Mercury (Hg) is a global pollutant with potentially severe health impacts on humans and wildlife, especially raptors, which face high exposure due to trophic magnification and long-term environmental integration. Raptors are widely used as Hg environmental biomonitors, with feathers and eggs favored for their easy, minimally invasive collection, transport, and storage. While raptor feathers and eggs have been commonly used to retrospectively analyze Hg time series, few studies have examined physiological and ecological processes driving matrix-specific patterns. This study compared 34-year (1986–2019) time series of Hg in tail feathers and eggs of tawny owls (Strix aluco) in central Norway, accounting for plasticity in their dietary sources (i.e., adjusted temporal trends), proxied by stable isotopes of nitrogen (δ15N) and carbon (δ13C; corrected for the Suess effect). Generalized Additive Models assessed temporal trends and potential drivers. Unadjusted temporal trends (Year only) differed between feathers and eggs, whereas unadjusted and adjusted (for dietary proxies) trends did not differ within each matrix. Differences between matrices may reflect varying Hg sequestration mechanisms or integration windows. δ13C appeared as the main driver of Hg variability in both matrices, likely indicating shifts in carbon sources in tawny owl diets over time. Future studies should focus on obtaining more accurate information on environmental and biological sources and pathways over time, to better understand their influence on Hg time series in this established biomonitoring species.
Over the past decades, the widespread use of pesticides has raised concerns about their effects on non-target organisms. Among pesticides, fungicides remain comparatively understudied, despite representing nearly 40% of total pesticide sales in Europe. Wild birds living in or close to farmlands are frequently exposed to tebuconazole, a triazole fungicide widely used in agroecosystems. While its effects on avian physiology and life-history traits have been the subject of several studies, the downstream effects that this agrochemical may exert on host-parasite interactions remain poorly understood. Here, we investigated whether chronic exposure to tebuconazole alters the dynamics of avian malaria chronic infection in house sparrows (Passer domesticus). Wild-caught adults were maintained under semi-natural conditions and malaria infection was monitored before and after an eleven-week exposure period to tebuconazole ingestion, starting in late autumn and ending in mid-winter. At the beginning of the experiment, 70% of the birds were chronically infected with malaria. Then, while prevalence declined in control individuals during winter, as typically expected in passerines living in temperate climates, it increased by 20% in tebuconazole-exposed individuals. No significant difference in parasite load was observed between control and exposed birds, suggesting that tebuconazole did enhance parasite replication rate but may instead have promoted the reappearance of parasites from exo-erythrocytic stages. Our findings highlight that exposure to tebuconazole can influence chronic malaria dynamics. Future work should assess how combined exposure to multiple pesticides and environmental stressors might exacerbate these effects, with broader implications for host-parasite interactions in agricultural landscapes.
Although trace metal toxicity has been extensively studied in laboratory settings, its long-term effects on wildlife are poorly understood. Most wild animals are likely to be exposed to low doses of trace metals throughout their lives; however, whether such chronic exposure affects fitness-related traits in natural populations remains to be investigated. In this study, we tested the relationships between trace metal burden and sex hormones, primary and secondary sexual traits in wild male roe deer. Using samples collected from 71 hunted males, we measured the hair and liver concentrations of various toxic trace metals, faecal testosterone metabolites (FTM), testis mass and antler length. We focused on cadmium (Cd), cobalt (Co), nickel (Ni) and lead (Pb) in roe deer tissues. Using linear (mixed effects) models, we found that Cd and, to a lesser extent, Co concentrations in the liver, but not in hair, were negatively associated with absolute testicular mass, a proxy of sperm production. However, metal burden, measured in either the liver or hair, was not related to antler length or FTM levels, despite their respective roles in male competitiveness for access to females and the underlying adjustments for seasonal breeding. Hence, our findings highlight the consequences of exposure to Cd and Co on male testicular function in a wild ungulate. Any alteration in male competitiveness for fertilization is expected to have lasting fitness consequences, which could subsequently alter population dynamics.
Preservation of biodiversity and ecosystem services is critical for sustainable development and human well-being. However, an unprecedented erosion of biodiversity is observed and the use of plant protection products (PPP) has been identified as one of its main causes. In this context, at the request of the French Ministries responsible for the Environment, for Agriculture and for Research, a panel of 46 scientific experts ran a nearly 2-year-long (2020–2022) collective scientific assessment (CSA) of international scientific knowledge relating to the impacts of PPP on biodiversity and ecosystem services. The scope of this CSA covered the terrestrial, atmospheric, freshwater, and marine environments (with the exception of groundwater) in their continuity from the site of PPP application to the ocean, in France and French overseas territories, based on international knowledge produced on or transposable to this type of context (climate, PPP used, biodiversity present, etc.). Here, we provide a brief summary of the CSA’s main conclusions, which were drawn from about 4500 international publications. Our analysis finds that PPP contaminate all environmental matrices, including biota, and cause direct and indirect ecotoxicological effects that unequivocally contribute to the decline of certain biological groups and alter certain ecosystem functions and services. Levers for action to limit PPP-driven pollution and effects on environmental compartments include local measures from plot to landscape scales and regulatory improvements. However, there are still significant gaps in knowledge regarding environmental contamination by PPPs and its effect on biodiversity and ecosystem functions and services. Perspectives and research needs are proposed to address these gaps.
Small plastic fragments (<5 mm, i.e., microplastics, MPs) accumulate in ecosystems, resulting in increasing concerns about their toxic effects in the terrestrial environment. While studies on MPs in the soil environment are expanding, gaps in knowledge still exist regarding their effects on soil (macro)organisms. Our study aimed to measure the response of Cantareus aspersus snails to long-term exposure to 0.1, 1 and 10 % w/w polyethylene (PE), polyamide (PA) or polystyrene (PS) particles in food. Overall, a concentration-dependent decrease in snail growth was observed, as was a general trend toward earlier maturity at low and middle MP concentrations. Mild (for PS) to severe (for PE and PA) effects on reproduction were detected but without a concentration-dependent trend. The fecundity was affected mainly by PE at 1 % (-32.9 %) and by PA at 1 % (-52.59 %), and their fertility was reduced by 43.9 % and 61.3 %, respectively. This decrease was related to increased survival, suggesting trade-offs in snail energy allocation and/or endocrine regulation. This study revealed that an environmentally relevant life-cycle assessment of toxic effects allows the detection of subtle effects regarding individual responses. These effects allowed us to demonstrate differential impacts on animal health status according to the polymer used and the exposure concentration.
Glyphosate (GLY) is the most widely used herbicide worldwide, and its use continues to increase. Accumulating evidence shows that GLY and its metabolite aminomethylphosphonic acid (AMPA) are more persistent and toxic than expected, but little is known about the risks to wildlife. Glufosinate (GLUF) was considered an alternative broad-spectrum herbicide, but its field ecotoxicology has rarely been studied. This study aimed to assess the exposure of free-ranging rodents and shrews from treated (cereals under conventional farming) and nontreated habitats (cereals under organic farming and hedgerows) in France to GLY, AMPA, and GLUF through residue analyses in hair. We investigated the patterns of accumulation according to species, habitat, and treatment intensity at the plot, landscape, or township scale. We showed a generalized exposure of small mammals to GLY, AMPA and GLUF, as they were detected in all of the species, and in 64%, 51% and 44% of the hair samples, respectively. The detection and levels of GLY, AMPA and GLUF were greater in herbivorous and omnivorous voles than in insectivorous shrews and omnivorous wild mice. The three compounds showed comparable ranges of concentrations: 0.018-7.74 pg/mg with an outlier of 522 pg/mg for GLY (median = 2.65 pg/mg), 0.240-33.6 pg/mg for AMPA (median = 1.39 pg/mg), and 1.16-25.5 pg/mg for GLUF (median = 3.51 pg/mg). The frequencies of detection and concentrations did not significantly differ according to the farming practices or proxies of pesticide treatment intensity. The concentrations of GLY were greater in individuals captured in hedgerows than in those captured in cereal fields. On the basis of dose reconstruction approaches and toxicological thresholds from the literature, GLY and GLUF levels may be associated with risk in small mammals and endanger local populations. Our findings raise issues about the omnipresence of GLY, AMPA and GLUF in agricultural landscapes, including in animals from habitats considered refuges, questioning their ecological safety. This work provides new insights into current broad-spectrum herbicide wildlife ecotoxicology that may support decision-making to protect biodiversity.
European farmland bird populations have declined by over 60% in 40 years, with the use of pesticides suspected to be one of the main causes of this decline. However, it remains difficult to test the impact of these pesticides in field studies due to confounding environmental variables that can also affect avian wildlife (e.g., food resources, habitat fragmentation and alteration). Triazoles are a family of fungicides that are ubiquitous in agro-ecosystems due to their use on a wide range of crops. Triazoles are suspected to affect non-target avian species by disrupting key physiological mechanisms and by detrimentally affecting their reproduction. In this captive study, we experimentally investigated the effect of the most commonly used triazole fungicides (i.e., tebuconazole) on the reproduction of an avian species representative of farmlands, the house sparrow (Passer domesticus). We examined the impacts of tebuconazole at realistic concentrations (550 μg.L-1 in drinking water to achieve ∼ 60 pg g-1 in plasma of sparrows) under controlled conditions on multiple indicators of breeding performance (clutch size, hatching success, chick growth and survival). We found that chronic exposure to tebuconazole (9 months, including the breeding period) significantly altered the reproduction of sparrows. Although clutch size and hatching success were not affected by tebuconazole, chicks from the exposed group showed reduced growth and a higher mortality rate. Interestingly, these effects were exacerbated in female chicks, highlighting a sex-dependent effect of tebuconazole on sparrow offspring. This study demonstrates that tebuconazole can be detrimental to the reproduction of farmland birds. Further studies are now required to distinguish the direct effects of tebuconazole (toxic and sublethal effects on the developing chick/embryo) from the indirect ones (alteration of egg quality and parental care).
Plant protection products (PPPs) have historically been one of the classes of chemical compounds at the frontline of raising scientific and public awareness of the global nature of environmental pollution and the role of trophic interactions in shaping the impacts of chemicals on ecosystems. Despite increasingly strong regulatory measures since the 1970s designed to avoid unintentional effects of PPPs, their use is now recognised as a driver of biodiversity erosion. The French Ministries for the Environment, Agriculture and Research commissioned a collective scientific assessment to synthesise the current science and knowledge on the impacts of PPPs on biodiversity and ecosystem services. Here we report a literature review of the state of knowledge on the propagation of PPP residues and the effects of PPPs in food webs, including biopesticides, with a focus on current-use PPPs. Currently used PPPs may be stronger drivers of the current biodiversity loss than the banned compounds no longer in use, and there have been far fewer reviews on current-use PPPs than legacy PPPs. We first provide a detailed overview of the transfer and propagation of effects of PPPs through trophic interactions in both terrestrial and aquatic ecosystems. We then review cross-ecosystem trophic paths of PPP propagation, and provide insight on the role of trophic interactions in the impacts of PPPs on ecological functions. We conclude with a summary of the available knowledge and the perspectives for tackling the main gaps, and address areas that warrant further research and pathways to advancing environmental risk assessment.
Triazoles are among the most widely used fungicides in the world due to their efficacy against fungal crop diseases and their broad spectrum of action. Intensive use of triazoles has resulted in residual contamination in different compartments of agroecosystems and exposes non-target species to potential sublethal effects. Triazoles are known to be immunomodulators in medicine and therapeutic treatments, but very little data is available on their potential effect on immune parameters of non-target vertebrate species living in agroecosystems. In this study, we experimentally examined the impact of tebuconazole on three immune biomarkers (haemagglutination titre (HA), haemolysis titre (HL), and haptoglobin concentration (Hp)), as well as on the body condition of house sparrows (Passer domesticus). Our results suggest that tebuconazole had very little, if any, effect on the studied immune parameters. However, further studies are needed to better assess the effect of tebuconazole on bird immunity because (1) experimental individuals were kept under optimal conditions and the impact of tebuconazole on immunity may occur under suboptimal conditions, (2) only one concentration of tebuconazole was tested and its effect could be dose-dependent and (3) other complementary immunological biomarkers should be studied, given the complexity of the vertebrate immune system. Current knowledge on the potential effects of triazoles on the immunity of wild farmland vertebrates is still largely insufficient. Further physiological and immune studies should be conducted to better understand the effect of triazole fungicides on farmland birds.
“A Who’s Who of pesticides is therefore of concern to us all. If we are going to live so intimately with these chemicals eating and drinking them, taking them into the very marrow of our bones - we had better know something about their nature and their power.” — Rachel Carson, Silent Spring. In her day, Rachel Carson was right: plant protection products (PPP) like all the other chemical substances that humans increasingly release into the environment without further precaution, are among our worst enemies today (Bruhl and Zaller, 2019; Naidu et al, 2021; Tang et al, 2021; Topping et al, 2020). All compartments of the biosphere, air, soil and water, are potential reservoirs within which all species that live there are impaired. Birds are particularly concerned: PPP are recognized as a factor in the decline of their abundance and diversity predominantly in agricultural landscapes. Due to the restrictions on vertebrates testing, in silico based approaches are an ideal choice alternative given input data are available. This is where the problem lies as we will illustrate in this paper. We performed an extensive literature search covering a long period of time, a wide diversity of bird species, a large range of chemical substances and as many model types as possible to encompass all our future need to improve environmental risk assessment of chemicals for birds. In the end, we show that poultry species exposed to pesticides are the most studied at the individual level with physiologically based toxicokinetic models. To go beyond, with more species, more chemical types, over several levels of biological organization, we show that observed data are crucially missing (Gilbert, 2011). As a consequence, improving existing models or developing new ones could be like climbing Everest if no additional data can be gathered, especially on chemical effects and toxicodynamic aspects.
Agricultural practices are a major cause of the current loss of biodiversity. Among postwar agricultural intensification practices, the use of plant protection products (PPPs) might be one of the prominent drivers of the loss of wildlife diversity in agroecosystems. A collective scientific assessment was performed upon the request of the French Ministries responsible for the Environment, for Agriculture and for Research to review the impacts of PPPs on biodiversity and ecosystem services based on the scientific literature. While the effects of legacy banned PPPs on ecosystems and the underlying mechanisms are well documented, the impacts of current use pesticides (CUPs) on biodiversity have rarely been reviewed. Here, we provide an overview of the available knowledge related to the impacts of PPPs, including biopesticides, on terrestrial vertebrates (i.e. herptiles, birds including raptors, bats and small and large mammals). We focused essentially on CUPs and on endpoints at the subindividual, individual, population and community levels, which ultimately linked with effects on biodiversity. We address both direct toxic effects and indirect effects related to ecological processes and review the existing knowledge about wildlife exposure to PPPs. The effects of PPPs on ecological functions and ecosystem services are discussed, as are the aggravating or mitigating factors. Finally, a synthesis of knowns and unknowns is provided, and we identify priorities to fill gaps in knowledge and perspectives for research and wildlife conservation.
AbstractLow levels of essential mineral elements such as cobalt, copper, and iron, in organisms reduce immune function, increasing the chances of parasitic infection. This phenomenon has been demonstrated widely in domestic animals but rarely in wildlife. In this study, we used data from 7‐ to 9‐month‐old roe deer (Capreolus capreolus), living in two different populations facing contrasting environmental conditions (Trois‐Fontaines and Chizé), to investigate whether the parasitic and immunological statuses could be related to essential element status. Between 2016 and 2019, we collected feces to measure parasite burdens (gastrointestinal and pulmonary nematodes), blood to measure immunological parameters (globulins and white blood cells), and hair to assess the concentration of 11 essential elements (calcium [Ca], chromium [Cr], cobalt [Co], copper [Cu], iron [Fe], magnesium [Mg], manganese [Mn], potassium [K], molybdenum [Mo], selenium [Se], and zinc [Zn]). The results showed first heterogeneity in the individual phenotypes of the two populations. Roe deer with low body mass had high concentrations of all the essential elements (in particular, Ca, Fe, Cu, K, and Mn), a high parasitic burden, and high concentrations of globulins. An association between high concentrations of essential elements and a high parasite burden was found at the two study sites despite markedly different environmental conditions. A relationship between essential element concentrations and immune parameters was also detected, with more basophils and globulins being associated with high concentrations of essential trace elements (i.e., Ca, Fe, Cu, and, to a lesser extent, Se, Cr, and Zn). These results suggest that young individuals with low body mass and high parasitism may select feeding resources rich in mineral elements, which may improve their ability to control the infestation and/or mitigate the negative consequences of parasites by maintaining immune system functions.
Neonicotinoids are the most widely used class of insecticides in the world, but they have raised numerous concerns regarding their effects on biodiversity. Thus, the objective of this work was to do a critical review of the contamination of the environment (soil, water, air, biota) by neonicotinoids (acetamiprid, clothianidin, imidacloprid, thiacloprid, thiamethoxam) and of their impacts on terrestrial and aquatic biodiversity. Neonicotinoids are very frequently detected in soils and in freshwater, and they are also found in the air. They have only been recently monitored in coastal and marine environments, but some studies already reported the presence of imidacloprid and thiamethoxam in transitional or semi-enclosed ecosystems (lagoons, bays, and estuaries). The contamination of the environment leads to the exposure and to the contamination of non-target organisms and to negative effects on biodiversity. Direct impacts of neonicotinoids are mainly reported on terrestrial invertebrates (e.g., pollinators, natural enemies, earthworms) and vertebrates (e.g., birds) and on aquatic invertebrates (e.g., arthropods). Impacts on aquatic vertebrate populations and communities, as well as on microorganisms, are less documented. In addition to their toxicity to directly exposed organisms, neonicotinoid induce indirect effects via trophic cascades as demonstrated in several species (terrestrial and aquatic invertebrates). However, more data are needed to reach firmer conclusions and to get a clearer picture of such indirect effects. Finally, we identified specific knowledge gaps that need to be filled to better understand the effects of neonicotinoids on terrestrial, freshwater, and marine organisms, as well as on ecosystem services associated with these biotas.
The exposure assessment component of a Wildlife Ecological Risk Assessment aims to estimate the magnitude, frequency, and duration of exposure to a chemical or environmental contaminant, along with characteristics of the exposed population. This can be challenging in wildlife as there is often high uncertainty and error caused by broad-based, interspecific extrapolation and assumptions often because of a lack of data. Both the US Environmental Protection Agency (USEPA) and European Food Safety Authority (EFSA) have broadly directed exposure assessments to include estimates of the quantity (dose or concentration), frequency, and duration of exposure to a contaminant of interest while considering "all relevant factors." This ambiguity in the inclusion or exclusion of specific factors (e.g., individual and species-specific biology, diet, or proportion time in treated or contaminated area) can significantly influence the overall risk characterization. In this review, we identify four discrete categories of complexity that should be considered in an exposure assessment-chemical, environmental, organismal, and ecological. These may require more data, but a degree of inclusion at all stages of the risk assessment is critical to moving beyond screening-level methods that have a high degree of uncertainty and suffer from conservatism and a lack of realism. We demonstrate that there are many existing and emerging scientific tools and cross-cutting solutions for tackling exposure complexity. To foster greater application of these methods in wildlife exposure assessments, we present a new framework for risk assessors to construct an "exposure matrix." Using three case studies, we illustrate how the matrix can better inform, integrate, and more transparently communicate the important elements of complexity and realism in exposure assessments for wildlife. Modernizing wildlife exposure assessments is long overdue and will require improved collaboration, data sharing, application of standardized exposure scenarios, better communication of assumptions and uncertainty, and postregulatory tracking. Integr Environ Assess Manag 2024;20:674-698. © 2023 SETAC.
Essential trace elements play an important role in the development of optimal immune responses, in particular to fight a parasitic infection, as it has been demonstrated many times in domestic animals, but rarely in wildlife. The aim of this study was to assess whether trace element concentrations could be a factor influencing parasitic infection and immune phenotype in roe deer (Capreolus capreolus) using factor analyses. From 2016 to 2019, we collected data on 7-9 months-old roe deer to assess 11 trace element concentrations (e.g. Ca, Co, Cr, Cu, Fe, K, Mg, Mn, Mo, Se, Zn) in hair, parasite burden (gastro-intestinal and pulmonary nematodes), and immunological parameters (globulines and white blood cells) in two French populations with different ecological contexts (Trois-Fontaines and Chizé). We showed a heterogeneity of individual phenotypes, with clear gradients opposing animals with low body mass, high concentrations of all trace elements (in particular Ca, Fe, Cu, K, and Mn), high parasitic burden and high concentrations of globulins to animals with the opposite characteristics. The association between high concentration in essential trace elements and high parasite burden was found at the two study sites despite markedly different environmental conditions. A relationship between trace element concentrations and immunological parameters was also identified, with more basophils and globulins associated to high concentrations of essential trace elements (i.e. Ca, Fe, Cu and to a lesser extent Se, Cr and Zn). These results suggest primarily that high parasite burden could predispose young individuals with low body mass to select a diet with a higher proportion of high trace element feed to minimize the infection. They suggest also that young roe deer with higher trace element concentrations will have a more reactive immune system.
Triazoles belong to a family of fungicides that are ubiquitous in agroecosystems due to their widespread use in crops. Despite their efficiency in controlling fungal diseases, triazoles are also suspected to affect non-target vertebrate species through the disruption of key physiological mechanisms. Most studies so far have focused on aquatic animal models, and the potential impact of triazoles on terrestrial vertebrates has been overlooked despite their relevance as sentinel species of contaminated agroecosystems. Here, we examined the impact of tebuconazole on the thyroid endocrine axis, associated phenotypic traits (plumage quality and body condition) and sperm quality in wild-caught house sparrows (Passer domesticus). We experimentally exposed house sparrows to realistic concentrations of tebuconazole under controlled conditions and tested the impact of this exposure on the levels of thyroid hormones (T3 and T4), feather quality (size and density), body condition and sperm morphology. We found that exposure to tebuconazole caused a significant decrease in T4 levels, suggesting that this azole affects the thyroid endocrine axis, although T3 levels did not differ between control and exposed sparrows. Importantly, we also found that exposed females had an altered plumage structure (larger but less dense feathers) relative to control females. The impact of tebuconazole on body condition was dependent on the duration of exposure and the sex of individuals. Finally, we did not show any effect of exposure to tebuconazole on sperm morphology. Our study demonstrates for the first time that exposure to tebuconazole can alter the thyroid axis of wild birds, impact their plumage quality and potentially affect their body condition. Further endocrine and transcriptomic studies are now needed not only to understand the underlying mechanistic effects of tebuconazole on these variables, but also to further investigate their ultimate consequences on performance (i.e. reproduction and survival).