Hypernatremia in Dice snakes (Natrix tessellata) from a coastal population: implications for osmoregulation in marine snake prototypes

Abstract

The widespread relationship between salt excreting structures (e.g., salt glands) and marine life strongly suggests that the ability to regulate salt balance has been crucial during the transition to marine life in tetrapods. Elevated natremia (plasma sodium) recorded in several marine snakes species suggests that the development of a tolerance toward hypernatremia, in addition to salt gland development, has been a critical feature in the evolution of marine snakes. However, data from intermediate stage (species lacking salt glands but occasionally using salty environments) are lacking to draw a comprehensive picture of the evolution of an euryhaline physiology in these organisms. In this study, we assessed natremia of free-ranging Dice snakes (Natrix tessellata, a predominantly fresh water natricine lacking salt glands) from a coastal population in Bulgaria. Our results show that coastal N. tessellata can display hypernatremia (up to 195.5 mmol x l(-1)) without any apparent effect on several physiological and behavioural traits (e.g., hematocrit, body condition, foraging). More generally, a review of natremia in species situated along a continuum of habitat use between fresh- and seawater shows that snake species display a concomitant tolerance toward hypernatremia, even in species lacking salt glands. Collectively, these data suggest that a physiological tolerance toward hypernatremia has been critical during the evolution of an euryhaline physiology, and may well have preceded the evolution of salt glands.

Figure 1. Map of the study area.

The upper panel gives the location of the Poda Protected Areas in the vicinity of Bourgas, Bulgaria. Emergent lands are indicated in white, water is indicated in light grey. The lower panel shows the Poda Protected Area (dashed area). Emergent lands are indicated in white and water is indicated in light grey. Numbers designate salinity (‰) recorded for three ponds, two locations on the shore of the Black Sea, and one location at the mouth of the Mandra Lake. The two arrows show sites where tracks from snakes commuting between the land and the Black Sea were observed.

Figure 2. Natremia (plasma sodium concentration) of thirteen free-ranging individual N. tessellata captured at Poda Protected Area, Bulgaria.

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). For clarity, individuals are ranked by ascending order of natremia.

Figure 3. Published data on snake natremia.

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 , , –. 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). Numbers above the bars indicate survival rates (no number  = 100%). Data are mean values per species ± SD.