TheAuk 115(4):955-963, 1998
FOREST
SIZE AND
REPRODUCTIVE
ISOLATION
SUCCESS
HAVE
OF EURASIAN
NO EFFECT
ON
NUTHATCHES
(SITTA EUROPAEA) ERIK MATTHYSEN 1 AND FRANK ADRIAENSEN
Department of Biology,Universityof Antwerp,B-2610Antwerpen,Belgium
ABSTRACT.--We collecteddata on breedingsuccess, nestlingmass,fledgingdate,and recruitmentof EurasianNuthatch(Sittaeuropaea) nestingattemptsin a numberof small(200 ha) forests.Moststudyareas were dominatedby well-developedoak stands.We foundno differencesin reproductiveparametersbetweenfragmentsand the two largeforests,nor anyrelationshipwith thesizeor degreeof isolationof individual fragments.Failednestsmoreoftenwere takenoverby nest competitors(particularlystarlings)in fragments,but this did not seemto affectoverallsuc-
cessrates.Pairsnestingin parkshada lowerchance toproducerecruitsthanpairsin similarsizedoak fragments,and early broodsrecruitedmore offspringthan late broods.We con-
cludethatfragmentation doesnotaffectthesuitabilityofmatureoakstands forreproduction of nuthatches within thesizerangeof oakstandsfrequented by thisspecies. Received 14July 1997, accepted 12 March 1998.
FRAGMENTATION
OF NATURAL
HABITATS is a
potential threat to the persistenceof animal and plant populationsin many different kinds of landscapes andhabitattypes(Saunders et al. 1991,Andr•n 1992,Robinsonet al. 1995).Many studieshave demonstrateda lower diversity and/or abundanceof various organismsin habitatfragmentscomparedwith largerhabitat tracts (e.g. Soul• 1986, Opdam 1991, Matthysenet al. 1995b).Two majorgroupsof hypothesesto explain these patterns involve changesin populationstructureand habitat quality, respectively.Changesin population structure include a reduction in population size,diminishingdispersal betweenpatches or betweenlocalpopulations within a metapopulation,andlossof geneticvariation(Gilpinand Hanski1991).Changesin habitatqualitymay resultfrom the increasinginfluenceof abiotic andbioticelements fromthesurrounding landscape(the matrix) on the habitatremnant,or from changesin communitystructurewithin the habitat(e.g.abundance of prey,parasites, predators,competitors;Soul• 1986,Saunderset al. 1991).Consequently, fitnessparametersand ultimatelypopulationgrowthmaybenegatively (or positively)relatedto the natureof adjacenthabitatsaswell asthe size,shape,and degreeof isolationof theremainingpatches. Relativelyfew studieshavedocumentedthe
effectsof habitatfragmentation on fitnessparameters.The prominentexceptionis the reproductive successof open-nesting birds, whichgenerallydecreases in smallerfragments and/or nearhabitatedgesowingto increased predationor brood parasitism(Gatesand Gysel1978,BrittinghamandTemple1983,Moller 1988, Kurki and Linden 1995, Robinson et al.
1995). This pattern has been verified experimentallyby the useof artificialnestsin a wide variety of habitats(Andr•n 1992, Santosand Telleria 1992, Burkey 1993, Nour et al. 1993). However,nestpredationand broodparasitism are unlikely to provide a generalexplanation for the effectsof habitatfragmentationonbird species thatnestin moreprotectedsitessuchas tree cavities.Reproductivesuccessof cavitynestingbirds may be influencedby otherfactors suchas changesin competitionfor nest sitesor in foodavailability,but very few studies haveaddressed reproductivesuccess in forest fragments(Kuitunenand Helle 1988,Tjernberg et al. 1993, Nour et al. 1998).
The EurasianNuthatch (Sitta europaea) appearsideallysuitedto testwhetherforestfragmentationaffectsreproductivesuccess of a cavity-nesting bird species. Theeffectsoffragmentation are well documentedat the population level but the underlyingcausesare not resolved. Nuthatches have been shown to be less
abundant in small and isolated forest fragmentsand in that respectare amongthe most
E-mail:
[email protected] 955
956
MATTHYSEN AND ADRIAENSEN
[Auk, Vol. 115
fragmentation-sensitiveforest bird species (OpdamandSchotman 1987,vanDorp andOpdam 1987,Enoksson et al. 1995,Matthysenun-
publ. data). These negative effects have generally been attributedto lack of dispersal,or to
higher mortality during dispersal among fragments(Verboom et al. 1991,Enoksson et al. 1995,Matthysenet al. 1995a,Matthysenand
Currie1996),buteffects ofresource availability
(nest sites and/or food) have notbeen studied.
In thebreeding season, nuthatches aregeneralistinsectivores thatmainly gleanandprobe for arthropodsonbarkandleaves.Theyareob-
ligatesecondary cavitynesters, andcompetition for suitable
nest sites is well documented
(e.g. Nilsson 1984).Here, we report on reproductive success of nuthatches in a set of forest
and parkland fragmentsof varying sizes, as well as in two larger forests. METHODS
Study speciesand areas.--In western Europe, Eur-
o
o
5
lO
15
28
Size (ha) FIG.1. Sizedistributionof forestfragmentswith at leastone observationof EurasianNuthatches(n =
38), excludingonelarge(30ha) fragmentwith 16observations (see text).
asian Nuthatchestypically occurat relativelylow densities(oneto fivepairsper 10 ha) in maturedeciduouswoodland. They normally raise a single large, degree surrounded by agricultural land, broodper yearin a naturalcavityor oldwoodpecker whereasthe otherhalf of the parkswerelargelysurnest. Pairs defend the same territory year-round (Matthysen1990). Most of the data were collected from 1990 to 1994 in a 200-km2 study area closeto Antwerp, northern Belgium. The study area contained scatteredforest patchesor parkland areas with extensivewooded cover (henceforth"fragments")that togethercoveredonly 1.5%of the area (seeMatthysenet al. 1995a).Additionaldata were collected in two study plots within large forests (>200 ha; seebelow).Forthisstudy,fragmentswere definedas discretepatchesof a singlehabitattype ("oak forest"or "park") separatedfrom similarhabitat patchesby at least100m (typically•-500m). Using this definition,we neverobservedcolor-banded individuals to include more than one fragmentin their homerange.A few patcheswith nuthatches but belongingto otherforesttypeswere not considered in this study.All oak forestfragmentswerewell-developedstands(>20m canopyheight) of common oak (Quercusrobur),with at most 10% other trees suchasEuropeanbeech(Fagussylvatica), birch(Betula spp.), and red oak (Quercusrubra).Park areas were mostly old private estates,often turned into public parks, with a mixture of woodland, ponds, lawns and paved areas.The wooded vegetationin theseparks consistedof large old trees,often •-30 m tall, mainly oak and beechbut alsoornamentaltrees suchaslime (Tiliaplatyphyllos), horsechestnut(Aesculushippocastanum), and someconifers.All of the oak fragmentsand abouthalf of the parkswereto a
roundedby residentialareas.Only a few fragments were connectedby hedgerows,and thesewere usually onlyonetree-widthwide. Nestboxesof various types and sizeswere presentin only a few areas. Fragmentsizes as measuredfrom aerial photographsvariedfrom 0.8to 30 ha (Fig. 1).Adjacentgardens with scatteredtrees were not incorporatedin this measure, and lanes connected to a woodlot were
only incorporatedif at leastthreeor four treeswide. Becausemost fragmentswere small (Fig. 1), sizes werelogarithmicallytransformedto obtaina normal distribution for statistical analysis (KolmogorovSmirnov test, untransformed P = 0.02, transformed
P > 0.9). On average,parkswere somewhatsmaller (;• = 4.6 ha, range1.5to 14 ha) thanoak stands(;• = 6.9 ha, range0.8 to 28 ha), but the differencewasnot significant(Mann-WhitneyU-test,z = -0.97, P > 0.3).The degreeof isolation(I) from othernuthatch habitatwascalculatedby a modifiedversionof Whitcombet al.'s (1981) gravitationindex, calculatedfor eachfragmentas: I = -log •, (T,/d?),
(1)
whered = distancefromthe focalfragmentto the ith fragment(includingall fragmentswithin the 200km2studyareaandthe 2-km zonearoundit), and T = the maximum
number of nuthatch territories
in
the ith fragmentduringthe study.Weusednumber of territories rather than size because this allowed us
to integratedifferenttypesof habitatsupportingdif-
October1998]
Breeding Success ofNuthatches
ferent population densities.In particular, densities in parks were 50% higher than thosein oak fragments(Matthysenunpubl.data),which may be explained by differencesin canopyvolume,tree-speciesdiversity,or other factors.The number of territoriesin both habitattypeswasa simplelinearfunction
of
size
and
was
not
related
to
isolation
(Matthysenunpubl. data). Logarithmictransformation was used to obtain a normal distribution (Kolmogorov-Smirnov test, untransformed P • 0.001, transformed P > 0.5).
In additionto the fragments,we studiedtwo plots
of about28 ha within largerforests:Peerdsbos (PB; >200 ha, data collected1991 through 1994), and Meerdaalbos(MB; ca. 1,500 ha, data collected1992
through1994).Theseforestsarelocated15km north and 40 km southeastfrom the fragments,respectively. Bothstudyplotswere situatednear the edgeof the forestborderingon agriculturalland. The plots were dominated by oaks (>80%), and only nests within oak stands were studied. In all oak forests we measured
trunk
circumfer-
ence at breastheight of 20 commonoaks and convertedthisto diameterasan indexof habitatquality. This measurement
was chosen both for ease of mea-
957
per fragment,with the exceptionof the largestfragmentZR. In this30-hafragment,of which16ha were studied, 28 nesting attempts were monitored; ZR was treated separatelyin all analyses. Most nests were observed only from a distance. Breeding stage was inferred at least every 10 days basedon parentalbehavior(i.e. nestbuilding, incubation, feedingnestlingsand fledglings).Nestswere scoredas successfulif they producedlargenestlings or fledglings, or unsuccessfulif they failed before producinglarge nestlings.For eachsuccessfulnest, the range of possiblefledgingdateswas estimated using the followingassumptions(Matthysen1998): incubationor brooding (on eggsor small young)occurred until the young were at most 10 days old; nestlingswere fed for a maximum of 25 days, and were not seenin the nestentranceuntil 3 daysbefore fledging;and fledgedyoungstayedwith their parents for no more than 20 days. If this range couldbe narrowed down to 10 days or less,the midpoint was taken as the best estimateof fledging date (n = 57). A subsampleof nests(n = 88) wasinspectedwhen the youngwere suspectedto be between10 and 18 daysof age.Nestlingswere counted(i.e.brood size), aged (Winkel 1970),individually colorbanded, and weighed(in 1993and 1994only). In 11 broodsan exact count was not possible.Youngwere assumedto fledge at 23 days (Matthysen1998)unlessfledging
surementand becauseoak standswere very similar in other respectssuchas canopycover,tree-species composition,and understory.Treeswere chosenarbitrarily by tossinga pencilin theair at roughlyequi- was observeddirectly. Each spring and summer distant intervals along an arbitrary transect, and most fragmentswere searchedfor color-banded measuringthe nearesttree at about15 m in the in- nestlings(Matthysenet al. 1995a).Recruitmentwas dicated direction that had a circumference of at least definedas the probabilitythat at leastone nestling 50 cm. Mean trunk diameterswere larger in large from a successfulnest was observedagain at least foreststhan in fragments(œ= 55 vs. 46 cm;F = 4.7, one month after fledging, i.e. after the dispersalpedf = 1 and 14,P = 0.047),but therangesoverlapped riod had begun. completely(large forests,53 to 58 cm; fragments,37 Data analysis.--Variationin reproductiveparameto 60 cm).Habitatqualitywasnot estimatedin parks ters was studied on two levels. On the first level, we becauseof the large variation in tree species,tree analyzed variation among five categoriesof study size, and other characteristics that were difficult to area:oak fragments,park fragments,the 30-hafragassess(i.e. disturbance,degree of canopy cover, ment (ZR), and the two large forests.Becauseof the paved areas,lawns, etc.). smallsamplesfor broodsizeand fledglingmass,the Nestobservations.--Each springwe locatedasmany threelargestforestswerepooledfor analysisof these nestsas possible.Nestswere found by following fe- variables.On the secondlevel, we related reproducmalesduring nestbuilding and maleswho were pro- tive parametersto characteristics of individual fragvisioningtheir incubatingmates.A few nestswere ments,excludingthe 30-hafragment.Thesecharacfound during the nestlingstage.Includingrenesting teristicswere habitat type (oak or park), fragment attempts, we found 8 nests in 1990, 61 to 68 from size (log transformed),and isolation as defined 1991 to 1993, and 43 in 1994 (253 neststotal). There above.For oak and park fragmentswhere sample were no secondbroods.Only 16% of the nestswere sizes were sufficiently large, additional analyses in nest boxes. When we detected a nest failure, based comparedthe variablestrunk diameter(measuredin on nest inspectionor lack of parent attendanceon oak fragmentsonly) or matrix type (agricultural or successiveobservations,we searchedthe territory residentialin park fragmentsonly,becauseall oak againfor renestingattempts.Wecouldnot searchall fragmentsbelongedto the formertype).Fortheanalfragmentsfor renestingattempts,but we conducted ysisof recruitment,we alsoincludedthe distancebesuchsearches withoutbiasasto fragmentcharacter- tweenthe fragmentcenterand the centerof the enistics. Causes of failure were not established, but we tire studyarea,becausebirdsborn in the periphery noted whether the nest was taken over by another arelesslikely to be foundwithin thestudyarea(Matspeciesat the first observationfollowingfailure.We thysen et al. 1995a). We assumedthat nestswithin studied from 1 to 12 (median = 3) nesting attempts fragmentsprovide independentinformationrelative
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MATTHYSEN AND ADRIAENSEN
[Auk, Vol. 115
TABLE 1. Reproductive parameters of EurasianNuthatches in oakfragments, parks,andoakstandswithin largerforests(i.e.ZR, PB,MB). Valuesbetweenbracketsaresamplesizes(in the two top rows,numberof pairs or broods/numberof fragments). Proportionof
Proportionof Standardized pairs successful fledgingdatea
Area Oak fragments
0.69 (52/12)
Parks ZR (30 ha) PB (300 ha) MB (1,500ha) Total
0.84 (25/5) 0.79 (24) 0.86 (35) 0.61 (23) 0.75 (159)
0.8 (34/11) -1.6 (51/16) 0.03 (19) 0.9 (29) 3.3 (16) --
Brood size
Fledgling mass(g)
broodswith recruits
7.2 (20/8)
24.6 (10/5)
0.35 (17/8)
6.0 (35/15) 6.2 (4) 6.8 (13) 6.8 (5) 6.5 (77)
24.4 (9/4) __b 23.4 (10) __b 24.1 (29)
0.14 (37/16) __ -__ 0.20 (54)
Relativeto overallyearly mean. Pooled
with
PB.
to the investigatedfragment variables.Also, we not vary between years or areas (logisticrecould not checkfor independence of nestsby the gression,year effect:X2 = 2.4, df = 3, P > 0.3; sameindividualsbecause onlya sampleof themwas area effect: X2 = 8.0, df = 4, P = 0.09). Pairs in
banded. However, because the total number of nests
per fragmentwasratherlow (median= 3, different years combined), violation of these assumptions would haveonly a limited effect. Breedingsuccess, nest-sitetakeover,and recruitment were analyzedas0/1 responsevariablesin logisticregressionmodelsusingGLIM (Crawley1993). For analysesinvolvingonly one independentvariable, we calculatedFisher exactprobabilitieswith STATXACT.Breedingsuccesswas analyzedas success(0/1) of a pair, either from a first or a repeat nest.For this analysiswe omitteda numberof areas where we did not systematicallysearchfor repeat nests.Fledgingdate,broodsize,and meanfledgling masswere analyzedwith PROCGLM usingtype III sumof squares(SAS1994),or with ANOVAif all independentvariableswere factorial.Fledgingdates werestandardizedper year(seeResults).In bothlo-
oakfragmentshadan intermediatesuccess rate betweenthosein the two largestforests(Table 1).
We analyzedbreedingsuccessin relationto fragment characteristics for oak fragments only,because forparkareasboththenumberof failures (n = 4) and the number of different fragments(n = 5) wassmall.Theinitial model for oak fragmentsincludedyear,threehabitat parameters(size, isolation,trunk diameter), andtwo-wayinteractions amongthethreehabitat parametersonly.Noneof the variablesexplained a significantamount of variationin breedingsuccess (Ps > 0.1).Because the effect of isolationwas rejectedat P = 0.06 (X2 = 3.6 in a model also containing size, diameter, and their interaction),we reenteredthis variablein
gisticregressionand GLM, modelselectionwasperformedby backwardeliminationof leastsignificant eachsuccessive stepof themodelselection, but terms starting from a model including all interac-
it nevercamecloseto significance(all Ps > 0.2). The final modelwasslightlyoverdispersed (X2 not tested in analysesof brood size, fledging mass, = 64.2, df = 51) but this doesnot affectthe contions,unlessspecifiedotherwise.In particular,interactionsbetweenhabitatparametersandyearwere
or recruitmentwhere annual sample sizes were
clusions.
small.
Nest-site takeover.--Failednesting cavities weretakenoverby EuropeanStarlings(Sturnus vulgaris)in 11 casesand Great SpottedWoodpeckers(Dendrocopos major)in 9 cases(Table2).
Lower-order
terms
were
not
eliminated
as
longastheywereincorporatedin higher-orderterms still in the model.All testparametersreferto thelast modelthat includedthe parameteror interactionbefore it was removed.All final logisticmodelswere checkedfor overdispersion(Crawley 1993). Chisquaretestshave one degreeof freedomunlessin-
Because of the small number of failed nests in
parks(seeabove),theanalysiswasrestrictedto oak fragmentsand large forests.Takeoverby starlingswasmorecommonin fragmentsthan in the three large forestscombined(29% vs. RESULTS 6%,respectively; Fisherexacttest,P = 0.01;Tafollowedthe Breeding success.--Overall, 120 of 159 of nut- ble 2). Takeoverby woodpeckers hatch pairs (75%) successfully raised large sametrend,but the differencewasnot signifinestlingsor fledglings.Breedingsuccessdid cant (19% vs. 9%; P = 0.3; Table2). Within the dicated
otherwise.
October1998]
Breeding Success ofNuthatches
TABLE2. Proportionof failed EurasianNuthatch nests(%) that were takenoverby EuropeanStarlingsor GreatSpottedWoodpeckers; n = number of failures,with numberof fragmentsin parenthesesfor oak fragmentsand parks. Takeoverspecies Star-
Area
959
not shown) revealedthat in oak fragments, nestingwas earlier in small, nonisolatedfragmentsandin largeisolatedfragments,whereas in park fragmentsthe reversewas true.In addition, we found an interactionbetweenfragmentsizeand trunk diameterin oakfragments (F = 5.2, df = 1 and 28, P = 0.03). Broods
Wood-
ling pecker None
Oak fragments Parks ZR (30 ha) PB (300 ha) MB (1,500ha)
29 0 13 0 7
19 0 13 10 7
52 100 75 90 87
Total
16
13
71
n 31 (12) 4 (4) 8 10 15 68
fledgedearliestin smallfragmentswith small treesandin largefragments with largetrees.It should
be noted
that
when
the
interaction
termswere deletedfrom the previousmodels, noneof the main effectsof habitattype, isolation, fragmentsize,or trunk diameterwere sig-
nificant(all Ps • 0.1). In the park fragments, however, there was an additional effect of ma-
oak fragments,takeoverby starlingswas not related to fragment size, isolation,or trunk diameter(logisticregression, all Ps• 0.1;yeareffectsnot tested).Takeoverby woodpeckers was influencedby a size x diameter interaction term (X2 = 7.0,P < 0.01).Inspectionof thedata parameterestimatessuggestedthat takeovers occurredmoreoftenin large fragmentsif trees
trix type on fledgingdate (F = 7.0, df = 2 and 46, P < 0.01).Broodsin parkswithin residential areasfledgedan averageof 5.3 daysearlier
thanthosein parkssurrounded by agricultural land.Thiseffectremainedsignificantevenin a model without
interactions.
Broodsize.--Brood size varied from 2 to 10 (œ
= 6.5, n = 77). The three largestforestswere lumped in the analysis.Brood size varied were large.However,this effectwas not very amongareas(F = 4.2, df = 2 and 73, P = 0.02) robustbecauseit disappearedwhen a single nestin a very smallfragment(0.8 ha) was re- andwith fledgingdate(F = 5.0,df = 1 and73, studied in 1991, we first verified that no area x
P = 0.03)but not amongyears(P > 0.5). Brood size was largestin oak fragments,followedby larger forestsand parks (Table 1), and it de-
teraction, F = 11.3, df = 1 and 77, P = 0.001).
cline in brood
moved (X2 = 2.1, P > 0.1). Fledgingdates.--Becausearea MB was not
yearinteraction waspresentin the1992to 1994 creasedwith time by 0.08 + SE of 0.03 fledgdata (two-wayANOVA, F = 0.7, df = 8 and 84, lings per day. Mean brood size differed bebut neitherdifP • 0.5). A secondtest, without an interaction tweenoakandparkfragments, fered from brood size in large forests(Tukey term, on the four yearsof data showedthat test, c• = 0.05). fledgingdatesvariedbetweenyears(F = 13.7, An analysison broodsize in relationto fragdf = 3 and 130, P < 0.001) but not between arment characteristics (not includingthe three eas (F = 1.8, df = 4 and 130, P > 0.1). For furlarge forests) confirmed the effectsof habitat theranalysis,we recalculated fledgingdatesas type (F = 7.7, df = 1 and 52, P < 0.001)and date differencesfrom the overall yearly means. Thesevariedfrom25 May (1993and1994)to 1 (F = 6.2, df = 1 and 52, P = 0.02) but revealed June(1992).Mean standardizedfledgingdates no effectsof year, fragment size, or isolation (all Ps • 0.1).Accordingto this analysis,sucper areaare shownin Table1. Withinthefragments(n = 85broods),fledg- cessfulbroodsfledged 1.5 more young in oak ing datewasrelatedin a complexway to hab- fragmentsthan in parks when we controlled deitat, isolation,andfragmentsize(three-wayin- for theeffectsof fledgingdate.Theseasonal size was similar
to that in the
Whenthe analysiswas repeatedfor eachhab- completedataset(0.09per day).In thefollowitat type (includingextra variables,seeMeth- ing analysesbasedonhabitattype,yeareffects were no longer tested. In thesampleof oakfragmentsusedto study teractionsboth in oak and park fragments,but with oppositesignsfor the parameteresti- broodsize,the threehabitatparameters(size, mates (oak: F = 15.8, df = 1 and 28, P < 0.001; isolation, trunk diameter) were significantly park: F = 4.7, df = 1 and 46, P = 0.03). Inspec- correlated (r2 between 0.22 and 0.7, all Ps • tion of the predictedresponsesurfaces(details 0.05)and were thereforeenteredoneby onein ods), we found significantsize x isolationin-
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MATTHYSEN AND ADRIAENSEN
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the later stagesof model selection.Fragment size and isolationalsohad no effect(bothX2 < 0.3, P > 0.5). The final model containedonly fledgingdate(X2 = 9.9,P < 0.01)and habitat was also a date effect (F = 6.1, df = 1 and 32, type (X2 = 6.3, P = 0.01). Broodsin oak fragP = 0.02)and a significanteffectof matrixtype mentswere more than twice as likely to pro(F = 6.2, df = 1 and 32, P = 0.02);nestsin parks ducerecruitsthan were thosein parks (Table surroundedby agriculturalland containedan 1), andbroodswith recruitsfledgedan average averageof 1.8 more nestlings(correctedfor of 5.5 daysearlierthanthosewithoutrecruits. date)thanthosein residentialareas.Again,we foundno effectsof fragmentsizeor isolation(P DISCUSSION > 0.2).Note thatin thisanalysis,no higher-order interactions were included in the initial Our mainobjective wasto testthehypothesis model. that habitatfragmentation reducesthe reproMass at fiedging.--Meannestling mass was ductive successof a cavity-nestingbird. We recorded for 29 broods in 1993 and 1994 at esfound no evidencefor reduced reproductive timated agesof 14 to 17 days.Body massdid output in fragmentsversuslarge forests,nor notvarywith agebetweendays14 and17 (F = for relationships with fragmentsize or isola6.2, df = 3 and 25, P = 0.09) and thus is con- tion. Nuthatches in oak fragmentshad an insideredto representmassat fledging(f = 24.1 termediatesuccess ratecomparedwith thosein g). the two largerforestsandhad relativelyhigh Becauseof the smallsamplesizes,the three brood sizesand fledglingmasses,but no siglargestforestswere againlumpedfor analysis nificant differences were found. The mean (total n = 10 broods),and no higher-orderin- numberof youngper pair was very similarin teractionswere tested.Fledgingmassdid not oak fragmentsand parks (5.0young/pair) and differ amongareas(F = 2.6, df = 2 and 25, P = largeforests(5.1young/pair;threelargestfor0.1) or years (F = 2.0, df = 1 and 21, P > 0.1) estspooled).Fragmentation had no effecton and was not relatedto fledging date (F = 0.3, fledgingdate,whichis importantgiventheefseparatemodels.None of thesethreeparametershad a significanteffecton broodsize(all Ps > 0.1), but the effect of fledging date remained(P < 0.05).In theparkfragmentsthere
df = 1 and 24, P > 0.3) or brood size (F = 2.3,
fect of date on the chance of recruitment
df = 1 and 27, P > 0.1).Within the fragments (19 broodsin 9 fragments),therewasno relationshipwith year,habitattype,fragmentsize or isolation,fledgingdate,or brood size (all Ps > 0.1).No further testsweredoneonparksand oak fragmentsseparately. Recruitment.--Within thefragmentareas(excludingthe 30-hafragment),15 recruitswere found from 11 differentbroods(Matthysenet
the study area. A premium on early fledging had beenpredictedbasedon the severecompetition for summerterritoriesvery soonafter fledging (Matthysen1987, 1990) but is confirmedherefor the first time.The complexstatisticalinteractions amongthe effectsof fragmentsize,isolation,andhabitattype on fledging date are difficultto interpret,but they do not suggesta consistenteffect of fragmenta-
al. 1995a).We performed a logistic regression
tion.
on the probabilitythat a brood producedat least one recruit, with the independentvariableshabitattype,log fragmentsize,isolation, distancefrom the centerof the study area, fledging date, and number of young banded per brood. Becauseof the small sample,we only includedfour two-wayinteractions, chosena prioriin the initial model(habitatx size, habitatx isolation,habitatx fledgingdate,size
One couldarguethat breedingperformance is not a goodindicatorof habitatqualitybecausebirds may follow an "ideal free" distribution among territories of different quality
within
within and between habitats (Fretwell 1972,
Matthysen1990) such that expectedfitness doesnotvarywith theaveragequalityof a habitat. Accordingto this reasoning,the combinationof high breedingsuccess and low denx isolation). sity in oak fragmentsmight imply that on avSurprisingly,brood size and distancefrom erage,territoriesare poorer,but that only the the centerweredroppedin the earlystagesof best territories are occupied.However, obsermodel selection(both X2 < 0.2, P > 0.5) and re- vationson dispersaland territory establishmainednonsignificant evenwhenreenteredin mentsuggest thatthebestterritoriesarenotal-
October 1998]
Breeding Success ofNuthatches
961
ways selected(Matthysenand Currie 1996). areas.Dhondtet al. (1984)founda similarpatFurthermore, the fact that nuthatch densities tern in Great Tits but not Blue Tits, and sugare not correlated with the size or isolation of gestedan effect of anthropogenicfood (i.e. individualfragments(Matthysenunpubl.data) seeds,bread,fat) that is morereadilytakenby rules out any "ideal free" explanationfor the GreatTits, and alsoby nuthatches. lackof a relationship betweenbreedingsuccess Our conclusionthat forest fragmentation and fragmentcharacteristics. doesnot affect the quality of oak forest as The only parameterthat differedbetween breedinghabitatagreeswith thefewpublished fragmentsandlargeforestswastheprobability studiesof other cavity nesters.Kuitunenand of nesttakeoverby otherspecies.Aggressive Helle(1988)foundno relationshipbetweendistakeoverby EuropeanStarlingsis a common tanceto forestedgeandnestingsuccess, clutch cause of nest failure in Eurasian Nuthatches size, or laying date of EurasianTreecreepers (L6hrl 1956,1958;Nilsson1984)and othercav- (Certhia familiaris).Althoughtheydid not conity nesters(e.g.Troetschler1976,Kerpezand siderfragmentsize,any changein thisparamSmith 1990). Our observationsare not suffi- eter necessarilyleads to closer proximity to cientlydetailedto distinguishbetweenactive edges.Nour et al. (1998)foundno consistent efevictions that cause brood failure, and take- fectsof fragmentsize on reproductiveparamovers of previously abandonednests. Even eters of Great Tits and Blue Tits in forests simthoughit did notseemto affecttheoverallsuc- ilar to thosein ourstudy.Tjernberget al. (1993) cessratein fragments,thefrequentoccurrence foundno differencein breedingsuccessor layof takeovers suggests thatcompetition for nest ing dateof BlackWoodpeckers (Dryocopus marsiteswas intense.Indeed, starlingswere very tius)in a large forestand thosein an agriculabundantin somefragmentsbut ratherscarce tural area where eachterritory encompassed in thelargeforestplots.In a verydifferenthab- manysmallfragments.However,noneof these itat, Kerpezand Smith(1990)foundthatprox- studiesinvestigatedthe effectsof size or isoimity to agriculturalland increasedthe com- lation of a large numberof fragments. The contrastbetweenthe resultsfor cavity petition for nest sites between starlings and woodpeckers. nestersand open-nestingbirds is not entirely The differencesin reproductiveparameters unexpected,becausecavities are better probetweenoak fragmentsand parks, although tected from predatorsand brood parasites.A unrelatedto habitat fragmentation,revealed potential cost of cavity nesting is increased that our studyis sufficientlypowerfulto detect competitionfor nestsites,and our study sugeffectsof habitatquality.Broodsin parkswere gests that such competitionincreaseswith significantlysmallerby 1.5 nestlings,whichis fragmentation, eventhoughtheeffectonbreedprobablynot causedby variationin clutchsize. ing success appearsto be limited. The aboveIn similar habitats,Dhondt et al. (1990) found cited studies on cavity nesterscould not adconsiderable
between-area
differences
in brood
dress this issue, either because customized
sizes(but not clutchsizes)of Great Tits (Parus boxeswere provided (treecreeper,tits) or bemajor) and Blue Tits (Parus caeruleus).Food causethe focal specieswas a dominantcomavailabilitymight be lowerin parks,wherein- petitor (woodpecker).Food availability does sectpopulationson exotictreescanbe expected not appear to be lower in smaller or more iso-
to be less diverse(Kennedyand Southwood latedfragments,asshownby largebroodsize 1984), but this was not reflectedin lower nest- and high nestling body mass. This result ling masses.Broods in parks also were less agreeswith studieson food provisioningand likely to producerecruits.Again,foodcouldbe breedingsuccessin tits in similar areas(Nour an explanation througheffectsonpredispersal et al. 1998). Previousstudieshave reacheddimortality or on predispersalcondition affect- vergent conclusionson the effectsof forest ing futuresurvival.Anotherpossibilityis pre- fragmentation onarthropodpopulations. Some dationon youngnuthatches by corvids,which found reductionsin abundanceor speciesdiweremoreabundantin parksthanin oakfrag- versity (Faeth and Kane 1978, Nilsson and ments(Matthysenunpubl.data).A final result Ebenmann1981), whereasothersfound no efis that parks surroundedby residentialareas fects (Morse 1977, Middleton and Merriam had earlierfledgingdatesthan thosein rural 1983, Nilsson et al. 1985).
962
MATTHYSEN ANDADRIAENSEN
[Auk,Vol. 115
namics: Empirical and theoretical investigaThelowerbreedingdensitiesof nuthatches in tions. Academic Press, London. fragmentscomparedwith largeforestsareunlikely to be explainedby reducedhabitatqual- KENNEDY, C., AND t. g. E. SOUTHWOOD.1984. The number of speciesof insectsassociatedwith ity, a conclusionthat is further supportedby British trees: Re-analysis.Journal of Animal relativelyhigh survivalrates(MatthysenunEcology53:455-478. publ. data).This reinforcesour earlierconclu- KERPEZ,t. g., AND N. S. SMITH.1990. Competition sion(Matthysenand Currie 1996)that thevital between European Starlings and native wooddemographic parameteraffectedby forestfragpeckersfor nest cavitiesin saguaros.Auk 107: 367-375. mentationis survival during or shortly after dispersal,rather than reproductiveperfor- KUITUNEN,M., ANDP. HELLE.1988.Relationshipof mance of established birds. ACKNOWLEDGMENTS
the Common TreecreeperCerthiafamiliaristo edgeeffectand forestfragmentation.OrnisFennica 65:150-155.
KURKI,S., ANDH. LINDI2N.1995.Forestfragmentation due to agricultureaffectsthe reproductive We are grateful to Luc Wautersand Luc Lens for success of the ground-nesting BlackGrouseTehelp in the field, to Andr• Dhondt for discussions trao tetrix. Ecography 18:109-113. and encouragement, and to JeufSpitsfor providing L•bHRL,H. 1956. Der Star als Bruth6hlenkonkurrent. data on trunk diameter.EM was supportedby the Vogelwelt77:47-50. National Fund for ScientificResearch(FWO) as se-
niorresearchassistant andresearch associate, andby researchgrantnumber1.5.503.93N.For moreinformationon this and relatedresearch,consulthttp:// alt-www.uia.ac.be/ u/matthys/ ownwork.html.
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