Effects of Geographic Location and Habitat on Breeding Parameters of Great Tits

The Auk 115(4):1034-1051, 1998

EFFECTS OF GEOGRAPHIC LOCATION AND HABITAT ON BREEDING PARAMETERS OF GREAT TITS

JUAN Jos12SANZ • ZoologicalLaboratory, University of Groningen,P.O. Box 14, 9750 AA Haren,The Netherlands

ABSTRACT.--Istudied variation in laying date,clutch size, and numberof fledglingsin Great Tits (Parusmajor) in relationto habitat,elevation, and latitudeusing data from 137 breedingareas. Laying date was not affectedby habitattype but increasedwith elevation andshowed a significantquadratic relationship with latitude.Food availability, ambient temperature,and photoperiodtogether can explainwhy laying date increaseswith latitude. However,more information is neededto understandwhy birdsin northernAfrica start laying later than in nearbysouthwestern Europe. Variation in clutchsize and numberof fledg- lingswas significantly affected by habitattype, with lowervalues in coniferousforests. Mean clutchsize decreased with elevation.Mean clutch size and mean number of fledglingsof first and secondbroods showed a significantquadratic relationship with latitude,with thehigh- est valuesat about 55 to 60øN.The resultssuggest that latitudinal variationin life-history parametersis relatedto variationacross marginal and centralparts of the species'distri- butionand is influencedby factorssuch as daylength,temperature, and/or seasonalityof food resources.Birds at southernlatitudes are probablyunder time constraints,whereas birds at northernlatitudes are probablyunder energyconstraints. Alternatively, Great Tits at northernlatitudes might be less well adapted to thesehabitats because they invaded north- erly latitudesduring the last decades.The proportionof pairs laying a secondclutch de- creasedwith latitude.The observed pattern of a latestart of laying,lower variability in laying date,and lower frequencyof secondclutches in northernpopulations likely was due to the late and shortgrowing season for the GreatTit's main prey,caterpillars. Received 13 January 1997, accepted22 April 1998.

THE GEOGRAPHICTRENDS in reproductivepa- sivelycooler climates, the onsetof breedingis rameters of birds have been well known for de- expectedto be delayedowing to low tempera- cades(Lack 1947, Klomp 1970).The ultimate turesand slow developmentof the vegetation regulatorof the timing of breedingis the re- (Lack 1950, Slagsvoid1976, Orell and Ojanen quirementthat reproductiontake place during 1983a). the seasonin whichbirds can raise their young The evolution of clutch size is one of the most most efficiently (Lack 1950, Drent and Daan activelystudied of life-historytraits in birds 1980,Martin 1987).The availabilityof food for (Stearns1992). Clutch size is constrainedby layingfemales has been considered to be both severalfactors, the mostcommonly discussed an ultimate factor (Lack 1950, Perrins and beinglatitude and habitat (Klomp 1970, Perrins McCleery 1989,Daan et al. 1990) and a proxi- and Birkhead 1983, Murphy and Haukioja mate factor (Perrins 1970, Kallander 1974, 1987).For example,within temperateregions Drent and Daan 1980, Martin 1987) in the tim- clutchesof passerinesare larger in deciduous ing of theonset of laying.However, factors such woodlandsthan in coniferousforests (Klomp as habitat type (Klomp 1970, Blondel et al. 1970,van Balen 1973,Zang 1980,Blondel et al. 1993), temperature (Svensson and Nilsson 1987, Sanz 1995). The trend for clutch size of 1995), and photoperiod(Meijer 1989;Silverin passerinesto increasewith latitudeis oneof the 1995;Lambrechts et al. 1996,1997) also may in- moststriking patterns within and amongspe- fluencethe onsetof breeding.In areasat high cies of birds (Perrins and Birkhead 1983). latitudesand elevations,which haveprogres- Clutch size of passerinestends to be two or three eggsin tropicallatitudes (Moreau 1944, • Presentaddress: Departamento de EcologfaEv- Skutch1985), four or five eggsin middle lati- olutiva, Museo Nacional de Ciencias Naturales tudes,and five to seveneggs in arcticlatitudes (CSIC), Jos6Gutierrez Abascal 2, E-28006 Madrid, (Ricklefs 1969). This trend occursin both the Spain.E-mail: mcnsl 1 [email protected] Old World (Lack 1968) and the New World

1034 October1998] BreedingParameters of Great Tits 1035

(Cody 1971) in the Northern Hemisphere, riod or more energy to be investedin a single whereasthe trendin the SouthernHemisphere nestingattempt rather than in severalattempts is weak (Moreau 1944, Yom-Tov1987, Yom-Tov (Slagsvoid1982). The degreeof nestpredation et al. 1994, Martin 1996). seems to decrease with increasing latitude Threemain hypotheseshave been presented (Ricklefs 1969, Jehl 1971, Pedroli 1978, Kulesza to explainthe latitudinal trend in clutchsize in 1990;but see Martin 1996). passerines.First, Lack (1947) suggestedthat The precedinghypotheses predict a positive the increase in clutch size with latitude could relationshipbetween clutch size and latitude, be attributedto the increasein daylighthours but this trend may not be linear A linear in- available for parents to collect food for their crease in clutch size with latitude has been nestlings.Royarea (1969) extendedLack's hy- found in many studies(e.g. Lack 1947, Ash- pothesisto incorporatethe energy require- mole 1961, Cody 1966, Slagsvoid1975a, Kule- mentsof the youngrelative to ambienttemper- sza 1990, Young 1994), but exceptionsare not atureand the time availablefor foraging.Owen rare (e.g. Owen 1979, Orell and Ojanen 1983b, (1979)accepted Lack's daylength hypothesis as Mailer 1984, Isenmann 1987, Soler and Soler a partial explanationand introducedthe diver- 1992, Sanz 1997). Ecologicalfactors can influ- sity of potential food as an additional factor. ence to a different degree the breeding deci- Lack's(1947) hypothesis has been reformulated sions at different latitudes. At low latitudes, in a life-historycontext to encompassrepro- predationor the availabilityof daylightcan be ductive costs in terms of adult survival and/or the mostimportant factors (Sanz 1999), where- future reproductioninvolved in raising a cer- as at high latitudes,variability or unpredicta- tain number of young (Charnov and Krebs bility of food and weathermay be more impor- 1974), and with a focus on individual differ- tant (J•irvinen1983). Northern breeding popu- encesin quality (Drent and Daan 1980, Pettifor lations of passerines are more unstable, and et al. 1988,Slagsvoid and Lifjeld 1990). their environmentis more unpredictable,than Second,Ashmole (1961) suggestedthat bird are southern populations (O. J•irvinen 1979, populationsin temperateareas are regulatedin Slagsvoid1981, A. J•irvinen1983). Stability is the nonbreedingseason by foodresources. The defined as year-to-yearpersistence of commu- breedingdensity thus tendsto be low in north- nity structure(i.e. total density,number of spe- ern latitudes, and competition for food in cies, diversity and frequenciesof species;J•ir- spring and summer is relaxed. Reduced com- vinen 1979).J•irvinen (1979) showedthat pop- petition favors large clutches(Ashmole 1961, ulationstability of birds is greatestin the areas Ricklefs 1980, Koenig 1984). Studies typically of maximum density (usually in the southern relate clutch size to differences between winter or centralparts of the range).At high latitudes, and summer evapotranspiration(AE), a mea- birds under severe climatic conditions are sure that is tightly correlatedwith primary probablynear their ecologicallimit in termsof productivity (Rosenzweig1968) and, presum- acquiringenough energy for maintenanceand ably, with food availability.Correlations be- reproduction (J•irvinen 1983). Moreover, for tween clutchsize and seasonalityof AE have somepasserines clutch size tends to be lowerin been found in some studies (Ricklefs1980; Ko- marginalhabitats than in nearbyoptimal hab- enig 1984,1986) but not in others(Mailer 1984, itats (Klomp 1970, van Balen 1973, K•illander Dunn and Macinnes 1987,Young 1994). It may 1975,Alatalo et al. 1985,Sanz 1995). Peripheral be questionedwhether so crudean estimateof and central parts of the geographicranges of resourcelevels can justify rejectionor accep- speciesare associatedwith marginal and op- tanceof this hypothesis(Mailer 1984). timal habitats,respectively (Slagsvoid 1981). Third, Skutch(1949) invoked predation as a The existenceof a distributionallimit may re- possiblefactor in the evolutionof clutchsize. flect that the conditionsfor reproductionare The classicinterpretation has been that re- poor and larger clutchescannot be selectedfor duced nest predation favors larger clutches (Slagsvoid1981). Therefore,a nonlinear rela- (Skutch1949, Cody 1966, Perrins1977, Slags- tionshipof clutchsize or brood size with lati- void 1982, Ekman and Askenmo 1986, Lima tude may exist, with the maximum valuesoc- 1987, Kulesza 1990, Martin 1992) by allowing curring in the centralparts of the distribution more young to be fed over a longernestling pe- (Sanz 1997, 1999). 1036 JUANJose 5ANZ [Auk, Vol. 115

The GreatTit (Parusmajor) is oneof the most factorsaffecting the evolutionof breedingtime well-studied bird species.Great Tits breed and clutch size in Great Tits. from about10øS to 71øN(Gosler 1993), and they The aims of my study are to: (1) document are resident even at the northern limit of their latitudinalvariation in layingdate, clutch size, breeding distribution (Cramp and Perrins numberof fledglings,and proportionof second 1993,Silverin 1995). In a pioneeringstudy, Lack clutchesin the GreatTit usinga large dataset (1950) showedthat clutch size increaseswith collectedover an extensivegeographic range; latitude for different races of Great Tits breed- (2) determinewhether a linear or nonlinearre- ing in Asia. He suggestedthat clutchsize is lationshipexists between clutch size and lati- smallerin the Mediterraneanregion than far- tude; (3) determinewhether the inclusionof thernorth, although data from this regionwere habitat type and elevationaffect latitudinal limited at the time. BreedingGreat Tits have trends;and (4) discussthese results relative to beenstudied in manyparts of Europe,and the the hypothesesthat attempt to explain geo- resulting data have been subjectedto geographictrends in thesebreeding parameters. graphiccomparisons (Berndt et al. 1983,Orell andOjanen 1983b). However, these studies dis- METHODS agreedabout clutch-size variation over the geo- I obtained from the literature the mean, standard graphicalrange. A tendencyfor clutchsize to deviation,and coefficientof variation of laying date, increasenorthward in Europe (Berndt et al. clutchsize, and numberof fledglings(in somecases, 1983)or an unclearpattern with respectto lat- the numberof nestlingsin the nesttwo or threedays itude were claimed (Orell and Ojanen 1983b). before fledMing)at differentbreeding sites. These These different conclusionspossibly resulted studiesincluded only broodsin which at leastone from the relatively small number of studies youngfledged. Therefore, the estimatesof reproduc- consideredin both reviews(n = 28 in Berndtet tive successpresented are overestimatesand do not correspondexactly to the naturalaverage reproduc- al. 1983;n = 27 in Orett and Ojanen1983b) and tive successof the populations.Clutches were sepa- from the narrow latitudinal range studied(50 rated into two categories:first and secondbroods to 55øN in Berndt et at. 1983). Becauseof the (clutchlaid followinga successfulone). Data were largenumber of studiespublished on the Great available for 137 study areas (see Appendices 1 and Tit near the peripheralparts of its rangein the 2). No effect of nest-boxsize on mean clutchsize or Palearctic(Gosler 1993), it is now possibleto laying date was assumed.If data for several years analyze variation in reproductiveparameters were available, I included the mean values for each using a large data set (n = 137 areas)from an areain the analyses.In addition,I usedmy own data fromtwo breedingpopulations in Lauwersmeer,The extensivegeographic range (33 to 70øN). Netherlands(see Sanz et al. 1998)and Valsafn, Spain My review is basedon breedingdata collect- (see Sanz 1995). ed from a varietyof studiesthat were conduct- For all areas,the coordinates(latitude and longi- ed using woodennest boxes in which ratesof tude in decimal degrees)and elevationwere deter- predation and partial lossesof nestlingsoften mined. In some study areas,I obtainedthe geo- are lowerthan in natural cavities(Nilsson 1984, graphicvariables from topographicmaps. Addition- 1986). Nest-boxstudies are designedto reduce al variablesincluded in the analyseswere number of levelsof predation,and this may have obscured study years, number of nests per study area, and main habitattype. Data from urbanhabitats were not importantselective pressures on the life-his- includedin the analyses.The habitattypes were co- tory strategiesof the birds (Lindenand Moller niferous forest (n = 42), mixed coniferous/decidu- 1989).The presenceof nestboxes alleviates the ous (n = 31), and deciduous forests (n = 53). The typically severeshortage of nestingsites, and southernmoststudy area was in northern Africa in the absenceof this limitation,reproduction (33ø30'N;Chabi 1998), and the northernmostwas in may occur at a maximum rate (Linden and northern Finland (69ø42'N;Veistola et al. 1995). El- Molter 1989). Rates of predation at nest boxes evationsranged from 5 to 1,600m. Themean number and the densityof predatorsare rarelyreport- of studyyears was 7.1, with a rangeof 1 to 25 years (in eight study areas,the numberof yearswas not ed. Therefore,the effectof predationrate on lat- reportedprecisely but was alwaysmore than one). itudinal variation in breeding parameterscan- The meannumber of clutchesper study area was 178, not be testedwith publisheddata. My review with a rangeof 4 to 2,346. will thusunavoidably give a partial view of the The distributions of mean clutch size, number of October1998] BreedingParameters ofGreat Tits 1037

TABLE1. Layingdate (1 = 1 April), clutchsize, and number of fledglingsof firstclutches of GreatTits with respectto habitattype. Values are • _+SD, with n in parentheses.

Habitat type Variable Coniferous Mixed Deciduous Laying date 31.53 +--10.98 (30) 31.72 +- 8.48 (23) 29.78 -+ 9.96 (36) Clutchsize 8.74 _+0.78 (40) 8.88 +- 0.91 (31) 9.15 _+0.82 (52) No. of fledglings 6.00 _+1.38 (23) 6.37 _+1.04 (5) 7.09 _+1.44 (23) fledglings,and layingdate of firstand secondbroods a quadraticmodel (63.2%) than by a linear did not differ from normal (Kolmogorov-Smirnov model (54.6%). Including elevationinto the test,P > 0.05).Elevation was normalizedusing log- model, 65.1% of the variancein laying date arithmic transformation.I used analysisof covari- along the latitudinal cline was explainedby ance(ANCOVA) with habitatas a factorand latitude thesevariables. The variabilityin meanlaying and elevationas covariatesto separatethe relative importanceof thesevariables to GreatTit breeding date(coefficient of variation)declined with lat- parameters.Latitude and longitudefor eachbreed- itude (r = -0.68, df = 43, P < 0.001). ing populationwere positively correlated(r = 0.50, Mean clutch size in all areas was 9.01 + 0.89 df = 137, P < 0.001),and I includedonly latitudein eggs(n = 130).The habitattype of the study the analysesbecause the distributionof GreatTits areahad a significanteffect on mean clutch size shows a southwest to northeast trend. I included lat- (Table 1) when the effectsof latitude and ele- itudesquared as a covariatewhen it significantlyin- vation were controlled (ANCOVA; model, F = creasedthe explainedvariance. When one covariate 10.76, df = 5 and 117, P < 0.001; factor habitat, did not show a significanteffect on the dependent F = 4.16, df = 2 and 117, P = 0.018; covariate variable,I excludedit from the analysis.As a post- latitude, F = 6.78, df = 1 and 117, P = 0.010; hoccomparison of means,I usedthe Tukeytest for unequalsample sizes (Spjotvoll and Stoline1973). covariatelatitude squared, F = 4.46, df = 1 and Valuesare presentedas means _+SD. 117, P = 0.037; covariate elevation, F = 5.68, df = 1 and 117,P = 0.019).Clutch sizes were sig-

RESULTS nificantlylarger in deciduousforests than in coniferousforests (Tukey test, P = 0.03; Table First clutches.--Norelationships were found 1). Mean clutchsize showeda significantqua- (multiplelinear regression)between either the draticrelationship with latitude(Fig. 1) and de- numberof studyyears or numberof clutches creasedsignificantly with elevation(•B = -0.21, usedin the analysisand meanlaying date(F = t = 2.38, df = 117, P = 0.019) after controlling 2.50, df = 2 and 71, P = 0.09), mean clutchsize for the other variables. Latitudinal variation in (F = 2.12, df = 2 and 101, P = 0.12), or mean clutchsize was explainedbetter by a quadratic number of fledglings(F = 2.34, df = 2 and 34, model(22.7%) than by a linearmodel (18.5%). P = 0.06) per study area. Includingelevation and habitat into the model, The meanlaying date for all areaswas 1 May 30.5% of the variancein clutchsize along the _+SD of 9.98 days (n = 97). Mean laying date latitudinal cline was explainedby thesevari- did not differ betweenhabitats (Table 1) when ables.The variabilityin clutchsize (coefficient the effects of latitude and elevation were con- of variation)did not showany trendwith lati- trolled (ANCOVA; model, F = 34.24, df = 5 and tude (r = 0.04, df = 50, P = 0.77). 83, P < 0.001; factor habitat, F = 1.23, df = 2 The mean number of fledglingsin all areas and 83, P = 0.30; covariate latitude, F = 16.53, was 6.61 + 1.57 young (n = 52). The habitat df = 1 and 83, P < 0.001; covariate latitude type of the study area had a significanteffect squared,F = 30.43, df = 1 and 83, P < 0.001; on the mean number of fledglings(Table 1) covariate elevation, F = 7.90, df = 1 and 83, P when the effectof latitude was controlled(AN- = 0.006).The meanlaying date showeda sig- COVA; model, F = 6.34, df = 4 and 46, P < nificant quadraticrelationship with latitude 0.001; factor habitat, F = 4.06, df = 2 and 46, P (Fig. 1) and increasedsignificantly with eleva- = 0.024; covariate latitude, F = 6.26, df = 1 and tion (•B= 0.19, t = 2.81, df = 83, P = 0.006)after 46, P = 0.016;covariate latitude squared,F = controllingfor the othervariables. Latitudinal 4.87, df = 1 and 46, P = 0.032). Significantly variationin laying datewas explained better by more nestlingswere fledgedin deciduousfor- 1038 JUANJose SANZ [Auk, Vol. 115

lationshipwith elevation([3 = 0.02,t = 0.13,df = 45, P = 0.90). Latitudinal variation in number of fledglings was explained better by a quadratic model (24.9%) than by a linear model (13.0%).Including habitat in the model,36.0% of the variancein numberof fledglingsalong 2O the latitudinal cline was explainedby these 10 variables.The meannumber of fledglingsand

0 • the meanclutch size of eachstudy population 30 35 40 4• 50 • 60 • 70 were positivelycorrelated when the effectof latitude was controlled(partial r = 0.48, df = l.•timde 47, P < 0.001). Secondclutches.--The mean proportion of sec- 12 o ond clutchesdecreased significantly with lati-

11 tude (Fig. 2). The meanclutch sizes of first and secondbroods of eachstudy population were positivelycorrelated when the effectof latitude was controlled(partial r = 0.44, df = 34, P = 0.01). Mean clutch size showeda significant oo o oo oø quadraticrelationship with latitude(Fig. 2), as 7 8 o did themean number of fledglingsfrom second clutches(Fig. 2). 6 3O 35 40 45 50 55 60 65 70 DISCUSSION Latitude

12 Layingdate.--The mean laying date of Great

11 C o Tits typicallydiffers among habitats (van Balen

10 1973,Zang 1980,Blondel et al. 1987,Sanz 1995).

9 o In the presentstudy, mean laying datedid not

S differ amonghabitats after I controlledfor ele- o o o o ß vational and latitudinal variation. Mean laying 7 o o 6 datewas affected by elevationwhen the effects o oo o o of habitatand geographicvariation were con- øo 4 trolled. Great Tits bred earlier at lower eleva- 3 tions, presumably because conditions (food 30 35 40 45 50 55 60 65 availability,weather) were favorableearlier at lower elevations(Zang 1980,Sanz 1995). Latitude Mean laying date increased significantly FIc. 1. Relationshipsbetween: (upper panel) with latitude when the effects of habitat and el- meanlaying date (1 = 1 April); (middlepanel) mean evationwere controlled.The meanlaying date clutchsize; and (lowerpanel) mean number of fledg- occursin April in southwesternand centralEu- lings of first clutchesand latitude (øN). Relativeto rope and in May in northernEurope. However, laying date: Y = 75.69 - 2.76X + 0.04X2 (F = 82.73, in northern Africa birds start to breed later df = 1 and 94, P < 0.001). Relative to clutch size: Y than in nearbysouthwestern Europe. This qua- = -0.54 + 0.31X - 0.002X2 (F = 18.60, df = 2 and 127, P < 0.001).Relative to numberof fledglings:Y draticrelationship between mean laying date - 17.00 + 0.84X - 0.007X 2 (F = 8.14, df = 2 and and latitudehas alsobeen found in Pied Fly- 49, P < 0.001). catchers(Ficedula hypoleuca; Sanz 1997). Food availabilityfor the younghas been suggested asthe ultimatefactor determining the onsetof eststhan in coniferousforests (Tukey test, P = breeding (Lack 1950, Drent and Daan 1980, 0.01;Table 1). The mean numberof fledglings Perrins and McCleery 1989, Daan et al. 1990). showed a significant quadratic relationship The timing of the peakdate of caterpillarsis a with latitude(Fig. 1) but did not showany re- major selectionpressure on the timing of October1998] BreedingParameters ofGreat Tits 1039

1.20 o o laying femaleshas been postulatedas an im- o 1.00 o portant factor (Perrins 1970, von Haartman

0.•0 1971,Drent and Daan 1980).When experimen- tally providedwith extrafood, tits (Parusspp.) 0.60 advancethe timing of the egglaying by two to 0.40 eightdays (see Svensson and Nilsson1995, Na- ger et al. 1997).Therefore, above a certaincrit- 0.20 ical level of food availability, laying females 0.00 probably use other cues in their decisionto 7O 3O 40 45 •0 S5 60 65 start breeding(Svenson and Nilsson 1995). Latitude Ambienttemperature has been suggestedto influencelaying date along an elevationalor 10 latitudinal cline. As pointed out by many au- o o thors(e.g. Kluijver 1951; Perrins 1965, 1991; van 9 o Balen1973; van Noordwijket al. 1995),the on-

8 set of laying is correlatedwith ambienttemperature in two ways: first by the sum of the 7 daily meanambient temperature a few daysbe-- fore laying, and secondby somepeaks of tem- 6 o peratureabove 10øC. Ambient temperature de-

5 creaseswith latitude and elevationand might 3O 35 40 45 50 S5 60 65 be an ultimate factor causingenvironmental changesin vegetationphenology that deter- L•tude mine the peak of food abundance(Perrins 1970,

9 Perrinsand McCleery 1989,Blondel et al. 1993).

8 In tits, caterpillarsare the preferredfood dur- o o 7 ing the nestlingperiod (Perrins 1965, van Balen

6 1973, Blondel et al. 1991, Banbura et al. 1994).

5 As hasbeen demonstrated, the timingof breed-

4 ing by insectivorousbirds is adjustedto the

3 emergenceof caterpillars,and their youngare present in the nest around the peak of food 2 abundance(Perrins 1965, Perrins and McCleery 1 3O 1989, Blondel et al. 1993, Svenssonand Nilsson 1995). The onsetof gonadaldevelopment in Great FiG.2. Relationshipsbetween: (upper panel) pro- Tits is probably determinedby photoperiod portion of second clutches (arcsine transformed); (Silverin1994). In a proximatesense, photope- (middle panel) mean clutchsize; and (lower panel) riod opensand closesa window duringwhich numberof fledglingsof secondclutches and latitude reproductionin birds is possible,but within (øN). Relativeto proportionof secondclutches: Y = this window,the actualonset of egg laying is 1.46 - 0.02X (F = 8.28, df = 1 and 43, P = 0.006). determinedby additionalfine-tuning and sup- Relative to clutch size: Y = -10.10 + 0.65X - 0.006X 2 plementarymechanisms that optimizethe tim- (F = 5.52, df = 2 and 31, P = 0.009).Relative to num- ing of breeding(Martin 1987;Perrins 1991; Na- ber of fledglings:Y: -29.10 + 1.30X - 0.012X2 (F = 4.67, df = 2 and 14, P = 0.028). ger and van Noordwijk 1995;Lambrechts et al. 1996,1997). The onsetof gonadaldevelopment is regulatedby an increasein the secretionof breeding in tits (Blondelet al. 1993).Presum- gonadotrophinthat is regulatedby thenumber ably,parents must have mechanismsto antici- of hours of daylight (i.e. the photoperiodic patethe mostfavorable period for raisingtheir threshold;Silverin et al. 1989).Variation in pho- young(Perrins 1970). The onsetof breedingis toperiodicthreshold values may accountfor thereforeinfluenced by a varietyof proximate latitudinal differencesin the timing of breed- factors.The amountof food availablefor egg- ing amongbirds (Silverinet al. 1993).The pho- 1040 JUANJose SANZ [Auk, Vol. 115 toperiodicthreshold increases with increasing higher instability and unpredictabilityin cli- latitude (Silverinet al. 1993).Comparing the mate at higher elevations(Cody 1966,Stearns criticaldaylength when the photoperiodiniti- 1976).Clutch size was smallerin montanehab- atesgonadal development with the time of year itats, presumablybecause breeding conditions daylengthreaches this thresholdat different (food availability,weather) were lessfavorable latitudes, Silverin (1995) concludedthat pro- for insectivores (Zang 1980, J•irvinen 1983, viding extra food during the prebreedingpe- Sanz 1995). Alternatively,predation rate has riod cannever advance egg laying more than a beenproposed to explainthis elevational trend week, which is in agreementwith food-provi- (Slagsvoid1982). Nest predationprobably in- sioningexperiments (see Svensson and Nilsson creaseswith increasingelevation because pas- 1995, Nager et al. 1997). At different latitudes, serinesbreed early in the year relativeto the the onsetof breedingcannot occur much earlier stageof vegetationdevelopment at higherele- than the observeddates for the laying of the vations(Slagsvold 1975b, 1977, 1982).Also, be- firsteggs in thepopulation (Silverin et al. 1993). causethe structureof the vegetationis less Silverin et al. (1993) showedthat although complex,nest detection by predators may be Great Tits normally do not breed at the earliest easierat higherthan at lowerelevations (Slags- time possible,the delay in breedingonce con- vold 1982). ditions are favorable becomes shorter the far- Clutchsize and numberof fledglingsof first ther north the birds breed. This reflects the fact and secondbroods showed a quadraticrela- that the breedingseason of northernbirds is tionshipwith latitude,with increasingvalues short(Ricklefs 1966, Orell and Ojanen1983a). up to 55 to 60øN.Similar relationships occurred Thus, three related factors--food availability, for the Pied Flycatcheramong different breed- ambient temperature,and photoperiod--to- ing populations in Europe (Sanz 1997). An in- gethercan explain why laying date increases creasein clutchsize with increasinglatitude with latitude.However, why do birds breeding has beenattributed to the increasein daylight in northernAfrica startlaying solate? Photo- hours availablefor parentsto collectfood for periodcannot explain this fact,but the peakof their nestlings(Lack 1947, Royama 1969, Owen food abundancemay be later in northern Af- 1979). Daylengthincreases with latitude,but rica. More information is necessaryto under- the lengthof activity periodsduring the nest- stand this difference. ling period(i.e. the time betweenthe first and The coefficientof variationin mean laying lastfeeding visits to the nest)for bothPied Fly- date decreasedsignificantly with latitude, in- catchers(Sanz 1999) and GreatTits (Sanzet al. dicatinga shorterbreeding season at high lat- 1998) is asymptoticallyrelated to daylight itudes.A similarbreeding synchrony occurred hours.That is, at southernlatitudes, parents in Great Tits during yearswith "late" springs useall of the availabledaylight hours to collect (Slagsvoid1976). Hence, increased synchrony food for their young,which is not the caseat aslaying date increases may be the rule in this northernlatitudes (Sanz et al. 1998,Sanz 1999). species (Slagsvoid 1976, Orell and Ojanen Lack (1954)suggested that "... an increasein 1983a).This patternmight be due to local ad- daylengthfrom 12 to 18 hours is probably justmentto environmentalconditions and may much more effective than an increase from 18 be a consequenceof later and shortergrowing to 24 hours..." and that the increase in clutch seasons farther north for the Great Tit's main size should be small from central to northern prey, caterpillars(Slagsvold 1975a). Europe.However, as in Pied Flycatchers(Sanz Clutchsize.--Mean clutch size and the pro- 1997),I foundthat clutchsize in GreatTits does ductionof fledglingsin GreatTits typicallydif- not increase from central toward northern Eu- fer amonghabitats (van Balen 1973, Zang 1980, rope. This suggeststhat the amountof time Blondelet al. 1987).In the presentstudy, these availablefor foraging is not the only variable differencesremained after controllingfor vari- that affects latitudinal variation in clutch size. ation in elevation and latitude. In agreement Theenergy requirement of thebrood relative with an earlierstudy (Zang 1980),I observeda to ambienttemperature has beenproposed as decreasein clutchsize with increasingeleva- one of the factors that affect latitudinal variation. This is in contrastto the suggestionthat tion in clutch size in altricial birds (Royama clutch size increaseswith elevationowing to 1969).Because ambient temperature during the October1998] BreedingParameters ofGreat Tits 1041 nestlingperiod decreaseswith latitude(Sanz large-scalemodification of the environment 1999),the energyrequirements of the brood may have reducedevolutionary constraints of should increase. The balance between the en- nestpredation on life-historytraits in Europe- ergy requirementsof the broodrelative to the an populationsof birds (Martin and Clobert duration of the activity period and ambient 1996).Consequently, patterns of nestpredation temperaturemight explain latitudinal variation and the importanceof foodversus nest preda- in clutchsize. Parentsin the southernpart of tion to life-historyvariation may changesuch the rangehave smaller clutches than in thecen- that foodmay be a moreimportant influence in tral part becausethey areprobably under time Europe (Martin and Clobert 1996). constraints.In contrast,parents in thenorthern For passerines,clutch size tendsto be lower part of the rangemay be under energycon- in marginalhabitats than in nearbyoptimal straintsbecause the energy requirements of the habitats(Klomp 1970,van Balen 1973, Zang brood in relation to ambient temperatureare 1980, Sanz 1995, Dias 1996). Peripheraland higherthan in the centralpart of the range centralparts of the geographicranges of spe- (Sanz 1999). ciesare associatedwith marginaland optimal Ashmole's(1961) hypothesis,which is a habitats,respectively (Slagsvoid 1981). It has modificationof Lack's(1947) hypothesis, sug- beensuggested that breeding populations near gests that competitionfor resourcesmay be the margins of the distributionalrange are more severe at southern latitudes than at north- moreunstable than those in the centralparts of ern ones.This may be due to the factthat north- the range(Slagsvoid 1981). This is partlybased ern populationsapparently are more variable on the finding that the degreeof annualfluc- than southernones and thus are frequently tuationin breedingdensity is higherin mar- kept below the carryingcapacity of the envi- ginalthan in nearbyoptimal habitats (Kluijver ronment. Because seasonality probably in- and Tinbergen1953, von Haartman1971). The creaseslinearly with latitude,the hypothesis existenceof distributional limits may reflect predictsa linearincrease in clutchsize with lat- that conditionsfor reproductionare poor such itude (Ashmole 1961, Ricklefs1980). However, that larger clutchescannot be selectedfor I did not find a linear increase in clutch size or (Slagsvoid1981, Sanz 1997).A nonlinearrela- numberof fledglingswith latitude.Ashmole's tionshipbetween clutch size or the numberof hypothesishas been supported in somestudies fledglingsand latitudecan be predicted,with (Ricklefs 1980; Koenig 1984, 1986) but not in maximumvalues occurring near the centerof others(Moller 1984,Dunn and Macinnes1987, the distribution(Sanz 1997).My resultsagree Young 1994). with this prediction;mean clutch size and An alternative hypothesis (Skutch 1949, numberof fledglingswere highest more or less Cody 1966,Perrins 1977, Slagsvoid 1982, Lima near the centralpart of the species'distribu- 1987,Kulesza 1990) suggests that a decreasein tion. Maximumvalues of productionwill be af- nest predationwith latitude might result in fectedby habitat quality and also by factors larger clutches.The presentdata set includes suchas daylength/activityperiod (Lack 1947, only nest-boxstudies, and data on predation Sanz1999), energy requirements of the nest- ratesand densitiesof predatorswere not avail- lings relative to temperature(Royama 1969), able.However, comparative analyses using dif- and seasonalityof food resources(Ashmole ferentmethods that considerthe phylogenetic 1961,Ricklefs 1980). The lack of a geographic relationshipsamong species indicate that pre- trend in clutch-sizevariation (i.e. coefficientof dation rate may be an important factor deter- variation)and the positivecorrelation between mining clutch size in some studies (Martin clutchsize and number of fledglingsreflect that 1995) but not in others(Trevelyan and Read parentslay a clutchsize that theycan success- 1989, Yanesand Su•rez 1997).Factors that di- fully rear giventhe localenvironment (Moller rectly affectnest predation potentially may ex- 1984, Sanz 1997). ert a stronginfluence on life-historyevolution Finally,there might be alternativeexplana- (Martin and Clobert1996). For example, Martin tionsto localspecialization. For example, Great (1995)showed that the type of nestsite and mi- Tits retreated to the southwestern corner of Eu- gratoryhabit (i.e. residentvs. migrant)affect ropeduring the lastglaciation, rapidly extend- nestpredation and life-history traits. Moreover, ed their distribution northeastward after the 1042 JUANJOSS SANZ [Auk, Vol. 115 end of the last ice age (Gosler1993, Silverin tores y Tecn61ogos(PB94-0070-C02-01) from the 1995), and invaded northern latitudes about Ministerio Espafiolde Educaci6ny Cultura. 1,000years ago (Silverin et al. 1993). However, they havealso changed their distributiondur- LITERATURE CITED ing the last decades.Before 1930, the GreatTit ALATALO, R. V., A. LUNDBERG,AND $. ULFSTRAND. did not breednorth of 63øN,but todaythey are 1985. Habitat selectionin the Pied Flycatcher. common up to 70øN (Haftorn 1957, Silverin Pages 59-63 in Habitat selection in birds (M. 1995).This spread to the northis probablydue Cody, Ed.). AcademicPress, Orlando, Florida. to climaticfactors and the ability to winter in ALLANDER, K., AND G. E BENNETT. 1995. Retardation areas of human settlement (Haftorn 1957, of breedingonset in Great Tits (Parusmajor) by Cramp and Perrins 1993, Silverin 1995). Re- blood parasites.Functional Ecology 9:677-682. cently,Meril• et al. (1996,1997) discovered that ASHMOLE,N. P. 1961. The biology of certain terns. Ph.D. dissertation,Oxford University,Oxford. the geneticvariability of the Greenfinch(Car- BALAT,E 1970. Clutch size in the Great Tit, Parusma- duelischloris) is extremely low and decreases jor Linn., in pine forestsof southernMoravia. with increasinglatitude across continental Eu- Zoologick6 Listy 19:321-331. rope.Meril• et al. explainedthis resultin terms BALAT,E 1976.Fortpflanzungs6kologie der H6hlen- of a Pleistocenebottleneck and gradual lossof brtitenden V6gel im stidmahrischenKiefern- variationassociated with serial bottlenecking wald. Acta Scientiarum Naturalium Academiae during the recolonizationof northernEurope. Scientiarum Bohemicae Brno 10:1-44. GreatTits expandedafter the lastglaciation to B•LDI, g., AND t. CS•RG•. 1993. Effect of habitat on the clutchsize and egg dimensionsof the Great new habitatsin which they might be lesswell Tit (Parusmajor). Aquila 100:201-209. adapted.The declinein clutchsize and number BALEN,J. H. VAN.1973. A comparativestudy of the of fledglingsfrom centraltoward northern Eu- breedingecology of the GreatTit Parusmajor in ropemay be in agreementwith thishypothesis. different habitats. Ardea 61:1-93. By producinga secondclutch, an individual BANBURA,J., J. BLONDEL,H. DE WILDE-LAMBRECHTS, Great Tit can enlarge its production of fledg- AND M. J. GALAN.1994. Nestling diet variation lings in a breeding season (den Boer-Haze- in an insular Mediterraneanpopulation of Blue winkel 1987,Verboven and Verhulst1996). Ver- Tit Paruscaeruleus: Effect of years,territories and individuals. Oecologia100:413-420. bovenand Verhulst(1996) recently showed that BARBA,E., D. M. GARCIA,J. g. GIL-DELGADO,AND G. the probability of a secondclutch is related M. LOPEZ.1994. Moth abundanceand breeding mainly to the layingdate of the first clutch.In successin a Great Tit populationwhere moths agreementwith Orell and Ojanen(1983a), the are the main nestlingfood. Ardea 82:329-334. meanproportion of secondclutches was nega- BELLAVITA,M., AND A. SORACE.1991. Date of laying, tively correlatedwith latitude. This likely is clutch size and secondbrood percentagein due to the shortbreeding season in the north- Great Tit Parusmajor and Blue Tit Paruscaeruleus in the Natural Reserve "Monte Rufeno" (VT, ern part of the species'distribution, there being Central Italy). Avocetta15:43-49. no time to completetwo breeding attemptsin BERNDT,R., W. WINKEL, AND H. ZANG.1983. Ober le- oneseason. The observedpattern of a late start gebeginnund gelegestarkevon Kohl- und Blau- of laying, lower variability in laying date,and meise(Parus major, P. caeruleus) in beziehungzur low frequencyof secondclutches in northern geographischenlage des brutortes.Die Vogel- populationsmay be a consequenceof a late and warte 32:46-56. short growingseason for the Great Tit's main BJ•RKLUND,M., AND B. WESTMAN.1986. Adaptive prey, caterpillars(Slagsvold 1975a). advantangesof monogamyin the GreatTit (Par- usmajor): An experimentaltest of the polygyny threshold model. Animal Behaviour 34:1426- ACKNOWLEDGMENTS 1440. BLONDEL,J., g. CLAMENS,P. CRAMM, H. GAUBERT, I am very gratefulto E Isenmannand Y. Chabifor AND P. ISENMANN.1987. Population studies on providing data from northernAfrica and to J. Tin- tits in the Mediterraneanregion. Ardea 75:21- bergen,S. Verhulst, J. Moreno J. Ekman, A. Gosler,M. 34. Orell, and an anonymousreviewer for constructive BLONDEL,J., g. DERVIEUX, M. MAISTRE, AND M. PER- commentson the manuscript.I was supportedby a RET.1991. Feeding ecology and life historyvari- postdoctoralgrant (Formaci6nde PersonalInvesti- ation of the Blue Tit in Mediterranean mainland gador) and a Contratode Reincorporaci6npara Doc- and islandhabitats. Oecologia 88:9-14. October1998] BreedingParameters ofGreat Tits 1043

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t"-,I t"-,I t"-,I 1050 JUANJose SANZ [Auk, Vol. 115

o c, +1 +1 +1 • +1 +1 +1 +1 +1 +1 +1 +1 +1 +1 • +1 +t +1 •

+1 +1 +1 October1998] BreedingParameters ofGreat Tits 1051

APPENDIX2. Breedingdata (;7 -+ SD) for secondclutches of GreatTits fromdifferent study sites in Eurasia. For layingdate, 1 = 1 April (roundedto nearestday).

Layingdate Clutchsize No. of fledglings Reference Latitude 60 to 70øN 7.2 ñ 2.04 1.8 +- 2.29 Veistola et al. (1995) 91 +_ 6.3 7.5 -+ 1.59 6.0 Orell and Ojanen(1983a, b, c) 7.8 Haartman (1969) 6.9 6.3 Johansson(1972, 1974, 1977) Latitude 50 to 60øN 7.8 Glutz von Blotzheim and Bauer (1993) 7.3 Orell and Ojanen(1983b) 7.1 5.9 Larsen (1974) 9.5 7.8 Likhachev(1953, 1967) 74 _+ 9.1 7.4 _+ 1.57 5.8 -+ 1.71 Sanz (unpubl.) 8.4 Glutz von Blotzheim and Bauer (1993) 8.4 Lack (1958) 7.9 Lack (1958) 8.6 Kluijver (1951) 8.5 Kluijver (1951) 7.9 Kluijver (1951) 7.0 Kluijver (1951) 7.6 Lack (1958) 7.3 Lack (1958) 7.3 4.9 Orell and Ojanen(1983b, c) 7.1 4.5 Orell and Ojanen(1983b, c) 6.8 4.8 Orel! and Ojanen(1983b, c) Latitude 40 to 50øN 9.4 G!utz von Blotzheim and Bauer (1993) 7.7 De!mee et al. (1972) 7.7 Muller (1985) 8.0 Muller (1985) 7.4 Muller (1985) 7.2 G!utz von Blotzheim and Bauer (1993) 8.1 Warga (1939) 61 _+ 2.7 8.8 _+ 0.60 5.7 -+ 0.90 Isenmann (1983) 7.9 3.6 Cramm (1982) 7.0 _+ 1.80 5.8 -+ 2.40 Bel!avita and Sotace(1991) 6.5 _+ 2.00 5.4 _+ 1.80 Bel!avita and Sorace(1991) 6.5 -+ 0.50 3.5 _+ 2.50 Bel!avita and Sorace(1991) 69 _+ 9.1 5.7 -+ 0.87 2.8 Fidalgo (1990) 6.5 5.3 Kiziroglu (1982)