Selenium speciation influences bioaccumulation in Limnodynastes peronii tadpoles

doi:10.1016/j.aquatox.2017.03.009

Aquatic Toxicology

Volume 187, June 2017, Pages 1-8

https://doi.org/10.1016/j.aquatox.2017.03.009 Get rights and content

Highlights

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Differences in SeIV and SeVI bioaccumulation and biodistribution were assessed.
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Limnodynastes peronii tadpoles accumulated more selenite than selenate.
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Selenium depuration kinetics was similar for both forms.
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Tadpoles accumulated Se predominantly in the digestive and excretory organs.

Abstract

Despite being essential for animal health and fitness, Se has a relatively narrow range between deficiency and toxicity, and excess Se can cause a variety of adverse effects in aquatic organisms. Amphibians are particularly vulnerable to contaminants during larval aquatic life stage, because they can accumulate toxic ions through various routes including skin, gills, lungs and digestive tract. Few attempts have been made to understand the tissue-specific accumulation of trace elements, including the impacts of chemical speciation in developing amphibian larvae. We used radiolabelled ⁷⁵Se to explore the biokinetics and tissue distributions of the two dominant forms occurring in surface waters, selenite (SeIV) and selenate (SeVI). Tadpoles of the native Australian frog Limnodynastes peronii were exposed to Se in both forms, and live-animal gamma spectroscopy was used to track accumulation and retention over time. Tissue biodistributions were also quantified at the end of the uptake and depuration phases. Results showed the bioconcentration of SeIV to be 3 times greater compared to SeVI, but rates of elimination were similar for both forms. This suggests a change of Se speciation within the organism prior to excretion. Depuration kinetics were best described by a one-phase exponential decay model, and tadpoles retained approximately 19% of the accumulated Se after 12 days of depuration in clean water. Selenium bioaccumulation was greatest in digestive and excretory organs, as well as the eye, which may directly relate to previously reported Se-induced impairments. Results demonstrate how the use of radiotracing techniques can significantly improve our understanding of trace element toxicokinetics and tissue distributions in developing amphibians. From an environmental monitoring perspective, the findings highlight the importance of considering chemical speciation as this could influence the accuracy of risk assessment.

Introduction

Selenium (Se) naturally and ubiquitously occurs in the environment in both organic and inorganic forms. Despite being essential to most living organisms, anthropogenic activities, such as mining and agriculture, can introduce toxic levels of Se into aquatic environments (Lemly, 2004). In the worst cases, Se pollution stemming from such activities has been associated with local extinctions of several fish species (Lemly, 2002). In other instances, elevated Se has been reported to adversely impact growth, development, behaviour and reproduction, and to cause oxidative stress and deformities in aquatic biota (Hamilton, 2004, Janz et al., 2010). Selenium may pose serious long-term threats to aquatic ecosystems because it has the capacity to bioaccumulate and biomagnify in the food chain, making it difficult for ecosystems to recover from Se contamination (Lemly, 1985).

Importantly, the bioavailability and toxicity of Se depends not only on its concentration in the environment, but also its speciation (Franz et al., 2011, Kleinow and Brooks, 1986a, Maier and Knight, 1993). Se can exist in five oxidation states (VI, IV, 0, −I, − II), with Se oxyanions selenite (SeIV) and selenate (SeVI) representing the dominant forms of dissolved Se in surface waters. In aquatic systems, the relative abundance of SeIV and SeVI often vary substantially, and is generally dependent on the regional geology and the different anthropogenic sources of Se that are present. Selenite is more prevalent in systems receiving contaminated discharges from coal fly ash or oil refineries, whereas agricultural activities and run-off from crop irrigation typically result in greater mobilization of selenate (Maher et al., 2010). The different forms of Se are known to behave differently with respect to their sorption, bioavailability and mobility in aquatic ecosystems. In general, Se solubility has been observed to increase with increasing redox potential, and while both forms are considered readily soluble in water, SeVI has greater water solubility compared to SeIV (Masscheleyn and Patrick, 1993). As such, the bioaccumulative potential and toxicity of inorganic Se species has been shown to differ in some organisms, with SeIV generally exhibiting greater bioavailability and toxicity compared to SeVI (Franz et al., 2011, Kleinow and Brooks, 1986a, Maier et al., 1993). However, while the accumulation kinetics and toxicity of aquatic Se has been well documented for various fish and invertebrates, much less is known regarding Se toxicokinetics in amphibians (Hopkins et al., 2006, Janz et al., 2010).

Amphibians are highly susceptible to the bioaccumulation of metals and metalloids, in part because they may take up toxic ions through multiple exposure pathways (i.e., skin, gills and diet), during their various life stages. They are extremely vulnerable to pollutants in general, and are currently listed amongst the most threatened organisms on the planet with many species apparently suffering local and regional declines (Monastersky, 2014). Considering their sensitivity to pollutants and globally threatened status, it is critical that we strive to understand the various factors that may be driving the toxicity of widespread environmental pollutants to amphibians. This holds particularly true for amphibians during sensitive larval developmental stages, when Se can be readily accumulated from contaminated aquatic environments (Lanctôt et al., 2016, Unrine et al., 2007).

The present study investigated accumulation and depuration kinetics as well as the resultant tissue distributions of Se administered in the dissolved forms of selenite and selenate, in striped marsh frog (Limnodynastes peronii) tadpoles. Radiotracing techniques were applied to monitor the bioaccumulation kinetics of Se in live tadpoles. This technique has the advantage of being non-lethal, and therefore provides robust longitudinal data on individual organisms that is ideal for kinetic assessments.

Section snippets

Animals

A single fertilized L. peronii egg mass was collected from an ephemeral pool in Elanora, Queensland, Australia and hatched in the laboratory in natural pond water (QLD Government Permit No. WISP16587715). After hatching, water levels were slowly increased and replaced with reconstituted moderately hard water made according to standard test guidelines (US EPA, 2002). This water was used for control and diluent water. Tadpoles were held in a 52 L clear plastic container filled with aerated water

Longitudinal verification of water chemistry

Measured concentration throughout the 7-d exposure to SeIV was 1.56 ± 0.08 μg/L (52 Bq/mL), 0.4 μg/L over the nominal concentration of 1.2 μg/L, whereas SeVI was 1.12 ± 0.04 μg/L (37 Bq/mL), 0.1 μg/L below our target concentration. Concentrations fluctuated by less than 10% between water changes, with the average of fresh solutions being 1.59 μg/L for SeIV and 1.14 μg/L for SeVI compared to 1.53 and 1.11 μg/L, respectively, after 24 h. ⁷⁵Se was not detected in controls and depuration water after 15-min

Tadpoles accumulated significantly more SeIV than SeVI

Results demonstrate that L. peronii tadpoles readily accumulate both selenite and selenate from water when exposed to environmentally relevant concentrations. However, tadpoles accumulated selenite at a much faster rate than selenate. Greater selenite bioaccumulation has also been reported in other species (Franz et al., 2011, Kleinow and Brooks, 1986a). Speciation differences in accumulation likely relate to differences in metabolism between Se oxyanions. Once absorbed, selenate must first be

Conclusion

Selenium has been garnering increasing interest as a contaminant of concern due to industrial sources of this element in the environment, but there is a recognised paucity of information regarding Se accumulation and toxicity in amphibians. This study used radiotracing techniques to explore speciation differences in Se toxicokinetics and tissue distributions during larval amphibian development. Findings demonstrate differential uptake and retention of the two major Se oxyanions, SeIV and SeVI,

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.

References (55)

R. Alquezar et al.
Comparative accumulation of ¹⁰⁹Cd and ⁷⁵Se from water and food by an estuarine fish (Tetractenos glaber)
J. Environ. Radioact.
(2008)
N. Creighton et al.
Bioaccumulation from food and water of cadmium selenium and zinc in an estuarine fish, Ambassis jacksoniensis
Mar. Pollut. Bull.
(2010)
S.J. Hamilton
Review of selenium toxicity in the aquatic food chain
Sci. Total Environ.
(2004)
P. Hervé-Fernández et al.
Cadmium bioaccumulation and retention kinetics in the Chilean blue mussel Mytilus chilensis: Seawater and food exposure pathways
Aquat. Toxicol.
(2010)
K.M. Kleinow et al.
Selenium compounds in the fathead minnow (Pimephales promelas)-I. Uptake, distribution, and elimination of orally administered selenate, selenite and l-selenomethionine
Comp. Biochem. Physiol.
(1986)
K.M. Kleinow et al.
Selenium compounds in the fathead minnow (Pimephales promelas)-II. Quantitative approach to gastrointestinal absorption, routes of elimination and influence of dietary pretreatment
Comp. Biochem. Physiol.
(1986)
C.M. Lanctôt et al.
Behaviour, development and metal accumulation in striped marsh frog tadpoles (Limnodynastes peronii) exposed to coal mine wastewater
Aquat. Toxicol.
(2016)
A.D. Lemly
Teratogenic effects of selenium in natural populations of freshwater fish
Ecotoxicol. Environ. Saf.
(1993)
A.D. Lemly
A teratogenic deformity index for evaluating impacts of selenium on fish populations
Ecotoxicol. Environ. Saf.
(1997)
A.D. Lemly
Symptoms and implications of selenium toxicity in fish: the Belews Lake case example
Aquat. Toxicol.
(2002)

A.D. Lemly

Aquatic selenium pollution is a global environmental safety issue

Ecotoxicol. Environ. Saf.

(2004)

N.J. Mackay et al.

Selenium and heavy metals in black marlin

Mar. Pollut. Bull.

(1975)

L.L. Miller et al.

Effects of acute and subchronic exposures to waterborne selenite on the physiological stress response and oxidative stress indicators in juvenile rainbow trout

Aquat. Toxicol.

(2007)

S. Misra et al.

Tissue-specific accumulation and speciation of selenium in rainbow trout (Oncorhynchus mykiss) exposed to elevated dietary selenomethionine

Comp. Biochem. Physiol.

(2012)

J. Phibbs et al.

Evaluating the trophic transfer of selenium in aquatic ecosystems using caged fish, X-ray absorption spectroscopy and stable isotope analysis

Ecotoxicol. Environ. Saf.

(2011)

J. Phibbs et al.

Selenium uptake and speciation in wild and caged fish downstream of a metal mining and milling discharge

Ecotoxicol. Environ. Saf.

(2011)

J.W. Snodgrass et al.

Species-specific responses of developing anurans to coal combustion wastes

Aquat. Toxicol.

(2004)

J.M. Unrine et al.

Bioaccumulation of trace elements in omnivorous amphibian larvae: implications for amphibian health and contaminant transport

Environ. Pollut.

(2007)

R. Altig et al.

Percent assimilation and clearance times of five anuran tadpoles

Herpetologica

(1975)

C.L. Browne et al.

Toxicity of selenium to developing Xenopus laevis embryos

J. Toxicol. Environ. Health

(1979)

R.F. Burk et al.

Regulation of selenium metabolism and transport

Annu. Rev. Nutr.

(2015)

S. Choudhury et al.

Selenium preferentially accumulates in the eye lens following embryonic exposure: a confocal x-ray fluorescence imaging study

Environ. Sci. Technol.

(2015)

T. Cresswell et al.

Bioaccumulation kinetics and organ distribution of cadmium and zinc in the freshwater decapod crustacean Macrobrachium australiense

Environ. Sci. Technol.

(2015)

L. Flohé

Selenium, selenoproteins and vision

Dev. Ophthalmol.

(2005)

E.D. Franz et al.

Selenium bioaccumulation and speciation in Chironomus dilutus exposed to water-borne selenate, selenite, or seleno-DL-methionine

Environ. Toxicol. Chem.

(2011)

K.L. Gosner

A simplified Table for staging anuran embryos and larvae with notes on identification

Herpetologica

(1960)

W.A. Hopkins et al.

Elevated trace element concentrations and standard metabolic rate in banded water snakes (Nerodia fasciata) exposed to coal combustion wastes

Environ. Toxicol. Chem.

(1999)

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Research PaperSelenium speciation influences bioaccumulation in Limnodynastes peronii tadpoles

Highlights

Abstract

Introduction

Section snippets

Animals

Longitudinal verification of water chemistry

Tadpoles accumulated significantly more SeIV than SeVI

Conclusion

Acknowledgements

J. Environ. Radioact.

Mar. Pollut. Bull.

Sci. Total Environ.

Aquat. Toxicol.

Comp. Biochem. Physiol.

Comp. Biochem. Physiol.

Aquat. Toxicol.

Ecotoxicol. Environ. Saf.

Ecotoxicol. Environ. Saf.

Aquat. Toxicol.

Ecotoxicol. Environ. Saf.

Mar. Pollut. Bull.

Aquat. Toxicol.

Comp. Biochem. Physiol.

Ecotoxicol. Environ. Saf.

Ecotoxicol. Environ. Saf.

Aquat. Toxicol.

Environ. Pollut.

Percent assimilation and clearance times of five anuran tadpoles

Herpetologica

Toxicity of selenium to developing Xenopus laevis embryos

J. Toxicol. Environ. Health

Regulation of selenium metabolism and transport

Annu. Rev. Nutr.

Selenium preferentially accumulates in the eye lens following embryonic exposure: a confocal x-ray fluorescence imaging study

Environ. Sci. Technol.

Bioaccumulation kinetics and organ distribution of cadmium and zinc in the freshwater decapod crustacean Macrobrachium australiense

Environ. Sci. Technol.

Selenium, selenoproteins and vision

Dev. Ophthalmol.

Selenium bioaccumulation and speciation in Chironomus dilutus exposed to water-borne selenate, selenite, or seleno-DL-methionine

Environ. Toxicol. Chem.

A simplified Table for staging anuran embryos and larvae with notes on identification

Herpetologica

Elevated trace element concentrations and standard metabolic rate in banded water snakes (Nerodia fasciata) exposed to coal combustion wastes

Environ. Toxicol. Chem.

Research Paper
Selenium speciation influences bioaccumulation in Limnodynastes peronii tadpoles