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 firstname.lastname@example.org 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. 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