ABSTRACT.--An understanding of geographic and phylogenetic variation in passerine life .... We studied a color-banded population of S. f. fron- talis in and ...
TheAuk 117(2):479-489, 2000
LIFE
IN THE
SLOW
WHITE-BROWED
LANE:
REPRODUCTIVE
LIFE HISTORY
SCRUBWREN, AN AUSTRALIAN
OF THE
ENDEMIC
ROBERTD. MAGRATH,• ASHLEYW. LEEDMAN,JANETL. GARDNER, ANTHONY GIANNASCA, ANJELI C. NATHAN, STEPHENM. YEZERINAC,AND JAMESA. NICHOLLS Divisionof BotanyandZoology, AustralianNationalUniversity,Canberra0200,Australia
ABSTRACT.--An understanding of geographicandphylogenetic variationin passerine life historiesis hamperedby the scarcityof studiesfrom the SouthernHemisphere.We documentedthe breedingbiologyof the White-browedScrubwren(Sericornis frontalis),an Australia endemicin the Pardalotidae(parvorderCorvida).Like othermembersof the Pardalotidae,scrubwrenshad a longlaying interval (two days),a longincubationperiod(declining from 21 to 17 daysthroughthe season),and a long periodof postfiedgingparentalcare(6 to 7 weeks).Scrubwrens appearedto be typicalof the AustralianCorvidain havinga small clutchsize(threeeggs)and a longbreedingseason(5.4months),andtheyalsohad a long intervalbetweenbreedingattempts(10 daysafter a failed attempt,21 daysaftera successful attempt).Scrubwrenswere multibrooded,often raising two broodssuccessfullyand occasionallyraisingthreebroods.The breedingbiologyof scrubwrensaddsfurther supportto claimsof a distinctlife-historystrategyfor membersof the Corvidabut alsoreinforcesevidencethatsome"Corvida"life-historytraitsmorespecifically arethoseof thePardalotidae. Received17 November1998, accepted 18 October1999.
MOSTSTUDIES of thebreedingbiologyof pas- few specieshave been studied(e.g. Acanthiza serines have been carried out in the Northern
Hemisphere, primarilyonmembersof theparvorder Passerida(sensuSibleyand Ahlquist 1990).Thisbiasesourunderstanding of passerine biologybecausethesespeciesare not representativeof passerinesas a whole.For example, the Australian Corvida have smaller clutchsizesthan passerines that breedat similar latitudesin the NorthernHemisphereand
pusilia,A. reguloides, and A. lineata[BellandFord 1986];A. chrysorrhoa [Ford 1963];Sericornis frontalis[Ambroseand Davies 1989];Pardalotus spp. [Woinarskiand Bulman 1985]).Even for these species,samplesizesoftenare small,and quan-
titativedatadonotcoverthewholebreedingcycle. Indeed, for eachof thesespecies,little is knownaboutpostfledging care,durationof the breedingseason,and number of breedingatPasseridathat are residentin Australia (Yom- temptsper seasonmadeby individualfemales.
Tov 1987, 1994; Rowley and Russell 1991). It
Here, we provide a quantitative description
of the breedingbiologyof a populationof the frontalis), endemic" Corvida of Australia have a syn- White-browedScrubwren(Sericornis dromeof slowreproduction, with smallclutch a sedentary,cooperativelybreedingspeciesin the Pardalotidae that is common in southern sizes,prolongedperiodsof parentalcareat all and eastern Australia. Ours is the first detailed stagesof nesting, and long breedingseasons (Ford 1989, Rowley and Russell1991). Never- study of the breedingcycleand breedingseatheless, other than clutch size, most features of sonof any memberof the genusand is based the breedingbiologyof thesespeciesare not on data gatheredfrom a color-markedpopuwell known,andcomparisons of manylife-his- lation over five years.Our goal is to provide a tory attributesare inconclusiveowing to the detailed accountof the breeding cycle of a lack of data from the SouthernHemisphere memberof this speciosefamily of Australian birds as a first step toward disentanglingthe (Martin 1996). effectsof environmentand phylogenyon the Althoughthe 49 speciesin the Pardalotidae life historyof passerines. that are residentin Australiaappearto epitomize the syndromeof slowreproduction, onlya METHODS
has also been claimed that members of the "old
Studyspecies.--The White-browedScrubwrenis a small (ca. 11 to 15 g) passerinethat is endemicto
E-mail: robert.magrath@anu. edu.au 479
480
MAGRATHETAL.
[Auk, Vol. 117
mainland Australia (Christidis and Boles1994). It is
hatchingdateand regressionof incubationperiodon oneof six membersof the genusendemicto Austra- laying date (seebelow). The incubationperiod was definedas the period lia. White-browedScrubwrensare largelysedentary as adults (Brown et al. 1990, Wilson 1994) and breed fromthelayingof thelasteggin theclutchuntil the in diversehabitatsfrom coastalrainforestto alpine completionof hatching.The dateof hatchingwasdeheath(Blakerset al. 1984).Scrubwrensfeed primar- terminedfrom daily visitsto neststowardtheendof ily onarthropodsonthegroundor in low shrubs,but theincubationperiod.We did not flushfemalesfrom theyalsosearchunderbark or in foliage,sometimes nestsduring this period, so we were unableto inin tree canopies (Keast 1978, Ambrose 1985, Cale spectthe contentson eachvisit and thereforealso 1994). The nest is domed with a side entranceand usedthe appearanceand size of youngnestlingsto usuallyis well hiddenunderleaf-litteror vegetation, estimatethe dayof hatching(MagrathandYezerinac on or near the ground.White-browedScrubwrens 1997).We gaveeachnestlinga uniquecombination are known to breed cooperatively(Bell 1982, Am- of colorbandswhen it was 9 or 10 daysold. brose and Davies 1989), including our study popuTo quantifythe durationof postfledgingparental lation (see below). care,we watched30 focalfledglingsin 15broodssevWe studied a color-bandedpopulation of S.f. fron-
talisin and adjacentto the AustralianNationalBotanic Gardens (35ø16'S,149ø06'E) in Canberra from
1992to 1996.The Gardensoccupyan areaof 40 ha, 27 ha of which are plantedexclusivelywith Australian nativeplants.Most of the remaining13 ha are naturalwoodlandsthat are contiguouswith a large area of natural
habitat in which
scrubwrens
breed.
eral times a week for 15 min during 1993 and re-
cordedwhether they were fed by an adult during this period.Watchesusuallywere conductedon differentdays,but a few fledglingswere watchedtwice per day,separatedby severalhours.The dateof terminationof parentalcarewas takento be the midpoint from the lastwatchin whichwe sawtheyoung beingfed andthefirstwatchof a sequence of at least threewatchesin whichwe did not seeit beingfed. Thesetwo dateswere a medianof threedaysapart
Althoughbreedingextendedbeyondthe end of Decemberin eachseason,we referto the seasonby the year in whichbreedingbegan. (range 0 to 11). Dataanalyses.--We analyzeddatawith SPSS(NoWhite-browedScrubwrensare residentthroughwhenever out the year,andduringthebreedingseasonwe vis- rusis1995).We usedparametricstatistics ited territories at least three times a week to docuassumptionsof the analysesappearedto be met or ment reproductive attempts. Between 35 and 48 breeding groups were present in any one breeding season.Scrubwrenstypically bred in pairs (46% of groups) or in trios consistingof a sociallydominant
the data could
be transformed
to meet those as-
sumptions.Data that weretransformedfor analyses were back-transformed for presentationin the text. When we had data (e.g.clutchsize,incubation,and nestlingperiods)from more than one nestof a female in a given year, we randomly selecteda single
pair and a subordinatemale(44%),although10%of the groupshad more than one subordinatemale (Magrathand Whittingham1997).Only the female attemptto maintain statisticalindependence.Sample builds the nest and incubates, but both members of
sizes varied among analyses becausenests were the dominantpair, and oftenthe subordinatemales, found at different times during the breedingcycle provisionthe nestlings(Magrathand Whittingham and becausemany nestsfailed before fledging(see 1997).Neither groupsize nor provisioningby sub- Magrathand Yezerinac1997).Analysesof timing of ordinate males had a detectable effect on the durabreeding and number of attempts per seasonwere tion of any stageof the reproductivecycle,the inter- restrictedto femalesthat we followedsufficiently val betweennestingattempts,or the reproductive closelyto detecteachnestingattempt. success of the group(Magrathand Yezerinac1997). As an index of the lengthof the breedingseason, Field methods.--We determined the sex of birds in we calculatedthe numberof "equallygoodmonths the field from the color of the lores (malesblack, fe- for breeding"followingMacArthur(1964:394). This males brown; Rogers et al. 1986). We detected no entailedenteringthe proportionof clutches initiated "brown-loredmales,"whichmightoccurin S.f. ma- in each month into the Shannon-Wienerdiversity culatus(Ambrose and Davies 1989). Nests usually formulaand then taking the antilogof the diversity were foundby watchingbuildingfemales,following value. femalesbackto the nest during incubation,or followingadultsthatwerefeedingnestlings.Mostnests RESULTS were on or near the ground.If a nestwas foundbeforelayingin 1992,it wascheckeddailyto determine Clutchsize and layinginterval.--Mostscrubthe date of layingof eacheggin the clutch.In subsequentyears,we checkednestsonly to determine wren clutchescontainedthree eggs(93.6%of had two eggs,one the dateon whichthe first eggwaslaid (the"laying 171),althoughnine clutches date").If the nestwasnot founduntil aftereggshad had oneegg, and onehad four eggs,giving a been laid, the laying date was estimatedfrom the meanclutchsizeof 2.94eggs.We did not mark
April 2000]
Breeding ofWhite-browed Scrubwrens
481
19
23
18
ß
17
..........
16 o
20
õ
•9
...........
15
17
16
Aug ,
11 30
60
90
120
150
180
30
i 60
i 90
Oct [
I
Nov [ I
120
Dec • I
150
Jan • I
180
210
Feb 240
Hatchingdate (1 = 1 July)
Laying date (1 = 1 July)
F•G.1. Seasonalchangein the incubationperiod of White-browedScrubwrenswith laying date (y = 28.7 - 5.2411og•0x], n = 92, r2= 0.51,P < 0.0001).The three outliers shown as crosses were not included
Sep •
FIG. 2. Seasonalchangein the nestlingperiod of White-browedScrubwrenswith hatchingdate (y = 22.4 - 3.5511og,0x], n = 124, r2 = 0.23, P < 0.001).
in
the regression.
ed in the sampleonlyonceperyear),or to some seasonal factor that affected each individual
eggsduring laying, so it is probablethat some clutchesof lessthan three eggsresultedfrom egglossduring layingor incubation.Eggswere laid at two-day intervalsin all 35 caseswhere the interval was known accurately.The 35 intervals include 13 casesof first to secondegg and 22 casesof secondto third egg.Thesedata comefrom 27 clutcheslaid by 21 different females.
Incubationperiod.--Themean incubationperiod was 18.8 _+SD of 1.3 days(n = 95), ranging
from 17to 22 days.Excludingthethreecasesof a 22-day incubationperiod (outliers) gives a meanvalueof 18.7 __+ 1.2 days.Only clutchesof three were used to calculateincubationperiods.
A dramaticdeclinein the length of the in-
fe-
male.Weaddressed thisissueby examiningthe slopeof the regressionof incubationperiodon date (log transformed)for individual females for whom
we had measures
of the incubation
period for different clutcheswithin a season. The mean slopeof the regressionwas -5.0 + SE of 0.6, which is significantlylessthan zero (t = 8.4, df = 34, P < 0.001)but is not significantlydifferentfrom the populationregression slopeof -5.2 (t = 0.4, df = 34, P = 0.70).Thus, the seasonaldeclinein lengthof the incubation period affectedindividual femalesand wasnot a consequence of differentfemaleslaying at different
dates.
Nestlingperiod.--Eggsin a clutch hatched roughlysynchronously. In 37 out of 45 broods (82%), all nestlingshad hatchedbetweenin-
cubationperiod (from 21 to 17 days) occurred spectionsof nest contentson sequentialdays;
overthe courseof thebreedingseason(Fig.1). We detectedno differencebetweenyearsin the mean incubationperiod or in the slopeof decline (ANOVA, including date as a covariate, year effectafter droppinginteractionterm, F = 0.5, df = 4 and 86, P = 0.80; year x date interaction, F = 1.9, df = 4 and 82, P = 0.12; outliers
identified in Fig. I were excludedfrom analyses).
in the remaining8 broods,all nestlingshad hatchedby the next day. This implies that hatchingusuallytakesplaceovera few hours, or perhapsthat it occursovernight. The meannestlingperiod was 15.1 __+ SD of 1.1 days(n = 124,range 12 to 18 days).The nestlingperioddeclinedthroughthebreeding season(Fig. 2), and neither the mean nor the pattern of seasonaldecline differed among
The seasonaldeclinein incubationperiodil- years (year, after dropping interactionterm, F lustratedin Figure I may have resultedfrom = 1.3, df = 4 and 118, P = 0.30; year x date femaleswith differentincubationabilitieslay- interaction, F = 1.5, df = 4 and 114, P = 0.20). ing at differentdates(eachfemaleis representThe declinein the nestlingperiod through
482
MAGRATHET AL.
[Auk, Vol. 117
4O 2O
3O
t53t8
15
t17+52
10
i
i
i
i
10
i
0
14
171•116 • 92
Laying Incubation Nestling FledgingSuccessful
I
i
i
i
93
94
95
96
Year
Fate of previousnesting attempt
FIC. 4. Yearlyvariationin the intervalbetween breedingattemptsof White-browedScrubwrens. The delayto relayingis the numberof daysfrom the previousnestingattempt.The delayto relaying fledgingor failureof thefirstnestuntil thelayingof is the numberof daysfromfledgingor failureof the thefirsteggin thenextclutch.Filledsquares= delay first nestuntil the layingof the first eggin the next after successfulattempts;untilled squares= delay clutch.Laying,incubation,nestling,and fledgingreafterfailedattempts.Valuesareœwith 95%CI; numFIG.
3.
Interval between breeding attempts of White-browedScrubwrensaccordingto the fate of
fer to when the nestfailed;successful nestsproduced bers are sample sizes. one or moreyoungthat survivedat leastoneweek afterfledging.Valuesareœwith 95%CI; numbersare sample sizes. test,P > 0.05),perhapsbecauseof smallsam-
ple sizes.
The shortestinterval until relaying,which did not appearin the randomsampleabove, the seasonoccurredfor sequentialbroodsof 31 wastwo daysafterthe fledgingof a successful females,not merely for the populationas a brood.This wasthe only intervalshorterthan whole.The meanslopeof theregression for infivedaysthatwe recordedduringthestudy(n dividual females was -2.6 ___ SE of 0.7, which = 173, including multiple samplesfrom indiis significantly lessthanzero(t = 3.6,df = 30, vidual femaleswithin years),and in this case P = 0.001) but is not significantlydifferent thefemalecompleted buildingthenewnestbefrom the populationregression slopeof -3.6 (t foreheryounghadfledged. = 1.4, df = 30, P = 0.20). One extreme outlier Variability in the delay until relaying was wasdroppedfrom theseanalyses(a deformed higherif theinitialnestwassuccessful thanif nestlingthat had a longnestlingperiodcom- it failed, and the mean delay varied among paredwith nestlingsin an earlierbrood). years.If thenestwassuccessful, thedelayuntil Intervalbetween nestingattempts.--The inter- relayingrangedfrom12to 43 days,with aninval between the terminationof a nesting at- terquartilerangeof 11 days(n = 29); if a nest tempt and the initiationof layingof the next failed,thedelayrangedfrom5 to 22days,with clutchin the sameseasonwas longerif a nest an interquartilerangeof 4 days(n = 78;7 nests was successful(• = 21 days) than if it had that failed during laying were excluded).An failed (œ= 10 to 14 daysdependingon time of analysisof variancecontrollingfor the fateof failure; F = 26.1, df = 4 and 109, P < 0.001;Fig. thepreviousnest(failedor successful) revealed 3). We defineda successful nestasonein which no seasonaltrend in the intervaluntil relaying at least one young survived for at least one (F = 1.4, df = 1 and 100,P --- 0.20),but there week after leavingthe nest.The intervalap- wasa smalldifferenceamongyears(F = 2.9,df pearedto belongerif thenestfailedduringlay- = 4 and 100, P = 0.03;Fig. 4). ing (œ= 14 days)than at a laterstage(œ= 10 Careoffiedglings.--Young were fed by adults to 11 days),but the differencewasnot signifi- for a meanof 46 + SD of 5.7 daysafterleaving cant (Student-Newman-Keulsmultiple range thenest(range32.5to 57.5).All but4 of the30
April2000] TABLE 1.
Breeding ofWhite-browed Scrubwrens
Number
of clutches laid and number
of
successful broodsaraisedper femaleper seasonin White-browed
483
Scrubwrens.
200-
•'
x
180x
•,•
Num-
ber
1992 1993 1994 1995 1996 Total(%) Clutches
0 1 2 3 4 5 6
0 5 4 16 5 0 1
1 1 8 12 7 1 0
4 6 12 5 1 0 0
Successful
laid
0 2 10 10 5 0 2
0 2 7 13 4 0 2
5 (3.4) 16 (11.0) 41 (28.1) 56 (38.4) 22 (15.1) 1 (0.7) 5 (3.4)
160-
x
• 140-
._
ß
120-
•
100-
..c
c-
20-
broods
O-
0 1 2 3
9 7 12 3
6 17 7 0
17 11 0 0
9 15 5 0
9 12 7 0
50 (34.2) 62 (42.5) 31 (21.2) 3 (2.1)
Total
31
30
28
29
28
146
• Successful broodswerethosein whichat leastoneyoungsurvived until a week after fledging.
caseswerebetween39 and51 days.Theseanalyseswerebasedon a meanof 25 watches(6.25 h) on eachof 30 juvenilesin 15 broods. Breeding seasons.--Scrubwrens initiatedclutchesfromJulyuntil Januaryof thefollowingyear, with 96%of clutches beinginitiatedfromAugust to DecemberThus,thebreedingseason extended from the australwinter (Juneto August)until summer(Decemberto February).MacArthur's (1964)indexof thelengthof thebreedingseason was 5.4 months.
Scrubwrens laidup to sixclutches duringthe breedingseasonandraisedup to threebroods successfully (Table1). The numberof clutches laid, andparticularlythe numberof nestsproducing surviving fledglings, differed among years(numberlaid, X2= 22.0,df = 8, P = 0.005; successfulbroods, X2 = 32.5, df = 8, P = 0.0001;
x
31
29
24
ß
ß
ß
ß
92
93
94
95
29
28 ß
96
Year
F•G.5. Duration of the breedingseasonfor individual
female
White-browed
Scrubwrens
in each
year. Data are summarizedby boxplotsin which heavybarsdenotemedians,boxesdenoteinterquartile ranges,and verticallinesdenotethe rangeof values within 1.5 interquartilerangesof the top and bottom of the boxes; crosses are extreme values.
Numbersinsidefigure are samplesizes.
from 56.5 days in 1994 to 101 days in 1992 (X2 = 20.0, df = 4, P = 0.0005). DISCUSSION
White-browed
Scrubwrens
show all of the
featuresthat have been suggestedto distinguishthe "old endemic"passerines of Australia from the passerines of northtemperateregions (Ford 1989, Rowley and Russell 1991). They havesmall,relativelyconstantclutches, long breeding seasonscoupledwith multibrooding, and a long period of dependencyafter leavingthe nest.Like the few othermembers of the Pardalotidae that have been studied,
adjacentcellspooledto keepexpectedfrequenciesabovefive). In particular,mostof the femaleshad no successful breedingattemptsin 1994,the year with the shortestbreedingseason (seebelow). Themedianlengthof thebreedingseason for
White-browedScrubwrenslay their eggs at two-dayintervalsandhavelongincubationpe-
females
Tov1987).It is not knownwhy thesebirdshave small clutchsizes. Yom-Tov(1987) suggested
that
laid
at least one clutch
varied
amongyears, ranging from 42 days in 1994to 90 daysin 1996,with a maximumfor an individual of 183 daysin 1996(Kruskal-Wallistest, X2 = 20.3, df = 4, P = 0.0004;Fig. 5). Including only femalesthat laid at leasttwo clutches,the
riods.
Clutch size.iScrubwrens
usually laid a
three-eggclutch,whichis typicalof the old endemic passerines(Woinarski 1985, 1989; Yom-
that small clutches evolved when Australia
was
coveredby rainforestand were retainedin the lineagedespiteincreasedaridity,or that small clutchsizeis adaptivein environments with er-
medianlengthof the breedingseasonranged ratic rainfall. In contrast, Woinarski (1985) fa-
484
MAGRATHETAL.
[Auk, Vol. 117
manipulationof clutchsize vored Ashmole'shypothesisthat small clutch only experimental size results from an aseasonal environment in yielded equivocalresults(Poiani 1993).In parwhich mild winters allow high survival and ticular, starvationappears to be rare among there is no major peak of food in spring, re- nestling passerinesin Australia in general suitingin fewerresourcesper capitafor breed- (Ford 1989) and in scrubwrensin particular that ing (Ashmole1963,Ricklefs1980,Ford1989). (Magrathand Yezerinac1997),suggesting Ashmole'shypothesismay be relevant to foodsupplyduringthenestlingperiodis nota Australian birds, but little is known about the proximatelimit on clutchsize, therebychalseasonality of resources for insectivorous lengingthe aseasonality hypothesis. birds. Some authors state that the winter deLayinginterval.--Ithasoftenbeenstatedthat is one clinein foliagearthropodsin theevergreen for- the typicallaying intervalin passerines estsof temperateAustraliais relativelyminor day (Lack1968,WeltyandBaptista1988).This (Woinarski and Cullen 1984, Ford 1989, Ford misleadingstatementreflectsa phylogenetic and Recher1991),whereasothersemphasize bias in detailed studiesof passerinebreeding seasonalchanges(Recheret al. 1'991,1996). biology.Two-daylayingintervalsarethenorm Most informationrelatesto eucalyptfoliage,in in the Tyranni (Skutch1976,Astheimer1985, which arthropod abundancein spring is no Ricklefs1993), and they occurin severalfamimore than twice that in winter (Recheret al. lies of the Corvida (Courtneyand Marchant 1996). This increasepresumablyis far lower 1971).Moreover,two-day laying intervalsapthan in deciduousforestsand suggeststhat pearto be universalin thePardalotidae andthe (Marchant1986,Frith 1994), food is not superabundantduring breeding. Ptilonorhynchidae No study, however, has assessedseasonal theyoccurin somemembersof theCorviniand changesin arthropodabundanceacrossyears, the Artamini, and they are suspectedto occur leucophaea in the Climacteridae andnonehasspecifically measuredvariationin in Climacteris (Marchant1986). the majorfooditemsof scrubwrens. Indirect evidencesuggeststhat scrubwrens Giventhehigh risk of nestpredationin small suffer relatively minor seasonalchangesin passerines, long laying intervalsseemanomathatlonglayinginfood availability.First, severalspeciesof insec- lous.It hasbeensuggested tivorouspasserinesforagemore often on the tervalsare related to a female'sdifficulty in acgroundin winter than in summer,suggesting quiring food during egg formation(Thomas thatforagingonthegroundbecomes moreprof- 1974),but this is an unlikely proximatecause giventheirfixedlayinginterval. itablein winter, at leastcomparedwith above- in scrubwrens groundsites(Fordet al. 1990,Cale1994).These Two featuresof the Pardalotidaemay reduce findingssuggestthat scrubwrens,which are the costof longlayingintervals.First,theyare ground-feedingspecialiststhat can also feed hole or dome nesters,which may reducethe aboveground,are likely to sufferrelativelymi- risk of predationon theeggs.Theverylow dai(0.9%) nor seasonalvariationin food availability.Sec- ly rateof clutchmortalityin scrubwrens ond, scrubwrensin the study populationare supportsthis idea.Second,the longbreeding sedentaryand had an annualmortalityof only seasonmay mean that delaysin initiatingin15 to 20% (Magrathand Yezerinac1997),sug- cubation have little effect on the success of a gestingthat conditionsin winter were not se- brood. This contrast• with birds like the Great vere. Tit (Parusmajor),in whichdelaysof evena day beAlthoughthe small, fairly constantclutch or two may reduce reproductivesuccess sizesof endemicAustralianpasserinesare con- causeof rapid declinesin foodavailability(Petsistentwith Ashmole'shypothesis,there still tifor et al. 1988). The benefitsof two-daylaying intervalsare needs to be quantificationof seasonalconditions for breedingand an assessment of hy- unknown.One potentialbenefitis that it bepothesesfor the evolutionof clutchsizeunre- comesphysiologicallypossiblefor a femaleto lated to the directeffectof food supply(Wink- lay large eggs, which might improve the ler and Walters 1983, Murphy and Haukioja growthand survivalof young(Williams1994). 1986).For example,the role of nestpredation We suggesta secondand relatedbenefit:that and the life-history correlatesof clutch size for a giveneggand clutchsize,a femalewill not have not been adequatelyassessed, and the haveto carry as muchadditionalmassat any
April2000]
Breeding ofWhite-browed Scrubwrens
485
one time becauseof reducedtemporal overlap Blackbird(Turdusmerula),for example,the inin the development of eggs.In thismanner,the cubation period declines from 13.7 days in birdswouldavoidthelowerflightperformance March to 12.7 days in June(Snow 1958). Seaand subsequentincrease in vulnerability to sonaldeclinespresumablyresultfromtheeggs predationthataccompany increased bodymass being kept at optimal temperaturesfor a great(Witter and Cuthill 1993, Witter et al. 1994, er percentage of the time whenit is warmer,or
earlyin theseasonincubationdoesnot Gosleret al. 1995).A clutchof threeeggstrans- because startassoonasthelasteggis laid (Nilssonand scrubwren(R. Magrath unpubl. data), so the Svensson 1993).The synchronous hatchingof addedbody massthat would resultfrom a one- scrubwrennestlingssuggeststhat incubation day laying interval could substantially com- startsonor afterthedaythelasteggis laid.The promiseher agility duringthe layingperiod. large seasonaldecline in incubationlength Incubation andnestlingperiods.--Based on the probablyreflectsthe longbreedingseasonand equationsof Rahn et al. (1975),the incubation markedincreasein meantemperature;the seaperiodof scrubwrens(œ= 18.8days)is much son extends from midwinter (mean August longerthan the 14.9dayspredictedfor a pas- temperature = 6.9øC) to almost midsummer lates to about 63% of the mass of a female
serinelaying an egg of 2.7 g and still longer (meanJanuarytemperature= 20.3øC).Seasonal than the 13.9dayspredictedfor a passerineof changesin incubationlength might be more 12.8 g body mass (mean for breeding females markedin speciesin whichonly onesexincuin thispopulation;R. Magrathunpubl.data).In bates,but we know of no publisheddata that a comparativeanalysiscontrollingfor egg vol- are relevantto this question. ume,Ricklefs(1993)showedthat the long inThe nestlingperiod of scrubwrens(œ= 15 cubationperiodis a featureof the Pardalotidae days)is not unusualfor a small passerinethat in particular, rather than the Corvida as a builds a domed nest (seeLack 1968). We do not whole. knowwhy thenestlingperioddeclinesthrough The longperiodof incubationmightreflect the season;perhapsnestlingsgrow fasterlater the securityof holeor domenestsfoundin the in the season,or they can afford to leavethe Pardalotidae, or it maybe relatedto thespecies' nest sooner when ambient temperaturesare longevity (Ricklefs 1993). Hole nestsare rela- higher. dwly •,de from predators,and domenestsmay suffer reduced predation of eggs compared with open-cupnestsin similarlocations.Dome nestsalsomay offer greaterprotectionfrom inclementweather(H. Recherpers.comm.).Ricklefs (1993)suggestedthat long incubationpe-
Interval between nesting attempts.--Scrub-
wrensappearto havea longerintervalbetween nesting attempts(œ= 10 to 14 days after failed
attempts)than is typical of north temperate speciesin the Passerida.For example,Song Sparrows(Melospiza melodia) havean intervalof riodsassistin the maturationand subsequent about5 days,EuropeanStarlings(Sturnusvulefficiencyof the immunesystem,and in com- garis) 8 days (Welty and Baptista 1988), Eurparativestudieshe foundthat longincubation asianBlackbirds5 days (Magrath 1992), and periodsfor a given eggvolumewere associated American Robins (Turdusmigratorius)7 days with highannualadultsurvival(Ricklefs1993) (Weatherhead1990). Similarly, 11 speciesin and low prevalenceof bloodparasites(Ricklefs North Americahad a meanintervalof 8.6 days 1992).Thehigh annualsurvivalof scrubwrens (Ricklefs1966).In contrast,the delayuntil rewassimilarto thatof the in the study population(ca. 80% for females nestingin scrubwrens and85%for dominantmales;MagrathandYez- SplendidFairy-Wren(Malurussplendens; 5 to 14 erinac1997)and the maximumlongevityof at days; Rowley et al. 1991), an old endemic of least 17 years(R. Magrathunpubl.data) are Australia,andto thoseof fourNeotropicalspeconsistent with thishypothesis. cies(œ= 14 days;Ricklefs1966). The incubationperiod of scrubwrensdeThe longerand morevariabledelayuntil reclinedfrom about21 to 17 daysoverthebreed- nesting after a successfulattempt in scrubing seasonand was associated with a decline wrens (œ= 21 days)may relateto the costsof for eachfemale.Incubationperiodstend to be caringfor fledglingsand the variabilityin the shorterwhenambienttemperatures arehigher duration of care by females(A. Leedman and (Skutch1976,O'Connor1984).In the Eurasian R. Magrathunpubl.data).Again,themeande-
486
MAGRATH ETAL.
lay is moresimilarto thoseof Neotropicalspecies(œ= 29 days)than to thoseof Nearcticspecies (œ= 8.5 days;Ricklefs1966), reinforcing the suggestionthat the life historiesof south temperatespeciesare more similar to thoseof tropicalspeciesthan to thoseof north temperate species(Martin 1996), or at least that they are intermediate between the two groups (Rowley and Russell1991). The yearly variation in the interval between nestingattemptsgenerallyhad a similarinfluenceon the delayafter a failedor successful attempt.The meandelaywaslongestin 1994,the year with the fewestbreedingattemptsandthe shortestbreeding season(see below). These data suggestthat female scrubwrensface energetic constraintsin the timing of relaying, particularlyif their previousnestsare successful, or that they assess conditionsfor breeding beforethey attemptanotherclutch. Postfledging care.--Theperiodofpostfledging care of young scrubwrens(ca. 6 to 7 weeks)is longerthanthat of northtemperatespecies but similarto or shorterthan that of tropicalspecies(Skutch1976).Small passerinesin north temperatelatitudestypicallybecomenutritionally independentof their parentstwo to four weeks after leaving the nest (Skutch 1976, O'Connor1984).The long periodof postfledging care in scrubwrenssupportsRowley and Russell's(1991)suggestionthat parentalcareis prolonged in Australian passerines.Fogden (1972)suggestedthat the longperiodof careof passerinesin Sarawakresultedfrom the difficulty of findingsuitableprey.Thatis, if insects are sparselydistributedand havemany forms of antipredatorydefense,it may take a long time for youngbirds to learn how to forageefficiently.We suggestan explanation thatis related to seasonalityof food supplies.If the seasonalincrementavailablefor breedingis small thentheyoungmaynotfledgeduringa period of food abundance, which is in contrast to
[Auk, Vol. 117
The few data on old endemic Corvida
of Aus-
tralia suggestthat a long period of postfledging careis common.Pardalotidstypicallyhave periods of postfledgingcare of 6 to 7 weeks (BrownThornbill[Acanthiza pusilia],D. J.Green pers. comm.; Yellow-rumped [A. chrysorrhoa] and Buff-rumped [A. reguloides] thornbills,D. Ebert pers. comm.;SpeckledWarbler [Chthonicolasagittatus],J. Gardner pers. comm.).Similarly, HelmetedHoneyeaters(Lichenostomus melanops)do not reach80% self sufficiencyuntil about6 to 8 weeksafterleavingthenestandare occasionally fed up to 14 weeks(Franklinet al. 1996),and RufousWhistlers(Pachycephala ruffventris)are fed for at least 8 weeks (Bridges 1994). Speciesof Malurus appear to be an exceptionin that SplendidFairy-Wrens(Rowley et al. 1991) and Superb Fairy-Wrens(M. cyaneus;A. Cockburnpers. comm.) reach independencein about4 weeks.Among the large Corvida, extremely long periods of parental careoccurin White-wingedChoughs(Corcorax melanorhamphos; ca. 29 weeks;Heinsohn1991) and SuperbLyrebirds(Menuranovaehollandiae; ca. 37 weeks;Lill 1986). Lengthof breeding season andmultibrooding.The 5.4-monthbreedingseasonof scrubwrens is typical of thoseof tropicalbirds (3.9 to 7.8 months)but longer than thoseof north temperate species(2.7 to 3.1 months; Ricklefs 1966).Thebreedingseasonappearsto be at the long end of range among the Pardalotidae (Woinarski1985).It is similar to that estimated for the SpottedPardalote(Pardalotus punctatus)
but abouttwo monthslongerthan thatfor the Buff-rumped Thornbill and the Chestnut-rumped Thornbill(Acanthiza uropygialis). Evencontrolling for the effectof latitude(onemonthper 11ø;Wyndham 1986), the Pardalotidaeexamined by Woinarski (1985) have long breeding
seasons (3 to 5 months)relativeto ecologically comparable Northern Hemisphere species, whichtypicallyhavebreedingseasons of 2 to 3
manynorth temperatespecies.Thus,theyoung months. Our data from White-browed Scrubwrens may takelongerto acquirethe necessary skills for survival,notbecause Australianarthropods support Rowley and Russell's(1991) conclurequireparticular skill to find and eat, but be- sion that variation in reproductiveeffort in causea greaterlevel of skill is required for sur- Australianpasserines comesnot throughdifvival when food is not abundant. This second ferencesin clutchsize,but throughvariationin hypothesisseemsmore plausible,becauseit the numberof breedingattemptsper season. In doesnot requirethe assumption thatmoreskill contrastto the durationof individualbreeding or learningis requiredto capturearthropodsin attempts,thelengthof thebreedingseason and differentgeographicregions. the numberof breedingattemptsper yearvar-
April 2000]
Breeding ofWhite-browed Scrubwrens
ied significantly among years. However, it is
unclearwhethermultibrooding perseisanimportant differencebetween passerinesin Aus-
tralia versusthosein northtemperateregions (e.g.Woinarski1985,Rowleyand Russell1991).
Martin (1996) argued such differenceshave been overstated,becausemany north temperate specieshavemultiplebroods(seeCricket al. 1993). Doesa generallife-history"syndrome" existfor Australian old endemics?--Our
data show that
the breedingcycle of White-browedScrubwrensis slowcomparedwith thoseof Northern Hemisphere passerines, particularlyin having a two-daylaying interval,a longincubationperiod, and a long period of postfledgingparental care.However,thesedifferencesappearto be characteristic of the Pardalotidae, and possiblysomeotherfamilies,but not of the old endemicCorvidain general.Overall,the suggestionthata generalsyndromeof leisurelyreproduction exists among Australian passerines originatesfrom a sample of leaf-gleaninginsectivores, with all of the Australianrepresentativescomingfrom the Pardalotidae(Woinarski 1985,Ford 1989). Clearly,a more representativesampleof taxais required.White-browed Scrubwrensappearto be typical of old endemic Australianpasserines in havinga smallclutch size (Yom-Tov1987) and a long interval between nesting attempts,and they resemble
487
Sam Portelli, and Linda Whittingham. Membersof the "fairy-wren group," includingAndrew Cockburn, Mike Double, Peter Dunn, David Green, Michelle Hall, Milton Lewis, and Raoul Mulder, also
helped catchand band birds. Sam Portelli was remarkablyefficientgettingthe data from field sheets into computerfiles. Hugh Ford, Harry Recher,and JeffWaltersmadehelpful commentson a draft of the paper.Membersof the AustralianBird andBatBanding Scheme,especiallyBarry Baker,BelindaDeftman, and JamiePook,have alwaysbeensupportive of this study and in recent yearshave even moved their officeinto our study site!Finally,we are grateful for financialsupportto RDM from the Australian Research Council.
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AssociateEditor: J. R. Walters
