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.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.

Salt tolerance's toll: prolonged exposure to saline water inflicts damage to the blood cells of dice snakes (<i>Natrix tessellata</i>)

“…The sublingual salt gland is the primary site of salt excretion in sea snakes (Babonis et al, 2009), but dice snakes lack salt glands. However, these snakes can spend long periods of time in brackish and saline waters (see Brischoux and Kornilev, 2014). The authors measured hypernatremia up to 195.5 mmol L −1 in some specimens.…”

“…Consequently, interpretation of results will be restricted to female individuals of this species. The snakes were collected from the southern Bulgarian Black Sea coast, around Poda, a protected site (PS) (42.445706 N, 27.462928 E, Datum: WGS84) and the neighbouring Foros Bay and Mandra Lake (map in Brischoux and Kornilev, 2014). The site ( ∼ 1.5 km 2 ) encompasses shallow (0-2 m) aquatic habitats, widely ranging in salinity from fresh (< 0.5 ‰) and brackish (0.5-30 ‰) to saline water (> 30 ‰).…”

“…Blood samples of 0.3-0.4 mL were obtained by cardiocentesis using a heparinized 30 G-needle and syringe (see Brischoux and Kornilev, 2014). The collected blood was transferred immediately into heparinized Eppendorf vials.…”

“…According to Ahmadzadeh et al (2011), N. tessellata in southeastern Iran thrives in waters with salinity between 1.3 and 28 ‰. Brischoux and Kornilev (2014) demonstrated that free-ranging N. tessellata from a coastal population in Bulgaria display highly variable plasma sodium concentrations ranging from normonatremia to hypernatremia without any apparent effect on several physiological and behavioural traits (e.g. hematocrit, body condition, foraging).…”

“…hematocrit, body condition, foraging). Those snakes inhabit the Black Sea coast and regularly hunt at sea Stojanov et al, 2011;Brischoux and Kornilev, 2014). However, the physiological mechanisms responsible for this tolerance are poorly known.…”