Stress induced by heavy metals on breeding of magpie (Pica pica) from central Iran

https://doi.org/10.1016/j.ecoenv.2017.04.047Get rights and content

Highlights

  • Heavy metals were measured in magpie's egg, eggshell, nestling feather and excrement.

  • Effects of HMs contamination on breeding performance of magpie were investigated.

  • Higher HMs concentrations were observed for samples collected from brick kiln site.

  • Higher concentration of Zn, Pb and Cd were observed for unhatched than hatched eggs.

  • Brick kilns emissions may cause stress to magpie lead to laying poor quality eggs.

Abstract

The aim of this study was to address the impacts of some heavy metals (Cd, Pb, Zn, Ni and Cu) contamination on laying behavior, egg quality and breeding performance of Pica pica in north of Isfahan Province, Iran. During the breeding season of 2013, magpie's egg content and eggshell as well as nestling excrements and feathers were collected and total concentrations of heavy metals were measured by ICP-OES. Except for Zn in nestling feathers, the significantly higher concentrations of heavy metals were observed in nestling excrements than other samples. Also, comparison of heavy metals concentrations in egg content and eggshell showed that egg content had significantly higher concentrations of Zn and Pb, instead eggshell had significantly higher amount of Cu and Cd. Except for Cu, all heavy metals concentrations in eggshell had a negative relationship with morphological characters; and also concentration of Cu in egg content showed a significantly negative correlation with egg weight and volume. The most of heavy metals in nestling feathers and excrements had strongly positive correlations with each other. Also all heavy metals levels in eggshell and egg content had significantly positive correlations (except for Cu). Unhatched eggs had significantly lower weight but also greater levels of Zn, Cd, and Pb, than randomly collected eggs. No significant differences were observed for morphometric measurements of eggs between different sites, however, a decreased gradient was observed in egg volume toward the brick kiln site. Samples collected in brick kiln site accumulated higher concentrations of heavy metals than other sites. Although numbers of clutch size in brick kiln site were significantly higher than other sites, however, other breeding variable were lower than other sites. It can be suggested that ecosystem contamination may be caused to decrease the reproduction rate of Pica pica in brick kiln, probably by laying more poor quality eggs per clutch and nestling mortality.

Introduction

Global concerns about long-term impacts of heavy metals (HMs) as environmental contaminants have been increased in the recent years (Abbasi et al., 2015, Burger et al., 2004). Maintaining healthy ecosystem provides the human welfare and living organisms within an ecosystem. Of realizing this ideal requires the identification of contaminants in the ecosystem and environment planning and management (Burger et al., 2004). HMs have harmful effects on various organizational levels, so that at the highest level can affect the population levels (Dauwe et al., 2004). As in numerous studies mentioned that environmental contamination can cause to the thinning eggshells and ultimately disrupt the reproduction of birds (Dauwe et al., 2004, Eeva and Lehikoinen, 1995; Ratcliffe, 1967). Eggshell thinning can negatively affect the breeding success because thinner eggshells may break during incubation (Dauwe et al., 2004). Exposure to HMs can also have a negative effect on egg size of birds as showed by Eeva and Lehikoinen (1995); this may disrupt the early growth and nestling survival (Dauwe et al., 2004). In environmental monitoring studies, the analysis of HMs in soil, water and even air alone is not sufficient to evaluate the potential effects of HMs to resident people and wildlife (Talmage and Walton, 1991, Zarrintab and Mirzaei, 2017). Avian species are sensitive to anthropogenic contamination, and are useful bioindicators of metal contaminants (Battaglia et al., 2005, Fu et al., 2014, Varela et al., 2016). So, measurement of HMs in birds can indicate a better view of the risks to human than their measurement in physical environment, plants and invertebrates (Zarrintab et al., 2016). However, there are doubts about the effectiveness of a certain regions on the HMs exposure in the birds because birds can fly and exposed to HMs in the other areas. That is why many researchers are interested in investigation of HMs in eggs of laying birds and/or their chicks. So that adult female can reduce body burden of HMs through the excretion in their eggs (Fu et al., 2014). Hence, data obtained from HMs levels in bird's eggs can provide us useful information about exposure to chemicals in laying birds (Lam et al., 2005). Since the most of breeding females spend a lot of time before laying around the nest to get their primary resources for egg production (and so any related contaminants), so, eggs of birds are appropriate for monitoring of local exposure to contaminants (Lam et al., 2005). On the other hand, many biomonitoring studies of HMs in birds are focused on chickens, so that in some of them non-destructive sampling such as feathers and feces were used (e.g. Dauwe et al., 2000; Eeva et al., 2009), and in some others, destructive sampling with internal tissues were used (e.g. Berglund et al., 2010). Sampling from chickens is useful to get information from a limited time and territory, while the adult birds may accumulate HMs in a longer period or during migration (Berglund et al., 2011).

In order to have a continuous and regular monitoring of HMs, there is a pressing need to the development of non-destructive biomonitoring tools. So, increased demand for non-invasive methods in one hand and effective measurements of contaminants levels on the other hand have caused to the introduction and development of feathers, eggs, and feces as useful biomonitoring tools to assess the birds exposure (Fu et al., 2014).

One of the most important and industrial cities in central Iran is Aran-O-Bidgol City which various industries causing contaminants emissions in this region. As the comprehensive study of soil HMs contamination in Aran-O-Bidgol showed that there was HMs contamination in this region, and one of the main sources of HMs especially cadmium and lead were brick kilns (Ravankhah et al., 2017). Also, a biomonitoring study of HMs using magpie's feathers in this region showed that the birds collected from the industrial sites and brick kilns were at the greatest exposure to HMs (Zarrintab et al., 2016).

To our knowledge, in Iran, no data are available about HMs concentrations in eggs and nestling of an urban dwelling bird's; and also no studies investigated the effects of HMs on breeding success of an urban bird to monitor the urban environment. Hence, the magpie's eggs and nestling were selected as this species have suitable characteristics for urban biomonitoring of HMs (Zarrintab et al., 2016).

In the present study, HMs concentrations in egg content (EC), eggshells (ES), nestling feathers (NF) and nestling excrement (NE) of magpie from Aran-O-Bidgol City, were investigated for the first time. This study was conducted to investigate six objectives: 1) to compare the accumulation of HMs in different samples (ES, EC, NF and NE); 2) to evaluate the variation pattern of HMs concentrations in samples collected from different sampling sites; 3) to investigate the variation pattern of morphometric measurements of eggs collected from different sampling sites; 4) to investigate that is there any differences between morphometric measurements and HMs concentrations in randomly collected eggs (RCE) and unhatched eggs (UE) 5) whether is there a relationship between HMs concentration in different samples as well as in the eggs and their morphological characters and 6) to investigate the variation pattern of breeding success in different sampling sites.

Section snippets

Study area

This study was performed in Aran-O-Bidgol City located in central Iran at 50° 15ʹ-52° 29ʹ E and 33° 30ʹ-34° 27ʹ N. There are several anthropogenic contamination sources in around of the city that caused to emission of contaminants such as HMs to this region (Zarrintab et al., 2016). As in the recent study on soil contamination in this area, it was demonstrated that brick kilns were the most important emission sources of HMs specially Cd and Pb (Ravankhah et al., 2017). Due to presence of

Comparison of heavy metals concentrations among different samples

Comparisons of overall mean concentrations of HMs in different samples are presented in Fig. 2. The results showed that except for Zn in NF, all other HMs concentration were significantly higher in NE than other samples (p<0.05). So that, overall mean concentrations of HMs in different samples were calculated for Zn as: NF (174.35)>NE (132.43)>EC (50.31)>ES (21.26), for Cu were as NE (33.02)>NF (20.36)>ES (5.57)>EC (4.2), for Ni as: NE (1.7)>NF (0.55)>ES (0.49)>EC (0.38), for Cd as: NE

Heavy metals accumulation

Avian species are exposed to HMs in different ways. HMs entered into the bodies of birds and may be accumulated in their tissues; however, there are several routes to reduce HMs from the body of a bird including feces, feathers and eggs and eggshells (Fu et al., 2014). Although the HMs concentrations in different samples were varied for each HMs, however, except for Zn, most of HMs concentrations in the NE were significantly higher than concentrations in NF (p<0.05) (Fig. 1). Similar to these

Conclusion

This study suggested that bird's exposure to HMs may lead to the negative effects on breeding success and their nestlings. Our investigation showed that eggs collected in BK had lower weight but higher HMs concentrations than other sites; in line with this issue UE had a significant lower weight than RCE but had higher concentrations of non-essential HMs in both ES and EC. A significantly greater clutch size in BK was observed (it's may be because of higher stress to laying females in BK) but

Acknowledgements

This work was supported by University of Kashan (grant No. 573610). We thank Ms. Neda Ravankhah with her laboratory assistance and Mr. Mohammadsadegh Zarrintab for his help during field work. We are also thankful to Dr. Tapio Eeva from University of Turku, Finland for his valuable suggestions during field work. We are also indebted Aran-O-Bidgol Department of Environment specially Mr. Allahyar Dovlatkhah for providing facilities during sampling.

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