Abstract

Background/ObjectiveExposure to environmental contaminants may result in reduced reproductive success and long-lasting population declines in vertebrates. Emerging data from laboratory studies on model species suggest that certain life-stages, such as development, should be of special concern. However, detailed investigations of long-term consequences of developmental exposure to environmental chemicals on breeding performance are currently lacking in wild populations of long-lived vertebrates. Here, we studied how the developmental exposure to a mine spill (Aznalcóllar, SW Spain, April 1998) may affect fitness under natural conditions in a long-lived bird, the White Stork (Ciconia ciconia).MethodologyThe reproductive performance of individually-banded storks that were or not developmentally exposed to the spill (i.e. hatched before or after the spill) was compared when these individuals were simultaneously breeding during the seven years after the spill occurred (1999–2005).Principal FindingsFemale storks developmentally exposed to the spill experienced a premature breeding senescence compared with their non-developmentally exposed counterparts, doing so after departing from an unusually higher productivity in their early reproductive life (non-developmentally exposed females: 0.5±0.33SE fledglings/year at 3-yr old vs. 1.38±0.31SE at 6–7 yr old; developmentally exposed females: 1.5±0.30SE fledglings/year at 3-yr old vs. 0.86±0.25SE at 6–7 yr old).Conclusions/SignificanceFollowing life-history theory, we propose that costly sub-lethal effects reported in stork nestlings after low-level exposure to the spill-derived contaminants might play an important role in shaping this pattern of reproduction, with a clear potential impact on population dynamics. Overall, our study provides evidence that environmental disasters can have long-term, multigenerational consequences on wildlife, particularly when affecting developing individuals, and warns about the risk of widespread low-level contamination in realistic scenarios.

Highlights

  • Long-term consequences of exposure to environmental contaminants upon individual performance and wildlife population dynamics have long been a focus of research interest for several disciplines including ecotoxicology, endocrinology and population biology [1,2,3,4,5,6]

  • Conclusions/Significance: Following life-history theory, we propose that costly sub-lethal effects reported in stork nestlings after low-level exposure to the spill-derived contaminants might play an important role in shaping this pattern of reproduction, with a clear potential impact on population dynamics

  • The diversity of animals’ life histories and of environmental stressors they usually have to deal with in nature, introduces the possibility of specific responses to contaminants under field conditions that may not be evident in controlled laboratory experiments [15,16]

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Summary

Introduction

Long-term consequences of exposure to environmental contaminants upon individual performance and wildlife population dynamics have long been a focus of research interest for several disciplines including ecotoxicology, endocrinology (endocrine disruption) and population biology [1,2,3,4,5,6] Developmental exposure to these chemicals, even at low levels, may be detrimental, with potential long-term effects on reproduction and individual fitness [7,8,9]. It is often the case that no previous studies have been conducted in the affected areas and on species of concern [20], still less that long-term monitoring of individuals has been performed These data are essential to evaluating some long-term effects of the exposure to contaminants, especially of those occurring during critical life cycle stages, such as development, which may have profound impacts on fitness only detectable with longitudinal studies at individual level

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