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

https://doi.org/10.1016/j.envres.2020.110494Get rights and content

Highlights

  • Total mercury concentration in neonates Paleosuchus trigonatus.

  • Claw sampling to quantify mercury through maternal transfer.

  • Effects of mercury concentration on body size of neonates.

Abstract

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.

Introduction

Mercury (Hg) is a worldwide environmentally dangerous contaminant (Chen et al., 2018). Its chronic effects on humans and wildlife impact reproduction, offspring quality, embryonic development, hormonal synthesis and secretion, cellular respiration, metabolic processes and immune functions, and further cause neurobehavioral and neuronal dysfunctions (Fingerman et al., 1996; Zahir et al., 2005; Bergeron et al., 2011; Hopkins et al., 2013; Schneider et al., 2013; Tartu et al., 2013; Bridges et al., 2016; Landler et al., 2017; Whitney and Cristol, 2017).

Since more than 30 years, several studies report Hg contamination in a variety of tissues of alligators, caimans and true crocodiles (e.g. Delany et al., 1988; Jagoe et al., 1998; Burger et al., 2000; Almli et al., 2005; Vieira et al., 2011; Eggins et al., 2015; Nilsen et al., 2017; Buenfil-Rojas et al., 2020). In certain geographical areas (e.g., Amazon region), the abundant natural Hg in soil and biota (e.g. an average of 0.3 μg.g−1 in forest soil in French Guiana, Richard et al., 2000), human activities such as deforestation, gold mining activities and agriculture additionally contribute to increase Hg bioavailability (Roulet et al., 1998; Maurice-Bourgoin et al., 2000; Vieira et al., 2011; Schneider et al., 2012, 2015; Correia et al., 2014; Eggins et al., 2015; Lázaro et al., 2015; Rivera et al., 2016; Marrugo-Negrete et al., 2019; Lemaire et al., 2021).

Mercury concentrations obtained in crocodilian tissues have been shown to reflect the contamination of the individual's environment across different temporal scales (Lázaro et al., 2015; Schneider et al., 2015). Blood Hg concentration is thought to reflect relatively recent exposure, while keratinized tissues (e.g., scales and claws) seem to reflect Hg concentration accumulated during longer time periods (Schneider et al., 2015). Despite such tissue-specific variations in Hg burden, ingestion of contaminated food is thought to be the primary source of Hg exposure in crocodilians (Smith et al., 2007; Lemaire et al., 2021). Although relatively elevated Hg concentrations are found in crocodilians (e.g. up to 42.15 ± 6.64 μg.g−1 in liver and 6.33 ± 1.04 μg.g−1 in scutes of the American alligator, Alligator mississippiensis, Yanochko et al., 1997), few studies have investigated actual impact of Hg contamination on these taxa (Jagoe et al., 1998; Almli et al., 2005; Nilsen et al., 2017; Marrugo-Negrete et al., 2019). A negative impact of Hg contamination on body condition has been shown in the American alligator, Alligator mississippiensis (Nilsen et al., 2017) and DNA damages related to Hg exposure have been indicated in the Spectacled caiman, Caiman crocodilus (Marrugo-Negrete et al., 2019).

In addition to the direct influence of trophic level on an individual's contamination, Hg can also be maternally transferred to the progeny in vertebrate species (Evers et al., 2003; Bergeron et al., 2010; Heinz et al., 2010; Ackerman et al., 2017). In mammals, Hg is transferred directly across the placenta and via lactation during nursing while in reptiles sensu lato (i.e., including birds), Hg can be transferred to the eggs during vitellogenesis. The maternal transfer of Hg is a particular source of contamination that is directly related to the female Hg burden (Akearok et al., 2010; Nilsen et al., 2020). Importantly, Hg contamination during early development has been shown to negatively affect embryonic development, embryonic mortality and can have relatively long-lasting effects on the physiology and behavior of neonates (Wolfe et al., 1998; Scheuhammer et al., 2007; Cusaac et al., 2016, Nilsen et al., 2020). Although a recent study reported a positive relationship between the Hg concentration of reproductive American Alligators, Alligator mississippiensis, and its eggs indicating vertical (maternal) transfer of Hg during vitellogenesis (Nilsen et al., 2020), to our knowledge, no study has examined the Hg concentration in hatchling crocodilians yet.

The Smooth-fronted Caiman (Paleosuchus trigonatus) is a small neotropical caiman living in rainforest and wetland habitats with a largely unknown ecology and biology (Magnusson and Lima 1991; Lemaire et al., 2018). In French Guiana, few data is available on this species and the regional population is classified as decreasing (IUCN France et al., 2017). Because of their lifestyle and habitat, Paleosuchus trigonatus can be directly impacted by anthropogenic activities such as deforestation and gold mining that both lead to elevated values of available Hg. In this study, we assessed the total Hg concentration in neonate Smooth-fronted Caimans, Paleosuchus trigonatus, from different nests in French Guiana in order to investigate inter-nest variations that may be linked to maternal transfer of Hg to the progeny, to document Hg concentration in different tissues (blood, scutes and claws) of hatching caimans and to explore potential relationships between neonate phenotype (body size) at birth and Hg burden.

Section snippets

Sample collection

From November 2017 to February 2020, we captured 38 neonates from 4 distinct nests in 3 different areas in French Guiana (Fig. 1). Neonates were found and caught in close proximity to the nests (<5 m), indicating that they hatched recently (Magnusson and Lima, 1991). We also collected eggshells and shell membrane remnants from each nest. For each individual, claw and scute samples were clipped using pliers and were then placed in dry plastic containers; blood samples were collected on a

Statistical analysis

All analyses were performed using the software R, v.3.6.1 (R development Core Team).

The normality and the homogeneity of variance were first checked, and data were log-transformed when necessary. The comparison of Hg concentration and body size (SVL and TL) in neonates between the 4 nests was assessed by one-way ANOVAs, as well as for shell membranes. We did not perform statistical analysis for eggshells due to absence of variation. In order to assess the relationship between total blood and

Results

For all neonates, Hg concentrations in keratinized tissues were the highest in claws with average concentrations ranging from 0.171 to 0.663 μg.g−1 dw and the lowest in scutes with average concentrations ranging from 0.092 to 0.251 μg.g−1 dw (Table 1). The Hg concentration in eggshells did not vary between nests with a value of 0.001 μg.g−1 dw, while the Hg concentration in shell membranes varied between nests with average concentrations ranging from 0.020 to 0.040 μg.g−1 dw (Table 1). Our

Discussion

Overall, we found relatively high Hg concentrations in hatchling caimans. Our results show that inter-nest differences in Hg concentration may indicate that this metal is transferred from the mother during vitellogenesis. This process seems further supported by the relationship between alleged mother and offspring Hg concentrations on a limited sample. Finally, we showed that nests having higher Hg concentrations produced smaller hatchling caimans.

Conclusion

Our results highlight the use of keratinized tissues, particularly claws, to quantify the fetal Hg exposure and to evaluate maternal transfer in crocodilians. The variation of Hg concentrations between nests reinforces the fact that the contamination of the reproductive female has a direct effect on the concentration in its eggs. Finally, Hg concentration in the egg may influence hatchling morphology, thus potentially reducing survival and increasing susceptibility to later chronic exposure.

Credit authors statement

Jérémy Lemaire: Conceptualization, Investigation, Formal analysis, Software, Funding acquisition, Writing – original draft, Writing – review & editing. Paco Bustamante: Conceptualization, Investigation, Funding acquisition, Writing – original draft, Writing – review & editing, Supervision. Olivier Marquis: Conceptualization, Investigation, Funding acquisition, Writing – original draft, Writing – review & editing, Supervision. Rosanna Mangione: Conceptualization, Investigation, Writing –

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We are grateful to the authorities of Conseil Scientifique Régional du Patrimoine Naturel (CSRPN) and La Direction générale des Territoires et de la Mer de Guyane (DGTM), who authorized our fieldwork and sample collection. We would also like to thank the teams of “Réserve Naturelle des Nouragues” and “Réserve Naturelle du Mont-Grand Matoury” for logistics and assistance in the field. This work was supported by the Office de l’Eau de Guyane (OEG); the Office Française pour la Biodiversité (OFB);

References (56)

  • J. Marrugo-Negrete et al.

    Mercury levels and genotoxic effect in caimans from tropical ecosystems impacted by gold mining

    Sci. Total Environ.

    (2019)
  • L. Maurice-Bourgoin et al.

    Mercury distribution in waters and fishes of the upper Madeira rivers and mercury exposure in riparian Amazonian populations

    Sci. Total Environ.

    (2000)
  • F.M. Nilsen et al.

    Trace element biodistribution in the American alligator (Alligator mississippiensis)

    Chemosphere

    (2017)
  • F.M. Nilsen et al.

    Examining maternal and environmental transfer of mercury into American alligator eggs

    Ecotoxicol. Environ. Saf.

    (2020)
  • S.J. Rivera et al.

    Low total mercury in Caiman yacare (Alligatoridae) as compared to carnivorous, and non-carnivorous fish consumed by Amazonian indigenous communities

    Environ. Pollut.

    (2016)
  • M. Roulet et al.

    The geochemistry of mercury in central Amazonian soils developed on the Alter-do-Chao formation of the lower Tapajos River Valley, Para state, Brazil

    Sci. Total Environ.

    (1998)
  • L. Schneider et al.

    An evaluation of the use of reptile dermal scutes as a non-invasive method to monitor mercury concentrations in the environment

    Chemosphere

    (2015)
  • P.N. Smith et al.

    Contaminant exposure in terrestrial vertebrates

    Environ. Pollut.

    (2007)
  • F. Zahir et al.

    Low dose mercury toxicity and human health

    Environ. Toxicol. Pharmacol.

    (2005)
  • L. Alibardi

    Adaptation to the land: the skin of reptiles in comparison to that of amphibians and endotherm amniotes

    J. Exp. Zool. B Mol. Dev. Evol.

    (2003)
  • C.M. Bergeron et al.

    Bioaccumulation and maternal transfer of mercury and selenium in amphibians

    Environ. Toxicol. Chem.

    (2010)
  • C.M. Bergeron et al.

    Interactive effects of maternal and dietary mercury exposure have latent and lethal consequences for amphibian larvae

    Environ. Sci. Technol.

    (2011)
  • K.N. Bridges et al.

    Embryotoxicity of maternally transferred methylmercury to fathead minnows (Pimephales promelas)

    Environ. Toxicol. Chem.

    (2016)
  • J. Burger et al.

    Metals and metalloids in tissues of American Alligators in three Florida lakes

    Environ. Contam. Toxicol.

    (2000)
  • C.Y. Chen et al.

    A critical time for mercury science to inform global policy

    Environ. Sci. Technol.

    (2018)
  • T. Colborn et al.

    Developmental effects of endocrine disrupting chemicals in wildlife and humans

    Environ. Health Perspect.

    (1993)
  • J. Correia et al.

    Mercury contamination in alligators (Melanosuchus niger) from Mamirauá Reservoir (Brazilian Amazon) and human health risk assessment

    Environ. Sci. Pollut. Res.

    (2014)
  • J.P.W. Cusaac et al.

    Effects of maternally transferred methylmercury on stress physiology in northern water snake (Nerodia sipedon) neonates

    Bull. Environ. Contam. Toxicol.

    (2016)
  • Cited by (11)

    • Assessing multigenerational exposure to metals in elasmobranchs: Maternal transfer of contaminants in a yolk-sac viviparous species

      2022, Marine Pollution Bulletin
      Citation Excerpt :

      Despite this, maternal transfer is better understood through experimental conditions. Maternal offloading of inorganic elements has been demonstrated in several vertebrates (Hopkins et al., 2006; Paéz-Ozuna et al., 2010; Lahaye et al., 2007; Lemaire et al., 2021), including elasmobranchs. Mercury is the most studied element regarding maternal transfer of metals (Adams and McMichael, 1999; Lyons and Lowe, 2013a; Lyons et al., 2013; Frías-Espericueta et al., 2015; van Hees and Ebert, 2017; Hauser-Davis et al., 2020).

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

      2021, Environmental Pollution
      Citation Excerpt :

      Few studies which focused on a limited number of species have evaluated Hg and Pb concentrations in crocodilians (Burger et al., 2000; Jeffree et al., 2001; Correia et al., 2014; Trillanes et al., 2014; Nilsen et al., 2017b). Further knowledge on their negative effects is restricted to four crocodilian species (Alligator mississippiensis, Caiman crocodilus, Paleosuchus trigonatus and Crocodylus niloticus) and few markers (morphology, DNA and reproduction; Lance et al., 2006; Warner et al., 2016; Nilsen et al., 2017a; Marrugo-Negrete et al., 2019; Lemaire et al., 2021b). To our knowledge, no studies have investigated the combined effects of Hg, Pb and Se, and the possible protective effect of Se on physiological parameters of caimans, particularly in French Guiana, where said contaminants are highly abundant in the environment.

    View all citing articles on Scopus
    View full text