Salinity tolerance and structure of external and internal gills in tadpoles of the crab-eating frog, Rana cancrivora

Abstract

Salinity tolerance and histology of gills were studied in Rana cancrivora larvae. The tadpoles at the external gill stages (W stages 21-22) were able to survive in media containing up to 40% seawater, but died in water of higher salinity. Their external gills appear to have no critical role in adaptation to seawater. However, advanced tadpoles with internal gills (T-K stages I-XVIII) were able to tolerate 50% or higher seawater. In the internal gills, there are numerous mitochondria-rich cells (MR cells) scattered on the ventral and lateral epithelia of the gill arches and the gill tufts in both freshwater- and seawater-acclimated tadpoles. In freshwater-acclimated tadpoles there are three types of MR cell: (1) microplicated, (2) microvillous, and (3) apically vacuolated. In tadpoles acclimated to dilute seawater, the ratio of type-1 to type-2 cells is lower, although all three types of MR cell are present. In 60%-seawater-acclimated tadpoles, a few MR cells with a lumen and concave cytoplasm at the apical membrane (type 4) are present. The changes in MR cell morphology under ambient conditions of low or high salinity may reflect alterations in the physiological roles of the gills with regard to transport of ions.

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

“…Tadpoles experiencing low salinity in early development (before Gosner stage 38) had much higher survival rates (100%) than tadpoles exposed to high salinity during the same period, even if they were later switched to low salinity. Gills are the main organs responsible for ion and water balance in tadpoles (Dietz and Alvarado 1974;Uchiyama and Yoshizawa 1992;Ultsch et al 1999), and tadpoles may lack sufficient salt-excreting ability to cope with high osmotic stress until internal gills develop (Chinathamby et al 2006). Uchiyama and Yoshizawa (1992) suggested that the euryhaline tadpoles of Fejervarya cancrivora (Rana cancrivora) tolerated higher salinity once they had internal gills than those still relying on external ones because the former are more abundant in mitochondria-rich cells (MR cells), thought key in ion excretion.…”

“…Gills are the main organs responsible for ion and water balance in tadpoles (Dietz and Alvarado 1974;Uchiyama and Yoshizawa 1992;Ultsch et al 1999), and tadpoles may lack sufficient salt-excreting ability to cope with high osmotic stress until internal gills develop (Chinathamby et al 2006). Uchiyama and Yoshizawa (1992) suggested that the euryhaline tadpoles of Fejervarya cancrivora (Rana cancrivora) tolerated higher salinity once they had internal gills than those still relying on external ones because the former are more abundant in mitochondria-rich cells (MR cells), thought key in ion excretion. Concordantly, MR cells only appeared in Rana dalmatina tadpoles once internal gills had developed, but were absent in their external gills (Brunelli et al 2004).…”

Ultrastructure and development of the gills in Rana dalmatina (Amphibia, Anura)

“…The MRC has been noted in the epithelium of the external gills of R. cancrivora tadpoles, adapted to 10% seawater (Uchiyama and Yoshizawa 1992), even if in a rather reduced number; in the same paper the authors reported the presence of a few MRCs even in the epidermis of the early larvae of R. cancrivora. In the experiments conducted by the same authors on tadpoles acclimatized to different concentrations of seawater, the tadpoles at external gill stages showed a lower tolerance compared to tadpoles of internal gill stages, managing to survive only until a concentration equal to 40% of seawater in comparison to 100% for tadpoles with internal gills.…”

“…The respiratory apparatus of Anura has been the subject of different studies relating to anatomy and gill ultrastructure in different species: Discoglossus pictus Otth, 1837 (Hourdry 1974), Rana cancrivora Gravenhorst, 1829 (Uchiyama and Yoshizawa 1992;Uchiyama et al 1990), Litoria ewingii Dumeril &Bibron, 1841 (McIndoe andSmith 1984). Others have studied gill apparatus in connection with blood circulation (De Saint-Aubain 1981) or with regard to different aspects which involve pharyngeal organs (Seale et al 1982;Viertel 1982Viertel , 1985aWassersug 1972Wassersug , 1976Wassersug , 1984; moreover larval oral cavity morphology has also been used in studies of evolutionary relationships (Wassersug 1980;Wassersug and Heyer 1988).…”

“…In Amphibia, the hypothesis of the involvement of permanent gills in osmoregulation was advanced by Hourdry (1974): using the structural and ultrastructural analysis of the gills in D. pictus, the gill chamber was recognized, according to physiological studies, as the principal site of ionic exchange. The presence of specialized cells in the transient gills of R. cancrivora adapted to different levels of salinity (Uchiyama and Yoshizawa 1992) make one consider the morphological differences in the different species of Amphibia Anura in relation to environmental conditions.…”