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Publications

2024

Preliminary assessment of blood mercury contamination in Four African crocodile species 

J. Lemaire, P. Bustamante, M.H., Shirley

Environment International 190, (2024) 108877

Heavy metal contamination in the environment is an increasingly pervasive threat to the long-term persistence of wildlife. As high trophic level consumers, crocodylians are at substantial risk from bioaccumulation of mercury (Hg). Despite that they are generally well-studied and the focal species of many conservation efforts around the world, little is known about Hg contamination levels in most crocodylians. Here we preliminarily evaluate blood Hg contamination in four African species – Central African slender-snouted crocodile (Mecistops leptorhynchus), African dwarf crocodile (Osteolaemus tetraspis), West African crocodile (Crocodylus suchus), and Nile crocodile (Crocodylus niloticus) – from a diversity of sites and habitats across 5 different countries representing varying degrees of environmental pollution. All of our sampled crocodiles were Hg contaminated and, worryingly, these

African crocodiles generally showed the highest levels of Hg contamination of any crocodylian species examined to date. Of most concern was that Hg concentrations were not only highest in M. leptorhynchus, the most threatened amongst our study species, but also in individuals sampled in what are believed to be some of the most remote and pristine natural areas left in Africa – Gabon’s national parks. Our results underscore the need to better understand the impact of longstanding petroleum, mining, forestry, and agricultural industries on the entire aquatic food chain throughout much of Africa, including on the threatened species in these habitats and the human populations that depend on them for their subsistence and livelihoods.

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Mercury biomagnification in the food web of Agami Pond, Kaw-Roura Nature Reserve, French Guiana

J. Lemaire, R. Mangione, S. Caut, P. Bustamante

Heliyon 10 (2024), e28859

Freshwater ecosystems are among the most important ecosystems worldwide, however, over the last centuries, anthropogenic pressures have had catastrophic effects on them. Mercury (Hg) is one of the main environmental contaminants which globally affect ecosystems and particularly freshwater wildlife. While Hg originates from natural sources, anthropogenic activities such as agriculture, biomass combustion, and gold mining increase its concentrations. Gold mining activities are the main drivers of Hg emission in tropical ecosystems and are responsible for up to 38% of global emissions. Once in its methylated form (MeHg), mercury biomagnifies through the trophic chain and accumulates in top predators. Due to the toxicity of MeHg, long-lived predators are even more subjected to chronic effects as they accumulate Hg over time. In the present study we quantified Hg contamination in two top predators, the Black caiman

Melanosuchus niger and the Agami heron Agamia agami, and in their prey in the Kaw-Roura Nature Reserve in French Guiana and evaluated the biomagnification rate in the trophic chain. Our results show that despite a TMF in the range of others in the region (4.38 in our study), top predators of the ecosystem present elevated concentrations of Hg. We have found elevated Hg concentrations in the blood of adult Black caiman (2.10 ±0.652 μg g− 1 dw) and chicks of Agami heron (1.089 ±0.406 μg g− 1 dw). These findings highlight the need to better evaluate the potential impact of Hg in freshwater top predators, especially regarding reprotoxic effects.

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Spatial distribution of selenium-mercury in Artic searbirds

M. Cruz-Flores, J. Lemaire, M. Brault-Favrou, et al. 

Environmental Pollution 343 (2024), 123110

Mercury (Hg) is a metallic trace element toxic for humans and wildlife that can originate from natural and anthropic sources. Hg spatial gradients have been found in seabirds from the Arctic and other oceans, suggesting contrasting toxicity risks across regions. Selenium (Se) plays a protective role against Hg toxicity, but its spatial distribution has been much less investigated than that of Hg. From 2015 to 2017, we measured spatial co-exposure of Hg and Se in blood samples of two seabird species, the Brünnich’s guillemot (Uria lomvia) and the black-legged kittiwake (Rissa tridactyla) from 17 colonies in the Arctic and subarctic regions, and we calculated their molar ratios (Se:Hg), as a measure of Hg sequestration by Se and, therefore, of Hg exposure risk. We also evaluated concentration differences between species and ocean basins (Pacific-Arctic and Atlantic-Arctic), and examined the influence of trophic ecology on Hg and Se concentrations using nitrogen and carbon stable isotopes. In the Atlantic-Arctic ocean, we found a negative west-to-east gradient of Hg and Se for guillemots, and a positive west-to-east gradient of Se for kittiwakes, suggesting that these species are better protected from Hg toxicity in the European Arctic. Differences in Se gradients between species suggest that they do not follow environmental Se spatial variations. This, together with the absence of a general pattern for isotopes influence on trace element concentrations, could be due to foraging ecology differences between species. In

both oceans, the two species showed similar Hg concentrations, but guillemots showed lower Se concentrations and Se:Hg than kittiwakes, suggesting a higher Hg toxicity risk in guillemots. Within species, neither Hg, nor Se or Se:Hg differed between both oceans. Our study highlights the importance of considering Se together with Hg, along with different species and regions, when evaluating Hg toxic effects on marine predators in international

monitoring programs.

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Seabirds reveal mercury distribution across the North Atlantic

C. Albert, B. Moe, Strøm, H, et al. 


Proceedings of the National Academy of Sciences of the United States of America 121, (2024) e2315513121

Mercury (Hg) is a heterogeneously distributed toxicant affecting wildlife and human health. Yet, the spatial distribution of Hg remains poorly documented, especially in food webs, even though this knowledge is essential to assess large-scale risk of toxicity for the biota and human populations. Here, we used seabirds to assess, at an unprecedented population and geographic magnitude and high resolution, the spatial distribution of Hg in North Atlantic marine food webs. To this end, we combined tracking data of 837 seabirds from seven different species and 27 breeding colonies located across the North Atlantic and Atlantic Arctic together with Hg analyses in feathers representing indi- vidual seabird contamination based on their winter distribution. Our results highlight an east-west gradient in Hg concentrations with hot spots around southern Greenland and the east coast of Canada and a cold spot in the Barents and Kara Seas. We hypoth- esize that those gradients are influenced by eastern (Norwegian Atlantic Current and West Spitsbergen Current) and western (East Greenland Current) oceanic currents and melting of the Greenland Ice Sheet. By tracking spatial Hg contamination in marine ecosystems and through the identification of areas at risk of Hg toxicity, this study provides essential knowledge for international decisions about where the regulation of pollutants should be prioritized.

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Poison in the nursery: Mercury contamination in the tadpole-rearing sites of an Amazonian frog

L. Schlippe-Justicia, J. Lemaire, C. Dittrich, M. Mayer, P. Bustamante, B. Rojas

Science of the Total Environment 912 (2024), 169450

Artisanal and small-scale gold mining (ASGM) has become a major threat for Neotropical forests. This technique for obtaining gold is a substantial driver of small-scale deforestation and the largest contributor of Hg emissions to both the atmosphere and freshwater systems globally. Previous studies have demonstrated the impacts of Hg accumulation on various aquatic ecosystems and organisms. However, its consequences in other, more discrete

systems such as phytotelmata (water-holding plant structures), and the organisms therein, have so far gone unnoticed. Here, we show high concentrations of Hg (mean ±SD: 1.43 ±2.19 ppm) in phytotelmata and other small pools, the aquatic microenvironments used by the Neotropical poison frog Dendrobates tinctorius as tadpole- rearing sites. In 17 % of the cases, we detected Hg concentrations above the severe effect level (SEL =2 ppm) for  freshwater sediments. Hg concentrations varied depending on pool characteristics and tended to increase in

proximity to known ASGM sites. We did not find an effect of Hg concentration on the number of D. tinctorius tadpoles in a given pool. Tadpoles were found in pools with concentrations of up to 8.68 ppm, suggesting that D. tinctorius fathers do not avoid pools with high Hg levels for tadpole deposition. While further research is

needed to determine the potential effects of Hg on tadpole development, we found an intriguing tendency for tadpoles in later developmental stages to have lower body condition when occurring in pools with higher Hg concentrations. Our findings provide evidence of relevant Hg concentrations in the terrestrial water systems used by phytotelm-breeding anurans, and highlight the need of further field and experimental studies investigating the

implications of Hg contamination for tadpole development and behaviour and the overall conservation of Amazonian biodiversity.

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2023

Using Crocodylians for monitoring mercury in the tropics

J. Lemaire

Ecotoxicology 32, (2023) 977-993

Artisanal Small Scale Gold Mining (ASGM) activities are responsible for more than a third of atmospheric Hg emission. Due to Hg toxicity and its broad and elevated prevalence in the environment resulting from ASGM activities in the tropics, its biomonitoring is essential to better understand the availability of its methylmercury (MeHg) form in the environment. The Minamata Convention was ratified with the objective to “protect human health and the environment from anthropogenic emissions and releases of mercury compounds”. Biomagnification of MeHg occurs through the trophic food web, where it biomagnifies and bioaccumulates in top predators. To monitor environmental MeHg contamination, studies have evaluated the use of living organisms; however, reptiles are among the least documented vertebrates regarding MeHg exposure. In this review we evaluate the use of crocodylians for Hg biomonitoring in tropical ecosystems. We found that out of the 28 crocodiles species, only 10 have been evaluated regarding Hg contamination. The remaining challenges when using this taxon for Hg biomonitoring are inconsistencies in the applied methodology (e.g., wet versus dry weight, tissues used, quantification method). However, due to their life history traits, crocodylians are particularly relevant for monitoring MeHg contamination in regions where ASGM activities occur. In conclusion and given their ecological and socio-economic importance, crocodylians are at great risk of MeHg contamination and are excellent bioindicators for tropical ecosystems.

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2022

Relationships between stable isotopes and trace element concentrations in the crocodilian community of French Guiana 

J. Lemaire, F. Brischoux, O. Marquis, R. Mangione, S. Caut, M. Brault-Fabrou, C. Churlaud, P. Bustamante

Science of the Total Environment 837, (2022) 155846

Trace elements in the blood of crocodilians and the factors that influence their concentrations are overall poorly doc- umented. However, determination of influencing factors is crucial to assess the relevance of caimans as bioindicators of environmental contamination, and potential toxicological impact of trace elements on these reptiles. In the present study, we determined the concentrations of 14 trace elements (Ag, As, Cd, Cr, Co, Cu, Fe, Hg, Pb, Mn, Ni, Se, V, and Zn) in the blood of four French Guiana caiman species (the Spectacled Caiman Caiman crocodilus [n = 34], the Black Caiman Melanosuchus niger [n = 25], the Dwarf Caiman Paleosuchus palpebrosus [n = 5] and the Smooth- fronted Caiman Paleosuchus trigonatus [n = 20]) from 8 different sites, and further investigated the influence of individual body size and stable isotopes as proxies of foraging habitat and trophic position on trace element concentra- tions. Trophic position was identified to be an important factor influencing trace element concentrations in the four caiman species and explained interspecific variations. These findings highlight the need to consider trophic ecology when crocodilians are used as bioindicators of trace element contamination in environmental studies.

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2021

Lead, mercury, and selenium alter physiological functions in wild caimans (Caiman crocodiles)

J. Lemaire, P. Bustamante, R. Mangione, O. Marquis, C. Churlaud, M. Brault-Favrou, C. Parenteau, F. Brischoux

Environmental Pollution 286, (2021) 117549

Environmental contaminants affect ecosystems worldwide and have deleterious effects on biota. Non-essential mercury (Hg) and lead (Pb) concentrations are well documented in some taxa and are described to cause multiple detrimental effects on human and wildlife. Additionally, essential selenium (Se) is known to be toxic at high concentrations but, at lower concentrations, Se can protect organisms against Hg toxicity. Crocodilians are known to bioaccumulate contaminants. However, the effects of these contaminants on physiological processes remain poorly studied. In the present study, we quantified Hg, Pb and Se concentrations in spectacled caimans (Caiman crocodilus) and investigated the effects of these contaminants on several physiological processes linked to osmoregulatory, hepatic, endocrine and renal functions measured through blood parameters in 23 individuals.

Mercury was related to disruption of osmoregulation (sodium levels), hepatic function (alkaline phosphatase levels) and endocrine processes (corticosterone levels). Lead was related to disruption of hepatic functions (glucose and alanine aminotransferase levels). Selenium was not related to any parameters, but the Se:Hg molar ratio was positively related to the Na+and corticosterone concentrations, suggesting a potential protective effect against Hg toxicity. Overall, our results suggest that Hg and Pb alter physiological mechanisms in wild caimans

and highlight the need to thoroughly investigate the consequences of trace element contamination in crocodilians.

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I got it from my mother: Inter-nest variation of mercury concentration in neonates Smooth-fronted Caiman (Paleosuchus trigonatus) suggest maternal transfer and possible phenotypical effects

J. Lemaire, O. Marquis, P. Bustamante, R. Mangione, F. Brischoux

Environmental Research 194 (2021), 110494

The deleterious effects of mercury (Hg) contamination are well documented in humans and wildlife. Chronic exposure via diet and maternal transfer are two pathways which increase the toxicological risk for wild populations. However, few studies examined the physiological impact of Hg in crocodilians. We investigated the Hg contamination in neonate Smooth-fronted Caimans, Paleosuchus trigonatus, and the use of keratinized tissues and blood to evaluate maternal transfer. Between November 2017 and February 2020, we sampled 38 neonates from 4 distinct nests. Mercury concentration was measured in claws, scutes and total blood. Highest Hg concentrations were found in claws. Strong inter-nest variations (Hg ranging from 0.17 ±0.02 to 0.66 ±0.07 μg.g− 1 dw) presumably reflect maternal transfer. Reduced body size in neonates characterized by elevated Hg concentrations suggests an influence of Hg during embryonic development. We emphasize the use of claws as an alternative to

egg collection to investigate maternal transfer in crocodilians. Our results demonstrated the need of further investigation of the impact of Hg contamination in the first life stages of crocodilians.

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Influence of sex, size and trophic level on blood Hg concentrations in Black caiman, Melanosuchus niger (Spic, 1825) in French Guiana

J. Lemaire, P. Bustamante, O. Marquis, S. Caut, F. Brischoux 


Chemosphere 262 (2021) 127819

Mercury (Hg) is a contaminant that is impacting ecosystems worldwide. Its toxicity is threatening wildlife and human populations, leading to the necessity of identifying the most affected ecosystems. Therefore, it is essential to identify pertinent bioindicator organisms to monitor Hg contamination. In this study, we determined the stable carbon ðd13CÞ and nitrogen ðd15NÞ isotope ratios in the red blood cells (RBCs), and the total Hg concentration in total blood of 72 Melanosuchus niger in French Guiana. The goals of our study were to assess the level of Hg contamination in total blood of Black caimans and to further investigate the influence of individual traits (i.e., sex, size/age, diet) on Hg concentrations. Mercury concentration in total blood of Black caimans ranged from 0.572 to 3.408 mg g1 dw (mean ± SD is 1.284 ± 0.672 mg g1 dw) and was positively correlated to individual body size and trophic position ðd15NÞ. We did not find any sexual or seasonal effects on Hg concentrations in the blood. The use of blood of M. niger is relevant to determine Hg concentrations within the population and suggests that this species can be used as a bioindicator for environmental contamination. In addition, our results emphasize trophic position as a major source of Hg variation and further suggest that it is essential to take trophic position ðd15NÞ into account for future studies.

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Variation of total mercury concentrations in different tissues of three neotropical caimans: Implications for minimally invasive biomonitoring

J. Lemaire, F. Brischoux, O. Marquis, R. Mangione, P. Bustamante

Archives of Environmental Contamination and Toxicology 81 (2021) 15-24

Mercury (Hg) is a global environmental contaminant that affects ecosystems. It is known to biomagnify through food webs and to bioaccumulate especially in the tissues of top predators. Large-scale comparisons between taxa and geographic areas are needed to reveal critical trends related to Hg contamination and its deleterious effects on wildlife. Yet, the large variety of tissues (keratinized tissues, internal organs, blood) as well as the variability in the units used to express Hg concentrations (either in wet- or dry-tissue weight) limits straightforward comparisons between studies. In the present study, we assessed the moisture content that could influence the total Hg (THg) concentrations measured in several tissues (claws, scutes, total blood, and red blood cells) of three caiman species. We evaluated the moisture content from the different tissues to provide information on THg concentrations in various matrices. Our results show a difference of THg concentrations between the tis- sues and intra- and interspecific variations of moisture content, with the highest THg values found in keratinized tissues (scute keratinized layers and claws). For the three species, we found positive relationships between body size and THg concentration in keratinized tissues. In the blood, the relationship between body size and THg concentration was species-dependent. Our results emphasize the need for a standardized evaluation of THg concentration and trace elements quantification based on dry weight analytical procedures. In addition, the use of both blood and keratinized tissues offers the possibility to quantify different time scales of THg exposure by non-lethal sampling.

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2020

Observation on breeding site, bioacoustics and biometry of hatchlings of Paleosuchus trigonatus (Schneider, 1801) from French Guiana (Crocodylia: Alligatoridae)

O. Marquis, Mathevon, N., Aubin, T., Gaucher, P., J. Lemaire

Herpetology Notes 13, (2020) 513-516

This note reports a field observation of a breeding site of Paleosuchus trigonatus in the protected area “Réserve Naturelle Nationale des Nouragues” in French Guiana.  It includes a description of its nest, hatchlings and habitat, with an emphasis on hatchlings’ vocal signal. It also reports the result of a playback experiment on an adult. 

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2019

The dark side of the black caiman: Shedding light on species dietary ecology and movement in Agami Pond, French Guiana

S. Caut, V. Francois, M. Bacques, D. Guiral, J. Lemaire, G. Lepoint, O. Marquis, N. Sturaro

PLoS ONE 14(6), (2019) e02117239

The black caiman is one of the largest neotropical top predators, which means that it could play a structuring role within swamp ecosystems. However, because of the difficulties inher- ent to studying black caimans, data are sorely lacking on many aspects of their general biol- ogy, natural history, and ecology, especially in French Guiana. We conducted a detailed study of the Agami Pond black caiman population using a multidisciplinary approach. The aim was to better understand the species’ dietary ecology and movements in the pond, and thus its functional role in pond system. We gathered natural history data, tracked caiman movements using satellite transmitters, and characterized feeding ecology via stable iso- tope analysis. Our study was carried out over three sampling periods and spanned both wet and dry seasons, which differ in their hydrological and ecological conditions. Our results show that black caiman abundance and age demographics differed between seasons in Agami Pond. In the dry season, Agami Pond is one of the only areas within the marsh to hold water. It thus contains large quantities of different fish species, which form the basis of the black caiman’s diet. Caiman body size, a proxy for age class, was around 1.5 meters. During the wet season, which corresponds to the breeding period for migratory birds (e.g., Agami herons), adult black caimans are present in Agami Pond. Adults were most abundant in the inundated forest. There, most individuals measured up to 2 meters. They also exhib- ited a particular “predatory” behavior near bird nests, preying on fallen chicks and adults. Juveniles and subadults were present during both seasons in the pond’s open waters. These behavioral observations were backed up by stable isotope analysis, which revealed ontogenetic variation in the caiman’s isotopic values. This isotopic variation reflected varia- tion in diet that likely reduced intraspecific competition between adults and young. The telemetry and microchip data show that different age classes had different movement pat- terns and that seasonal variation in the pond may influence caiman prey availability and reproductive behavior. The new information gathered should help predict this species’ responses to potential ecosystem disturbance (e.g., water pollution, habitat destruction) and inform the development of an effective conservation plan that involves locals and wildlife officials.

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2018

Determinants of mercury contamination in viperine snakes, Natric maura, in Western Europe

J. Lemaire, P. Bustamante, A. Olivier, O. Lourdais, B. Michaud, A. Boissinot, P. Galán, F. Brischoux

Science of the Total Environment 635, (2018) 20-25

The effects of Hg contamination are presumably widespread across the components of aquatic ecosystems, but investigations have been mainly focused on freshwater fish, because this biota represents a major source of Hg for human populations. Yet, the possible bioaccumulation of Hg on other freshwater meso- and apex- predators (e.g., amphibians, reptiles) has been largely overlooked, especially in Western Europe. In this study, the determinants of Hg concentrations were assessed for the viperine snake (Natrix maura) across 6 populations (N130 individuals sampled in 2016 and 2017) in France and Spain. Specifically, body size, sex, and diet were com- pared with Hg concentrations measured in ventral scales. Overall, N. maura accumulated Hg in their scales. Sex did not seem to influence Hg concentrations in this species. Significant differences in Hg concentrations were ob- served between study sites, and these differences were likely to be mediated by site-specific diet. Frog-eating in- dividuals were characterized not only by lower mean values of Hg (0.194 ± 0.018 μg·g−1 versus 0.386 ± 0.032 μg·g−1 for piscivorous individuals), but also by weaker slopes of the body size-Hg relationship as compared to fish-eating snakes, suggesting strong differences in accumulation rates due to food resources. Importantly, the highest slope of the body size-Hg relationship and the highest values of Hg were found in individuals foraging on trout raised by a fish farm, suggesting that fish farming may contribute to Hg contamination in inland freshwater systems. Finally, our results are compared with data on Hg concentrations in other species of aquatic

snakes, in order to provide a comparative point for future studies.

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