The Aglomerular Kidney of the Deep-sea Fish, Ateleopus japonicus (Ateleopodiformes: Ateleopodidae): Evidence of Wider Occurrence of the Aglomerular Condition in Teleostei
Hitherto, aglomerular kidneys have been found in some species within three groups of teleosts: Elopomorpha, Paracanthopterygii, and Percomorpha. Here we report the presence of an aglomerular kidney in the benthopelagic deep-sea fish Ateleopus japonicus (Ateleopodidae: Jellynose fish). The kidney consists of a pair of strap-like bands located in the typical retroperitoneal position. Light microscopic observation of serial longitudinal and cross sections revealed no glomerulus. The kidney is composed of renal tubules, sinusoidal capillaries of the renal portal system, and extensive interstitial lymphoid tissues. Each renal tubule is highly convoluted and surrounded by the well-developed renal portal system. The tubules are well separated within the kidney. An updated species list of teleosts with aglomerular kidneys is presented. Water content of A. japonicus was found to be very high for a marine fish (ca. 90%), and we discuss the functional significance of the aglomerular kidney in A. japonicus in terms of neutral buoyancy.Abstract

Gross morphology of A. japonicus. (A) External shape. Note swollen snout containing gelatinous substance. Defrosted specimen. (B) Transverse section of the body just caudal to the anus. The level of section is indicated in (A). Note the presence of gelatinous matrix (Gm) dorsal and ventral to the vertebra (asterisk). The borderline of Gm in the right half is indicated by dotted line. Formalin-fixed specimen. An, anus; M, muscle. Scale bar = (A) 10 cm; (B) 1 cm.

Gross morphology of the kidney. Rostral is to the right in all panels. Line drawing of the kidney in each photograph is shown in the bottom of each panel. (A) Right-side view showing the location of the kidney. Muscles and the peritoneum were removed to expose the kidney. The caudal vein (Cv) and corpuscle of Stannius (Cs) are illustrated in the line drawings of (A) and (B), which are not visible in the photographs. (B) Dorsal view of the kidney removed from the abdominal cavity. Asterisks indicate the area in close contact with the wall of the dorsal aorta. (C) Ventral view of the kidney. An, anus; Es, esophagus; L, liver; Liv, large intrarenal vein; M, muscle; P, peritoneum (left inside); Pv, postcardinal vein; S, stomach; Sp, spleen; U, ureter; white arrows, segmental intercostal arteries. Scale bar = 1 cm.

Schematic drawing of the caudal part of the kidney of A. japonicus based on gross and histological observations of the present study. Rostral is to the left, and the right kidney is drawn by dotted line. The mesonephric duct (Md) collects renal tubules (Rt) and finally leads to the ureter (U). The caudal vein (Cv) is connected to the large intrarenal vein (Liv) that branches out into the sinusoids of renal portal system (Rps). The blood drains out of the kidney through the postcardinal vein (Pv). Cs, corpuscle of Stannius; Ilt, interstitial lymphoid tissue.

Histology of the kidney. (A) Horizontal section of a dorsal part of bilateral kidney. Rostral is to the top. Renal tubules (Rt) are convoluted and appear at various places in the section. Mesonephric duct (Md) of the left kidney is visible running rostrocaudally. Md branches into Rts (arrows). The sectioning angle was slightly oblique to the horizontal plane, and the right kidney was sectioned more ventrally than the left kidney. It should be noted that Rts are frequently observed to run mediolaterally toward the Md at this dorsoventral level. (B) A higher magnification photograph of the boxed area in (A). The round structure has an aggregate of red blood cells (Rb) within the sinusoid of renal portal system (Rps). (C) Cross section of the anterior part of the left kidney. Dorsal is to the top. (D) Cross section of the middle part of right and left kidneys. Dorsal is to the top. Da, dorsal aorta; Ilt, interstitial lymphoid tissue; Liv, large intrarenal vein; Pv, postcardinal vein. Scale bar = (A), (C), (D) 1 mm; (B) 50 µm.

Histology of the renal tubule and renal portal system. (A) A renal tubule (Rt) is surrounded by renal portal system (Rps) that is in turn surrounded by the interstitial lymphoid tissue (Ilt). Rps are compartmentalized by connective tissue (Ct). Red blood cells (Rb) that are coagulated in the Rps are larger than the cells in the Ilt, and the Rps thus can be discriminated from the Ilt. (B) A lower magnification photograph of the section shown in (A). Asterisks indicate the space around the Rts, which is most likely an artifact caused by the shrinkage of the tubules, because the Rts are seen to attach to the basement membrane at a point (arrows). (C) Pseudocolor analysis of the section shown in (B). The sinusoid of Rps is colored with semi-transparent red and Ct with black. Scale bar = (A) 50 µm; (B), (C) 200 µm.

Diagram of a nephron of A. japonicus drawn after Portmann (1976). Dorsal is to the top and rostral is to the left. The renal tubule (Rt) without a glomerulus is surrounded by the well-developed renal portal system (Rps) and forms primitive urine by tubular secretion. Black arrows indicate the direction of venous blood flow and white arrows that of urine flow. Ilt, interstitial lymphoid tissue; Liv, large intrarenal vein; Md, mesonephric duct; Pv, postcardinal vein.
Contributor Notes
Associate Editor: E. Schultz.