TheAuk 117(2):479-489, 2000

LIFE IN THE SLOW LANE: REPRODUCTIVE LIFE HISTORY OF THE WHITE-BROWED SCRUBWREN, AN AUSTRALIAN ENDEMIC

ROBERTD. MAGRATH,• ASHLEYW. LEEDMAN,JANET L. GARDNER, ANTHONY GIANNASCA, ANJELI C. NATHAN, STEPHENM. YEZERINAC, AND JAMESA. NICHOLLS Divisionof Botanyand Zoology, Australian National University, Canberra 0200,

ABSTRACT.--Anunderstanding of geographicand phylogeneticvariation in passerinelife historiesis hamperedby the scarcityof studiesfrom the SouthernHemisphere. We docu- mentedthe breedingbiology of the White-browedScrubwren ( frontalis), an Aus- tralia endemicin the Pardalotidae(parvorder ). Like othermembers of the Pardal- otidae,scrubwrens had a longlaying interval (two days),a long incubationperiod (declining from 21 to 17 daysthrough the season),and a long periodof postfiedgingparental care (6 to 7 weeks).Scrubwrens appeared to be typicalof the AustralianCorvida in havinga small clutchsize (threeeggs) and a longbreeding season (5.4 months), and they alsohad a long intervalbetween breeding attempts (10 daysafter a failed attempt,21 daysafter a successful attempt). Scrubwrenswere multibrooded,often raising two broodssuccessfully and occa- sionallyraising three broods.The breedingbiology of scrubwrensadds further supportto claimsof a distinctlife-history strategy for membersof the Corvidabut alsoreinforces ev- idencethat some"Corvida" life-history traits more specifically are those of thePardalotidae. Received17 November1998, accepted18 October1999.

MOSTSTUDIES of thebreeding biology of pas- few specieshave been studied(e.g. serines have been carried out in the Northern pusilia,A. reguloides,and A. lineata[Bell and Ford Hemisphere,primarily on membersof the par- 1986];A. chrysorrhoa[Ford 1963];Sericornis fron- vorder (sensu Sibley and Ahlquist talis [Ambroseand Davies 1989];Pardalotus spp. 1990).This biases our understandingof passer- [Woinarskiand Bulman 1985]).Even for these ine biologybecause these species are not rep- species,sample sizes often are small,and quan- resentativeof passerinesas a whole. For ex- titativedata do notcover the whole breeding cy- ample, the Australian Corvida have smaller cle. Indeed, for each of thesespecies, little is clutchsizes than passerinesthat breedat sim- knownabout postfledging care, duration of the ilar latitudesin the NorthernHemisphere and breeding season,and number of breeding at- Passeridathat are residentin Australia (Yom- temptsper seasonmade by individual females. Tov 1987, 1994; Rowley and Russell 1991). It Here, we provide a quantitative description has also been claimed that members of the "old of the breedingbiology of a populationof the endemic" Corvida of Australia have a syn- White-browedScrubwren (Sericornis frontalis), dromeof slowreproduction, with smallclutch a sedentary,cooperatively breeding species in the Pardalotidae that is common in southern sizes,prolonged periods of parentalcare at all and eastern Australia. Ours is the first detailed stagesof nesting, and long breeding seasons (Ford 1989, Rowley and Russell 1991). Never- study of the breedingcycle and breedingsea- theless, other than clutch size, most features of sonof any memberof the genusand is based the breedingbiology of thesespecies are not on data gatheredfrom a color-markedpopu- well known,and comparisonsof 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 as a first step toward disentanglingthe (Martin 1996). effectsof environmentand phylogenyon the Althoughthe 49 speciesin the Pardalotidae life historyof . that are residentin Australiaappear to epito- mize the syndromeof slowreproduction, only a METHODS

Studyspecies.--The White-browed Scrubwren is a E-mail: robert.magr ath@anu. edu. au small (ca. 11 to 15 g) passerinethat is endemicto

479 480 MAGRATHET AL. [Auk, Vol. 117 mainland Australia (Christidis and Boles1994). It is hatchingdate and regressionof incubationperiod on oneof six membersof the genusendemic to Austra- laying date (seebelow). lia. White-browedScrubwrens are largelysedentary The incubationperiod was definedas the period as adults (Brown et al. 1990, Wilson 1994) and breed from the layingof the lastegg in the clutchuntil the in diversehabitats from coastalrainforest to alpine completionof hatching.The dateof hatchingwas de- heath (Blakerset al. 1984).Scrubwrens feed primar- terminedfrom daily visitsto neststoward the end of ily on arthropodson theground or in low shrubs,but theincubation period. We did not flushfemales from they alsosearch under bark or in foliage,sometimes nestsduring this period, so we were unableto in- in 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 youngnestlings to usuallyis well hiddenunder leaf-litter or vegetation, estimatethe day of hatching(Magrath and Yezerinac on or near the ground.White-browed Scrubwrens 1997).We gaveeach nestling a uniquecombination are known to breed cooperatively(Bell 1982, Am- of colorbands when it was 9 or 10 daysold. brose and Davies 1989), including our study popu- To quantifythe durationof postfledgingparental lation (see below). care,we watched30 focalfledglings in 15broods sev- We studied a color-bandedpopulation of S.f. fron- eral times a week for 15 min during 1993 and re- talisin and adjacentto the AustralianNational Bo- cordedwhether they were fed by an adult during tanic Gardens (35ø16'S, 149ø06'E) in Canberra from this period.Watches usually were conductedon dif- 1992to 1996.The Gardensoccupy an area of 40 ha, ferentdays, but a few fledglingswere watchedtwice 27 ha of which are plantedexclusively with Austra- per day,separated by severalhours. The dateof ter- lian native plants.Most of the remaining13 ha are minationof parentalcare was takento be the mid- naturalwoodlands that are contiguouswith a large point from the lastwatch in whichwe sawthe young area of natural habitat in which scrubwrens breed. beingfed and the first watchof a sequenceof at least Althoughbreeding extended beyond the end of De- three watchesin which we did not seeit beingfed. cemberin eachseason, we refer to the seasonby the Thesetwo dateswere a medianof three daysapart year in whichbreeding began. (range 0 to 11). White-browedScrubwrens are residentthrough- Dataanalyses.--We analyzed data with SPSS(No- out the year,and duringthe breeding season we vis- rusis1995). We usedparametric statistics whenever ited territories at least three times a week to docu- assumptionsof the analysesappeared to be met or ment reproductive attempts. Between 35 and 48 the data could be transformed to meet those as- breeding groups were present in any one breeding sumptions.Data that were transformedfor analyses season.Scrubwrens typically bred in pairs (46% of were back-transformedfor presentationin the text. groups) or in trios consistingof a sociallydominant When we had data (e.g.clutch size, incubation, and pair and a subordinatemale (44%),although 10% of nestlingperiods) from more than one nestof a fe- the groupshad more than one subordinatemale male in a given year, we randomly selecteda single (Magrathand Whittingham1997). Only the female attemptto maintain statisticalindependence. Sample builds the nest and incubates, but both members of sizes varied among analyses because nests were the dominantpair, and often the subordinatemales, found at different times during the breedingcycle provisionthe nestlings(Magrath and Whittingham and becausemany nestsfailed before fledging (see 1997).Neither group size nor provisioningby sub- Magrath and Yezerinac1997). Analyses of timing of ordinate males had a detectable effect on the dura- breeding and number of attempts per seasonwere tion of any stageof the reproductivecycle, the inter- restrictedto femalesthat we followedsufficiently val between nesting attempts,or the reproductive closelyto detecteach nesting attempt. successof the group (Magrathand Yezerinac1997). As an index of the lengthof the breedingseason, Field methods.--We determined the sex of birds in we calculatedthe numberof "equallygood months the field from the color of the lores (malesblack, fe- for breeding"following MacArthur (1964:394).This males brown; Rogers et al. 1986). We detected no entailedentering the proportionof clutchesinitiated "brown-loredmales," which might occurin 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 found by watchingbuilding females,following value. femalesback to the nest during incubation,or fol- lowingadults that were feeding nestlings. Most nests RESULTS were on or near the ground.If a nestwas foundbe- forelaying in 1992,it waschecked daily to determine the date of laying of eachegg in the clutch.In sub- Clutchsize and layinginterval.--Most scrub- sequentyears, we checkednests only to determine clutchescontained three eggs (93.6% of the dateon which the first eggwas laid (the "laying 171),although nine clutcheshad two eggs,one date").If the nestwas not founduntil aftereggs had had one egg, and onehad four eggs,giving a been laid, the laying date was estimatedfrom the meanclutch size of 2.94 eggs.We did not mark April 2000] Breedingof White-browedScrubwrens 481

23 19

18 ß

17 ......

16 ...... o 20 15 õ •9

17

Aug Sep Oct Nov Dec Jan Feb 16 11 , i • i [ I [ I • I • I 30 60 90 120 150 180 30 60 90 120 150 180 210 240

Laying date (1 = 1 July) Hatching date (1 = 1 July) F•G.1. Seasonalchange in the incubationperiod FIG. 2. Seasonalchange in the nestlingperiod of of White-browed Scrubwrenswith laying date (y = White-browedScrubwrens with hatchingdate (y = 28.7 - 5.2411og•0x],n = 92, r2 = 0.51,P < 0.0001).The 22.4 - 3.5511og,0x],n = 124, r 2 = 0.23, P < 0.001). three outliers shown as crosses were not included in the regression. ed in the sampleonly onceper year),or to some seasonal factor that affected each individual fe- eggsduring laying, so it is probablethat some male.We addressedthis issue by examiningthe clutchesof lessthan three eggsresulted from slopeof the regressionof incubationperiod on eggloss during layingor incubation.Eggs were date (log transformed)for individual females laid at two-day intervalsin all 35 caseswhere for whom we had measures of the incubation the interval was known accurately.The 35 in- period for different clutcheswithin a season. tervals include 13 casesof first to secondegg The mean slopeof the regressionwas -5.0 + and 22 casesof secondto third egg.These data SE of 0.6, which is significantlyless than zero come from 27 clutcheslaid by 21 different fe- (t = 8.4, df = 34, P < 0.001)but is not signifi- males. cantlydifferent from the populationregression Incubationperiod.--The mean incubationpe- slopeof -5.2 (t = 0.4, df = 34, P = 0.70).Thus, riod was 18.8 _+SD of 1.3 days (n = 95), ranging the seasonaldecline in lengthof the incubation from 17 to 22 days.Excluding the three cases of period affectedindividual femalesand wasnot a 22-day incubation period (outliers) gives a a consequenceof differentfemales laying at dif- mean valueof 18.7 __+1.2 days.Only clutchesof ferent dates. three were used to calculateincubation peri- Nestlingperiod.--Eggs in a clutch hatched ods. roughlysynchronously. In 37 out of 45 broods A dramaticdecline in the length of the in- (82%), all nestlingshad hatchedbetween in- cubation period (from 21 to 17 days) occurred spectionsof nest contentson sequentialdays; overthe courseof the breedingseason (Fig. 1). in the remaining8 broods,all nestlingshad We detectedno differencebetween years in the hatchedby the next day. This implies that mean incubationperiod or in the slopeof de- hatchingusually takes place over a few hours, cline (ANOVA, including date as a covariate, or perhapsthat it occursovernight. year effectafter droppinginteraction term, F = The mean nestlingperiod was 15.1 __+SD of 0.5, df = 4 and 86, P = 0.80; year x date inter- 1.1 days (n = 124, range 12 to 18 days).The action, F = 1.9, df = 4 and 82, P = 0.12; outliers nestlingperiod declined through the breeding identified in Fig. I were excludedfrom analy- season(Fig. 2), and neither the mean nor the ses). pattern of seasonaldecline differed among The seasonaldecline in incubationperiod il- 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 different incubationabilities lay- interaction, F = 1.5, df = 4 and 114, P = 0.20). ing at differentdates (each female is represent- The declinein the nestlingperiod through 482 MAGRATHET AL. [Auk, Vol. 117

4O 2O

3O

15 3t8 10 t5 t 17+ 52 10 14 171•116

I i i i i i i i i 0 • 92 93 94 95 96 Laying Incubation Nestling FledgingSuccessful Year Fate of previousnesting attempt FIC. 4. Yearly variationin the interval between FIG. 3. Interval between breeding attempts of breeding attemptsof White-browedScrubwrens. White-browedScrubwrens according to the fate of The delay to relayingis the numberof daysfrom the previousnesting attempt. The delayto relaying fledgingor failureof the first nestuntil thelaying of is the numberof daysfrom fledging or failureof the the firstegg in the nextclutch. Filled squares= delay first nestuntil the layingof the first eggin the next after successfulattempts; untilled squares= delay clutch.Laying, incubation, nestling, and fledgingre- afterfailed attempts. Values are œ with 95%CI; num- fer to when the nestfailed; successful nests produced bers are sample sizes. one or more youngthat survivedat leastone week afterfledging. Values are œ with 95%CI; numbersare sample sizes. test,P > 0.05),perhaps because of smallsam- ple sizes. The shortestinterval until relaying, which did not appearin the random sampleabove, the seasonoccurred for sequentialbroods of 31 wastwo daysafter the fledgingof a successful females,not merely for the populationas a brood.This was the only intervalshorter than whole.The meanslope of the regressionfor in- five daysthat we recordedduring the study(n dividual females was -2.6 ___SE of 0.7, which = 173, including multiple samplesfrom indi- is significantlyless than zero (t = 3.6, df = 30, vidual femaleswithin years),and in this case P = 0.001) but is not significantlydifferent thefemale completed building the new nest be- from the populationregression slope of -3.6 (t foreher younghad fledged. = 1.4, df = 30, P = 0.20). One extreme outlier Variability in the delay until relaying was was droppedfrom theseanalyses (a deformed higherif the initialnest was successful than if nestlingthat had a long nestlingperiod com- it failed, and the mean delay varied among paredwith nestlingsin an earlierbrood). years.If the nestwas successful, the delayuntil Intervalbetween nesting attempts.--The inter- relayingranged from 12 to 43 days,with anin- val between the terminationof a nesting at- terquartilerange of 11 days (n = 29); if a nest tempt and the initiationof laying of the next failed,the delay ranged from 5 to 22days, with clutchin the sameseason was longerif a nest an interquartilerange of 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 daysdepending on time of analysisof variancecontrolling for the fate of failure; F = 26.1, df = 4 and 109, P < 0.001;Fig. theprevious nest (failed or successful)revealed 3). We defineda successfulnest as one in 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 smalldifference among years (F = 2.9, df pearedto be longerif thenest failed during lay- = 4 and 100, P = 0.03; Fig. 4). ing (œ= 14 days)than at a later stage(œ = 10 Careoffiedglings.--Young were fed by adults to 11 days),but the differencewas not signifi- for a mean of 46 + SD of 5.7 days after leaving cant (Student-Newman-Keulsmultiple range thenest (range 32.5 to 57.5).All but 4 of the30 April 2000] BreedingofWhite-browed Scrubwrens 483

TABLE 1. Number of clutches laid and number of successfulbroods a raised per femaleper seasonin 200- White-browed Scrubwrens. •' 180- x x

Num- •,• 160- x ber 1992 1993 1994 1995 1996 Total(%) • 140-

Clutches laid ß 120- 0 0 1 4 0 0 5 (3.4) • 100- 1 5 1 6 2 2 16 (11.0) ._ 2 4 8 12 10 7 41 (28.1) 3 16 12 5 10 13 56 (38.4) 4 5 7 1 5 4 22 (15.1) 5 0 1 0 0 0 1 (0.7) ..c 6 1 0 0 2 2 5 (3.4) c- 20- Successful broods O- x 31 29 24 29 28 0 9 6 17 9 9 50 (34.2) ß ß ß ß ß 1 7 17 11 15 12 62 (42.5) 92 93 94 95 96 2 12 7 0 5 7 31 (21.2) Year 3 3 0 0 0 0 3 (2.1) Total 31 30 28 29 28 146 F•G.5. Duration of the breeding seasonfor indi- vidual female White-browed Scrubwrens in each • Successfulbroods were thosein whichat leastone young survived until a week after fledging. year. Data are summarizedby boxplotsin which heavybars denote medians, boxes denote interquar- tile ranges,and verticallines denote the rangeof val- ues within 1.5 interquartileranges of the top and caseswere between 39 and51 days.These anal- bottom of the boxes; crosses are extreme values. yseswere based on a meanof 25 watches(6.25 Numbersinside figure are samplesizes. h) on eachof 30 juvenilesin 15 broods. Breedingseasons.--Scrubwrens initiated clutch- from 56.5 days in 1994 to 101 days in 1992 (X2 es fromJuly until Januaryof the followingyear, = 20.0, df = 4, P = 0.0005). with 96%of clutchesbeing initiated from August to DecemberThus, the breeding season extended DISCUSSION from the australwinter (Juneto August)until summer(December to February).MacArthur's White-browed Scrubwrens show all of the (1964)index of thelength of thebreeding season featuresthat have been suggestedto distin- was 5.4 months. guishthe "old endemic"passerines of Austra- Scrubwrenslaid up to sixclutches during the lia from the passerinesof north temperatere- breedingseason and raised up to threebroods gions (Ford 1989, Rowley and Russell 1991). successfully(Table 1). The numberof clutches They have small, relativelyconstant clutches, laid, andparticularly the numberof nestspro- long breeding seasonscoupled with multi- ducing surviving fledglings, differed among brooding, and a long period of dependencyaf- years (numberlaid, X2= 22.0, df = 8, P = 0.005; ter leavingthe nest.Like the few other mem- successfulbroods, X2 = 32.5, df = 8, P = 0.0001; bers of the Pardalotidae that have been studied, adjacentcells pooled to keepexpected frequen- White-browed Scrubwrenslay their eggs at ciesabove five). In particular,most of the fe- two-dayintervals and have long incubation pe- maleshad no successfulbreeding attempts in riods. 1994,the year with the shortestbreeding sea- Clutch size.iScrubwrens usually laid a son (seebelow). three-eggclutch, which is typicalof the old en- Themedian length of thebreeding season for demic passerines(Woinarski 1985, 1989; Yom- females that laid at least one clutch varied Tov 1987).It is not knownwhy thesebirds have among years, ranging from 42 days in 1994 to small clutch sizes. Yom-Tov(1987) suggested 90 daysin 1996,with a maximumfor an indi- that small clutches evolved when Australia was vidual of 183 daysin 1996 (Kruskal-Wallistest, coveredby rainforestand were retainedin the X2 = 20.3, df = 4, P = 0.0004;Fig. 5). Including lineagedespite increased aridity, or that small only femalesthat laid at leasttwo clutches,the clutchsize is adaptivein environmentswith er- medianlength of the breedingseason ranged ratic rainfall. In contrast, Woinarski (1985) fa- 484 MAGRATHET AL. [Auk, Vol. 117 vored Ashmole'shypothesis that small clutch only experimentalmanipulation of clutchsize size results from an aseasonal environment in yielded equivocalresults (Poiani 1993).In par- which 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 suiting in fewer resourcesper capitafor breed- (Ford 1989) and in scrubwrensin particular ing (Ashmole1963, Ricklefs 1980, Ford 1989). (Magrathand Yezerinac1997), suggesting that Ashmole'shypothesis may be relevant to foodsupply during the nestlingperiod is not a Australian birds, but little is known about the proximatelimit on clutchsize, therebychal- seasonality of resources for insectivorous lengingthe aseasonalityhypothesis. birds. Some authors state that the winter de- Layinginterval.--It has often been stated that clinein foliagearthropods in theevergreen for- the typical laying intervalin passerinesis one estsof temperateAustralia is relativelyminor day (Lack1968, Welty and Baptista1988). This (Woinarski and Cullen 1984, Ford 1989, Ford misleadingstatement reflects a phylogenetic and Recher1991), whereasothers emphasize bias in detailed studiesof passerinebreeding seasonalchanges (Recher et al. 1'991,1996). biology.Two-day laying intervals are the norm Most informationrelates to eucalyptfoliage, in in the Tyranni (Skutch1976, Astheimer1985, which arthropod abundancein spring is no Ricklefs1993), and they occur in severalfami- more than twice that in winter (Recheret al. lies of the Corvida (Courtneyand Marchant 1996). This increasepresumably is far lower 1971). Moreover,two-day laying intervalsap- than in deciduousforests and suggeststhat pearto be universalin thePardalotidae and the food is not superabundantduring breeding. Ptilonorhynchidae(Marchant 1986, Frith 1994), No study, however, has assessedseasonal theyoccur in somemembers of the Corviniand changesin arthropodabundance across years, the Artamini, and they are suspectedto occur andnone has specifically measured variation in in Climacterisleucophaea in the Climacteridae the majorfood itemsof scrubwrens. (Marchant 1986). Indirect evidencesuggests that scrubwrens Giventhe high risk of nestpredation in small suffer relatively minor seasonalchanges in passerines,long laying intervalsseem anoma- food availability.First, severalspecies of insec- lous.It hasbeen suggested that longlaying in- tivorouspasserines forage more often on the tervals are related to a female'sdifficulty in ac- groundin winter than in summer,suggesting quiring food during egg formation(Thomas thatforaging on theground becomes more prof- 1974),but this is an unlikely proximatecause itablein winter, at leastcompared with above- in scrubwrensgiven their fixed laying interval. groundsites (Ford et al. 1990,Cale 1994). These Two featuresof the Pardalotidaemay reduce findingssuggest that scrubwrens,which are the costof longlaying intervals. First, they are ground-feedingspecialists that can also feed hole or dome nesters,which may reduce the aboveground, are likely to sufferrelatively mi- risk of predationon the eggs.The verylow dai- nor seasonalvariation in food availability.Sec- ly rateof clutchmortality in scrubwrens(0.9%) ond, scrubwrensin the study populationare supportsthis idea. Second,the longbreeding sedentaryand had an annualmortality of only seasonmay mean that delaysin initiating in- 15 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 whichdelays of evena day Although the small, fairly constantclutch or two may reduce reproductivesuccess be- sizesof endemicAustralian passerines are con- causeof rapid declinesin food availability(Pet- sistentwith Ashmole'shypothesis, there still tifor et al. 1988). needs to be quantificationof seasonalcondi- The benefitsof two-daylaying intervalsare tions for breedingand an assessmentof hy- unknown.One potentialbenefit is that it be- pothesesfor the evolutionof clutchsize unre- comesphysiologically possible for a femaleto lated to the directeffect of food supply(Wink- lay large eggs, which might improve the ler and Walters 1983, Murphy and Haukioja growthand survivalof young(Williams 1994). 1986).For example,the role of nestpredation We suggesta secondand relatedbenefit: that and the life-history correlatesof clutch size for a givenegg and clutchsize, a femalewill not have not been adequatelyassessed, and the haveto carry as muchadditional mass at any April 2000] BreedingofWhite-browed Scrubwrens 485 one time becauseof reducedtemporal overlap Blackbird(Turdus merula), for example,the in- in the developmentof eggs.In thismanner, the cubation period declines from 13.7 days in birdswould avoid the lower flight performance March to 12.7 days in June(Snow 1958). Sea- and subsequentincrease in vulnerability to sonaldeclines presumably result from theeggs predationthat accompanyincreased body mass being kept at optimal temperaturesfor a great- (Witter and Cuthill 1993, Witter et al. 1994, er percentageof the time whenit is warmer,or Gosleret al. 1995).A clutchof threeeggs trans- becauseearly in the seasonincubation does not lates to about 63% of the mass of a female startas soon as the lastegg is laid (Nilssonand scrubwren(R. Magrath unpubl. data), so the Svensson1993). The synchronoushatching of addedbody massthat would resultfrom a one- scrubwrennestlings suggests that incubation day laying interval could substantially com- startson or afterthe day the last egg is laid.The promiseher agility duringthe laying period. large seasonaldecline in incubationlength Incubationand nestling periods.--Based on the probablyreflects the longbreeding season and equationsof Rahn et al. (1975),the incubation markedincrease in meantemperature; the sea- periodof scrubwrens(œ = 18.8 days)is much son extends from midwinter (mean August longerthan the 14.9 dayspredicted for a pas- temperature = 6.9øC) to almost midsummer serine laying an egg of 2.7 g and still longer (meanJanuary temperature = 20.3øC).Seasonal than the 13.9days predicted for a passerineof changesin incubationlength might be more 12.8 g body mass (mean for breeding females markedin speciesin whichonly one sexincu- in thispopulation; R. Magrathunpubl. data). In bates,but we know of no publisheddata that a comparativeanalysis controlling for egg vol- are relevantto this question. ume, Ricklefs(1993) showed that the long in- The nestlingperiod of scrubwrens(œ = 15 cubationperiod is 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 thenestling period declines through The long periodof incubationmight reflect the season;perhaps nestlings grow fasterlater the securityof hole or domenests found in 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 nests are rela- higher. dwly •,de from predators,and dome nestsmay Interval between nesting attempts.--Scrub- suffer reduced predation of eggs compared wrensappear to havea longerinterval between with open-cupnests in similarlocations. Dome nesting attempts (œ= 10 to 14 days after failed nestsalso may offer greaterprotection from in- attempts)than is typical of north temperate clementweather (H. Recherpers. comm.). Rick- speciesin the Passerida.For example,Song lefs (1993)suggested that long incubationpe- Sparrows(Melospiza melodia) have an intervalof riods assistin the maturationand subsequent about 5 days, EuropeanStarlings (Sturnus vul- efficiencyof the immunesystem, and in com- garis) 8 days (Welty and Baptista 1988), Eur- parativestudies he foundthat long incubation asian Blackbirds5 days (Magrath 1992), and periodsfor a given egg volumewere associated American Robins (Turdusmigratorius) 7 days with high annualadult survival(Ricklefs 1993) (Weatherhead1990). Similarly, 11 speciesin and low prevalenceof bloodparasites (Ricklefs North Americahad a meaninterval of 8.6 days 1992).The high annualsurvival of scrubwrens (Ricklefs1966). In contrast,the delayuntil re- in the study population(ca. 80% for females nestingin scrubwrenswas similar to thatof the and85% for dominantmales; Magrath and Yez- SplendidFairy-Wren (Malurus splendens; 5 to 14 erinac1997) and the maximumlongevity of at days; Rowley et al. 1991), an old endemic of least 17 years (R. Magrathunpubl. data) are Australia,and to thoseof four Neotropicalspe- consistentwith this hypothesis. cies(œ = 14 days;Ricklefs 1966). The incubation period of scrubwrensde- The longerand morevariable delay until re- clinedfrom about21 to 17 daysover the breed- nesting after a successfulattempt in scrub- ing seasonand was associatedwith a decline (œ= 21 days)may relateto the costsof for eachfemale. Incubation periods tend to be caringfor fledglingsand the variabilityin the shorterwhen ambienttemperatures are higher duration of care by females (A. Leedman and (Skutch1976, O'Connor 1984). In the Eurasian R. Magrathunpubl. data). Again, the meande- 486 MAGRATHET AL. [Auk, Vol. 117 lay is moresimilar to thoseof Neotropicalspe- The few data on old endemic Corvida of Aus- cies(œ = 29 days)than to thoseof Nearcticspe- tralia suggestthat a long period of postfledg- cies (œ= 8.5 days; Ricklefs1966), reinforcing ing careis common.Pardalotids typically have the suggestionthat the life historiesof south periods of postfledgingcare of 6 to 7 weeks temperatespecies are more similar to thoseof (BrownThornbill [Acanthiza pusilia], D. J.Green tropical speciesthan to thoseof north temper- pers. comm.; Yellow-rumped [A. chrysorrhoa] ate species(Martin 1996), or at least that they and Buff-rumped [A. reguloides]thornbills, D. are intermediate between the two groups Ebert pers. comm.;Speckled Warbler [Chthoni- (Rowley and Russell1991). colasagittatus], J. Gardner pers. comm.). Simi- The yearly variation in the interval between larly, HelmetedHoneyeaters (Lichenostomus me- nestingattempts generally had a similar influ- lanops)do not reach 80% self sufficiencyuntil enceon the delayafter a failed or successfulat- about6 to 8 weeksafter leavingthe nestand are tempt.The meandelay was longest in 1994,the occasionallyfed up to 14 weeks(Franklin et al. year with the fewestbreeding attempts and the 1996),and RufousWhistlers (Pachycephala ruff- shortestbreeding season(see below). These ventris)are fed for at least 8 weeks (Bridges data suggestthat female scrubwrensface en- 1994). Speciesof Malurus appear to be an ex- ergetic constraintsin the timing of relaying, ceptionin that Splendid Fairy-Wrens(Rowley particularly if their previousnests are success- et al. 1991) and Superb Fairy-Wrens (M. cy- ful, or that they assessconditions for breeding aneus;A. Cockburnpers. comm.) reach inde- beforethey attemptanother clutch. pendencein about 4 weeks. Among the large Postfledgingcare.--The period of postfledging Corvida, extremely long periods of parental care of young scrubwrens(ca. 6 to 7 weeks)is careoccur in White-wingedChoughs (Corcorax longerthan that of northtemperate species but melanorhamphos;ca. 29 weeks;Heinsohn 1991) similar to or shorterthan that of tropicalspe- and SuperbLyrebirds (Menuranovaehollandiae; cies (Skutch1976). Small passerinesin north ca. 37 weeks;Lill 1986). temperatelatitudes typically becomenutrition- Lengthof breedingseason and multibrooding.- ally independentof their parents two to four The 5.4-monthbreeding season of scrubwrens weeks after leaving the nest (Skutch 1976, is typical of thoseof tropical birds (3.9 to 7.8 O'Connor1984). The long period of postfledg- months)but longer than thoseof north tem- ing care in scrubwrenssupports Rowley and perate species (2.7 to 3.1 months; Ricklefs Russell's(1991) suggestion that parentalcare is 1966).The breeding season appears to be at the prolonged in Australian passerines.Fogden long end of range among the Pardalotidae (1972)suggested that the longperiod of careof (Woinarski1985). It is similar to that estimated passerinesin Sarawakresulted from the diffi- for the SpottedPardalote (Pardalotus punctatus) culty of finding suitableprey. That is, if insects but abouttwo monthslonger than that for the are sparselydistributed and havemany forms Buff-rumped Thornbill and the Chestnut-rum- of antipredatory defense,it may take a long ped Thornbill(Acanthiza uropygialis). Even con- time for youngbirds to learn how to forageef- trolling for the effectof latitude(one month per ficiently.We suggestan explanationthat is re- 11ø;Wyndham 1986), the Pardalotidaeexam- lated to seasonalityof food supplies.If the sea- ined by Woinarski (1985) have long breeding sonalincrement available for breedingis small seasons(3 to 5 months)relative to ecologically thenthe young may not fledge during a period comparable Northern Hemisphere species, of food abundance, which is in contrast to whichtypically have breeding seasons of 2 to 3 many north temperatespecies. Thus, the young months. may takelonger to acquirethe necessaryskills Our data from White-browed Scrubwrens for survival,not becauseAustralian arthropods support Rowley and Russell's(1991) conclu- require particular skill to find and eat, but be- sion that variation in reproductive effort in causea greaterlevel of skill is required for sur- Australianpasserines comes not throughdif- vival when food is not abundant. This second ferencesin clutchsize, but throughvariation in hypothesisseems more plausible,because it the numberof breedingattempts per season.In doesnot requirethe assumptionthat moreskill contrastto the durationof individualbreeding or learningis requiredto capturearthropods in attempts,the length of thebreeding season and different geographicregions. the numberof breedingattempts per yearvar- April 2000] Breedingof White-browedScrubwrens 487

ied significantly among years. However, it is Sam Portelli, and Linda Whittingham. Membersof unclearwhether multibrooding per seis an im- the "fairy-wren group," including Andrew Cock- portant differencebetween passerinesin Aus- burn, Mike Double, Peter Dunn, David Green, Mich- tralia versusthose in northtemperate regions elle Hall, Milton Lewis, and Raoul Mulder, also helped catchand band birds. Sam Portelli was re- (e.g.Woinarski 1985, Rowley and Russell1991). markablyefficient getting the data from field sheets Martin (1996) argued such differenceshave into computerfiles. Hugh Ford, Harry Recher,and been overstated,because many north temper- JeffWalters made helpful commentson a draft of the ate specieshave multiple broods (see Crick et paper.Members of the AustralianBird and BatBand- al. 1993). ing Scheme,especially Barry Baker,Belinda Deft- Doesa generallife-history "syndrome" exist for man, and JamiePook, have alwaysbeen supportive Australian old endemics?--Our data show that of this study and in recent years have even moved the breeding cycle of White-browedScrub- their officeinto our study site!Finally, we are grate- wrensis slowcompared with thoseof Northern ful for financialsupport to RDM from the Australian Research Council. Hemispherepasserines, particularly in having a two-daylaying interval,a long incubationpe- LITERATURE CITED riod, and a long period of postfledgingparen- tal care.However, these differences appear to AMBROSE,S.J. 1985.Aspects of thephysiological and be characteristicof the Pardalotidae,and pos- behaviouralecology of the White-browedScrub- siblysome other families, but not of the old en- wren Sericornisfrontalis (Aves: ) in demicCorvida in general.Overall, the sugges- WesternAustralia. Ph.D. dissertation, University tion thata generalsyndrome of leisurelyrepro- of Western Australia, Perth. duction exists among Australian passerines AMBROSE,S. J., AND S. J. J. F. DAVIES.1989. The social originatesfrom a sample of leaf-gleaningin- organisationof the White-browed Scrubwren Sericornisfrontalis Gould (Acanthizidae)in arid, sectivores,with all of the Australianrepresen- semi-arid and mesic environments of Western tativescoming from the Pardalotidae(Woinar- Australia. Emu 89:40-46. ski 1985,Ford 1989). Clearly, a more represen- ASHMOLE,N. P. 1963.The regulationof numbersof tativesample of taxais required.White-browed tropical oceanicbirds. Ibis 103:458-473. Scrubwrensappear to be typical of old endemic ASTHEIMER,L. B. 1985.Long laying intervals:A pos- Australianpasserines in havinga small clutch siblemechanism and its implications.Auk 102: size (Yom-Tov1987) and a long interval be- 401-409. tween nesting attempts,and they resemble BELL,H. L. 1982.Cooperative breeding by the White- Australianpasserines in generalin havinghigh browed Scrub-WrenSericornis frontalis. Emu 82: adult survival(Yom-Tov et al. 1992).They also 315-316. havea longbreeding season, which appears to BELL,H. L., AND H. A. FORD.1986. A comparisonof the socialorganization of threesyntopic species be typical of Australian birds (Wyndham of Australian Thornbill, Acanthiza. Behavioral 1986). Ecologyand Sociobiology19:381-392. We agree with Rowley and Russell(1991) BLAKERS,M., S. J. J. E DAVIES, AND P. N. REILLY. 1984. and Martin (1996)that fundamentalgaps exist The atlas of Australian birds. Uni- in our knowledgeof thebasic breeding biology versity Press,Melbourne. of Corvida in the SouthernHemisphere. Fur- BRIDGES,L. 1994. Breedingbiology of a migratory ther study of thesebirds will increaseour un- populationof the RufousWhistler Pachycephala derstandingof the evolutionof reproductive rufiventris.Emu 94:106-115. traits and help disentanglethe effectsof envi- BROWN, R. J., M. N. BROWN, AND E. M. RUSSELL.1990. Survivalof four speciesof passerinein Karri for- ronmentand phylogenyon the life historiesof ests in southwestern Australia. Corella 14:69-78. passerines. In particular, we need detailed CALE,P. 1994.Temporal changes in the foragingbe- studiesof a phylogeneticallydiverse range of haviourof insectivorousbirds in a schlerophyll taxa and more emphasison verifyingperiods forest in Tasmania. Emu 94:116-126. of postfledgingcare, renestingintervals, and CHRISTIDIS,L., ANDW. E. BOLES.1994. The the extentof multiplebrooding. and speciesof birds of Australia and its territo- ries. Royal AustralasianOrnithologists Union, ACKNOWLEDGMENTS Melbourne. COURTNEY,J., AND S. MARCHANT.1971. Breedingde- We were assistedin the field by Camille Crowley, tails of some common birds in south-eastern Megan McKenzie, Lynda Sharpe, Helen Osmond, Australia. Emu 71:121-133. 488 MAGRATHET AL. [Auk, Vol. 117

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