Brood Reduction and Siblicide in Black-Billed Magpies (Pica Pica)

The Auk 113(1):189-199, 1996

BROOD REDUCTION AND SIBLICIDE IN BLACK-BILLED MAGPIES (PICA PICA)

P. S. REYNOLDS Divisionof BiologicalSciences, University of Montana,Missoula, Montana 59812, USA

ABSTR•CT.--Inmany avian species,brood reduction is consideredto be adaptive and may be attributed either to sibling competition (passivestarvation, active sibling aggression)or parentaleffects (manipulation of hatching spread,active infanticide). However, nonadaptive factorssuch as environmentaleffects, may contributesubstantially to nestling mortality. I determinedmechanisms of brood reductionand survivalprobabilities of nestlingBlack-billed Magpies(Pica pica) in relation to intraclutchegg-size variation, brood size, nestlingage and size, and weather. Median brood survival time was weakly, but positively, correlatedwith intraclutchegg-mass variation. Starvationaccounted for most nestlingmortality within the first 9 daysposthatching, although 12 deadand moribund nestlingswere found badly bruised around the head. Siblicide and sibling cannibalismwere observedin two broodsand implicated in the deaths of nestlings in three other broods. Siblicidal events occurred when nestlingswere between 15 and 20 daysold. Expectedmedian survival times and probability of survival to fledging of nestlingswas not linearly related to brood size at hatching,being highest for broods of five, lowest for broods of three, and intermediate for broods of four and six.Dead nestlingswere smallerand lighter than survivingsiblings at any age;however, asymptoticbody massand linear measurementswere negativelycorrelated with brood size at fledging.The probabilityof mortality wasaffected by prevailing weatherconditions; rain and low temperaturesdoubled the estimatedrisk of deathfor young nestlings,independent of brood size. Thesedata suggestthat factorsinfluencing the occurrenceand maintenance of brood-reductionstrategies in a populationmay be morecomplex than previouslythought. Brood-reductionmechanisms are affectedby the interactionof biotic and abioticfactors, and may vary in responseto factorsoutside of either parentalor offspringcontrol. Received 9 September1994, accepted 25 April 1995.

IN MANY SPECIESof birds, brood reduction can 1976,Clark and Wilson 1981,Husby 1986,Mock be attributed to starvationof the youngestor 1994). In particular, hatching asynchronywas weakest nestlings in a brood; this may be re- interpretedby Lack (1954, 1968)as an adaptive garded as a type of passivesibling competition mechanismfor producing marginal offspring. (Lack 1954, 1968, Ricklefs 1965, Clark and Wil- Because hatch order determines size differences son 1981,Mock 1994).Brood reduction also may between siblings, and the relative size differ- result from direct sibling aggression,in which encesbetween young in a brood contribute to "marginal" young are killed by siblings(Mey- competitive outcome, this leads to the second burg 1974, Edwards and Collopy 1983, Mock assumption,namely, that mechanismsof brood 1985,1994, Stanback and Koenig 1992).Parental reduction should be directed towards the small- manipulation of hatching spread (hatching est and weakest brood members.Finally, food asynchrony)may influence both the occurrence supply is assumedto be the critical factor lim- and outcomeof sibling competition by gener- iting nestling survival. Sibling competition is ating competitively--disadvantagedoffspring expectedto increasein importancewhen there (Lack1954, 1968, Mock 1994);additionally, par- are major discrepanciesbetween food supply entsmay directly manipulatebrood size by kill- and offspringdemand. Total offspringdemand ing young (Stanbackand Koenig 1992). will increaseboth with brood size and nestling There are at least three basicassumptions in- age; thus, becauseof the relative increaseof herentto manymodels of broodreduction. First, potential competitors,nestlings in large broods both brood reductionand hatching asynchrony may be proportionately more restricted in ac- are assumed to be adaptive, inasmuch as the cess to food than those in smaller broods. decrease of the brood to a size which can be fed Becauseadaptive explanationsfor brood-re- results in the maximization of the number of duction mechanisms have received most atten- viable young fledged (Lack 1954, 1968, Howe tion, the effectsof nonadaptivefactors on brood 189 190 ?. s. REYNOLDS [Auk,Vol. 113 loss have rarely been considered. However, METHODS breedingsuccess and nestlingsurvival for many I studiedbreeding Black-billedMagpies in Missou- birds are strongly affected by environmental la County, Montana (46ø55'N 114ø6'W,elevation 973 factors(Murphy 1985).Extremes in temperature m), from late March to late June 1994. I measured and rainfall will significantly impact nesting length and width of 118eggs in 25 completeclutches successof many speciesof birds by depressing to the nearest0.01 mm with digital calipers.I obtained insectavailability, therefore affecting the major morphometricdata for a total of 110 nestlingsfrom food sourcefor nestlings and curtailing avail- 22 broodsevery two days from hatch to fledging or able foraging time (Lack 1954). Ambient con- death/disappearance.Nestlings were individually ditionsalso may affectnestlings directly. When marked with nontoxic permanent marker on the un- ambienttemperatures are low, young nestlings dersideof the manusand tarsusuntil old enoughto color band. I measuredlength of head, culmen,ma- may show thermoregulatorycompromise and rius, and tarsus,to the nearest0.01 mm with digital chilling independent of brood size (Hill and calipers;body masswas measuredwith Pesolascales. Beaver1982); very high-temperatureand solar- Whenever possible,dead young were collected,mea- radiationloads also may be implicatedin deaths suredand examinedfor injuries.When nestlingsdis- of exposednestlings (Murphy 1985). Thus, the appearedbetween censusdays, I used data obtained incidenceand timing of brood-reductionmech- during the last censusday young were seenalive in anismsmay be the result of nonadaptivecon- comparisonswith surviving young on that day. I ob- straintson individuals,rather than purely adap- taineddaily weatherdata from the National Weather tive responsesto current conditions. Service, Missoula; the weather station was within a radiusof 2 km of the study sites. In this paper, ! present data on patternsand Mortality.--I examined the effectsof biotic and abi- probability of nestling mortality for the Black- otic factorson nestlinglifetime using survival anal- billed Magpie (Picapica). Magpie clutch size is ysis.The key featureof survivalanalysis which dis- unusually large in comparisonto most corv- tinguishesit from other typesof statisticalanalysis is ids--clutchesgenerally average six to eight eggs, that it handles "censored"data. Censoring occurs in contrastto the three to five egg clutch char- when certain individuals cannot be observed for their acteristicof many corvidspecies (Goodwin 1986, entire lifetime, and the event of interest(in this case, Birkhead1991). However, magpiesrarely fledge death) has not occurred within the duration of the more than two to four young (HSgstedt1981, study;thus, exactsurvival times are known only for Goodwin 1986, Buitron 1988, Birkhead 1991). a certainsubset of the studypopulation. Survival dis- I examined the combined effects of three bio- tributionsand instantaneousprobability of deathwere modelled by survival functions S(t) and the cumu- logical factors (nestling age, brood size, and lative hazard function h(t); thesefunctions are related within-brood nestling-size differences) and to each other by h(t) = -log S(t) (Lawless1982). severalweather variableson the probabilities I usedthe Kaplan-Meier, or product-limit, survival and distribution of nestling survival over the estimator (Kaplan and Meier 1958) to estimate the nesting period. I compared the relative influ- cumulativesurvival probabilitiesof nestlingsfrom ence of these factors on the incidence of two different brood sizesat hatch. The Kaplan-Meier es- major types of brood-reductionmechanisms-- timator is given as: starvation and siblicide. Starvation has been demonstratedexperimentally to be a majorfac- õ(t)=h n,-d,, (1) tor in magpienestling mortality (HSgstedt 1981, Hochachkaand Boag1987); however, siblicide where n• is the number of nestlingsalive at the be- ginning of a given time interval (specifiedas t•_• to and sibling cannibalismhave not been previ- t•),and di is the numberof nestlingsthat died during ouslyreported for magpies(or, in fact,for any that interval. The standard error of S(t) is: other passerinespecies). The occurrenceof both brood-reductionmechanisms in the samepop- SE[g(t)]= S(t) ((d,)/[n,(n,- d,)])0.s (2) ulation, and even within a single nest,suggests that factorsinfluencing the both the incidence and the timing of specific brood-reduction (Kaplan and Meier 1958, Lawless 1982, White and Garrott 1990). The median survival time is the first mechanismsmay be more complexthan pre- observed time when the cumulative survival is 50% viously thought. Brood-reductionmechanisms or less. are affectedby the interactionof bioticand abi- I usedpairwise log-rank tests(Lawless 1982) to test otic factors,and may vary in responseto factors the null hypothesisthat survival did not differ be- outsideof either parentalor offspringcontrol. tween sizesof brood at hatching.The test statisticis January1996] MagpieBrood Reduction 191

selectedfor in magpiesand other speciescharacter- U= • [do•,(i)- d,xp(i)], (3) ized by large clutchsizes, hatching asynchrony, and broodreduction (Slagsvoid et al. 1984).Unfortunate- wheredobs(i) and dex•(i) are the observedand expected ly, it wasnot possibleto obtainprecise measurements numberof deaths,respectively, at eachtime interval of hatchling massfor the majority of nestlings,nor i. The probabilitylevels were multiplied by the num- could I matcheach egg with a specificnestling once ber of comparisonsmade (Bonferroni'scorrection) to hatched.I estimatedegg mass Me• from the formula adjust the significancelevels for multiple compari- •r(LW•)/6 (where L is egglength and W is egg width), sons (Neter et al. 1985). andintraclutch egg-size variation from the coefficient I assessed the relative influence of environmental of variationof eggmass (CV = SD/averageegg mass) variableson nestlingsurvival times with Cox,or pro- for each brood. I assessed the association of intra- portionalhazards, regression (Cox 1972, Lawless 1982, clutchegg mass variation (ln CV) with medianbrood- White and Garrott1990). The generalform of the Cox survivaltime by the survival function regressionmodel usedwas: S(t IX) = So(t)•, (6) h(t) = [ho(t)]e•...... x•...... x,•, (4) where g is e•x, B is the regressioncoefficient, and X where h(t) is the hazard function, or the instanta- is (In CV). neousprobability of deathat time t, hois the baseline I evaluateddifferences in bodymass and four linear probabilityof death,B• throughBp are the regression variables (head, culmen, manus, and tarsus) between coefficients,and X• throughX• are the predictorvari- surviving and dead young for three age classes.Age ables.Variables with positiveregression coefficients classeswere defined as: (age classI) days 0-8 (rapid are associated with decreased survival times, whereas growth phase);(age classII) days 9-15 (commence- variableswith negativecoefficients are associatedwith ment of feathergrowth and beginningof thermoreg- increasedsurvival times. The percentagechange in ulatory competence);and (age classIII) days 16-24 the hazardrate for a unit changein a given predictor (asymptoticgrowth phase).Morphometric data were variable is calculatedas e•. For binary variables, e• is analyzedby multivariateANOVA (linear measure- the relative risk, or the ratio of the estimated hazard mentsonly) and univariatet-tests. Because the alter- for a case when the factor occurs to that for a case nativehypothesis of interestis that survivingyoung when the factor is absent. are larger than dead young in a given age class,uni- I considered the effects of brood size at hatch and variate tests were one-tailed. Data were log,-trans- five environmental variables:maximum daily tem- formed before analysisto meet normality and ho- perature (TMAX, øC), minimum daily temperature moscedasticityassumptions (Steel and Tottie 1980, (TMIN, øC),total daily sunshine(SUN, min), wind Johnson and Wichern 1982). Association between speed(WIND, km/h), and precipitation (PRECIP;no brood size at fledging and asymptoticvalues of the = 0, yes = 1). I fitted separateregression models to five morphometricvariables were assessedby corre- data for four nestlingages: day of hatching (day 0), lation. day 5, day 10 (the postulatedage of thermoregulatory Siblicidal broods were designatedas broods for competence for medium-sized altricial birds; Dunn which at least one siblicidal event, defined as the 1975),and day 20. Predictorvariables were selected severephysical wounding or killing of a broodmem- for inclusionin the model for eachnestling age class ber, could be documented (Mock 1994). To determine by backwardsselection (Draper and Smith 1981),with if disruptionof growth was associatedwith the in- the criterion for removal based on the conditional- cidence of siblicide in a brood, I compared mass likelihood estimates of the likelihood-ratio statistic changesof individualnestlings from siblicidalbroods and observedsignificance level of 0.1 (Norusis1993). to that for nestlingsfrom nonsiblicidalbroods for The partial correlationr• of the estimateddeath rate which at least two members survived to day 24. I with eachindependent variable was calculated by the eliminated autocorrelation between consecutive ob- relation: servationsby calculatingordinary first differences between observations (Neter et al. 1985). I then calcu- r• = +([W - (2df)]/(-2LL))% (5) lated averagemass change and the respectivestan- where W is the Wald statistic(distributed as chi square), dard deviation from these differenced observations; df is degreesof freedomfor the coefficient,and LL is standard deviations were log•-transformedbefore the log-likelihoodfor the initial model (Norusis1993). analysis.These calculationswere performedsepa- I used chi-squaretests to assesswhether the pro- ratelyfor ageclasses II and III. I testedwhether mass portion of young fledgedwas associatedwith brood gain and variationin massgain differedbetween sib- size at hatching. licidal and nonsiblicidalbroods and betweenage class Morphometrics.--Eggmass is correlatedwith both by two-factorANOVA. hatchling massand the probability of nestling sur- Significancetests were specifiedfor an a of 0.05; vival (Howe 1976,Slagsvoid et al. 1984,Birkhead 1991). the power of the test (the probability of correctly Increasedintraclutch variation in egg size may be rejectinga falsenull hypothesisof no differencebe- 192 P. $. REYNOLDS [Auk,Vol. 113 tween groups)was given by 1 - fl (Steel and Tottie 14 1981). All statisticalprocedures were performed in A. BeforeHatching SPSS for Windows (Norusis 1993). 12

RESULTS 10

Causesof death.--In six instances,the entire 8 brood (brood size, œ= 4.5 + 0.5) disappeared simultaneously;in thesecases, young were less 6 than 15 days old. Lossof two completebroods was due to predation by Common Ravens(Cor- 4 vus corax). Partial brood loss occurred in 18 of the remaining 19 broods;62 of 117 nestlings 2 died or disappearedfrom time of hatching to time of fledging. 0 When cause of death could be determined, 2 3 4 5 6 7 8 9 nonpredation nestling mortality usually could be attributed to either starvation (i.e. a consis- Clutch Size tent failure to gain massand progressiveema- 14 ciation) or siblicide (i.e. where at least one nest- B. At Hatching ling in a brood was injured or killed by nest 12 mates;Mock 1994). Two nestlingsapparently chokedto deathon food itemstoo largeto swal- 10 low. Starvation accounted for at least 30 deaths. "Starvelings" tended to hatch between one to o' three dayslater than survivors.Most starvelings E 6 (n = 25) died before day 16 posthatching;four u. young hatched more than two days after other brood membersdied within three daysof hatching. Extensivebruising on the head and nape was noted for 12 dead or moribund starvelings in nine broods;these injuries were noted only o for very young nestlings(i.e. during the first 2 3 4 5 6 7 8 9 nine daysposthatching). Siblicide was implicated in the deaths of at Brood Size leastfive nestlingsin two broods,and possibly Fig. 1. Frequenciesof (A) clutch size and (B) brood in the deaths of nestlings in three other nests size at hatching for Black-billedMagpies. (Appendix). Severe laceration injuries were noted for nine nestlingsin these five broods; these injuries were observedon the lateral and for broodsof threewas significantlylower than synsacralareas and upper thigh, and occasion- that for broods of five (U = 17.06, P < 0.001) ally resultedin penetration of the visceralcav- and six (U = 8.43, P = 0.037); all remaining ity, and disembowelling.Siblicidal episodesoc- comparisonswere not statisticallysignificant (P curredin broodswhere nestlingswere between > 0.2). The probability of a nestling surviving 15 and 24 daysof age. to fledgingage was approximately 0.63 for nest- Survival and brood size.--Mean clutch size was lingsfrom broodsof five, 0.42for broodsof four, 6.4 + SD of 1.0 for 25 broods; brood size av- six,and seven,and 0.00 for broodsof three (Fig. eraged4.7 + 1.5 young at the time of hatching 2A). Median survival time was longest(21 days) (Fig. 1). for broods of five, and shortest(8.7 days) for The Kaplan-Meier cumulative survival func- broods of three; intermediate median survival tions indicated that brood size at hatching in- times (15 to 17 days) were exhibited by broods fluenced nestling survival of magpiesin this of four, six, and sevenyoung at hatching (Fig. population (Fig. 2A). The survival distribution 2B). January1996] MagpieBrood Reduction 193

1.1 given in Table 1 (if criteriafor model inclusion 1.0 were not met, variables were omitted from table). The incidence of rainfall (PRECIP) was the 0.9 predominantinfluence on early nestling mor- 0.8 tality; the estimated risk of death was twice as 0.7 great for nestlingsif rain occurredon day of hatchingand at day 5, beforethe presumedage 0.6 of thermoregulatorycompetence. An increase o.5 in the minimum daily temperature(TMIN) re- 0.4 ducedestimated risk by 22%for 5-day-old nest- 0.3 lingsand by 49%for 20-day-oldnestlings. Wind significantlyaffected survival of day-10 nest- 0.2 lings; estimatedrisk increasedby 1.3 times on 0.1 windy days. 0.0 Survivaland morphometrics.--Increasedintra- 0 4 8 12 18 20 24 28 clutch variation in egg mass(In CV) was posi- Age (days) tively, but weakly, associatedwith estimated brood survival time (r = 0.19, B = -2.006 + SE 30 of 0.979,P = 0.040;Fig. 3). Hatching intervals between the averagefor • 25 (25) the clutch and the last-hatchedyoung varied T (14) between one to three days. Starvelingswere ;' 20 always the last-hatchedand/or penultimate nestlingsin a brood,always grew more slowly than older nest mates, and were smaller and • 15 (32• lighter in massthan survivingnest mates at the time of death (Fig. 4A). ._• • lO Young dying beforeday 9 (age classI) were significantlysmaller in linear dimensionsthan survivors (P < 0.025, and [1 - /•] > 0.63 in all 2 3 4 5 6 7 8 cases);however, the multivariate test on all four linear variables did not result in statistically BroodSize At Hatching significantdifferences between groups (Hotell- Fig. 2. Effectsof broodsize at hatchingon survival ing's T• = 0.230,df = 4 and 29, P = 0.184,[1 - of Black-billedMagpie nestlings.(A) Kaplan-Meier /•] = 0.59). The massof dead young was signif- estimatesof cumulativesurvival probability; (B) median survivaltime of individualnestlings. Error bars icantly lessthan that of survivors(P = 0.010,[1 represent95% confidenceintervals; number of nest- - /•] = 0.76; Table 2). lings shown in parentheses. For nestlings of age classII, there were no statisticallysignificant differences in linear dimensions (T • = 1.304, df = 4 and 5, P = 0.300, An averageof 2.1 + 2.0 young in 15 broods [1 -/•] = 0.39; univariate tests,P > 0.40 and [1 survived to day 24. No young fledged from -/•] > 0.40) or body mass(P = 0.373) between broodsof sizethree at hatching(n = 3 broods). survivorsand dead young. There was no statisticallysignificant effect of For nestlingsof ageclass III, the massof dead broodsize on the proportionof youngfledged young was significantlyless than that of sur- from larger broods(X 2 = 2.45, df = 3, P > 0.2). vivors (P = 0.032, [1 -/•] = 0.72). However dead Survival and weather.--The probability of nestlingsdid not differ statisticallyfrom sur- nestling death was affectedstrongly by envi- vivors in linear dimensions (T • = 0.207, df = 4 ronmentalvariables, independent of broodsize and 13, P = 0.622, [1 - /•] = 0.37; univariate (P > 0.2). The relative influence of weather on tests,P > 0.1 and [1 - /•] > 0.55; Table 2). nestlingsurvival declined with increasingnest- Nestlingsin siblicidalbroods were charac- ling age.Cox regressionmodels describing the terizedby a periodof fluctuatingmass gain and association of various environmental variables lossprior to the deathof a sibling (Fig. 4B and with the probability of nestling mortality are Table 3). Variation in masswas significantly 194 P. $. REYNOLDS [Auk,Vol. 113

T^BLE1. Parameterestimates and associationof environmentalvariables with the probabilityof survivalof nestling Black-billedMagpies, as determined by Cox regression.

Variables B' SE (B) eB P Day of hatching (n• = 110; -2 log likelihood = 501.079,P < 0.001) TMIN - 0. ! 10 0.047 0.896 - 0.080 0.020 PRECIP 0.777 0.180 2.175 0.177 <0.00! WIND -0.205 0.1!2 0.815 -0.050 0.068 Day 5 (n = 107; -2 log likelihood = 485.437,P < 0.001) TMAX -0.173 0.037 0.84! -0.199 <0.001 TMIN -0.247 0.064 0.781 -0.157 <0.001 PRECIP 0.752 0.194 2.120 0.159 <0.001 Day 10 (n = 87; -2 log likelihood = 344.330,P = 0.062) WIND 0.246 0.!33 !.279 0.064 0.064 Day 20 (n = 52; -2 log likelihood = 24.707,P = 0.041) TMIN -0.670 0.337 0.512 -0.248 0.047

ßCox regressioncoefficient. bPartial correlation of independentvariable with expecteddeath rate at time t. c Number of nestlingsat each age. greaterin siblicidalbroods as compared to non- Averagemass of nestlingssurviving to 24 days siblicidal broods (F = 8.47, P = 0.005), and was of agewas negatively correlated with broodsize significantly greater in younger (age classII) at fledge (r = -0.70, P < 0.01, n = 15 broods). nestlings(F -- 38.12, P < 0.001). In contrast, There wasa negativeassociation between linear averagemass gain did not differ between sib- measurementsand broodsize at fledging;how- licidal and nonsiblicidal broods for either age ever, correlations were too weak for statistical class(F = 1.00, P = 0.321). As expected,mass significance(head length, r = -0.25; culmen gained by younger (age classII) nestlingsthat length, r = -0.21; manus length, r = -0.44; are still growing was significantlygreater (F = tarsuslength, r = -0.29). 101.24,P < 0.001) than that of older nestlings, which were approachingthe growth asymp- DISCUSSION tote. For Black-billedMagpies in my study, there

3o was variation within a single nest, as well as within the population as a whole, in both the incidenceand the timing of specifictypes of

• 25 ß brood-reduction.Both starvation (passivesibling competition)and siblicide(active and ag- gressivesibling competition)were implicated in nestling mortality, as were certain modesof parental control, such as egg-size variation, ß ß hatchingasynchrony, and possiblyinfanticide. However, the significantimpact of abiotic fac- ß ß torson nestlingmortality, independent of brood size, suggestedthat brood reduction was not ß necessarilyunder the direct control of either r=0.19 offspringor parents.Although broodreduction refers specificallyto adaptive mechanismscon- trolling brood size (Mock 1994), probabilities 0.01 0.02 0.03 0.04 0.05 0.06 0.07 0.08 of nestling survival may be equally influenced IntraclutchEgg-mass Variation by nonadaptivefactors, such as weather. Fig. 3. Association of median brood survival time Parental control of brood reduction is man- and intraclutch egg-sizevariation for 22 Black-billed ifested by active infanticide (Trail et aL 1981, Magpie broods. Stanbackand Koenig 1992), as well as by vari- January1996] MagpieBrood Reduction 195

250 TABLE2. Mean morphologicalmeasurements (+ SD) A for surviving and dead Black-billed Magpie nestlings in age classes:(I) ages0 to 8 days;(II) ages9 200 - to 15 days;and (III) ages 16 to 24 days.

Variable Survived Died 150- Age classI (n• = 34) Head (mm) 33.21 + 6.46 29.61 + 8.89 0.019 100- Culmen (mm) 13.02 + 2.88 10.65 + 3.08 0.024 Manus (mm) 19.70 + 6.47 14.95 + 6.26 0.021 Tarsus (mm) 21.90 + 7.17 15.99 + 6.72 0.014 Mass (g) 51.1 + 25.3 30.3 + 26.4 0.010 Age classII (n = 10) Head (mm) 43.78 + 5.96 41.29 + 8.59 0.550 0 Culmen (mm) 17.52 + 2.43 17.03 + 4.00 0.731 '1' 8 12 16 2 24 28 Manus (mm) 33.13 + 7.39 28.86 + 11.50 0.406 250 Tarsus (mm) 34.41 + 5.98 30.60 + 9.41 0.402 Mass (g) 95.8 + 32.8 78.4 + 44.4 0.373 B Age classIII (n = 10) 2OO Head (mm) 58.51 + 3.83 56.35 + 4.26 0.266 Culmen (ram) 24.00 + 2.32 22.99 + 2.34 0.372 Manus (mm) 48.16 + 1.83 45.52 + 3.89 0.089 Tarsus (mm) 47.72 + 1.52 46.53 + 2.44 0.230 • 150 Mass (g) 169.4 + 14.2 145.9 + 24.1 0.032 ßProbability obtained from one-tailed t-tests on 1og•-transformed variables. • Numberof comparisonsfor deadyoung and averagefor surviving / siblingsin a brood.

of young has been observed in other corvid 0 species;for example, adult female Pition Jays 28 (Gymnorhinuscyanocephala) have been observed Age (days) to kill and eat their own hatchlings(Balda and Fig. 4. Pa•erns of body m• g•n in magpiebroo• Bateman1976). However, the bruisingobserved •pifying broodreduction through either sta•ation on the heads of young magpie nestlings is or siblicide. Solid lines indicate young su•i•ng to equally consistentwith observationsthat the day 24; dottedlines indicateyoung dying beforeday female encouragesnestling beggingresponse 24; arrows indicate time of hatching. (A) Brood re- by tapping nestlings on the head (Goodwin duction through sta•ation of the youngestnestling. The deadnestling hatched •o daysafter its su•iving 1986), and by attempts to force feed young nest•tes. (B) Br•d reduc•on t•ough siblicide;note (Bengtssonand Ryden 1981).It is possiblethat fluc•ating m•s gain and lossin week prior to nestling death. TABLE3. Massgain (g) and variability (g; SD) in mass gain in Black-billedMagpie nestlingsfrom siblicidal and nonsiblicidal broods. ation in egg size within a clutch (Slagsvoidet al. 1984) and hatching asynchrony(Lack 1954, Brood status a 1968, Ricklefs 1965, Mock 1994). Parental ma- Non- nipulationof broodsize may increaseparental Variable siblicidal Siblicidal fitnessby affectingboth the number of young Age classII survivingto fledgingand the numberof young Average masschange 9.5 9.6 surviving to independence(Husby 1986). Variation in masschange 10.3 17.0 It was not possibleto determineif adult mag- Age classIII pies deliberatelykilled young. However, direct Average masschange 3.8 1.8 parental involvement in early nestling mortal- Variation in masschange 7.1 6.8 ity was suggestedby injuries observedfor 12 ßFor nonsiblicidalbroods, n = 31 (nine broods).For siblicidal broods, nestlingsunder nine daysof age.Active killing n = 12 (five broods). 196 P.s. REYNOLDS [Auk, Vol. 113 more intense efforts to stimulate a weak or mor- At this time, linear size differences between ibund nestling could kill it. magpiesiblings were relativelysmall, although Differencesin nestling size may be initiated large massdiscrepancies still existed between by differencesin egg size within a clutch; a surviving and dead young. However, the in- relationship between egg size, initial nestling teractionbetween brood size, nestling age, and size differencesand concomitantnestling sur- environmental factors on the outcome of sib- vival have been demonstrated for Snow Geese ling competition and probability of nestling (Chencaerulescens; Ankney 1980),as well ascer- survivalsuggests that there is no explicitcause- tain passerinespecies (O'Connor 1975, 1979). and-effectrelationship. The relationship between intraclutch egg size Morphologicaldata suggested that young that variation and nestling survival is suggestedby are smaller than their siblings are lesslikely to comparative eagle data; those speciescharac- survive to fledging. The differencesin linear terized by obligate siblicide showed a greater measurementsbetween surviving and dead degree of intraclutch variation than speciesex- youngwere not statisticallysignificant for age hibiting facultativesiblicide (Edwards and Col- classes II and III; however, failure to detect dif- lopy 1983). In magpies,intraclutch egg-mass ferences in at least some of these comparisons variationwas positively,although weakly, cor- may be partially attributedto the low statistical related with median brood survival time. This power (1 - fi) of the tests.Statistical power is observationis consistentwith Slagvoidet al.'s determinedby the magnitudeof the difference (1984) conceptof a brood reduction "strategy," between groups,sample size, and samplevari- which hypothesizesthat increasedvariation in ability. The magnitudeof the differencesin ma- egg size within clutchesmay be selectedfor in nus length, tarsuslength (ca.4 ram), and body specieswith a high incidenceof nestling mor- mass(17 g) for surviving and dead age classII tality from starvation. young (Table 2) may be biologicallyimportant; Initial size differencesbetween nestlingsare however, small sample sizes and large vari- further exaggeratedby the spreadin hatching ability precluded statistical detection. In con- times inducedby asynchronoushatching. In all trast, the smaller (1 to 2 mm) differences ob- speciesobserved to date, early mortality from servedlinear measurementsof ageclass III nest- starvationis influenced by the size hierarchy lings are lesslikely to influence the probability determinedby hatching order within a brood; of nestling mortality. Controlled growth ex- this effect is exacerbatedwhen parental food periments are required to determine the prac- delivery rates are inadequate (Bryant 1978). tical significance (DeVore 1987) of morpho- Starvation has been demonstrated experimen- metric differencesin relation to nestling risk of tally to be the majorfactor contributing to early mortality. nestling mortality of magpies(Hfgstedt 1981, Overall size differencesamong nestlingsare Hochachkaand Boag 1987). In my study, star- not the only factor influencing the occurrence vation of the youngestand weakestyoung oc- of sibling competition.Experimental food sup- curredprimarily during the firstnine dayspost- plementation has been demonstrated to in- hatching, as has been observed in previous crease average number of young magpies studies(Hfgstedt 1981,Tatner 1984, H ochachka fledgedper brood (Hochachkaand Boag1987, and Boag 1987, Birkhead 1991). When active Dhindsa and Boag 1990). In this study, both siblicidehas been implicatedin nestling deaths, nestling massloss and death were associated the victim is invariably the smallestand weak- primarily with coldand wet weather.Although estnestling in the brood (Ingram 1959,Fujioka I did not collect data on food availability or 1985).However, the timing of siblicidalevents parental delivery rates, it is reasonableto as- may be related to the biology of the speciesin sume that insect availability was greatly re- question.In semialtricialspecies, siblicide gen- duced and constraintson parental food delivery erally occursshortly after hatchingof the small- rates,therefore, could contributeto nestling est young (Ingram 1959, Meyburg 1974, Bor- mortality. Fluctuationsin prey densitieshave tolotti et al. 1991); in these species,motor con- beenshown to significantlyinfluence nestling trol is establishedshortly after hatching.In con- survival of American Kestrels(Falco sparverius) trast,siblicide in magpiesappears to occuronly and othersmall raptors independently of brood during the lasttrimester of the nestlingperiod, size, supporting the hypothesisthat parental when motor coordination was well established. ability to feed young is the predominantfactor January1996] MagpieBrood Reduction 197 limiting brood size at fledging (Gard and Bird on the corvid bill is appropriate for grasping 1992). and pinchingoff piecesof tissue,although it is Foodsupply alsomay influencethe incidence not specificallyadapted as a penetratingweap- of nestling mortality due to sibling aggression. on (Rowley 1970). Magpies apparently killed Although there are few experimentaldata to siblingsby peckingand tearingat the relatively stronglysupport the role of nestlinghunger as thin, unfeathered skin on the flanks and dot- a proximate factor inducing siblicide (Mock sum;this behavioroccurred only during the last 1985), relative food supply has been observed week of the nestling period. If siblicide only to affect ratesof siblicide in small raptors(Bor- occursin magpiesduring the late nestling pe- tolotti et al. 1991) and Black-leggedKittiwakes riod under conditions of limited food, the (Rissatrydactyla; Braun and Hunt 1983).The rate chancesof observingthis behavioron a regular of siblicidein kittiwakessignificantly increased basis are low. after extended periods of inclement weather Fledgingsuccess was influencedby brood size; (Braunand Hunt 1983). For speciesexhibiting broodsnumbering five young at hatchinghad obligate siblicide, food shortageis not a nec- a substantiallyhigher probabilityof fledgingat essarycondition inducing siblicide, nor does least one young than did smaller or larger food supplementationappear to influencelev- broods.However, fledgling size (massand lin- els of nestling aggression.Instead, it appears ear measurements)was negatively correlated that lethal levels of aggressionare selectedfor with brood size. Similar results have been dem- if food is deliveredto young in monopolizable, onstrated experimentally for both American small units (Mock 1985).Magpies would appear Kestrels(Gard and Bird 1992)and Collared Fly- to meetboth the prey-sizecriteria (small, mon- catchers (Fideculaalbicollis; Gustafsson and Suth- opolizable food items delivered directly in a erland 1988); more young fledged from en- bolus)and morphologicalcriteria (tearing bill, larged broods,but fledgling size was smaller. peckingresponse, and motor coordination)nec- In Collared Flycatchers,the main cost of en- essaryfor siblicideto occur.However, it is like- largedclutches appeared to be increasedjuve- ly that siblicidalattacks in magpiesare precip- nile mortality and, therefore, reduced second- itated by inadequate food delivery rates; the generation recruitment (Gustafssonand Suth- wide variation in massgain exhibitedby mag- erland 1988).There is someevidence to suggest pie nestlingsin siblicidal broodssupports this that larger and heavier magpie nestlingshave contention. a higher probability of surviving at least the Siblicide(which runs the gamut from active first few monthsafter fledging(Birkhead 1991). fighting between nestlingsto cannibalism)oc- Thus, there is a complexinteraction of factors cursrelatively lessfrequently than other mech- governingthe probabilityof survival to fledg- anisms of brood reduction. To date, siblicide ing and factorsinfluencing the probability of andsibling cannibalism have been reported pri- survival after fledging.The situationis further marily for hawks,owls, and ardeidsand not for complicatedby year-to-yearvariations in en- any passerine species (Stanback and Koenig vironmental conditionsand, by inference, food 1992).Both sibling aggressionand cannibalism supplyand delivery rates.In AmericanKestrels, might be expectedin any speciesthat dismem- low prey densitieswere associatedwith higher bers food items, regardlessof the averagesize nestling mortality regardlessof nestling body of prey deliveredto young (Bortolottiet al. 1991); size and brood size; significant between-year siblicide in passetinesmight be expected dur- effectsconfounded the effectsof experimental ing the period in the nestlingstage when food brood-sizemanipulations (Gard and Bird 1992). demandsare greatestand motor coordination Variation in probabilitiesof nestlingsurvival is established.For magpies, siblicide and sibling are influenced by the effectsof ambient tem- cannibalismhave not beenreported previously, peratureand precipitation.In other species,en- although cannibalistic behavior of adults di- vironmentaleffects are associatedwith impacts rectedat another adult conspecifichas been ob- on nestling size and survival, and may be in- served(Crease 1992). Magpies are primarily in- duced either by direct effectsof exposureon sectivorous,but will opportunisticallytake oth- unprotected nestlings,or indirectly by effects er animal foods. In common with other corvid on food supply (Murphy 1985).The interaction species,magpies dismember prey itemstoo large of ambientconditions with (presumably)adap- to swallow (Goodwin 1986). The terminal hook tive phenotypictraits characteristic of broodre- 198 P.S. REYNOLDS [Auk,Vol. 113 duction suggeststhe potential confoundingof DRAPER,N. R., ANDH. SMITH. 1981. Applied regres- evolutionary and nonevolutionary processes. sion analysis.John Wiley & Sons,New York. These considerationswill have important im- DuNN, E.H. 1975. The timing of endothermyin the plications for future determinations of brood developmentof altricial birds. Condor 77:288- 293. reduction strategiesin wild populations. EDWARDS,T. C., JR., AND M. W. COLLOPY. 1983. Ob- ligate and facultativebrood reduction in eagles: ACKNOWLEDGMENTS An examination of factors that influence fratri- cide. Auk 100:630-635. I thank F. Bucknam, C. Wright, T. and J. K. Lloyd, FUJIOKA,M. 1985. Sibling competitionand siblicide and J.and C. Shepardfor permissionto work on their in asynchronously-hatchingbroods of the Cattle land. I am grateful to R. Bowlds, R. M. Lee III, P. Egret Bubulcusibis. Anim. Behav. 33:1228-1242. Ziegler, and especiallyJ. K. Lloyd and J. R. Lloyd for GARD,N. W., ANDD. M. BIRD. 1992. Nestling growth field assistance.I thank P. Kukuk for key references, and fledging successin manipulatedAmerican and R. M. Lee III and severalanonymous reviewers Kestrel broods. Can J. Zool. 70:2421-2425. for valuable commentsand suggestionsthat greatly GOODWIN, D. 1986. Crows of the world, 2nd ed. improved the manuscript. Univ. WashingtonPress, Seattle. GUSTAFSSON,L., AND W. J. SUTHERLAND. 1988. The LITERATURE CITED costsof reproductionin the Collared Flycatcher Fidecula albicollis. Nature 335:813-815. ANKNEY,C.D. 1980. Egg weight, survival and growth HILL, R. W., AND D. L. BEAVER. 1982. Inertial ther- of LesserSnow Goosegoslings. J. Wildl. Manage. mostability and thermoregulation in broods of 44:174-182. Redwing Blackbirds.Physiol. Zool. 55:250-266. BALDA,R. P., AND G. C. BATEMAN. 1976. Cannibalism HOCHACHKA,W., AND D. BOAG 1987. Food shortage in the Pition Jay.Condor 78:562-564. for the Black-billed Magpie Picapica: An exper- BENGTSSON,H., AND O. RYDEN. 1981. Development iment using supplementalfood. Can. J. Zool. 65: of parent-young interaction in asynchronously 1270-1274. hatchedbroods of altricial young. Z. Tierpsych. HbGSTEDT,G. 1981. Effect of additional food on re- 56:255-272. productive successin the Magpie (Pica pica). J. BIRKHEAD,T. 1991. The Magpies. T & A D Poyser, Anim. Ecol. 50:219-229. London. HOWE,H. F. 1976. Egg size, hatching asynchrony, BORTOLOTTI,G. R., K. L. WIœBœ,AND W. M. IKO. 1991. sex, and brood reduction in the Common Grackle. Cannibalism of nestling American Kestrelsby Ecology57:1195-1207. their parentsand siblings.Can. J. Zool. 69:1447- HusI•Y, M. 1986. On the adaptive value of brood 1453. reductionin birds:Experiments with the Magpie BI•UN, B. M., AND G. L. HUNT, JR. 1983. Brood re- Pica pica.J. Anim. Ecol. 55:75-83. duction in Black-leggedKittiwakes. Auk 100:469- INGR,XM,C. 1959. The importanceof juvenile can- 476. nibalism in the breeding biology of certainbirds BRY.•NT,D.M. 1978. Establishmentof weight hier- of prey. Auk 76:218-226. archies in the broods of House Martins Delichon JOHNSON,R. A., ANDD. W. WICHERN1982. Applied urbica. Ibis 120:16-26. multivariate statistical analysis. Prentice-Hall, BUITRON,D. 1988. Female and male specialization EnglewoodCliffs, New Jersey. in parental care and its consequencesin Black- KAPLAN,E. L., AND P. MEIER. 1958. Nonparametric billed Magpies. Condor 90:29-39. estimationfrom incompleteobservations. J. Am. CL•RK, A. B., AND D. S. WILSON. 1981. Avian breed- Star. Assoc. 53:457-481. ing adaptations:Hatching asynchrony,brood re- LACK,D. 1954. The natural regulation of animal duction and nest failure. Q. Rev. Biol. 56:253- numbers. Oxford Univ. Press, London. 277. LACK,D. 1968. Ecologicaladaptations for breeding Cox, D.R. 1972. Regressionmodels and life tables in birds. Methuen, London. (with discussion).J. Roy. Stat. Soc. Lond. B 34: LAWLESS,J.F. 1982. Statistical models and methods 187-220. for lifetime data. John Wiley & Sons,New York. CREASE,A.J. 1992. Cannibalismby Magpies.Br. Birds ME¾1•URG,B. 1974. Sibling aggressionand mortality 85:87-88. among nestling eagles.Ibis 116:224-228. DœVORE,J.L. 1987. Probability and statisticsfor en- MOCK, D.W. 1985. Siblicidal brood reduction: The gineering and the sciences,2nd ed. Brooks/Cole prey-sizehypothesis. Am. Nat. 125:327-343. Publishing Company, Monterey. MOCK, D. W. 1994. Brood reduction: Narrow sense, DHINDSA, M., AND D. A. BOAG. 1990. The effect of broad sense. J. Arian Biol. 25:3-7. food supplementationon the reproductive suc- MUm,H,/, M. T. 1985. Nestling Eastern Kingbird cessof Black-billedMagpies Picapica. Ibis 132: growth: Effectsof initial size and ambient tem- 595-602. perature. Ecology66:162-170. January1996] MagpieBrood Reduction 199

NETER,J., W. WASSERMAN,AND M. H. KUTNER. 1985. mum and minimum temperatureswere 21ø and 6øC Applied linear statisticalmodels, 2nd ed. Richard respectively;temperatures were below normal for 10 D. Irwin, Homewood, Illinois. of 17 days. NORUSlS,M.J. 1993. SPSS for Windows: Advanced In one nest, the smallestnestling (aged 20 days) statistics,release 6.1. SPSS,Chicago. had been killed and disembowelledby one or both O'CONNOR,R. J. 1975. Initial size and subsequent of its larger siblings;it was still warm when found, growth in passerinenestlings. Bird-Banding 85: and the gut was being pulled out of the body cavity 208-219. by the largest nestling. The largest nestling regur- O'CONNOR,R.J. 1979. Egg weights and brood re- gitatedsmall pieces of fleshwhen handled.The dead duction in the EuropeanSwift (Apusapus). Con- nestlingweighed 124g as comparedto an averageof dor 81:133-145. 177 g for the survivors.Two dayslater, the smaller PdCKLE•S,R.E. 1965. Brood reduction in the Curve- of the two survivingnestlings was apparently driven billed Thrasher. Condor 67:505-510. out of the nest by its larger sibling, and was found RowhEy,I. 1970. Lamb predation in Australia: In- on the ground, alive but seriouslyinjured with the cidence,predisposing conditions and the iden- right femur stripped completely of skin and muscle tification of wounds. CSIRO Wildl. Res. 15:79- and severalsmall lacerationsover the right synsacral 123. region.This nestlinghad lost 25 g over the previous $LAGSVOLD,T., J. SANDVIK, G. RObSTAD,{•. LOP, ENTS•q, four days,and had a mass35 g lessthan the aggressor ANDM. H•JSB¾.1984. On the adaptivevalue of at the time of the attack.Previously, two other nest- intraclutchegg-size variation in birds. Auk 101: lings had died at days9 and 11, respectively,after a 685-697. prolonged period of massloss. The single survivor STANBACK,M. T., AND W. D. KOENIG. 1992. Canni- fledged successfullyat 26 days, and was observed balism in birds. Pages277-298 in Cannibalism: within 30 m of the nest tree on day 40. Ecologyand evolution among diverse taxa (M. In the secondnest, a 16-day-oldnestling was found A. Elgar and B. J. Crespi, Eds.). Oxford Univ. deadand partially dismemberedat the bottomof the Press, Oxford. nestcup. Although it had hatchedwithin 12 h of its STEEL,R. G. T., AND J. H. TORRm. 1980. Principles siblings,it weighedonly 93 g at the time of its death, and proceduresof statistics:A biometrical ap- as comparedto the averagemass of 150 g for the four proach,2nd ed. McGraw-Hill Book Company, survivors.Two dayslater, a seconddead nestling was New York. found in the nest,disembowelled with the gut partly TATNER,P. 1984. Bodycomponent growth and com- eaten.Two survivorshad extensivebruising and open positionof the Magpie Picapica. J. Zool. (Lond.) ragged wounds over the left synsacrum;the third 197:559-581. nestling had wounds on the right tibiotarsus.The TRAIl, P. W., S. D. STRAH[, AND J. L. BROWN. 1981. extent of wounding on nestlingsincreased over the Infanticide in relation to individual and flock next six days. On day 24 the middle nestling was historiesin a communallybreeding bird, the found dead and partly eaten; the smallestnestling Mexican Jay (Aphelocomaultramarina). Am. Nat. was seriouslyinjured, the entire right femur being 118:72-82. completelystripped of flesh,and the extremitiescold WHITE,G. C., ANDR. A. GARROTT.1990. Analysisof and without motor control.The injuries on the largest wildlife radio-trackingdata. Academic Press, San nestlinghad scabbedover. Both nestlingssurvived Diego. to leave the nest at 28 days. However, the smaller survivor was incapable of perching and, although I APPENDIX observedit on two occasionsbeing fed on the ground Siblicideand Sibling Cannibalismin by at least one parent, it disappearedapproximately Black-billedMagpies. one week after leaving the nest. In three other broods, dead nestlings had disap- Siblicidalevents were observedbetween 19 May pearedbefore they could be examined.However, all and 4 June 1994. During this time, rainfall totalled nestlingshad been wounded prior to disappearance. 0.55cm, and occurredon 11 of 17 days;rainfall levels In two cases,the nestling'scolor band and the gizzard were normal for this time of year. The averagedaily were found in the nest lining. One nestling fledged air temperaturewas 13øC,and the meandaily maxi- from each of these three nests.