ECOTOXICOLOGY: MAMMALS
ANTEATERS, ARMADILLOS, AND SLOTHS
de Carvalho G. O., Meire R. O., Lino A. S., Yogui D. R., Desbiez A. L. J., Torres J. P. M., Malm O. (2021): Biomonitoring mercury contamination using fur from roadkilled giant anteaters. Chemosphere 270: 128644.
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The giant anteater (Myrmecophaga tridactyla) can occur in both preserved and anthropogenic environments in Brazilian biomes. The Cerrado biome, where the samples were collected, is considered one of the world’s biodiversity hotspots; however, a large part of it has been converted to pasture and agricultural land. In this environment, animals may be exposed to contaminants, such as mercury (Hg). Despite its immense biodiversity, there are few studies investigating Hg contamination in terrestrial mammals in Brazil. This study aimed to create a baseline for Hg levels in giant anteater fur and establish which biotic and abiotic variables can influence its concentration. Total Hg (THg) concentrations were determined by cold vapor atomic absorption spectrometry in 141 individuals sampled on highways between January and October 2017, in the state of Mato Grosso do Sul, Brazil. THg concentrations in fur ranged from 0.27 to 4.77 μg g −1. The decomposition stage of the carcasses and vehicular traffic volume on highways did not influence the THg concentrations. Juveniles presented lower THg concentrations than adults. A spatial pattern of higher concentrations in the eastern-southeastern region of the state was found, which could be related to anthropogenic impacts; however, no clear links have been established. The THg concentrations in giant anteaters’ fur seems higher than expected considering the trophic position of the species. Despite this, the range was in accordance with studies of other Brazilian terrestrial mammals and within safe threshold levels. This study indicates the potential of utilizing roadkilled fauna to monitor large-scale contamination in wildlife.
BATS
Flache L., Becker N. I., Kierdorf U., Czarnecki S., Düring R. A., Encarnação J. A. (2015): Hair samples as monitoring units for assessing metal exposure of bats: a new tool for risk assessment. Mammalian Biology 80: 178-181.
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Metals occur naturally and are ubiquitous in the Earth’s crust. In addition to their release from natural sources, larger amounts of metals enter the environment through use in diverse industries, and accumulate mostly in the pedosphere close to emission sources. Bat species foraging for prey insects in different cultural landscape types (urbanized areas, forests, agricultural areas, water bodies) may show site-specific trace metal concentrations, partly due to variations in exposure among habitats. As all European bat species are protected, a non-invasive method is required to monitor their exposure to potentially toxic metals in their foraging habitats. The analysis of hair samples offers such a possibility. In the present study, hair samples of Myotis bechsteinii, Myotis daubentonii, Myotis myotis and Pipistrellus pipistrellus were analyzed for cadmium (Cd), copper (Cu), manganese (Mn), lead (Pb) and zinc (Zn) using ICP-OES. We found the same order of trace metals concentrations (Zn > Mn > Cu > Pb > Cd) in M. bechsteinii and M. myotis, while M. daubentonii (Zn > Cu > Mn > Pb > Cd) and P. pipistrellus (Zn > Cu > Pb > Mn > Cd) differed from the above species and from each other. The observed differences between the bat species may reflect varying metal levels in their foraging areas as well as differences in preferred prey species and metal kinetics. Analysis of trace metal concentrations in hairs as a non-invasive and cost-effective method should be included in risk assessments regarding metal toxicity in bats.
Afonso E., Tournant P., Foltête J. C., Giraudoux P., Baurand P. E., Roué S., Canella V., Vey D., Scheifler R. (2016): Is the lesser horseshoe bat (Rhinolophus hipposideros) exposed to causes that may have contributed to its decline? A non-invasive approach. Global Ecology and Conservation 8: 123-137.
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While the lesser horseshoe bat (Rhinolophus hipposideros) was common in most western and Central Europe, this species endured a dramatic decline in the 1950s–1970s. The causes are thought to comprise the extensive spread of chemical pollutants affecting both bat and prey populations, changes in landscape composition and structure leading to population fragmentation or roost deterioration, and infectious diseases. While lesser horseshoe bat populations recently increased after nearly thirty years of decline in the Franche-Comté region (eastern France), it is unclear whether bats are currently confronted with causes that may have contributed to former demographic disturbances. Although stressors are generally studied separately, we simultaneously measured several variables directly or indirectly reflecting the supposed causes of bat decline: availability of woodland habitats around bat roosts, genetic differentiation amongst colonies, and exposure to chemical pollutants and to a protozoan parasite, Eimeria hessei. Twenty maternity colonies were sampled using a non-invasive approach based on droppings. Maternity roosts were located in buildings mainly surrounded by woodland and shrubland (48% of a 2500 m radius buffer around the colonies), which are preferentially used by the lesser horseshoe bat as foraging areas. Low genetic differentiation (FST=0.023-0.028, D=0.076-0.097) and no genetic clusters were found among the 20 sampled colonies, in which 449 individuals were distinguished over two sampling sessions (2010 and 2011). This suggests that no obvious physical barrier acts as a constraint with respect to gene flow, and we conclude that all individuals sampled belong to a unique non-fragmented population. Among the 66 chemical substances measured in bat droppings, the insecticides endosulfan alpha (0.035 ug/g dm) and lindane (from 0.013 to 0.112 ug/g dm) were the only organic compounds found at detectable concentrations in one and 7 colonies, respectively. Fourteen metals were measured in the guano. Metal concentrations were lower than or of the same order of magnitude as concentrations reported in bats in the literature. The overall faecal prevalence of E. hessei was 42% (range: 0%–80%) and did not differ between the two sampling sessions. Faecal prevalence was not related to lindane concentrations in droppings. Despite the low concentrations of metals, a positive relationship was found between cadmium and zinc concentrations and E. hessei faecal prevalence. Although it is difficult to conclude on the risks of adverse effects due to the lack of both toxicological references and knowledge on E. hessei pathogenicity, this study stresses out the interest of systemic approaches in the study of ecology of wildlife species, especially via the investigation of multiple exposures.
Hernout B. V., McClean C. J., Arnold K. E., Walls M., Baxter M., Boxall A. B. (2016): Fur: A non-invasive approach to monitor metal exposure in bats. Chemosphere 147: 376-381.
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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.
Becker D. J., Chumchal M. M., Broders H. G., Korstian J. M., Clare E. L., Rainwater T. R., Platt S. G., Simmons N. B., Fenton M. B. (2018): Mercury bioaccumulation in bats reflects dietary connectivity to aquatic food webs. Environmental Pollution 233: 1076-1085.
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Mercury (Hg) is a persistent and widespread heavy metal with neurotoxic effects in wildlife. While bioaccumulation of Hg has historically been studied in aquatic food webs, terrestrial consumers can become contaminated with Hg when they feed on aquatic organisms (e.g., emergent aquatic insects, fish, and amphibians). However, the extent to which dietary connectivity to aquatic ecosystems can explain patterns of Hg bioaccumulation in terrestrial consumers has not been well studied. Bats (Order: Chiroptera) can serve as a model system for illuminating the trophic transfer of Hg given their high dietary diversity and foraging links to both aquatic and terrestrial food webs. Here we quantitatively characterize the dietary correlates of long-term exposure to Hg across a diverse local assemblage of bats in Belize and more globally across bat species from around the world with a comparative analysis of hair samples. Our data demonstrate considerable interspecific variation in hair total Hg concentrations in bats that span three orders of magnitude across species, ranging from 0.04 mg/kg in frugivorous bats (Artibeus spp.) to 145.27 mg/kg in the piscivorous Noctilio leporinus. Hg concentrations showed strong phylogenetic signal and were best explained by dietary connectivity of bat species to aquatic food webs. Our results highlight that phylogeny can be predictive of Hg concentrations through similarity in diet and how interspecific variation in feeding strategies influences chronic exposure to Hg and enables movement of contaminants from aquatic to terrestrial ecosystems.
Flache L., Becker N. I., Kierdorf U., Czarnecki S., Düring R. A., Encarnação J. A. (2018): Similar but not the same: metal concentrations in hair of three ecologically similar, forest-dwelling bat species (Myotis bechsteinii, Myotis nattereri, and Plecotus auritus). Environmental Science and Pollution Research 25: 5437-5446.
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Recently, a number of studies demonstrated the suitability of hair analysis to assess metal exposure of bats. As many bat species are endangered, such a non-destructive method is particularly suited for this taxon. The present study analyzed the levels of two non-essential (cadmium and lead) and four essential metals (copper, manganese, molybdenum, and zinc) in hairs of three ecologically similar, sympatric bat species, Bechstein’s bat (Myotis bechsteinii), Natterer’s bat (Myotis nattereri), and Brown long-eared bat (Plecotus auritus) from an area in Central Hesse (Germany), as well as metal concentrations in soil samples from the bats’ foraging habitats. Applying a previously established protocol, the analyses were performed using microwave-assisted extraction followed by inductively coupled plasma optical emission spectrometry. Cadmium and lead concentrations in hair did not differ significantly among the three studied species, whereas the following significant differences existed for levels of essential metals in hair. Manganese concentrations in hair were higher in M. bechsteinii and P. auritus than in M. nattereri and Cu concentrations were higher in M. nattereri than in P. auritus. Myotis bechsteinii showed higher Zn concentrations compared to P. auritus and lower Mo concentrations compared to M. nattereri. Reasons for the observed differences among the three studied species could be differential exposure to these metal elements in their foraging areas, related to variation in the species composition of their arthropod diet in combination with different metal levels in the respective prey species, and/or species-specific requirements for essential metals and related variation in physiological regulation of these elements in the bats.
Heiker L. M., Adams R. A., Ramos C. V. (2018): Mercury bioaccumulation in two species of insectivorous bats from urban China: influence of species, age, and land use type. Archives of Environmental Contamination and Toxicology 75: 585-593.
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Mercury (Hg) is a widespread, toxic pollutant, and China is the world’s largest emitter. We investigated Hg concentrations of fur in Japanese pipistrelles (Pipistrellus abramus) and Chinese noctules (Nyctalus plancyi) from Chengdu, Sichuan Province, in relation to degree of urbanization. Bats were mist-netted in June and July 2013, and the fur was analyzed via atomic absorption. Statistical comparisons were made between ages, species, and site types with unpaired t tests and between Hg concentration and body condition with Spearman’s rank correlations. Across sites, adult pipistrelles (n = 10) had significantly greater concentrations than adult noctules (n = 16). Adult N. plancyi (n = 16) had significantly greater concentrations than juvenile N. plancyi (n = 14). Contrary to our predictions, there was no significant difference in Hg values between urban (n = 3) and peri-urban (n = 6) locations for P. abramus. While small sample sizes precluded additional comparisons, the highest value (33 mg/kg) came from an adult female P. abramus in the agricultural area. The relationship between body condition and Hg concentration was insignificant. However, most pipistrelles (7/13) and no noctules (0/31) had concentrations > 10 mg/kg, a threshold associated with disruption of homeostatic control and mobility. All bats had concentrations > 0.2 mg/kg, which is associated with compromised immunity. These are the first published records of contaminant concentrations from bats in China. For future studies, we recommend P. abramus as a regional bioindicator, longer term assessments of pre- and post-exposure effects, and simultaneous assessment of blood and fur Hg concentrations.
Kumar A., Divoll T. J., Ganguli P. M., Trama F. A., Lamborg C. H. (2018): Presence of artisanal gold mining predicts mercury bioaccumulation in five genera of bats (Chiroptera). Environmental Pollution 236: 862-870.
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Mercury, a toxic trace metal, has been used extensively as an inexpensive and readily available method of extracting gold from fine-grained sediment. Worldwide, artisanal mining is responsible for one third of all mercury released into the environment. By testing bat hair from museum specimens and field collected samples from areas both impacted and unimpacted by artisanal gold mining in Perú, we show monomethylmercury (MMHg) has increased in the last 100 years. MMHg concentrations were also greatest in the highest bat trophic level (insectivores), and in areas experiencing extractive artisanal mining. Reproductive female bats had higher MMHg concentrations, and both juvenile and adult bats from mercury contaminated sites had more MMHg than those from uncontaminated sites. Bats have important ecological functions, providing vital ecosystem services such as pollination, seed dispersal, and insect control. Natural populations can act as environmental sentinels and offer the chance to expand our understanding of, and responses to, environmental and human health concerns.
Ruiz S. R., Eeva T., Kanerva M., Blomberg A., Lilley T. M. (2019): Metal and metalloid exposure and oxidative status in free-living individuals of Myotis daubentonii. Ecotoxicology and Environmental Safety 169: 93-102.
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Metal elements, ubiquitous in the environment, can cause negative effects in long-lived organisms even after low but prolonged exposure. Insectivorous bats living near metal emission sources can be vulnerable to such contaminants. Although it is known that bats can bioaccumulate metals, little information exists on the effects of metal elements on their physiological status. For example, oxidative status markers are known to vary after detoxification processes and immune reactions. Here, for two consecutive summers, we sampled individuals from a natural population of the insectivorous bat, Myotis daubentonii, inhabiting a site close to a metal emission source. We quantified metals and metalloids (As, Ca, Cd, Co, Cu, Mn, Ni, Pb, Se, Zn) from individual fecal pellets. We measured enzymatic antioxidants (GP, CAT, SOD), total glutathione (tGSH) and ratio between reduced and oxidized glutathione (GSH:GSSG) from their red blood cells together with biometrics, hematocrit and parasite prevalence. In general, metal concentrations in feces of M. daubentonii reflected the exposure to ambient contamination. This was especially evident in the higher concentrations of Cd, Co, Cu and Ni close to a smelter compared to a site with less contaminant exposure. Annual differences were also observed for most elements quantified. Sex-specific differences were observed for calcium and zinc excretion. SOD and CAT enzymatic activities were associated with metal levels (principal components of six metal elements), suggesting early signs of chronic stress in bats. The study also shows promise for the use of non-invasive sampling to assess the metal exposure on an individual basis and metal contamination in the environment.
Cory-Toussaint D., Taylor P. J., Barnhoorn I. E. (2021): Non-invasive sampling of bats reflects their potential as ecological indicators of elemental exposure in a diamond mining area, northern Limpopo Province, South Africa. Environmental Science and Pollution Research 29: 13647-13660.
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Bats have been proposed as reliable bioindicators for monitoring bioaccumulation of elements and chemicals in natural and transformed ecosystems. Non-invasive methods are becoming more popular as research moves away from destructive methodologies. We present the first concentrations of 23 elements in Mops condylurus and Tadarida aegyptiaca (Molossidae) fur and blood from an opencast diamond mine and reference area using inductively coupled plasma mass spectrometry (ICP-MS). Concentrations of B, K, Rb and Cd in the bats’ fur were significantly higher in the mining footprint compared to the reference area (P < 0.05). Other elements such as Zn and Hg were significantly higher in the blood of bats from the mining footprint than the reference area (P < 0.05), whereas Mn was significantly higher in the blood of bats from the reference area than from the mining footprint (P < 0.05). Sixteen of the 22 elements above the limit of detection, with the exception of Ba, were significantly higher in the fur samples than in the blood due to elements being incorporated over time into the fur as it grows, whereas blood reveals short-term exposure to elements. Concentrations of most of the elements were reasonably low except Al, Fe and Zn. In general, the element concentrations particularly in the fur samples were comparable with other international studies reporting elemental fur concentrations from anthropogenically impacted and natural areas. Fur and blood have the potential to be viable indicators of environmental toxicity, but research is required on toxic thresholds and physiological and ecological unknowns around element concentrations in bat tissues and organs.
Drinkwater R., Goodwin A., Cush J., Korstian J. M., Chumchal M. M., Herrera M. L. G., Valdez M., Otálora-Ardila A., Flores-Martinez J. J., Clare E. L. (2021): Molecular diet analysis of the marine fish-eating bat (Myotis vivesi) and potential mercury exposure. Canadian Journal of Zoology 99: 752-759.
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Mercury is a toxic element acquired by animals through feeding which can accumulate within food chains through biomagnification. This possesses particular risks to higher trophic levels and may unduly impact marine foraging species or individuals. The fish-eating bat (Myotis vivesi Menegaux, 1901) inhabits islands in the Gulf of California and can act as a predator in the marine environment. A predominantly marine diet and a high trophic position increase the risk of mercury exposure owing to increased bioaccumulation. Using molecular techniques to reconstruct diet, we show that M. vivesi regularly feeds on small fishes and crustaceans, particularly on the Californian anchovy (Engraulis mordax Girard, 1854) and a krill species (Nyctiphanes simplex Hansen, 1911). Additionally, we identify significant interannual variation in diet composition within this population, but measured levels of total mercury in faecal samples were not related to dietary diversity or trophic level.
Hooper S. E., Amelon S. K., Lin C. H. (2022): Development of an LC-MS/MS method for non-invasive biomonitoring of neonicotinoid and systemic herbicide pesticide residues in bat hair. Toxics 10: 73.
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With over a quarter of the world’s bats species facing extinction, there is a need for ecotoxicological studies to assess if acute and sublethal exposure to newer pesticides such as neonicotinoids and carbonates contribute to population declines. Pesticide exposure studies in bats have been limited to terminal sampling methods, therefore we developed a non-invasive liquid chromatography-tandem mass spectrometry (LC-MS/MS) method utilizing hair trimmings. The hair of big brown bats (Eptesicus fuscus) was collected and pooled by county to assess the best extraction solvent and solid-phase-extraction (SPE) clean-up cartridges. Using the best performing extraction solvent, methanol, and the best performing SPE cartridge, Chromabond HR-X, we developed an optimized multiple reaction monitoring (MRM) LC-MS/MS method for simultaneous determination of 3 neonicotinoids, clothianidin, imidacloprid, and thiamethoxam; 1 carbonate, carbaryl; and 4 systemic herbicides, 2,4-D, atrazine, dicamba, and glyphosate. The optimized protocol yielded the detection of 3–8 of the compounds in the county-level bat hair pools. 2,4-D, glyphosate, and imidacloprid were found in all samples with two of the county-level hair samples having glyphosate concentrations of over 3500 pg/mg of hair. This approach has great potential to facilitate non-terminal ecotoxicological studies assessing the effects of subacute (chronic) pesticide exposure in threatened and endangered bat species and other species experiencing population declines.
CARNIVORES
Van den Brink N. W., Jansman H. A. (2006): Applicability of spraints for monitoring organic contaminants in free‐ranging otters (Lutra lutra). Environmental Toxicology and Chemistry: An International Journal 25: 2821-2826.
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In the current study, the use of spraints for monitoring levels of polychlorinated biphenyls (PCBs) in individual otters was experimentally validated. On the basis of a detailed pattern analysis, it is concluded that in the current study, PCB concentrations in spraints that contain relatively high concentrations of nonmetabolizable PCB congeners (PCB 138 and 153>42.5% of total PCB concentrations) reflect the internal PCB concentrations of the otter that produced the spraint. In general, however, spraints should be selected that contain relative concentrations of PCB 138 and PCB 153>95th percentile of these congeners in samples from local food items of otters. On the basis of relationships between levels in spraints and internal levels and on earlier reported effect concentrations, a threshold level range of 1.0 to 2.3 μg/g (lipid normalized) in such spraints is proposed. The validated methods to monitor PCBs in otters may be combined with genetic marker techniques that can assess the identity of the otter that produced the spraints. In such a design, it is feasible to monitor PCB levels in individual free-ranging otters in a truly animal friendly way.
Andrade S., Carlini A. R., Vodopivez C., Poljak S. (2007): Heavy metals in molted fur of the southern elephant seal Mirounga leonina. Marine Pollution Bulletin 54: 602-605.
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Given the lack of information on heavy metals in the southern elephant seal, concentrations of Cd, Cu, Cr, Ni, Pb and Zn were determined in molted fur samples of M. leonina from the South Shetland Islands. The aim of the study was to provide a baseline of heavy metals at the top level of the Antarctic marine food web, and to assess the reliability of molted fur samples as a harmless sampling tool for heavy metals assessment in seals.
Elliott J. E., Guertin D. A., Balke J. M. (2008): Chlorinated hydrocarbon contaminants in feces of river otters from the southern Pacific coast of Canada, 1998–2004. Science of the Total Environment 397: 58-71.
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Chlorinated hydrocarbon contaminants in coastal river otters (Lontra canadensis) were evaluated by sampling feces (scats) collected on the south coast of British Columbia, Canada. A broad survey of industrialized areas of the Strait of Georgia region was conducted in 1998, and a subsequent survey of working harbours in 2004. Samples from 1998 were analyzed for polychlorinated biphenyls (PCBs), organochlorine (OC) pesticides, and polychlorinated dioxins (PCDDs) and furans (PCDFs), while in 2004, chemistry was confined to ∑PCBs and OC pesticides. Concentrations of OC pesticides were low in both years, with only dichlorodiphenyldichloroethylene (DDE; range: 0.01–2.12 mg/kg lw) and hexachlorocyclobenzene (HCB; range: 0.003–0.25 mg/kg lw) detected in all samples. In 1998, octachlorodibenzo-p-dioxin (OCDD) and other higher chlorinated PCDD/Fs were found in most samples, with OCDD ranging from 120 ng/kg lw in Clayoquot Sound to 19,100 ng/kg lw in a pooled sample from two latrines in Nanaimo. PCBs were present in all samples. In 1998 geometric mean concentrations of the sum of 59 PCB congeners ranged from 0.49 mg/kg lw in Nanaimo to 12.3 mg/kg lw in Victoria Harbour. Six years later, mean ∑PCBs remained elevated (geometric mean 9.5 mg/kg lw) in Victoria Harbour. Geometric mean concentrations of ∑PCBs from Victoria Harbour in 1998 and 2004 were > 9 mg/kg lw, a published adverse effect level for reproduction. At some latrines in both Victoria and Esquimalt Harbours, concentrations of TCDD-toxic equivalents exceeded 1500 ng/kg lw, a value for health effects in otters that we derived using published information. As shown in previous studies, analysis of scats provides an efficient and non-intrusive approach to assessing contaminant threats to otter populations, and to documenting spatial trends in residues.
Guertin D. A., Harestad A. S., Ben‐David M., Drouillard K. G., Elliott J. E. (2010): Fecal genotyping and contaminant analyses reveal variation in individual river otter exposure to localized persistent contaminants. Environmental Toxicology and Chemistry 29: 275-284.
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The present study investigated polyhalogenated aromatic hydrocarbon (PHAH) concentrations in feces of known river otters (Lontra canadensis) along the coast of southern Vancouver Island, British Columbia, Canada. Specifically, we combined microsatellite genotyping of DNA from feces for individual identification with fecal contaminant analyses to evaluate exposure of 23 wild otters to organochlorine pesticides (OCPs), polychlorinated biphenyls (PCBs), and polybrominated diphenylethers (PBDEs). Overall, feces collected from otters in urban/industrial Victoria Harbor had the greatest concentrations of nearly all compounds assessed. Fecal concentrations of OCPs and PBDEs were generally low throughout the region, whereas PCBs dominated in all locations. Re‐sampling of known otters over space and time revealed that PCB exposure varied with movement and landscape use. Otters with the highest fecal PCB concentrations were those inhabiting the inner reaches of Victoria Harbor and adjacent Esquimalt Harbor, and those venturing into the harbor systems. Over 50% of samples collected from eight known otters in Victoria Harbor had total‐PCB concentrations above the maximum allowable concentration as established for Eurasian otter (Lutra lutra) feces, with a geometric mean value (10.6 mg/kg lipid wt) that exceeded the reproductive toxicity threshold (9 mg/kg lipid wt). Those results are consistent with our findings from 1998 and 2004, and indicate that the harbors of southern Vancouver Island, particularly Victoria Harbor, are a chronic source of PCB exposure for otters. The present study further demonstrates the suitability of using otter feces as a noninvasive/destructive biomonitoring tool in contaminant studies, particularly when sampling of the same individuals at the local population‐level is desired.
Richards N. L., Cook G., Simpson V., Hall S., Harrison N., Scott K. S. (2011): Qualitative detection of the NSAIDs diclofenac and ibuprofen in the hair of Eurasian otters (Lutra lutra) occupying UK waterways with GC–MS. European Journal of Wildlife Research 57: 1107-1114.
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The pervasiveness of pharmaceuticals such as nonsteroidal anti-inflammatory drugs (NSAIDs) in the aquatic ecosystem through the discharge of wastewater, and their potential to biomagnify within this ecosystem, is now recognised. Residues of diclofenac and ibuprofen are currently being detected in surface waters and aquatic organisms throughout the UK and Europe. However, the levels of these residues in fish and other aquatic organisms, particularly lower trophic level prey species, have not yet been determined. While exposure to diclofenac is known to adversely affect fish, the degree to which other aquatic organisms are exposed and impacted through continuous ingestion of contaminated prey and interaction with the aquatic habitat remains unknown. The extent and effects of exposure to ibuprofen also remain largely unknown. As an exploratory subset of a broader study to investigate the detectability of diclofenac in alternative biological matrices, we analysed hair samples from Eurasian otters (Lutra lutra, n = 28) for residues of the two NSAIDs using GC–MS. The otters were collected from six counties in England as part of an ongoing otter health monitoring project at the Wildlife Veterinary Investigation Centre in Chacewater, UK. Diclofenac was qualitatively detected in five hair wash and 15 extract samples, and ibuprofen was determined to be present in at least two of the hair extract samples. Here, we provide preliminary evidence that otters are exposed to both NSAIDs and argue for further studies to identify residue loads in the otters and their prey to fully assess the pervasiveness of these compounds and potential risks of ongoing exposure to them.
Curi N. H. D. A., Brait C. H. H., Talamoni S. A. (2012): Heavy metals in hair of wild canids from the Brazilian Cerrado. Biological Trace Element Research 147: 97-102.
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In this study, we aimed to assess whether free-ranging wild canids are exposed to heavy metals in one of the most developed and populated regions of Brazil. Hair of 26 wild canids (maned wolves Chrysocyon brachyurus, crab-eating foxes Cerdocyon thous, and hoary foxes Lycalopex vetulus) from the Cerrado biome in Southeast Brazil were analyzed by spectrophotometry to detect cadmium, chromium, and lead, and also the essential copper, iron, manganese, and zinc traces. All samples showed traces of copper, iron, manganese, and zinc. Non-essential lead was detected in 57% (2.35 ± 0.99 mg/kg), and chromium in 88% (2.98 ± 1.56 mg/kg) of samples. Cadmium traces (detection limit 0.8 mg/kg) were not found. Crab-eating foxes had more copper, iron, and manganese in hair than maned wolves. Correlations among element levels differed between maned wolves and crab-eating foxes. Concentrations of chromium and lead were outstandingly higher than in wild canids from other areas. Addressing the causes of such levels and the impacts of the heavy metal pollution in Neotropical ecosystems is urgent for animal health and conservation purposes. We argue that heavy metal pollution should be considered as dangerous threats to wildlife health in Brazil and recommend hair sampling as a biomonitoring tool for heavy metals in Neotropical terrestrial mammals.
Christensen J. R., Yunker M. B., MacDuffee M., Ross P. S. (2013): Plant consumption by grizzly bears reduces biomagnification of salmon‐derived polychlorinated biphenyls, polybrominated diphenyl ethers, and organochlorine pesticides. Environmental Toxicology and Chemistry 32: 995-1005.
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The present study characterizes the uptake and loss of persistent organic pollutants (POPs) in grizzly bears (Ursus arctos horribilis) by sampling and analyzing their terrestrial and marine foods and fecal material from a remote coastal watershed in British Columbia, Canada. The authors estimate that grizzly bears consume 341 to 1,120 µg of polychlorinated biphenyls (PCBs) and 3.9 to 33 µg of polybrominated diphenyl ethers daily in the fall when they have access to an abundant supply of returning salmon. The authors also estimate that POP elimination by grizzly bears through defecation is very low following salmon consumption (typically <2% of intake) but surprisingly high following plant consumption (>100% for PCBs and organochlorine pesticides). Excretion of individual POPs is largely driven by a combination of fugacity (differences between bear and food concentrations) and the digestibility of the food. The results of the present study are substantiated by a principal components analysis, which also demonstrates a strong role for log KOW in governing the excretion of different POPs in grizzly bears. Collectively, the present study’s results reveal that grizzly bears experience a vegetation-associated drawdown of POPs previously acquired through the consumption of salmon, to such an extent that net biomagnification is reduced.
Hernández-Moreno D., de la Casa Resino I., Fidalgo L. E., Llaneza L., Rodríguez F. S., Pérez-López M., López-Beceiro A. (2013): Noninvasive heavy metal pollution assessment by means of Iberian wolf (Canis lupus signatus) hair from Galicia (NW Spain): a comparison with invasive samples. Environmental Monitoring and Assessment 185: 10421-10430.
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The current study represents the first investigation of the suitability of wolf hair as indicator tissue for metal exposure and accumulation within NW Spanish ecosystems. Dead animals, which were not specifically killed for these purposes, were necropsied, and further toxicological analyses were performed in order to establish the heavy metal content (Pb, Cd, and Zn) in liver, kidney, and hair, by means of inductively coupled plasma optical emission spectrometry. Two different factors, gender and age, were considered in order to determine their influence on heavy metal accumulation. Mean liver, kidney and hair concentrations of both toxic element, Cd (0.528, 2.692, and 0.026 ppm) and Pb (4.108, 0.031, and 0.196 ppm) considered on a dry weight basis, were situated below the established as acute toxicity levels for mammals. The highest concentrations were quantified for Zn, with means ranging from a maximum in hair samples (150.9 ppm) to a minimum in kidney samples (25.81 ppm). When the variable of gender and age were considered, female and adult wolves had higher concentrations of Cd in all the considered organs, although differences were only statistically significant for kidney. Neither the sex nor the age had a significant effect on Pb and Zn concentrations. A significant positive correlation (p < 0.05) was identified between hair and liver Pb concentrations, as well as between hair and kidney Cd concentrations, thus suggesting the interest of the noninvasive sample for future ecotoxicological biomonitoring studies.
Noël M., Spence J., Harris K. A., Robbins C. T., Fortin J. K., Ross P. S., Christensen J. R. (2014): Grizzly bear hair reveals toxic exposure to mercury through salmon consumption. Environmental Science and Technology 48: 7560-7567.
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Mercury obtained from the diet accumulates in mammalian hair as it grows thus preserving a record of mercury intake over the growth period of a given hair segment. We adapted a microanalysis approach, using laser ablation inductively coupled plasma mass spectrometry, to characterize temporal changes in mercury exposure and uptake in wild and captive grizzly bears. Captive grizzlies fed diets containing known and varied amounts of mercury provided data to allow prediction of Hg ingestion rates in wild bears. Here, we show, for the first time, that 70% of the coastal grizzly bears sampled had Hg levels exceeding the neurochemical effect level proposed for polar bears. In a context where the international community is taking global actions to reduce Hg emissions through the “Minamata Convention on Mercury”, our study provides valuable information on the exposure to mercury of these grizzly bears already under many threats.
Bechshoft T., Derocher A. E., Richardson E., Mislan P., Lunn N. J., Sonne C., Dietz R., Janz D. M., St Louis V. L. (2015): Mercury and cortisol in Western Hudson Bay polar bear hair. Ecotoxicology 24: 1315-1321.
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Non-invasive methods of assessing animal health and life history are becoming increasingly popular in wildlife research; hair samples from polar bears (Ursus maritimus), are being used to study an ever broader range of anthropogenic and endocrine compounds. A number of contaminants are known to disrupt endocrine function in polar bears. However, the relationship between mercury and cortisol remains unknown, although mercury is an endocrine disruptor in other species. Here, we examine the relationship between concentrations of cortisol and total mercury (THg) analyzed in guard hair from 378 polar bears (184 females, 194 males) sampled in Western Hudson Bay, 2004–2012. The difference in mean cortisol concentration between female (0.8 ± 0.6 pg/mg) and male (0.7 ± 0.5 pg/mg) polar bears bordered on significance (p = 0.054). However, mean mercury concentration was significantly greater (p = 0.009) in females (4.7 ± 1.4 μg/g) than males (4.3 ± 1.2 μg/g). Hair cortisol in males was significantly influenced by mercury, age, and fatness, as well as interactions between mercury and year, mercury and fatness, and year and fatness (all: p < 0.03) (multiple regression analysis, whole model: r2 = 0.14, F7,185 = 4.43, p = 0.0001). Fatness was the only significant variable in the multiple regression analysis for females (r2 = 0.06, F1,182 = 13.0, p = 0.0004). In conclusion, a significant, but complex, relationship was found between mercury and cortisol concentrations in hair from male, but not female, polar bears.
Pedroso N. M., Dias S. V., Diniz-Reis T. R., Santos-Reis M., Verdade L. M. (2018): Non-invasive hair sampling of Neotropical otters. Biota Neotropica 18: e20180579.
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Sampling wild animal populations using non-invasive techniques is advised when dealing with threatened species. Hair samples provide ecological information like species and individual identification. However, hair trapping is scarcely used in otters, due to their aquatic habits. Most studies are with captive individuals, so there is the need to test non-invasive hair trapping methods in otters in the wild. The aim of this study was to develop a simple and cost-effective method to collect hair from otter species in a non-invasive way. The study was carried out in the Paranapanema River, São Paulo State, Brazil, with the Neotropical otter (Lontra longicaudis Olfers, 1818), a protected species. Hair traps (wooden sticks and tree roots with adhesive tape or wax bands) were set during six nights on river banks, otter trails and scent-marking sites. Traps were baited with otter fresh spraints from other river locations. From the 23 traps, 10 (43.7%) were successful in collecting otter hairs, mostly guard-hair. The sticks were much more efficient than the roots at capturing otter hair (70.6.% vs. 0%) as well as adhesive tape when compared to wax (71.4% vs. 0%). Method simplicity and efficiency suggest that it can be a cost-effective way for collecting otter hairs without the need for capturing individuals. This method can be used for: assessment of local otter distribution; collecting otter hair samples for sex and individual identification (by molecular analysis), trophic ecology (by isotopic analyses), ecotoxicology (by contamination analysis) or behaviour ecology (by hormonal and stress levels analysis). More trapping campaigns should be implemented to further test the method’s efficiency.
Bechshoft T., Dyck M., Pierre K. A. S., Derocher A. E., Louis V. S. (2019): The use of hair as a proxy for total and methylmercury burdens in polar bear muscle tissue. Science of The Total Environment 686: 1120-1128.
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Polar bears (Ursus maritimus) are an ecologically important species in the Arctic, whose health, and that of the people whose livelihoods depend on them, are increasingly affected by climate change and the bioaccumulation of contaminants such as mercury (Hg). Although methylmercury (MeHg) is the toxic form of Hg that biomagnifies up food webs, risk assessment studies typically only report on total Hg (THg) concentrations because it is cheaper to quantify. Furthermore, hair is commonly analysed for THg in polar bear as well as human risk assessment studies because it is relatively non-invasive to collect, yet we know little of how THg and MeHg concentrations differ between hair and muscle tissues. In this study, we quantified THg and MeHg concentrations in hair and muscle from 44 polar bears (24 sub-adults: 9 females, 15 males; 18 adults: 5 females, 13 males, and 2 males of unknown age group), harvested in 2015 and 2016 from four subpopulations in Nunavut, Canada (Davis Strait, n = 3; Gulf of Boothia, n = 8; Baffin Bay, n = 15; Foxe Basin, n = 18). We found only moderately positive correlations (0.4 ≤ r ≤ 0.5) between THg concentrations in hair and THg and MeHg concentrations in muscle. Further, 75% and 88% of THg was MeHg in hair and muscle, respectively. High concentrations of THg in hair – 71% of the samples were above the suggested neurochemical no observed effect level for polar bears – suggest some of the bears may be adversely affected by Hg-related health effects. Despite this, all MeHg concentrations in muscle (0.1 to 0.4 mg/kg (wet weight, ww)) were below the consumption maximum Hg concentration of 0.5 mg/kg (ww) set by Canadian health authorities.
Grajewska A., Falkowska L., Saniewska D., Pawliczka I. (2020): Fur and faeces–Routes of mercury elimination in the Baltic grey seal (Halichoerus grypus grypus). Science of The Total Environment 717: 137050.
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This study focused on evaluating the elimination of Hg by Baltic grey seals (Halichoerus grypus grypus) via faeces and pelage. In addition, we investigated the potential for ecosystem contamination via these routes. Faeces and fur were collected in 2014–2017 from captive adult grey seals and their pups. The concentrations of total mercury (THg) and methylmercury (MeHg) were measured in the samples. The amount of mercury eliminated in a labile form (the sum of the bioavailable Hg(II) and methylmercury) was also determined. An adult seal removed about 46% of mercury supplied with food via the faeces, of which only 17% was MeHg. Considering that mercury is mainly supplied to the body as MeHg, it can be assumed that mercury excreted along with faeces has undergone transformation inside the animal body. Despite the much higher THg and MeHg concentrations measured in fur, the incorporation of mercury into newly formed fur is a less effective method of Hg elimination removing just 4% of mercury entering the body via the alimentary route. The presence of mercury in lanugo is evidence of maternal transfer. First droppings of the pups were characterised by the highest content of MeHg and a low THg concentration. Then, despite the limited supply of mercury with food, and the rapid growth of the pup, the concentration of THg increased, suggesting that mercury started to be transformed into less toxic forms. It was estimated that faeces and fur expelled by seals could deliver about 800 g of mercury to the Baltic Sea. For both faeces and fur, most of the mercury (>95% for excrements and >85% for fur) was expelled in a labile form that can be quickly recycled.
Lippold A., Aars J., Andersen M., Aubail A., Derocher A. E., Dietz R., Eulaers I., Sonne C., Welker J. M., Wiig Ø., Routti H. (2020): Two decades of mercury concentrations in Barents Sea polar bears (Ursus maritimus) in relation to dietary carbon, sulfur, and nitrogen. Environmental Science and Technology 54: 7388-7397.
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Temporal trends of total mercury (THg) were examined in female polar bear (Ursus maritimus) hair (n = 199) from the Barents Sea in 1995–2016. In addition, hair values of stable isotopes (n = 190–197) of carbon (δ13C), sulfur (δ34S), and nitrogen (δ15N) and information on breeding status, body condition, and age were obtained. Stable isotope values of carbon and sulfur reflect dietary source (e.g., marine vs terrestrial) and the nitrogen trophic level. Values for δ13C and δ34S declined by −1.62 and −1.18‰ over the time of the study period, respectively, while values for δ15N showed no trend. Total Hg concentrations were positively related to both δ13C and δ34S. Yearly median THg concentrations ranged from 1.61 to 2.75 μg/g and increased nonlinearly by 0.86 μg/g in total over the study. Correcting THg concentrations for stable isotope values of carbon and sulfur and additionally breeding status and age slightly accelerated the increase in THg concentrations; however, confidence intervals of the raw THg trend and the corrected THg trend had substantial overlap. The rise in THg concentrations in the polar bear food web was possibly related to climate-related re-emissions of previously stored Hg from thawing sea-ice, glaciers, and permafrost.
Rodríguez-Estival J., Ortiz-Santaliestra M. E., Mateo R. (2020): Assessment of ecotoxicological risks to river otters from ingestion of invasive red swamp crayfish in metal contaminated areas: use of feces to estimate dietary exposure. Environmental Research 181: 108907.
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The invasive red swamp crayfish (Procambarus clarkii) has become a major food resource for Eurasian otters (Lutra lutra) in the Iberian Peninsula. Crayfish accumulate large amounts of metals, and hence otters could be at risk of exposure and intoxication through crayfish consumption. We conducted a food safety risk assessment for otters inhabiting two historical mining areas in central Spain affected by lead (Pb) and mercury (Hg) pollution. Estimated daily intakes (EDI) of Pb and Hg were non-invasively calculated from the proportion of crayfish remains and metal levels in otter feces. We considered that the abdominal muscle and the carcass of crayfish differ significantly in relative weight, total metal content and bioavailability of metals to reduce the uncertainty of risk characterization. Fecal concentrations of Hg and Pb in the polluted areas were 1.878 and 6.554 μg/g d. w., respectively (13-fold and 7-fold higher compared to a non-polluted area). EDI of Hg and Pb in the polluted areas were 66.02 and 78.26 μg/kg-day, respectively (14- and 8-fold higher than in the reference area). EDI from the Hg area were above minimum levels susceptible to cause neurotoxicity in mustelids, and 6.3% were above levels susceptible to cause histopathological lessions. In the Pb area, 16.7% of EDI were consistent with levels causing reproductive effects. Metal exposure through crayfish consumption might prevent or slow the recovey of otters in these polluted environments, thus this factor should be considered in management strategies aimed to protect otter populations.
Tian Z., Liu X., Sun W., Ashraf A., Zhang Y., Jin X., He X., He B. (2020): Characteristics of heavy metal concentrations and risk assessment for giant pandas and their habitat in the Qinling Mountains, China. Environmental Science and Pollution Research 27: 1569-1584.
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High concentrations of heavy metals in the environment threaten the quality of ecosystems and the health of human beings and animals. Giant panda (Ailuropoda melanoleuca), which is endemic to China and a global conservation icon, has the largest density in the Qinling Mountains. This paper investigated the spatiotemporal variation of heavy metal concentrations in soil (N = 44) at the regional scale with three zones of urban areas, mountain edges, and central mountains, the temporal variation of heavy metal concentrations in three bamboo species (N = 19) and two types of feces (N = 10), and assessed the ecological risk and health risk for giant pandas and their habitat in the Qinling Mountains. The results showed that the median concentrations of studied eight heavy metals mercury (Hg), arsenic (As), copper (Cu), manganese (Mn), zinc (Zn), chromium (Cr), lead (Pb), and cadmium (Cd) in soil exceeded the background values of Shaanxi Province except Pb. The median concentrations of Hg, Zn, Cr, Pb, and Cd in bamboo surpassed the reference standard (RS) of national food safety limits in vegetables for human intake, but the concentration of Zn was within the nutrient range in the bamboo plants. Heavy metals were enriched more in feces of captive than the wild giant pandas, which illustrated either higher ingestion or lower digestibility for captive giant panda. Ecological risk assessment of soil by the geo-accumulation index (Igeo) and risk index (RI) showed strong pollution by Hg and moderate pollution by Cd. Health risk assessment by the hazard index (HI) showed a potential to strong risk for giant pandas exposed to Pb, As, and Hg. In addition, the concentrations of heavy metals in feces showed a higher exposure risk for captive giant pandas than wild giant pandas. We suggest that attention should be paid to and all effective measurements should be taken for reducing the emission of Hg, As, Pb, and Cd in the study area.
Carlsson P., Singdahl-Larsen C., Lusher A. L. (2021): Understanding the occurrence and fate of microplastics in coastal Arctic ecosystems: The case of surface waters, sediments and walrus (Odobenus rosmarus). Science of The Total Environment 792: 148308.
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The Arctic ecosystem receives contaminants transported through complex environmental pathways – such as atmospheric, riverine and oceanographic transport, as well as local infrastructure. A holistic approach is required to assess the impact that plastic pollution may have on the Arctic, especially with regard to the unseen microplastics. This study presents data on microplastics in the Arctic fjords of western Svalbard, by addressing the ecological consequences of their presence in coastal surface waters and sediment, and through non-invasive approaches by sampling faeces from an apex predator, the benthic feeder walrus (Odobenus rosmarus). Sample locations were chosen to represent coastal areas with different degrees of anthropogenic pollution and geographical features (e.g., varying glacial coverage of catchment area, winter ice cover, traffic, visitors), while also relevant feeding grounds for walrus. Microplastics in surface water and sediments ranged between <LOD (limit of detection)-3.5 particles/m3 and <LOD-26 particles/kg dry weight, respectively. This study shows that microplastics may also enter the Arctic food web as the microplastic concentration in walrus faeces were estimated at an average of 34 particles/kg. Polyester was identified by Fourier transformation infrared spectroscopy (FT-IR) as the most common plastic polymer (58% in water, 31% in walrus), while fibres were the most common shape (65% water, 71% in sediment, 70% walrus). There was no significant difference in microplastic occurrence between water samples from populated or remote fjords, suggesting that microplastics are a ubiquitous contaminant which is available for interaction with Arctic marine animals even at distances from settlements. The present study contributes to our understanding of microplastics in the remote Arctic ecosystem. It also identifies the potential of non-invasive sampling methods for investigating Arctic pinnipeds. This approach will need further development and standardisation before utilisation to monitor plastic pollution in other marine mammals.
Evans M. N., Waller S., Müller C. T., Goossens B., Smith J. A., Bakar M. S. A., Kille P. (2021): The price of persistence: Assessing the drivers and health implications of metal levels in indicator carnivores inhabiting an agriculturally fragmented landscape. Environmental Research 2021: 112216.
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Patterns and practices of agricultural expansion threaten the persistence of global biodiversity. Wildlife species surviving large-scale land use changes can be exposed to a suite of contaminants that may deleteriously impact their health. There is a paucity of data concerning the ecotoxicological impacts associated with the global palm oil (Elaeis guineensis) industry. We sampled wild Malay civets (Viverra tangalunga) across a patchwork landscape degraded by oil palm agriculture in Sabah, Malaysian Borneo. Using a non-lethal methodology, we quantified the levels of 13 essential and non-essential metals within the hair of this adaptable small carnivore. We robustly assessed the biological and environmental drivers of intrapopulation variation in measured levels. Metal concentrations were associated with civet age, weight, proximity to a tributary, and access to oxbow lakes. In a targeted case study, the hair metal profiles of 16 GPS-collared male civets with differing space use patterns were contrasted. Civets that entered oil palm plantations expressed elevated aluminium, cadmium, and lead, and lower mercury hair concentrations compared to civets that remained exclusively within the forest. Finally, we paired hair metal concentrations with 34 blood-based health markers to evaluate the possible sub-lethal physiological effects associated with varied hair metal levels. Our multi-facetted approach establishes these adaptable carnivores as indicator species within an extensively altered ecosystem, and provides critical and timely evidence for future studies.
Zhao Y., Chen Y. P., Macdonald D. W., Li J., Ma Q. Y. (2021): Organochlorine compounds pose health risks to the Qinling giant panda (Ailuropoda melanoleuca qinlingensis). Environmental Pollution 273: 116427.
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To assess organochlorine compound (OC) contamination, its possible sources, and adverse health impacts on giant pandas, we collected soil, bamboo, and panda fecal samples from the habitat and research center of the Qinling panda (Ailuropoda melanoleuca qinlingensis)—the rarest recognized panda subspecies. The polychlorinated biphenyls (PCBs) and organochlorine pesticides (OCPs) concentrations were comparatively low which suggests that moderate sources of OC pollution currently. OC levels were lower in samples from nature reserve than in those collected from pandas held in captivity, and OC levels within the reserve increased between functional areas in the order: core, buffer and experimental. The distribution patterns, and correlation analyses, combined with congener distributions suggested PCBs and OCPs originated from similar sources, were dispersed by similar processes, being transported through atmosphere and characterized by historical residues. Backward trajectory analyses results, and detected DRINs (aldrin, dieldrin, endrin and isodrin) both suggest long-range atmospheric transport of pollution source. PCBs pose potential cancer risk, and PCB 126 was the most notable toxicant as assessed be the high carcinogenic risk index. We provide data for health risk assessment that can guide the identification of priority congeners, and recommend a long-term monitoring plan. This study proposes an approach to ecotoxicological threats whereby giant pandas may be used as sentinel species for other threatened or endangered mammals. By highlighting the risks of long-distance transmission of pollutants, the study emphasizes the importance of transboundary cooperation to safeguard biodiversity.
Baos R., Cabezas S., González M. J., Jiménez B., Delibes M. (2022): Eurasian otter (Lutra lutra) as sentinel species for the long-term biomonitoring of the Guadiamar River after the Aznalcóllar mine spill. Science of The Total Environment 802: 149669.
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Accidents at mines involving stored tailings have produced catastrophic environmental damage. In April 1998 the dam of the Aznalcóllar mine tailings pond in the surroundings of the Doñana National Park (southwestern Spain) broke, discharging into the Guadiamar River more than 6 million m3 of toxic mud and acidic water with high concentrations of heavy metals and arsenic. We used the Eurasian otter (Lutra lutra) as sentinel species to assess the potential impact of the toxic spill on the river ecosystems and their recovery with time by studying the spatial and temporal variation (1999-2003, 2006) of selected trace element (Cu, Zn, Cd, Pb and As) concentrations in feces. Throughout the sampling period, the highest heavy metal and As levels were found in the most spill-affected reaches of the Guadiamar River (i.e., the Middle and, to a lesser extent, the Lower reaches), pointing out the mining accident as the main origin of the contamination. Overall, levels of trace elements decreased with the time elapsed since the toxic spill, except for Cd (F1,352 = 0.29, P = 0.59). However, rebounds for some elements (Pb, As, and Cu) were also observed, especially in the Middle and Lower reaches of the river, which might be attributed to the residual contamination in abiotic compartments and/or new inputs from industrial and agricultural activities in the nearby areas. Concentrations were relatively high when compared to those reported for both our reference area (Guadalete River) and other metal-polluted zones. We found that the estimated amounts of Pb and As ingested during the first years after the spill in the Guadiamar Middle reach would be high enough to cause reproductive issues. This could affect the local population recovery, although evidence on distribution range and numbers suggests otherwise, with thriving populations at regional scale. Our results support the role of otters as sentinel species for biomonitoring contaminants and thus to evaluate fluvial ecosystem health.
Desclos‐Dukes L., Butterworth A., Cogan T. (2022): Using a non‐invasive technique to identify suspected microplastics in grey seals (Halichoerus grypus) living in the western North Sea. Veterinary Record 2022: e1484.
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Plastic pollution is of growing concern in marine ecosystems worldwide. Specifically, microplastics (<5 mm) may interact with a variety of biota with the potential to cause harm to organism health. Studies investigating microplastics are increasing, yet their occurrence within free-ranging and living marine mammals remains largely unexplored. By using a protocol involving enzymatic digestion, filtration and microscopic identification, faecal samples collected from a grey seal (Halichoerus grypus) haul-out site in the North Sea were investigated for microplastic presence. Altogether, 71 suspected microplastic particles, consisting of both fibres and fragments in a variety of colours and sizes, were identified across 66 analysed faecal subsamples. The present study indicates that marine mammals are ingesting microplastics and that faecal material can be used to indirectly and non-invasively record microplastic uptake data in pinnipeds. Since the current paper is the first to document potential microplastic exposure among wild, living and free-ranging grey seals of the western North Sea, further research is needed to begin to understand the biological significance of these findings.
O’Connor J. D., Lally H. T., Mahon A. M., O’Connor I., Nash R., O’Sullivan J. J., Bruen M., Heerey L., Koelmans A. A., Marnell F., Murphy S. (2022): Microplastics in Eurasian otter (Lutra lutra) spraints and their potential as a biomonitoring tool in freshwater systems. Ecosphere 13: e3955.
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The ubiquitous nature of microplastics in aquatic ecosystems may have serious implications for aquatic biota. While microplastic research in freshwater ecosystems is increasing, very few studies have assessed the physical presence of microplastics among top predators. The Eurasian otter (Lutra lutra), a top predator of aquatic ecosystems, is one of the most widely distributed otter species and has a broad habitat niche. The opportunistic collection of otter spraints (i.e., feces) presents a valuable opportunity to assess pollutants of freshwater ecosystems through noninvasive means. Here, we assessed the prevalence, abundance, and concentration of microplastics (100 μm to 5 mm), as well as dietary remains, in 53 spraint samples collected over eight river catchments spanning three regions of Ireland. We found microplastics present in 57% of spraints at an abundance of 1.2 ± 0.1 microplastics (MPs)/spraint (mean ± SE) and a concentration of 3.8 ± 0.6 MPs/g (dry weight). Fibers were the dominant particle type recovered (85%), followed by film (10%). No significant differences in microplastic concentrations were detected between the three regions assessed, or between spraints collected from areas upstream (i.e., “lower” exposure) or downstream (“higher” exposure) of putative microplastic sources, which were defined using spatial vector data. While microplastic concentrations were not explained by spraint condition (i.e., fresh, drying, or dry), spraints collected in autumn had a significantly higher concentration than spring and summer. Furthermore, microplastic abundance or concentration could not be linked to dietary composition based on the items identified. From a trophic perspective, this study showed that the presence of microplastics in the feces of otter is most likely being obtained through its prey (i.e., secondary ingestion). While there may be limitations associated with using spraints as a biomonitoring tool for microplastics in freshwater systems, particularly with respect to otter home range and dietary niche breadth, they could still be employed for a regional assessment of microplastic levels.
Technau B., Unnsteinsdóttir E. R., Schaafsma F. L., Kühn S. (2022): Plastic and other anthropogenic debris in Arctic fox (Vulpes lagopus) faeces from Iceland. Polar Biology 45: 1403-1413.
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Anthropogenic debris, including plastic pollution, is a growing concern in the Arctic and negatively impacts both marine and coastal organisms. The aim of this study was to investigate the potential for using Arctic fox (Vulpes lagopus) faeces as a monitoring tool for plastic pollution in the Arctic environment. Arctic fox faeces were collected in different regions of Iceland and analysed for anthropogenic debris presence larger than 300 µm, and diet composition. In total, 235 faecal samples from 1999, 2017, 2018 and 2020 were analysed. The overall frequency of occurrence of plastic and other anthropogenic material was 5.11% and was found in samples across all regions and years. There were no statistical differences in anthropogenic debris ingested, depending on year or region. There were no obvious differences in diet composition between samples that contained anthropogenic debris and samples without. The suitability of Arctic fox faeces as a method to monitor plastic and anthropogenic debris levels in the Arctic environment remains debatable: Whilst the vast distribution range of the Arctic fox and the non-invasive collection methodology of faecal samples could be utilised as a good monitoring tool, the overall low uptake and unclear source of plastic and anthropogenic debris (marine or terrestrial) makes the interpretation of the data difficult. Nevertheless, debris ingestion by Arctic foxes remains a concern and warrants further studies.
Treu G., Sinding M. H. S., Czirják G. Á., Dietz R., Gräff T., Krone O., Marquard-Petersen U., Mikkelsen J.B., Schulz R., Sonne C., Søndergaard J., Sun J., Zubrod J., Eulaers I. (2022): An assessment of mercury and its dietary drivers in fur of Arctic wolves from Greenland and High Arctic Canada. Science of The Total Environment 838: 156171.
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Mercury has become a ubiquitous hazardous element even ending up in pristine areas such as the Arctic, where it biomagnifies and leaves especially top predators vulnerable to potential health effects. Here we investigate total mercury (THg) concentrations and dietary proxies for trophic position and habitat foraging (δ15N and δ13C, respectively) in fur of 30 Arctic wolves collected during 1869–1998 in the Canadian High Arctic and Greenland. Fur THg concentrations (mean ± SD) of 1.46 ± 1.39 μg g −1 dry weight are within the range of earlier reported values for other Arctic terrestrial species. Based on putative thresholds for Hg-mediated toxic health effects, the studied Arctic wolves have most likely not been at compromised health. Dietary proxies show high dietary plasticity among Arctic wolves deriving nutrition from both marine and terrestrial food sources at various trophic positions. Variability in THg concentrations seem to be related to the wolves’ trophic position rather than to different carbon sources or regional differences (East Greenland, the Foxe Basin and Baffin Bay area, respectively). Although the present study remains limited due to the scarce, yet unique historic study material and small sample size, it provides novel information on temporal and spatial variation in Hg pollution of remote Arctic species.
Lazarus M., Sergiel A., Ferenčaković M., Orct T., Kapronczai L., Pađen L., Janz D. M., Reljić S., Zwijacz-Kozica T., Zięba F., Selva N. (2023): Stress and reproductive hormones in hair associated with contaminant metal (loid) s of European brown bear (Ursus arctos). Chemosphere 325: 138354.
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Environmental contaminants like arsenic (As), cadmium (Cd), mercury (Hg) or lead (Pb) may disrupt hypothalamic–pituitary–adrenal (HPA) and hypothalamic-pituitary-gonadal (HPG) axes due to their endocrine toxicity potential. Resulting long-term physiological stress or adverse effects on wildlife reproduction and ontogeny may cause detrimental effects at the individual and population levels. However, data on environmental metal(loid)sʼ impact on reproductive and stress hormones in wildlife, especially large terrestrial carnivores, are scarce. Hair cortisol, progesterone and testosterone concentrations were quantified and modelled with hair As, Cd, total Hg, Pb, biological, environmental and sampling factors to test for potential effects in free-ranging brown bears (Ursus arctos) from Croatia (N = 46) and Poland (N = 27). Testosterone in males (N = 48) and females (N = 25) showed positive associations with Hg and an interaction between Cd and Pb, but a negative association with interaction between age and Pb. Higher testosterone was found in hair during its growth phase compared to quiescent phase. Body condition index was negatively associated with hair cortisol and positively associated with hair progesterone. Year and conditions of sampling were important for cortisol variation, while maturity stage for progesterone variation (lower concentrations in cubs and yearlings compared to subadult and adult bears). These findings suggest that environmental levels of Cd, Hg and Pb might influence the HPG axis in brown bears. Hair was shown to be a reliable non-invasive sample for investigating hormonal fluctuations in wildlife while addressing individual and sampling specificities.
Picone M., Distefano G. G., Zangrando R., Gambaro A., Ghirardini A. V. (2023): Neonicotinoids and pharmaceuticals in hair of the Red fox (Vulpes vulpes) from the Cavallino-Treporti peninsula, Italy. Environmental Research 228: 115837.
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Neonicotinoids (NEOs) and active pharmaceuticals ingredients (API) are contaminants widely diffused worldwide, causing increasing concern for potential adverse effects on wildlife. However, research on these contaminants have focused on target and non-target invertebrates, while information on potential effects in terrestrial mammals is lacking. We performed preliminary non-invasive monitoring of NEOs and API in a suburban and agricultural area using hair of the Red fox. The Red fox is a widely diffused mesopredator in Europe, and its plasticity in feeding habits makes it an excellent indicator for assessing exposure to environmental contamination. We observed the presence of NEOs in many Red fox hair samples (n = 11), including imidacloprid (IMI), acetamiprid (ACE), and clothianidin (CLO). The highest quantified concentrations were 6.4 ng g−1 dry weight (dw), 6.7 ng g−1 dw, and 0.9 ng g−1 dw for IMI, ACE, and CLO, respectively. The targeted APIs included non-steroidal anti-inflammatory drugs (NSAIDs) and antidepressants. APIs were less frequently detected than NEOs, and the compounds with the highest prevalence were the NSAID ketoprofen (36%), the antidepressant sertraline (36%), and its active metabolite norsertraline (27%). The presence of human pharmaceuticals such as the NSAID ibuprofen and the antidepressants sertraline, fluoxetine, and their active metabolites norsertraline and norfluoxetine suggest environmental contamination due to untreated and partially treated wastewater discharged in surface waters and soils of the study area. The detection and quantification of ketoprofen and flunixin also suggest the possible use of contaminated manure on farmland. Findings indicate that hair may be used for monitoring environmental exposure to NEOs and provide evidence that hair is a good marker of exposure for antidepressants and certain NSAIDs, including ibuprofen, ketoprofen, and flunixin.
CETACEANS
Lefebvre K. A., Bargu S., Kieckhefer T., Silver M. W. (2002): From sanddabs to blue whales: the pervasiveness of domoic acid. Toxicon 40: 971-977.
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Domoic acid (DA) is a potent food web transferred algal toxin that has caused dramatic mortality events involving sea birds and sea lions. Although no confirmed DA toxicity events have been reported in whales, here we present data demonstrating that humpback and blue whales are exposed to the toxin and consume DA contaminated prey. Whale fecal samples were found to contain DA at levels ranging from 10 to 207 μg DA g−1 feces via HPLC–UV methods. SEM analysis of whale feces containing DA, collected from krill-feeding whales, revealed the presence of diatom frustules identified as Pseudo-nitzschia australis, a known DA producer. Humpback whales were observed feeding on anchovies and sardines that contained DA at levels ranging from 75 to 444 μg DA g−1 viscera. DA contamination of whale feces and fish occurred only during blooms of toxic Pseudo-nitzschia. Additionally, several novel fish species collected during a toxic diatom bloom were tested for DA. Fish as diverse as benthic sanddabs and pelagic albacore were found to contain the neurotoxin, suggesting that DA permeates benthic as well as pelagic communities.
Doucette G. J., Mikulski C. M., King K. L., Roth P. B., Wang Z., Leandro L. F., DeGrasse S. L., White K. D., De Biase D., Gillett R. M., Rolland R. M. (2012): Endangered North Atlantic right whales (Eubalaena glacialis) experience repeated, concurrent exposure to multiple environmental neurotoxins produced by marine algae. Environmental Research 112: 67-76.
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The western North Atlantic population of right whales (Eubalaena glacialis) is one of the most critically endangered of any whale population in the world. Among the factors considered to have potentially adverse effects on the health and reproduction of E. glacialis are biotoxins produced by certain microalgae responsible for causing harmful algal blooms. The worldwide incidence of these events has continued to increase dramatically over the past several decades and is expected to remain problematic under predicted climate change scenarios. Previous investigations have demonstrated that N. Atlantic right whales are being exposed to at least two classes of algal-produced environmental neurotoxins—paralytic shellfish toxins (PSTs) and domoic acid (DA). Our primary aims during this six-year study (2001–2006) were to assess whether the whales’ exposure to these algal biotoxins occurred annually over multiple years, and to what extent individual whales were exposed repeatedly and/or concurrently to one or both toxin classes. Approximately 140 right whale fecal samples obtained across multiple habitats in the western N. Atlantic were analyzed for PSTs and DA. About 40% of these samples were attributed to individual whales in the North Atlantic Right Whale Catalog, permitting analysis of biotoxin exposure according to sex, age class, and reproductive status/history. Our findings demonstrate clearly that right whales are being exposed to both of these algal biotoxins on virtually an annual basis in multiple habitats for periods of up to six months (April through September), with similar exposure rates for females and males (PSTs: ∼70–80%; DA: ∼25–30%). Notably, only one of 14 lactating females sampled did not contain either PSTs or DA, suggesting the potential for maternal toxin transfer and possible effects on neonatal animals. Moreover, 22% of the fecal samples tested for PSTs and DA showed concurrent exposure to both neurotoxins, leading to questions of interactive effects. Targeted studies employing both in vivo and in vitro model systems represent the next logical step in assessing how and to what extent these algal biotoxins might compromise the health and reproduction of this endangered population.
Lundin J. I., Dills R. L., Ylitalo G. M., Hanson M. B., Emmons C. K., Schorr G. S., Ahmad J., Hempelmann J. A., Parsons K. M., Wasser S. K. (2016): Persistent organic pollutant determination in killer whale scat samples: optimization of a gas chromatography/mass spectrometry method and application to field samples. Archives of Environmental Contamination and Toxicology 70: 9-19.
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Biologic sample collection in wild cetacean populations is challenging. Most information on toxicant levels is obtained from blubber biopsy samples; however, sample collection is invasive and strictly regulated under permit, thus limiting sample numbers. Methods are needed to monitor toxicant levels that increase temporal and repeat sampling of individuals for population health and recovery models. The objective of this study was to optimize measuring trace levels (parts per billion) of persistent organic pollutants (POPs), namely polychlorinated-biphenyls (PCBs), polybrominated-diphenyl-ethers (PBDEs), dichlorodiphenyltrichloroethanes (DDTs), and hexachlorocyclobenzene, in killer whale scat (fecal) samples. Archival scat samples, initially collected, lyophilized, and extracted with 70 % ethanol for hormone analyses, were used to analyze POP concentrations. The residual pellet was extracted and analyzed using gas chromatography coupled with mass spectrometry. Method detection limits ranged from 11 to 125 ng/g dry weight. The described method is suitable for p,p′-DDE, PCBs-138, 153, 180, and 187, and PBDEs-47 and 100; other POPs were below the limit of detection. We applied this method to 126 scat samples collected from Southern Resident killer whales. Scat samples from 22 adult whales also had known POP concentrations in blubber and demonstrated significant correlations (p < 0.01) between matrices across target analytes. Overall, the scat toxicant measures matched previously reported patterns from blubber samples of decreased levels in reproductive-age females and a decreased p,p′-DDE/∑PCB ratio in J-pod. Measuring toxicants in scat samples provides an unprecedented opportunity to noninvasively evaluate contaminant levels in wild cetacean populations; these data have the prospect to provide meaningful information for vital management decisions.
Lundin J. I., Ylitalo G. M., Giles D. A., Seely E. A., Anulacion B. F., Boyd D. T., Hempelmann J. A., Parsons K. M., Booth R. K., Wasser S. K. (2018): Pre-oil spill baseline profiling for contaminants in Southern Resident killer whale fecal samples indicates possible exposure to vessel exhaust. Marine Pollution Bulletin 136: 448-453.
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The Southern Resident killer whale population (Orcinus orca) was listed as endangered in 2005 and shows little sign of recovery. Exposure to contaminants and risk of an oil spill are identified threats. Previous studies on contaminants have largely focused on legacy pollutants. Here we measure polycyclic aromatic hydrocarbons (PAHs) in whale fecal (scat) samples. PAHs are a diverse group of hazardous compounds (e.g., carcinogenic, mutagenic), and are a component of crude and refined oil as well as motor exhaust. The central finding from this study indicates low concentrations of the measured PAHs (<10 ppb, wet weight), as expected; however, PAHs were as high as 104 ppb prior to implementation of guidelines mandating increased distance between vessels and whales. While causality is unclear, the potential PAH exposure from vessels warrants continued monitoring. Historical precedent similarly emphasizes the importance of having pre-oil spill exposure data available as baseline to guide remediation goals.
Marangi M., Airoldi S., Beneduce L., Zaccone C. (2021): Wild whale faecal samples as a proxy of anthropogenic impact. Scientific Reports 11: 5822.
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The occurrence of protozoan parasite, bacterial communities, organic pollutants and heavy metals was investigated in free-ranging species of fin (Balaenoptera physalus, n. 2) and sperm (Physeter macrocephalus, n. 2) whales from the Pelagos Sanctuary, Corsican-Ligurian Provencal Basin (Northern-Western Mediterranean Sea). Out of four faecal samples investigated, two from fin whales and one from sperm whale were found positive to Blastocystis sp. A higher number of sequences related to Synergistetes and Spirochaetae were found in sperm whales if compared with fin whales. Moreover, As, Co and Hg were found exclusively in sperm whale faecal samples, while Pb was found only in fin whale faecal samples. The concentration of both PAH and PCB was always below the limit of detection. This is the first report in which the presence of these opportunistic pathogens, bacteria and chemical pollutants have been investigated in faecal samples of free-ranging whale species and the first record of Blastocystis in fin and sperm whales. Thus, this study may provide baseline data on new anthropozoonotic parasite, bacterial records and heavy metals in free-ranging fin and sperm whales, probably as a result of an increasing anthropogenic activity. This survey calls for more integrated research to perform regular monitoring programs supported by national and/or international authorities responsible for preservation of these still vulnerable and threatened whale species in the Mediterranean Sea.
ELEPHANTS
Sach F., Yon L., Henley M. D., Bedetti A., Buss P., de Boer W. F., Dierenfeld E. S., Gardner A., Langley-Evans S. C., Hamilton E., Lark R. M. (2020): Spatial geochemistry influences the home range of elephants. Science of the Total Environment 729: 139066.
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The unique geochemistry surrounding the Palabora Mining Company (PMC) land may act as a micronutrient hotspot, attracting elephants to the area. The PMC produces refined copper and extracts phosphates and other minerals. Understanding the spatial influence of geochemistry on the home range size of African elephants is important for elephant population management and conservation. The home ranges of collared elephants surrounding the PMC were significantly smaller (P = 0.001) than conspecifics in surrounding reserves, suggesting that their resource needs were met within these smaller areas. Environmental samples (soil, water and plants) were analysed from the mine area and along six transects radiating from the mine centre. Tail hair and faecal samples from elephants at the PMC, and conspecifics within the surrounding area were analysed. All samples were analysed for minerals essential to health and potentially toxic elements (PTEs; As, Ca, Cd, Cu, Fe, K, Mg, Mn, Na, P, Pb, Se, U, V and Zn). Results show that the geochemistry at the PMC is different compared to surrounding areas, with significant elevations seen in all analysed minerals and PTEs in soil closer to the mine, thereby drawing the elephants to the area. Additionally significant elevations were seen in elements analysed in water and vegetation samples. Elephant tail hair from elephants at the mine was significantly greater in Cd, whilst Mg, P, Cu, As, Cd, Pb and U concentrations were significantly greater in elephant faecal samples at the mine compared to the non-mine samples. When micronutrient hotspots overlap with human activity (such as mining), this can lead to poor human-elephant coexistence and thus conflict. When managing elephant populations, the influence of mineral provision on elephant movement must be considered. Such detailed resource information can inform conservation efforts for coordinated programmes (UN SDGs 15 and 17) and underpin sustainable economic activity (UN SDG 8, 11 and 12).
Sach F., Fields L., Chenery S., Yon L., Henley M. D., Buss P., Dierenfeld E. S., Langley-Evans S. C., Watts M. J. (2022): Method development to characterise elephant tail hairs by LA-ICP-MS to reflect changes in elemental chemistry. Environmental Geochemistry and Health 45: 1153-1164.
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This paper evaluated analytical methods used to generate time-series data from elephant tail hairs, which can be used to reflect changing exposure to environmental geochemistry. Elephant tail hairs were analysed by three methods sequentially, each providing data to inform subsequent analysis. Scanning Electron Microscopy (SEM) and X-ray Microanalysis visually showed the structure of the hair, specific structures such as tubules, and the mineral crusting around the edge of the hair, informing targeting of subsequent analysis by Laser Ablation-Inductively Coupled Plasma Mass Spectrometry (LA-ICP-MS). LA-ICP-MS generated time-series data which informed sectioning of the tail hairs for subsequent quantitative analysis for potentially toxic elements and micronutrients using Inductively Coupled Plasma Mass Spectrometry (ICP-MS) of dissolved tail hairs. This novel approach to characterise the tail hair enabled time-series analysis to reflect changes in environmental exposure which may result from seasonal or geochemical spatial variation and could inform elephant movement patterns. The seasonal change between wet and dry seasons was reflected down the length of the hair. Correlations were seen between LA-ICP-MS data and ICP-MS data in several elements including Mg, P, Ca, Fe, Na, Mn and U. This study provided time-series data for the analysis of elephant tail hairs by evaluating analytical challenges to obtaining quantitative data, such as improving protocols to ensure removal of extraneous material, determining where to section the tail hairs to best reflect environmental changes/exposure and ensuring representative analyses. A protocol was established to determine mineral status across a 12–18 month time period utilizing single elephant tail hairs.
HEDGEHOGS, SHREWS, AND DESMANS
D’Havé H., Scheirs J., Mubiana V. K., Verhagen R., Blust R., De Coen W. (2005): Nondestructive pollution exposure assessment in the European hedgehog (Erinaceus europaeus): I. Relationships between concentrations of metals and arsenic in hair, spines, and soil. Environmental Toxicology and Chemistry: An International Journal 24: 2356-2364.
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Conventional metal exposure assessment in terrestrial mammals is generally based on organ analyses of sacrificed animals. Few studies on mammals use nondestructive methodologies despite the growing ethical concern over the use of destructive sampling. Nondestructive methods involve minimal stress to populations and permit successive biomonitoring of the same populations and individuals. In the present study we assessed metal exposure of hedgehogs (Erinaceus europaeus) by investigating relationships between concentrations of metals (Ag, Al, Cd, Co, Cr, Cu, Fe, Mn, Ni, Pb, Zn) and As in soil samples and in hair and spines of hedgehogs. Samples were collected in seven study sites along a metal pollution gradient, characterized by decreasing total soil Ag, As, Cd, Cu, Ni, and Pb concentrations with increasing distance from a nonferrous metallurgic factory. For a number of elements, soil contamination was related both to distance to the smelter and to habitat. Soil concentrations were positively related to levels in hair and spines for Ag, As, Cd, and Pb and thus to hedgehog exposure. Metal concentrations in soil did not relate to metal concentrations in hair and spines for essential elements (e.g., Cu, Fe, Mn, Ni, and Zn), except Co in hair and soil. Our results demonstrate that, at least for nonessential elements, concentrations in soils can be used to predict contamination of these elements in hedgehogs or vice versa. Furthermore, hedgehog exposure increased toward the smelter and was higher for hedgehogs foraging in grasslands than for animals foraging in the forest. Moreover, we believe that hair and spines are promising tools in terrestrial wildlife exposure assessment studies of metals and As.
D’Havé H., Scheirs J., Mubiana V. K., Verhagen R., Blust R., De Coen W. (2006): Non-destructive pollution exposure assessment in the European hedgehog (Erinaceus europaeus): II. Hair and spines as indicators of endogenous metal and As concentrations. Environmental Pollution 142: 438-448.
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The role of hair and spines of the European hedgehog as non-destructive monitoring tools of metal (Ag, Al, Cd, Co, Cr, Cu, Fe, Ni, Pb, Zn) and As pollution in terrestrial ecosystems was investigated. Our results showed that mean pollution levels of a random sample of hedgehogs in Flanders are low to moderate. Yet, individual hedgehogs may be at risk for metal toxicity. Tissue distribution analyses (hair, spines, liver, kidney, muscle and fat tissue) indicated that metals and As may reach considerable concentrations in external tissues, such as hair and spines. Positive relationships were observed between concentrations in hair and those in liver, kidney and muscle for Al, Co, Cr, Cu, and Pb (0.43 < r < 0.85). Spine concentrations were positively related to liver, kidney and muscle concentrations for Cd, Co, Cr, Cu and Pb (0.37 < r < 0.62). Hair Ag, As, Fe and Zn and spine Ag, Al, As and Fe were related to metal concentrations in one or two of the investigated internal tissues (0.31 < r < 0.45). The regression models presented here may be used to predict metal and As concentrations in internal tissues of hedgehogs when concentrations in hair or spines are available. The present study demonstrated the possibility of using hair and spines for non-destructive monitoring of metal and As pollution in hedgehogs.
D’Havé H., Scheirs J., Covaci A., Schepens P., Verhagen R., De Coen W. (2006): Nondestructive pollution exposure assessment in the European hedgehog (Erinaceus europaeus): III. Hair as an indicator of endogenous organochlorine compound concentrations. Environmental Toxicology and Chemistry: An International Journal 25: 158-167.
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Concentrations of organochlorine persistent pollutants were investigated in tissues of the European hedgehog (Erinaceus europaeus). Road kills and carcasses from wildlife rescue centers were used to characterize organochlorine compound tissue distribution and tissue profile dissimilarities (hair, liver, kidney, muscle, and adipose tissue). The most important contaminants were polychlorinated biphenyls (PCBs), chlordanes (CHLs), and DDTs, with median concentrations of 75, 5.1, and 1.4 ng/g liver wet weight, respectively. Median levels for the remaining compounds—hexachlorobenzene (HCB), hexachlorocyclohexanes (HCHs), and octachlorostyrene—were less than 0.5ng/gliver wet weight. Compared to results with other mammalian wildlife, the present results indicate that hedgehogs may accumulate considerable concentrations of organochlorine compounds. Polychlorinated biphenyls and HCB preferably accumulated in liver and muscle tissue. Concentrations of DDTs and HCHs were highest in muscle tissue and hair, respectively. Octachlorostyrene and CHL levels were predominant in liver. The observed positive relationships between concentrations in hair and internal tissues for PCBs, DDTs, HCB, HCHs, and CHLs (0.49 < r < 0.91) and for several individual PCB, DDT, and CHL compounds (0.31 < r < 0.76) indicate the usefulness of hair as a biomonitoring tool of organochlorine compounds. Multivariate profile analyses revealed a higher dominance of less-persistent compounds (p,p′-DDT, α-HCH, and PCBs 95, 101, and 149) in hair compared to internal tissues. The present study demonstrates the suitability of hedgehog hair as a nondestructive biomonitoring tool regarding pollution with organochlorine compounds and the promising role of the hedgehog as a mammalian indicator species of pollution in terrestrial environments.
Vermeulen F., D’Havé H., Mubiana V. K., Van den Brink N. W., Blust R., Bervoets L., De Coen W. (2009): Relevance of hair and spines of the European hedgehog (Erinaceus europaeus) as biomonitoring tissues for arsenic and metals in relation to blood. Science of the Total Environment 407: 1775-1783.
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Hair has been proven to be suitable for non-destructive and non-invasive exposure assessments in human and mammal populations. A previous study with European hedgehog (Erinaceus europaeus) showed that, for some metals, hair and spine metal concentrations were positively correlated to levels in liver, kidney and muscle. Although blood has been studied in a wide variety of species, the relationship between hair and blood metal concentrations has yet to be quantified in many mammalian species. Tissue concentrations from hedgehogs residing in a park with known metal pollution were compared with those from a reference park and correlations between contaminant levels in hair and blood, and spines and blood were studied. Moreover, the relative distribution of arsenic and metals in hair, spines and blood was determined. Elevated concentrations were found in hedgehogs residing in the polluted site for As (8.2 μg/g, 6.3 μg/g, 3.6 μg/ml), Cd (0.48 μg/g, 0.17 μg/g, 0.02 μg/ml) and Pb (7.6 μg/g, 7.3 μg/g, 54 μg/ml), in hair, spines and blood respectively. Positive correlations were identified for exposure levels between hair and blood as well as between spines and blood for three elements (As, Cd, and Pb), whereas a negative correlation was found between Cr concentrations in spines and blood. In conclusion, hair and spines can be used to monitor blood concentrations of some metals, although more data are needed on uptake from the food chain and on the incorporation dynamics of these contaminants.
Dahmardeh Behrooz R., Poma G., Barghi M. (2022): Non-destructive mercury exposure assessment in the Brandt’s hedgehog (Paraechinus hypomelas): spines as indicators of endogenous concentrations. Environmental Science and Pollution Research 29: 56502-56510.
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Due to its persistence, bioaccumulation characteristics, and toxicity, environmental contamination with mercury (Hg) is of high concern for human health, living organisms, and ecosystems, and its biological monitoring is highly relevant. In this study, the levels of total Hg were measured in organs, tissues, and spines of 50 individuals of Brandt’s hedgehog collected in Iran in 2019. The Hg median levels in kidneys, liver, muscle, and spines were 156, 47, 47, and 20 ng/g dry weight, respectively. The results showed a significant positive correlation between the levels of Hg in kidneys and liver (r = 0.519; p < 0.01) and in spines and muscle (r = 0.337, p < 0.01) and kidneys (r = 0.309, p < 0.05). Significant differences (p < 0.05) in Hg levels in organs and tissues were also observed depending on the sex, weight, length, and age of the individuals. In addition, the median levels of total Hg in kidneys of Brandt’s hedgehogs from an agricultural ecotype (median 190 ± 65) were significantly higher (p < 0.05) than those collected from a forest ecotype (median 126 ± 50), suggesting that the habitat could have a significant impact on animal contamination.
MARSUPIALS
Burger J., Marquez M., Gochfeld M. (1994): Heavy metals in the hair of opossum from Palo Verde, Costa Rica. Archives of Environmental Contamination and Toxicology 27: 472-476.
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Levels of lead, cadmium, mercury, chromium, and manganese were measured in the hair of opossum (Didelphis virginiana) from Palo Verde, Guanacaste, Costa Rica. This area has some agriculture, but is slated for extensive water development that will increase ecosystem exposure to a variety of agricultural chemicals. Metal levels were generally not inter-correlated except for chromium and lead, chromium and cadmium, and cadmium and lead. There were significant gender differences only for lead and chromium, with the significantly smaller females having higher levels. It is suggested that hair from mammals, particularly abundant ominivores may be useful, bioindicators of environmental quality over a long time period.
Penrose B., MacIntosh A. E., Parbhakar-Fox A., Smith L. B., Sawyer T., D’Agnese E., Carver S. (2022): Heavy metal wombats? Metal exposure pathways to bare-nosed wombats (Vombatus ursinus) living on remediated tin mine tailings. Science of The Total Environment 835: 155526.
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Rehabilitation of disused mine sites through stabilisation and botanical restoration is ecologically important, but metal transfer pathways to colonising wildlife are often less understood and have never been studied in marsupials. The rehabilitated Royal George tin mine tailings (Tasmania, Australia) and colonisation by bare-nosed wombats (Vombatus ursinus) represented an opportunity to examine potential metal transfer from mine tailings to an herbivorous marsupial. The aim of this study was to examine metal transfer pathways from the mine tailings to wombats, and to determine if wombats are at risk from metal exposure. Concentrations of metals were measured in the tailings substrate, surface water and vegetation, as well as fur samples from a resident wombat, and non-resident (control) wombats. The mineralogy of the tailings is dominated by quartz, muscovite, feldspars, topaz, kaolinite and calcite. Concentrations of several metals were high (exceeding varying health standards) in the tailings (As, Cu, Hg, Pb, Ni, Zn), water (As, Cd, Cu, Zn) and vegetation (As, Cd, Cu, Pb, Mn, Zn). Relative to non-resident wombats, elevated levels of As, Cd, Cu, Pb and Sn were measured in the fur of a resident wombat. Based on modelling of the exposure pathways, consumption of plant material is the most likely metal transfer pathway for As, Cu and Pb, although the risks from ingestion of tailings to this fossorial marsupial should not be discounted. This study is the first to investigate metal exposure pathways to marsupials using rehabilitated mine tailings. Further research is needed to accurately quantify ecological risks and toxicity for wombats and other marsupials native to mining landscapes.
PRIMATES
Liu Q., Chen Y. P., Maltby L., Ma Q. Y. (2015): Exposure of the endangered golden monkey (Rhinopithecus roxellana) to heavy metals: a comparison of wild and captive animals. Environmental Science and Pollution Research 22: 6713-6720.
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Golden monkeys are endemic to China and of high conservation concern. Conservation strategies include captive breeding, but the success of captive breeding programs may be being compromised by environmental pollution. Heavy metal exposure of wild and captive golden monkeys living in the Qinling Mountains was assessed by measuring fecal metal concentrations (As, Cd, Cr, Co, Cu, Mn, Hg, Ni, Pb, and Zn). Captive monkeys were exposed to higher concentrations of As, Hg, Pb, and Cr than monkeys living in the wild, while high background levels of Mn led to high exposure of wild monkeys. Seasonal variations in metal exposures were detected for both wild and captive monkeys; possible reasons being seasonal changes in either diet (wild monkeys) or metal content of food (captive monkeys). Coal combustion, waste incineration, and traffic-related activities were identified as possible sources of heavy metals exposure for captive animals. Efforts to conserve this endangered primate are potentially compromised by metal pollutants derived from increasing anthropogenic activities. Providing captive animals with uncontaminated food and relocating captive breeding centers away from sources of pollution will reduce pollutant exposure; but ultimately, there is a need to improve environmental quality by controlling pollutants at source.
Hassim N. A., Hambali K., Idris N. S. U., Amir A., Ismail A., Zulkifli S. Z., Sow A. Y. (2018): Lead concentration in long-tailed macaque (Macaca fascicularis) hair in kuala Selangor, Malaysia. Tropical Life Sciences Research 29: 175.
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Long-tailed macaque (Macaca fascicularis) has the potential to be a good biological indicator for toxic exposure because they have an almost similar physiology and behaviour to humans. The objective of this study is to determine the concentration of lead (Pb) in hair samples of long-tailed macaques which were found in and out of the Kuala Selangor Nature Park (KSNP) area. The hypothesis is long-tailed macaques that live in the anthropogenic area (outside KSNP) may be exposed to high levels of lead compared to long-tailed macaques living in the forest area (inside KSNP). Analysis of hair samples were carried out using Inductively Coupled Plasma-Mass Spectrometry (ICP-MS). The study found that the average mean of lead concentration in the anthropogenic area is 6.31 μg/g while for the forest area it is 3.16 μg/g. Lead concentration in the two areas are statistically insignificant. Nevertheless, lead concentration in the anthropogenic area recorded a slightly higher mean concentration than in the forest area. Even so, results of this study indicate that long-tailed macaques in Kuala Selangor are not exposed to high levels of lead. This study is the first in Malaysia to utilise long-tailed macaques as a biological indicator for testing the concentration of toxic substances in the environment. This study is still in its early stages; thus, future research requires improvements.
Wang S., Steiniche T., Rothman J. M., Wrangham R. W., Chapman C. A., Mutegeki R., Quiros R., Wassermann M. D., Venier M. (2020): Feces are effective biological samples for measuring pesticides and flame retardants in primates. Environmental Science and Technology 54: 12013-12023.
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The habitats of wild primates are increasingly threatened by surrounding anthropogenic pressures, but little is known about primate exposure to frequently used chemicals. We applied a novel method to simultaneously measure 21 legacy pesticides (OCPs), 29 current use pesticides (CUPs), 47 halogenated flame retardants (HFRs), and 19 organophosphate flame retardants in feces from baboons in the U.S.A., howler monkeys in Costa Rica, and baboons, chimpanzees, red-tailed monkeys, and red colobus in Uganda. The most abundant chemicals were α-hexachlorocyclohexane (α-HCH), β-hexachlorocyclohexane (β-HCH), and hexachlorobenzene among OCPs across all sites, chlorpyrifos among CUPs in Costa Rica and Indiana, decabromodiphenylethane (DBDPE) in Costa Rica and Indiana and 2, 2′, 4, 4′-tetrabromodiphenyl ether (BDE-47) in Uganda as HFRs, and tris(2-butoxyethyl) phosphate (TBOEP) as OPFRs across all sites. The detected chemical concentrations were generally higher in red-tailed monkeys and red colobus than in chimpanzees and baboons. Our methods can be used to examine the threat of chemical pollutants to wildlife, which is critical for endangered species where only noninvasive methods can be used.
Krief S., Iglesias-González A., Appenzeller B. M., Rachid L., Beltrame M., Asalu E., Okimat J. P., Kane-Maguire N., Spirhanzlova P. (2022): Chimpanzee exposure to pollution revealed by human biomonitoring approaches. Ecotoxicology and Environmental Safety 233: 113341.
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Wildlife is increasingly exposed to environmental pollution, but data illustrating to what extent this exposure can impact health and survival of endangered species is missing. In humans, hair matrix analysis is a reliable tool for assessing cumulative exposure to organic pollutants such as pesticides but has rarely been used in other primates for this purpose. LC/MS-MS and GC/MS-MS multi-residue methods were used to screen the presence of 152 organic pollutants and their metabolites belonging to 21 different chemical families in hair samples from our closest relative, the chimpanzee. Samples were collected from 20 wild chimpanzees in Sebitoli, Kibale National Park, Uganda and 9 captive chimpanzees in the Réserve Africaine de Sigean, France. In total, 90 chemicals were detected, 60 in wild chimpanzees and 79 in captive chimpanzees. The median concentrations of detected chemicals in captive individuals were significantly higher than those in wild chimpanzees. Hair from the captive individuals at RAS was sampled a second time after 6 months in an environment of reduced exposure to these pollutants (diet of organic food, decreased use of plastic food and water containers). The number of chemicals detected in captive chimpanzees reduced from 79 to 63, and their concentrations were also significantly reduced. In the present study we report for the first time the use of hair analysis to detect organic pollutants in primate hair. We conclude that both wild and captive chimpanzees are exposed to a large range of different chemicals through their diet. Our study provides surprising and alarming evidence that besides the direct threats of poaching, deforestation and diseases, wild chimpanzees might be endangered by indirect consequences of anthropic activities. As chimpanzees are our closest relatives, our results should be considered as an alert for human health as well.
Steiniche T., Wang S., Chester E., Mutegeki R., Rothman J. M., Wrangham R. W., Chapman C. A., Venier M., Wasserman M. D. (2023): Associations between faecal chemical pollutants and hormones in primates inhabiting Kibale National Park, Uganda. Biology Letters 19: 20230005.
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While anthropogenic pollutants are known to be a threat to primates, our understanding of exposure to pollutants in situ and their sub-lethal effects is still limited. We used non-invasive biomonitoring to examine associations between faecal concentrations of 97 chemical pollutants and faecal hormone metabolites of cortisol and oestradiol in four primate species inhabiting Kibale National Park, Uganda (chimpanzees—Pan troglodytes, olive baboons—Papio anubis, red colobus—Piliocolobus tephrosceles and red-tailed monkeys—Cercopithecus ascanius). Across all species (n = 71 samples), results demonstrated positive associations of organochlorine pesticides (OCPs) (β = 0.143, p = 0.020) and organophosphate esters (β = 0.112, p = 0.003) with cortisol in adult females. Additionally, we observed positive associations of OCPs (β = 0.192, p = 0.013) and brominated flame retardants (β = 0.176, p = 0.004) with cortisol in juveniles. Results suggest that cumulative pesticides and flame retardants are disruptive to endocrine function in these populations, which could have implications for development, metabolism and reproduction. Our study further demonstrates that faeces can be an important, non-invasive matrix for examining pollutant–hormone associations in wild primates and other critical wildlife populations.
RABBITS, HARES, AND PIKAS
Kompiš M., Ballová Z. K. (2021): The influence of preferred habitat and daily range of the European hare on its contamination by heavy metals: a case study from the West Carpathians. Environmental Science and Pollution Research 28: 52093-52105.
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The Spišská Magura mountain range, located in the Middle Spiš, is one of the regions in Slovakia most contaminated by heavy metals resulting from mining and smelting activities. Heavy metals and other potentially toxic elements have accumulated in mountain areas via atmospheric transport. The influence of the daily range size of the European hare on its contamination by heavy metals was investigated in three habitat types (forest, woodland edge, meadow) in the Spišská Magura mountain range in the West Carpathians. Individual hares (n = 21) were traced and located by GPS following snowfall. Pair samples of their faeces (n = 64) and food (n = 64) were collected from feeding sites. The maps created were used for determination of the size of the daily range as being small or large. All hares that have a small daily range avoid meadows and open spaces due to the higher predation risk. However, individuals with a large daily range feed in all habitats, including meadows. Hares with a small daily range in a forest habitat ingested higher amounts of bio-elements Ca, Cr, S, and Mn as well as higher amounts of heavy metals Ba and Pb than hares with a large daily range. Moreover, dominant hares with a small daily range, with access to abundant food sources in a forest habitat, may gradually take on higher levels of bio-elements including heavy metals that are present in their food source. In contrast, in the woodland edge, hares with a small daily range had a smaller concentration of Ca, Cr, Mn, S, Ba, and Pb compared to hares with a large daily range. Caecotrophy plays a very significant role as far as the intake of nutrients and other elements is concerned. We found significant dependence between concentrations of the elements Cr, S, Ba, Pb, and Cd in the food of European hares and in their faeces.
RODENTS
Beernaert J., Scheirs J., Leirs H., Blust R., Verhagen R. (2007): Non-destructive pollution exposure assessment by means of wood mice hair. Environmental Pollution 145: 443-451.
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Concentrations of cadmium, copper, lead and zinc were measured in hair, kidney, liver, lung and muscle tissue of wood mice captured along a pollution gradient. We found positive relationships between cadmium concentrations in hair and all internal tissues. Hair lead concentrations were positively correlated with lead contents in kidney and liver. Age had a significant effect on cadmium accumulation in all tissues and hair. Apart from a very weak relationship between zinc concentrations in hair and liver, no significant relation between copper or zinc content in hair and any of the internal organs was observed. In summary, our observations suggest that hair of wood mice can be used for monitoring exposure to non-essential metals like cadmium and lead, but not to homeostatically regulated metals such as copper or zinc.
Marcheselli M., Sala L., Mauri M. (2010): Bioaccumulation of PGEs and other traffic-related metals in populations of the small mammal Apodemus sylvaticus. Chemosphere 80: 1247-1254.
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The accumulation of the platinum group elements (PGEs), Pd, Pt, Rh, and other heavy metals (Cd, Cr, Cu, Mn, Ni, Pb, Zn) in the wood mouse Apodemus sylvaticus was investigated in relation to environmental availability, comparing levels in the commonly used target tissues, the liver and kidney, to hair responses. In particular the research aimed to evaluate the suitability of a non-destructive hair-based biomonitoring approach and the responsiveness of PGEs as tracers for the environmental hazard assessment of pollutants linked to traffic in intensively anthropized areas. The four populations considered, inhabiting an urban, a suburban, an agricultural and a reference site, respectively, were shown to be capable of characterizing the differently polluted areas. In particular, multivariate analysis showed a significant correlation between metal levels in tissues and soils. Animals from both the urban and suburban sites, compared to those from the reference site, showed higher levels of those elements (PGEs, Cd, Cr, Ni, Pb and Zn), the availability of which is likely to be related to road traffic. On the contrary, Mn and Cu characterized the animals from the agricultural site. Even though the detected metal concentrations in tissues did not exceed the LOAEL levels, stress indices such as the PGE, Cd and Pb kidney/liver ratios and the kidney/body weight ratios were found to be altered. Significant correlations were established between hair and both internal tissues and soils, for non-essential metals PGEs, Cd, Ni and Pb, and also for biologically essential Zn, the level of which was high in urban soils. Hair proved to be a suitable non-invasive tool for monitoring metal exposure responses in small mammals.
Tête N., Afonso E., Crini N., Drouhot S., Prudent A. S., Scheifler R. (2014): Hair as a noninvasive tool for risk assessment: do the concentrations of cadmium and lead in the hair of wood mice (Apodemus sylvaticus) reflect internal concentrations?. Ecotoxicology and Environmental Safety 108: 233-241.
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There is an increasing need for developing noninvasive markers of accumulation when studying the transfer of pollutants in wildlife, in response to problems caused by sacrifice of animals (disturbed population dynamics, respect of ethical protocols). Thus, the aim of this work was to determine whether trace metal (TM) concentrations in hair could be used as an accurate noninvasive estimator of internal and environmental concentrations. For that purpose, on a 40 km² site surrounding an ancient smelter, 321 wood mice (Apodemus sylvaticus) were sampled on seven squares (500×500 m) and 4 squares in fall 2010 and spring 2011, respectively. The relationships between the cadmium (Cd) and lead (Pb) concentrations in hair and those in the liver, kidneys, and soils were described. The results indicated that hair concentration was a relatively good predictor of Pb concentrations in organs (p<0.001, 0.46<R²<0.53). In contrast, Cd concentrations in organs were only weakly predicted by hair concentrations in session 2010 (p<0.001, R2=0.10 for both organs), and no significant relationship was found in session 2011 (p=0.252 for liver and p=0.971 for kidneys). The Cd and Pb concentrations in the soil and in hair were not linearly related, but concentrations in hair increased with soil concentrations (Spearman’s rank correlations). Linear relationships between internal and hair concentrations differed significantly between the sampling sessions, especially for Cd. When they were included in models analyzing the relationships between TM concentrations in organs and in hair, individual characteristics (gender and body mass as a non-lethal estimation of relative age) increased the explained variability of Cd in organs but not of Pb. In conclusion, hair should be used cautiously to predict internal Cd concentrations but can be considered as an accurate noninvasive estimator of internal Pb concentrations. Further studies should be performed to develop, generalize, and apply this useful possible tool for risk assessment in ecotoxicology.
Lurz P. W., Krauze-Gryz D., Gryz J., Meredith A., Schilling A. K., Thain C., Heller E. (2017): Invisible threats to native mammals-mercury levels in three Eurasian red squirrel populations. Hystrix 28: 280-283.
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Understanding how biodiversity, ecosystem function and species conservation are affected by factors such as climate or land use change, disease and pollution is an important aspect of species conservation and a key focus of the field of Conservation Medicine. Mammals such as squirrels can be valuable biological sentinels for environmental pollution and the intention of this pilot project was to test a new, rapid technique that allows direct detection of mercury (Hg) in hair samples. Our aim was to establish, for the first time, if red squirrels in Europe show any indication of mercury pollution; and to compare levels from red squirrels in two rural UK (Arran and Brownsea Island) and one Polish city population (Warsaw). The latter is exposed to higher levels of Hg from coal-fired power plants. Total mercury levels ranged from 11.1 to 801.95 μg/kg. Contrary to our expectations, females from the Island of Arran had significantly higher Hg values than either males or females from the two other sites. Although the Isle of Arran was the only site where the difference between females and males was significant, our findings for both Poland and the UK suggest that mercury does not only accumulate in marine food chains and the arctic ecosystem, but is present in urban ecosystems and terrestrial woodlands. Data on trends to determine if Hg values are accumulating in arboreal mammals are completely lacking, and point to a need for a monitoring strategy of mercury levels and associated, potential health impacts in endangered species.
da Silva Yang S. G. N., da Silva I. J. S., e Souza D. D. S., da Fonseca C. F., da Silva Santiago A. C., Soares P. C., de Oliveira J. B. (2021): Multi-elemental exposure assessment through concentrations in hair of free-ranging capybaras (Hydrochoerus hydrochaeris Linnaeus, 1766) in the Atlantic Forest remnants, Northeast of Brazil. Chemosphere 262: 127800.
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This study aimed to determine the mineral profile of hair samples of free-ranging capybaras (Hydrochoerus hydrochaeris) in remnants of the Atlantic Forest located in the Northeast of Brazil, and to evaluate the effects of origin, gender and age of the animals on their mineral accumulation in hair. Twenty hair samples from animals of different areas, genders and ages were prepared using microwave-assisted digestion, employing 5 mL of HNO3 and 2.5 mL of H2SO4 for 100 mg of sample. Digestion efficiency was assessed by residual carbon content. The digested samples were analyzed by inductively coupled plasma optical emission spectrometry (ICP OES). Principal component analysis (PCA) was performed considering the composition data of 11 elements (Al, Ca, Cd, Co, Cr, Cu, Fe, K, Mn, Mo, and Na). The digestion method applied was efficient and the most abundant elements with their respective concentration ranges in mg kg−1 were Al (396–2746), Ca (36–3420), Fe (476–51180), K (115–4843), and Na (72–473). ANOVA and PCA differentiated among the capybaras regarding age (adults) and origin (A3), both associated with higher concentrations of Al, Cd, Fe, and K. Although a higher metal bioaccumulation was observed in adult animals, it is important to highlight that this result could have been affected by diet and physiological parameters. The results suggest that A3 was the most anthropized remnant area due to agricultural and urban influences. Multi-elemental determination in hair can be used as a non-invasive method to assess heavy metal contamination in capybaras.
Fritsch C., Appenzeller B., Burkart L., Coeurdassier M., Scheifler R., Raoul F., Driget V., Powolny T., Gagnaison C., Rieffel D., Afonso E., et al. (2022): Pervasive exposure of wild small mammals to legacy and currently used pesticide mixtures in arable landscapes. Scientific Reports 12: 15904.
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Abstract
Knowledge gaps regarding the potential role of pesticides in the loss of agricultural biodiversity worldwide and mixture-related issues hamper proper risk assessment of unintentional impacts of pesticides, rendering essential the monitoring of wildlife exposure to these compounds. Free-ranging mammal exposure to legacy (Banned and Restricted: BRPs) and currently used (CUPs) pesticides was investigated, testing the hypotheses of: (1) a background bioaccumulation for BRPs whereas a “hot-spot” pattern for CUPs, (2) different contamination profiles between carnivores and granivores/omnivores, and (3) the role of non-treated areas as refuges towards exposure to CUPs. Apodemus mice (omnivore) and Crocidura shrews (insectivore) were sampled over two French agricultural landscapes (n = 93). The concentrations of 140 parent chemicals and metabolites were screened in hair samples. A total of 112 compounds were detected, showing small mammal exposure to fungicides, herbicides and insecticides with 32 to 65 residues detected per individual (13–26 BRPs and 18–41 CUPs). Detection frequencies exceeded 75% of individuals for 13 BRPs and 25 CUPs. Concentrations above 10 ng/g were quantified for 7 BRPs and 29 CUPs (in 46% and 72% of individuals, respectively), and above 100 ng/g for 10 CUPs (in 22% of individuals). Contamination (number of compounds or concentrations) was overall higher in shrews than rodents and higher in animals captured in hedgerows and cereal crops than in grasslands, but did not differ significantly between conventional and organic farming. A general, ubiquitous contamination by legacy and current pesticides was shown, raising issues about exposure pathways and impacts on ecosystems. We propose a concept referred to as “biowidening”, depicting an increase of compound diversity at higher trophic levels. This work suggests that wildlife exposure to pesticide mixtures is a rule rather than an exception, highlighting the need for consideration of the exposome concept and questioning appropriateness of current risk assessment and mitigation processes.
UNGULATES
Pokorny B., Al Sayegh-Petkovšek S., Ribarič-Lasnik C., Vrtačnik J., Doganoc D. Z., Adamič M. (2004): Fungi ingestion as an important factor influencing heavy metal intake in roe deer: evidence from faeces. Science of the Total Environment 324: 223-234.
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In nature, animals have to cope with the fluctuating bioavailable metal pool in their habitat, which results in a seasonal variability of heavy metal levels in the animal body. Indeed, a pronounced summer–autumnal peak of heavy metals in roe deer (Capreolus capreolus L.) kidney was recently found in Slovenia. Considering the well-known hyperaccumulative ability of fungi, their ingestion was hypothesised to be one of the main reasons for the peak. Although fungi as a group are known to be a seasonally important food source for roe deer, data on their composition in the nutrition of the species have been lacking. To ascertain the importance of fungi ingestion on heavy metal intake in roe deer, we simultaneously studied fungal spores (by microscopic determination) and heavy metal levels (by inductively coupled plasma mass spectrometry and atomic absorption spectrometry) in roe deer faeces, collected in the period July–November 2001 at Veliki Vrh, the Šalek Valley, Slovenia. Irrespective of species, fungal spores were present in 89% of faeces; the following genera were found to be consumed by roe deer: Lycoperdon, Calvatia, Hypholoma, Coprinus, Russula, Elaphomyces, Xerocomus, Enteloma, Amanita, Cortinarius, Agaricus, Inocybe, Boletus, Macrolepiota, Suillus and Pluteus. While the importance of fungi ingestion on the seasonal variability of other metals is less clear, it doubtless influences Hg intake in roe deer, which is confirmed by: (a) the high frequency of fungi in roe deer nutrition; (b) their hyperaccumulative ability; (c) the temporal distribution of Hg in roe deer faeces; (d) differences among three classes of faeces established on the basis of the frequency of spores present; (e) the correlation between the number of fungal genera present and Hg levels in faeces. Therefore, the influence of fungi ingestion has to be taken into consideration in assessing the hazard due to the accumulation of mercury along the food-chain.
Sobańska M. A. (2005): Wild boar hair (Sus scrofa) as a non-invasive indicator of mercury pollution. Science of the Total Environment 339: 81-88.
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This paper investigates the usefulness of wild boar (Sus scrofa) hair as a non-invasive indicator of mercury pollution. Samples were collected in two hunting seasons (1998/1999 and 1999/2000) by hunters from four differently polluted regions of Poland. Mercury content was determined by AAS methods. Different washing procedures were compared. De-ionised water was found to be suitable for the removal of exogenous mercury sources in hair analysis. Metal distribution along hair was analysed. It was found that problems arising from differences in distribution of metal along a single hair strand as well as differences in the hair colour can be eliminated through the careful homogenisation of the samples before analysis. The influences of physiological, ecological and environmental factors that might significantly affect the obtained results (age, gender, season, location of habitat and diet of the sampled animals) were estimated and taken into account. The present study revealed that female hair contained a higher amount of mercury than male hair. Moreover the highest mercury content was found in young individuals between 1 and 2 years of age. A positive correlation of the present results with environmental data taken from the State Offices showed an influence of environmental pollution on the mercury level in wild boar hair.
Beyer W. N., Gaston G., Brazzle R., O’Connell Jr A. F., Audet D. J. (2007): Deer exposed to exceptionally high concentrations of lead near the Continental Mine in Idaho, USA. Environmental Toxicology and Chemistry: An International Journal 26: 1040-1046.
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Habitat surrounding the inactive Continental Mine in northern Idaho, USA, supports bear (Ursus arctos, Ursus americanus), moose (Alces alces), elk (Cervus elaphus), woodland caribou (Rangifer tarandus caribou), and abundant mule (Odocoileus hemionus) and white-tailed deer (Odocoileus virginianus). Tailings on the mining site were capped and remediated in 2003 to reduce environmental exposure of surrounding soil and sediments of Blue Joe Creek, downslope of the mine. Before capping, the mean Pb concentration in deer pellets collected on-site was 920 mg/kg of Pb (dry wt). This exposure, if chronic, would be comparable to an exposure that could be lethal to cattle or horses. Surprisingly, the mean pellet Pb concentration of 950 mg/kg in 2004 was as high as it was before remediation, and it was related to a high rate of soil ingestion. Mean soil content of the pellets collected from the capped site in 2004 was 22% dry weight, estimated from the acid-insoluble ash, a marker of soil ingestion. Clumps of sand and bits of rock were observed inside some of the pellets, and Pb concentrations in the pellets were correlated (p < 0.05) with soil content. Although terrestrial risk assessments generally estimate exposure from diets and from incidentally ingested soil, the deer at this site were directly ingesting contaminated soil or mining waste. The mean Pb concentration of this ingested soil was estimated as 6,700 mg/kg and the maximum as 25,000 mg/kg, well above the Pb concentrations measured in the remediated cap. The deer seemed to be ingesting soil or mining waste from one or more small but highly contaminated sources located beyond the remediated cap.
Pacyna A. D., Frankowski M., Kozioł K., Węgrzyn M. H., Wietrzyk-Pełka P., Lehmann-Konera S., Polkowska Ż. (2019): Evaluation of the use of reindeer droppings for monitoring essential and non-essential elements in the polar terrestrial environment. Science of the Total Environment 658: 1209-1218.
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Excess or toxic metals, non-metals and metalloids can be eliminated from the organism by deposition in inert tissue (e.g. fur) or excretion with body secretions, urine and faeces. Droppings are one of the main routes for the elimination of multiple elements and they can be collected without direct contact with the animal. Contaminant concentration has been examined in non-lethally collected tissues of several species (especially reptilian, avian and mammalian). However, studies on species residing in polar areas are still limited, especially of mammals from the European Arctic. Reindeers are the only large herbivores living in Svalbard, being an essential part of the Arctic terrestrial ecosystem. Although reindeer presence has a high impact on their surroundings, those huge mammals are rarely part of ecotoxicological studies regarding metal pollution. In this paper, the droppings of Svalbard reindeer were used as a non-invasively collected tissue to examine the excretion pathway of 30 elements. Samples were collected in mesic and moss tundra, representing summer, winter and winter-transitional excretion. For more than a half of the studied elements, significant differences occurred between the samples collected in the two tundra types. The feasibility of older and fresh samples was assessed based on summer droppings, and significant differences were found for K, As, Mn, Na, Ni, and Sb concentrations. No relevant differences in element levels were observed for samples collected from adult females, adult males and calves, except for zinc and potassium. Results show that reindeer droppings are an important vector for the transfer of many metals, non-metals and metalloids including calcium, phosphorus, zinc, aluminium and lead. As a sedentary species, feeding on local food sources, Svalbard reindeer is a valuable indicator of trace element presence in the polar terrestrial ecosystem.
Pacyna-Kuchta A. D., Wietrzyk-Pełka P., Węgrzyn M. H., Frankowski M., Polkowska Ż. (2020): A screening of select toxic and essential elements and persistent organic pollutants in the fur of Svalbard reindeer. Chemosphere 245: 125458.
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Reindeers play an important role in the polar ecosystem, being long-lived sole vegetarians feeding on local vegetation. They can be used as a valuable bioindicator, helping us to understand contaminants’ impact on the polar terrestrial ecosystem. Still, scarce data exist from research in which polar herbivores (especially those from the European parts of the Arctic) were a major study subject for trace elements and persistent organic pollutant determination. Here, Svalbard reindeer fur has been used to determine metals, non-metals and metalloids using ICP-MS, and several persistent organic pollutants including polycyclic aromatic hydrocarbons (PAHs), organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) using gas chromatography coupled to a tandem mass spectrometer (GC-MS/MS). Samples were collected from reindeer populations living in the area near Ny-Ålesund and Longyearbyen. Essential elements like Fe, Mg, Zn, K, Ca, Cu predominated in the trace elements profile. Median values of As, Cd, Co, Li, Ni, Se and V were all below 0.5 μg/g dw. Mercury was below detection limit in all samples, while the Pb median varied from 0.35 to 0.74 μg/g dw. Except acenaphthylene and fluorene, PAHs were detectable only in samples collected in the vicinity of Longyearbyen. Of 15 studied pesticides, only DDT and its metabolites were above the detection limit, and, of PCBs, only PCB28.
Draghi S., Agradi S., Riva F., Tarhan D., Bilgiç B., Dokuzeylül B., Ercan A. M., Or M. E., Brecchia G., Vigo D., Arioli F. (2023): Roe deer (Capreolus capreolus) hair as a bioindicator for the environmental presence of toxic and trace elements. Toxics 11: 49.
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The return to pasture use as an alternative to intensive livestock farming implies some risks with the lack or the excessive presence of potentially toxic elements; in this regard, wild animals have been used as bioindicators for decades. Thus, the purpose of this study is quantifying Cu, Cr, Mn, Zn, Se, As, Cd, Ni, Pb, Al, Fe, and Mg in fur from roe deer and understanding if it is a valid bioindicator tool. Hair was collected from 39 hunted roe deer and divided by age (<36 months old/≥36 months old), sex (male/female), and area of origin (urbanized/rural area). The mean concentrations of Fe, Mg, Mn, Al, Cr, and Pb were higher (p < 0.05) in the urbanized group; the mean levels of Mg and Cr were higher (p < 0.05) in older animals; and Cu, Fe, Mg, Cd, and Cr showed a higher accumulation in females. Our findings showed an age-related variation of elements, with higher concentrations in adult animals and females. In conclusion, our findings prove that hair is a valid matrix for this type of survey, and wild animals are good bioindicators for monitoring the presence of trace elements in pastures.
MULTIPLE SPECIES
Yin X., Xia L., Sun L., Luo H., Wang Y. (2008): Animal excrement: a potential biomonitor of heavy metal contamination in the marine environment. Science of the Total Environment 399: 179-185.
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To assess the feasibility of using animal excrement to biomonitor the extent of heavy metal contamination in the marine environment, concentrations of mercury (Hg), lead (Pb), copper (Cu) and zinc (Zn) in the fresh excrement of seabirds and marine mammals, along with other biomaterials, from the Arctic, Antarctica (West and East), and Xisha Archipelago of the South China Sea were determined. Results show that the excrement of marine animals at higher trophic levels generally contained high levels of Hg, demonstrating the biomagnification of Hg through food chains in different remote regions. Significant variations in metal accumulation in the excrements were observed among the distinctive geographical areas, with the highest Hg concentration in Xisha Archipelago and the highest Pb concentration in the Arctic, which reflects different levels of air metal pollution at various sampling locations. Concentrations of Cu in the excrements primarily correlate to the geochemical background levels in the regions. High Cu concentrations were found near the Great Wall Station in West Antarctica where a copper mineralized belt exists. No clear spatial variation pattern was found for Zn accumulation in the excrement. This study shows that animal excrement can be used as bioindicators for the level of metal contamination in the marine environment, with the advantages of easy sampling, accurate detection (i.e., with high levels of metal accumulation), and reconstructing historical metal contamination trends by long-term monitoring of sedimentary excrements.
McLean C. M., Koller C. E., Rodger J. C., MacFarlane G. R. (2009): Mammalian hair as an accumulative bioindicator of metal bioavailability in Australian terrestrial environments. Science of the Total Environment 407: 3588-3596.
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The current study represents the first investigation of the suitability of marsupial and eutherian mammalian hair as indicator tissue for metal exposure and accumulation within contaminated Australian terrestrial ecosystems. A soil metal contamination gradient was established across 22 sites at increasing distances from a decommissioned Lead/Zinc smelter in NSW, Australia. Within each site, soil and small mammal populations were sampled. An Australian native marsupial, the insectivorous Brown Antechinus, Antechinus stuartii: Dasyuridae, and introduced rodents, the omnivorous Brown or Norway Rat, Rattus norvegicus: Muridae and the Black Rat, Rattus rattus: Muridae were assessed for hair concentrations of Cadmium (Cd), Copper (Cu), Lead (Pb) and Zinc (Zn). Metals in soil were most elevated at sites within close proximity to the smelter, with soil metal concentrations decreasing with distance from the smelter. The non-essential metals Pb and Cd were accumulated in hair, both metals exhibiting positive linear relationships with environmental exposure (soil metal concentrations). When the variables of weight and snout-vent length were considered, no further contribution in terms of explaining the variability in hair Cd or Pb was observed for all species examined. The essential metals Cu and Zn were regulated in hair, remaining similar across the metal contamination gradient. A significant negative correlation between snout-vent length and hair Cu concentration was found for the Brown Rat; greater hair Cu concentrations were found in smaller individuals of this species. Accumulation of Pb to hair was similar among species while concentrations of Cd in Brown Rat hair were higher than both Black Rat and Brown Antechinus hair. As each of the three aforementioned species exhibit similar bioaccumulation relationships for Pb, we suggest that sampling hair from introduced rodents (pest species) may provide a suitable proxy for the assessment of Pb bioavailability for a range of small mammals within Australian urban remnants.
Gil-Jiménez E., Mateo R., de Lucas M., Ferrer M. (2020): Feathers and hair as tools for non-destructive pollution exposure assessment in a mining site of the Iberian Pyrite Belt. Environmental Pollution 263: 114523.
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Mining is responsible of releasing trace elements to the environment with potential negative effects on wildlife. Traditionally, wildlife exposure assessment has been developed by analyzing mainly environmental compartments or internal tissues. Nowadays, the use of non-destructive matrices such as hair or feathers has increased. Nevertheless, its use in free-living terrestrial mammals or in birds other than raptors or passerines is less frequent. The main objective of our study was to determine the potential for hair and feathers in a rabbit and bird species to be used as non-invasive proxy tissues for assessing internal metal concentrations at polluted sites from mining. We tested whether hair of European rabbit (Oryctolagus cuniculus) and feathers of red-legged partridge (Alectoris rufa) can be used as non-destructive biological monitoring tools of both essential (Cu, Zn) and non-essential (Pb, Cd, As) trace elements in a currently active copper mining site. We found significant different concentrations, particularly in non-essential elements, between reference area and mining site. Non-essential elements Pb and Cd showed higher correlations between tissues and hair/feathers, while few significant patterns were observed for essential elements such as Cu and Zn. Although feathers showed lower levels of correlation with internal tissues than hair, both could be useful as non-destructive biological monitoring tools. Further tissues, and more importantly, hair and feathers allowed discrimination between polluted and reference sites to indicate bioavailability and pollution status. In addition, hair and feathers can be used in monitoring pollution of an active mining site, being specially interesting for biomonitoring a certain period of time in the event of a particular episode of pollution, in addition to the chronic exposure. As occurred with hair in rabbits, feathers seem to be a good compartment to detect differences between a potential polluted area, such the surrounding of an active mine site, and a non-polluted area.
Fritsch C., Appenzeller B., Burkart L., Coeurdassier M., Scheifler R., Raoul F., Driget V., Powolny T., Gagnaison C., Rieffel D, Afonso E., Goydadin A.-C., Hardy E. M., Palazzi P., Schaeffer C., Gaba S., Bretagnolle V., Bertrand C., Pelosi C. (2022): Pervasive exposure of wild small mammals to legacy and currently used pesticide mixtures in arable landscapes. Scientific Reports 12: 15904.
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Knowledge gaps regarding the potential role of pesticides in the loss of agricultural biodiversity worldwide and mixture-related issues hamper proper risk assessment of unintentional impacts of pesticides, rendering essential the monitoring of wildlife exposure to these compounds. Free-ranging mammal exposure to legacy (Banned and Restricted: BRPs) and currently used (CUPs) pesticides was investigated, testing the hypotheses of: (1) a background bioaccumulation for BRPs whereas a “hot-spot” pattern for CUPs, (2) different contamination profiles between carnivores and granivores/omnivores, and (3) the role of non-treated areas as refuges towards exposure to CUPs. Apodemus mice (omnivore) and Crocidura shrews (insectivore) were sampled over two French agricultural landscapes (n = 93). The concentrations of 140 parent chemicals and metabolites were screened in hair samples. A total of 112 compounds were detected, showing small mammal exposure to fungicides, herbicides and insecticides with 32 to 65 residues detected per individual (13–26 BRPs and 18–41 CUPs). Detection frequencies exceeded 75% of individuals for 13 BRPs and 25 CUPs. Concentrations above 10 ng/g were quantified for 7 BRPs and 29 CUPs (in 46% and 72% of individuals, respectively), and above 100 ng/g for 10 CUPs (in 22% of individuals). Contamination (number of compounds or concentrations) was overall higher in shrews than rodents and higher in animals captured in hedgerows and cereal crops than in grasslands, but did not differ significantly between conventional and organic farming. A general, ubiquitous contamination by legacy and current pesticides was shown, raising issues about exposure pathways and impacts on ecosystems. We propose a concept referred to as “biowidening”, depicting an increase of compound diversity at higher trophic levels. This work suggests that wildlife exposure to pesticide mixtures is a rule rather than an exception, highlighting the need for consideration of the exposome concept and questioning appropriateness of current risk assessment and mitigation processes.
Webster A. B., Callealta J. F., Bennett N. C., Ganswindt A. (2022): Non-lethal assessment of potentially toxic elements across mammalian trophic levels in African savannahs. Frontiers in Environmental Science 9: 794487.
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South Africa is one of the most diverse countries in the world but the increase in agricultural, industrial and technological development to meet the needs of the growing human population has led to increased amounts of potentially toxic elements (PTEs) and other chemicals in the environment. As regional and global environmental processes influence local conditions to differing degrees, all organisms within a specific environment are exposed to highly complex, ill-defined PTE and chemical mixtures. Differences in feeding strategies within and between vertebrate trophic levels are likely to influence the degree to which individuals may be exposed to and affected by PTE presence. Using vertebrate faeces as a biological matrix, we investigate and compare quantitative differences in PTE concentrations in herbivorous, omnivorous and carnivorous terrestrial vertebrates from two protected areas in South African savannah. Of the eleven PTEs assessed [aluminium (Al), arsenic (As), barium (Ba), cadmium (Cd), chromium (Cr), mercury (Hg), lead (Pb), antimony (Sb), tin (Sn), strontium (Sr), and vanadium (V)], the highest concentrations of Al, As, Cr, Pb, Sn, and V were found in carnivores. General patterns were evident between groups at each site for specific elements, but absolute values for the same elements were site-specific. This is the first study to non-invasively examine and compare PTE concentrations in a variety of free-ranging mammalian wildlife occupying different trophic levels within South African protected areas. Our results confirm that all individuals across trophic levels within these sites are exposed to multiple and varied PTE mixtures on a continuous basis. Whether PTEs at these concentrations cause synergistic or antagonistic disruption of physiological and biological systems alone or in combination in free-ranging African wildlife species is still unclear and requires further investigation.