Sulfate transport kinetics and toxicity are modulated by sodium in aquatic insects

Scheibener, Shane; Conley, Justin M.; Buchwalter, David B.

doi:10.1016/j.aquatox.2017.06.027

Cited by 30 publications

(31 citation statements)

References 43 publications

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“…Somehow, the ionic composition of the water mattered as waters high in sulfate, but low in sodium, were toxic to the mayfly, but when the ratios of SO 4 to Na were considerably lower, toxicity was not observed despite the high conductivity. Subsequent work identified Na as a modifier of acute SO 4 toxicity, with increasing Na associated with decreased SO 4 uptake and toxicity [30]. This finding is important, because in streams affected by surface coal mining, it is common to find elevated SO 4 against a low Na background.…”

Section: Discussionmentioning

confidence: 99%

“…Scheibener et al [30] previously characterized Michaelis-Menten-type uptake kinetics for SO 4 in N. triangulifer and showed that even at a very high SO 4 concentration, uptake of the ion was not saturated. To determine whether this situation could lead to 'self-poisoning' through excessive SO 4 accumulation in tissues, we analysed the total body S content of the subimagos that emerged during the study.…”

Section: Discussionmentioning

confidence: 99%

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Are sulfate effects in the mayfly Neocloeon triangulifer driven by the cost of ion regulation?

Buchwalter

Scheibener

Chou

et al. 2018

Phil. Trans. R. Soc. B

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Elevated major ion concentrations in streams are commonly observed as a consequence of resource extraction, de-icing and other anthropogenic activities. Ecologists report biodiversity losses associated with increasing salinity, with mayflies typically being highly responsive to increases of different major ions. In this study, we evaluated the performance of the mayfly Neocloeon triangulifer reared for its entire larval phase in a gradient of sulfate concentrations. Two natural waters were amended with SO 4 as a blend of CaSO 4 and MgSO 4 and exposures ranged from 5 to 1500 mg l –1 SO 4. Survival (per cent successful emergence to the subimago stage) was significantly reduced at the highest SO 4 concentration in both waters, while development was significantly delayed at 667 mg l −1 SO 4 . Final sub-adult body weights were consistent across treatments, except at the highest treatment concentration. Despite evidence for sulfate uptake rates increasing with exposure concentrations and not being saturated at even extremely high SO 4 concentrations, total body sulfur changed little in subimagos. Together, these results suggest that elevated SO 4 imposes an energetic demand associated with maintaining homeostasis that is manifested primarily as reduced growth rates and associated developmental delays. We identified two genes related to sulfate transport in N. triangulifer . This article is part of the theme issue ‘Salt in freshwaters: causes, ecological consequences and future prospects’.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Are sulfate effects in the mayfly Neocloeon triangulifer driven by the cost of ion regulation?

Buchwalter

Scheibener

Chou

et al. 2018

Phil. Trans. R. Soc. B

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“…Uptake of SO 2À 4 in five mayfly species (including Maccaffertium sp.) increased with increasing external SO 2À 4 concentration, but unlike Na þ , saturation of SO 2À 4 was observed ( [30]; see also from this issue Buchwalter et al [49]). That is, the rate of increase in SO 2À 4 uptake decreased with increasing external SO 2À 4 concentration.…”

Section: Hypothesis 1-energetics Of Ion Uptakementioning

confidence: 93%

Why are mayflies (Ephemeroptera) lost following small increases in salinity? Three conceptual osmophysiological hypotheses

Kefford

2018

Phil. Trans. R. Soc. B

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The salinity of many freshwaters is increasing globally as a result of human activities. Associated with this increase in salinity are losses of Ephemeroptera (mayfly) abundance and richness. The salinity concentrations at which Ephemeroptera decline in nature are lower than their internal salinity or haemolymph osmolality. Many species also suffer substantial mortality in single species laboratory toxicity tests at salinities lower than their internal salinity. These findings are problematic as conventional osmoregulation theory suggests that freshwater animals should not experience stress where external osmolality is greater than haemolymph osmolality. Here I explore three hypotheses to explain salt sensitivity in Ephemeroptera. These conceptual hypotheses are based on the observations that as the external sodium ion (Na + ) concentration increases so does the Na + turnover rate (both uptake and elimination rates increase). Sulphate ( ) uptake in mayflies also increases with increasing external although, unlike Na + , its rate of increase decreases with increasing external . The first hypothesis is premised on ion turnover being energetically costly. The first hypothesis proposes that individuals must devote a greater proportion of their energy to ion homeostasis at the expense of other uses including growth and development. Lethal levels of salinity presumably result from individuals not being able to devote enough energy to maintain ion homeostasis without critical loss of other vital functions. The second hypothesis is premised on the uptake of Na + exchanged for (an outgoing) H + , leading to (localized) loss of pH regulation. The third hypothesis is premised on localized Na + toxicity or poisoning with increased Na turnover as salinity increases. None of the proposed hypotheses is without potential problems, yet all are testable, and research effort should be focused at attempting to falsify them. This article is part of the theme issue ‘Salt in freshwaters: causes, ecological consequences and future prospects’.

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“…Previous research found that salinization of freshwater systems from the increasing use of deicing salt can negatively affect the performance of freshwater organisms (Bernabò et al, 2013;Kearney et al, 2014;Dananay et al, 2015;Hopkins et al, 2016), and threaten the viability of some populations (Silberbush et al, 2005;Petranka and Doyle, 2010;Van Meter et al, 2011;Searle et al, 2016;Castillo et al, 2018;Timpano et al, 2018). Salinization can impose physiological stresses for freshwater organisms including impaired osmoregulation (Marshall and Grosell, 2006;Griffith, 2016;Sala et al, 2016;Scheibener et al, 2016Scheibener et al, , 2017 and decreased respiratory performance (Roast et al, 1999;McAllen and Taylor, 2001;Tollefsen et al, 2015;Botwe et al, 2018). Consequently, road salt has been recognized as a potentially harmful substance and added to the "List of Toxic Substances" in Canada (Environment Canada, 2012).…”

Section: Introductionmentioning

confidence: 99%

Chronic Exposure to High Concentrations of Road Salt Decreases the Immune Response of Dragonfly Larvae

2019

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Salinization of freshwater ecosystems, due to the application of road salts, is recognized as a potential threat to aquatic communities. Much of the research on the impact of salinity has focused on performance metrics in vertebrates, including respiration and osmoregulation. Here we focus on immune function in larvae of the dragonfly Anax junius, a top predator in fishless aquatic habitats. Impacts on this top predator have the potential to cascade through the community, and immune function is known to be both plastic and sensitive to stress. We injected larvae with monofilaments (simulating a parasite) and placed them in one of three environmentally relevant concentrations of deicing road salt: control (dechlorinated tap water with no added salt), low (1,000 mgL −1), or high salt (3,000 mgL −1), for either acute (24 h) or chronic (96 h) exposure. We hypothesized that elevated salinity would suppress the immune response and that longer exposure magnifies this effect. As predicted, chronic exposure to high salt concentrations resulted in significantly reduced larval immune response compared to control conditions, however, there were no detectable treatment effects in larvae exposed to low concentrations of road salt or to acute high concentrations. Our results demonstrate that prolonged exposure to high levels of road salt can compromise the immune response of dragonfly larvae. Our findings suggest that insects in aquatic environments that experience sustained environmental salt pollution will be more susceptible to parasites, which in turn may affect the impact of this major predator on aquatic community dynamics.

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Sulfate transport kinetics and toxicity are modulated by sodium in aquatic insects

Cited by 30 publications

References 43 publications

Are sulfate effects in the mayfly Neocloeon triangulifer driven by the cost of ion regulation?

Are sulfate effects in the mayfly Neocloeon triangulifer driven by the cost of ion regulation?

Why are mayflies (Ephemeroptera) lost following small increases in salinity? Three conceptual osmophysiological hypotheses

Chronic Exposure to High Concentrations of Road Salt Decreases the Immune Response of Dragonfly Larvae

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