Heavy metal pollution exposure affects egg coloration but not male provisioning effort in the pied flycatcher Ficedula hypoleuca

Heavy metal pollution is known to negatively affect numerous traits in birds, including foraging, metabolism, immunity, and reproductive success. In this study, our primary aim was to assess the impact of metal pollution exposure on the visual appearance of the pied flycatcher (Ficedula hypoleuca) eggs. Specifically, we focused on blue-green biliverdin-based coloration, a trait expected to function as a signal of female quality to males. In line with the sexually selected egg coloration (SSEC) hypothesis, which posits that males respond to more intensely colored eggs by increasing their provisioning effort, our second objective was to investigate whether metal pollution exposure affects this specific signaling mechanism and subsequent male behavior. Our results showed that although coloration did not correlate with female quality or male provisioning effort, egg blue-green coloration decreased in polluted areas compared to non-polluted control areas. Our analysis of reflectance data revealed that this difference was due to an increased ultraviolet reflectance of eggs from polluted areas, likely caused by changes in eggshell microstructure (e.g. porosity). We therefore propose that metal pollution exposure may compromise crucial color signals of bird eggs. Avian visual modeling indicated that eggs laid by different flycatcher females are generally very similar, making discrimination by males challenging and perhaps impossible especially in dark cavities. Overall, our results suggest that the SSEC hypothesis may lack adaptive relevance for the pied flycatcher in Northern Europe, even in environments influenced by anthropogenic activities.

众所周知，重金属污染会对鸟类的多项生理与行为性状产生负面影响，涵盖觅食能力、新陈代谢、免疫功能以及繁殖成功率。本研究的首要目标为评估重金属污染暴露对斑姬鹟（pied flycatcher，*Ficedula hypoleuca*）卵外观视觉特征的影响。具体而言，本研究聚焦于以胆绿素（biliverdin）为基础的蓝绿色着色——该性状被认为可作为雌性个体向雄性传递自身质量的信号。本研究契合性选择卵色（sexually selected egg coloration, SSEC）假说，该假说提出雄性会对颜色更浓郁的卵增加育雏投入；我们的第二项目标为探究重金属污染暴露是否会影响这一特定的信号传递机制，以及后续的雄性行为。研究结果显示，尽管卵的着色与雌性质量或雄性育雏投入并无关联，但相较于未受污染的对照区域，污染区域内的卵蓝绿色着色程度有所降低。我们对反射光谱数据的分析表明，这一差异源于污染区域卵的紫外反射率升高，该现象或由蛋壳微观结构（如孔隙度）的改变所引发。据此我们提出，重金属污染暴露可能会损害鸟类卵的关键颜色信号。鸟类视觉模型分析显示，不同雌性斑姬鹟所产的卵外观整体极为相似，这使得雄性难以甚至无法区分这些卵，在黑暗的树洞巢穴中这一问题尤为突出。总体而言，本研究结果表明，性选择卵色（SSEC）假说或许并不具备北欧地区斑姬鹟种群的适应性意义，即便在受人类活动影响的环境中亦是如此。