Evolution of osmoregulatory patterns and gill ion transport mechanisms in the decapod Crustacea: a review

Abstract

Decapod crustaceans exhibit a wide range of osmoregulatory patterns and capabilities from marine osmoconformers to brackish and freshwater hyperregulators to terrestrial hyporegulators. The principal gill salt transport mechanisms proposed to underlie the ability of the better-known taxa to occupy these specific habitats are examined here. Traditional thinking suggests that a graduated series of successively stronger adaptive mechanisms may have driven the occupation of ever more dilute osmotic niches, culminating in the conquest of freshwater and dry land. However, when habitat and osmoregulatory parameters are analyzed quantitatively against the phylogenies of the taxa examined, as illustrated here using a palaemonid shrimp clade, their association becomes questionable and may hold true only in specific cases. We also propose a putative evolution for gill epithelial ion pump and transporter arrangement in a eubrachyuran crab clade whose lineages occupy distinct osmotic niches. By including the systematics of these selected groups, this review incorporates the notion of a protracted time scale, here termed 'phylophysiology', into decapod osmoregulation, allowing the examination of putative physiological transformations and their underlying evolutionary processes. This approach assumes that species are temporally linked, a factor that can impart phylogenetic structuring, which must be considered in comparative studies. Future experimental models in decapod osmoregulatory physiology should contemplate the phylogenetic relationships among the taxa chosen to better allow comprehension of the transformations arising during their evolution.

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 response may also be called a hypo-conformation, as in Moreira et al (1983) for M.acanthurus and other species of the genus. This strong tolerance to increases in salinity is in fact expected from the components of a clade that has invaded the freshwater relatively recently (Murphy and Austin 2005, Augusto et al 2007a, b, 2009, Pileggi and Mantelatto 2010, Collins et al 2011, McNamara and Faria 2012.…”

“…The family Palaemonidae has a marine origin and passed through various independent events of freshwater invasion (Murphy and Austin 2005, Ashelby et al 2012, McNamara and Faria 2012, Anger 2013. These events have occurred quite recently, ~30 mya (Tertiary), and are still happening (Murphy and Austin 2005, Augusto et al 2007a, b, 2009, Pileggi and Mantelatto 2010, Collins et al 2011, McNamara and Faria 2012. The family comprises about 116 genera.…”

“…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).…”

“…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). Hyporegulation mechanisms, by contrast, have been much less investigated and remain elusive (Freire et al 2008b, McNamara andFaria 2012).…”

Effect of environmental salinity and dopamine injections on key digestive enzymes in hepatopancreas of the euryhaline crab <i>Cyrtograpsus angulatus</i> (Decapoda: Brachyura: Varunidae)

“…Hypo and hyper-osmoregulation involves the absorption or secretion of ions, respectively, to maintain hemolymph ion homeostasis Faria 2012, Romano andZeng 2012). Hyper-osmoregulation requires the involvement of various branchial ion transport mechanisms such as Na + /K + -ATPase activity and carbonic anhydrase, although the extent, timing and activity in individual gills can be speciesspecific; hypo-osmoregulation responses appear more variable and may require different mechanisms (López Mañanes et al 2000, 2002, Schleich et al 2001, Bianchini et al 2008, Freire et al 2008, McNamara and Faria 2012, Romano and Zeng 2012. Biochemical adaptation to environmental salinity appears to be a complex process involving also the participation of enzymes and transport systems in extrabranchial tissues (Jahn et al 2006, Pinoni and López Mañanes, 2004, 2009, Martins et al 2011.…”