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Phalangeal Bone Anomalies in the European Common Toad Bufo Bufo from Polluted Environments

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Phalangeal Bone Anomalies in the European Common Toad Bufo Bufo from Polluted Environments Environ Sci Pollut Res DOI 10.1007/s11356-016-7297-6 RESEARCH ARTICLE Phalangeal bone anomalies in the European common toad Bufo bufo from polluted environments Mikołaj Kaczmarski1 & Krzysztof Kolenda 2 & Beata Rozenblut-Kościsty2 & Wioletta Sośnicka 2 Received: 7 March 2016 /Accepted: 20 July 2016 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract Every spring, many of amphibians are killed by ximately 20 % from the rural and semi-urban sites. In partic- motor vehicles on roads. These road-killed animals can be ular, we found hypertrophic bone cells, misaligned intercellu- used as valuable material for non-invasive studies showing lar substance, and irregular outer edges of bones. We suggest the effect of environmental pollution on amphibian popula- that these malformations are caused by different pollution, e.g. tions. The aims of our research were to check whether the with heavy metals. phalanges of road-killed toads may be useful as material for histological analysis, and whether various degrees of human Keywords Amphibians . Phalangeal bone . Poland . impact influence the level in bone abnormalities in the com- Pollution . Roadkilling . Skeletochronology . Urban area mon toad. We also examined whether the sex and age struc- ture of toads can differ significantly depending in the different sites. We chose three toad breeding sites where road-killed Introduction individuals had been observed: near the centre of a city, the outskirts of a city, and a rural site. We collected dead individ- Current knowledge widely indicates a direct relationship be- uals during spring migration in 2013. The sex of each individ- tween anthropogenic pressures and the deteriorating environ- ual was determined and the toes were used to determine age mental state and/or global extinction of amphibian popula- using the skeletochronology method. While performing age tions (Blaustein and Johanson 2003; Collins and Storfer estimates, we looked for abnormalities in relation to normal 2003; Stuart et al. 2005). Negative impacts include direct kill- bone tissue structure. In urban site, females dominate males ing (Santos et al. 2015), destruction of habitats (Denoël 2012), (sex ratio 2.6:1), but in populations from rural and semi-urban and poisoning of the environment (Egea-Serrano et al. 2012). sites, sex ratio was reverse (1:2.2 and 1:1.4, respectively). In Europe, many amphibian populations are threatened However, we did not find any significant differences between (Temple and Cox 2009;BonkandPabijan2010;Denoël age structure of all populations (average age of each popula- 2012; Kaczmarek et al. 2015). In terms of the challenge of tion: approximately 4 years). We observed abnormalities in preventing these negative processes, it is necessary to develop more than 80 % of all toads from the city, compared to appro techniques for detecting disorders in natural processes and changes in the environment and to study their impact on am- phibians (Egea-Serrano et al. 2012). Research on the effects of Responsible editor: Thomas Braunbeck chemicals on the development and survival of tadpoles have been carried out in laboratories around the world (Skei and * Krzysztof Kolenda Dolmen 2006; Hayes et al. 2010b; Distel and Boone 2011; [email protected] Orton and Routledge 2011). Impact of pollution on amphib- ians, encompassing pathology and histological analysis, is 1 Institute of Zoology, Poznan University of Life Sciences, Wojska usually based on captured living adults. However, these stud- Polskiego 71 C, 60-625 Poznań,Poland ies are controversial, raising ethical issues, as they make it 2 Department of Vertebrate Biology and Conservation, University of necessary to capture and kill adult individuals (Söderman Wroclaw, Sienkiewicza 21, 50-335 Wrocław, Poland et al. 2007; Dmowski et al. 2015). Therefore, this kind of Environ Sci Pollut Res survey is not as frequent as research on tadpoles or laboratory histological analysis, and whether various degrees of human research. Considering that over 30 % of amphibian species are impact (urban, semi-urban and rural localities) influence the threatened with extinction, the attention of researchers is being level in bone abnormalities in the common toad. Our hypoth- directed toward non-invasive methods (Simon et al. 2009, esis assumes that toads occurring at an urban site are more 2012; Orton et al. 2014). The road mortality of vertebrates prone to the formation of anomalies in bone tissue than those offers great opportunities for obtaining material for further from rural localities. We also examined whether the sex and research (D’Amico et al. 2015; Santos et al. 2015), including age structure of toads can differ significantly depending in the studies on bioindication (Simon et al. 2012). For instance, different sites. road-killed toads were used in research on heavy metals absorbed by bone tissues (Simon et al. 2009, 2012). The accumulation of contamination, e.g. heavy metals or Material and methods biogenic compounds, in amphibians’ body organs and tissues, and its impact on their physiology and behaviour are well We chose three breeding sites of the common toad that known (Huey and Beitinger 1980; Lefcort et al. 1997; Rouse characterised by varied in the degree of urbanisation and pol- et al. 1999; Greulich and Pflugmacher 2003;Dobrovoljcetal. lution. During the site selection, we analysed the use of catch- 2012; Egea-Serrano et al. 2012). Unfortunately, there is still ment basin, in particular the ratio between the forest/tree cover little knowledge about the effect of these contaminants on life with open green area compared to the paved surfaces (parking history traits and recruitment of amphibians (Rowe et al. 2001; lots, railroad, road) with buildings or industrial plants (Fig. 1.). Hayes et al. 2010a). Some studies exhibit an enhanced asso- We evaluated the characteristics of the surface runoff which is ciation between the occurrence of body malformation (e.g. reflected in the accumulation of pollutants. Site 1.—the most missing or extra limbs, limb deformities) in amphibians and polluted urban site was ‘Kajka’, situated near the center of the the increasing land use in human-associated (Blaustein and Poznań city (52.2518° N, 16.5910° E). In the immediate vi- Johanson 2003; Taylor et al. 2005; but see Ballengée and cinity, there are located an illegal settlement and degraded Sessions 2009). allotment gardens without sanitary sewer lines. Furthermore, Common species with wide distributions are useful for re- there are two railway lines, and on the east, there is a forest search, as it is relatively easy to obtain sufficiently large sam- area (approximately 0.5 km from the pond). In ‘Kajka’ site, ples and to conduct research on a large spatial scale (Sparks there is a large proportion of industrial plants in the catchment et al. 2007). In Europe, including Poland, one of the most basin. The pond and surrounding settlement are contaminated widespread species, but also one of the most vulnerable to by factory halls and storage sites located in the vicinity. road mortality, is the common toad Bufo bufo (Głowaciński Presence of heavy metals and petroleum hydrocarbons have and Rafiński 2003;Elzanowskietal.2009; Temple and Cox been revealed in sediments which pose a threat for aquatic 2009). Moreover, this species is used with increasingly fre- environment (Grabia 2013). Occasionally, mass fish deaths quency in attempts to assess the state of environmental pollu- are observed (Sołtysiak 2013). Site 2.—semi-urban site was tion (Orton and Routledge 2011; Dobrovoljc et al. 2012; ‘Krzesiny’ located in the southern periphery of the Poznań Simon et al. 2012; Orton et al. 2014; Dmowski et al. 2015; city (52.3370° N, 16.9795° E). In the nearest vicinity of the Pickford et al. 2015). Research in urban areas has shown that pond, there are farmlands, meadows, fallow lands and small the number of sites occupied by amphibians, including com- forest. Among the anthropogenic structures, we distinguished mon toads, has decreased slightly (Budzik et al. 2013; railways, roads, a military air base and a few houses—arem- Kaczmarek et al. 2015). A similar situation is observed in nant of the old farms. On the east, the railway line forms a less-urbanised habitats (Orłowski 2007;Beebee2014). This barrier between the surrounding area of toads’ breeding site may be caused not only by road mortality and habitat loss but and the area occupied by residential houses—the developed also by high levels of water and soil pollution which pene- area. There is no direct discharge of water surface to the pond, trates into amphibians’ bodies and contributes to increasing but in the whole area, there are drains with the system of wells their mortality rates and reducing their level of fitness. B. bufo which causes water seepage. Aquatic vegetation is systemat- exhibits a broad range of environmental tolerances and there- ically removed every year. Site 3.—the rural site, natural veg- fore may be exposed to the influence of various substances etation (meadows) and a pond located in the forest, are situat- that disrupt its development, particularly in anthropogenic en- ed near the Owiesno village (50.6623° N, 16.7034° E). The vironments (Dmowski et al. 2015; Pickford et al. 2015). To catchment area is similar to the natural environment with the the best of our knowledge, there are no data which demon- small watercourse flowing in the nearest vicinity of the breed- strate the appearance of pathological changes in the bones of ing site. A slight extensive farm and local road with little car amphibians inhabiting a polluted environments. traffic is located within a radius of 1000 m is only. We investigated two main aims of this study: whether the Very clean water in the pond promotes the development phalanges of road-killed toads may be useful as material for of freshwater plants. Environ Sci Pollut Res Fig.
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