Renal responses to salinity change in snakes with and without salt glands

Abstract

SUMMARYTo understand renal responses to salinity change in aquatic reptiles, we examined the structure and function of the kidney in three species of snake: a marine species with a salt gland (Laticauda semifasciata), a marine species without a salt gland (Nerodia clarkii clarkii) and a freshwater species without a salt gland (Nerodia fasciata). Both marine species maintained relatively constant plasma ions, even after acclimation to saltwater. By contrast, both plasma Cl -and mortality increased with salinity in the freshwater species. To investigate putative renal ion regulatory mechanisms, we examined the distribution and abundance of Na -cotransporter (NKCC2). In all species, NKA localized to the basolateral membranes of the distal tubule and the connecting segments and collecting ducts only; there was no effect of salinity on the distribution of NKA or on the abundance of NKA mRNA in any species. NKCC2 protein was undetectable in the kidney of any of the species and there was no effect of salinity on NKCC2 mRNA abundance. We also examined the distribution and abundance of aquaporin 3 (AQP3) in the kidney of these species; although putative AQP3 localized to the basolateral membranes of the connecting segments and collecting ducts of all three species, there was no effect of salinity on the localization of the protein or the abundance of the transcript. Interestingly, we found very few differences across species, suggesting that the snake kidney may play a trivial role in limiting habitat use.

Hypernatremia in Dice Snakes (Natrix tessellata) from a Coastal Population: Implications for Osmoregulation in Marine Snake Prototypes

“…These data were available from strictly fresh water species ( Nerodia fasciata and N. sipedon [24], [26]), salt tolerant species lacking salt glands ( N. clarckii clarckii , N. clarckii compressicauda , Thamnophis valida [24], [26]), amphibious sea kraits with functional salt glands ( Laticauda saintgironsi , L. laticaudata , L. semifasciata [24], [25]) and fully marine sea snakes with functional salt glands ( Acrochordus granulatus , Hydrophis elegans , H. cyanocinctus , Pelamis platurus [18], [19], [21]–[23]. The dashed lines indicate the range of normonatremia (130–160 mmol.l −1 [45]) and the horizontal black line indicates mean normonatremia (145 mmol.l −1 ).…”

“…These studies have led to the hypothesis that the development of a physiological tolerance to hypernatremia may have been an important feature of the evolution of marine snakes [25]. However, data gathered under experimental conditions show that fresh water species lacking salt glands (including coastal presumably salt tolerant species) rapidly accumulate large salt loads when acclimated in brackish and salt water [24], [26]. In most of these cases, the resulting hypernatremia was lethal [24], [26].…”

“…However, data gathered under experimental conditions show that fresh water species lacking salt glands (including coastal presumably salt tolerant species) rapidly accumulate large salt loads when acclimated in brackish and salt water [24], [26]. In most of these cases, the resulting hypernatremia was lethal [24], [26]. Taken together, these elements highlight the lack of information from groups thought to resemble transitional forms between the land and the sea (species lacking salt glands but occasionally using salty environments) to draw a comprehensive picture of the evolution of an euryhaline physiology in these organisms.…”

Tubular localization and expressional dynamics of aquaporins in the kidney of seawater-challenged Atlantic salmon

“…A signal for Aqp3a was also seen in the sub-apical space, suggesting a role in volume regulation of intracellular vesicles, which are plentiful in the proximal tubules of rainbow trout (Anderson and Loewen 1975), in addition to trans-cellular water exchange (secretion). In amphibians, reptiles, birds and mammals, AQP3 is found in basolateral membranes of late distal and collecting ducts as well as the urinary bladder of the tree frog (Nielsen et al 2002;Akabane et al 2007;Babonis et al 2011;Nishimura and Yang 2013). This apparent shift in cellular/sub-cellular localization from teleosts to terrestrial vertebrates may be due to the increased need for water reabsorption in the latter as well as the more specialized architecture of the metanephric kidneys of birds and mammals.…”

Salinity influences the distribution of marine snakes: implications for evolutionary transitions to marine life

“…First, four phylogenetic lineages of snakes independently underwent the transition to marine life; and those four lineages are spread across three Families (Homalopsidae, Acrochordidae and within Elapidae, the subfamilies Laticaudinae and Hydrophiini [Heatwole 1999]). Second, all of these independent transitions exhibit convergent evolution of salt‐secreting glands (modified sub‐lingual glands in Acrochordidae, Laticaudinae and Hydrophiini [Dunson 1976] and modified pre‐maxillary glands in Homalopsidae [Dunson and Dunson 1979]), whereas no extant terrestrial or freshwater snakes are known to possess any such salt‐secreting adaptations (Babonis et al 2011). Third, the high ratio of surface area to volume imposed by the snake body plan (Brischoux and Shine 2011) likely makes maintaining osmotic balance a major physiological challenge for marine snakes, and some species cannot survive without access to fresh or brackish water (Lillywhite and Ellis 1994, Lillywhite et al 2008).…”