(milvus migrans): counteracting hatching asynchrony?

0 downloads 0 Views 631KB Size Report
tins mi•qrans) with respect to laying order, egg size, clutch size, and timing of the start of incu- bation. ..... is an important selective force acting on the du- ration of ...
The Auk 114(2):1q2 It)% lC)C)7

LAYING

ORDER

AFFECTS

INCUBATION

DURATION

IN THE

BI,ACK KITE (MILVU$ MIGRAN$): COUNTERACTING HATCHING

ASYNCHRONY?

JAVIERVIKIUELA I)et•arlamento deEcologla Evolutiva, MuseoNacional deCiencias Naturales, CSIC, ]os• • GutierrezAbascal2, 28006-Madrid,Spain

ABSTRACT.--I studiedvariationin thedurationof the incubationperiodof BlackKites(Mil-

tinsmi•qrans) withrespect to layingorder,eggsize,clutchsize,andtimingof thestartof incubation.I estimated thedurationof the incubation periodand theeffectof the onsetof incubationby experimentally advancing or delayingthe startof incubation. Eggmassand clutch sizehad no cleareffecton incubationduration.First-laideggsin clutcheswhereI delayedthe startof incubation hadthelongestincubation periods.Hatchingin theseexperimental clutches occurredin reverseorderto that of laying.High environmental temperatures duringthe pe-

riod thateggsweremaintained unincubated prolonged thedurationof incubation. Third-laid eggsm clutches whereI advancedthestartof incubation hadtheshortest incubation periods. This resultwasconsistent with cnrrelations foundbetweentotaland partialhatchingspreads of controlclutches. Recentstudieshaveprovidedevidenceof shortened incubation periodsof last-laideggsin severalgroupsof birds.Shortened incubation periodsof last-laideggscould be due to advancedhatchingthroughvocalcommunication amongembryos,which could counteract thenegativeinfluenceof longhatchingspreadson survivalof last-hatched chicks. Asidefrombenefitsto chicksnf last-laideggs,shortened incubation periodsin theBlackKite alsomayserveparentalinterests, because thereis evidence of a parent-offspring conflictover broodreduction.Finalhatchingspread(timebetweenend of hatchingof firstand lasteggs) mirroredinitialhatching spread(timebetweenstartof hatching of firstandlasteggs)butwas

slightlylonger.An additional(or alternative) functionof vocalizations by unhatched chicks couldbe to enhance parentalincubation of later-laideggsafterearlier-laideggshavehatched. Rec•'iv•,d 1'1March 1996, •wccpted 8 October1996.

IIA'FC'IIlNœ; ASYNCItI,•ONY affectsmortality and vancedhatchingof late eggsand/or retarded growth of last-hatchedchicksby establishing hatchingof early ones(i.e. by variableduration size hierarchies within broods (Newton 1979; of incubation;Vince 1968). One study has reAmundsenand Slagsvoid1991;Vifiuela 1991, portedembryoniccontrolof hatchingtimesin a species (Schwagmeyer et al. 1991), 1996).At least 17 hypotheseshave been pro- semiprecocial posed to explain the origin and function of but no such evidence exists for semialtricial hatching asynchronyin birds (Stolesonand birds (despiteits potentialinfluenceon hatchStolesonand Beissinger1995). Beissinger1995). In raptors, hatching asyn- ing asynchrony; chronyis thoughtto be an adaptationthat pro- Recentevidencesuggeststhat other factors, motesmortality of the youngestchickswhen suchas femalebodysize,affecthatchingasynthereis not enoughfoodto raisethe entirebrood chronyin semialtricial species(Bortolottiand (1,ackt954, Meyburg 1974,Edwardsand Col- Wiebe 1993). Incubationperiods may vary considerably Iopy 1983). It is possible,however, that mortality of last-hatchedchicksis a nonadaptivecon- within species(Ricklefsand Smeraski1983),but sequenceof hatchingasynchrony when the lat- few studies have examined this variation or its ter is fawnred for other reasons (Amundsen and effect on hatching asynchrony.Intraspecific variation in incubationperiods usually is exSlagsw•ld1991). [latching asynchronyusually is assumedto plained by differencesin nest microclimateor (Drent1975).In addition, reflectthe patternof incubationduring the lay- parentalattentiveness ing period, althoughdocmnentationis scarce siblingcompetitioncanbe a powerfulselective (Veigaand Vifiuela 1993,Ricklefs1993,Stoleson forcein promotingadaptivevariationin the duand Beissinger 1995).In precocialspecies,highly ration of incubation (Ricklefs 1993). Lastbroodswould sw•chronizedhatchingis attainedthroughad- hatchedchicksin asynchronous 192

April1997]

Incubation Duration in Black Kites

benefitby shortincubationperiodsif this enhancedtheir survival,but no empiricalstudies supportthis hypothesis. The BlackKite (Milvusmigrans)is a mediumsized raptor that exhibitsfacultativesiblicide and slow growth and high mortality of lasthatchedchicks(Hiraldo et al. 1990, Veiga and Hiraldo 1990, Vifiuela 1991). Incubation dura-

tion of BlackKite eggsis highly variable(25 to 38 days; Meyburg 1971). Possiblereasonsfor thisvariationincludedifferences in eggsize,an effectof layingorderon the durationof incubation, and/or variation in the start of incubation

193

oneto two days.Nestswerevisiteddailyduringlaying, and eggs were marked with felt pens and weighed(+ 1 g) usinga Pesolaspringbalance.I con-

sideredlayingto haveendedwhenI foundthe third eggor afterfour dayshad elapsedsincethe previous eggwas found.SeeVifiuela(1996)for additionaldetails.

During 1988 and 1989, I experimentallyaltered hatchingasynchrony of 52randomlyselected clutches. Only two- and three-eggclutcheswere includedin this experiment.At thesenests,I took the first two eggson the daysthattheywerefound(dayof laying for second eggs,andwithinonedayof layingfor first eggs).Kite eggswerereplacedwith domesticchicken eggswith artificialmarkingsto mimicthe pigmentationof kite eggs.Threedaysafterthesecondeggwas laid, I put the originaleggsback in their respective nests,markingandweighingthethird egg(if present) withoutremovingit. I madea final visit on the next daytoassess acceptance ofneweggsandto determine if a third egghad beenlaid. In all three-eggclutches includedin this sample,the third eggwas laid three (19 cases)or four (1 case)daysafterthe secondegg. Clutcheswereassigned to oneof two treatments: (1) synchronous clutches(eggsmaintainedat ambient temperature until theywerereturnedto thenest);and (2) asynchronous clutches(eggsmaintainedthroughout theremovalperiodat 37-38øC,with watercontain-

(Meyburg1971).Additionally,behavioraldata onBlackKitessuggestthatparent-offspring conflict existsover brood size (a trait apparently commonin speciesexhibitinghatchingasynchrony and brood reduction;Nilsson 1995). Last-hatchedchicks may die from siblicide shortly after hatching independentof food abundance,but female parents(malesusually do not feed chicks)selectivelyfeedthe smallest chicksand exhibitbehaviorsthat reducesibling aggression(Vifiuela1991). Thelengthof theincubationperiodis difficult to estimateaccuratelyin the field becausethe ers insidethe incubatorsand below the eggs;Campstart of incubation

often differs

for individual

eggs dependingon their laying order (Lack 1966)and becauseincubationconstancyduring the laying periodmay be intermittent(Newton 1979).By artificiallycontrollingthe startof incubation, I obtained accurate estimatesof incu-

bationdurationin relationto laying order,egg mass, and incubation initiation in Black Kites. I

bell and Flood 1977;Burnham 1978, 1983).Eggs in both experimenttreatmentswere turned 180ø twice

daily.Hereafter,I referto experimental nestsaseither "asynchronous" or "synchronous" nests,and to nests with unaltered hatching asynchronyas "control" nests.Asidefromtheexperimental manipulations, all methods,includingthenumberof nestvisits,werethe sameat controland experimentalnests. FemalesBlackKitesusuallyinitiateincubationbetweenthe laying of the first and secondeggs,but slightly later in three-eggclutches(Vifiuela 1991, 1996).Eggswere mild or warm to the touchduring all of the nestchecksmade on days that third eggs

provide the first documentationof reducedincubationperiodsof last-laideggsin a semialtricial speciesand suggestthat shortenedincubation is a mechanismto counteractthe negative effectsof hatchingasynchronyon the growth were laid (Vifiuela 1991). Thus, females attained conand survival

of last-hatched

chicks.

STUDY AREA AND METHODS

stantincubationsometimebetweenthe layingof their secondand third eggs(Vifiuela1991).Consequently,

my experiments providedaccurate dataon theduration of incubation, becauseI controlled the onset of in-

My studywasconducted in MatasGordas,North-

cubationduring laying and returnedexperimental

ern DofianaNationalPark, southwestern Spain(37øN eggsto thenestsonceconstant incubation behaviorof 6ø05'W).Matas Gordascontainsopen Mediterranean adults was reached. I define incubationperiod as the number of comforest(dominatedby corkoak [Quercus suber]), scrub-

land,andgrassland nearseasonally inundatedmarshland (seeVifiuelaand Veiga1992,Vifiuela1993).I visitedthestudyareaalmostdailythroughout thebreeding seasons (mid-Marchto lateJuly)of 1987to 1989. Beforelaying,nestswere visitedeverytwo to eight days,dependingon the stageof the nestduringthe previousvisit. Advancednestswith well-developed linings(i.e.layingwasimminent)werechecked every

pletedaysof incubation elapsedbetweentheday that incubationstarted (i.e. when eggs in synchronous nestswerereturnedto thenestandwheneggsin asynchronous nestswereput in theincubator)andtheday that hatchingstarted.Soundscouldbe heardinside the eggevenbeforeany signof hatchingin the eggshell could be detected (see Vifiuela 1996). Conse-

quently,the day in whichincubation startedand the

194

J^VIER VL•UELA

TABLE 1. ANCOVAexaminingeffectsof layingorder, year,experimentaltreatment(eggsincubatedfrom day of layingvs. eggskept unincubated until end of layingperiod),and clutchsizeon durationof incubationperiodof eggsof BlackKites(hatchingperiod excluded).The covariate(eggmass)and other interactions had no significanteffectson incubation duration

and were removed Variable

[Auk,Vol.114

21}

25

29 28.5

from the final model. df

F

P

4.23

0.02

2O

Laying order (lst, 2nd, or 3rd)

2

Year (1988 vs. 1989)

I

1.67

0.20

Treatment

1

8.06

0.006

Clutch size (2 vs. 3)

1

2.67

0.11

1 67

8.37

0.005

Year x treatment Residual

interaction

27.5

• First

• Second

•YTNG

day in whichhatchingstartedwereexcluded.Because eggsin the asynchronous treatmentusuallywere put in incubatorsin the afternoon,and eggsin the synchronoustreatmentwere returnedto the nestsat approximatelythe same'time,no appreciable biascould affectmy resultswith respectto the start of incubation.The samewastruefor the startof hatching,and unless the hour at which the chicks started to hatch

couldbe biasedwith respectto layingorderor treatment,thiscouldnothaveaffectedmy results.Forcomparative purposes,I measuredincubationduration from 37 last-laideggsin controldutches. Meteorologicaldata were obtainedfrom the Instituto Nacionalde Meteorologiastationlocated2-5 km fromthestudynests.Forclutches indudedin thesynchronizationexperiment,I calculatedthe average maximumdaily temperatureduring the period that eggsweremaintainedunincubated. I usedmaximum temperatures because minimum temperatures in Dofianaduring this time of year are relativelyhigh and approximatethe optimaltemperaturesneededto maintain the viability of unincubatedeggs (about 10øC;Olsenand Haynes1948,Campbelland Flood 1977).In contrast,maximum temperaturesoften exceed the "physiological zero" temperature(i.e. 2427øC,belowwhichno embryonicdevelopment occurs; Haftorn 1981,Webb 1987).Exposureof unincubated eggsto temperatures below that for optimalincubation (i.e.35-38øC;Webb1987)but abovephysiological zero, is more deleteriousthan exposureto temperatures below physiologicalzero (White and Kinney 1974, Haftorn 1988).

• ThJ. vd

ORDER

FIG.1. Variationin incubationperiod (g -+ SE;excludinghatchingperiod)amonglayingorders.Experimental synchronousand asynchronousdutches pooled.Samplesizesabovebars.

rorsthetimingof startof hatching.With thispurpose, I calculated theinitialhatchingspread(estimated time elapsedbetweenthe startof hatchingof firstand last eggs)andfinalhatchingspread(timeelapsedbetween the endof hatchingof firstand lasteggs)for all nests in whichthe hatchingprocesswas recorded(experimentaland controlpooled;seeVifiuela 1996). I testedthe effectsof layingorder,year,experimental treatment, and clutch size on incubation duration

usingANCOVA,with eggmassasthecovariate(Table 1). To avoid confoundinginteractions (therewere no experimentalclutchesin 1987or accurateestimatesof

incubationduration for first-laid eggs in control dutches),onlyexperimental eggswereincluded.Nonsignificantinteractionsand covariateswere removed from the final modelto increasethe power of the test. RESULTS

Incubation duration.--Incubation

duration was

determinedfor 74 eggsin experimentalclutches (:•= 28.3+ SDof 0.88days,range27to 31days), and37 last-laideggsin controlclutches(28.2+ 0.97days).The differencebetweenexperimental andcontroleggswasnotsignificant(t = 0.79,

Nestswere visiteddaily during hatchingto record P = 0.43).

the conditionof eachegg or recentlyhatchedchick Egg size did not influenceincubationdura(seeVifiuela 1996).Hatchingasynchrony(in hours) tion (F = 1.2, df = 1 and 71, P = 0.27) and was was estimatedfrom these daily visits (see Vifiuela 1996). Because I studied the duration of incubation

with respectto the startof hatching,and durationof the hatchingprocess variesamongeggs(A. B. Clark pers.comm.,J. Vifiuelaunpubl.data),it may be important to exploreif timing of chickemergencemir-

removed from the final model. Clutch size and

year alsohad no significanteffectson incubation duration (Table 1). Incubation duration was

influencedby layingorder(Table1), with thirdlaid eggshavingthe shortestincubationperiods

April1997]

Incubation Duration inBlack Kites

29.5

195

29.5

29

16

29

28.5 23

28 28.5

27.5 First

Second

21

Third

27

17

LAYING

ORDER

2O

T

T

28

FIG.2. Variationin incubationperiod (• + SE;excluding hatchingperiod) amonglaying ordersand 1989

treatments.Circles = asynchronousnests;squares=

synchronousnests; triangles = second (two-egg clutches)and third (three-eggclutches)eggsof control clutches.Samplesizesabovebars.

27.5

YEAR

FIG.3. Variationin incubationperiod (• + SE;excludinghatchingperiod)amongyearsandtreatments. Symbolsas in Figure2. Samplesizesabovebars.

(Fig. 1). Treatmentalsohad a significanteffect on thelengthof the incubationperiod(Table1); eggsin synchronous clutcheshad longerincu- clutcheswere exposedduringthe layingperiod bation periods(28.5 _+0.9 days,n = 36) than werehigherduring1988than during1989(21.1 eggsin asynchronous clutches(28.0_+0.8 days, _+2.6øCvs. 18.9 ñ 1.7øC,n = 7 and 11, respecn = 38).

tively; t = 2.1, P = 0.049).

Hatching asynchrony.--Theinitial hatching Third-laideggsof asynchronous dutcheshad shorterincubationperiodsthan third-laideggs spread was smaller than the final hatching of synchronous clutches(t = 2.51, P = 0.02), spread(59.4 ñ 33.8h vs. 65.3 _+32.8h; paired whereasthird eggsof controlclutcheshad in- t-test, t = 3.98, P < 0.001), although they termediatevaluesof incubationduration (Fig. were stronglypositivelycorrelated(r = 0.93, 2). First-laideggshad longerincubationperiods P < 0.001).For 21 three-eggcontrolclutches,I in synchronous clutchesthan in asynchronous recordedtotal initial hatchingspread(81.6 + clutches,but the differencewas not significant 19.2h, range22 to 103h), initialhatchingspread (t = 1.88,P = 0.07;Fig.2). Third-laideggswere betweenfirst and secondeggs(16.8 _+14.1 h, not manipulated,sodelayor advanceof the on- range-8 to 52h; negativevaluesfor threenests set of incubationin experimentalclutchesdid in whichthe secondeggbeganhatchingbefore not affectthird-laid eggs.In 12 out of 13 syn- the first), and initial hatchingspreadbetween chronousnestsin which more than one egg secondand third eggs(62.6 + 20.6,range0 to hatched,the first-hatched eggswerelaid in sec- 93.5h). Initialhatchingspreadbetweenfirstand ond or third order.Theseresultssuggestthat a secondeggswas more variablethan that bedelay in the start of incubationmay inducea tween secondand third eggs (coefficientof protractedincubationperiod of first-laideggs, variation 84% vs. 32.8%; F = 6.5, df = 20 and spreadwas whereasstartingincubationwith the first egg 20, P < 0.001).Totalinitial hatcbJng may inducea shorteningof the incubationfor positivelycorrelatedwith hatchingspreadbetweenfirstandsecondeggs(rs = 0.7,P = 0.001), third-laideggs. The interactionbetween treatmentand year but notwith thatbetweensecondandthird eggs was significant(Table1). Incubationperiodsof (rs = 0.23,P = 0.3). Hatchingspreadbetween synchronous eggsfrom 1988were longerthan firstandsecondeggswasnegativelycorrelated andthird thoseof asynchronous eggs(F = 6.4,df = 1 and with hatchingspreadbetweensecond 29, P = 0.01).This differencewas due to a pro- eggs(rs = -0.44, P = 0.05).Theseresultscontractedincubationperiodof synchronous eggs firm thoseprovidedby experimentalclutches; during 1988,but no similar variation for asyn- i.e.whenhatchingspreadbetweenfirstandsecthat betweensecondand chronouseggswas found (Fig. 3). The maxi- ond eggsincreases, mum temperatures to which synchronous thirdeggsdecreases. Thelackof correlation be-

196

JAVIER VIl•IUELA

[Auk, Vol. 114

(Parsons 1972, Runde and Barret 1981, Nol and

PeregrineFalcons(Falcoperegrinus) unincubated for six days after laying, and by Lessellsand Avery (1989),who found a negativecorrelation betweenhatchingasynchrony and lengthof the incubationperiod of the first egg in the EuropeanBee-eater(Meropsapiaster). The shortestincubation periods occurredin third eggs in asynchronousclutches.Because theseeggswere not removedfrom nests,their incubationdurationwas not affectedby experimental treatments.Thus, advancedhatchingof third eggsmustbe a consequence of the startof hatching of previous eggs, a result also supportedby the negativecorrelationbetweenpartial hatchingspreadsof three-eggclutchesin controlnests.This resultcouldbe explainedby vocal communicationamong siblings during hatching,ashasbeenobservedin precocialbirds (Vince 1966).The soundsemitted by precocial chicksbeforeand during hatchingfacilitatesynchronyby advancinghatchingof last-laideggs and slowing hatching of first-hatchedchicks (Vince1966,Vinceand Cheng1970).Unhatched chicks of Black Kites called loudly and frequently before any external signs of shellbreakingcouldbe detected(Vifiuela1996).This behavioris rarein nonprecocial species(Oppen-

Blokpoel1983,Ricklefsand Smeraski1983,Mar-

heim 1972, O'Connor 1984) but has been re-

tin and Arnold 1991, Kattan 1995).

ported in raptors(Gargett1990),parrots(A. B. Clark pers. comm.),and pelicans(Evans1988, 1989). Additional research is required before concludingthat embryoniccontrolof hatching

tween total hatching spread and hatching spreadbetweensecondand third eggsalsomay be explainedby the confoundingeffectof a reductionin hatchingasynchronybetweensecond

and third eggswhen hatchingasynchronybetween first and secondegg increases. DISCUSSION

Much of thepreviouslydescribedvariationin incubationduration of BlackKite eggsmay be erroneous, because some authors have assumed

that incubationstarts with the first egg (e.g. Meyburg 1971). However, Black Kites in my study area delayedthe start of incubationuntil one to three days after the first egg was laid (Vifiuela 1991). Moreover, incubation periods rangedfrom27 to 31 days(29to 33 daysincluding two daysof hatchingperiod;Vifiuela 1996), which is well below the publishedmaximum periodof 38 days(Meyburg1971).I did not find any clear effectof egg masson duration of incubation.A clear positivecorrelationexistsbetweeneggmassand incubationdurationamong bird species(Rahnand Ar 1974),but the availableinformationwithin speciesis contradictory

Lengthof the incubationperiod was affected by the amount of incubationduring the laying period and by laying order.I observeda trend toward protractedincubationof early eggsin synchronous clutchesand a shorteningof incubationdurationof third eggs,especiallyin asynchronousclutches(Fig. 2). Exposureof eggsto temperaturesbelow that for optimal incubation may reduceviability (Arnold et al. 1987,Vifiuela 1991,Veiga1992,Veigaand Vifiuela 1993)or induce sub-lethaleffectson embryonicdevelopment, such as a protracted incubation period (Webb1987).Exposureof eggsto temperatures below optimalincubationtemperature,but near physiological zero,seemsto be especiallydetrimental (White and Kinney 1974, Webb 1987, Haftorn 1988).In agreementwith this idea, the incubationperiod of synchronousBlack Kite eggswas longerduring 1988than during 1989, and the maximum temperaturesto which the eggs were exposedduring the laying period were higherin 1988but still were lower than the optimum temperature.Similar resultswere reported by Campbell and Flood (1977), who found protractedincubationperiodsfor eggsof

times occurs in Black Kites. Evidence

for this

mechanismhas been found in precocialspecies (Vince1968,Vinceand Cheng 1970)and in one laboratory study of a semiprecocialspecies

(Schwagmeyer et al. 1991). Shortenedincubationperiodsof last-laideggs in BlackKitescouldreducehatchingasynchrony and its possiblenegativeeffectson survival of last-hatched chicks, which often die from sibli-

cide or starvation (Veiga and Hiraldo 1990, Vifiuela 1991). Thus, acceleratedhatching of last-laideggscould servethe selfishinterestof chicks.However,giventhe evidencefor parentoffspringconflictoverbroodsizein thisspecies (Vifiuela 1991),the acceleratedhatchingof lastlaid eggsalsocouldbenefitthe parents.Specifi-

cally,if first-hatchedchickstend to kill their smaller siblingseven when food is abundant (i.e. cainism; Simmons 1988), then the shortened

incubationperiod of last-laideggswould be favored (becauseit increasestotal reproductive success),and females(the only sex that incu-

April 1997]

Incubation Durationin BlackKites

bates,broods,and feedsthe chicksin this species)would collaborate in the process by keeping incubationas constantas possible. Indirectevidencesuggests that amongnonprecocialspecies,shortenedincubationperiods of last-laideggsare not confinedto BlackKites. For example, although hatching asynchrony doesnot vary with broodsizein EuropeanBeeeaters,incubationduringlayingbeginsearlierin larger clutches(Lessellsand Avery 1989). In AmericanKestrels(Falcosparverius), hatchingintervals of last-laid eggs are shorter than expected,and eggsfrequentlyhatchin reverseorder to thatof laying(BortolottiandWiebe1993). Among boobies,incubationapparently starts with the first egg, but hatchingintervalsare shorterthanlayingintervals(e.g.Drummondet al. 1986,Anderson1989).Theseresultssuggest that shortenedincubationperiods of last-laid eggsare moreprevalentin nonprecocialspecies than previouslyrealized. A naggingquestionremains:Why shouldso complexa mechanismhavedevelopedto counteracthatchingasynchron)•which could have beenreducedsimplyby delayingthe startof in-

197

explain,at leastpartly,the long incubationperiodsexhibitedby bird speciesin whicheggneglectis common(Boersma1982).My resultsalso give supportto the idea that siblingcompetition is an importantselectiveforceactingon the duration of incubation (Ricklefs 1993). However,

Ricklefs(1993) postulatedthat variation in the length of the incubationperiod cannotreverse the competitivehierarchyestablished by hatching asynchron)•given the relatively low intraspecificvarianceof this trait. Although the relatively short incubationperiod of last-laid eggscannotcompletelycompensate for the large

difference in sizeamongsiblingsthatisimposed by hatchingasynchrony(Vifiuela1996),it nonethelesscouldcontributeto reducethis discrepancy.

ACKNOWLEDGMENTS

Thisis a contribution to Research ProjectPB87•3405

of theDirecci6n Generalde Investigaci6n Cientffica y T•cnica,duringwhichI wassupportedby a predoctoral fellowship from P.EEI. of Ministerio de Educa-

ci6ny Ciencia.Jos•E Veigaprovidedinvaluablesupportandadvicethroughoutthework.He, ToddW. Arcubation?A delay in the start of incubationof nold, Steven R. Beissinger, Anne B. Clark, Hugh firsteggsin three-eggclutches mayinducea loss Drummond, Kathy Martin, Kate Lessells,Karen of viabilityof the embryos(Vifiuela1991,Veiga Wiebe, and an anonymousrefereeprovided useful 1992),so the early onsetof incubationmay be criticismon previousdrafts.During final analysesand necessaryto preserveegg viability. Moreover,if writing,supportwasprovidedby a FulbrightPostdochatching asynchronyarises for reasonsother toralFellowshipat YaleUniversityandby NSF grant than promotingsiblinghierarchiesor differen- IBN-9407349to StevenR. Beissinger.

tial mortality of chicks, then counteracting mechanisms may appear,suchas shortenedincubationperiodsof last-laideggs(Howe 1978, Clark and Wilson 1981, Arnold et al. 1987).

LITERATURE CITED

AMUNDSEN, T., AND T. SLAGSVOLD. 1991. Hatching

asynchrony: Facilitatingadaptiveor maladaptive The durationof thefinal hatchingspreadmirbrood reduction?Pages 1701-1719in Acta XX roredthat of the initial hatchingspreadbut was CongressusInternationalisOrnithologici(B. D. slightlylonger.Thismay haveresultedfrom reBell, Ed.). Christchurch, New Zealand, 1990. New duced constancyof incubationafter first-laid Zealand OrnithologicalCongressTrust Board, eggshad hatched,becausefemaleshave to deWellington. vote time to feedingthe first hatchlings(Evans ANDERSON, D. J. 1989. The role of hatchingasyn1990). Thus, an additional (or alternative) func-

tion of embryonicvocalizationscould be to en-

hanceincubationof last-laideggs,againin the same contextof cooperationbetween females and their last-hatched chicks (Evans 1988, 1989; Brua et al. 1996).

chronyin siblicidalbroodreductionof two booby species.BehavioralEcology and Sociobiology 25:363-368.

ARNOLD,T. W., E C. ROHWER,AND T. ARMSTRONG.

1987. Eggviability,nestpredation,and theadaptive significanceof clutchsize in prairie ducks. American

Naturalist

130:643•553.

My resultsindicatethat lengthof the incubaBOERSMA, P.D. 1982.Why somebirdstakesolongto tion periodmay be affectedby the conditionsto hatch. American Naturalist 120:733-750. which the eggsare exposedduring early stages BORTOLOT]'I, G., AND K. L. WIEBE. 1993. Incubation beof development. Adverseconditionsduringthis haviourand hatchingpatternsin the American

delicatestageof development may prolongincubation(Webb1987).This phenomenoncould

KestrelFalcosparverius. OrnisScandinavica 24:4147.

198

JAVIER VllqUELA

[Auk,Vol. 114

BRUA,R. B., G. L. NUECHTERLEIN, AND D. BUITRON. LACK,D. 1966. Populationstudiesof birds.Clarendon Press, Oxford. 1996. Vocalresponseof EaredGrebeembryosto

C. M., AND M. I. AVERY.1989. Hatching eggcoolingand eggturning.Auk 113:525-533. LESSELLS, BURNHAM, W. 1978. Incubation,hatchingand breedasynchronyin EuropeanBee-eaters Meropsapiaster.Journalof Animal Ecology58:8154338. ing equipmentat the PeregrineFtmd'sWestern Project.Hawk Chalk 17:47-55. MARTIN, P.A.,ANDT.W.ARNOLD.1991.Relationships BURNHAM, W. 1983. Artificial incubation of falcon amongfresh mass,incubationtime, and water eggs.Journalof WildlifeManagement 47:158-168. lossin Japanese Quail eggs.Condor93:28-37. CAMPBELL, J.,ANDR. FLOOD.1977. Incubationin rap- MEYBURG, B.-U. 1971. On the questionof the incubator breeding.Hawk Chalk 16:38-50. tion period of the BlackKite Milvus migrans.Ibis CLARK,A. B., AND D. S. WILSON. 1981. Avian breed-

113:530.

ing adaptations: Hatchingasynchrony, broodreductionand nestfailure.QuarterlyReviewof Bi-

MEYBURG, B.-U. 1974. Siblingaggression and mortality amongnestingeagles.Ibis 116:224-228. ology56:253-277. NEWTON,I. 1979 Populationecologyof raptors. DRENT,R. 1975. Incubation.Pages333-420in Avian T. and A.D. Poyser,London. biology,vol. 5 (D. S. FamerandJ. R. King,Eds.). NILSSON, J-A. 1995. Parent-offspring interactionover Academic Press, New York. bmod size: Cooperationor conflict.Journalof DRUMMOND, H., E. GONZ.,•LEZ, AND J. L. OSORNO. AvianBiology26:255-259. 1983. Incubationperiod 1986. Parent-offspring cooperationin the Blue- NOL, E., ANDH. BLOKPOEL. footedBooby(Sulanebouxii): Socialrolesin infanof Ring-billedGull and the eggimmersiontechnique. Wilson Bulletin 95:283-286. ticidalbroodreduction.BehavioralEcologyand Sociobiology 19:365-372. O'CONNOR, R. J. 1984. The growthand development EDWARDS, T. C., ANDM. W. COLLOPY. 1983. Obligate of birds.JohnWiley and Sons,London. and facultativebroodreductionin eagles:An ex- OLSEN,M. W., AND S. K. HAYNES.1948. The effect of amination of factors that influence fratricide. Auk 100:630-635.

EVANS,R. M. 1988. Embryonicvocalizationsand the removalof foot websfrom pipped eggsin the American

White Pelican. Condor 90:721-723.

EVANS,R. M. 1989. Egg temperaturesand parental behaviorduringthetransitionfromincubationto broodingin the AmericanWhite Pelican.Auk 106:26-33.

differentholdingtemperatures on the hatchability of hen'seggs.PoultryScience 27:420-426. OPPENHEIM, R.W. 1972.Prehatchingandhatchingbehaviourin birds:A comparativestudyof altricial and precocialspecies. Animal Behaviour20:644655.

PARSONS, J. 1972. Egg size,laying date, and incubation periodin the Herring Gull. Ibis 114:536-541. RAHN,H., ANDA. AR. 1974. The avianegg:Incuba-

tion time and water loss. Condor 76:147-152. EVANS, R. M. 1990. Terminal-egg chillingand hatching intervalsin theAmericanWhitePelican.Auk RICKLEFS, R. E. 1993. Siblingcompetition,hatching 107:431-434. asynchrony, incubationperiodand lifespanin alGARGETT, V. 1990. The Black Eagle. Acorn Books, tricialbirds.CurrentOrnithology11:199-276. RICKLEFS, g. E., AND C. A. SMERASKI.1983. Variation Randburg,SouthAfrica. HAFrORN, S. 1981. Incubationduring the egg-laying in incubationperiod within a populationof the periodin relationto clutchsizeand otheraspects EuropeanStarling.Auk 100:926-931. of reproductionin the Great Tit Parusmajor.Or- RUNDE, O. J.,ANDR. t. BARRET. 1981.Variationin egg nis Scandinavica 12:169-185. sizeand incubationperiodof the KittiwakeRissa HAFrORN,S. 1988. Incubatingfemalepasserines do tridactyla in Norway.OrnisScandinavica 12:80-86. P. L., D. W. MOCK, T. C. LAMEY,C. S. not let the eggtemperaturefall below the 'physi- SCHWAGMEYER, LAMEY,AND M.D. BEECHER.1991. Effects of sibologicalzero temperature'during their absences from the nest. Ornis Scandinavica 19:97- 110. ling contacton hatchtimingin an asynchronously HIRALDO,E, J.P. VEIGA,AND M. MA•,IEZ. 1990. Growth hatchingbird. AnimalBehaviour41:8874394. of nestlingsBlackKitesMilvusmigrans: Effectsof SIMMONS, R. 1988. Offspringqualityand the evolution of cainism. Ibis 130:339-357. hatchingorder,weatherand timeof season. JourSTOLESON, S. H., AND S. R. BEISSINGER.1995. Hatchnal of Zoology(London)222:197-214. HOWE,H. F. 1978. Initial investment, clutch size and ing asynchronyand the onset of incubationin brood reduction in the Common Grackle (Quiscabirds,revisited:When is the criticalperiod?Curlusquiscula L.). Ecology59:1109-1122. rent Ornithology12:191-270. KATI'AN,G. H. 1995. Mechanisms of short incubation VEIGA, J.P. 1992. Hatchingasynchrony in the House periodin bmod-parasiticcowbirds.Auk 112:335Sparrow:A test of the egg viability hypothesis. 342.

LACK,D. 1954.Thenaturalregulationof animalnumbers. Clarendon Press,Oxford.

American

Naturalist

139:669475.

VEIGA,J.P., AND E HIRALDO. 1990. Food habits and

the survivaland growthof nestlingsin two sym-

April1997]

Incubation Duration in Black Kites

199

J. 1993. Variaci6nen la fechade puestade patric kites (Milvusmilvusand Milvus migrans). VIICrUEL^, unapoblaci6nde MilanoNegro(Milvusmigrans). HolarcticEcology13:62-71. VEIGA,J.P., AND J. VII•UELA.1993. Hatching asynEfectode la experienciade los reproductores. Ardeola 40:55-63. chronyand hatchingsuccess in the HouseSparrow: Evidencefor the egg viability hypothesis. VnqUEL^,J. 1996. Establishment of mass hierarchies Ornis Scandinavica

24:237-242.

in broods of the Black Kite. Condor 98:93-99.

VINCE,M.A. 1966.Potentialstimulationproducedby VnqvE•, J.,ANDJ.P.VEIGA.1992. Importanceof rabbitsin the diet and reproductive success of Black avianembryos.Animal Behaviour14:34-40. VINCE,M. A. 1968. Retardation asa factorin the synKitesin southwestern Spain.OrnisScandinavica 23:132-138. chronizationof hatching. Animal Behaviour 16:332-335.

WEBB,D. R. 1987. Thermal tolerance of avian em-

VINCE, M. A., AND R. CHENG. 1970. The retardation

bryos:A review.Condor89:8744398. of hatchingin Japanese Quail. Animal Behaviour WHITE, F. N., ^ND J. L. KINNEY. 1974. Avian incuba18:210-214.

VIIqUEL^, J. 1991. Ecolog/areproductiva del Milano NegroMilvusmigransen el ParqueNacionalde Dofiana.Ph.D. thesis,UniversidadComplutense de Madrid, Madrid, Spain.

tion. Science 186:107-115.

Associate Editor: K. Martin

Suggest Documents