Developmental Alterations and Osmoregulatory Physiology of a Larval Anuran under Osmotic Stress

Abstract

Water salinity represents an environmental stress for many species. Amphibians are particularly sensitive because they are generally poor osmoregulators, and most species are completely absent from brackish and saline environments. We experimentally examined the effect of different salinity levels on larvae of the toad Bufo calamita L., a species that occupies freshwater ponds but can also breed in brackish ponds. Two independent experiments are reported here. In both experiments, tadpoles under saline conditions (ranging between 85 and 200 mOsm) showed a slower developmental rate, metamorphosing between 4 and 9 d later than the controls. Bufo calamita tadpoles reared in brackish water increased their osmolality and solute concentration (mainly sodium and chloride), decreased their levels of glucose, and decreased the total protein content, all measured from whole-animal extracts. Although most larval anurans are strictly ammoniotelic until the completion of metamorphosis, a few species exposed to dehydrating environments have evolved the ability to use urea as an osmolyte during the larval phase. The data presented here reveal that although B. calamita seems to be yet another exception to the rule of larval strict ammoniotelism, the tadpoles are not able to use urea as an osmolyte and rely on sodium-chloride balance instead. Preliminary immunoassays of thyroid hormone content suggest a possible decrease in hormone levels induced in water salinity conditions that correlate with a decreased developmental rate.

Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity

“…Across species, the evolution of short larval periods in Spea and Scaphiopus was achieved through changes in TH physiology, as they show increased tissue TH content and sensitivity compared with Pelobates (41). We suggest that, initially, environmental acceleration of larval development in New World spadefoot toad ancestors was likely achieved through increased TH levels (55,56). Over time, direct selection would have favored genetic changes regulating TH levels and tissue sensitivity to TH, causing developmental acceleration in response to pond desiccation that would have further reduced the larval period in those lineages.…”

“…As for the regulatory mechanism, the amphibian developmental rate is highly conditioned by the environment and regulated by THs (24-27) so that intraspecific alterations in the larval period are often related to changes in TH concentration (55,56). Across species, the evolution of short larval periods in Spea and Scaphiopus was achieved through changes in TH physiology, as they show increased tissue TH content and sensitivity compared with Pelobates (41).…”

Irreversibility of a bad start: early exposure to osmotic stress limits growth and adaptive developmental plasticity

“…Hence, we established a total of six treatments as follows: constant low salinity (LLL), low salinity with early switch to high salinity (LHH), low salinity with late switch to high salinity (LLH), constant high salinity (HHH), high salinity with early switch to low salinity (HLL), and high salinity with late switch to low salinity (HHL). Because higher salinity slows down the rate of tadpole development (Gomez-Mestre et al 2004;Wu and Kam 2009), tadpoles reached the specific developmental stages at different time intervals. Because the time required for animals to develop from one stage to the next is not uniform, but depends on the specific stages and environmental conditions, the timing of salinity switches varied across treatments and were determined by average developmental stage.…”

“…All tadpoles are sensitive to salinity, and moderate salinity (2-9 parts per thousand; ppt) decreases tadpole survival, growth, and development (Christy and Dickman 2002;Gomez-Mestre et al 2004;Chinathamby et al 2006;Wu and Kam 2009). In most systems, pond salinity is lowest at the beginning of the amphibian reproductive period, as ponds fill up, and gradually increases over time as ponds evaporate and are maximal just prior to pond desiccation.…”

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

“…Some amphibians and cold-blooded amniotes can tolerate increased water salinity and some even reproduce in brackish water and seawater (Neill, 1958;Chakko, 1968;Christman, 1974;Dunson, 1977;Sillero and Ribeiro, 2010;Natchev et al, 2011). However, the effects of increased water conductivity on the populations of aquatic ectothermic tetrapods are not fully understood (Bentley and SchmidtNielsen, 1971;Spotila and Berman, 1976;Shoemaker et al, 1992;Gomez-Meste et al, 2004;Karraker, 2007;OrtizSantaliestra et al, 2010).…”