jay,Calocitta formosa. Animal Behaviour51:575- 789. 588. EMLEN,S. T. 1991.Evolution of cooperativebreeding LANGEN,t. A. 1996c.Social learning of a novel for- in birds and mammals.Pages 301-337 in Behav- agingskill by White-throatedMagpie-Jays (Cal- ioral ecology,3rd ed. (J.R. Krebsand N. B. Da- vies, Eds.).Blackwell Scientific Publishing, Ox- ocittaformosa, Corvidae): A field experiment. ford. Ethology102:157-166. LANGEIN, t. A., AND S. L. VEHRENCAMP. 1998. Eco- EMLEN, S. T., AND P. H. WREGE. 1992. Parent-offspring conflictand the recruitmentof helpers logicalfactors affecting group and territory size among Bee-eaters.Nature 356:331-333. in White-throated Magpie-Jays.Auk 115:327- 339. ESPINOSADE LOS MONTEROS,g., AND J. CRACRAFT. 1997. Intergeneric relationshipsof the New LEONARD, g. L., A. G. HORN, AND S. E EDEN. 1989. WorldJays inferred from cytochromeb genese- Does juvenile helping enhancebreeder repro- quences.Condor 99:490-502. ductive success?A removal experiment on FEDIGAN, L. M., L. M. ROSE,AND R. MORERA-AVILA. Moorhens.Behavioral Ecology and Sociobiology 1996. See how they grow: Trackingcapuchin 25:357- -361. monkey (Cebuscapucinus) populations in a re- MAGRATH, g. D., AND S. M. YEZERINAC. 1997. Fac- generatingCostan Rican forest. Pages 289-307 in ultativehelping does not influencereproductive Adaptive radiationsof Neotropicalprimates (M. successor survival in cooperativelybreeding A. Norconk,A. L. Rosenberger,and P.A. Garber, White-browed Scrubwrens. Journal of Animal Eds.). Plenum Press,New York. Ecology66:658-670. GAYOU,D. 1986.The social system of theTexas Green MARZLUFF,J. M., ANDR. P.BALDA. 1990. Pinyon Jays: Jay.Auk 103:540-547. Making the bestof a bad situationby helping. HARDY,J. W. 1976. Comparativebreeding behavior Pages197-237 in Cooperativebreeding in birds. and ecologyof the Bushy-crestedand Nelson Long-termstudies of ecologyand behavior (EB. SanBias jays. Wilson Bulletin 88:96-120. Staceyand W. D. Koenig,Eds.). Cambridge Uni- HARDY, J. W., T. A. WEBBER,AND R. J. RAITT. 1981. versityPress, Cambridge, United Kingdom. Communalsocial biology of the SouthernSan MARZLUFF,J. M., ANDR. P.BALDA. 1992. The Pinyon 140 LANGENAND VEHRENCAMP [Auk, Vol. 116

Jay:Behavioral ecology of a colonialand coop- and behavior. Cambridge University Press, erative corvid. T. and A.D. Poyser,London. Cambridge,United Kingdom. McGOWAN, K. J., AND G. E. WOOLFENDEN.1990. STALLCUP,J. A., AND G. E. WOOLFENDEN.1978. Fam- Contributionsto fledglingfeeding in theFlorida ily statusand contributionsto breedingby Flor- Scrub Jay.Journal of Animal Ecology59:691- ida ScrubJays. Animal Behaviour26:1144-1156. 707. STRAHL, S. D., AND g. SCHMITZ. 1990. Hoatzins: Co- McLAUGHLIN, R. L., AND g. D. MONTGOMERIE. 1985. operative breeding in a folivorousNeotropical Brood division in Lapland Longspurs.Auk 102: bird. Pages132-155 in Cooperativebreeding in 687-695. birds.Long-term studies of ecologyand behavior (P. B. Staceyand W. D. Koenig, Eds.). Cam- MORENO,J. 1984.Parental care of fledgedyoung, di- bridge University Press, Cambridge, United visionof labor,and the developmentof foraging Kingdom. techniquesin the NorthernWheatear (Oenanthe VERHULST,S., ANDg. HUT. 1996.Post-fledging care, oenanthe).Auk 101:741-752. multiplebreeding and the costsof reproduction MUMME,R. L. 1992. Do helpersincrease reproduc- in the Great Tit. Animal Behaviour 51:957-966. tive success?An experimentalanalysis in the WEATHERHEAD,P. J., AND S. B. MCRAE. 1990. Brood FloridaScrub Jay. Behavioral Ecology and Socio- carein AmericanRobins: Implications for mixed biology 31:319-328. reproductivestrategies by females.Animal Be- RABENOLD,K. N. 1984.Cooperative enhancement of haviour 39:1179-1188. breedingsuccess in tropicalwren societies.Ecol- WEBBER,t., ANDJ. L. BROWN.1994. Natural history ogy 65:871-885. of the UnicolorJay in Chiapas,Mexico. Proceed- RAITT, R. J., S. R. WINTERSTEIN,AND J. W. HARDY. ings of the WesternFoundation of VertebrateZo- 1984. Structure and dynamics of communal ology 5:135-160. groupsof BeecheyJays. Wilson Bulletin 96:206- WINTERSTEIN,S. g. 1985.Ecology and sociobiologyof 227. the Black-throatedMagpie-Jay. Ph.D. disserta- ROWLEY,I. C. R., AND E. RUSSELL.1990. Splendid tion, New Mexico StateUniversity, Las Cruces. Fairy-Wrens:Demonstrating the importanceof WITH, K. g., AND g. P. BALDA. 1990. Intersexual var- longevity.Pages 1-30 in Cooperativebreeding iation and factors affecting parental care in in birds. Long-termstudies of ecologyand be- WesternBluebirds: A comparisonof nestling and fledging periods. Canadian Journalof Zo- havior (P. B. Staceyand W. D. Koenig, Eds.). ology 68:733-742. CambridgeUniversity Press, Cambridge, United WOOLFENDEN,G. E., AND J. W. FITZPATRICK.1990. Kingdom. Florida Scrub-Jays:A synopsisafter 18 yearsof RUSSELL,E., AND I. C. R. R¸WLEY. 1988. Helper con- study.Pages 239-266 in Cooperativebreeding in tributionsto reproductivesuccess in the Splen- birds. Long-termstudies of ecologyand behav- did Fairy-Wren(Malurus 'splendens). Behavioral ior (P. B. Staceyand W. D. Koenig, Eds.). Cam- Ecologyand Sociobiology22:131-140. bridge University Press, Cambridge, United SKUTCH,A. E 1960. Life histories of Central Ameri- Kingdom. can birds. II. Pacific Coast Avifauna No. 34. ZAIAS,J., AND g. BREITWISCH.1989. Intra-pair coop- SKUTCH,A. E 1961.Helpers among birds. Condor 63: eration,fledgling care, and renestingby North- 198-226. ern Mockingbirds(Mimus polyglottus). Ethology STACEY,P. g., AND W. D. KOENIG.1990. Cooperative 80:94-110. breedingin birds. Long-termstudies in ecology Associate Editor: K. Martin