The impact of climate and cyclic food abundance on the timing of breeding and brood size in four...

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Oecologia ISSN 0029-8549Volume 165Number 2 Oecologia (2010) 165349-355DOI 101007s00442-010-1730-1

The impact of climate and cyclic foodabundance on the timing of breeding andbrood size in four boreal owl species

1 23

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Oecologia (2011) 165349ndash355

Authors personal copy

DOI 101007s00442-010-1730-1

POPULATION ECOLOGY - ORIGINAL PAPER

The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species

Aleksi Lehikoinen middot Esa Ranta middot Hannu Pietiaumlinen middot Patrik Byholm middot Pertti Saurola middot Jari Valkama middot Otso Huitu middot Heikki Henttonen middot Erkki Korpimaumlki

Received 8 October 2009 Accepted 7 July 2010 Published online 28 July 2010copy Springer-Verlag 2010

Abstract The ongoing climate change has improved ourunderstanding of how climate aVects the reproduction ofanimals However the interaction between food availabilityand climate on breeding has rarely been examined While ithas been shown that breeding of boreal birds of prey is Wrstand foremost determined by prey abundance little informa-tion exists on how climatic conditions inXuence this rela-tionship We studied the joint eVects of main preyabundance and ambient weather on timing of breeding and

reproductive success of two smaller (pygmy owl Glauci-dium passerinum and Tengmalmrsquos owl Aegolius funereus)and two larger (tawny owl Strix aluco and Ural owl Strixuralensis) avian predator species using long-term nation-wide datasets during 1973ndash2004 We found no temporaltrend either in vole abundance or in hatching date andbrood size of any studied owl species In the larger speciesincreasing late winter or early spring temperature advancedbreeding at least as much as did high autumn abundance ofprey (voles) Furthermore increasing snow depth delayedbreeding of the largest species (Ural owl) presumably byreducing the availability of voles Brood size was stronglydetermined by spring vole abundance in all four owl spe-cies These results show that climate directly aVects thebreeding performance of vole-eating boreal avian predatorsmuch more than previously thought According to earlierstudies small-sized species should advance their breedingmore than larger species in response to increasing tempera-ture However we found an opposite pattern with largerspecies being more sensitive to temperature We argue thatthis pattern is caused by a diVerence in the breeding tacticsof larger mostly capital breeding and smaller mostlyincome breeding owl species

Keywords Global warming middot Reproduction middot Weather conditions middot Rodent abundance middot Capital and income breeding

Introduction

Food abundance and weather conditions are key factorsinXuencing the reproductive success and distribution of ani-mals (Newton 1998 Cox and Moore 2005 Begon et al2006) There has been an upsurge of accounts documenting

Communicated by Herwig Leirs

Esa Ranta deceased during the preparation of the manuscript

Electronic supplementary material The online version of this article (doi101007s00442-010-1730-1) contains supplementary material which is available to authorized users

A Lehikoinen (amp) middot P Saurola middot J ValkamaFinnish Museum of Natural History University of Helsinki PO Box 17 00014 Helsinki Finlande-mail aleksilehikoinenhelsinkifi

E Ranta middot H Pietiaumlinen middot P ByholmDepartment of Biological and Environmental Sciences Ecology and Evolutionary Biology University of Helsinki PO Box 65 00014 Helsinki Finland

O HuituSuonenjoki Research Unit Finnish Forest Research Institute Juntintie 154 77600 Suonenjoki Finland

H HenttonenVantaa Research Unit Finnish Forest Research Institute PO Box 18 01301 Vantaa Finland

E KorpimaumlkiSection of Ecology Department of Biology University of Turku 20014 Turku Finland

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350 Oecologia (2011) 165349ndash355


the eVects of the ongoing global climate change on wildlifeFor example among birds it has been shown that bothhigher temperature and higher food abundance can sepa-rately lead to an advancement of breeding (eg Newton1998 Dunn 2004) Timing of breeding is a crucial life his-tory variable as the earliest breeders typically have thehighest breeding success (Daan and Tinbergen 1997) butbreeding too early or too late may decrease reproductiveoutput if breeding time does not meet the food peak (Visseret al 2004)

The relative importance of food and weather for avianbreeding has rarely been compared in the same study (but seeKruumlger 2004 Nooker et al 2005) This is particularly true forbirds of prey whose breeding success is known to dependon prey abundance (eg Mikkola 1983 Newton 1998)Heikkinen et al (2007) modelled and predicted the futuredistribution of four owl species in Finland as a function ofchanges in temperature and land-use patterns Howeverchanges in species distribution rarely occur in such a linearmanner Climate-induced changes in species distribution areconditional on changes in local population demography iethe sum of the eVects of breeding survival and dispersalBreeding success can be expected to be particularly impor-tant because as in animals in general young birds are moreprone to disperse than adults (Clobert et al 2001) Since cli-mate may aVect breeding of species directly eg throughincreases or decreases in the survival of oVspring caused bychanging weather conditions (Ludwig et al 2006) or indi-rectly through the food chain eg changes in food or preda-tor abundance (Both et al 2006 Martin 2007) it isimperative to determine the relative importance of food sup-ply and direct weather conditions on owl reproduction

Here we aim to analyze the joint eVects of prey abun-dance and weather conditions on the timing of breeding andbreeding success of two small (pygmy owl Glaucidiumpasserinum L Tengmalmrsquos owl Aegolius funereus L) andtwo larger (tawny owl Strix aluco L and Ural owl Strixuralensis Pall) boreal forest avian predators belonging tothe same vole-eating avian predator guild and over-winter-ing at northern latitudes (Mikkola 1983) In particular wewanted to Wnd out (1) what is the role of temperature inrelation to main food abundance in determining the timingof breeding and reproductive success in four owl speciesand (2) are the responses diVerent between smaller(Tengmalmrsquos and pygmy owls) and larger species (Ural andtawny owls) To the best of our knowledge this is the Wrstlarge-scale long-term study (including over 38000 broodrecords during 32 years Table 1) that investigates howfood abundance and weather conditions aVect the reproduc-tion of an assemblage of bird of prey species Stevensonand Bryant (2000) have suggested that as a response toincreasing temperature small species are capable ofadvancing their breeding more readily than large birds

Therefore we could expect that the smaller owl specieswould show a stronger response to increasing temperature

Materials and methods

Our study includes four owl species native to the northernboreal forests pygmy owl Tengmalmrsquos owl tawny owland Ural owl (Table 1) All species are primarily residentbut pygmy owl and Tengmalmrsquos owl show some degree ofnomadic behaviour (Schoumlnn 1980 Mikkola 1983 Korpimaumlkiet al 1987) Breeding of all species is strongly aVected bylocal rodent abundance Egg-laying typically occurs fromMarch to April except in the pygmy owl which breedsapproximately 2ndash4 weeks later in April and May (Mikkola1983 Fig 1a)

We used brood ringing records from Finland (data ofMuseum of Natural History) to study breeding phenologyand reproductive success during 1973ndash2004 The timing ofbreeding was determined as the date of hatching This wascalculated based on the wing length of the largest nestling(Jokinen 1975 Korpimaumlki 1981 Pihlaja 1999 httpwwwnicfiraquomattisj) If wing length data were not available weassumed that the brood was ringed at the species-speciWcmean age of ringing (Table 1 see also Electronic supple-mentary material ESM Fig 1)

Prey abundance was measured by snap-trapping voles(genera Microtus and Myodes) in spring and autumn ateight trapping sites The location and time periods of trap-ping sites are shown in Fig 2 For each trapping site thetrapping results (voles100 trapping nights) were log(x + 1)transformed into both autumn and spring indices (Hanssonand Henttonen 1985 Brommer et al 2002 Korpimaumlki et al2005) The annual mean vole abundance did not show atemporal trend during the study period (Lehikoinen et al2009) On the whole despite ongoing climate change thevole cycles are still prevailing in our study sites unlike insome other areas in northern Europe (Ims et al 2008Brommer et al 2009)

Table 1 Number of ringed broods for the four owl species includingannual minimum and maximum numbers proportion of broods whichinclude wing length data mean age during ringing used in hatchingdate calculations (see also Electronic supplementary material Fig 1)and mean weight in grams (Cramp 1985)

Species No broods Wing data ()

Mean age sect SD

Mean weight (g)

Pygmy owl 3738 (0ndash656) 723 159 sect 40 65

Tengmalmrsquos owl

13267 (80ndash1473) 322 189 sect 43 130

Tawny owl 9125 (93ndash437) 391 220 sect 53 500

Ural owl 12396 (87ndash793) 525 191 sect 45 800

123

Oecologia (2011) 165349ndash355 351


Broods that were situated within a 50-km radius aroundthe trapping sites were used for model Wtting (data wasannually pooled and locations with less than three broodswere omitted) The spatial scale of the synchrony of voledynamics exceeds this 50 km (Sundell et al 2004 Huituet al 2008) By using data of the nearest weather station(n = 70 stations) of each brood we calculated the meanmonthly temperature both before and during laying (Februaryand March March and April in pygmy owl) and at the timeof brood rearing (May June in pygmy owl) The onlyweather variable that showed a temporal trend was Apriltemperature which has increased signiWcantly since the1970s (Lehikoinen et al 2009) We modelled how tempera-ture before and around laying was associated with the tim-ing of breeding and whether temperature around laying andduring brood rearing was associated with reproductive suc-cess For each species we built 15 multiple linear regressionmodels using combinations of the following explanatoryvariables vole abundance in the spring of breeding and inthe preceding autumn two monthly temperatures and snowdepth on 15 March (ESM Tables 1ndash4) Vole abundancein spring and in autumn were both included when vole

abundance was included Variables were standardised(mean zero standard deviation one) before analysisModels were ranked according to AIC and species-speciWcparameter estimates for the variables were obtained byusing model averaging without any AIC weight ()threshold (Burnhamn and Anderson 2002) All statisticswere done in MATLAB 70

Results

None of the owl species showed a signiWcant long-termtrend in the timing of breeding or brood size (Spearman

Fig 1 Timing of breeding (a) and brood size (b) of four owl species inFinland in 1973ndash2004 There were no temporal trends in timing ofbreeding (trends and their 95 conWdence intervals 0026 sect 0378iexcl0109 sect 0273 iexcl0061 sect 0301 iexcl010 sect 0239 for pygmy owlTengmalmrsquos owl tawny owl and Ural owl respectively) or in broodsize (trends and their 95 conWdence intervals 0039 sect 00530005 sect 0021 0003 sect 0014 0000 sect 0014 for pygmy owl Teng-malmrsquos owl tawny owl and Ural owl respectively) in any of the species

Fig 2 Map of Finland showing vole trapping sites (black dots)weather stations (open dots) and brood ringing sites of Ural owls (greydots) for example Trapping sites are situated in Heinola (61degN 26degE1987ndash2004 Brommer et al 2002) Kauhava (63degN 23degE 1973ndash2004Korpimaumlki et al 2005) Paimio (60degN 23degE 1989ndash2004 the data ofFinnish Forest Research Institute as in rest of the sites) Hauho (61degN24degE 1981ndash1998) Korpilahti (62degN 25degE 1979ndash2004) Lieksa(63degN 30degE 1987ndash2004) Toholampi (64degN 24degE 1987ndash2004) andPuolanka (65degN 28degE 1990ndash2004)

123



rank correlation all P gt 005 Fig 1a b) For hatching datethe coeYcients of determination of the top-ranked modelswere 016 035 058 and 058 for pygmy owl Tengmalmrsquosowl tawny owl and Ural owl respectively (ESM Tables 1ndash4)High vole abundances in the previous autumn advancedthe timing of breeding in all but the smallest species thepygmy owl Additionally the timing of breeding in thetawny (iexcl186 daysdegC in March) and the Ural owls (iexcl048daysdegC in February) was negatively related to late winteror early spring temperature Increasing snow depth delayedbreeding in the Ural owls (009 dayscm) and there wasalso a similar non-signiWcant tendency in Tengmalmrsquos owls(010 dayscm cf Table 2) The breeding phenology of thepygmy owl was not signiWcantly associated with the mea-sured weather variables (Table 2) There were diVerencesbetween species in the relative impact of vole abundanceand weather The summed Akaike weights of the tempera-ture variables had as high importance on hatching dates asvole variables in the tawny and the Ural owls (100 forvoles and temperature in both species) but in the pygmyowl and Tengmalmrsquos owl temperatures were not as impor-tant (pygmy owl 071 vs 052 for voles and temperaturerespectively and Tengmalmrsquos owl 100 vs 068 for volesand temperature respectively ESM Tables 1ndash4)

For brood size the coeYcients of determination of thetop-ranked models were 031 038 028 and 033 forpygmy owl Tengmalmrsquos owl tawny owl and Ural owlrespectively (ESM Tables 1ndash4) As expected brood sizesin all four owl species were positively related to vole abun-dance in the current spring Furthermore snow depth in

March was positively associated with brood size inTengmalmrsquos owl (Table 2)

Discussion

Our main Wnding was that breeding performance of borealforest owls was to a substantial degree determined byweather conditions and not just determined by the abun-dance of their main prey Weather variables have been sel-dom included in the earlier breeding analysis of boreal owls(eg Korpimaumlki 1987a b Pietiaumlinen and Kolunen 1993but see Korpimaumlki and Hakkarainen 1991) Increasing pre-laying temperature advanced breeding in the two largestspecies Ural and tawny owls This kind of result has beenshown in many other studies mainly with passerines butalso with larger non-passerines (reviewed by Dunn 2004)Climatic factors especially snow cover have an importantrole in the boreal zone by aVecting the availability of volesfor hunting owls on one hand and inXuencing the mam-malian community structure and thus vole populationdynamics on the other (Hansson and Henttonen 1985 1988Korpimaumlki 1986)

The smaller pygmy owl and Tengmalmrsquos owl showedthe weakest temperature response in hatching dates whichis in disagreement with earlier Wndings reporting that bodysize is inversely related to the ability of a bird species toadvance its breeding in relation to temperature (Stevensonand Bryant 2000) On the contrary the timing of breedingin tawny and Ural owl was strongly aVected by late winter

Table 2 Impact of vole abundance and weather on the timing of breeding and brood size in four species of owls

Pre-laying laying and brood rearing months February March and May respectively for Tengmalmrsquos owl tawny owl Ural owl March Apriland June respectively for pygmy owla CoeYcients and their 95 conWdence intervals of normalized variables for hatching date models after model averaging CoeYcients that diVersigniWcantly from zero are in boldb CoeYcients and their 95 conWdence intervals of normalized variables of brood size models after model averaging CoeYcients that diVer sig-niWcantly from zero are in bold

Speciesa Voles Temperature Snow depth

Autumn Spring February March April March

Pygmy owl iexcl006 sect 030 iexcl024 sect 043 iexcl006 sect 028 001 sect 016 iexcl003 sect 020

Tengmalmrsquos owl iexcl046 sect 022 iexcl013 sect 028 002 sect 015 iexcl012 sect 028 020 sect 027

Tawny owl iexcl030 sect 022 iexcl023 sect 037 iexcl009 sect 030 iexcl046 sect 032 011 sect 026

Ural owl iexcl040 sect 016 iexcl002 sect 030 iexcl025 sect 022 iexcl013 sect 025 027 sect 018

Speciesb Voles Temperature Snow depth

Autumn Spring March April May June March

Pygmy owl iexcl013 sect 030 049 sect 043 001 sect 015 iexcl021 sect 038 010 sect 031

Tengmalmrsquos owl 004 sect 021 033 sect 029 015 sect 026 000 sect 010 039 sect 022

Tawny owl 015 sect 027 046 sect 030 002 sect 017 000 sect 014 004 sect 021

Ural owl 030 sect 020 036 sect 023 013 sect 025 iexcl002 sect 013 iexcl005 sect 018

123



or early spring temperature Larger species the tawny owland the Ural owl resemble capital breeders (Drent andDaan 1980 Joumlnsson 1997) where breeding is largely basedon stored energy resources (Hirons et al 1984 Pietaumlinenand Kolunen 1993) For example in the Ural owl supple-mentary feeding prior to and during the laying period didnot substantially advance timing of breeding nor result inobvious increases in clutch size during the current spring(Karell et al 2008) In contrast breeding dates of Teng-malmrsquos owl were advanced due to supplementary feeding(Korpimaumlki 1990 Houmlrnfeldt and Eklund 1990) The smallerpygmy owl and Tengmalmrsquos owl are closer to incomebreeders which acquire resources for laying and incubationduring the breeding season (Schoumlnn 1980 Korpimaumlki1987b 1990 Houmlrnfeldt and Eklund 1990 Houmlrnfeldt et al1990 Korpimaumlki and Hakkarainen 1991)

In general larger species show a higher degree of capitalbreeding (Meijer and Drent 1999) We propose that thebreeding conditions of capital breeding birds are enhancedif the winter has been mild and thus they are able to breedearlier This is because re-tapping of energy reserves is eas-ier during mild than during harsh winters (Birkhead et al1983 Newton 1998 Lehikoinen et al 2006) This is alsosupported by the known fact that in the tawny owl ovariangrowth starts about 3 months prior to the breeding seasonand is positively associated with body mass (Hirons et al1984) The severity of the winter has also been shown tohave a negative eVect on tawny owl survival (Francis andSaurola 2004) but not on Tengmalmrsquos owl survival InTengmalmrsquos owl over-winter survival is largely deter-mined by ambient vole abundance (Hakkarainen et al2002) Thus capital breeders may begin to mature physio-logically for breeding well in advance of egg laying andthey can be aVected both by weather conditions and foodabundance over a long period of time We encourage fur-ther investigation on how increasing temperatures eitherdirectly or via changes in food abundance will aVect capitaland income breeders in other study systems also includingother taxa than birds

Decreasing breeding success during the course of thebreeding season is a well-documented phenomenonin birds (reviewed by Brinkhof et al 1993 in owls seeeg Korpimaumlki 1987b Pietiaumlinen 1989 Korpimaumlki andHakkarainen 1991) and birds in good condition areable to breed earlier than birds in poor condition (egKorpimaumlki 1990 Pietiaumlinen and Kolunen 1993 Daan andTinbergen 1997) Nevertheless early breeding is not ben-eWcial if it increases the cost of breeding due to colderweather or if food conditions are clearly improving onlylater in the season Thus breeding too early may cause amismatch between resources and breeding (Thomas et al2001 Visser et al 2004 Ludwig et al 2006 Charmantieret al 2008)

High autumn vole abundance advanced breeding of thethree early breeding owl species Only in the later-layingpygmy owl did spring vole abundance appear to have astronger albeit non-signiWcant eVect on hatching datesThe pygmy owl begins to lay eggs 2ndash3 weeks later than theother species and thus their breeding is likely to be moreaVected by spring than autumn vole abundance The pygmyowl is the only one of the species in question which dis-plays hoarding behaviour during early winter (Schoumlnn1980 Mikkola 1983 Solheim 1984) Thereby food cachescan work as a buVer during adverse weather conditions(Halonen et al 2007) Since none of the tested variablesshowed a signiWcant eVect on the timing of pygmy owlbreeding it can also be possible that the late breedingpygmy owls use alternative prey species such as passerinesas a source of energy needed for the initiation of breedingThe two largest species also need to start to accumulatetheir body reserves for breeding earlier than the smallerspecies and thus autumn prey density may have longer-last-ing carryover eVects necessary for breeding (eg Brommeret al 2004) In addition vole trappings were conducted inMay at least 1 month later than the laying of most of theowl species This can also partly explain why autumn voleabundances are more strongly connected with timing ofbreeding than spring vole numbers During the late peakphase of the vole cycle owls also face a well-knowndilemma breeding is begun in good conditions duringtimes of high prey abundance but the collapse of vole pop-ulations may occur in the beginning or middle of breedingor even after the reproductive season Since the timing ofthe collapse varies between cycles it can have immenseimpacts on the reproduction success despite pre-laying con-ditions being otherwise equal (Korpimaumlki and Hakkarainen1991 Karell 2007)

In Tengmalmrsquos owl breeding success improved with thethickness of the snow cover in March (Table 2) Thinnersnow cover and earlier snow melt may increase predationon voles (Hansson and Henttonen 1985 Korpimaumlki 1986Halonen et al 2007) and alternating thaw and freezingcycles (frost seesaw) can be harmful for wintering voles(Aars and Ims 2002 Solonen 2006) Reduction of the snowlayer could lead to a paradoxical pattern where huntingconditions and even winter survival are improved due tothinner snow cover (Korpimaumlki 1986 Francis and Saurola2004 Ural owl in Table 2) and breeding could be startedearlier due to better body condition However increasedpredation during late winter and early spring may result indecreased vole densities at the time when owl parentsshould start to feed their oVspring Compared to the otherstudied owl species Tengmalmrsquos owl is more of a vole spe-cialist whereas the other species to some extent also usebirds in their diet during breeding (eg Schoumlnn 1980Korpimaumlki 1981 Mikkola 1983 Kullberg 1995) This may

123



be a reason why only the breeding success of Tengmalmrsquosowls showed a positive relationship with snow cover InTengmalmrsquos owls deep snow layer could theoretically cause adelay in the timing of breeding (Korpimaumlki 1987b) butsince the general impact of voles on the timing of breedingis larger than that of snow depth (Table 2) this eVect willlikely vary between vole-cycle phases

Our results are based on correlation analysis and thus wemust stress that making further conclusions is not necessarilystraightforward compared to experimental studies Howeverbased on the large geographical scale of the study and long-term datasets of several species we are conWdent that thestrong patterns we have found are also biologically relevant

As a conclusion our results suggest that increasing tem-peratures in the future may aVect the breeding of owls bychanges in the reproductive phenology As early breeding isoften associated with larger clutches (Pietiaumlinen 1989Korpimaumlki and Hakkarainen 1991 Daan and Tinbergen1997) global warming may also aVect reproductive outputespecially in larger capital breeding species Furthermoremilder climate can improve body condition and winter sur-vival of owls since increasing temperature decreases energyrequirements and decreasing snow cover may improve hunt-ing success (Korpimaumlki 1986 Francis and Saurola 2004Altwegg et al 2006) However since voles play a major partin the life history of boreal owls (eg Mikkola 1983Korpimaumlki 1987a b Pietiaumlinen 1989 Hakkarainen et al2002 Francis and Saurola 2004 Table 2) changing climatemay aVect breeding of owls through alterations in populationdynamics of voles (Bierman et al 2006 Solonen 2006 Imset al 2008) This in turn is not necessarily a direct impact ofthe climate on voles but possibly through the changes in thecommunity structure of prey and predators (Hansson andHenttonen 1988 Hanski et al 1991 Korpimaumlki et al 2005)

Acknowledgments Many voluntary bird ringers and observers havetaken part in collecting the breeding and vole trapping data The RingingCentre of Finnish Museum of Natural History has maintained theelectronic ringing databases since the 1970s and kindly helped with thedata delivery A large bulk of the long-term vole data have been col-lected in the national vole monitoring program by the Finnish ForestResearch Institute we thank Asko Kaikusalo for his help We thankNigel G Yoccoz and an anonymous referee for their valuable commentsThis work was supported by grants from Jenny and Antti Wihuri Foun-dation (to AL) and Weld work in Paumlijaumlt-Haumlme was Wnanced by theAcademy of Finland (1985ndash1988 and 2000ndash2002)

References

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Altwegg R Roulin A Kestenholz M Jenni L (2006) DemographiceVects of extreme winter weather in the barn owl Oecologia14944ndash51 doi101007s00442-006-0430-3

Begon M Townsend CR Harper JL (2006) Ecology individuals pop-ulations and communities 4th edn Blackwell Boston

Bierman SM Fairbairn JP Petty SJ Elston DA Tidhar D Lambin X(2006) Changes over time in the spatiotemporal dynamics ofcyclic population of Weld voles (Microtus agrestis L) Am Nat167583ndash590 doi101086501076

Birkhead M Bacon P Walter P (1983) Factors aVecting the breedingsuccess of the mute swan Cygnus olor J Anim Ecol 52727ndash741doi1023074450

Both C Bouwhuis S Lessels CM Visser ME (2006) Climate changeand population declines in a long-distance migratory bird Nature44181ndash83 doi101038nature04539

Brinkhof MWG Caveacute AJ Hage FJ Verhulst S (1993) Timing ofreproduction and Xedging success in the coot Fulica atra evi-dence for a causal relationship J Anim Ecol 62577ndash587

Brommer JE Pietiaumlinen H Kolunen H (2002) Reproduction and sur-vival in a variable environment Ural owls (Strix uralensis) andthe three-year vole cycle Auk 119544ndash550 doi1016420004-8038(2002)119[0544RASIAV]20CO2

Brommer JE Karell P Pietiainen H (2004) Supplementary fed Uralowls increase their reproductive output with a one year time lagOecologia 139354ndash358 doi101007s00442-004-1528-0

Brommer JE Pietiaumlinen H Ahola K Karell P Karstinen T Kolunen H(2009) The return of the vole cycle in southern Finland refutes thegenerality of the loss of cycles through lsquoclimatic forcingrsquo GlobChange Biol 15 doi101111j1365-2486200902012x

Burnhamn K Anderson D (2002) Model selection and multimodelinference a practical information-theoretic approach 2nd ednSpringer New York

Charmantier A McCleery RH Cole LR Perrins C Kruuk LEBSheldon BC (2008) Adaptive phenotypic plasticity in response toclimate change in a wild bird population Science 320800ndash803doi101126science1157174

Clobert J Danchin E Dhondt AA Nichols JD (2001) DispersalOxford University Press Oxford

Cox CB Moore PD (2005) Biogegraphy An ecological and evolution-ary approach 7th edn Blackwell Boston

Cramp S (1985) The birds of the Western Palearctic vol IV OxfordUniversity Press Oxford

Daan S Tinbergen JM (1997) Adaptation of life history In Krebs JRDavies NB (eds) Behavioural ecology 4th edn Blackwell Oxfordpp 311ndash333

Drent RH Daan S (1980) The prudent parent energetic adjustments inavian breeding Ardea 68225ndash252

Dunn P (2004) Breeding dates and reproductive performance InMoslashller AP et al (eds) Advances in ecological research birds andclimate change Elsevier London pp 69ndash87

Francis CM Saurola P (2004) Estimating components of variance indemographic parameters of tawny owls Strix aluco Anim Biodi-vers Conserv 27(1)489ndash502

Hakkarainen H Korpimaumlki E Koivunen V Ydenberg R (2002) Survivalof male Tengmalmrsquos owls under temporally varying food condi-tions Oecologia 13183ndash88 doi101007s00442-001-0865-5

Halonen M Mappes T Meri T Suhonen J (2007) InXuence of snowcover on food hoarding in pygmy owls Glaucidium passerinumOrnis Fenn 84105ndash111

Hanski I Hansson L Henttonen H (1991) Specialistpredators generalistpredators and the microtine rodent cycleJ Anim Ecol 60353ndash367

Hansson L Henttonen H (1985) Gradients in density variations ofsmall rodents the importance of latitude and snow cover Oeco-logia 67394ndash402 doi101007BF00384946

Hansson L Henttonen H (1988) Rodent dynamics as community pro-cesses Trends Ecol Evol 3195ndash200 doi1010160169-5347(88)90006-7

Heikkinen RK Luoto M Virkkala R Pearson RG Koumlrber JH (2007)Biotic interactions improve predictions of boreal bird distributions

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at macro-scales Glob Ecol Biogeogr 16754ndash763 doi101111j1466-8238200700345x

Hirons GJM Hardy AR Stanley PI (1984) Body weight gonaddevelopment and moult in the tawny owl (Strix aluco) J Zool202145ndash164

Houmlrnfeldt B Eklund U (1990) The eVect of food on laying date andclutch-size in Tengmalmrsquos owl Aegolius funereus Ibis 132395ndash406

Houmlrnfeldt B Carlsson BG Loumlfgren O Eklund U (1990) EVects ofcyclic food-supply on breeding performance in Tengmalmrsquos owl(Aegolius funereus) Can J Zool 68522ndash530

Huitu O Laaksonen J Klemola T Korpimaumlki E (2008) Spatial dynam-ics of Microtus vole populations in continuous and fragmentedagricultural landscapes Oecologia 15553ndash61 doi101007s00442-007-0885-x

Ims RA Henden J-A Killengreen ST (2008) Collapsing populationcycles Trends Ecol Evol 2379ndash86 doi101016jtree200710010

Jokinen M (1975) Lehtopoumllloumlpoikasten kasvu ja energiankaumlyttouml ja ni-iden vaikutus pesimaumltuloksen maumlaumlrittaumlmiseen MSc thesisUniversity of Turku

Joumlnsson KI (1997) Capital and income breeding as alternative tacticsof resource use in reproduction Oikos 7857ndash66 doi1023073545800

Karell P (2007) Short- and long-term consequences of food resourceson Ural owl Strix uralensis reproduction PhD thesis Universityof Helsinki

Karell P Kontiainen P Pietiaumlinen H Siitari H Brommer JE (2008)Maternal eVects on oVspring Igs and eggsize in relation to naturaland experimentally improved food supply Funct Ecol 22682ndash690 doi101111j1365-2435200801425x

Korpimaumlki E (1981) On the ecology and biology of Tengmalmrsquos Owl(Aegolius funereus) in Southern Ostrabothnia and Suomenselkaumlwestern Finland Acta Universitatis Ouluensis A 118 Biol 131ndash84

Korpimaumlki E (1986) Seasonal changes in the food of Tengmalmrsquos owlAegolius funereus in western Finland Ann Zool Fenn 23339ndash344

Korpimaumlki E (1987a) Clutch size breeding success and brood sizeexperiments in Tengmalmrsquos owl Aegolius funereus a test ofhypotheses Ornis Scan 18277ndash284

Korpimaumlki E (1987b) Timing of breeding of Tengmalmrsquos owl Aegoliusfunereus in relation to vole dynamics in western Finland Ibis12958ndash68

Korpimaumlki E (1990) Body mass of breeding Tengmalmrsquos owls Aego-lius funereus seasonal between year site and age related varia-tion Ornis Scand 21169ndash178

Korpimaumlki E Hakkarainen H (1991) Fluctuating food supply aVectsthe clutch size of Tengmalmrsquos owl independent of laying dateOecologia 85543ndash552 doi101007BF00323767

Korpimaumlki E Lagerstroumlm M Saurola P (1987) Field evidence fornomadism in Tengmalm owl Aegolius funereus Ornis Scan181ndash4

Korpimaumlki E Norrdahl K Huitu O Klemola T (2005) Predator-in-duced synchrony in population oscillations of co-existing smallmammal species Proc R Soc Lond B 272193ndash202 doi101098rspb20042860

Kruumlger O (2004) The importance of competition food habitat weath-er and phenotype for the reproduction of Buzzard Buteo buteoBird Study 51125ndash132 doi10108000063650409461344

Kullberg G (1995) Strategy of the pygmy owl while hunting avian andmammalian prey Ornis Fenn 7272ndash78

Lehikoinen A Oumlst M Kilpi M (2006) Winter climate aVects subse-quent breeding success of common eiders Glob Change Biol121355ndash1365 doi101111j1365-2486200601162x

Lehikoinen A Byholm P Ranta E Saurola P Valkama J KorpimaumlkiE Pietiaumlinen H Henttonen H (2009) Reproduction of commonbuzzard at its northern range margin under climate change Oikos118829ndash836 doi101111j1600-0706200817440x

Ludwig GX Alatalo RV Helle P Lindeacuten H Lindstroumlm J Siitari H(2006) Short- and long-term population dynamical consequencesof asymmetric climate change in black grouse Proc R Soc LondB 2732009ndash2016 doi101098rspb20063538

Martin TE (2007) Climate correlates of 20 years of trophic changes inhigh-elevation riparian system Ecology 88367ndash380 doi1018900012-9658(2007)88[367CCOYOT]20CO2

Meijer T Drent R (1999) Re-examination of the capital and incomedichotomy in breeding birds Ibis 141399ndash414 doi101111j1474-919X1999tb04409x

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dance weather and female condition on reproduction in treeswallows (Tachycineta bicolor) Auk 1221225ndash1238 doi1016420004-8038(2005)122[1225EOFAWA]20CO2

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Pihlaja T (1999) Growth of nestling Ural owls MSc thesis Universityof Helsinki

Schoumlnn S (1980) Der Sperlingkauz Die Neue Brehm-Buumlcherei Wit-tenberg-Lutherstadt

Solheim R (1984) Caching behaviour prey choice and surplus killingby pygmy owls Glaucidium passerinum during winter a func-tional response of a generalist predator Ann Zool Fenn 21301ndash308

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Web-page of ageing of owls httpwwwnicfiraquomattisj

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DOI 101007s00442-010-1730-1








Introduction










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Mean age sect SD

Mean weight (g)


Tengmalmrsquos owl

13267 (80ndash1473) 322 189 sect 43 130



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Results




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Discussion

















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References


























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DOI 101007s00442-010-1730-1








Introduction










123













Mean age sect SD

Mean weight (g)


Tengmalmrsquos owl

13267 (80ndash1473) 322 189 sect 43 130



123





Results




123






Discussion

















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123







References


























123









































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Mean age sect SD

Mean weight (g)


Tengmalmrsquos owl

13267 (80ndash1473) 322 189 sect 43 130



123





Results




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Discussion

















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References


























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Results




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Discussion

















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References


























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Discussion

















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References


























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The impact of climate and cyclic food abundance on the timing of breeding and brood size in four...

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