Emissions from smelting not only contaminate water and soil with metals, but also induce extensive forest dieback and changes in resource availability and microclimate. The relative effects of such co-occurring stressors are often unknown, but this information is imperative in developing targeted restoration strategies. We assessed the role and relative effects of structural alterations of terrestrial habitat and metal pollution caused by century-long smelting operations on amphibian and reptile communities by collecting environmental and time- and area-standardized multivariate abundance data along three spatially replicated impact gradients. Overall, species richness, diversity, and abundance declined progressively with increasing levels of metals (As, Cu, and Ni) and soil temperature (T(s)) and decreasing canopy cover, amount of coarse woody debris (CWD), and relative humidity (RH). The composite habitat variable (which included canopy cover, CWD, T(s), and RH) was more strongly associated with most response metrics than the composite metal variable (As, Cu, and Ni), and canopy cover alone explained 19-74% of the variance. Moreover, species that use terrestrial habitat for specific behaviors (e.g., hibernation, dispersal), especially forest-dependent species, were more severely affected than largely aquatic species. These results suggest that structural alterations of terrestrial habitat and concomitant changes in the resource availability and microclimate have stronger effects than metal pollution per se. Furthermore, much of the variation in response metrics was explained by the joint action of several environmental variables, implying synergistic effects (e.g., exacerbation of metal toxicity by elevated temperatures in sites with reduced canopy cover). We thus argue that the restoration of terrestrial habitat conditions is a key to successful recovery of herpetofauna communities in smelting-altered landscapes.
Pollution can affect wildlife directly through toxicity and indirectly through changes in biotic and abiotic factors, however, how these mechanisms interact in affecting free‐ranging animals remains poorly understood. By examining effects on individual fitness proxies, we aimed to determine the mechanisms behind documented amphibian and reptile declines in barren landscapes where vegetation was nearly decimated due to atmospheric metal and sulfur deposition from smelting operations in Sudbury, Ontario, Canada. We examined individual characteristics of snakes (Thamnophis sirtalis, Storeria occipitomaculata) and frogs (Lithobates clamitans, L. pipiens, L. septentrionalis) in replicated barren and reference sites, including standard metabolic rates (in snakes), body condition (all species), female reproductive status (snakes), limb deformity (frogs), and fluctuating asymmetry (all species). Frogs in barren sites (except L. septentrionalis) were in poor body condition, and all but one case of limb deformities in frogs were found in barren sites. However, neither frogs nor snakes exhibited elevated frequency of fluctuating asymmetry in barren sites. Standard metabolic rates (SMR) were not elevated in either snake species, suggesting that metal toxicity does not present an energetic burden. Instead, female T. sirtalis from barren sites exhibited lower SMR and were in poor body condition, which is a predicted response to reduced food intake. By contrast, SMR and body condition of S. occipitomaculata were not different between barren and reference sites. While physiological responses differed between T. sirtalis and S. occipitomaculata, both species exhibited lower reproductive rates (proportion of pregnant females) in barren sites compared to reference sites. Thus, energy deficiency may explain reduced reproduction in T. sirtalis while reduced availability of suitable gestation microhabitat may be a limiting factor for S. occipitomaculata. Populations in smelting‐impacted habitats include individuals with potentially compromised fitness. The low values of our measured fitness proxies appear to have resulted from pollution‐induced changes in biotic and abiotic factors, in addition to (for frogs) or rather than (for snakes) from the direct toxicity. These results suggest that impact assessment based solely on toxicological data and species distributions can underestimate the full impacts of pollution, highlighting the need for integrated examination at multiple levels of biological organization.
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