A systematic review of trace elements in the tissues of bats (Chiroptera).

Bats constitute about 22% of known mammal species; they have various ecological roles and provide many ecosystem services. Bats suffer from several threats caused by anthropization, including exposure to toxic metals and metalloids. We analyzed 75 papers in a systematic literature review to investigate how species, diet, and tissue type impact bioaccumulation. Most studies documented element accumulation in fur, liver, and kidney; at least 36 metals and metalloids have been measured in bat tissues, among the most studied were mercury and zinc. Comparisons with known toxicological thresholds for other mammals showed concerning values for mercury and zinc in bat hair, lead and some essential metals in liver, and iron and calcium in kidneys. Moreover, accumulation patterns in tissues differed depending on bat diet: insectivorous bats showed higher metal concentrations in fur than in liver and kidney while frugivorous species showed higher values in liver and kidney than in fur. Finally, among the bat species that have been studied in more than two papers, the big brown bat (Eptesicus fuscus) show values of mercury in hair and copper in liver that exceed the known thresholds; as does copper in the liver of the little brown bat (Myotis lucifugus). Most studies have been conducted in temperate North America and Eurasia, areas with the lowest bat species diversity; there is a paucity of data on tropical bat species. This review points out several information gaps in the understanding of metal contamination in bats, including a lack of measured toxicity thresholds specific for bat tissues. Data on trace element bioaccumulation and its associated health effects on bats is important for conservation of bat species, many of which are threatened.

Trace Element Bioaccumulation in Stone Curlew (Burhinus oedicnemus, Linnaeus, 1758): A Case Study from Sicily (Italy).

: The study aimed to highlight the degree of trace element contamination along three sites of Sicily: the Magnisi peninsula (MP), located in proximity to the Augusta-Priolo-Melilli petrochemical plant; the Ragusa agro-ecosystem (RA), characterized by a rural landscape; and the Gela plain (GP), characterized by intensive agriculture and a disused petrochemical plant. We collected biological samples (abraded back feathers and blood) of the Stone Curlew (Burhinus oedicnemus Linnaeus, 1758) as well as soil samples to determine the trace elements concentrations of As, Cd, Co, Cr, Cu, Hg, Mn, Ni, Pb, Zn, Se and V using ICP-MS analysis. The results found for the three sites show different trends of accumulation, which depend on the different management and geological characteristics of the areas. The Gela plain and Magnisi peninsula showed a higher degree of contamination (As, Co, Cu, Mn and Se for the Gela plain; Pb and Hg for the Magnisi peninsula). Nevertheless, no critical values were found for either the environment-if the results are compared with the legal limits fixed by the Legislative Decree No. 152/2006, approving the Code on the Environment-or for living organisms-if the results are compared with the toxicological thresholds for birds, especially if the short-term exposure results from the blood values are considered. Only the Se levels in animal blood from the RA and GP were found slightly higher than the minimum level required in bird diets. The positive scenario can be attributed on the one hand to the interruptions of emissions of the Gela refinery around 5 years ago, and on the other hand to the more intense and strict controls that are implemented in the area surrounding the petrochemical pole of Augusta-Priolo-Melilli.

Interspecific variation in the spatially-explicit risks of trace metals to songbirds.

Many wild animals can be adversely affected by trace metals around point sources but little is known about the risks to birds across their ranges. Trace metals in the soil are ubiquitously, if heterogeneously distributed, across the world due to natural and anthropogenic sources. Here, we built, parameterized and applied a spatially explicit modelling framework to determine the risks of soil-associated metals to 30 invertebrate-consuming passerine species across their spatial distribution in England and Wales. The model uses a risk characterization approach to assess the risks of soil-associated metals. Various monitoring datasets were used as input parameters: soil metal concentrations in England and Wales, bird spatial distribution; bird diet, bioaccumulation and toxicity data were extracted from the literature. Our model highlights significant differences in toxicity risks from Cd, Cu, Pb and Zn across the UK distributions of different species; Pb and Zn posed risks to all species across most of species' distributions, with more localised risks to some species of conservation concern from Cd and Cu. No single taxa of invertebrate prey drove avian exposure to metal toxicity. Adults were found to be at higher risk from Pb and Zn toxicity across their distributions than nestlings. This risk was partially driven by diet, with age differences in diets identified. Our spatially explicit model allowed us to identify areas of each species' national distribution in which the population was at risk. Overall, we determined that for all species studied an average of 32.7 ±â€¯0.2%, 8.0 ±â€¯0.1%, 86.1 ±â€¯0.1% and 93.2 ±â€¯0.1% of the songbird spatial distributions in the UK were characterized at risk of Cd, Cu, Pb and Zn, respectively. Despite some limitations, our spatially explicit model helps in understanding the risks of metals to wildlife and provides an efficient method of prioritising areas, contaminants and species for environmental risk assessments. The model could be further evaluated using a targeted monitoring dataset of metal concentration in bird tissues. Our model can assess and communicate to stakeholders the potential risks of environmental contaminants to wildlife species at a national and potentially international scale.

A national level assessment of metal contamination in bats.

Many populations of bat species across the globe are declining, with chemical contamination one of many potential stressors implicated in these demographic changes. Metals still contaminate a wide range of habitats, but the risks to bats remain poorly understood. This study is the first to present a national scale assessment of toxic metal (Cd, Pb) and essential trace metal (Cu, Zn) concentrations in bats. Metal concentrations in tissues (kidneys, liver, stomach -stomach content, bones and fur) were measured in 193 Pipistrellus sp. in England and Wales using ICP-MS, and compared to critical toxic concentrations for small mammals. The concentrations of metals determined in bat tissues were generally lower than those reported elsewhere. Strong positive associations were found between concentrations in tissues for a given metal (liver and kidneys for Cd, Cu and Pb; stomach and fur and fur and bones for Pb), suggesting recent as well as long term exposure to these contaminants. In addition, positive correlations between concentrations of different metals in the same tissues (Cd and Zn, Cu and Zn, Cd and Pb, Pb and Zn) suggest a co-exposure of metals to bats. Approximately 21% of the bats sampled contained residues of at least one metal at concentrations high enough to elicit toxic effects (associated with kidney damage), or to be above the upper level measured in other mammal species. Pb was found to pose the greatest risk (with 7-11% of the bats containing concentrations of toxicological concern), followed by Cu (4-9%), Zn (0.5-5.2%) and Cd (0%). Our data suggest that leaching of metals into our storage matrix, formaldehyde, may have occurred, especially for Cu. The overall findings suggest that metal contamination is an environmental stressor affecting bat populations, and that further research is needed into the direct links between metal contamination and bat population declines worldwide.

Fur: A non-invasive approach to monitor metal exposure in bats.

This paper presents a novel assessment of the use of fur as a non-invasive proxy to biomonitor metal contamination in insectivorous bats. Concentrations of metals (cadmium, copper, lead and zinc) were measured using ICP-MS in tissues (kidneys, liver, stomach and stomach content, bones and fur) obtained from 193 Pipistrellus pipistrellus/pygmaeus bats. The bats were collected across a gradient of metal pollution in England and Wales. The utility of small samples of fur as an indicator of metal exposure from the environment was demonstrated with strong relationships obtained between the concentrations of non-essential metals in fur with concentrations in stomach content, kidneys, liver and bones. Stronger relationships were observed for non-essential metals than for essential metals. Fur analyses might therefore be a useful non-invasive proxy for understanding recent, as well as long term and chronic, metal exposure of live animals. The use of fur may provide valuable information on the level of endogenous metal exposure and contamination of bat populations and communities.

Interspecies variation in the risks of metals to bats.

A modeling framework was used to assess the risk of four metals to UK bat species. Eight species of bats were predicted to be "at risk" from one or more of the metals in over 5% of their ranges. Species differed significantly in their predicted risk. Contamination by Pb was found to pose the greatest risk, followed by Cu, Cd and Zn. A sensitivity analysis identified the proportion of invertebrates ingested as most important in determining the risk. We then compared the model predictions with a large dataset of metals concentrations in the tissues (liver, kidney) of Pipistrellus sp. from across England and Wales. Bats found in areas predicted to be the most "at risk" contained higher metal concentrations in their tissues than those found in areas predicted "not at risk" by the model. Our spatially explicit modeling framework provides a useful tool for further environmental risk assessment studies for wildlife species.

Implications of in vitro bioaccessibility differences for the assessment of risks of metals to bats.

Food chain modeling is often used to assess the risks of chemical contaminants to wildlife. In modeling efforts, bioaccessibility from different dietary components is assumed to be similar. The present study explored potential differences in the in vitro bioaccessibility of metals from a range of insect orders, which are common components of the diet of insectivorous bats, and assessed the implications of this for environmental exposure assessment. Bioaccessibility of metals was assessed using an in vitro gastric model simulating gastric and intestinal conditions of insectivorous bats. In vitro-derived metal bioaccessibility was found to differ significantly across insect orders. Bioaccessibility was found to be greatest in Coleoptera, followed by Lepidoptera and Diptera. To establish the implications for risk assessment, a spatially explicit risk model was employed that included and excluded in vitro bioaccessibility data; to examine the daily oral exposure of metals to 14 bat species. The results show that when bioaccessibility data are included in the model, metal exposure predictions across species are changed and that the ranking of bat species, in terms of metal exposure, are altered. The authors recommend that in vitro bioaccessibility data begin to be employed when establishing the risks of contaminants to wildlife species.

A spatially-based modeling framework for assessing the risks of soil-associated metals to bats.

Populations of some species of bats are declining in some regions of Europe. These declines are probably due to a range of pressures, including climate change, urbanization and exposure to toxins such as metals. This paper describes the development, paramaterisation and application of a spatially explicit modeling framework to predict the risks of soil-associated metals (lead, copper, zinc and cadmium) to bat health. Around 5.9% of areas where bats reside were predicted to have lead levels that pose a risk to bat health. For copper, this value was 2.8%, for cadmium it was 0.6% and for zinc 0.5%. Further work is therefore warranted to explore the impacts of soil-associated metals on bat populations in the UK.