Oecologia (2010) 162:533–539

DOI 10.1007/s00442-009-1468-9

CONSERVATION ECOLOGY - ORIGINAL PAPER

Polluted environment and cold weather induce laying gaps in great tit and pied Xycatcher

Tapio Eeva · Esa Lehikoinen

Received: 2 April 2009 / Accepted: 27 August 2009 / Published online: 26 September 2009© Springer-Verlag 2009

Abstract We studied the occurrence of laying gaps infree-living populations of the pied Xycatcher, Ficedula hyp-oleuca, and the great tit, Parus major, in a pollution gradi-ent of a copper smelter in south-west Finland. Laying gapswere 2.8 times more common in F. hypoleuca than inP. major. The probability of laying gaps was highest in theheavily polluted zone and lowest in the unpolluted zone forboth bird species. Cold weather at the time of layingincreased the number of laying gaps in both species, but inP. major this eVect was most pronounced in the heavilypolluted environment. In the most heavily polluted environ-ment the laying gaps were more likely to occur near thebeginning of the laying sequence in both species. The lay-ing gap probability increased with increasing laying date inP. major but not in F. hypoleuca. We suggest that theincreased number of laying gaps in the polluted environmentresults from limited Ca availability and the interference ofheavy metals with Ca metabolism in laying females.

Keywords Air pollution · Ficedula hypoleuca · Invertebrate food · Calcium limitation · Heavy metals · Parus major

Introduction

Small passerines normally lay one egg per day (Cramp andPerrins 1993). Sometimes, however, they interrupt laying

but may continue it after one or several days (Winkel 1970;Schmidt and Hamann 1983). These interruptions are calledlaying gaps, and they have been shown to be causedby several ambient factors, such as low temperatures(Winkel 1970; Dhondt et al. 1983; Schmidt and Hamann1983; Von Haartman 1990; Yom-Tov and Wright 1993;Pulliainen et al. 1994; Lessells et al. 2002), food limitation(Bryant 1975; Nilsson and Svensson 1993), Ca deWciency(Graveland and Berends 1997; Buren and Weidinger 2003),environmental pollution (Janssens et al. 2003; Dauwe et al.2005) and social disturbance (Low 2008). The occurrenceof laying gaps may also vary along the laying sequence(Schmidt and Hamann 1983) and timing of breeding(Lessells et al. 2002). Many of these factors are likely to beinterrelated. For example, cold weather normally nega-tively aVects the food availability of insectivorous birds andenvironmental pollution may cause nutritional stress, e.g.by decreasing food or Ca availability (Eeva et al. 1997;Eeva and Lehikoinen 2004). Timing of breeding is also cru-cial for food availability in insectivorous birds, which try totime their breeding to coincide with peak food availability(e.g. Van Noordwijk et al. 1995). Several studies suggestthat the occurrence of laying gaps is not related to femaleage in wild bird populations (Dhondt et al. 1983; Schmidtand Hamann 1983; Nilsson and Svensson 1993; Low2008).

Laying gaps may be related to environmental pollutionin several ways. First, invertebrate abundance tends todecrease in heavily polluted environments (Heliövaara andVäisänen 1993). Such pollution-related food limitation hasbeen shown to occur in birds at smelter sites with highheavy metal emissions (Eeva et al. 1997). A food source ofspecial importance for laying females is Ca-rich inverte-brates such as snails, which tend to be less abundant inacidiWed and heavily polluted environments (Graveland

Communicated by Chris Whelan.

T. Eeva (&) · E. LehikoinenSection of Ecology, University of Turku, 20014 Turku, Finlande-mail: tapio.eeva@utu.fi; teeva@utu.fi

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and van der Wal 1996; Eeva and Lehikoinen 2004).Graveland and Berends (1997) showed experimentally thata Ca-deWcient diet caused laying gaps in the great tit, Parusmajor, 1–3 days after the restricted access to Ca. This andother similar studies (e.g. Buren and Weidinger 2003) showthat laying birds need to acquire extra Ca on a daily basis,and that egg shell quality and egg production quicklyrespond to Ca shortage. Some classic environmental pollu-tants, like heavy metals, are further known to interfere withCa metabolism (Goyer 1997), posing an additional stressfactor to laying birds in heavy metal-polluted areas. Finally,natural stress factors, such as cold weather, might aVect thelaying birds more severely in the polluted areas where birdsare simultaneously exposed to nutritional stress and/orpollutants.

We studied the occurrence of laying gaps in free-livingpopulations of the pied Xycatcher, Ficedula hypoleuca, andP. major in a well-known pollution gradient of a coppersmelter in south-west Finland. For this purpose we usedlong-term data on nests which we visited several times dur-ing the laying period, enabling us to assess the occurrenceof laying gaps. On the basis of earlier studies we includedin our analysis several factors which could aVect the occur-rence of laying gaps, such as pollution level, laying timeminimum temperatures, laying date and position of the gapin the laying sequence as explaining factors. Earlier studiesin our study area have shown reduced snail numbers (Eevaand Lehikoinen 2004), decreased clutch size and poor eggshell quality in F. hypoleuca, but to a lesser extent inP. major (Eeva and Lehikoinen 1995). Therefore, we alsoexpected that laying gaps might be more common inF. hypoleuca in the polluted area. Furthermore, we wereinterested in whether the occurrence of laying gaps was asso-ciated with egg shell quality, clutch size or hatching success.

Materials and methods

Study area

The data were collected in south-west Finland during along-term (1991–2008) study on the eVects of air pollutionon wild birds. We established 21 study sites, each with 40–50nest-boxes, in the pollution gradient of a copper smelter(61°20�N, 22°10�E) in three main directions (south-west,south-east and north-west), in a range of 0.5–74 km fromthe smelter (Fig. 1). Sulphuric oxides and heavy metals(e.g. As, Cd, Cu, Ni, and Pb) are common pollutants in thearea (Kiikkilä 2003). Elevated heavy metal concentrationsoccur in the soil and biota of the polluted area due to cur-rent and historical deposition, and metal contents decreaseexponentially with increasing distance from the smelter,approaching background levels at sites further than 5 km

from it (Eeva and Lehikoinen 1996; Derome and Nieminen1998). For example, heavy metal levels in diet and tissuesof F. hypoleuca and P. major nestlings are increased in thepolluted area (Eeva and Lehikoinen 2000; Eeva et al.2005). The forests in the area are dominated by Scots pine(Pinus sylvestris), which forms mixed stands with spruce(Picea abies) and birch (Betula spp.). Special attention waspaid to the selection of study areas so that they would repre-sent the same habitat type, i.e. relatively barren pine-domi-nated forests typical of the study area.

Because there are no data on heavy metal levels whichcould be directly connected to the focal nests we analyse thedata according to the distance to the pollution source. Ana-lysing the data in this way, however, is reasonable in thesense that we can also observe any indirect eVects of envi-ronmental pollution, such as those due to changed food quan-tity and quality which are shown to occur in the area (Eevaet al. 1997). The study area was divided into three zones(Fig. 1): sites closer than 2 km to the smelter are hereaftercalled “zone I”, denoting the most heavily polluted area; sites2–5 km from the smelter are called “zone II”, denotingmoderately polluted area; and sites more than 5 km from thesmelter are called “zone III”, denoting an unpolluted area.

Data on laying gaps

During the course of the long-term population follow-upthe nest-boxes were normally checked once or twice per

Fig. 1 A map of the study area showing the locations of study sites(Wlled circles) in three distance zones (separated by circles) around theheavy metal pollution source (in the middle). The four most distantsites (48, 64 and 74 km south-west from the pollution source) are notshown on the map. A cross indicates village centres

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week to determine breeding parameters such as laying date(of the Wrst egg) and clutch size. Because most of the nestswere not visited daily during the laying period the occur-rence of laying gaps was assessed for all those nests thatwere visited at least twice during the laying period. Secondand replacement nests were omitted from the data. Toexclude deserted nests from the data, only those nestswhere incubation started were used. Since our study speciesnormally lay one egg per day we deWned the laying gap asa day without laying between the Wrst and last egg in alaying sequence. As pointed out by Dhondt et al. (1983) itis usually not possible to determine if the eggs laid afterlong laying interruptions should rather be considered asreplacement clutches. Therefore, we also excluded thecases where a laying interruption took more than 10 days(5.3% in F. hypoleuca; no cases in P. major). We furtherexcluded the nests with signs of predation (e.g. mixed nestmaterial, lost eggs, etc.). In total, the data include informa-tion on the occurrence of laying gaps in 335 nests ofP. major and 320 nests of F. hypoleuca. It should be notedthat not all the observed laying interruptions may be reallaying gaps, since Ca-deWcient birds have been found tolay premature eggs outside the nest box or remove the eggswithout a shell from the nest (Graveland and Berends1997). Such cases cannot be separated from true layinggaps in our data.

Because large clutches have a wider time-window tobecome visited multiple times during the laying period thansmall clutches, we checked whether our sample of nestswas biased in relation to clutch size. We compared themedian clutch sizes between sampled nests and the rest ofthe population (F. hypoleuca, n = 3,840 nests; P. major,n = 1,421 nests). In P. major the median clutch size wasnine in both groups and in F. hypoleuca the median clutchsize was six in both groups. Therefore, our sample is notbiased as regards to the clutch size.

Egg shell quality

The quality of a bird egg shell can be visually assessed. Wechecked the full clutches for the following abnormalitiesindicative of thin egg shells: eggs with no shell, translucentshell, rough or dull shell surface, abnormally large airspace, and pigmentation disorders. These deviations,including abnormal pigmentation, have been shown to beassociated with Ca deWciency and occurrence of layinggaps (Graveland and Drent 1997; Gosler et al. 2005). Typi-cally an abnormal pigmentation pattern is obvious inP. major when pigmentation spots are spread out, and inextreme cases all the pigment particles end up at the bluntend of the eggs (Graveland and Drent 1997). Since thereare no pigmentation spots in the eggs of F. hypoleuca thiscue cannot be used in this species.

Statistics

The number of laying gap days was calculated as the num-ber of days from Wrst to last visit (hereafter “observationinterval”) during a laying period minus the number of laideggs during that period. The average observation intervalwas 3.7 days for F. hypoleuca and 5.7 days for P. major.The observation interval varies among the clutches,depending on which days the nest was visited. The propor-tions of laying gaps among the three distance zones wereanalysed with generalised linear mixed models (GLMM)by the Glimmix procedure of SAS statistical software (SASInstitute 2003). The probability of a female having a layinggap day was modelled by using the event/trial type responseand binomial error distribution of the Glimmix procedure(event = number of laying gap days; trial = observationinterval in days). Year was included in each model as arandom factor and the df were always calculated with theKenward–Roger method.

For both bird species we used pollution zone (I–III), min-imum temperature at the time of laying, laying date (of theWrst egg) and position of the observation interval in a layingsequence as independent factors. Several authors have notedthat cold temperatures produce a laying gap with a delayof 1–4 days (Winkel 1970; Schmidt and Hamann 1983;Von Haartman 1990; Yom-Tov and Wright 1993; Pulliainenet al. 1994). To take account of this lag we used the mini-mum temperature of the observation interval minus 2 days(i.e. the observation interval for temperature was sifted2 days back) as an independent factor, hereafter referred toas “minimum temperature”. Many studies also suggest thatlaying gaps are not randomly distributed over the layingsequence, as they are usually more common near the begin-ning of the sequence (Schmidt and Hamann 1983; Nilssonand Svensson 1993; Graveland and Berends 1997; Lessellset al. 2002). Since we did not visit the nests every day it wasnot possible to deWne the exact positions of laying gaps inthe sequence. However, we took into account the variationin the location of the observation interval along the layingsequence by including egg number at the beginning of theobservation interval (hereafter “position in sequence”) as anadditional independent factor in the models.

Since some of the independent factors (e.g. laying date)besides pollution level tend to be pollution dependent, weWrst tested, for both bird species, the gross diVerences inlaying gap probabilities between the pollution zones withone-way GLMM with year as a random factor. These prob-abilities are presented in Fig. 2. Next we ran the modelscontaining all the independent factors: pollution zone, tem-perature, laying date, laying date £ laying date, position insequence and all the second-order interactions with pollu-tion zone. Non-signiWcant terms (with � > 0.1) were thendropped from the models one by one, starting from the

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interactions. Final models are presented in Table 1. SigniW-cant interactions were explored with separate univariateGLMM. We further tested with one-way GLMM the rela-tionship between egg shell quality (all eggs normal vs. atleast one abnormal egg in a clutch) and laying gap probabil-ity. This variable was not included in the model containingthe pollution zone, because it is strongly dependent on thepollution level. Finally, the associations between the pro-portion of laying gaps (laying gaps/observation interval)and clutch size or hatching success (% eggs hatched) wereexplored with Spearman correlations.

Results

The probability of laying gaps varied signiWcantly amongthe pollution zones, and was highest in the heavily pollutedzone and lowest in the unpolluted zone for both bird species

(F. hypoleuca, F2,317 = 10.6, P < 0.0001; P. major,F2,332 = 13.0, P < 0.0001; Fig. 2). There was, however, nosigniWcant diVerence between zones I and II for F. hypol-euca. The zone eVect remained even after the other inde-pendent factors were introduced into the model (Table 1).In general, laying gaps were 2.8 times more common inF. hypoleuca than in P. major.

In F. hypoleuca, the laying gaps occurred more fre-quently at low temperatures, irrespective of the pollutioneVect (Table 1; Fig. 3). The probability of a laying gap alsovaried along the position in laying sequence, but thedirection of this eVect was dependent on the pollutionlevel (Table 1). While the probability of laying gaps tendedto stay constant or increase along the sequence in unpol-luted (F1,75 = 0.61, P = 0.44) and moderately polluted(F1,98 = 6.24, P = 0.014) zones, in the heavily polluted zonethe laying gaps were more common at the beginning of thesequence (F1,141 = 4.22, P = 0.042). Laying gap probabilitydid not depend on laying date in F. hypoleuca (result notshown).

In P. major, the relationship between laying gap proba-bility and temperature depended on the pollution level(Table 1). The probability of laying gaps increased at lowtemperatures in the heavily polluted zone (F1,108 = 11.3,P = 0.0011; Fig. 3), whereas there was not such an eVect inthe moderately polluted (F1,86 = 0.52, P = 0.47) or unpol-luted zone (F1,85.02 = 2.14, P = 0.15). The probability of alaying gap also varied along the position in laying sequencein this species. While the probability of laying gapsincreased along the sequence in the unpolluted zone(F1,135 = 7.56, P = 0.0068) and stayed constant in the mod-erately polluted zone (F1,86 = 0.69, P = 0.41), in the heavilypolluted zone the laying gaps were more common at thebeginning of the sequence (F1,108 = 12.6, P = 0.0006).Unlike in F. hypoleuca, the laying gap probabilityincreased with increasing laying date in P. major (Table 1).

In F. hypoleuca and P. major, abnormal eggs were foundin 6.9% (zone I, 13%; zone II, 3.0%; zone III, 0%) and

Fig. 2 Probabilities (§95% conWdence limits) of laying gaps in Ficedu-la hypoleuca (grey bars, n = 320 nests) and Parus major (white bars,n = 335 nests) in three pollution zones around a Finnish non-ferroussmelter complex. Tukey’s test for pairwise diVerence within each species(means with diVerent letters are signiWcantly diVerent at � = 0.05)

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Table 1 The eVects of independent factors on the probability of laying gaps in Ficedula hypoleuca (n = 320 nests) and Parus major (n = 335 nests)

Generalised linear mixed models, with event/trial type response, binomial error distribution and year as a random factora Minimum temperature of the observed laying interval, shifted back 2 days to take into account a delay eVect of low temperaturesb Number of eggs at the beginning of the observation interval

F. hypoleuca P. major

df �2 P df �2 P

Pollution zone 2,313 9.62 <0.0001 2,325 20.7 <0.0001

Minimum temperaturea 1,313 8.99 0.0029 1,325 4.90 0.028

Position in sequenceb 1,313 5.77 0.017 1,325 0.58 0.45

Laying date 1,325 9.16 0.0027

Zone £ temperature 2,325 4.13 0.017

Zone £ position 2,313 3.34 0.037 2,325 10.5 <0.0001

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6.3% (zone I, 5.5%; zone II, 1.1%; zone III, 2.2%) of nests,respectively (F1,653 = 0.22, P = 0.64). It should be recalledthat the data set of P. major included the information onabnormal pigmentation (3.3% of nests), a cue could not beused in F. hypoleuca. When the pigmentation criterion wasexcluded there were more abnormal eggs in F. hypoleucathan in P. major (F1,653 = 5.68, P = 0.017). In both specieslaying gaps were more common in those nests where abnor-mal egg shells were also found (F. hypoleuca, F1,318 = 47.5,P < 0.0001; P. major, F1,333 = 64.8, P < 0.0001; Fig. 4). Inboth bird species, the proportion of laying gaps was nega-tively correlated with clutch size (F. hypoleuca, r = ¡0.43,P < 0.0001, n = 320; P. major, r = ¡0.31, P < 0.0011,n = 335) and hatching success (F. hypoleuca, r = ¡0.25,P < 0.0001, n = 320; P. major, r = ¡0.26, P < 0.0001,n = 335).

Discussion

Our study showed that laying gaps occurred frequently inboth focal bird species, but were clearly more common inF. hypoleuca. Interestingly, there also seems to be a marked

diVerence in the need and ability to acquire dietary Ca dur-ing breeding between the two species. For example, thetotal amount of Ca in the egg shells of an average-sizedclutch is about 1.8 times higher in P. major than in F. hyp-oleuca, and the faecal Ca concentration of P. major nes-tlings is about 4 times higher than that of F. hypoleucanestlings (Eeva and Lehikoinen 1995; Eeva and Lehikoinen2004). Therefore, owing to its lower Ca requirements,F. hypoleuca can be considered to be better adapted tobreeding in habitats with low Ca levels (see also Graveland1996). On the other hand, this species may also have a morelimited ability to acquire extra Ca than P. major, whichmay be better able to Wnd and process hard Ca-rich materi-als like snail shells (Graveland 1996). Living on the vergeof suYcient Ca availability, F. hypoleuca, however, seemsto be more vulnerable to disturbances in Ca metabolism,like ones caused by the interference of heavy metals withCa (Eeva and Lehikoinen 2004). This is probably whyF. hypoleuca has suVered from egg shell thinning andpoorly developing bones of nestlings in the vicinity of thesmelter, whereas such eVects have been less severe inP. major (Eeva and Lehikoinen 1995). Therefore, we sug-gest that a larger number of laying gaps in F. hypoleuca isat least partly related to the lower level of Ca turnover andsimultaneous interference of heavy metals with Ca. The rel-atively common occurrence of laying gaps in F. hypoleucamight, however, also be seen as an adaptation to cope withlimited resources like food or Ca deWciency (Pulliainenet al. 1994).

Laying gaps were more common in the vicinity of thepollution source in both bird species, not just in F. hypol-euca as we expected on the basis of more severe pollution

Fig. 3 Probabilities of laying gaps in F. hypoleuca (n = 320 nests) andP. major (n = 335 nests) in relation to ambient minimum temperaturesat the time of laying in heavily polluted (Wlled circle), moderately pol-luted (triangle) and unpolluted (unWlled circle) zones around a smeltercomplex

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Fig. 4 Probabilities (§95% conWdence limits) of laying gaps in nestsof F. hypoleuca (grey bars, n = 320 nests) and P. major (white bars,n = 335 nests) with normal and abnormal (eggs with no shell, translu-cent shell, rough or dull surface, abnormally large air space, andpigmentation disorders) egg shells

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Egg shell quality

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eVects on egg shell quality in this species (Eeva andLehikoinen 1995). A strong association between egg shellquality and the occurrence of laying gaps in both speciessuggests that Ca limitation and increased heavy metal lev-els may be a common reason for the increased number oflaying gaps in the polluted area. Ca deWciency has beenexperimentally shown to cause poor-quality egg shells andlaying gaps in P. major (Graveland and Berends 1997) andFicedula albicollis (Buren and Weidinger 2003). Besideslimited Ca availability, the decreased amount of inverte-brate food may further increase the occurrence of layinggaps in the heavily polluted area (Eeva et al. 1997), thoughfood shortage as such could primarily be expected to aVectclutch size and not be directly related to egg shell quality.Clutch size has decreased in the polluted area in bothspecies (Eeva and Lehikoinen 1995), and the negative asso-ciation between the occurrence of laying gaps and clutchsize/hatching success suggests that laying gaps are indica-tive of reduced Wtness. We consider resource limitation (Caand food shortage) and interference of heavy metals withCa metabolism the most likely reasons for inferior egg shellquality, increased number of laying gaps and decreasedclutch size. The number of laying gaps also increased in aheavy metal-polluted area in Belgium, with a simultaneousdecrease in hatchability (Janssens et al. 2003). However,clutch size and egg shell quality were not decreased inJanssens et al.’s (2003) study, perhaps due to a higheravailability of Ca and food in relatively luxuriant deciduousforests of their study area as compared to the more barrenpine forests of our area. We also found that laying gapsincreased along with increasing laying date in P. major.This relationship could mean that individuals experiencingproblems with Ca availability are also forced to postponethe start of laying, though such laying “gaps” before theWrst egg cannot be assessed from our data. On average,however, P. major starts laying earlier in the polluted area,probably due to more advanced phenology in the pollutedenvironment (Eeva et al. 2009).

Our study conWrmed the earlier Wndings that cold weatherat the time of laying induces laying gaps in P. major andF. hypoleuca. However, in P. major this eVect was mostpronounced in the heavily polluted environment. The resultsuggests that environmental pollution can make birds moresusceptible to natural stress factors such as cold weather.Cold temperatures are likely to decrease the availability ofinvertebrates, and possibly also the time that birds can useto acquire extra Ca for the eggs because laying females donot get enough Ca from their normal invertebrate foodbut need to acquire speciWc Ca-rich food items like snailshells (Graveland and van Gijzen 1994), sometimes from farbeyond their territory (Wilkin et al. 2009). Experimentalstudies in blue tits, Cyanistes caeruleus, however, suggestthat low temperatures may increase the number of laying

gaps irrespective of food availability, and vice versa.Yom-Tov and Wright (1993) showed that the number oflaying gaps decreased in C. caeruleus when the temperatureof nest-boxes was artiWcially raised, indicating that low tem-perature may aVect the occurrence of laying gaps without anassociated change in food availability. On the other hand,the food-manipulation experiment of Nilsson and Svensson(1993) suggested that in C. caeruleus there is a direct causalrelationship between food shortage and the occurrence oflaying gaps, irrespective of temperature. In our study therelationship between the number of P. major laying gapsand temperature varied spatially, suggesting that the eVect oftemperature depended on resource availability.

Several studies have shown that laying gaps tend tooccur more frequently at the beginning of the layingsequence than later (Schmidt and Hamann 1983; Nilssonand Svensson 1993), whereas some studies have found theopposite pattern (Lessells et al. 2002). In our study thisrelationship varied spatially. One possible reason forgreater laying gap frequencies at the beginning of thesequence might be a greater need for Ca during the Wrstdays of laying than later (Graveland and Berends 1997).We found that in both bird species laying gaps were morelikely to occur near the beginning of the sequence in themost heavily polluted environment, while there was a posi-tive or no relationship in the less polluted areas. We suggestthat laying gaps tend to occur near the beginning of thesequence especially when Ca availability is limited,because the need for Ca is greatest at that point. Since theCa availability is most limited in the polluted area andincreased heavy metal levels further disturb Ca metabolism,the laying gaps there occur more frequently at the begin-ning of the sequence than in less polluted areas. The depen-dence of the relationship between the occurrence of layinggaps and position in sequence on Ca availability might alsoexplain why diVerent studies have shown diVerent patterns.

Acknowledgments We thank Jorma Nurmi and all the other peopleinvolved in the Weld work over the years. Our study was Wnanced by theAcademy of Finland (project 8119367) and Finnish Cultural Foundation.

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