Regulation of Muscle Hydration Upon Hypo‐ or Hyper‐Osmotic Shocks: Differences Related to Invasion of the Freshwater Habitat by Decapod Crustaceans

Abstract

Decapod crustaceans have independently invaded freshwater habitats from the sea/estuaries. Tissue hydration mechanisms are necessary for the initial stages of habitat transitions but can be expected to diminish, as the capacity for extracellular homeostasis increases in hololimnetic species. Six decapod species have been compared concerning the maintenance of muscle hydration in vitro: Hepatus pudibundus (marine); Palaemon pandaliformis (estuarine resident), Macrobrachium acanthurus (freshwater diadromous), and the three hololimnetic Macrobrachium potiuna, Dilocarcinus pagei, and Aegla parana. The effects of inhibitors of potassium channels (barium chloride) and NKCC (furosemide) were evaluated under isosmotic, and respectively hypo- (50% below iso) or hyper- (50% above iso) conditions. There was high muscle hydration control in H. pudibundus with a possible role of NKCC in isosmotic conditions. Shrimps consistently showed small deviations in muscle hydration under anisosmotic conditions; P. pandaliformis has shown evidence of the presence of NKCC; M. potiuna was the species less affected by both inhibitors, under iso- or anisosmotic conditions. In the two hololimnetic crab species, both independent long-time inhabitants of freshwater, while the capacity to deal with hyper-osmotic shock is decreased, the capacity to deal with hyposmotic shock is retained, possibly because of hemolymph dilution during molting in fresh water. D. pagei apparently depends on potassium channels for volume recovery after swelling, whereas A. parana shows some dependence on NKCC to minimize volume loss in hyper-osmotic conditions. Although no molecular screening techniques have been tried here, data point to distinct cell/tissue transport mechanisms acting upon hydration/volume challenges in decapods of different habitats and lineages.

Oxygen consumption remains stable while ammonia excretion is reduced upon short time exposure to high salinity in Macrobrachium acanthurus (Caridae: Palaemonidae), a recent freshwater colonizer

“…The great ability of tissue to maitain its water concentration was also documented for M. acanthurus and the other palaemonids M. potiuna and P. pandaliformis, through an "in vitro" experiment in which tissues were exposed to hypo-and hyperosmotic saline solutions that corresponded to a 50% change with respect to the isosmotic control. In this study, the hydration of the shrimp tissues varied in only about 10% (Freire et al 2013). This high capacity to maintain tissue water levels is in part responsibe for the euryhalinity of M. acanthurus, which, throughout its life cycle, switches between freshwater and brackish water (Freire et al 2008a(Freire et al , 2013 The maintenance of tissue hydration happens through the regulation of the flux of inorganic ions and concentration of aminoacids or other nitrogenous compounds in the tissues or body fluids (e.g., Pierce 1982, Gilles 1987.…”

“…In this study, the hydration of the shrimp tissues varied in only about 10% (Freire et al 2013). This high capacity to maintain tissue water levels is in part responsibe for the euryhalinity of M. acanthurus, which, throughout its life cycle, switches between freshwater and brackish water (Freire et al 2008a(Freire et al , 2013 The maintenance of tissue hydration happens through the regulation of the flux of inorganic ions and concentration of aminoacids or other nitrogenous compounds in the tissues or body fluids (e.g., Pierce 1982, Gilles 1987. Under hyperosmotic challenges, osmolyte concentrations increase in tissues, as already shown for the crustaceans M. amazonicum, M. olfersii, Dilocarcinus pagei (Augusto et al 2007a, b).…”

“…The fact that freshwater Palaemonid shrimps have recently transitioned from saline waters to more dilute waters renders them quite tolerant to increased salinity (Freire et al 2008a(Freire et al , 2013. Freshwater Palaemonid shrimp adults -especially the more coastal and diadromous species -those whose larvae depend on brackish waters for their proper development (Charmantier 1998, Anger 2003, McNamara and Faria 2012, are particularly euryhaline (McNamara 1987).…”

“…It is during ecdysis that cell volume may be challenged in these shrimps, as their internal medium fluctuates (compared to the intermoult period), diluting strongly in fresh waters. However, crustaceans in general, palaemonid shrimps in particular, can face this challenge by regulating cell/tissue hydration quite efficiently (see Freire et al 2013). These hyper-regulation mechanisms, one of the most prominent features of freshwater crustaceans (second to the cuticle) have been frequently studied in Palaemonidae (e.g., Freire et al 2008b, McNamara andFaria 2012).…”

Molecular characterization and organ-specific expression of the gene that encodes betaine aldehyde dehydrogenase from the white shrimp Litopenaeus vannamei in response to osmotic stress

“…Therefore, LvBADH expression at low salinity concentrations suggests that GB is required to counteract hypo-osmotic stress. These results suggest that the accumulation of GB in muscle under osmotic stress may be due to the participation of a transport mechanism rather than in situ synthesis, as a response to hypo-or hyperosmotic salinities (Freire et al, 2013). The efflux and influx of organic osmolytes during osmotic changes is regulated by a swell-activated anion channel, also known as volume-sensitive organic osmolyte/anion channels (VSOAC).…”