Bats as bioindicators of heavy metal pollution: history and prospect

Bats today face a number of important threats, including that of heavy metal exposure. While the numerous adverse health effects of heavy metals have long been documented, exposure to heavy metal pollution continues, and is even increasing in some parts of the world. The eleven heavy metal elements of highest wildlife protection concern are arsenic, cadmium, cobalt, chromium, copper, mercury, manganese, nickel, lead, tin and thallium. This paper reviews 52 studies reporting on heavy metal concentrations in bats, their organs and guano, and aims to provide an overview of heavy metal research on wild bat populations, and particularly its temporal, geographic, methodological and biological aspects.The published data are biased both temporally and spatially, with the greatest number of articles published over the last decade. While most studies reporting on heavy metal contamination have come from North America and Europe, these are generally restricted to one or two reports per country/state. General trend analysis of heavy metal content in bats is not possible due to variation in the data and the analysis of stratigraphically dated guano deposits provides inconsistent results. Moreover, variability in heavy metal content observed in bat bodies is influenced by background levels and a direct comparison of results between geographically distant areas is, therefore problematic. Comparison of contaminated and reference localities at a regional scale is useful and is regularly used. From a methodological point of view, the determination of heavy metal concentration in tissues may be limited by the typically small sample sizes available. Heavy metals have been analyzed in a range of matrices, with the four most sampled types (liver, kidney, whole body/carcass and guano) and the actual number of compounds analyzed gradually increasing over time as more sophisticated and precise instrumentation are developed. Non-lethal sampling methods are increasingly used for monitoring as these have minimal impact on threatened and highly protected animals. In total, heavy metal content has been studied in 65 bat species, though the species, sex, age, year of collection and locality varies widely with no clear pattern. Only four species (big brown bat Eptesicus fuscus, gray bat Myotis grisescens, greater mouse-eared bat Myotis myotis and common pipistrelle Pipistrellus pipistrellus sensu lato) have been analyzed more than five times, and only five heavy metals (cadmium, chromium, copper, lead, and zinc) have been measured in fructivorous/nectarivorous species. Insectivorous bats have lower mean contaminant values in tissues than both fructivorous/nectarivorous species and guano. While exposure pathway may have influenced differences between the various food guilds, lowered bioavailability of heavy metals from digested food displaying lower bioaccumulation factors may account for differences observed between guano and other types of samples.While the number of articles confirming direct adverse effects and toxicity of heavy metals on bats is low some impacts and poisoning cases have been documented, including hepatopathy, DNA damage, hemochromatosis, renal inclusion bodies, ascending paralysis, and changes in cholinergic functions. Moreover, results suggest that the effects of chronic sub-lethal exposure to heavy metal contamination may be a more important threat to bat populations as bats under natural environmental conditions are frequently exposed to multiple anthropogenic stressors at the same time. One of the main challenges facing bat ecotoxicology today is the preparation of standardized monitoring programs using modern analytical technologies that offer more precise data on heavy metal contamination.