Uptake and tissue distributions of cadmium, selenium and zinc in striped marsh frog tadpoles exposed during early post-embryonic development

https://doi.org/10.1016/j.ecoenv.2017.06.047Get rights and content

Highlights

  • Bioaccumulation kinetics of Cd, Se and Zn were examined using radioisotope tracers.

  • Limnodynastes peronii tadpoles readily accumulated all dissolved radioisotopes.

  • Exposure conditions (i.e., mixture, feeding) influenced uptake and elimination.

  • Bioconcentration factor and overall retention was greatest for Se.

  • All three isotopes were detected in tadpole gut, tail and carcass.

Abstract

Metals and metalloids released through anthropogenic activities can accumulate in aquatic organisms, resulting in adverse effects in sensitive species. We investigated the influence of feeding regime and exposure complexity (i.e., mixture) on bioaccumulation kinetics and body distribution of common metal(loid) pollutants in Limnodynastes peronii during early post-embryonic development. Tadpoles were exposed to radiolabelled 109Cd, 75Se and 65Zn alone and in a mixture for 4 days, followed by 3 days depuration in clean water. One group was fed directly in exposure aquaria, whereas a second group was transferred to clean water for feeding, to investigate the potential influence of sorption to food on uptake. Bioconcentration factor and retention was observed to be greatest for Se. Results demonstrate that tadpoles accumulated and retained half the amount of Cd when exposed in mixture, suggesting that Se and/or Zn may have antagonistic effects against Cd uptake. Additionally, tadpoles fed directly in exposure water accumulated 2–3–times more Cd and Zn compared to tadpoles fed in clean water, indicating that the presence of food particles is an important factor that may influence uptake. Interestingly, this had a negligible impact on Se uptake. The study reveals how exposure conditions can influence the bioaccumulation of metal(loid)s, highlighting experimental factors as important considerations for both controlled toxicity experiments and for understanding exposure risks for amphibian populations.

Introduction

Metal pollution has long been recognized as an important environmental concern, since these elements can adversely impact aquatic animals and ecosystem health (Luoma, 1983, Rainbow, 2002; Wang, 1987). Many trace metals and metalloids (hereafter referred to as metals) occur naturally in the environment and are essential for the health and maintenance of physiological homeostasis in vertebrates. However, anthropogenic activities such as the combustion of fossil fuels, agriculture, mining and other processes can introduce unnatural levels of metals into aquatic environments. This introduces the risk of adverse effects in sensitive aquatic species, since metals are often highly persistent and bioaccumulative (Deb and Fukushima, 1999). The potential for toxicological impacts resulting from metal pollutants has been well studied for a number of aquatic species, but in general such research efforts have primarily focused on fish and invertebrates (Atchison et al., 1987, DeForest and Meyer, 2015, Rainbow, 2002). In these organisms, reported effects include (but are not limited to) tissue damage, decreased immunity, changes in behaviour, altered growth rates and nutritional status, effects on digestive enzyme activities, efficiency of food assimilation, carbohydrate metabolism, teratogenic, mutagenic and gonadotoxic effects, damage to lipid, protein, and peptide metabolism, as well as effects on productivity and life cycles. Importantly, metal toxicity has been found to be highly variable and is frequently dependent on the physicochemical characteristics of the environment (Luoma, 1983, Wren and Stephenson, 1991). As such, it is extremely important to understand the factors influencing the bioavailability and bioaccumulation of metals in understudied aquatic organisms in order to properly assess their risks under varying environmental conditions.

When considering aquatic species, some animals are inherently more susceptible than others to the potential for adverse toxicity associated with industrial contaminants. In particular, amphibians are expected to be quite vulnerable to metal bioaccumulation during larval aquatic life stages, due to their highly permeable skin and gills during this timeframe (Linder et al., 2010, Wake and Vredenburg, 2008). However, despite evidence that amphibians may be more sensitive to metals and other industrial pollutants during aquatic developmental stages (Ferrari et al., 1993, Herkovits et al., 1997, Melvin and Trudeau, 2012), metal bioaccumulation in larval amphibians has received relatively little attention. This represents an important shortcoming, since the limited studies that have explored bioaccumulation in amphibians have indeed linked metal uptake to severe physiological disruption (Davey et al., 2008, Lanctôt et al., 2016, Unrine et al., 2007, Zocche et al., 2013). However, previous studies with amphibians have typically focused on assessing metal burdens in field-captured individuals exposed to naturally occurring mixtures or single exposures in the laboratory. While such research is extremely important considering the threatened status of many amphibian populations globally (Monastersky, 2014), controlled mixture studies are necessary to fully explore and understand how common metal pollutants and mixtures are taken up by amphibians during sensitive larval-life stages.

To address some of the identified knowledge gaps, we investigated the bioaccumulation of three key elemental contaminants commonly occurring in industrial effluents, both alone and when exposed as a tertiary mixture, throughout early post-embryonic development in striped marsh frog (Limnodynastes peronii) tadpoles. Elements and forms were selected based on previous studies suggesting that they may pose high environmental risks, particularly due to their bioaccumulative nature and potential for additive and antagonistic interactions when present in mixtures (Dobrovoljc et al., 2012, Herkovits and Perez-Coll, 1990). Cadmium (Cd), a heavy metal with no known biological function in animals, has been associated with a number of reproductive and developmental effects in many species at relatively low concentrations (Hammons et al., 1978). Selenium (Se) is an essential micronutrient that plays an important role in reproduction, DNA synthesis, thyroid hormone metabolism and oxidative stress defense, although excess Se levels can also cause developmental abnormalities and reproductive failure in many species (Hamilton, 2004). Like Se, Zinc (Zn) is an essential trace element required for growth and reproduction, but is also the most ubiquitous heavy metal in the environment and can cause severe toxicological effects when present at concentrations above essential thresholds (Skidmore, 1964).

Radiotracing techniques have been shown to be highly valuable for studying trace element bioaccumulation, as they not only allow for environmental concentrations to be studied that may be undetectable with other analytical approaches, but also reduces the number of animals required by providing robust longitudinal data on individual organisms (Creighton and Twining, 2010, Cresswell et al., 2015, Cresswell et al., 2014, Metian et al., 2010). Gamma-emitting radioisotope tracers were used to trace low levels of the radiolabelled elements in individual live animals over time, and to assess their distribution within the organisms. While each of the studied metals has been deemed a risk to aquatic wildlife, little is know regarding the kinetics and interactions of these three elements, or other factors that may be important for influencing bioaccumulation and subsequent toxicity in developing amphibians. For this reason, we investigated the effect of trace metal mixture and feeding condition on the bioaccumulation kinetics and body distribution of Cd, Se and Zn in tadpoles exposed to environmentally relevant concentrations.

Section snippets

Animals

L. peronii was chosen for its wide distribution in Australia, including areas in Central Queensland and New South Wales characterized by intensive mining and other industrial activities. Fertilized eggs were collected from an ephemeral pond in Elanora, QLD, and hatched in the laboratory in pond water from the collection site (QLD Government Permit No. WISP16587715). After hatching, water levels were slowly increased and replaced with reconstituted moderately hard water (MHW) made according to

Tadpole growth and survival

Exposures did not affect tadpole survival, growth or development, and no obvious sign of stress were exhibited during acclimation, exposure or depuration. At the end of the depuration phase, all tadpoles survived and there was no difference in developmental stage among metal treatments (Average Gs (± SD) = 27 ± 0.4; F = 1.08, df = 4, p = 0.391) or feeding groups (F = 0.67, df = 1, p = 0.424). Tadpoles had an average weight of 42.9 ± 6.1 mg, and SVL and total lengths measuring 6.6 ± 0.6 mm and

Discussion

Amphibians are known to be vulnerable to the bioaccumulation of metals and metalloids during larval aquatic life stages due to their highly permeable skin and gills. However, despite evidence that amphibians may be more sensitive to metals and other industrial pollutants during aquatic stages (Ferrari et al., 1993, Herkovits et al., 1997, Melvin and Trudeau, 2012), few studies have investigative metal bioaccumulation in larval amphibians. In the present study, post-embryonic amphibian larvae

Conclusion

Metal pollution has been widely associated with many diverse human activities, and the prevalence of such activities is increasing globally. To understand the risks associated with metal pollution and protect sensitive wildlife, the various factors influencing bioaccumulation must first be characterized. Few studies have investigated metal bioaccumulation by amphibians compared to studies with other aquatic species, and knowledge gaps are particularly evident with respect to early larval

Acknowledgements

The study was carried out at the Australian Nuclear Science and Technology Organisation (ANSTO) with the assistance of an Australian Institute for Nuclear Science and Engineering (AINSE) Research Award (No. ALNGRA16029). We thank Lida Mokhber-Shahin for gamma analysis of standards, Henri Wong and Brett Rowling for ICP-MS analysis and Nicholas Howell for radioanalysis of body compartments.

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