Comparative sodium transport patterns provide clues for understanding salinity and metal responses in aquatic insects

Scheibener, Shane; Richardi, Vinícius Sobrinho; Buchwalter, David B.

doi:10.1016/j.aquatox.2015.12.006

Cited by 40 publications

(38 citation statements)

References 67 publications

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“…Also contradicting the conventional model of osmoregulation is Na regulation in the mayfly Maccaffertium sp; Na is the primary cation involved in osmoregulation in animals [20]. This species increases its rate of Na uptake as its external Na þ (and salinity) increases, with no sign of a decreasing slope of Na uptake with increasing external Na þ [47]. The external Na/salinity concentration had no effect on Maccaffertium sp.…”

Section: A Challenge To the Conventional Model Of Osmoregulationmentioning

confidence: 85%

“…The external Na/salinity concentration had no effect on Maccaffertium sp. 's respiration rate [47], as is the case with another mayfly species [48]. But these species should need to pull in less Na as their external Na þ (and thus salinity) concentration increases (figure 1a) and thus need less energy (figure 1b).…”

Section: A Challenge To the Conventional Model Of Osmoregulationmentioning

confidence: 99%

“…Despite Maccaffertium sp. 's Na þ uptake increasing, its total Na body burden is invariant of the external Na þ concentration [47], so as external Na þ increases Maccaffertium sp. 's turnover of Na is increasing ( figure 3).…”

Section: Hypothesis 1-energetics Of Ion Uptakementioning

confidence: 99%

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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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Section: A Challenge To the Conventional Model Of Osmoregulationmentioning

confidence: 85%

Section: A Challenge To the Conventional Model Of Osmoregulationmentioning

confidence: 99%

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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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“…have demonstrated a similar relationship between whole-body [Na + ] and NKA inhibition by metals (Supplemental Data, Table S3), but Na + uptake by Maccaffertium pudicum (Ephemeroptera), several Plecoptera, and another dipteran ( Atherix sp.) showed variable effects with exposure to Ag + or Cu 2+ [122], suggesting some differences in the Na + transporters between these insects and other freshwater animals.…”

Section: Transporters and Physiology Of Individual Ionsmentioning

confidence: 99%

Toxicological perspective on the osmoregulation and ionoregulation physiology of major ions by freshwater animals: Teleost fish, crustacea, aquatic insects, and Mollusca

Griffith

2016

Enviro Toxic and Chemistry

146

136

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Anthropogenic sources increase freshwater salinity and produce differences in constituent ions compared with natural waters. Moreover, ions differ in physiological roles and concentrations in intracellular and extracellular fluids. Four freshwater taxa groups are compared, to investigate similarities and differences in ion transport processes and what ion transport mechanisms suggest about the toxicity of these or other ions in freshwater. Although differences exist, many ion transporters are functionally similar and may belong to evolutionarily conserved protein families. For example, the Na+/H+-exchanger in teleost fish differs from the H+/2Na+ (or Ca2+)-exchanger in crustaceans. In osmoregulation, Na+ and Cl− predominate. Stenohaline freshwater animals hyperregulate until they are no longer able to maintain hypertonic extracellular Na+ and Cl− concentrations with increasing salinity and become isotonic. Toxic effects of K+ are related to ionoregulation and volume regulation. The ionic balance between intracellular and extracellular fluids is maintained by Na+/K+-adenosine triphosphatase (ATPase), but details are lacking on apical K+ transporters. Elevated H+ affects the maintenance of internal Na+ by Na+/H+ exchange; elevated HCO3− inhibits Cl− uptake. The uptake of Mg2+ occurs by the gills or intestine, but details are lacking on Mg2+ transporters. In unionid gills, SO42− is actively transported, but most epithelia are generally impermeant to SO42−. Transporters of Ca2+ maintain homeostasis of dissolved Ca2+. More integration of physiology with toxicology is needed to fully understand freshwater ion effects.

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“…In freshwater (FW) ecosystems, insects comprise the majority of invertebrate macrofauna and therefore are essential to FW ecosystem health (Scheibener et al., ). The benthic larvae of chironomids are ubiquitous in these ecosystems and Chironomus riparius are distributed throughout the northern hemisphere.…”

Section: Introductionmentioning

confidence: 99%

FLUID AND ION SECRETION BY MALPIGHIAN TUBULES OF LARVAL CHIRONOMIDS, Chironomus riparius: EFFECTS OF REARING SALINITY, TRANSPORT INHIBITORS, AND SEROTONIN

Zadeh-Tahmasebi

Bui

Donini

2016

Arch Insect Biochem Physiol

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Larvae of Chironomus riparius respond to ion-poor and brackish water (IPW, BW) conditions by activating ion uptake mechanisms in the anal papillae and reducing ion absorption at the rectum, respectively. The role that the Malpighian tubules play in ion and osmoregulation under these conditions is not known in this species. This study examines rates of fluid secretion and major cation composition of secreted fluid from tubules of C. riparius reared in IPW, freshwater (FW) and BW. Fluid secretion of tubules from FW and BW larvae was similar but tubules from IPW larvae secrete fluid at higher rates, are more sensitive to serotonin stimulation, and the secreted fluid contains less Na(+) . Therefore in IPW, tubules work in concert with anal papillae to eliminate excess water while conserving Na(+) in the hemolymph. Tubules do not appear to play a significant role in ion/osmoregulation under BW. Serotonin immunoreactivity in the nervous system and gastrointestinal tract of larval C. riparius was similar to that seen in mosquito larvae with the exception that the hindgut was devoid of staining. Hemolymph serotonin titer was similar in FW and IPW; hence, serotonin is not responsible for the observed high rates of fluid secretion in IPW. Instead, it is suggested that serotonin may work in a synergistic manner with an unidentified hormonal factor in IPW. Ion transport mechanisms in the tubules of C. riparius are pharmacologically similar to those of other insects.

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Comparative sodium transport patterns provide clues for understanding salinity and metal responses in aquatic insects

Cited by 40 publications

References 67 publications

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

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

Toxicological perspective on the osmoregulation and ionoregulation physiology of major ions by freshwater animals: Teleost fish, crustacea, aquatic insects, and Mollusca

FLUID AND ION SECRETION BY MALPIGHIAN TUBULES OF LARVAL CHIRONOMIDS, Chironomus riparius: EFFECTS OF REARING SALINITY, TRANSPORT INHIBITORS, AND SEROTONIN

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