Observations on the Sexual Segment of the Kidney of Snakes with Emphasis on Ultrastructure in the Yellow‐Bellied Sea Snake, Pelamis platurus

Abstract

The sexual segment of the kidney (SSK) is an accessory sex structure in male lizards and snakes (Squamata). We describe histology of the SSK in 12 species of snakes, including one from the basal Scolecophidia, Leptotyphlops dulcis, and from the more advanced Alethinophidia, species from the Acrochordidae (Acrochordus granulatus), Homalopsidae (Cerberus rynchops), Uropeltidae (Teretrurus sanguineus), and eight species from the Elapidae, including six species of sea snakes. We also describe the ultrastructure of the SSK of the sea snake, Pelamis platurus. The SSK of L. dulcis does not include the ureter but does include distal convoluted tubules (DCTs) and collecting ducts. In all other snakes examined, the SSK is limited to the DCTs and does not differ in histology by any consistent character. We found apparently mature individuals of several species with inactive SSKs. Hypertrophied SSKs give positive reactions for protein secretions but variable reactions for carbohydrates. Ultrastructure of the SSK of P. platurus reveals nuclei situated medially in the epithelium and mature electron dense secretory vacuoles in other areas of the cytoplasm. Product release is apocrine. Junctional complexes only occur at the luminal border, and intercellular canaliculi become widened and are open basally. No cytologically unique characters occur in the SSK of P. platurus. The ancestral condition of the SSK in squamates is the presence of simple columnar epithelium specialized for secretion of a protein þ carbohydrate product that matures and is released seasonally. Anat Rec,

Sexual segment of the kidney of the lizard, Eutropis carinata: A light microscopic and ultrastructural seasonal study

“…The hypertrophy of the SSK and the production of secretory granules culminates during the breeding phase. The highly columnar cells of the SSK are loaded with secretory granules and the euchromatic nuclei are pushed towards the basal membranes as in other squamates (Gabri, 1983; Kuhnel & Krisch, 1974; Rheubert et al, 2011; Sever et al, 2008; Sever & Hopkins, 2005; Siegel et al, 2009), unlike centrally placed nuclei in a couple of snakes (Sever et al, 2002, 2012). A marked reduction of the cells of the SSK from columnar to cuboidal, accompanied by reduction in the secretory granules, was observed during the post‐breeding phase.…”

“…Histochemical studies on 73 species of squamates representing 19 families found that the SSK was rich in protein secretion, but the PAS/AB reaction was quite variable (Saint Girons, 1972). Studies on snakes have shown that the secretory granules show PAS + reaction indicating the presence of neutral carbohydrates and Brilliant Indocyanine (BB) + reaction for proteins (Rojas et al, 2013; Sever et al, 2002, 2008, 2012; Siegel et al, 2009), except for the snake Teretrurus sanguineus which showed PAS—reaction (Sever et al, 2012). The secretory granules among most of the lizards have also shown positive reaction for PAS + and MBB + (Del Conte, 1972; Rheubert et al, 2011, 2015; Sever & Hopkins, 2005) except for the two neotropical lizards; N. frenata and A. dorsivittatum whose secretory granules have shown negative reaction for PAS—(Novelli et al, 2018).…”

“…Numerous histological studies on the SSK of squamates have been published (Novelli, de Oliveira, Castañon, Silva, & De Souse, 2018; Rheubert et al, 2011; Sever et al, 2002, 2008; Sever & Hopkins, 2005; Sever, Rheubert, Gautreaux, Hill, & Freeborn, 2012; Siegel, Aldridge, Clark, Poldemann, & Gribbins, 2009). During the breeding season, the cells of the SSK are high columnar with basal/centrally located nuclei and the cytoplasm is loaded with conspicuous large eosinophilic spherical droplets or secretory granules (Krohmer, 2004; Krohmer et al, 1987; Mathies et al, 2010; Novelli et al, 2018; Rheubert, Siegel, & Trauth, 2015; Sarkar & Shivanandappa, 1989; Sever et al, 2008, 2012; Sever & Hopkins, 2005; Siegel et al, 2009; Van Wyk, 1995).…”

“…Numerous histological studies on the SSK of squamates have been published (Novelli, de Oliveira, Castañon, Silva, & De Souse, 2018; Rheubert et al, 2011; Sever et al, 2002, 2008; Sever & Hopkins, 2005; Sever, Rheubert, Gautreaux, Hill, & Freeborn, 2012; Siegel, Aldridge, Clark, Poldemann, & Gribbins, 2009). During the breeding season, the cells of the SSK are high columnar with basal/centrally located nuclei and the cytoplasm is loaded with conspicuous large eosinophilic spherical droplets or secretory granules (Krohmer, 2004; Krohmer et al, 1987; Mathies et al, 2010; Novelli et al, 2018; Rheubert, Siegel, & Trauth, 2015; Sarkar & Shivanandappa, 1989; Sever et al, 2008, 2012; Sever & Hopkins, 2005; Siegel et al, 2009; Van Wyk, 1995). In several squamate species, histochemical and biochemical studies of the SSK granules indicate that they contain mucopolysaccharides, glycogen, neutral glyco‐ or mucoproteins, neutral carbohydrates, lipids, phospholipids, choline, and/or acid phosphatase (Bishop, 1959; Deb & Sarkar, 1963; Del Conte & Tamayo, 1973; Burtner et al, 1965; Kuhnel & Krisch, 1974; Misra, Sanyal, & Prasad, 1965; Prasad & Reddy, 1972; Prasad and Sanyal, 1969; Reddy et al, 1972a, 1972b; Sanyal & Prasad, 1966; Sanyal et al, 1966; Saint Girons, 1972; Sarkar & Shivanandappa, 1983, 1989; Sever & Hopkins, 2005; Sever et al, 2008, 2012; Rheubert et al, 2011; Weil, 1984; Weil & Aldridge, 1985).…”

“…The secretory granules are large and electron dense in the snakes Natrix natrix (Kuhnel and Krisch (1974), Agkistrodon piscivorus (Sever et al, 2008) and Pelamis platurus (Sever et al, 2012) and in the lizards S. laterale (Sever & Hopkins, 2005) and Hemidactylus turcicus (Rheubert et al, 2011). The SSK shows apocrine mode of secretion in the snakes N. natrix (Kuhnel & Krisch, 1974), Seminatrix pygaea (Sever et al, 2002) and P. platurus (Sever et al, 2012) and in the lizards Podarcis taurica (Gabri, 1983) and S. laterale (Sever & Hopkins, 2005). Whereas, merocrine mode of secretion was found in the snake Nerodia s sipedon (Krohmer, 2004) and in the lizard H. turcicus (Rheubert et al, 2011).…”