The Auk 118(1):176-190, 2001

VARIATION IN GROWTH OF NESTLING TREE SWALLOWS ACROSS MULTIPLE TEMPORAL AND SPATIAL SCALES

JOHN 1v. MCCARTY• Departmentof Ecologyand Systematics, Cornell University, Ithaca, New York14853, USA

ABSTRACT.--Differenceswithin a speciesin ratesof growth of nestlingscan be used as indicatorsof the quality of parental care,environmental conditions, and future successof offspring,whereas comparisons among different species may reflecta historyof different ecologicalconditions or life-historystrategies. The presesntstudy examines the patternsof variationin growth in nestlingTree Swallows(Tachycineta bicolor) from acrossthe species' range and comparesTree Swallowsto other species.Growth of Tree Swallowswas typical of other speciesin the family Hirundinidae.As a family, the Hirundinidaehave slower growth than typicalfor passerines.Growth rate of speciesof Hirundinidaewas not corre- lated with adult body massor averagebrood size. Contrary to predictions,species that are double-broodeddid not havehigher growth rates, but swallowspecies living at higherlat- itudes did have higher growth ratesthan tropical species.Substantial variation in growth rateswas observedamong populations of Tree Swallows,yet the amountof variationob- servedbetween breeding colonies only a few kilometersapart, or from the samecolony in differentyears, was as great as that seenin populationsseparated by hundredsof kilometers. Within a population,differences in growthamong years were correlatedwith temperature and food supply when nestlingswere being raised. No correlationbetween climate and growth was seenwhen comparingdifferent populations. Differences between populations werenot explainedby localhabitat, nor werelarge-scale geographic patterns evident. I used both experimentaland observationalevidence to evaluatethe implicationsof short-termre- ductionin growth for subsequentgrowth and survival.Nestlings were slowto recoverfrom evenvery shortperiods of delayedgrowth that occurearly in the nestlingphase. Return of nestlingswith experimentallyor naturallyinduced delayed growth was reduced, which sug- geststhat shortinterruptions in growthmay have long term effects on postfiedging survival, eventhough mass at fledgingis not affected.Received 9 August 1999, accepted 16 September 2000.

NESTLINGS OF ALTRICIAL BIRDS exhibit sub- growth.In a broadercontext, those energy de- stantialvariation in growth ratesboth within mands,coupled with physiologicalconstraints and amongspecies. Variation within a species on growth,accentuate the trade-offsthat exist is oftenused as an indicatorof variabilityin pa- betweenmaximizing growth and attempting to rental care, environmental conditions, or nes- optimize other aspectsof life histories(Lack tling quality. Growth ratesof nestlingsinflu- 1968, Ricklefs 1984, Ricklefs and Starck 1998, encelength of time offspringare dependenton Starck and Ricklefs 1998b). their parents,their energy requirementsand Within a species,nestlings with below-aver- rate of food delivery required of the parents, age growthor size at fledginggenerally suffer and length of time they are exposedto nest fromreduced postfledging survival (Gebhardt- predators(Lack 1968, Bosque and Bosque1995, Henrich and Richner1998). Reducedgrowth Halupka 1998).Variation among species is typ- may also have a long-term effect on fitness, icallyseen as a resultof variationin life-history evenwhen it doesnot appearto resultin lower strategies.Altricial birds are amongthe fastest growing vertebrates(Case 1978), with most postfledgingsurvival, by decreasingthe ability smallpassetines attaining full adultmass with- to obtain a breeding territory or mate or by in 10 to 20 daysof hatching.High ratesof en- lowering subsequent fecundity (Gustafsson ergy intakeare necessaryto sustainthat rapid and Sutherland 1988, Richner 1992, Richnet et al. 1989,Lozano 1994). Although it is clearthat • Presentaddress: Department of Biology,Univer- growth is a good indicatorof future success, sity of Maryland, College Park, Maryland 20742, factors that determine variation in size and USA. E-mail: [email protected] mass are not as well understood.

176 January2001] Variationin NestlingGrowth 177

Previousstudies have generallynot differ- into the degreeof plasticitypossible on an evo- entiated between growth reductionsthat are lutionary time scale,whereas differences in life due to chronic food shortagesor that are history among related speciesmay indicate causedby poor parentalcare and thosecaused how growthresponds to changesin therelative by short-termfluctuations in foodsupply with- demandsplaced on developingnestlings. Sec- in a season.Several groups of birds with food ond, I examinedthe significanceof short-term suppliesthat are subjectto short-termfluctua- periodsof reducedfeeding on growth and the tions, suchas seabirds(Hawksley 1957, Dunn possiblelong-term effects of thosereductions. 1975,Konarzewski and Taylor 1989)and aerial Althoughthe importanceof chronicfood short- insectivores (Koskimies 1950, Lack and Lack ages is well known, relatively little attention 1951,Bryant 1978,Wrege and Emlen 1991),are has been paid to short-termfluctuations in re- observedto undergo periods of interrupted sourcesand their effecton subsequentaspects growth and developmentunder adversecon- of an individual's biology. I present observa- ditions,resuming normal growth once condi- tional and experimental evidence to examine tions improve. The long-term effectsof those the importance of short-term reductions in temporary growth reductions have seldom growth. been explored,but if starvationinterferes with critical developmental stages, permanent METHODS changescould result. Previousstudies have found that nestlings subject to short-term Tree Swallowsbreeding in nestboxes were studied shortagesof food eventuallyattain full body at the CornellUniversity Experimental Ponds Facil- ity (42ø30'N76ø27'W), near Ithaca, New York. This mass(Wiggins 1990b, Negro et al. 1994),mak- facility consistsof two breeding sites located ap- ing it unclear whether such reductions in proximately 2 km apart. Unit One supported ap- growthhave a long-termeffect on postfledging proximately 55 to 75 pairs of breeding Tree Swal- survival if survival dependssolely on body lows, and Unit Two had between 10 and 23 pairs. size. Insect abundancewas measureddaily using suction In contrastto the view that intraspecificvar- trapsrunning during daylight hours, and high tem- iation is due to effects of the environment, var- peraturewas recordeddaily. Thesesites and meth- iation among speciesis often viewed as the ods for sampling insects are describedin detail in adaptive outcomeof different selectionpres- McCarty and Winkler (1999a, b). All values are re- ported as means + SE. sures.Predation rates, food availability,num- Nestlingsof all ageswere weighedto the nearest ber of breedingattempts per year, and level of 0.1 g during the 1990-1993breeding seasons using competitionamong siblings are all thoughtto either Pesolaspring scales or a portableOhaus elec- influenceinterspecific differences in growth tronic balance.In addition, nestlingswere measured (Lack1968, Bosque and Bosque1995, Halupka on day 10 only in 1989,and thosedata are included 1998).Even though the sourcesof intraspecific in analysesof return rates. Swallows breeding at and interspecificvariation in growth are ulti- thosesites are monitoredclosely for the exactdate of mately the same,the two types of variation hatchingto determinenestling age. All nestlingages have seldombeen consideredtogether. are given as hatch day equal to nestling day 1. Lengthsof flattenedand straightenedwing chord The presentstudy employed two approaches (hereafter"wing length"), the 9th (outermost)pri- to addressthe questionof the ecologicalsig- mary, and 6th (outermost)rectrix featherwere mea- nificanceof variation in growth rates of Tree suredto the nearest0.5 mm usinga ruler with a wing Swallows (Tachycinetabicolor) and variation and featherstop. Length of the manuswas calculated amongthe speciesin the Hirundinidae.First, I from difference between wing and 9th primary describedboth the inter- and intraspecificvar- length. Length of the tarsometatarsus(henceforth iation in growth. Variation in growth among "tarsus") was measuredto the nearest0.1 mm using differentspecies and amongdifferent groups of dial calipers. Nestling Tree Swallows typically Tree Swallows was comparedto factors that fledge on day 21; disturbing nestlingsafter day 15 may causepremature fledging, so sample sizes for might contributeto variation,such as climate, older nestlings are small and come primarily from life history (clutchsize and numberof broods nestlingsremoved for other studies. per season),habitat, food supply, and geo- Growth curves were fitted to mass data and graphiclocation. The absolutedegree of varia- growth rate constantswere calculatedfor nestlings tion among related speciesprovides insight from Ithaca in eachyear and at both breedingloca- 178 JOHNP. MCCARTY [Auk, Vol. 118 tions. Nestlingsat Ithaca were measuredat more metric Kendall rank correlationor Mann-Whitney than one age,but not every day, providing a mixed tests (Conover 1980). longitudinalsample (Ricklefs 1983). Logistic growth Growth of speciesin the Hirundinidae was com- curves are suitable for Tree Swallows (Zach and Ma- paredto otherspecies of passerines.Ricklefs (1968a) yoh 1982)and curveswere fitted to meanmasses for providesgrowth constantsand ratio of asymptotic eachpopulation using an iterative,least-squares pro- massto adult massfor smalland medium-sizedpas- cedure (non-lin module of SYSTAT;Wilkinson et al. serines(<100 g). Thosedata were used to compare 1992) and equation: membersof the other families of passerinesto the data on the Hirundinidae described above using M(•) nonparametricMann-Whitney tests (Conover 1980). M(x)= [M(•)-M(0)] -K (1) Postfiedgingsurvival.--All nestlingsin the Ithaca 1+[- •Vi70• -]e x population were banded prior to fledging. Adult swallowswere capturedin mist nets prior to breed- where x is the nestlingage, M(x) is body massat age ing or at their nest boxesduring breeding. Return x, M(0) is the initial mass,M(m) is the asymptotic ratesof birds banded as nestlingsare used as an es- body mass,and K is the growth rate constant(Rick- timate of survival by providing a sampleof those lefs 1983). nestlingsthat survive to one year. Becausenestling Variabilityin Tree Swallowgrowth rates.-•Growth massand wing were measuredat different agesin rates of nestling Tree Swallowsfrom Ithaca were different years (betweendays 8 and 12), measure- comparedto publisheddata on the growth of Tree ments were standardizedby subtractingthe mean Swallowsfrom other sitesthroughout North Amer- value for eachyear from eachindividual's mass or ica. For all data sets,logistic growth-rate constants wing length and then dividing by the standardde- were calculatedfor the meanpopulation growth us- viationfor that year,to producea meanof 0 and stan- ing equation1. For consistency,that equationwas dard deviation of 1 for each year's measurements. used even when the authorsof the original papers Data from 1989to 1993were then pooled and effects presenta valuefor K. That eliminatesvariation ow- of standardizedmass, wing length,and tarsus length ing to differencesin the methodused to calculateK on the probabilityof an individualbeing captured as (Starckand Ricklefs1998a). an adult were analyzed using logistic regression Whennot givenin the originalpaper, latitude and (Hosmer and Lemeshow1989). longitudeof the breedingsites were estimatedfrom Effectsof short-termfasting.--A fastingexperiment site descriptions.When possible,other study sites was conductedto determinethe importanceof short- were classifiedas being either near water or as dry term reductionsin growthto the subsequentgrowth uplands,and mean clutch size for thepopulation was of nestlings.Nests availableon days when experi- determinedon the basisof descriptionsin the orig- mentswere conductedwere paired to balancethe ex- inal papers.Climate data summariesfor the period perimental groups for nestling age,brood size, and 1961-1990were obtainedfrom regional climate da- pre-treatmentnestling mass. Nests were alsopaired tabasesfor locationswhere Tree Swallow growth by age of female parent so nests of second-year had been measured.The averagetemperature and (brown) females were compared to nests of other averagedaily high temperature for themonth of June second-yearfemales. Within thosepairs, nestswere randomly assignedto either control or treatment providedby thosesummaries were used as indica- groups.Initial masswas measuredon day 5 and the tors of breeding seasonclimate. Data for compari- morning of the start of the experiment(day 6). On sonsof climateamong individual years at the Ithaca the morning of day 6, nestlingswere weighedbe- site were based on data collected on site (see Mc- tween 0630 and 0730 EasternStandard Time (EST), Carty andWinkler 1999bfor details).Those variables and all nestlingsfrom the experimentalbroods were werecompared to variationin growth-rateconstants removed and were fasted until the eveningof the using nonparametricKendall rank correlation(Con- same day. One or two nestlings from a nonexperi- over 1980). mental nest were placedin the treatmentnests to Comparisonwith otherspecies.--Interspecific varia- keepthe parents from abandoningwhile theirchicks tion in growth amongthe Hirundinidaewas exam- were gone.Nestlings in controlbroods were weighed ined using publisheddescriptions of growth. For and returnedto the nest.Experimental broods were each speciesin the family Hirundinidae with an placedin controlledtemperature chambers under an availablegrowth curve,the mean massof nestlings incandescentlamp. As part of a separateexperiment, at eachage was usedto estimatethe growth-ratecon- nestlingswere held at either 20 or 30øC.The absolute stant using equation1. Information on adult body massof the two groupsdid not differ by day 7 (30øC mass,life history(clutch size and numberof broods = 10.7 _+0.7 g, 20øC= 10.4 + 0.6 g, U-test,Z < 0.01, per season),and locationstudied (latitude) was col- P > 0.99), so I pooled temperaturetreatments into a lectedfrom publishedsources. Those variables were singleexperimental group. Treatment nestlings were comparedto the growth constantsusing nonpara- returned to the nest between 1730 and 1845 EST. January2001] Variationin NestlingGrowth 179

Controland treatmentnestlings were weighedat the •t'"•'- time the treatment broods were returned to their 25' nests.Experimental nestlings differed from controls both in beingdeprived of food and in beingsubject to possiblestress induced by simplybeing separated 20' from their nest and parentsfor severalhours. How- ever, becausenestlings of that age group are too , youngto showany fear response and settled into ex- perimental nests in an apparently normal manner, that differenceis probablyof minor significancefor 1o,. differencesin growth. Nestlings in control and treatment nests were weighed between 1300 and 1800 EST on nestling 5! days 7, 8, 10, and 12. Paired nestswere weighed within onehour of eachother. Wing lengthof all nes- ß .... ! .... • .... i .... i tlingswas measured on days10 and 12, and the tar- 0 5 10 15 20 sus was measured on day 12. Masses and wing lengthswere not measuredon day 12 at four nests Age (days) that were disturbedby otherresearcher activities on that day.Tarsus length was still measuredon day 12 FIG.1. Changein massduring growth of nestling for thosenests, because adult tarsuslength is ob- Tree Swallows. Bold line representsmean mass(+2 tained before day 12 (seebelow). For statisticalanal- SE) of nestlingsfrom Ithaca, New York during the yses,each brood was treated as an experimentalunit period1990-1993. Thin linesshow the 10thand 90th and the mean masses(or other measurements)for percentilesof mean massesfor nestling Tree Swal- lows from 13 other locations across North America. the chicks within broods were compared using paired Wilcoxon signed-ranktests (Conover1980). Sample sizes (number of nestlings)for Ithaca data Theproportion of thebroods in eachgroup that were are givenacross the top of the figure.Data for other recapturedin subsequentyears are comparedusing sites from: Paynter 1954; Sheppard 1977; Marsh the Wilcoxontest to explorelong-term effects of fast- 1980;Zach and Mayoh 1982,1986; Wiggins 1990b; Pi- ing on survival. In addition, the relationshipbe- janowski1991; Fabro 1993; Nichols et al. 1995;Teath- tweenmass change of the experimentalgroup and er 1996; Secord and McCarty 1997; Ramstacket al. 1998. proportionof the brood subsequentlyrecaptured is examinedusing Kendall rank correlation. The experimentalresults are also comparedto a riod of this study,the heaviestnestling reached sampleof nestlingsthat underwenta natural period of weather-relatedfasting, resulting in reduced 27.6 g. Fitting the datafrom Ithacato a logistic growth. A wet, cool period in 1992 resultedin the growth curve gave a growth rate constant, deathsof all nestlingsin the population,except for K = 0.50, and an asymptotic mass of four broodsthat hatchedduring the adversecondi- 21.7 g. tions.The growth of thosenestlings after conditions Growth of the structural features wing improvedis comparedto thepopulation mean using lengthand flight featherswas more linear than one-groupsign tests (Conover 1980). The numberof the increasein mass(Fig. 2A). Flight feathers nestlingsfrom thosefour nestsreturning in subse- (primaries and rectrices)first emergedon day quent years is comparedto the number returning 7. Growthof thewing lengthand flight feathers from neststhat hatchedimmediately after the period continuedthroughout the nestlingperiod, with of adverseweather using Fisher's exact test. growthbeing completed some time afterfledg- ing (Fig. 2A). The bony structures,tarsus and RESULTS manuslength, were the first to reachadult size (Fig. 2B).Tarsus reached the adult lengthof 12 The growthof nestlingTree Swallows exhib- mm between day 8 and 9, whereas manus ited the classicsigmoidal curve found in other lengthreached its adult lengthof 25 to 26 mm passerines(Fig. 1). Nestlingstypically reached by day 9 (Fig. 2B). adult massof approximately20 g around day Variabilityin TreeSwallow growth rates.--With- 10 or 11, approximatelyhalf way throughthe in the Ithacapopulation, nestling growth rates 21-day nestling period. Nestlingscontinued to varied with breeding location and year Be- increasetheir massfor oneto three days,reach- tween the two Ithaca breeding sites, growth ing a peakmass of around22 g. During the pe- was consistentlyhigher at Unit Two (Fig. 3A), 180 JOHNP. MCCART¾ [Auk,Vol. 118

A 120 A ....ß.... Wing Chord i '• 25 1 ----o-- Primary oo • Rectrix • • ._.20 80 o• 15 60 ß 03 '' -•o••• UnitOne 40 20 j ---•- -.Unit Two 5 .... i .... i , , , ! i , , , , i o o 5 10 15 20 • 5 10 15 20 Age(days) = = Age (days)

30 25: B

.-.25 t« 20' E 20

• 15 . _J 10 ---o-- Manus 5' • Tarsus ....--=..... 1993 øo.... ' ' ' ib'' ' i5'' ' o .... i .... i .... i .... i o 5 lO 15 20 Age (days) • = Age (days) FIc. 2. Growthof wing and flight feathers(2A), and manusand tarsus(2B) of nestlingTree Swal- FIG.3. Variationin nestlinggrowth rates at Ithaca lows. Analogousdata for fledglings("Fledge") and amongyears and betweensites. For eachage, nes- adultsare alsoprovided. Mean ___SE givenfor each tling masswas compared using ANOVA and "*" in- age:Sample sizes for eachage vary from 10 to >600 dicatesthat the differencesbetween sites (A) and individuals. amongyears (B) are significantafter applicationof a sequentialBonferroni adjustment (Rice 1989). Error barsomitted for clarity. with K for Unit One = 0.49, and K for Unit Two = 0.53. Temporal variation also contributedto Among studies conducted acrossthe Tree the overallvariability in growthrates. Growth Swallow'srange, valuesfor the growth-rate variedamong years at the Ithacasite (Fig. 3B), constantsvaried between K = 0.41(Pijanowski with K varying from 0.49 in 1992 to 0.56 in 1991)to K = 0.59(Zach and Mayoh 1982), with 1991. Although sample size is small (four an averageK for the 15sites of 0.50 ___0.01. Nes- years),growth-rate constants were positively tling growth-rateconstants were not correlated correlatedwith mean high temperature during withthe latitude or longitude of the nesting site the breedingseason (Kendall rank correlation; (Kendall rank correlation, latitude •-= -0.04, Z •- = 1.00, Z = 2.04, n = 4, P = 0.042) and with = 0.21,n = 15, P - 0.83,longitude •- = -0.22, meaninsect abundance over the breedingsea- Z = 1.16, n = 15, P = 0.25). Growth-rate con- son (•- = 1.00, Z = 2.04, n = 4, P = 0.042). stants from those sites were not correlated with January2001] Variationin NestlingGrowth 181 either average daily mean temperature (r = = 1, n = 1,233, P = 0.011), and tarsi (X2 = 5.5, -0.19, Z = 0.80,n = 11,P = 0.42)or the average df = 1, n = 215, P = 0.019). daily high temperature(r = -0.35, Z = 1.51,n Effectsof short-term fasting.--An experimental = 11, P = 0.13). There was no difference in K group of nestlingswere fastedfor 10 to 12 h on betweensites classified as uplands (0.52 +_0.05, day 6 (Fig. 5A). Massof nestlingsin controland n = 5) and thosenear water (0.50 +_0.05; Mann- treatmentbroods did not differ at the begin- Whitney U-test,Z = 0.60,n = 9, P = 0.55).The ning of the experiment(control nestlings = 9.5 averageclutch size in a populationwas not cor- ___0.3 g, experimentalnestlings = 9.0 ___0.3 g; relatedwith nestlinggrowth rate constants(r Wilcoxon test, Z = 1.02, P = 0.31). Brood size = -0.16, Z = 0.75, n = 13, P = 0.45). of the two groupsdid not differ (control= 5.3 Comparisonwith other species.--Growthof ___0.2, experimental= 5.4 ___0.2; Wilcoxontest, nestlingTree Swallows was within therange of Z = 1.01, P = 0.31), and was well within the variabilityseen in the familyHirundinidae (Ta- typicalbrood size of 5 to 6 nestlingsof this and ble 1). Among swallow species,there was no other Tree Swallowpopulations (Robertson et correlationbetween adult body mass and nes- al. 1992, McCarty and Secord1999). tling growth rate (r = -0.17, Z = 0.91, n = 16, Experimentalnestlings lost an averageof 0.7 P = 0.36). Speciesknown to regularly lay two ___0.1 g per nestlingduring day 6 (8% of their broodsper season(Turner and Rose 1989) did startingmass), whereas control broods gained not have growth rates different from single- an averageof 1.9 ___0.3 g per nestling (20% of broodedspecies (double brood 0.43 ___0.03; sin- their starting mass) during the same period gle brood 0.46 ___0.02; Z = 0.36, n = 13, P = (Wilcoxon test, Z = 3.59, P < 0.001). Nestlings 0.72). There was a slight tendencyfor species in the experimentalbroods remained signifi- with larger clutchsizes to grow fasterbut that cantlylighter through day 10 (Fig. 5A). On day was not significant(r = 0.48, Z = 1.85, n = 16, 12, the two groupsno longer showedsignifi- P = 0.06) and confoundedby the increasein cant differencesthough the trend towards clutch size with latitude. Growth rates of swal- heaviernestlings in the controlgroup remained lows did vary with latitude,with speciesbreed- (Fig. 5A). The experimentaltreatment also re- ing closerto the equatorhaving slower growth sulted in a differencein structural size. Wing (Fig. 4). chord was smaller in experimentalbroods on Ricklefs(1968a) provides growth constants both day 10 (experimental= 32.8 ___1.1 mm, for 63 speciesof small and medium-size pas- control = 36.0 ___0.7 mm, Wilcoxon test, Z = serines (excluding Hirundinidae and species 2.94, P = 0.003) and day 12 (experimental = with adult massover 100 g) from 14 familiesor 32.8 ___1.1 mm, control = 36.0 ___0.7 mm, Wil- subfamilies.The averageK for thosepasserines coxontest, Z = 3.69,P = 0.007).Tarsus length is 0.501 ___0.01, significantlyhigher than the of day 12 experimentalnestlings (36.0 +__0.7 mean of 0.429 ___0.02 for 16 speciesof Hirun- mm) was significantlyshorter than controls dinidae (Z = 3.03, P = 0.003). Ricklefs (1968a) (36.0 ___0.7 mm Wilcoxon test, Z = 3.35, P < alsoprovides the ratiosof asymptoticmass to 0.001).All nestlingsin both experimentaland adult massfor 58 speciesof small and medium- controlbroods survived to fledging. size passerines(excluding Hirundinidae and Given the observed relationship between specieswith adult mass over 100 g). The Hi- growth andthe probabilityof beingrecaptured rundinidaein Table1 had a significantlyhigher as an adult in this population (above), one ratio (1.15 ___0.04) than do non-Hirundines wouldpredict that nestlingswith artificiallyre- (0.87 ___0.02; U-test, Z = 5.28, P < 0.001). duced growth rates would return at a lower Postfiedgingsurvival.--For the Ithacapopula- rate than unmanipulated nestlings. Sample tion as a whole, nestling growth was signifi- size is small, but there was no significantdif- cantlyrelated to the probabilitythat a nestling ferencein return ratesof nestlingsfrom exper- would be recaptured, either as a spring mi- imental and controlbroods (Fig. 6; Z = 0.85, n grant or a breedingindividual. Logisticregres- = 18, P = 0.39). However,among the experi- sion on the pooleddata for 1989-1993shows mental nestlingsthere was a significantrela- that heaviernestlings wet, • more likely to re- tionshipbetween the amountof masslost dur- turn (X2 = 12.4, df = 1, n 1,641, P < 0.001), ing the manipulationand the proportionof the as were thosewith longerwings (X2 = 6.55, df brood recaptured the following year (Fig. 6; 182 JOHNP. MCCARTY [Auk,Vol. 118 January2001] Variationin NestlingGrowth 183

0.55 25 A .... Contr.ol •',.i.,a 050ß 2O • 0.45 ,•.• 15 o o 0.40 • 10 ,- 0.35 5 • 0.30 o 0 ...... *'* '* ' '* ..... 0 5 10 15 C50.25 I ß i ß I ß i ß i" i ß 0 10 20 30 40 50 60 Age (days) Latitude (degrees) 25 B

FIo. 4. Growth ratesof nestlingsof 16 speciesof 2O Hirundinidae in relation to latitude. Growth rates in- creasedsignificantly with distancefrom the equator; n = 16, T = 0.43, Z = 2.33, P = 0.020. Sources of data given in Table 1. Line fit using least squaresregres- sion provided for illustration. :1o 5 Kendall rank correlation;•- = 0.35, Z = 2.02, n = 18, P = 0.043). 0 ' '* '*'*'*'* '**' '*'*' '* ß ß ' 0 5 10 15 Patternsof reducedgrowth similar to those observedin thefasting experiments can be seen Age (days) in cases of natural starvation due to inclement weather.During a four-dayperiod of low tem- FIc. 5. Effectsof experimental(A) and natural (B) peratures,rain, and reducedavailability of in- short-termfood deprivationon subsequentgrowth of nestling Tree Swallows. Effects of experimental sectsbeginning on 19 June 1992, most adult growth reductionon day 6 persisteduntil day 12 (A). TreeSwallows stopped feeding their nestlings. Linesfor eachcategory based on meanmass of nest- Althoughall nestlingsolder than 3 daysat the lings within broods + SE. Mass of deprived nests(n beginningof thisperiod died afterthree or four = 18 broods) and control nests(n =18 broods) com- days (McCarty 1995), some nestlings that paredusing paired Wilcoxon sign rank testsfor each hatchedat the beginning of the period sur- age.Ages where differencesremain significant after vived. Thosenestlings failed to grow or devel- applicationof a sequentialBonferroni adjustment to op throughthat period,and, oncefeeding re- P-values(Rice 1989) are indicatedby "*." Growth of sumedon 23 June,they remained several days nestlingTree Swallowsduring and after a naturally occurring period of adverse environmental condi- behind their normal growth trajectory (Fig. tions was retarded (B). The bold line representsnor- 5B).Wing length at days8 (14.4___ 0.8 mm, n = mal growthbased on Figure1. Circlesjoined by thin 9), 10 (26.6 ___1.2 mm, n = 17), and 12 (37.4 _ lines representthe mean massof nestlingsin four 1.8 mm, n = 17) were alsosignificantly shorter broodshatched during periodsof adverseweather. than the populationmean (one group sign Open circlesrepresent mean massduring the period tests,P < 0.001for eachday). Although those adverseweather was occurring;closed circles show nestlingsfledged successfully,the reduced mass after weather conditions returned to normal. growthexperienced resulted in a long-termef- Massat eachage is comparedto the populationmean fect on thosenestlings. Nestlings from the five using one sample sign tests. P-valuesthat remain significantafter applicationof a sequentialBonfer- neststhat hatched during the periodof adverse roni adjustmentare indicatedby ..... weatherwere less likely to be recaptured(1 of 23 nestlings)than nestlingsthat fledgedfrom the three nests that hatched in the week im- 184 JOHNP. MCCARTY [Auk, Vol. 118

have increased successat larger colonies 80 ß (Brown and Brown 1996).The differencemay lie, in part, in a moreeven distribution of the 60 ß insectsTree Swallowseat, eliminatingthe de- pendenceof Tree Swallowson colony-matesfor o finding food. Tree Swallows usually forage o 40 within sightof the nestsite, in contrastto Cliff ß ß Swallowswhere individualsmay fly an aver- o age of 500 to 700 m from the nest to forage 20 (Brown and Brown 1996,McCarty and Winkler

o trol• 1999a). 0 ; : .... Nestlings Somedifferences in growthamong years in -2 -1 0 1 the Ithacapopulation are probablyrelated to variationin weatherand food supply during Masschange on day six (g) nestlingrearing. Previouswork showsthat short-termtemporal variation in temperature FIG. 6. Effects of experimental food deprivation and food supply,on the scaleof 48 h, affects on the proportionof a brood recapturedin the fol- nestlinggrowth (McCarty and Winkler1999b). lowing year.Mass change during the experimentis basedon the mean changein massfor all nestlings The foodsupply of TreeSwallows is correlated in a brood. Return rates of experimentaland control with temperatureon a short-timescale (Mc- broods(_+ SE) did not differ, but amongexperimental Carty and Winkler 1999b)and that translates nestlingsthere was a correlationbetween the amount into a relationshipbetween mean temperature of masslost during the experimentand the propor- and food supply acrossan entire breeding sea- tion of the broodreturning. son.At Ithaca,the lowestgrowth rate occurred in 1992,a year when mostnestlings died dur- ing a period of poor weatherin mid-Juneand mediatelyfollowing the adverseweather (6 of when both temperatureand food supplywere 15 nestlings;Fisher's exact test, P = 0.009). belownormal; higher growth rates occurred in warmer years with higher abundancesof DISCUSSION insects. Across North America, substantial variation Variability in Tree Swallowgrowth rates.- in growthamong different populations of Tree Growthof nestlingTree Swallows at Ithacavar- Swallows was found, but none of the factors ex- ied with breedinglocation and year (Fig. 3). aminedthat differ amongthose sites explain The two breedingsites at Ithaca are separated that variation. The lack of a correlation between by only 2 km and are in very similarhabitats growth-rateconstant and either latitude or lon- (McCartyand Winkler 1999a,b). Theconsistent gitudesuggests that broad-scale patterns in cli- differencesin growthbetween those two sites mateacross North Americaare not responsible are not a functionof clutchsize (McCarty and for the variation(but seeDunn et al. 2000).Al- Winkler 1999b) or food availability,because in- sect abundance is similar at the two sites though this and previousstudies show that (McCarty 1995).Rather, the basisfor the differ- temperatureand food supplyhave important encesbetween the two Ithacasites probably lies effectson growth on a short-timescale and in in differencesin densityof breedingbirds. The a single location,those effects cannot be ex- density of nest boxesand hence,density of trapolatedto effectsthat occuron largerscales. breeders,is 3 to 6 timeshigher at Unit One,and Althoughchanges in climateover time have ef- parents at that site must forage further from fects on timing of laying in Tree Swallows their nests, possiblybecause of interference (Dunn and Winkler 1999), differences in cli- amongforagers (McCarty and Winkler 1999a). mateat differentsites do not influencegrowth. Higherdensities of breedingpairs reduces nes- Likewise, though breeding sites near water tling nutrition in some passerines(Wiklund may have larger and more reliablefood sup- and Andersson1994), but other swallows,no- plies (Quinney and Ankney 1985, Dunn and tably Cliff Swallows (Petrochelidonpyrrhonota), Hannon 1992), there was no consistentdiffer- January2001] Variationin NestlingGrowth 185 encein growthbetween nestlings at sitesnear Comparisonwith other species ofswallows.--Given water and thoseat upland sites. the similarity in ecologyamong speciesof The lack of a correlationbetween average swallows,it is interestingto notethe degreeof clutchsize for a populationand its growthrate variabilityseen in growthrates among the Hi- supportsresults of analysesthat have exam- rundinidae(Table 1). The overallecological and ined effectsof broodsize on growthrates with- morphologicalsimilarity among species make in populationsof Tree Swallows(Zach and Ma- the swallowsan appropriatefamily for inter- yoh 1982,Wheelwright et al. 1991,McCarty specificcomparisons of growth.Differences in and Winkler 1999b).It is not surprisingthat life historythat do existamong species are not natural brood size has little effecton growth correlatedwith variationin nestlinggrowth. rates.It is likely that decisionsabout the num- Althoughit has been suggestedthat species ber of offspringto produceare heavilyinflu- that do not attemptto rear morethan onebrood encedby differencesin individuals' abilitiesto per seasonshould have lower growth rates than raiseyoung successfully. Because rapid growth double-broodedspecies (Ricklefs 1984), the is suchan importantdeterminant of futuresuc- data for swallowsdo not supportthat hypoth- cess,adjustments in clutchsize and brood size esis:single-brooded species have growth rates will tend to minimize differencesin growth similar to those of regularly double-brooded ratesboth within and amongpopulations. The species.Likewise, whereas brood size changes effectsof broodsize on growthare morelikely with latitude,number of offspringraised does to be seen in experimentswhere individuals not appearto havean effectof growthrate. are forcedto raise additionalyoung. However. Swallowsdo supportthe generalpattern of the effectsof even enlargedbrood size on slowgrowth in tropicalspecies (Fig. 4; Ricklefs growth in Tree Swallowshas been difficult to 1968a,1976). The Hirundinidaeprovide a ro- document (DeSteven 1980, Wiggins 1990a, bust exampleof that patternboth becausesev- Wheelwrightet al. 1991). eral generacontain both temperate and tropical Like otherpasserines, mass and size of bone representativesand becauseof the overalleco- and featherstructures changes rapidly in Tree logical similarity among species.Additional datawill be neededto interpretpossible factors Swallows(Figs. 1 and 2). Bothbone structures measured in Ithaca Tree Swallows--tarsus and leading to that pattern in swallows, but it seemslikely that the patternof peak availabil- manus--reachedadult lengthby day 9. Rapid ity and degreeof variationin the supplyof ae- developmentof tarsushas been describedas a rial insectsmay be an important contributing possibleadaptation for intrabroodcompetition factorin that relationship.That is in contrastto during begging (O'Connor 1984), and rapid the intraspecificcomparison among Tree Swal- lengtheningof the wing bonesmay be neces- low populationswhere no correlationwith lat- sary to provide time for sufficientcalcification itude exists.The simplestexplanation for that beforefledging (Carrier and Leon 1990,Carrier differenceis that the latitudinalrange covered and Auriemma 1992) or may be a prerequisite by theinterspecific comparison (approximately for flight featherdevelopment. 53ø latitude) is far greaterthan the variability Tree Swallowsfly immediatelyupon exiting among Tree Swallow populationsthat have the nestfor the first time.However, the 9th pri- been studied (8ø latitude). mary feathers reach only 60-70% of adult As a group, the Hirundinidae have lower lengthprior to fledging,and full adult length growthrates than otherpasserines (this study) of primariesmay not be attaineduntil the first andthey also have longer nestling periods than or even secondprebasic molt (Robertsonet al. otherpasserines of similarsize (McCarty 1995). 1992), a pattern seen in many passerines(Ala- Differences between Hirundinidae and other talo et al. 1984).This is a surprisingresult for passerinesare alsoreflected in the significantly a speciesso dependenton flight for obtaining higherratio of theasymptotic mass of nestlings food and where selectionon flight efficiency to adult mass in swallows. The ratio of 1.15 in wouldbe expectedto be strong,though shorter the Hirundinidae indicates that swallows tend wings may reflect a tradeoff betweenincreased to reachand evenexceed adult massprior to maneuverabilityat the expenseof flight speed fledging,whereas the otherpasserines (ratio = (Alatalo et al. 1984) 0.87) fledge at an earlier developmentalstage. 186 JOHNP. MCCARTY [Auk, Vol. 118

Severalaspects of the ecologyof swallows,in- the size of structuralfeatures such as wing or cludingtheir relativelylarge brood sizes,sus- tarsuslength (McCarty 1995) suggests that in- ceptibility to short-termfluctuation in food creasedenergy stores are not primarily respon- supply,relatively safe nest sites, or the neces- siblefor the differencesin recaptureseen here. sity of greater developmentbefore fledging Garnett(1981) proposed that body size acting could influencepatterns of growth rates. If through dominance and social interactions swallows do have safer nest sites, their slow may be responsiblefor differencesin postfledg- growthwould tend to supportthe trade-off be- ing survival. That effect is seen in Carrion tweengrowth and mortalityproposed by Lack Crows (Corvuscorone; Richner et al. 1989, Ri- (1968),who suggestedthat predationrisk se- chner 1992) and may occur in Tree Swallows lected for faster growth, whereasstarvation (Lozano 1994). risk selectedfor slowergrowth. The effectson Effectsof short-termfasting.--The fasting ex- growthof thesusceptibility of swallowsto food perimentindicates that short-termreductions shortagesare difficult to predict. Although in growth have long-termeffects on the sub- slowergrowth may decreasemaximum energy sequentsize (as measuredby tarsuslength) demands(Lack 1968, Case 1978), rapid growth and massof nestlingTree Swallows(Fig. 5A). might limit the duration of the vulnerable An analogouspattern is seenassociated with (Lack 1968, Winkler 1993). naturalgrowth reductions caused by inclement Postfiedgingsurvival.--The lower probability weather(Fig. 5B). Compensatory growth is not of recapturein nestlingTree Swallows with be- observedafter either experimentalor natural low averagegrowth of mass,wing length,or periodsof short-termgrowth. Nestlings having tarsuslength, is typicalof otherspecies of pas- short periods of fasting do eventuallyreach serines(Gustafsson and Sutherland1988, Tin- normal massbut only after a longer period of bergenand Boerlijst1990, Gebhardt-Henrich growth.The delayedgrowth seen in thosenes- and van Noordwijk 1991, Gebhardt-Henrich tlings emphasizesthe importancethat just a and Richner 1998). Subsequentrecapture of few hoursor daysof delayedgrowth can have nestlingsas adults is frequentlyused as an in- effectscomparable to the cumulativeeffects of dicatorof postfledgingsurvival. Because not all chronicfood shortagethroughout the nestling surviving nestlingsare recaptured,that as- period. sumesthat all nestlingshave an equal proba- The conclusionsof this study differ from bility of dispersing.As is the casefor most thoseof Wiggins(1990b), who foundno long- small passerines,not enoughis known about termeffects of reducednestling growth in Tree natal dispersal of Tree Swallows to evaluate Swallows(see also Wheelwrightand Dorsey that assumption.Given the difficultythat cav- 1991).Wiggins produced differences in growth ity nesterssuch as Tree Swallowshave in se- by removingone or two nestlingsfrom each curing breedingsites (Robertson et al. 1992),it broodfor periodsof 4 h betweendays 5 and 8, seemsthat the ability to securea nestcavity at and then comparedthe growth of these"de- thenatal site, and thus be recaptured,would be prived"nestlings to theirsiblings who had not advantageous. beenremoved. Deprived nestlingsgrew slower The relationshipbetween nestling growth but there were no apparent differencesbe- and subsequentrecapture appears to be a caus- tween groupsby day 15. The manipulation al one (Tinbergenand Boerlijst1990), but the used by Wiggins is analogousto conditionsun- mechanismbehind the relationshipremains der whicha singlenestling finds itself at a com- unclear Perrins (1965) attributed the relation petitivedisadvantage relative to its siblingsfor betweennestling size and survivalin GreatTits a portionof the nestlingperiod. The manipu- (Parsusmajor) to the higher energy reserves lation used in the presentstudy is meant to availableto the heavieryoung birds. That in- mimic the conditionsexperienced by nestlings terpretationhas been challengedby Garnett during periods of poor environmentalcondi- (1981)who calculatedthat differencesin fat re- tions; the entire brood experiencesa food serveswere probablynot able to significantly shortagefor an extendedperiod, and when influencesurvival. The lack of a relationship conditionsreturn to normal the parentsmust between fat storesof individual nestling Tree then contendwith an entirebrood of deprived Swallowsand either their total body massor nestlings.In Wiggins'(1990b) experiment, par- January2001] Variationin NestlingGrowth 187 entshave more opportunity to compensatefor nestlingTree Swallowswith delayedgrowth the reducedcondition of the deprivednestling causedby inclementweather becauseits siblingsare in goodcondition. The Thoseresults emphasize the importanceof failure of nestlingsin either experimentto the interplaybetween both temporaland spa- show any compensatoryincrease in growth tial variationin understandingvariation in nes- ratesemphasizes the constraintsowing to the tling growth in Tree Swallows.There is in- alreadyhigh ratesof growth in nestlingpas- creasing interest in using growth as an serines(Lepczyk et al. 1998,Ricklefs et al. 1998) indicator of environmental conditions,espe- The ability to temporarilyinterrupt growth cially in Tree Swallows (Quinney et al. 1986, and development during periods of poor Blancher and McNicol 1988, St. Louis and Bar- weatherhas been cited as a possibleadaptation low 1993, McCarty and Secord 1999). To suc- to short-termfluctuations in foodsupply faced cessfully interpret environmental effects on by aerial insectivores(O'Connor 1977b,Emlen growth,it will be criticalto recognizethe mag- et al. 1991).Both the experimentaland natu- nitude of variation that can occur on small tem- rally occurring periods of nutritional stress poral and spatial scales.Complex interactions clearlyshow that occursin TreeSwallows (Fig. among variablesare likely to produce differ- 5). However,reduced growth and interrupted encesin growthrates, and pastevents can have developmentduring periodsof low food abun- longlasting effects on growththat mightmask dancehave also been reported in speciesother effectsof specificenvironmental stresses. than aerial insectivores (Dickerson and Mc~ Cance 1960, Ricklefs and Peters 1979, Price ACKNOWLEDGMENTS 1985, Schewand Ricklefs 1998). Further inves- This researchwas supportedby grantsfrom the tigationsof that phenomenonneed to discrim- North American Bluebird Society,the Frank M. inate betweentwo possibilities:(1) that the ChapmanFund of the AmericanMuseum of Natural ability to interruptgrowth is a specialadapta- History,the BenningFund of CornellLaboratory of tion of aerial insectivoresfor surviving periods Ornithology,Sigma Xi, and the Andrew W. Mellon of low food availability,or (2) that interruption StudentResearch Fund of CornellUniversity. Field in growthis an unavoidablebyproduct of low andexperimental work was approved by the Cornell body temperaturesand low food intake in University Institutional Animal Care and Use Com- "normal" passerines.Given the long nestling mittee(protocol 90-136). I am gratefulto Dawn Cha- period and potential for temporary reductions vez, MichelleEskeli, Heather Hill, CherylSisak, and Jen Zamon for assistancein the field and to Paul Al- in food supply,it is not surprisingthat inter- len for helping to coordinatefield work. Carlos rupted growthis mostoften observed in aerial Bosque,Stephen Emlen, Corey Freeman-Gallant, insectivores;it remains to be tested whether in- Nelson Hairston, Jr., David Haskell, William Schew, terruptedgrowth in speciessubject to severe David Winkler, L. LaReesaWolfenbarger, and two short-term fluctuations in food abundance are anonymousreviewers provided helpful comments special adaptationsto an unpredictable food on earlier drafts of this paper. supply. Giventhe relationshipbetween growth and LITERATURE CITED postfledgingsurvival in this population,those ALATALO, R. V., L. GUSTAFSSON,AND A. 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