Factors determining the occurrence of anthropogenic materials in nests of the white stork Ciconia ciconia

Factors determining the occurrence of anthropogenic materials in nests of the white stork Ciconia... Birds have been using anthropogenic materials for nest construction for the past few decades. However, there is a trade-off between the use of new nesting material, which is often linked to greater breeding success, and the higher risk of nestling mortality due to entanglement or ingestion of debris. Here, we investigate the incorporation of anthropogenic materials into nests of the white stork Ciconia ciconia, based on a long-term study of a population in Western Poland. We recorded at least one item of debris in 50 and 42% of nests at the egg and nestling stages, respectively. More debris was found in nests located in territories with higher number of anthropogenic material in the surrounding environment. We found a relationship between the age of females, the number of debris in the area surrounding a nest, and the number of debris in the nest. We found no significant effect of the total number of debris in nests on clutch size, number of fledglings, or breeding success. Studies on the influence of the age and sex of individuals in understanding this behaviour and its drivers in bird populations should be continued. . . . Keywords Nest-building behaviour Breeding success Debris Pollution Introduction padding of nests. Birds of different taxa are well known for incorporating anthropogenic materials into nests (Morin and Human activities induce significant changes in the natural Conant 1990; Huin and Croxall 1996;Blemetal. 2002; environment, which lead in turn to changes in the behaviour Hartwig et al. 2007; Townsend and Barker 2014). This behav- of animals living in urban environments (Carney and iour may be influenced by the abundance and availability of Sydeman 1999; Slabbekoorn and den Boer-Visser 2006; debris in marine, urban, and agricultural environments Miranda 2017). Increases in solid waste abundance as a result (Henriksen 2000;Wanget al. 2009;Bond et al. 2012, 2013; of the growth of urbanisation (Hoornweg et al. 2013)have Eriksen et al. 2014; Wilcox et al. 2015). Due to environmental made anthropogenic materials commonly available in terres- changes (e.g. large-scale modern farming, the development, or trial and marine environments. Debris, mainly in the marine spread of urbanisation), natural elements (e.g. wooden sticks, environment, is a cause of mortality in many animals straw, hay) may be scarce. Hence, incorporating easily avail- (Gregory 2009;Ryanet al. 2009;Votieret al. 2011). able debris can potentially reduce the costs of collecting nat- However, it is also used as material for the construction or ural material, especially when the debris is light and durable, e.g. plastic string (Antczak et al. 2010) or plastic foil. A study Responsible editor: Philippe Garrigues of the black-faced spoonbill Platalea minor showed that, in a highly polluted and changed environment, supplying natural Electronic supplementary material The online version of this article (https://doi.org/10.1007/s11356-018-1626-x) contains supplementary elements led to a reduction in the number of debris incorpo- material, which is available to authorized users. rated into nests (Lee et al. 2015). Collection of debris may be modified by several other factors. In terrestrial species, the * Marcin Tobolka number of anthropogenic materials used to construct the nest tobolkamarcin@gmail.com can be correlated with the level of urbanisation (Wang et al. 1 2009; Radhamany et al. 2016). However, the use of anthropo- Institute of Zoology, Poznań University of Life Sciences, Wojska genic materials in nests may also be triggered by mating be- Polskiego 71C, 60-625 Poznań, Poland 2 haviour, e.g. bowerbirds (Ptilonorhynchidae) build bowers to Department of Zoology and Physical Anthropology, Complutense attract females (Borgia 1985). Bower decoration can be a University of Madrid, Jose Antonio Novais, 12, 28040 Madrid, Spain Environ Sci Pollut Res (2018) 25:14726–14733 14727 decisive factor for females choosing a mate. Bowerbirds dec- Europe, white storks often forage in rubbish dumps, a practice orate bowers with flowers, plants, and debris—bottle tops, which has probably driven the population increase (Tortosa straws, etc. (Borgia 1985). Males with better decorated bowers et al. 2002). This species is known to incorporate debris from are more attractive and have better chances for reproduction; rubbish dumps in their nests (Henry et al. 2011). Eastern (in- this may ultimately increase the number of anthropogenic ma- cluding Polish) white stork populations rarely use rubbish terial in bowers. Incorporation of debris may be also depen- dumps (Kruszyk and Ciach 2010); instead, debris from the dent on the age (experience) of individual birds (Coleman immediate environment (e.g. plastic strings, foil) is collected et al. 2004). In black kites Milvus migrans, the number of from agricultural lands as nesting material and incorporated anthropogenic material in nests is related to the age of pair into nests (Tryjanowski et al. 2006). Plastic string is one of the members; it is also strongly linked to individual quality and most common anthropogenic materials used by terrestrial spe- therefore has a strong influence on breeding success. Higher- cies as nesting material (Antczak et al. 2010; Seacor et al. quality individuals collect more debris, are better breeders, 2014). This material has been commonly used in Polish agri- and occupy better territories (Sergio et al. 2011). What is culture since 1982 for tying, e.g. hay and straw (Ptaszyk more, nest decoration can signal the condition, experience, 1994). Due to its utility, fragments are ubiquitous in the agri- fighting capabilities, territory quality, and social dominance cultural landscape. It is available to foraging birds, along with of the individual or the breeding pair to other individuals plastic foil, which is used in farmlands to cover, e.g. hay bales (Canal et al. 2016). or certain types of crops. These materials are the main sources The use of anthropogenic materials may also have negative of plastic pollution in farmlands. Moreover, the white stork is consequences. Plastic string, fishing nets, and angling gear are characterised by its longevity, and thus studies on the impact resistant materials occurring in the sea (far from nest sites) as of age on nesting behaviour are feasible. This makes the white well in the nest (collected by adults). These items often cause stork a suitable subject for detailed research on the impact of entanglement, leading to mortality or injuries (Baker et al. anthropogenic material on nesting behaviour. We investigated 2002; Seacor et al. 2014). Entanglement has been recorded two factors which may influence the inclusion of debris in in 25% of 312 studied seabird species (Gall and Thompson nests: the availability of debris in the vicinity of nests 2015). Hence, birds collecting debris for their nests may in- (Henriksen 2000; Wang et al. 2009;Bond et al. 2012)and crease the risk of ingestion and entanglement, which may the age of individuals (Sergio et al. 2011; Canal et al. 2016). reduce breeding success (Mee et al. 2007). While this phe- With regard to age-assortative mating in white storks, we nomenon has been studied in marine birds (Provencher et al. know that the ages of both breeders constituting a pair are very 2017), it is rarely described in the cases of land birds and similar (in cases where the age of only one pair member is inland waterbirds. Other debris, e.g. cigarette butts, may have known) (Barbraud and Barbraud 1999). Hence, we an initial positive effect, i.e. may act as an ectoparasite repel- hypothesised that (1) the greater the density of anthropogenic lent (Suárez-Rodríguez et al. 2012). However, long-term ob- materials in the environment in the vicinity of the nest, the servations showed the cost of exposure to toxins, namely, a higher the number of anthropogenic materials incorporated higher genotoxicity level (damage to DNA or chromosomal into the nest, associated with the question of whether there is material) in nestlings’ blood cells (Suárez-Rodríguez and any preference for a particular type of debris; (2) the ages of Macías Garcia 2014). Ingestion of anthropogenic material, individuals have a direct impact on the number of anthropo- which may also occur in nests, is another cost associated with genic material included in the nest; and (3) birds incorporating individual survival (Houston et al. 2007; Mee et al. 2007; the greatest number of debris (pieces) into nests are not only Young et al. 2009; Henry et al. 2011; Finkelstein et al. 2012). older but also better breeders, as reflected in greater numbers In this study, we examine the impact of the incorporation of of eggs and fledglings. The incorporation of debris into nests anthropogenic materials into nests of a large migratory in agricultural landscapes has been shown in only a few stud- synanthropic water bird, the white stork Ciconia ciconia. ies (e.g. Antczak et al. 2010; Townsend and Barker 2014). Traditionally, this bird bred in colonies in river valleys but This is the first long-term research to explain the effect of has now moved closer to human settlements. Nowadays, it debris on a bird inhabiting farmlands, i.e. the white stork. is a common species which breeds and forages in agricultural areas and nests close to human settlements (Schulz 1998). At the same time, it is a well-studied bird species, with popula- Materials and methods tions being monitored over the long term (Bairlein 1991). The population has declined in Western Europe due to the intensi- Fieldwork fication of agriculture and to drought in the Sahel, where it winters. Following a precipitate decline, the population has We conducted the study in Western Poland near the town of recovered due to reintroduction and additional feeding Leszno (51°51′ N, 16°35′ E), within a mainly rural area of programmes in several countries (Bairlein 1991). In Western 4154 km comprising arable fields (54%), forests (17%), 14728 Environ Sci Pollut Res (2018) 25:14726–14733 human settlements (10%), a small proportion of meadows properties and to Townsend and Barker (2014), into catego- (7%) and pastures (< 1%), and other land-use types (12%) ries: foil, plastic string, other plastic, paper, textiles and other. (Tobolka et al. 2015). Additionally, we divided nest debris using a standardised First, we used data collected during a long-term study of the method (Provencher et al. 2017) in order to facilitate compar- white stork’s breeding and population ecology, which com- ison with future studies. Finally, we recorded breeding success prised ca 50 nests visited each year between 2009 and 2016 by counting fledglings, i.e. chicks over 50 days of age standing for recording clutch size, over 100 nests where the number of in the nest and considered able to fly (a standard method to fledglings was recorded during ringing, and over 300 nests estimate the breeding success of the white stork) (Tryjanowski where breeding results were recorded (for details, see et al. 2006). Breeding success was defined as the number of Tobolka et al. 2013, 2015). The data were collected for 342 fledglings divided by the number of eggs laid. broods at the egg stage and 445 broods at the chick stage during the years 2009–16; during this period, all anthropogen- Statistical analyses ic materials in the nests were counted (details in supplementary material, Table S1). To decrease the risk of nestling entangle- Prior to statistical analyses, we used the fitdistrplus package ment and avoid accumulation of recorded debris during sub- (Delignette-Muller and Dutang 2015) to check the distribution sequent visits, we removed all debris from the nest during each of dependent variables. To test the effect of the number of visit. Second, we searched for adults of known age and sex debris in the environment on the number of debris in white with alphanumeric rings (sexed by molecular procedures; see stork nests, we used a generalised linear mixed model details in Dubiec and Zagalska-Neubauer 2006; Fernandes (GLMM) with a Poisson error structure and a log link func- et al. 2006).White storks are marked mainly as nestlings; tion; specifically, we used a GLMM with a binomial error hence, we knew the exact age of adults that had been ringed structure with a logit link function to explain the effect of several years earlier and re-recorded during this study. Marked age and sex on the presence of debris in nests. As a binomial breeders of known age and sex can help to explain the possible response variable, we compared nests with debris (1) to nests impact of age and sex on debris-collecting behaviour and pa- without debris (0). We used GLMM to model variations in rental care. Additionally, we conducted more complex field clutch size, numbers of chicks, and breeding success. For each research during the 2015 breeding season. We conducted two dependent variable, we used a GLMM with a Gaussian error visits: during egg-laying (32 broods) and chick-rearing pe- structure and an identity link function with one fixed-effect riods, the latter amounting to 43 broods between 25 and predictor: total number of debris. In these GLMMs, we used 45 days of age. We visited accessible nests (the same included nest identity and year as random factors. To test the white in the long-term study) with a 7-m ladder, cherry-picker, and stork’s preference for particular types of debris (plastic string, climbing equipment. In the course of nest visits, we collected foil, paper or other), we used chi-square contingency indepen- data on clutch size and number of nestlings, and recorded all dence tests comparing the percentage of debris between white anthropogenic materials present in nests. Clutch size was re- stork nests and the environment for two stages (egg and corded during the second half of incubation (between the 15th chick). We analysed separately the number of debris during and 30th days) (details in Tobolka et al. 2015). The number of the egg and nestling stages because the availability of anthro- nestlings was recorded at the time nestlings were marked. We pogenic material might change due to growth of vegetation established a buffer area with a radius of 500 m around a nest, and intensification of agricultural works (e.g. hay collecting in which we created four random transects 150 m long. The and harvesting) during the breeding season proceeding. All width of each transect was 2 m on either side, or 4 m in analyses were performed in R, version 3.3.2 (R aggregate, at the beginning of the breeding season (egg stage), Development Core Team 2016), using the lme4 (Bates et al. and 1 m on either side (2 m in aggregate) during the nestling 2015) and ggplot2 (Wickham 2009) packages. stage due to the lower level of visibility caused by vegetation growth; however, dimensions were the same for each transect. The foraging range of the white stork is characterised by a Results radius up to 2 km (Ożgo and Bogucki 1999); however, the stork collects nesting material in the immediate vicinity of In the course of the study (2009–16), in 171 of 342 (50%) the nest, accordingly to personal observations (Tobółka, un- broods during egg stage and in 186 of 445 (42%) broods published). We counted all available potential anthropogenic during chick stage, anthropogenic materials were present. nest materials lying on the ground (Fig. S1). We recorded only The anthropogenic materials categories occurred in the fol- anthropogenic materials with dimensions over 1 cm in diame- lowing proportion: plastic string (38%), foil (33%), textile ter and easily detectable by human eyes (e.g. plastic string, (8%), paper (5%), other plastic (7%) and other (9%). In the foil, paper and other material). Later, we divided debris from surrounding area, the proportion of available debris was as white stork nests and transects, according to physical follows: plastic string (83%), foil (8%), textile (0.3%), paper Environ Sci Pollut Res (2018) 25:14726–14733 14729 (2%), other plastic (3%) and other (3%). The white stork at the chick stage revealed a positive preference for plastic foil (chi- square = 5.828, p = 0.02) and a negative preference regarding string (chi-square = 24.858, p < 0.001). However, during the egg stage, these relationships were not significant (Table 1). More debris was found in nests located in territories with higher rates of anthropogenic material in the surrounding en- vironment (β = 0.02075 ± 0.01351, Z =2.006, p =0.0453, N = 75).We found that probability of recording debris in a given nest was positively correlated with the age of the female (β = 0.9147 ± 0.385, Z =2.377, p =0.018, N = 33, Fig. 1). The age of the male did not explain the probability of recording debris in the nest (β = − 0.2638 ± 0.320, Z = − 0.824, p = 0.410, N =20). We found no significant effect of the total number of debris in a given nest on clutch size (p = 0.423, Table 2), number of fledglings (p = 0.956), or breeding success (p =0.106). Fig. 1 The probability of the presence of debris in nests in relation to the Discussion ages of white stork females In this study, we showed that 46% of white stork nests probable reason for incorporating anthropogenic materials in- contained anthropogenic material. The relationship between to the nest structure is that these materials are common and the numbers of debris in the vicinity of a nest and in the nest easily accessible in the agricultural landscape, which we have itself was significant. Thus, the white stork, as well as marine shown in the case of the white stork. At the moment, we do not birds, may be a potential indicator of debris pollution in the know why white storks prefer to collect foil and plastic, but surrounding environment, as incorporation of debris in nests the preference was shown only during chick stage. During egg may be related to its availability in the environment around stage, there was no preference, and probably white storks those nests (Votier et al. 2011; Avery-Gomm et al. 2012; Bond randomly use what is available in the local environment. et al. 2012). In many aspects of life, the white stork demon- Maybe the former are better insulation materials; however, strates its opportunism and ability to adapt to changing envi- more detailed studies, including experiments, are needed to ronments, e.g. its exploitation of a wide range of new food confirm this statement. Additionally, older individuals collect resources (Tortosa et al. 2002; Djerdali et al. 2008, 2016; these materials to a greater extent in the vicinity of the nest. Ciach and Kruszyk 2010; Gilbert et al. 2016), its use of new White storks may select debris in relation to its abundance, as nesting sites, and its tendency to nest close to human settle- the amount of plastic in the landscape increases (Thompson ments (Tryjanowski et al. 2009; Flack et al. 2016); the use of et al. 2009). Given that natural materials are probably limited debris as a lining material is another example. The most in an intensive agricultural landscape (Antczak et al. 2010), the use of anthropogenic nest material may be a beneficial Table 1 Results of a chi-square contingency independence test for white stork preferences for debris type Nest (%) Environment (%) Chi-square P Table 2 The GLMM’s with Gaussian error describing the relationship between clutch size (n = 342 broods), number of fledglings (n = 445 Egg stage broods) and breeding success (n = 196 broods) to total number of debris in nest String 55 76 3.366 0.07 Foil 10 13 0.391 0.53 Effect Estimate Error tP Paper 0 2 –– Other 35 9 15.364 < 0.001 Clutch size Chick stage No debris in nest 0.513 0.191 0.802 0.423 String 30 83 24.858 < 0.001 No of fledglings Foil 21 8 5.828 0.02 No debris in nest 4.168e-03 7.499e-02 0.056 0.956 Paper 11 2 6.231 0.01 Breeding success Other 38 7 21.356 < 0.001 No debris in nest 0.031 0.019 1.624 0.106 14730 Environ Sci Pollut Res (2018) 25:14726–14733 resource in nest construction. Our research showed that the 39 years of age (Schulz 1998). Therefore, records in subse- most common items of debris in the immediate vicinity of quent years may provide additional data which will render the white stork nests that were incorporated in nests were plastic character of the relationship more similar to that observed by string and foil. These anthropogenic materials were also most Sergio et al. (2011). common in nests of the American crow Corvus We found no significant relationships between total number brachyrhynchos (Townsend and Barker 2014)and thegreat of debris collected for nests and clutch size, number of fledg- grey shrike (Lanius excubitor)(Antczak et al. 2010)inagri- lings, or final breeding success. Assuming that the number of cultural landscapes. debris collected for the nest is a proxy for experience, we may In our study, the probability of the presence of debris in have observed its effect only on breeding success. Egg counts nests was associated with the age of females. However, we did alone do not explain the impact of debris collection because in not find a relationship between the probability of the presence particular cases, young, inexperienced white stork females may of debris in the nest and the age of male white storks. In this lay more eggs compared to older individuals (Aguirre and species, both partners collect nesting material, but we do not Vergara 2007). What is more, clutch size is related to current know whether bringing debris into the nest is a sex-dependent food supply (Tortosa et al. 2003) and to conditions in the win- activity. One local study suggests that males deliver more tering grounds during the previous winter (Schamber et al. nesting material, particularly in the beginning of the breeding 2012; Tobolka et al. in review). Although numbers of collected season (Bocheński and Jerzak 2006); however, we have no debris may be an indicator of innovative behaviour (Borgia knowledge of a more general pattern. In regard to age- 1985) and the age-related experience (Sergio et al. 2011)ofpair assortative mating in this species (Barbraud and Barbraud members,which may bereflected alsoin food provisioning, the 1999; Ferrer and Penteriani 2003), we can assume that the influence ofdebris ondevelopingnestlingsisnot equal.Several ages of white stork males were similar to those of their female typesofdebrismayproducenegativeconsequences,e.g.plastic partners. The lack of a significant relationship may be a result string which may cause entanglement (Antczak et al. 2010), of the small sample size of males (N = 20) of known age. Mate rubber elements, plastic tape or string which may cause stran- choice in the white stork is mostly dependent on nest site gulation (Henry et al. 2011), or wire and other metal elements occupancy. White storks prefer breeding sites with large nests which may cause injuries. Along with the common occurrence or a nest that has been occupied continuously for at least one of the incorporation of anthropogenic materials into nest struc- successful breeding season (Bocheński and Jerzak 2006; tures, only a few cases of entanglement were noticed. During Vergara et al. 2010). Storks collect and deliver debris to the 8 years of studies, 0.73% of 2043 nestlings (from 728 nests) middle part of the nest as a lining, whereas we recorded only were found entangled (11 dead, 4 with fatal injuries necessitat- debris in upper parts, which reflects collecting behaviour dur- ing euthanasia) and two cases of strangulation with plastic ele- ing the current breeding season; therefore, the age and size of a ments choked in nestling throats (Tobolka, unpublished data) nest should not influence the number of debris recorded there- during the ringing process. Hence, we recorded lethal conse- in within a single breeding season. Some bird studies have quences of collecting debris in only 2% of nests. However, the shown a relationship between anthropogenic materials incor- number of entangled nestlings may have been higher, as we did porated into nests by mates and pair formation (Coleman et al. not detect mortality in earlier stages. In this study, nests were 2004; Sergio et al. 2011). In this study, numbers of debris were visited when chicks were old enough to ring, in age of 25– positively correlated only with the ages of females. Sergio 40 days. White stork nestlings spend ca 55 days in the nest, et al. (2011) showed that numbers of debris in nests of black and their mortality varies from 21 to 85%, which is mainly kites were greatest for birds aged 8–11 years, whereas in youn- due to varying weather conditions (Tobolka et al. 2015); entan- ger and older individuals, this phenomenon was significantly glementmaybeanotherthreat.Thissituationwasalsoobserved less frequent. The probable explanation is that the experience intheAmericancrowinfarmlands,where5.6%of195nestlings (better quality) of the individual is age-related, although pos- were entangled in their nests (Townsend and Barker 2010). sibly, it exhibits an inverted U-pattern (Ortega et al. 2017). Environmental pollution with anthropogenic materials has The white stork also reveals this pattern, i.e. individuals aged been present only for the past several decades; therefore, incor- between 8 and 12 years are the best breeders (Profus 2006). In poration of debris in nests by birds is a relatively new behaviour our study, the relationship had a different character, being non- (Ptaszyk 1994). There are many reports of the incorporation of linear as well; nevertheless, the probability of incorporating debris into nests by various bird species (e.g. marine colonial debris into the nest increased continuously with a stork’sage. birds) (Votier et al. 2011; Verlis et al. 2014; Tavares et al. 2016), Experience comes with age, therefore, more experienced birds although the scale of this behaviour is still not known in detail. may be more likely to incorporate debris into their nests, ac- The white stork appears to be a species in which the phenome- cording to results published by Sergio et al. (2011). non is currently developing, at least in Poland. It may be worth Irrespective of this, the oldest female in our study was 10 years monitoring whether debris incorporation into nests becomes old, whereas the white stork can live much longer, even up to more widespread and exerts an impact on individuals and Environ Sci Pollut Res (2018) 25:14726–14733 14731 Baker GB, Gales R, Hamilton S, Wilkinson V (2002) Albatrosses and populations in future. However, the abundance of plastic string petrels in Australia: a review of their conservation and management. in the agricultural environment and its non-biodegradability (it Emu 102:71–97. https://doi.org/10.1071/MU01036 only breaks into smaller and smaller fragments) make it neces- Barbraud C, Barbraud JC (1999) Is there age assortative mating in the sary to constantly monitor the scale of entanglement and inges- European white stork? Waterbirds 22:478–481. https://doi.org/10. 2307/1522129 tion. Moreover, this behaviour may be widespread and may Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed- have an impact on more individuals/populations in the future effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10. (e.g. Antczak et al. 2010). 18637/jss.v067.i01 Blem CR, Blem LB, Harmata PJ (2002) Twine causes significant mortal- ity in nestlings ospreys. Wilson Bull 114:528–529. https://doi.org/ 10.1676/00435643(2002)114[0528:TCSMIN]2.0.CO;2 Conclusions Bocheński M, Jerzak L (2006) Behaviour of the white stork (Ciconia ciconia): a review. Bogucki Wydawnictwo Naukowe, Poznań Bond AL, Montevecchi WA, Guse N, Regular PM, Garthe S, Rail JF Considering all aspects, the white stork adapts easily to an- (2012) Prevalence and composition of fishing gear debris in the thropogenic changes and can use new nesting material avail- nests of northern gannets (Morus bassanus) are related to fishing able in the environment. In order to define the long-term con- effort. Mar Pollut Bull 64:907–911. https://doi.org/10.1016/j. marpolbul.2012.03.011 sequences (i.e. costs of incorporating debris) and individual Bond AL, Provencher JF, Elliot RD, Ryan PC, Rowe S, Jones IL, conditions for incorporating anthropogenic materials into Robertson GJ, Wilhelm SI (2013) Ingestion of plastic marine debris nests, this behaviour should be continuously monitored, and by common and thick-billed murres in the northwestern Atlantic more studies should be performed to understand this phenom- from 1985 to 2012. Mar Pollut Bullet 77:192–195. https://doi.org/ 10.1016/j.marpolbul.2013.10.005 enon better. Using more detailed methods (e.g. trapping cam- Borgia G (1985) Bowers quality, number of decorations and mating suc- eras) will help us to identify the exact pattern of collecting cess of male satin bowerbirds (Ptilonorhynchus violaceus): an ex- debris for nests, as well as to determine which sex is primarily perimental analysis. Anim Behav 33:266–271. https://doi.org/10. responsible for debris collection and when such incorporation 1016/S0003-3472(85)80140-8 takes place. Also, in this case, research on the impact of the Canal D, Mulero-Pázmány M, Negro JJ, Sergio F (2016) Decoration increases the conspicuousness of raptor nests. PLoS One 11: age of individuals on this behaviour should be continued. e0157440. https://doi.org/10.1371/journal.pone.0157440 Carney KM, Sydeman WJ (1999) A review of human disturbance effects Acknowledgements We are grateful to Nathalie Gilbert for assistance on nesting colonial waterbirds. Waterbirds 22:68–79. https://doi.org/ with English language editing and Jose I. Aguirre for critical comments 10.2307/1521995 on an earlier version of the manuscript. The study was funded by the Ciach M, Kruszyk R (2010) Foraging of white storks Ciconia ciconia on National Science Centre (MT) as part of the projects N/NZ8/01186 and rubbish dumps on non-breeding grounds. Waterbirds 33:101–104. T/NZ8/01001. In 2010/11 and 2013/14, MT was a scholarship holder https://doi.org/10.1675/063.033.0112 within a project co-financed by the European Social Fund. Coleman SE, Patricelli GA, Borgia G (2004) Variable females prefer- ences drive complex male displays. Nature 428:742–745. https:// doi.org/10.1038/nature02419 Open Access This article is distributed under the terms of the Creative Delignette-Muller ML, Dutang C (2015) Fitdistrplus: an R package for Commons Attribution 4.0 International License (http:// fitting distributions. J Stat Softw 64:1–34. https://doi.org/10.18637/ creativecommons.org/licenses/by/4.0/), which permits unrestricted use, jss.v064.i04 distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link Djerdali S, Tortosa FS, Hillstrom L, Doumandji S (2008) Food supply to the Creative Commons license, and indicate if changes were made. and external cues limit the clutch size and hatchability in the white stork Ciconia ciconia. Acta Ornithol 43:145–150. https://doi.org/10. 3161/000164508X395252 Djerdali S, Guerrero-Casado J, Tortosa FS (2016) The effects of colony size interacting with extra food supply on the breeding success of the References white stork (Ciconia ciconia). J Ornithol 157:941–947. https://doi. org/10.1007/s10336-016-1343-5 Aguirre JM, Vergara P (2007) Younger, weaker white stork (Ciconia Dubiec A, Zagalska-Neubauer M (2006) Molecular techniques for sex ciconia) became the best breeders. Evol Ecol Res 9:355–364 identification in birds. Biol Lett 43:3–12 Antczak M, Hromada M, Czechowski P, Tabor J, Zabłocki P, Grzybek J, Eriksen M, Lebreton LCM, Carson HS, Thiel M, Moore CJ, Borerro JC, Tryjanowski P (2010) A new material for old solutions—the case of Galgani F, Ryan PG, Reisser J (2014) Plastic pollution in the world’s plastic string used in great grey shrike nests. Acta Ethol 13:87–91. oceans: more than 5 trillion plastic pieces weighing over 250,000 https://doi.org/10.1007/s10211-010-0077-2 tons afloat at sea. PLoS One 9:e111913. https://doi.org/10.1371/ journal.pone.0111913 Avery-Gomm S, O’Hara PD, Kleine L, Bowes V, Wilson LK, Barry KL (2012) Northern fulmars as biological monitors of trends of plastic Fernandes M, Borges C, Simoes F, Caballero JM, Pacheco C, Franco C pollution in the eastern North Pacific. Mar Pollut Bull 64:1776– (2006) Molecular sexing of the black stork Ciconia nigra:sex ratios 1781. https://doi.org/10.1016/j.marpolbul.2012.04.017 in the Portuguese population. Biota 7:31–36 Ferrer M, Penteriani V (2003) A process of pair formation leading to Bairlein F (1991) Population studies of white stork (Ciconia ciconia)in Europe. In: Perrins CM, Lebreton JD, Hirons GJM (eds) Bird pop- assortative mating: passive age-assortative mating by habitat hetero- geneity. Anim Behav 66:137–143. https://doi.org/10.1006/anbe. ulation studies: relevance to conservation and management. Oxford University Press, Oxford, pp 207–229 2003.2158 14732 Environ Sci Pollut Res (2018) 25:14726–14733 Finkelstein ME, Doak DF, George D, Burnett J, Brandt J, Grantham J, the up? Proc. Int. Symp. White Stork Hamburg, 1996, NABU, Smith DR (2012) Lead poisoning and the deceptive recovery of the (Nafurschutzbund Deutchland e, V), Bonn, pp 481–492 critically endangered California condor. Proc Natl Acad Sci 109: Provencher JF, Bond AL, Avery-Gomm S, Borrelle SB, Bravo Rebolledo 11449–11454. https://doi.org/10.1073/pnas.1203141109 EL, Hammer S, Kuhn S, Lavers JL, Mallory ML, Trevail A, van Franeker JA (2017) Quantifying ingested debris in marine megafau- Flack A, Fiedler W, Blas J, Pokrovsky I, Kaatz M, Mitropolsky M, na: a review and recommendations for standardization. Anal Aghababyan K, Fakriadis I, Makrigianni E, Jerzak L, Azafzaf H, Methods 9:1454–1469. https://doi.org/10.1039/c6ay02419j Feltrup-Azafzaf C, Rotics S, Mokotjomela TM, Nathan R, Wikelski Ptaszyk J (1994) Binfadenaus PolypropylenalsUrsache des Todesjunger M (2016) Costs of migratory decisions: a comparison across eight Weißstorche (Ciconia ciconia) und anderer Tiere. Prace Zakładu white stork populations. Sci Adv 2:e1500931–e1500931. https:// Biologii i Ekologii Ptaków UAM 3:177–181 doi.org/10.1126/sciadv.1500931 Profus P (2006) Population changes and breeding ecology of the white GallSC,ThompsonRC(2015) Theimpactofdebrisonmarinelife.MarPollut stork Ciconia ciconia L. in Poland against a background of the Bull 92:170–179. https://doi.org/10.1016/j.marpolbul.2014.12.041 European population. Synthesis. Stud Nat 50, Kraków Gilbert NI, Correia RA, Silva JP, Pacheco C, Catry I, Atkinson PW, Gill Development Core Team R (2016) R: a language and environment for JA, Franco AMA (2016) Are white storks addicted to junk food? statistical computing. R Foundation for Statistical Computing, Impacts of landfill use on the movement and behaviour of resident Vienna white storks (Ciconia ciconia) from a partially migratory population. Radhamany D, Anoop Das KS, Abdul Azeez P, Sálim A, Wen L, Mov Ecol 4:7. https://doi.org/10.1186/s40462-016-0070-0 Sreekala LK (2016) Usage of nest materials by house sparrow Gregory MR (2009) Environmental implications of plastic debris in ma- (Passer domesticus) along an urban to rural gradient in rine settings – entanglement, ingestion, smothering, hangers-on, Coimbatore, India. Trop Life Sci Res 27:127–134. https://doi.org/ hitch-hiking and alien invasions. Philos Trans R Soc B, Biol Sci 10.21315/tlsr2016.27.2.10 364:2013–2025. https://doi.org/10.1098/rstb.2008.0265 Ryan PG, Moore CJ, van Franeker JA, Moloney CL (2009) Monitoring Hartwig E, Clemens T, Heckroth M (2007) Plastic debris as nesting ma- the abundance of plastic debris in the marine environment. Philos terial in a kittiwake (Rissa tridactyla) colony at the Jammerbugt, Trans R Soc B, Biol Sci 364:1999–2012. https://doi.org/10.1098/ Northwest Denmark. Mar Pollut Bull 54:595–597. https://doi.org/ rstb.2008.0207 10.1016/j.marpolbul.2007.01.027 Schamber JL, Sedinger JS, Ward DH (2012) Carry-over effects of winter Henriksen K (2000) Man-made materials in nests of blackbirds. Dan location contribute to variation in timing of nest initiation and clutch OrnitolForenTidss94:90–91 size in black Brant (Branta bernicla nigricans). Auk 129:205–210. Henry PY, Wey G, Balança G (2011) Rubber band ingestion by a rubbish https://doi.org/10.1525/auk.2012.11249 dump dweller, the white stork (Ciconia ciconia). Waterbirds 34: Schulz H (1998) Ciconia ciconia white stork. In: Cramp S, Simmons 504–508. https://doi.org/10.1675/063.034.0414 KEL (eds) Birds of the western Palearctic, update 2. Oxford Houston DC, Mee A, McGrady M (2007) Why do condors and vultures University Press, London, pp 69–105 eat junk?: the implications for conservation. J Raptor Res 41:235– Seacor R, Ostovar K, Restani M (2014) Distribution and abundance of 238. https://doi.org/10.3356/0892-1016(2007)41 baling twine in the landscape near osprey (Pandion haliaetus)nests: Hoornweg D, Bhada-Tata P, Kennedy C (2013) Waste production must implications for nestling entanglement. Can Field Nat 128:173–178. peak this century. Nature 502:615–617 https://doi.org/10.22621/cfn.v128i2.1582 Huin N, Croxall JP (1996) Fishing gear, oil and marine debris associated Sergio F, Blas J, Blanco G, Tanferna A, Lopez L, Lemus JA, Hiraldo F with seabirds at Bird Island, South Georgia, during 1993/1994. Mar (2011) Raptor nest decorations are a reliable threat against conspe- Ornithol 24:19–22 cifics. Science 331:327–330. https://doi.org/10.1126/science. Kruszyk R, Ciach M (2010) White storks, forage on rubbish dumps in Poland—a novel behaviour in population. Eur J Wildlife Res 56:83–87 Slabbekoorn H, den Boer-Visser A (2006) Cities change the songs of Lee K, Jang YC, Hong S, Lee J, Kwon IK (2015) Plastic marine debris birds. Curr Biol 16:2326–2331. https://doi.org/10.1016/j.cub.2006. used as nesting materials of the endangered species black-faced 10.008 spoonbill Platalea minor decreases by conservation activities. J Suárez-Rodríguez M, Lopez-Rull I, Macias Garcia C (2012) Korean Soc Mar Environ Energy 18:45–49. https://doi.org/10. Incorporation of cigarette butts into nests reduces nest ectoparasite 7846/JKOSMEE.2015.18.1.45 load in urban birds: new ingredients for an old recipe? Biol Lett 9: Mee A, Rideout BA, Hamber JA, Todd JN, Austin G, Clark M, Wallace 120931. https://doi.org/10.1098/rsbl.2012.0931 MP (2007) Junk ingestion and nestling mortality in a reintroduced Suárez-Rodríguez M, Macías Garcia C (2014) There is no such a thing as population of California condors Gymnogyps californianus.Bird a free cigarette; lining nests with discarded butts brings short-term Conserv Int 17:119 –130. https://doi.org/10.1017/ benefits, but causes toxic damage. J Evol Biol 27:2719–2726. S095927090700069X https://doi.org/10.1111/jeb.12531 Miranda AC (2017) Mechanisms of behavioural change in urban animals: Thompson RC, Moore CJ, Vom Saal FS, Swan SH (2009) Plastics, the the role of microevolution and phenotypic plasticity. In: Murgui E, environment and human health: current consensus and future trends. Hedblom M (eds) Ecology and conservation of birds in urban envi- Philos Trans R Soc Lond Ser B Biol Sci 364:2153–2166. https://doi. ronments. Springer international publishing, Cham, Switzerland, pp org/10.1098/rstb.2009.0054 113–132 Tobolka M, Kuźniak S, Zolnierowicz KM, Sparks TH, Tryjanowski P Morin M, Conant S (1990) Nest substrate between native and introduced (2013) New is not always better: low breeding success and different populations of Laysan finches. Wilson Bull 102:591–604. https:// occupancy pattern in newly built nests of a long-lived species, the doi.org/10.2307/4162932 white stork Ciconia ciconia. Bird Study 60:399–403. https://doi.org/ Ortega S, Sanchez-Macouzet O, Urrutia A, Rodriguez C, Drummond H 10.1080/00063657.2013.818934 (2017) Age-related parental care in a long-lived bird: implications Tobolka M, Zolnierowicz KM, Reeve NF (2015) The effect of extreme for offspring development. Behav Ecol Sociobiol 71:123. https:// weather events on breeding parameters of the white stork (Ciconia doi.org/10.1007/s00265-017-2364-7 ciconia). Bird Study 62:377–385. https://doi.org/10.1080/ 00063657.2015.1058745 Ożgo M, Bogucki Z (1999) Home range and intersexual differences in the foraging habitat use of a White Stork (Ciconia ciconia) breeding Tortosa FS, Caballero JM, Reyes-Lopez J (2002) Effect of rubbish dumps on breeding success in the white stork in southern Spain. Waterbirds pair. In: Schulz H (ed). Weißstorchim Aufwind? - White Storks on Environ Sci Pollut Res (2018) 25:14726–14733 14733 25:39–43. https://doi.org/10.1675/1524-4695(2002)025[0039: Swain Reefs, Great Barrier Reef, Australia. Mar Pollut Bull 87:180– 190. https://doi.org/10.1016/j.marpolbul.2014.07.060 EORDOB]2.0.CO;2 Tortosa FS, Pérez P, Hillström L (2003) Effect of food abundance on Votier SC, Archibald K, Morgan G, Morgan L (2011) The use of plastic laying date and clutch size in the white stork Ciconia ciconia.Bird debris as nesting material by a colonial seabird and associated en- Study 50:112–115. https://doi.org/10.1080/00063650309461302 tanglement mortality. Mar Pollut Bull 62:168–172. https://doi.org/ Townsend AK, Barker CM (2014) Plastic and the nest entanglement of 10.1016/j.marpolbul.2010.11.009 urban and agricultural crows. PLoS One 9:e88006. https://doi.org/ Wang Y, Chen S, Blair RB, Jiang P, Ding P (2009) Nest composition 10.1371/journal.pone.0088006 adjustments by Chinese bulbuls (Pycnonotus sinensis)in an urban- Tryjanowski P, Kosicki JZ, Kuźniak S, Sparks TH (2009) Long-term ized landscape of Hangzhou (E China). Acta Ornithol 44:185–192. changes and breeding success in relation to nesting structures used https://doi.org/10.3161/000164509X482768 by white stork (Ciconia ciconia). Ann Zool Fenn 46:34–38. https:// Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer- doi.org/10.5735/086.046.0104 Verlag, New York Tryjanowski P, Sparks TH, Jerzak L (2006) The white stork in Poland: Wilcox C, Van Sebille E, Hardesty BD (2015) Threat of plastic pollution studies in biology, ecology and conservation. Bogucki to seabirds is global, pervasive, and increasing. Proc Natl Acad Sci Wydawnictwo Naukowe, Poznań 112:11899–11904. https://doi.org/10.1073/pnas.1502108112 Vergara P, Gordo O, Aguirre JI (2010) Nest size, nest building behavior Young LC, Vanderlip C, Duffy DC, Afanasyev V, Shaffer SA (2009) and breeding success in a species with nest reuse: the white stork Bringing home the trash: do colony-based differences in foraging Ciconia ciconia. Ann Zool Fenn 47:184–194. https://doi.org/10. distribution lead to increased plastic ingestion in Laysan albatrosses? 5735/086.047.0303 PLoS One 4:e7623. https://doi.org/10.1371/journal.pone.0007623 Verlis KM, Campbell ML, Wilson SP (2014) Marine debris is selected as nesting material by the brown booby (Sula leucogaster)withinthe http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Environmental Science and Pollution Research Springer Journals

Factors determining the occurrence of anthropogenic materials in nests of the white stork Ciconia ciconia

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Environment; Environment, general; Environmental Chemistry; Ecotoxicology; Environmental Health; Atmospheric Protection/Air Quality Control/Air Pollution; Waste Water Technology / Water Pollution Control / Water Management / Aquatic Pollution
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0944-1344
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10.1007/s11356-018-1626-x
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Abstract

Birds have been using anthropogenic materials for nest construction for the past few decades. However, there is a trade-off between the use of new nesting material, which is often linked to greater breeding success, and the higher risk of nestling mortality due to entanglement or ingestion of debris. Here, we investigate the incorporation of anthropogenic materials into nests of the white stork Ciconia ciconia, based on a long-term study of a population in Western Poland. We recorded at least one item of debris in 50 and 42% of nests at the egg and nestling stages, respectively. More debris was found in nests located in territories with higher number of anthropogenic material in the surrounding environment. We found a relationship between the age of females, the number of debris in the area surrounding a nest, and the number of debris in the nest. We found no significant effect of the total number of debris in nests on clutch size, number of fledglings, or breeding success. Studies on the influence of the age and sex of individuals in understanding this behaviour and its drivers in bird populations should be continued. . . . Keywords Nest-building behaviour Breeding success Debris Pollution Introduction padding of nests. Birds of different taxa are well known for incorporating anthropogenic materials into nests (Morin and Human activities induce significant changes in the natural Conant 1990; Huin and Croxall 1996;Blemetal. 2002; environment, which lead in turn to changes in the behaviour Hartwig et al. 2007; Townsend and Barker 2014). This behav- of animals living in urban environments (Carney and iour may be influenced by the abundance and availability of Sydeman 1999; Slabbekoorn and den Boer-Visser 2006; debris in marine, urban, and agricultural environments Miranda 2017). Increases in solid waste abundance as a result (Henriksen 2000;Wanget al. 2009;Bond et al. 2012, 2013; of the growth of urbanisation (Hoornweg et al. 2013)have Eriksen et al. 2014; Wilcox et al. 2015). Due to environmental made anthropogenic materials commonly available in terres- changes (e.g. large-scale modern farming, the development, or trial and marine environments. Debris, mainly in the marine spread of urbanisation), natural elements (e.g. wooden sticks, environment, is a cause of mortality in many animals straw, hay) may be scarce. Hence, incorporating easily avail- (Gregory 2009;Ryanet al. 2009;Votieret al. 2011). able debris can potentially reduce the costs of collecting nat- However, it is also used as material for the construction or ural material, especially when the debris is light and durable, e.g. plastic string (Antczak et al. 2010) or plastic foil. A study Responsible editor: Philippe Garrigues of the black-faced spoonbill Platalea minor showed that, in a highly polluted and changed environment, supplying natural Electronic supplementary material The online version of this article (https://doi.org/10.1007/s11356-018-1626-x) contains supplementary elements led to a reduction in the number of debris incorpo- material, which is available to authorized users. rated into nests (Lee et al. 2015). Collection of debris may be modified by several other factors. In terrestrial species, the * Marcin Tobolka number of anthropogenic materials used to construct the nest tobolkamarcin@gmail.com can be correlated with the level of urbanisation (Wang et al. 1 2009; Radhamany et al. 2016). However, the use of anthropo- Institute of Zoology, Poznań University of Life Sciences, Wojska genic materials in nests may also be triggered by mating be- Polskiego 71C, 60-625 Poznań, Poland 2 haviour, e.g. bowerbirds (Ptilonorhynchidae) build bowers to Department of Zoology and Physical Anthropology, Complutense attract females (Borgia 1985). Bower decoration can be a University of Madrid, Jose Antonio Novais, 12, 28040 Madrid, Spain Environ Sci Pollut Res (2018) 25:14726–14733 14727 decisive factor for females choosing a mate. Bowerbirds dec- Europe, white storks often forage in rubbish dumps, a practice orate bowers with flowers, plants, and debris—bottle tops, which has probably driven the population increase (Tortosa straws, etc. (Borgia 1985). Males with better decorated bowers et al. 2002). This species is known to incorporate debris from are more attractive and have better chances for reproduction; rubbish dumps in their nests (Henry et al. 2011). Eastern (in- this may ultimately increase the number of anthropogenic ma- cluding Polish) white stork populations rarely use rubbish terial in bowers. Incorporation of debris may be also depen- dumps (Kruszyk and Ciach 2010); instead, debris from the dent on the age (experience) of individual birds (Coleman immediate environment (e.g. plastic strings, foil) is collected et al. 2004). In black kites Milvus migrans, the number of from agricultural lands as nesting material and incorporated anthropogenic material in nests is related to the age of pair into nests (Tryjanowski et al. 2006). Plastic string is one of the members; it is also strongly linked to individual quality and most common anthropogenic materials used by terrestrial spe- therefore has a strong influence on breeding success. Higher- cies as nesting material (Antczak et al. 2010; Seacor et al. quality individuals collect more debris, are better breeders, 2014). This material has been commonly used in Polish agri- and occupy better territories (Sergio et al. 2011). What is culture since 1982 for tying, e.g. hay and straw (Ptaszyk more, nest decoration can signal the condition, experience, 1994). Due to its utility, fragments are ubiquitous in the agri- fighting capabilities, territory quality, and social dominance cultural landscape. It is available to foraging birds, along with of the individual or the breeding pair to other individuals plastic foil, which is used in farmlands to cover, e.g. hay bales (Canal et al. 2016). or certain types of crops. These materials are the main sources The use of anthropogenic materials may also have negative of plastic pollution in farmlands. Moreover, the white stork is consequences. Plastic string, fishing nets, and angling gear are characterised by its longevity, and thus studies on the impact resistant materials occurring in the sea (far from nest sites) as of age on nesting behaviour are feasible. This makes the white well in the nest (collected by adults). These items often cause stork a suitable subject for detailed research on the impact of entanglement, leading to mortality or injuries (Baker et al. anthropogenic material on nesting behaviour. We investigated 2002; Seacor et al. 2014). Entanglement has been recorded two factors which may influence the inclusion of debris in in 25% of 312 studied seabird species (Gall and Thompson nests: the availability of debris in the vicinity of nests 2015). Hence, birds collecting debris for their nests may in- (Henriksen 2000; Wang et al. 2009;Bond et al. 2012)and crease the risk of ingestion and entanglement, which may the age of individuals (Sergio et al. 2011; Canal et al. 2016). reduce breeding success (Mee et al. 2007). While this phe- With regard to age-assortative mating in white storks, we nomenon has been studied in marine birds (Provencher et al. know that the ages of both breeders constituting a pair are very 2017), it is rarely described in the cases of land birds and similar (in cases where the age of only one pair member is inland waterbirds. Other debris, e.g. cigarette butts, may have known) (Barbraud and Barbraud 1999). Hence, we an initial positive effect, i.e. may act as an ectoparasite repel- hypothesised that (1) the greater the density of anthropogenic lent (Suárez-Rodríguez et al. 2012). However, long-term ob- materials in the environment in the vicinity of the nest, the servations showed the cost of exposure to toxins, namely, a higher the number of anthropogenic materials incorporated higher genotoxicity level (damage to DNA or chromosomal into the nest, associated with the question of whether there is material) in nestlings’ blood cells (Suárez-Rodríguez and any preference for a particular type of debris; (2) the ages of Macías Garcia 2014). Ingestion of anthropogenic material, individuals have a direct impact on the number of anthropo- which may also occur in nests, is another cost associated with genic material included in the nest; and (3) birds incorporating individual survival (Houston et al. 2007; Mee et al. 2007; the greatest number of debris (pieces) into nests are not only Young et al. 2009; Henry et al. 2011; Finkelstein et al. 2012). older but also better breeders, as reflected in greater numbers In this study, we examine the impact of the incorporation of of eggs and fledglings. The incorporation of debris into nests anthropogenic materials into nests of a large migratory in agricultural landscapes has been shown in only a few stud- synanthropic water bird, the white stork Ciconia ciconia. ies (e.g. Antczak et al. 2010; Townsend and Barker 2014). Traditionally, this bird bred in colonies in river valleys but This is the first long-term research to explain the effect of has now moved closer to human settlements. Nowadays, it debris on a bird inhabiting farmlands, i.e. the white stork. is a common species which breeds and forages in agricultural areas and nests close to human settlements (Schulz 1998). At the same time, it is a well-studied bird species, with popula- Materials and methods tions being monitored over the long term (Bairlein 1991). The population has declined in Western Europe due to the intensi- Fieldwork fication of agriculture and to drought in the Sahel, where it winters. Following a precipitate decline, the population has We conducted the study in Western Poland near the town of recovered due to reintroduction and additional feeding Leszno (51°51′ N, 16°35′ E), within a mainly rural area of programmes in several countries (Bairlein 1991). In Western 4154 km comprising arable fields (54%), forests (17%), 14728 Environ Sci Pollut Res (2018) 25:14726–14733 human settlements (10%), a small proportion of meadows properties and to Townsend and Barker (2014), into catego- (7%) and pastures (< 1%), and other land-use types (12%) ries: foil, plastic string, other plastic, paper, textiles and other. (Tobolka et al. 2015). Additionally, we divided nest debris using a standardised First, we used data collected during a long-term study of the method (Provencher et al. 2017) in order to facilitate compar- white stork’s breeding and population ecology, which com- ison with future studies. Finally, we recorded breeding success prised ca 50 nests visited each year between 2009 and 2016 by counting fledglings, i.e. chicks over 50 days of age standing for recording clutch size, over 100 nests where the number of in the nest and considered able to fly (a standard method to fledglings was recorded during ringing, and over 300 nests estimate the breeding success of the white stork) (Tryjanowski where breeding results were recorded (for details, see et al. 2006). Breeding success was defined as the number of Tobolka et al. 2013, 2015). The data were collected for 342 fledglings divided by the number of eggs laid. broods at the egg stage and 445 broods at the chick stage during the years 2009–16; during this period, all anthropogen- Statistical analyses ic materials in the nests were counted (details in supplementary material, Table S1). To decrease the risk of nestling entangle- Prior to statistical analyses, we used the fitdistrplus package ment and avoid accumulation of recorded debris during sub- (Delignette-Muller and Dutang 2015) to check the distribution sequent visits, we removed all debris from the nest during each of dependent variables. To test the effect of the number of visit. Second, we searched for adults of known age and sex debris in the environment on the number of debris in white with alphanumeric rings (sexed by molecular procedures; see stork nests, we used a generalised linear mixed model details in Dubiec and Zagalska-Neubauer 2006; Fernandes (GLMM) with a Poisson error structure and a log link func- et al. 2006).White storks are marked mainly as nestlings; tion; specifically, we used a GLMM with a binomial error hence, we knew the exact age of adults that had been ringed structure with a logit link function to explain the effect of several years earlier and re-recorded during this study. Marked age and sex on the presence of debris in nests. As a binomial breeders of known age and sex can help to explain the possible response variable, we compared nests with debris (1) to nests impact of age and sex on debris-collecting behaviour and pa- without debris (0). We used GLMM to model variations in rental care. Additionally, we conducted more complex field clutch size, numbers of chicks, and breeding success. For each research during the 2015 breeding season. We conducted two dependent variable, we used a GLMM with a Gaussian error visits: during egg-laying (32 broods) and chick-rearing pe- structure and an identity link function with one fixed-effect riods, the latter amounting to 43 broods between 25 and predictor: total number of debris. In these GLMMs, we used 45 days of age. We visited accessible nests (the same included nest identity and year as random factors. To test the white in the long-term study) with a 7-m ladder, cherry-picker, and stork’s preference for particular types of debris (plastic string, climbing equipment. In the course of nest visits, we collected foil, paper or other), we used chi-square contingency indepen- data on clutch size and number of nestlings, and recorded all dence tests comparing the percentage of debris between white anthropogenic materials present in nests. Clutch size was re- stork nests and the environment for two stages (egg and corded during the second half of incubation (between the 15th chick). We analysed separately the number of debris during and 30th days) (details in Tobolka et al. 2015). The number of the egg and nestling stages because the availability of anthro- nestlings was recorded at the time nestlings were marked. We pogenic material might change due to growth of vegetation established a buffer area with a radius of 500 m around a nest, and intensification of agricultural works (e.g. hay collecting in which we created four random transects 150 m long. The and harvesting) during the breeding season proceeding. All width of each transect was 2 m on either side, or 4 m in analyses were performed in R, version 3.3.2 (R aggregate, at the beginning of the breeding season (egg stage), Development Core Team 2016), using the lme4 (Bates et al. and 1 m on either side (2 m in aggregate) during the nestling 2015) and ggplot2 (Wickham 2009) packages. stage due to the lower level of visibility caused by vegetation growth; however, dimensions were the same for each transect. The foraging range of the white stork is characterised by a Results radius up to 2 km (Ożgo and Bogucki 1999); however, the stork collects nesting material in the immediate vicinity of In the course of the study (2009–16), in 171 of 342 (50%) the nest, accordingly to personal observations (Tobółka, un- broods during egg stage and in 186 of 445 (42%) broods published). We counted all available potential anthropogenic during chick stage, anthropogenic materials were present. nest materials lying on the ground (Fig. S1). We recorded only The anthropogenic materials categories occurred in the fol- anthropogenic materials with dimensions over 1 cm in diame- lowing proportion: plastic string (38%), foil (33%), textile ter and easily detectable by human eyes (e.g. plastic string, (8%), paper (5%), other plastic (7%) and other (9%). In the foil, paper and other material). Later, we divided debris from surrounding area, the proportion of available debris was as white stork nests and transects, according to physical follows: plastic string (83%), foil (8%), textile (0.3%), paper Environ Sci Pollut Res (2018) 25:14726–14733 14729 (2%), other plastic (3%) and other (3%). The white stork at the chick stage revealed a positive preference for plastic foil (chi- square = 5.828, p = 0.02) and a negative preference regarding string (chi-square = 24.858, p < 0.001). However, during the egg stage, these relationships were not significant (Table 1). More debris was found in nests located in territories with higher rates of anthropogenic material in the surrounding en- vironment (β = 0.02075 ± 0.01351, Z =2.006, p =0.0453, N = 75).We found that probability of recording debris in a given nest was positively correlated with the age of the female (β = 0.9147 ± 0.385, Z =2.377, p =0.018, N = 33, Fig. 1). The age of the male did not explain the probability of recording debris in the nest (β = − 0.2638 ± 0.320, Z = − 0.824, p = 0.410, N =20). We found no significant effect of the total number of debris in a given nest on clutch size (p = 0.423, Table 2), number of fledglings (p = 0.956), or breeding success (p =0.106). Fig. 1 The probability of the presence of debris in nests in relation to the Discussion ages of white stork females In this study, we showed that 46% of white stork nests probable reason for incorporating anthropogenic materials in- contained anthropogenic material. The relationship between to the nest structure is that these materials are common and the numbers of debris in the vicinity of a nest and in the nest easily accessible in the agricultural landscape, which we have itself was significant. Thus, the white stork, as well as marine shown in the case of the white stork. At the moment, we do not birds, may be a potential indicator of debris pollution in the know why white storks prefer to collect foil and plastic, but surrounding environment, as incorporation of debris in nests the preference was shown only during chick stage. During egg may be related to its availability in the environment around stage, there was no preference, and probably white storks those nests (Votier et al. 2011; Avery-Gomm et al. 2012; Bond randomly use what is available in the local environment. et al. 2012). In many aspects of life, the white stork demon- Maybe the former are better insulation materials; however, strates its opportunism and ability to adapt to changing envi- more detailed studies, including experiments, are needed to ronments, e.g. its exploitation of a wide range of new food confirm this statement. Additionally, older individuals collect resources (Tortosa et al. 2002; Djerdali et al. 2008, 2016; these materials to a greater extent in the vicinity of the nest. Ciach and Kruszyk 2010; Gilbert et al. 2016), its use of new White storks may select debris in relation to its abundance, as nesting sites, and its tendency to nest close to human settle- the amount of plastic in the landscape increases (Thompson ments (Tryjanowski et al. 2009; Flack et al. 2016); the use of et al. 2009). Given that natural materials are probably limited debris as a lining material is another example. The most in an intensive agricultural landscape (Antczak et al. 2010), the use of anthropogenic nest material may be a beneficial Table 1 Results of a chi-square contingency independence test for white stork preferences for debris type Nest (%) Environment (%) Chi-square P Table 2 The GLMM’s with Gaussian error describing the relationship between clutch size (n = 342 broods), number of fledglings (n = 445 Egg stage broods) and breeding success (n = 196 broods) to total number of debris in nest String 55 76 3.366 0.07 Foil 10 13 0.391 0.53 Effect Estimate Error tP Paper 0 2 –– Other 35 9 15.364 < 0.001 Clutch size Chick stage No debris in nest 0.513 0.191 0.802 0.423 String 30 83 24.858 < 0.001 No of fledglings Foil 21 8 5.828 0.02 No debris in nest 4.168e-03 7.499e-02 0.056 0.956 Paper 11 2 6.231 0.01 Breeding success Other 38 7 21.356 < 0.001 No debris in nest 0.031 0.019 1.624 0.106 14730 Environ Sci Pollut Res (2018) 25:14726–14733 resource in nest construction. Our research showed that the 39 years of age (Schulz 1998). Therefore, records in subse- most common items of debris in the immediate vicinity of quent years may provide additional data which will render the white stork nests that were incorporated in nests were plastic character of the relationship more similar to that observed by string and foil. These anthropogenic materials were also most Sergio et al. (2011). common in nests of the American crow Corvus We found no significant relationships between total number brachyrhynchos (Townsend and Barker 2014)and thegreat of debris collected for nests and clutch size, number of fledg- grey shrike (Lanius excubitor)(Antczak et al. 2010)inagri- lings, or final breeding success. Assuming that the number of cultural landscapes. debris collected for the nest is a proxy for experience, we may In our study, the probability of the presence of debris in have observed its effect only on breeding success. Egg counts nests was associated with the age of females. However, we did alone do not explain the impact of debris collection because in not find a relationship between the probability of the presence particular cases, young, inexperienced white stork females may of debris in the nest and the age of male white storks. In this lay more eggs compared to older individuals (Aguirre and species, both partners collect nesting material, but we do not Vergara 2007). What is more, clutch size is related to current know whether bringing debris into the nest is a sex-dependent food supply (Tortosa et al. 2003) and to conditions in the win- activity. One local study suggests that males deliver more tering grounds during the previous winter (Schamber et al. nesting material, particularly in the beginning of the breeding 2012; Tobolka et al. in review). Although numbers of collected season (Bocheński and Jerzak 2006); however, we have no debris may be an indicator of innovative behaviour (Borgia knowledge of a more general pattern. In regard to age- 1985) and the age-related experience (Sergio et al. 2011)ofpair assortative mating in this species (Barbraud and Barbraud members,which may bereflected alsoin food provisioning, the 1999; Ferrer and Penteriani 2003), we can assume that the influence ofdebris ondevelopingnestlingsisnot equal.Several ages of white stork males were similar to those of their female typesofdebrismayproducenegativeconsequences,e.g.plastic partners. The lack of a significant relationship may be a result string which may cause entanglement (Antczak et al. 2010), of the small sample size of males (N = 20) of known age. Mate rubber elements, plastic tape or string which may cause stran- choice in the white stork is mostly dependent on nest site gulation (Henry et al. 2011), or wire and other metal elements occupancy. White storks prefer breeding sites with large nests which may cause injuries. Along with the common occurrence or a nest that has been occupied continuously for at least one of the incorporation of anthropogenic materials into nest struc- successful breeding season (Bocheński and Jerzak 2006; tures, only a few cases of entanglement were noticed. During Vergara et al. 2010). Storks collect and deliver debris to the 8 years of studies, 0.73% of 2043 nestlings (from 728 nests) middle part of the nest as a lining, whereas we recorded only were found entangled (11 dead, 4 with fatal injuries necessitat- debris in upper parts, which reflects collecting behaviour dur- ing euthanasia) and two cases of strangulation with plastic ele- ing the current breeding season; therefore, the age and size of a ments choked in nestling throats (Tobolka, unpublished data) nest should not influence the number of debris recorded there- during the ringing process. Hence, we recorded lethal conse- in within a single breeding season. Some bird studies have quences of collecting debris in only 2% of nests. However, the shown a relationship between anthropogenic materials incor- number of entangled nestlings may have been higher, as we did porated into nests by mates and pair formation (Coleman et al. not detect mortality in earlier stages. In this study, nests were 2004; Sergio et al. 2011). In this study, numbers of debris were visited when chicks were old enough to ring, in age of 25– positively correlated only with the ages of females. Sergio 40 days. White stork nestlings spend ca 55 days in the nest, et al. (2011) showed that numbers of debris in nests of black and their mortality varies from 21 to 85%, which is mainly kites were greatest for birds aged 8–11 years, whereas in youn- due to varying weather conditions (Tobolka et al. 2015); entan- ger and older individuals, this phenomenon was significantly glementmaybeanotherthreat.Thissituationwasalsoobserved less frequent. The probable explanation is that the experience intheAmericancrowinfarmlands,where5.6%of195nestlings (better quality) of the individual is age-related, although pos- were entangled in their nests (Townsend and Barker 2010). sibly, it exhibits an inverted U-pattern (Ortega et al. 2017). Environmental pollution with anthropogenic materials has The white stork also reveals this pattern, i.e. individuals aged been present only for the past several decades; therefore, incor- between 8 and 12 years are the best breeders (Profus 2006). In poration of debris in nests by birds is a relatively new behaviour our study, the relationship had a different character, being non- (Ptaszyk 1994). There are many reports of the incorporation of linear as well; nevertheless, the probability of incorporating debris into nests by various bird species (e.g. marine colonial debris into the nest increased continuously with a stork’sage. birds) (Votier et al. 2011; Verlis et al. 2014; Tavares et al. 2016), Experience comes with age, therefore, more experienced birds although the scale of this behaviour is still not known in detail. may be more likely to incorporate debris into their nests, ac- The white stork appears to be a species in which the phenome- cording to results published by Sergio et al. (2011). non is currently developing, at least in Poland. It may be worth Irrespective of this, the oldest female in our study was 10 years monitoring whether debris incorporation into nests becomes old, whereas the white stork can live much longer, even up to more widespread and exerts an impact on individuals and Environ Sci Pollut Res (2018) 25:14726–14733 14731 Baker GB, Gales R, Hamilton S, Wilkinson V (2002) Albatrosses and populations in future. However, the abundance of plastic string petrels in Australia: a review of their conservation and management. in the agricultural environment and its non-biodegradability (it Emu 102:71–97. https://doi.org/10.1071/MU01036 only breaks into smaller and smaller fragments) make it neces- Barbraud C, Barbraud JC (1999) Is there age assortative mating in the sary to constantly monitor the scale of entanglement and inges- European white stork? Waterbirds 22:478–481. https://doi.org/10. 2307/1522129 tion. Moreover, this behaviour may be widespread and may Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed- have an impact on more individuals/populations in the future effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10. (e.g. Antczak et al. 2010). 18637/jss.v067.i01 Blem CR, Blem LB, Harmata PJ (2002) Twine causes significant mortal- ity in nestlings ospreys. Wilson Bull 114:528–529. https://doi.org/ 10.1676/00435643(2002)114[0528:TCSMIN]2.0.CO;2 Conclusions Bocheński M, Jerzak L (2006) Behaviour of the white stork (Ciconia ciconia): a review. Bogucki Wydawnictwo Naukowe, Poznań Bond AL, Montevecchi WA, Guse N, Regular PM, Garthe S, Rail JF Considering all aspects, the white stork adapts easily to an- (2012) Prevalence and composition of fishing gear debris in the thropogenic changes and can use new nesting material avail- nests of northern gannets (Morus bassanus) are related to fishing able in the environment. In order to define the long-term con- effort. Mar Pollut Bull 64:907–911. https://doi.org/10.1016/j. marpolbul.2012.03.011 sequences (i.e. costs of incorporating debris) and individual Bond AL, Provencher JF, Elliot RD, Ryan PC, Rowe S, Jones IL, conditions for incorporating anthropogenic materials into Robertson GJ, Wilhelm SI (2013) Ingestion of plastic marine debris nests, this behaviour should be continuously monitored, and by common and thick-billed murres in the northwestern Atlantic more studies should be performed to understand this phenom- from 1985 to 2012. Mar Pollut Bullet 77:192–195. https://doi.org/ 10.1016/j.marpolbul.2013.10.005 enon better. Using more detailed methods (e.g. trapping cam- Borgia G (1985) Bowers quality, number of decorations and mating suc- eras) will help us to identify the exact pattern of collecting cess of male satin bowerbirds (Ptilonorhynchus violaceus): an ex- debris for nests, as well as to determine which sex is primarily perimental analysis. Anim Behav 33:266–271. https://doi.org/10. responsible for debris collection and when such incorporation 1016/S0003-3472(85)80140-8 takes place. Also, in this case, research on the impact of the Canal D, Mulero-Pázmány M, Negro JJ, Sergio F (2016) Decoration increases the conspicuousness of raptor nests. PLoS One 11: age of individuals on this behaviour should be continued. e0157440. https://doi.org/10.1371/journal.pone.0157440 Carney KM, Sydeman WJ (1999) A review of human disturbance effects Acknowledgements We are grateful to Nathalie Gilbert for assistance on nesting colonial waterbirds. Waterbirds 22:68–79. https://doi.org/ with English language editing and Jose I. Aguirre for critical comments 10.2307/1521995 on an earlier version of the manuscript. The study was funded by the Ciach M, Kruszyk R (2010) Foraging of white storks Ciconia ciconia on National Science Centre (MT) as part of the projects N/NZ8/01186 and rubbish dumps on non-breeding grounds. Waterbirds 33:101–104. T/NZ8/01001. In 2010/11 and 2013/14, MT was a scholarship holder https://doi.org/10.1675/063.033.0112 within a project co-financed by the European Social Fund. Coleman SE, Patricelli GA, Borgia G (2004) Variable females prefer- ences drive complex male displays. Nature 428:742–745. https:// doi.org/10.1038/nature02419 Open Access This article is distributed under the terms of the Creative Delignette-Muller ML, Dutang C (2015) Fitdistrplus: an R package for Commons Attribution 4.0 International License (http:// fitting distributions. J Stat Softw 64:1–34. https://doi.org/10.18637/ creativecommons.org/licenses/by/4.0/), which permits unrestricted use, jss.v064.i04 distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link Djerdali S, Tortosa FS, Hillstrom L, Doumandji S (2008) Food supply to the Creative Commons license, and indicate if changes were made. and external cues limit the clutch size and hatchability in the white stork Ciconia ciconia. Acta Ornithol 43:145–150. https://doi.org/10. 3161/000164508X395252 Djerdali S, Guerrero-Casado J, Tortosa FS (2016) The effects of colony size interacting with extra food supply on the breeding success of the References white stork (Ciconia ciconia). J Ornithol 157:941–947. https://doi. org/10.1007/s10336-016-1343-5 Aguirre JM, Vergara P (2007) Younger, weaker white stork (Ciconia Dubiec A, Zagalska-Neubauer M (2006) Molecular techniques for sex ciconia) became the best breeders. Evol Ecol Res 9:355–364 identification in birds. Biol Lett 43:3–12 Antczak M, Hromada M, Czechowski P, Tabor J, Zabłocki P, Grzybek J, Eriksen M, Lebreton LCM, Carson HS, Thiel M, Moore CJ, Borerro JC, Tryjanowski P (2010) A new material for old solutions—the case of Galgani F, Ryan PG, Reisser J (2014) Plastic pollution in the world’s plastic string used in great grey shrike nests. Acta Ethol 13:87–91. oceans: more than 5 trillion plastic pieces weighing over 250,000 https://doi.org/10.1007/s10211-010-0077-2 tons afloat at sea. PLoS One 9:e111913. https://doi.org/10.1371/ journal.pone.0111913 Avery-Gomm S, O’Hara PD, Kleine L, Bowes V, Wilson LK, Barry KL (2012) Northern fulmars as biological monitors of trends of plastic Fernandes M, Borges C, Simoes F, Caballero JM, Pacheco C, Franco C pollution in the eastern North Pacific. Mar Pollut Bull 64:1776– (2006) Molecular sexing of the black stork Ciconia nigra:sex ratios 1781. https://doi.org/10.1016/j.marpolbul.2012.04.017 in the Portuguese population. Biota 7:31–36 Ferrer M, Penteriani V (2003) A process of pair formation leading to Bairlein F (1991) Population studies of white stork (Ciconia ciconia)in Europe. In: Perrins CM, Lebreton JD, Hirons GJM (eds) Bird pop- assortative mating: passive age-assortative mating by habitat hetero- geneity. Anim Behav 66:137–143. https://doi.org/10.1006/anbe. ulation studies: relevance to conservation and management. Oxford University Press, Oxford, pp 207–229 2003.2158 14732 Environ Sci Pollut Res (2018) 25:14726–14733 Finkelstein ME, Doak DF, George D, Burnett J, Brandt J, Grantham J, the up? Proc. Int. Symp. White Stork Hamburg, 1996, NABU, Smith DR (2012) Lead poisoning and the deceptive recovery of the (Nafurschutzbund Deutchland e, V), Bonn, pp 481–492 critically endangered California condor. Proc Natl Acad Sci 109: Provencher JF, Bond AL, Avery-Gomm S, Borrelle SB, Bravo Rebolledo 11449–11454. https://doi.org/10.1073/pnas.1203141109 EL, Hammer S, Kuhn S, Lavers JL, Mallory ML, Trevail A, van Franeker JA (2017) Quantifying ingested debris in marine megafau- Flack A, Fiedler W, Blas J, Pokrovsky I, Kaatz M, Mitropolsky M, na: a review and recommendations for standardization. Anal Aghababyan K, Fakriadis I, Makrigianni E, Jerzak L, Azafzaf H, Methods 9:1454–1469. https://doi.org/10.1039/c6ay02419j Feltrup-Azafzaf C, Rotics S, Mokotjomela TM, Nathan R, Wikelski Ptaszyk J (1994) Binfadenaus PolypropylenalsUrsache des Todesjunger M (2016) Costs of migratory decisions: a comparison across eight Weißstorche (Ciconia ciconia) und anderer Tiere. Prace Zakładu white stork populations. Sci Adv 2:e1500931–e1500931. https:// Biologii i Ekologii Ptaków UAM 3:177–181 doi.org/10.1126/sciadv.1500931 Profus P (2006) Population changes and breeding ecology of the white GallSC,ThompsonRC(2015) Theimpactofdebrisonmarinelife.MarPollut stork Ciconia ciconia L. in Poland against a background of the Bull 92:170–179. https://doi.org/10.1016/j.marpolbul.2014.12.041 European population. Synthesis. Stud Nat 50, Kraków Gilbert NI, Correia RA, Silva JP, Pacheco C, Catry I, Atkinson PW, Gill Development Core Team R (2016) R: a language and environment for JA, Franco AMA (2016) Are white storks addicted to junk food? statistical computing. R Foundation for Statistical Computing, Impacts of landfill use on the movement and behaviour of resident Vienna white storks (Ciconia ciconia) from a partially migratory population. Radhamany D, Anoop Das KS, Abdul Azeez P, Sálim A, Wen L, Mov Ecol 4:7. https://doi.org/10.1186/s40462-016-0070-0 Sreekala LK (2016) Usage of nest materials by house sparrow Gregory MR (2009) Environmental implications of plastic debris in ma- (Passer domesticus) along an urban to rural gradient in rine settings – entanglement, ingestion, smothering, hangers-on, Coimbatore, India. Trop Life Sci Res 27:127–134. https://doi.org/ hitch-hiking and alien invasions. Philos Trans R Soc B, Biol Sci 10.21315/tlsr2016.27.2.10 364:2013–2025. https://doi.org/10.1098/rstb.2008.0265 Ryan PG, Moore CJ, van Franeker JA, Moloney CL (2009) Monitoring Hartwig E, Clemens T, Heckroth M (2007) Plastic debris as nesting ma- the abundance of plastic debris in the marine environment. Philos terial in a kittiwake (Rissa tridactyla) colony at the Jammerbugt, Trans R Soc B, Biol Sci 364:1999–2012. https://doi.org/10.1098/ Northwest Denmark. Mar Pollut Bull 54:595–597. https://doi.org/ rstb.2008.0207 10.1016/j.marpolbul.2007.01.027 Schamber JL, Sedinger JS, Ward DH (2012) Carry-over effects of winter Henriksen K (2000) Man-made materials in nests of blackbirds. Dan location contribute to variation in timing of nest initiation and clutch OrnitolForenTidss94:90–91 size in black Brant (Branta bernicla nigricans). Auk 129:205–210. Henry PY, Wey G, Balança G (2011) Rubber band ingestion by a rubbish https://doi.org/10.1525/auk.2012.11249 dump dweller, the white stork (Ciconia ciconia). Waterbirds 34: Schulz H (1998) Ciconia ciconia white stork. In: Cramp S, Simmons 504–508. https://doi.org/10.1675/063.034.0414 KEL (eds) Birds of the western Palearctic, update 2. Oxford Houston DC, Mee A, McGrady M (2007) Why do condors and vultures University Press, London, pp 69–105 eat junk?: the implications for conservation. J Raptor Res 41:235– Seacor R, Ostovar K, Restani M (2014) Distribution and abundance of 238. https://doi.org/10.3356/0892-1016(2007)41 baling twine in the landscape near osprey (Pandion haliaetus)nests: Hoornweg D, Bhada-Tata P, Kennedy C (2013) Waste production must implications for nestling entanglement. Can Field Nat 128:173–178. peak this century. Nature 502:615–617 https://doi.org/10.22621/cfn.v128i2.1582 Huin N, Croxall JP (1996) Fishing gear, oil and marine debris associated Sergio F, Blas J, Blanco G, Tanferna A, Lopez L, Lemus JA, Hiraldo F with seabirds at Bird Island, South Georgia, during 1993/1994. Mar (2011) Raptor nest decorations are a reliable threat against conspe- Ornithol 24:19–22 cifics. Science 331:327–330. https://doi.org/10.1126/science. Kruszyk R, Ciach M (2010) White storks, forage on rubbish dumps in Poland—a novel behaviour in population. Eur J Wildlife Res 56:83–87 Slabbekoorn H, den Boer-Visser A (2006) Cities change the songs of Lee K, Jang YC, Hong S, Lee J, Kwon IK (2015) Plastic marine debris birds. Curr Biol 16:2326–2331. https://doi.org/10.1016/j.cub.2006. used as nesting materials of the endangered species black-faced 10.008 spoonbill Platalea minor decreases by conservation activities. J Suárez-Rodríguez M, Lopez-Rull I, Macias Garcia C (2012) Korean Soc Mar Environ Energy 18:45–49. https://doi.org/10. Incorporation of cigarette butts into nests reduces nest ectoparasite 7846/JKOSMEE.2015.18.1.45 load in urban birds: new ingredients for an old recipe? Biol Lett 9: Mee A, Rideout BA, Hamber JA, Todd JN, Austin G, Clark M, Wallace 120931. https://doi.org/10.1098/rsbl.2012.0931 MP (2007) Junk ingestion and nestling mortality in a reintroduced Suárez-Rodríguez M, Macías Garcia C (2014) There is no such a thing as population of California condors Gymnogyps californianus.Bird a free cigarette; lining nests with discarded butts brings short-term Conserv Int 17:119 –130. https://doi.org/10.1017/ benefits, but causes toxic damage. J Evol Biol 27:2719–2726. S095927090700069X https://doi.org/10.1111/jeb.12531 Miranda AC (2017) Mechanisms of behavioural change in urban animals: Thompson RC, Moore CJ, Vom Saal FS, Swan SH (2009) Plastics, the the role of microevolution and phenotypic plasticity. In: Murgui E, environment and human health: current consensus and future trends. Hedblom M (eds) Ecology and conservation of birds in urban envi- Philos Trans R Soc Lond Ser B Biol Sci 364:2153–2166. https://doi. ronments. Springer international publishing, Cham, Switzerland, pp org/10.1098/rstb.2009.0054 113–132 Tobolka M, Kuźniak S, Zolnierowicz KM, Sparks TH, Tryjanowski P Morin M, Conant S (1990) Nest substrate between native and introduced (2013) New is not always better: low breeding success and different populations of Laysan finches. Wilson Bull 102:591–604. https:// occupancy pattern in newly built nests of a long-lived species, the doi.org/10.2307/4162932 white stork Ciconia ciconia. Bird Study 60:399–403. https://doi.org/ Ortega S, Sanchez-Macouzet O, Urrutia A, Rodriguez C, Drummond H 10.1080/00063657.2013.818934 (2017) Age-related parental care in a long-lived bird: implications Tobolka M, Zolnierowicz KM, Reeve NF (2015) The effect of extreme for offspring development. Behav Ecol Sociobiol 71:123. https:// weather events on breeding parameters of the white stork (Ciconia doi.org/10.1007/s00265-017-2364-7 ciconia). Bird Study 62:377–385. https://doi.org/10.1080/ 00063657.2015.1058745 Ożgo M, Bogucki Z (1999) Home range and intersexual differences in the foraging habitat use of a White Stork (Ciconia ciconia) breeding Tortosa FS, Caballero JM, Reyes-Lopez J (2002) Effect of rubbish dumps on breeding success in the white stork in southern Spain. Waterbirds pair. In: Schulz H (ed). Weißstorchim Aufwind? - White Storks on Environ Sci Pollut Res (2018) 25:14726–14733 14733 25:39–43. https://doi.org/10.1675/1524-4695(2002)025[0039: Swain Reefs, Great Barrier Reef, Australia. Mar Pollut Bull 87:180– 190. https://doi.org/10.1016/j.marpolbul.2014.07.060 EORDOB]2.0.CO;2 Tortosa FS, Pérez P, Hillström L (2003) Effect of food abundance on Votier SC, Archibald K, Morgan G, Morgan L (2011) The use of plastic laying date and clutch size in the white stork Ciconia ciconia.Bird debris as nesting material by a colonial seabird and associated en- Study 50:112–115. https://doi.org/10.1080/00063650309461302 tanglement mortality. Mar Pollut Bull 62:168–172. https://doi.org/ Townsend AK, Barker CM (2014) Plastic and the nest entanglement of 10.1016/j.marpolbul.2010.11.009 urban and agricultural crows. PLoS One 9:e88006. https://doi.org/ Wang Y, Chen S, Blair RB, Jiang P, Ding P (2009) Nest composition 10.1371/journal.pone.0088006 adjustments by Chinese bulbuls (Pycnonotus sinensis)in an urban- Tryjanowski P, Kosicki JZ, Kuźniak S, Sparks TH (2009) Long-term ized landscape of Hangzhou (E China). Acta Ornithol 44:185–192. changes and breeding success in relation to nesting structures used https://doi.org/10.3161/000164509X482768 by white stork (Ciconia ciconia). Ann Zool Fenn 46:34–38. https:// Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer- doi.org/10.5735/086.046.0104 Verlag, New York Tryjanowski P, Sparks TH, Jerzak L (2006) The white stork in Poland: Wilcox C, Van Sebille E, Hardesty BD (2015) Threat of plastic pollution studies in biology, ecology and conservation. Bogucki to seabirds is global, pervasive, and increasing. Proc Natl Acad Sci Wydawnictwo Naukowe, Poznań 112:11899–11904. https://doi.org/10.1073/pnas.1502108112 Vergara P, Gordo O, Aguirre JI (2010) Nest size, nest building behavior Young LC, Vanderlip C, Duffy DC, Afanasyev V, Shaffer SA (2009) and breeding success in a species with nest reuse: the white stork Bringing home the trash: do colony-based differences in foraging Ciconia ciconia. Ann Zool Fenn 47:184–194. https://doi.org/10. distribution lead to increased plastic ingestion in Laysan albatrosses? 5735/086.047.0303 PLoS One 4:e7623. https://doi.org/10.1371/journal.pone.0007623 Verlis KM, Campbell ML, Wilson SP (2014) Marine debris is selected as nesting material by the brown booby (Sula leucogaster)withinthe

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