The pelvic kidney of male Ambystoma maculatum (Amphibia, urodela, ambystomatidae) with special reference to the sexual collecting ducts

Abstract

This study details the gross and microscopic anatomy of the pelvic kidney in male Ambystoma maculatum. The nephron of male Ambystoma maculatum is divided into six distinct regions leading sequentially away from a renal corpuscle: (1) neck segment, which communicates with the coelomic cavity via a ventrally positioned pleuroperitoneal funnel, (2) proximal tubule, (3) intermediate segment, (4) distal tubule, (5) collecting tubule, and (6) collecting duct. The proximal tubule is divided into a vacuolated proximal region and a distal lysosomic region. The basal plasma membrane is modified into intertwining microvillus lamellae. The epithelium of the distal tubule varies little along its length and is demarcated by columns of mitochondria with their long axes oriented perpendicular to the basal lamina. The distal tubule possesses highly interdigitating microvillus lamellae from the lateral membranes and pronounced foot processes of the basal membrane that are not intertwined, but perpendicular to the basal lamina. The collecting tubule is lined by an epithelium with dark and light cells. Light cells are similar to those observed in the distal tuble except with less mitochondria and microvillus lamellae of the lateral and basal plasma membrane. Dark cells possess dark euchromatic nuclei and are filled with numerous small mitochondria. The epithelium of the neck segment, pleuroperitoneal funnel, and intermediate segment is composed entirely of ciliated cells with cilia protruding from only the central portion of the apical plasma membrane. The collecting duct is lined by a highly secretory epithelium that produces numerous membrane bound granules that stain positively for neutral carbohydrates and proteins. Apically positioned ciliated cells are intercalated between secretory cells. The collecting ducts anastomose caudally and unite with the Wolffian duct via a common collecting duct. The Wolffian duct is secretory, but not to the extent of the collecting duct, synthesizes neutral carbohydrates and proteins, and is also lined by apical ciliated cells intercalated between secretory cells. Although functional aspects associated with the morphological variation along the length of the proximal portions of the nephron have been investigated, the role of a highly secretory collecting duct has not. Historical data that implicated secretory activity concordant with mating activity, and similarity of structure and chemistry to sexual segments of the kidneys in other vertebrates, lead us to believe that the collecting duct functions as a secondary sexual organ in Ambystoma maculatum.

Genital and Pelvic Kidney Renal Corpuscles of the Red-spotted Newt,Notophthalmus viridescens(Amphibia, Urodela, Salamandridae)

“…With light microscopy, Spengel (1876) noted that nephron structure (regionality) was identical between the two kidney regions and thus hypothesized that nephrons from the pelvic and genital kidneys were both involved in urine formation, with the added function of sperm transport in genital kidney nephrons. Siegel et al (2010Siegel et al ( , 2013 and Nicholson and Siegel (2014) confirmed Spengel's hypothesis that regionality of nephrons in the genital and pelvic kidneys was identical but also provided evidence with the use of transmission electron microscopy that genital kidney proximal and distal tubules were modified from those of pelvic kidney proximal and distal tubules for sperm transport. These modifications included ciliated proximal tubule epithelial cells in the genital kidney and reduced basal plasma membrane folding of the epithelia in both genital kidney proximal and distal tubules in Ambystoma maculatum and Notophthalmus viridescens.…”

“…All other studies with light microscopy provided the same results; i.e., all salamanders possess both pelvic and genital kidney nephrons and the same nephron regions can easily be identified in the pelvic and genital kidneys; i.e., renal corpuscles with glomeruli (although evidence of reduction was observed in Plethodontidae), proximal tubules, distal tubules, and collecting tubules (Siegel et al, 2010(Siegel et al, , 2012b(Siegel et al, , 2013(Siegel et al, , 2014aNicholson and Siegel, 2014).…”

“…M ALE salamanders possess kidneys with two distinct regions: a caudal region (termed the pelvic kidney) that is primarily involved in urine formation (Siegel et al, 2010; for an alternate function during mating see Siegel et al, 2012a) and a cranial portion (termed the genital kidney) that consists of nephrons that transport sperm from the vasa efferentia to the Wolffian ducts ( Fig. 1; Siegel et al, 2013).…”

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

“…A SSK also occurs as a secondary sexual structure in male Gasterosteidae (stickleback fish : Courrier, 1922;Jakobsson et al, 1999), in which the secretion is involved in construction of foam nests, and some male Caudata (salamanders: Siegel et al, 2010), in which the function of the secretion is unknown. The modified portions of the kidney tubules are considered to be independently evolved in squamates, fish, and salamanders (Siegel et al, 2010).…”

“…Within stickleback fishes, it is found within the ventral kidney (Courrier, 1922), and within salamanders, it is restricted to the collecting ducts (Siegel et al, 2010). Within the Squamata, the location of the SSK can include the intermediate segment, distal convoluted tubule (DCT), collecting duct, ureter (Ur), and combinations of the aforementioned (for review, see Rheubert et al, 2011).…”