Organisms born into the same contaminated environment as their parents can be exposed both maternally and environmentally to contaminants, potentially placing them at greater risk of adverse effects than when exposed via either of the two pathways independently. We examined whether embryonic exposure to maternally derived mercury (Hg) interacts with dietary exposure to negatively influence larval development in American toads ( Bufo americanus ). We collected eggs from breeding pairs at reference and Hg-contaminated sites and monitored performance, development, and survival of larvae fed three experimental Hg diets (total Hg, 0.01, 2.5, and 10 μg/g). The negative sublethal effects of maternal and/or dietary Hg manifested differently, but maternal Hg exposure had a greater overall influence on offspring health than dietary exposure. However, the combination of sublethal effects of the two exposure routes interacted with lethal consequences; larvae exposed to maternal Hg and high dietary Hg experienced 50% greater mortality compared to larvae from reference mothers fed the control diet. This study is the first to demonstrate that the latent effects of maternally transferred contaminants may be exacerbated by further exposure later in ontogeny, findings that may have important implications for both wildlife and human health.

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Amphibians with biphasic life histories occupy aquatic and terrestrial habitats at different times in their lives, leading to a double jeopardy of contaminant risk in both habitats. The present study examines individual and interactive effects of mercury exposure to terrestrial adults and aquatic larvae on fitness-related traits of American toads, Bufo americanus. Eggs from reference mothers or contaminated mothers were allowed to hatch and larvae were fed diets of either no added Hg or 2.5 or 10 µg/g total Hg (dry wt). Both dietary and maternal Hg had adverse effects on developing larvae, but there was no interaction between these factors. Dietary Hg had a marginal effect of decreased survival with increasing Hg in the diet. Animals from Hg-exposed mothers weighed 14% less than those from reference mothers, and size at metamorphosis was directly correlated with hopping performance. Animals from Hg-exposed mothers also took longer to complete metamorphosis and had 2.5 times the prevalence of spinal malformations compared with those from reference mothers. Results of the present study demonstrate that amphibians do indeed face a double jeopardy of contaminant exposure stemming from terrestrial and aquatic environments, because both exposure pathways adversely affected developing offspring. The present study also demonstrates that all possible routes of exposure over an organism's life history must be examined to provide a comprehensive picture of the ecological consequences of habitat contamination.

There is growing recognition of the ways in which maternal effects can influence offspring size, physiological performance, and survival. Additionally, environmental contaminants increasingly act as stressors in maternal environments, possibly leading to maternal effects on subsequent offspring. Thus, it is important to determine whether contaminants and other stressors can contribute to maternal effects, particularly under varied ecological conditions that encompass the range under which offspring develop. We used aquatic mesocosms to determine whether maternal effects of mercury (Hg) exposure shape offspring phenotype in the American toad (Bufo americanus) in the presence or absence of larval predators (dragonfly naiads). We found significant maternal effects of Hg exposure and significant effects of predators on several offspring traits, but there was little evidence that maternal effects altered offspring interactions with predators. Offspring from Hg-exposed mothers were 18% smaller than those of reference mothers. Offspring reared with predators were 23% smaller at metamorphosis than those reared without predators. There was also evidence of reduced larval survival when larvae were reared with predators, but this was independent of maternal effects. Additionally, 5 times more larvae had spinal malformations when reared without predators, suggesting selective predation of malformed larvae by predators. Lastly, we found a significant negative correlation between offspring survival and algal density in mesocosms, indicating a role for top-down effects of predators on periphyton communities. Our results demonstrate that maternal exposure to an environmental stressor can induce phenotypic responses in offspring in a direction similar to that produced by direct exposure of offspring to predators.Electronic supplementary materialThe online version of this article (doi:10.1007/s00442-011-1961-9) contains supplementary material, which is available to authorized users.