Resource-dependent weather effect in the reproduction of the White Ciconia ciconia

Damijan Denac1

Denac D. 2006. Resource-dependent weather effect in the reproduction of the White Stork Ciconia ciconia. Ardea 94(2): 233–240.

Weather affects the breeding success of White Stork Ciconia ciconia, but the effect has not been studied in the context of different food resources or habitat quality. The aim of this study was to determine whether the impact of weather conditions on breeding success was dependent on habitat quality. The effect of weather on reproduction was analysed in two populations that differed significantly in the availability of suitable feeding habitats. Multiple regression analyses revealed that of the weather variables analysed (average temperature and rainfall in April, May and June), rainfall in May and temperature in June explained a sig- nificant part of the variation in numbers of fledged chicks per pair, but only in the population with poorer food resources. The lack of weather influence in the population with richer food resources was tentatively explained by the larger brood sizes. More effective heat conservation in larger broods, and thus lower chick mortality during cold weather, could be the underlying mechanism for the different response to weather in the two populations.

Key words: breeding success, Ciconia ciconia, habitat quality, resource dependent weather-effect, White Stork

1National Institute of Biology, Vecv na pot 111, SI–1000 Ljubljana, Slovenia ([email protected])

INTRODUCTION optimal feeding habitats, whereas fields, especially cornfields, are suboptimal (Sackl 1987, Pinowski et The influences of food as a resource and weather al. 1991). Consequently, breeding pairs surrounded as an agent affecting the ’ distribution, migra- by optimal feeding habitats are more productive tion and reproduction are particularly well known than those breeding in suboptimal sites (Barbraud (Gill 1995, Newton 1998, Elkins 2004). Reproduc- et al. 1999, Dziewiaty 2002, Nowakowski 2003). tion success of the White Stork Ciconia ciconia is Similarly, adults and nestlings are affected by directly affected by food availability, being higher weather. Adults both during migration and winter- in peak vole years (Tryjanowski & Ku´zniak 2002), ing (Sæther et al. 2006) and after arrival on the in pairs breeding closer to rich feeding sites breeding grounds (Tryjanowski et al. 2004). Until (Tortosa et al. 2002, 2003) or in the presence of young develop thermoregulatory ability livestock, where storks have better access to the (Tortosa & Castro 2003), rainy and cold weather food resources (Tryjanowski et al. 2005). White conditions can significantly reduce breeding suc- Storks select foraging habitats according to prey cess by causing high chick mortality (Jovani & availability and accessibility (Alonso et al. 1991). Tella 2004). The effect of weather on reproduction In Europe, meadows, pastures and wetlands are of White Stork has been studied in univariate 234 ARDEA 94(2), 2006

Figure 1. The representative habitat of the White Stork population in the north-eastern part of Slovenia is composed of large, intensively used fields (left). Storks of the south-eastern population have larger areas of food-rich meadows avai- lable (right) (photos D. Denac). models only, assuming stable food resources ond, south-eastern population has been recently (Carrascal et al. 1993, Bert & Lorenzi 1999, Moritzi established and is situated in two mesoregions – et al. 2001, Jovani & Tella 2004). However, the Bela krajina and the Krsvka lowland (together effect of one environmental parameter (e.g. ambi- 658 km2), colonized by White Storks from 1975 ent temperature) may become evident only when onwards. Since then, their numbers have increas- other environmental parameters (e.g. food avail- ed, and the south-eastern population accounts for ability) affecting reproduction are also taken into 7–12% of the 1999–2004 national breeding popu- account. Recently, attempts were made to study a lation (Denac 2001, D. Denac unpubl. data). number of environmental parameters jointly in Number of chicks fledged was recorded for all multi-way models, e.g. for the Buzzard Buteo buteo nests in each year from 1999 to 2004 (see Results (Krüger 2004). So far, the influence of weather on for sample sizes in each year). Breeding success reproduction success of White Stork has not been was measured as the number of chicks fledged per studied under different food conditions. The aim breeding pair, and breeding pairs were determined of this study was to explore the impact of weather following standardised census methodology conditions on breeding success in conjunction with (Schulz 1999). Habitat quality between both popu- habitat quality. lations was compared as the size of potential feed- ing habitat within the defined survey area around each nest. The survey area was a circle with a METHODS radius 1.5 km from the nest, which is the distance from the nest covered by the majority of foraging Two White Stork populations in Slovenia were flights (Sackl 1985, Alonso et al. 1991, Dziewiaty chosen to test how the weather influences breed- 1992, Nowakowski 2003). Using GIS and the ing success under different food conditions. The Actual land use map (Ministry of Agriculture, first, north-eastern population was situated in two Forestry and Food 2002), the surface of potential geographical mesoregions – the Murska and Dravs- White Stork feeding habitats (intensive meadows, ka lowlands (together 1026 km2), both of which extensive meadows, fields) within the survey areas have been traditional White Stork breeding sites was calculated. The fields category included all for at least 100 years, with 53–62% of the land sown with annual crops or temporarily uncul- 1999–2004 national breeding population. The sec- tivated due to crop rotation, as well as vegetable Denac: RESOURCE-DEPENDENT WEATHER EFFECT 235

and flower gardens. Intensive meadows included intensive meadows) within the defined survey improved meadows that are frequently mown or areas and significantly more (P < 0.001) subopti- grazed, and the extensive meadows category mal foraging habitat (fields) than pairs in the included all land covered with natural vegetation south-eastern population (Fig. 2). Pooled for all that is grazed or mown, but not intensively. Exten- years, the south-eastern population had signifi- sive and intensive meadows were defined as opti- cantly better breeding success than the north-east- mal and fields as suboptimal foraging habitats ern population (t-test: t = –5.18, P < 0.001; (Sackl 1987, Pinowski et al. 1991; Fig. 1). The null Fig. 3). hypothesis of no difference in habitat quality between the populations was tested using one-way MANOVA, followed by the post hoc Tu key honest 6 North-eastern population significant difference (HSD) test for unequal n. South-eastern population 5 )

Daily measurements of rainfall and average 2 temperature were gained from all climatic stations 4 in each mesoregion (Murska lowland – seven sta- tions, Dravska lowland – four, Krsvka lowland – 3 three, Bela krajina – three) for the period between 2

1 April and 30 June for 1999–2004. Data from the surface area (km stations were averaged to obtain daily values char- 1 acteristic for a single mesoregion. Rainfall 0 amounts were summed and the temperatures aver- fields intensive extensive meadows meadows aged to produce characteristic values for rainfall and temperature for each month (April, May, Figure 2. White Stork breeding pairs in the south-eastern June), within each year and mesoregion. population had more optimal feeding habitats (extensive Two-way ANOVAs were used to test whether and intensive meadows) and fewer suboptimal habitats mesoregions differed in rainfall and temperature, (fields) within the survey areas than pairs from the north- introducing month and mesoregion as factors. eastern population. Box plots indicate median, 25th and Forward multiple regression analysis was used to 75th percentiles, and outliers. explain the specific contribution of independent weather variables (rainfall in April, May and June and temperature in April, May and June) to the 123 15 113 16 119 17 111 18 101 18 126 28 variability in breeding success. Analyses were car- 5 poorer population ried out separately for each population. Both pop- richer population ulations occurred in two mesoregions, and data 4 were gained for six years, thus correlations were calculated for twelve data for the population. 3

2 RESULTS 1 mean breeding success

The surface areas of potential feeding habitats dif- 0 fered significantly between the populations (one- 1999 2000 2001 2002 2003 2004 way ANOVA: F = 0.533, P < 0.001). The 3,171 Figure 3. Mean (± SD) White Stork breeding success Tu key HSD test further revealed that pairs in the (number of fledged chicks/breeding pairs) in the popula- north-eastern population had significantly less tion with poorer (north-eastern) and richer food resources (P < 0.001) optimal foraging habitat (extensive, (south-eastern). Numbers of breeding pairs are indicated. 236 ARDEA 94(2), 2006

Table 1. Partial regression coefficients (± standard error of the estimate and P-values) between weather variables and breeding success in the poorer (n = 12) and richer population (n = 12). Coefficients were only calculated for variables included in the final model. Multiple R2 (adjusted) = percentage of variance explained including all factors; R2 (adjus- ted) = percentage of variance explained by final model.

Poorer population Richer population Partial B ± SE P Partial B± SE P

Mean temperature April - 0.412 - 0.854 May - 0.073 - 0.483 June 0.095 ± 0.030 0.010 - 0.883 Rainfall April - 0.420 - 0.223 May –0.004 ± 0.001 0.014 - 0.942 June - 0.726 - 0.799 Constant 0.51 ± 0.619 Multiple R2 (adjusted) 0.693 0.057 R2 (adjusted) 0.700 none significant

Forward multiple regression revealed that two rainfall in May and coldest June the difference was of the weather variables, rainfall in May and tem- as much as 32%. This gives us an idea of the rela- peratures in June, significantly explained 70.0% of tive contribution of food supply and weather upon the reproductive variation (F2,9 = 13.85, P = the breeding success of White Stork in the study 0.002; Table 1), but only in the north-eastern years. Being in the poorer population in terms of (poorer food resources) population, even though food resources implied a reduction of around 25%, the average temperature (F3,80 = 1.394, P = and rain together with low temperature further 0.251) and rain variability (F3,80 = 0.642, P = reduced breeding success by around 7%, indicat- 0.590) did not differ significantly between the ing food as a generally more important reproduc- mesoregions. In the south-eastern population tive predictor than weather. (richer food resources) not a single weather vari- Since weather explained the reproductive vari- able explained significantly any variation in repro- ability of the poorer population only, weather ductive success (Table 1, Fig. 4). influence can be considered to be resource-depen- dent. Dawson & Bortolotti (2000) concluded simi- larly that variations in weather affected the repro- DISCUSSION duction of the American Kestrel Falco sparverius when prey abundance was above the minimum The south-eastern population was recognised as threshold necessary to support successful repro- breeding on higher quality patches (richer popula- duction. Weather may have generally reduced tion) than the north-eastern (poorer population). stork nestling numbers and growth in two ways. The richer population achieved a higher breeding First, directly, by chilling and eventually killing success, although both populations experienced chicks during prolonged cold weather and storms, equal weather variability. In the year with least and secondly, indirectly, through reduced food rainfall in May and highest June temperature the availability, either causing starvation of chicks or difference in breeding success between both popu- hampering growth and thereby making them more lations was 25%, but in the year with the heaviest susceptible to direct mortality due to chilling. The Denac: RESOURCE-DEPENDENT WEATHER EFFECT 237

3.5 richer poorer 3.0

2.5

2.0 APRIL 1.5

91011121314050100150 200 3.5

3.0

2.5

2.0 breeding success MAY 1.5

13 14 15 16 17 18 19 050100150 200 3.5

3.0

2.5

2.0 JUNE 1.5

17 18 19 20 21 22 23 24 050100150 200 mean temperature (°C) rainfall (mm)

Figure 4. Breeding success (number of fledged chicks/breeding pairs) plotted against weather variables under condi- tions of richer and poorer food resources (regression analyses for each panel and population separately). The only signi- ficant relationships (indicated by bold lines) were for the poorer population with the amount of rainfall in May and tem- perature in June. latter effect may also be important in the prenatal produce eggs and incubate mostly in April (Denac phase, as the body mass of the female determines 2001). The majority of chicks in the study area clutch size (Elkins 2004). Moreover, reduced food hatch at the beginning of May so that, by the end availability and severe weather are stress factors of the month, they are approximately 20 days old. often associated with parasite infections (Newton In this period much of chick mortality occurs 1998), which might have additionally increased (Jovani & Tella 2004) since they still do not have the mortality of the White Stork chicks. thermoregulatory ability (Tortosa & Castro 2003) In the poorer area, breeding success was corre- and suffer from stressful conditions (Jovani & Tella lated to May rainfall. In Slovenia, White Storks 2004). In the studies of Carrascal et al. (1993), 238 ARDEA 94(2), 2006

Moritzi et al. (2001), Sasvári & Hegyi (2001) and ACKNOWLEDGEMENTS Jovani & Tella (2004) May rainfall was also found to be a factor significantly lowering breeding suc- I am grateful to my friends who helped me in the field, especially D. Bombek, L. Bozv icv , F. Bracv ko, A. Hudoklin, cess, confirming this general pattern across popu- v v M. Kercek, C. Marhold, M. Premzl, J. Smole, B. Stumber- lations. ger and A. Tomazv icv . I thank D. Tome, A. Vrezec, and M. v Results of this study indicate that temperature Sisv ko for their early comments on the draft, R. Jovani, in June also influenced the breeding success of the D. Heg and an anonymous referee for their valuable com- v v v poorer population, probably due to limited food ments on the manuscript, and B. Zupancic for providing supply under cold and rainy conditions (Sackl the weather data. The study was supported by Slovenian Research Agency in the programme of financing the post- 1985, Dawson & Bortolotti 2000, Pasinelli 2001). graduate education of junior researchers. In June, nestlings already develop thermoregula- tory ability, making them less sensitive to air tem- perature (Tortosa & Redondo 1992), but at the REFERENCES cost of increased food requirements. Small mam- mals, one of the most important foods of the Alonso J.C., Alonso J.A. & Carrascal L.M. 1991. Habitat selection by foraging White Storks, Ciconia ciconia, White Stork in the Continental biogeographic during the breeding season. Can. J. Zool. 69: region (Sackl 1987, Antczak et al. 2002), are less 1957–1962. active in cold and wet weather than in warm and Antczak M., Konwerski S., Grobelny S. & Tryjanowski P. dry weather (Stokes et al. 2001). In addition, birds’ 2002. The food composition of immature and non- foraging activity is reduced under heavy rain breeding White Storks in Poland. Waterbirds 25: (Wijnandts 1984, Elkins 2004). 424–428. Barbraud C., Barbraud J.-C. & Barbraud M. 1999. Two reasons could explain why there was no Population dynamics of the White Stork Ciconia cico- effect of weather on reproductive success in the nia in western France. 141: 469–479. richer population, even though weather conditions Bert E. & Lorenzi M.C. 1999. The influence of weather did not differ between the two populations. First, conditions on the reproductive success of the White chicks become heavier sooner under better forag- Stork (Ciconia ciconia) in Piedmont/Italy. In: Schulz H. (ed) Weißstorch im Aufwind? – White Storks on ing conditions, develop homeothermy sooner, and the up? Proc. Int. Symp. on the White Stork, Hamburg thus can better withstand lower temperatures 1996: 437–442. Naturschutzbund Deutschland, Bonn. (Tortosa & Redondo 1992, Tortosa & Castro 2003) Carrascal L.M., Bautista L.M. & Lázarom E. 1993. in the richer population compared to the poorer Geographical variation in the density of the White population. Secondly, within larger broods individ- Stork Ciconia ciconia in Spain: Influence of habitat uals achieve earlier effective homeothermy primar- structure and climate. Biol. Conserv. 65: 83–87. Clark L. 1982. The development of effective homeo- ily due to inertial effects retarding heat loss thermy and endothermy by nestling starlings. Comp. (Mertens 1969, Dunn 1979, Clark 1982), as the Biochem. Physiol. 73: 253–260. broods of the richer population were larger than Dawson R.D. & Bortolotti G.R. 2000. Reproductive suc- those of the poorer one and thus were more resis- cess of American Kestrels: the role of prey abundance tant to cold and rainy weather. Moreover, White and weather. Condor 102: 814–822. Denac D. 2001. Gnezditvena biologija, fenologija in Storks isolate their nests with cow dung to min- v v razsirjenost bele storklje Ciconia ciconia v Sloveniji imise chicks’ heat loss (Tortosa & Villafuerte 1999) (Breeding biology, phenology and distribution of further indicating retarding heat loss as a very White Stork Ciconia ciconia in Slovenia). Acro- important factor in the early period of chick cephalus 22: 89–103. growth. Dunn E.H. 1979. Age of effective homeothermy in nestling Tree Swallows according to brood size. Wilson Bull. 91: 455–457. Dziewiaty K. 1992. Nahrungsökologische Untersuchungen am Weißstorch Ciconia ciconia in der Dannenberger Elbmarsch (Niedersachsen). Vogelwelt 113: 133–144. Denac: RESOURCE-DEPENDENT WEATHER EFFECT 239

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voedselomstandigheden. Om dat te onderzoeken werden werd gevonden voor de hoeveelheid neerslag in mei en twee gebieden in Slovenië – een in het noordoosten en de gemiddelde temperatuur in juni, met respectievelijk een in het zuidwesten van het land – geselecteerd die een negatief en positief effect op het broedsucces. sterk in voedselrijkdom verschilden, maar qua weersom- Kortom, de gevoeligheid voor weersomstandigheden tij- standigheden vergelijkbaar waren. Het onderzoeksgebied dens het broedseizoen kan voor naburige Ooievaar-popu- in het noordoosten (1026 km2) was relatief voedselarm, laties sterk verschillen afhankelijk van de voedselrijkdom het gebied in het zuidwesten (658 km2) zeer voedselrijk. van het gebied. Gesuggereerd wordt dat de gevonden Gedurende vijf jaren werd in de twee gebieden het broed- verschillen in broedsucces tussen de gebieden veroor- succes (gedefinieerd als het aantal uitgevlogen jongen zaakt kunnen zijn door (1) een direct voedseleffect (meer per broedpaar) van de Ooievaars vastgesteld. Ondanks voedsel betekent een snellere groei van de jongen met de grote verschillen in weersomstandigheden tussen de een hogere overlevingskans), en (2) de thermoregulatie jaren bleek het broedsucces in het voedselrijke gebied in het nest (de grotere broedsels in voedselrijke gebieden geen verband te vertonen met de gemeten weersvariabe- zouden minder last van kou en regen hebben doordat de len (omgevingstemperatuur en de hoeveelheid neerslag jongen elkaar beter warm houden). (DH) gedurende het broedseizoen). Het voedselarme gebied daarentegen liet een volledig ander patroon zien: maar liefst 70% van de jaarlijkse variatie in broedsucces was te Corresponding editor: D. Heg herleiden tot verschillen in het weer. De sterkste invloed Received 15 June 2006; accepted 21 September 2006