Publisher Summary This chapter analyzes the role of kidney in some marine creatures. In freshwater forms, the kidney functions largely as a water excretory device. With rare exceptions, this is accomplished by filtration at the renal glomerulus and implies the presence of suitable cellular components to conserve filtered ions and excrete dilute urine. In marine teleost forms, the kidney functions chiefly as an excretory device for magnesium and sulfate ions. In glomerular marine forms, associated machinery must be present to conserve water, monovalent ions, and other filtered plasma constituents. The cartilaginous sharks, skates, and rays, because they are hyperosmotic in a marine environment, have combined the principal functions of the kidneys of both freshwater and marine bony fishes. The chapter assembles all available information concerning the structure and function of the fish kidney and provides a unifying synthesis for the understanding of this organ's role in body fluid regulation, of specific nephron function in fishes, and of the evolutionary significance of the regions of the nephron in fishes and higher vertebrates.

2 The Kidney

Patterns of chondrichthyan reproduction and development are diverse. Species either are reproductively active throughout the year, or have a poorly defined annual cycle with one or two peaks of activity, or have a well defined annual or biennial cycle. Based on embryological origin and adult morphology, their reproductive system is more similar to tetrapods than to teleosts. Primordial germ cells are of endodermal origin. The Wolffian ducts in males and Mullerian ducts in females become the functional urogenital ducts. Differentiation is under hormonal control. Unusual features of the reproductive system include an epigonal organ in males and females. It contains lymphoid and hemopoietic tissue. Leydig's gland, a modified region of the kidney, produces seminal fluid. In some species, sperm passing through the vas deferens, is enclosed in spermatophores. Rotating about their long axis, helical spermatozoa can move forward or reverse direction. Spermatogenesis often occurs in bicellular units, spermatocysts. These consist of a spermatogonium enclosed in a Sertoh cell. Fertilization is internal. Claspers, modified portions of the pelvic fins act as intromittent organs. In many viviparous sharks and rays, the female reproductive system is asymmetrical. Eggs of some sharks are the largest known cells. Yolk platelets contain lipovitellin. Oocytes have lampbrush chromosomes. Eggs released from the ovary into the body cavity are transported by ciliary action to the ostium of the oviduct. There they are fertilized. Physiological polyspermy is normal. The shell gland, a specialized region of the anterior oviduct, functions both in long term sperm storage and in egg case production. Egg cases of sharks and skates consist of unique collagenous protein with a 400 A period, organized as a cholesteric liquid crystal. Chimaeroid egg cases contain 550 A pseudotubules in orthogonal lattices. In small sharks, males copulate by coiling around the female. A parallel position is assumed by large sharks. Skates and rays copulate with ventral surfaces apposed or by a dorsal approach. Biting is a pre-copulatory release mechanism. Parental care, except for selective oviposition, is lacking. Heavily yolked eggs undergo meroblastic, discoidal cleavage. Development is lengthy, shortest (2–4 months) in rays, longer in skates (3–8 months) and longest (9–22 months) in sharks and chimaeras. Most sharks and all rays are viviparous. Chimaeras, skates, and some sharks are oviparous. Viviparity either involves a yolk sac placenta or is aplacental. If aplacental, the embryo derives nutrients either from yolk reserves, or by intra-uterine embryonic cannibalism, or from placental analogues which secrete “uterine milk.” Phylogenetic position, geographical distribution, benthic vs. pelagic habitat, adult size, egg-embryo size, feeding ecology, and embryonic osmoregulation are factors in the retention of oviparity or the evolution of viviparity.

Reproduction and Development in Chondrichthyan Fishes

There are diverse physiological functions of nitrogen end products in different animal groups, including excretion, acid-base regulation, osmoregulation and buoyancy. Animals excrete a variety of nitrogen waste products, but ammonia, urea and uric acid predominate. A major factor in determining the mode of nitrogen excretion is the availability of water in the environment. Generally, aquatic animals excrete mostly ammonia, whereas terrestrial animals excrete either urea or uric acid. Ammonia, urea and uric acid are transported across cell membranes by different mechanisms corresponding to their different chemical properties in solution. Ammonia metabolism and excretion are linked to acid-base regulation in the kidney, but the role of urea and uric acid is less clear. Both invertebrates and vertebrates use nitrogen-containing organic compounds as intracellular osmolytes. In some marine invertebrates, NH4+ is sequestered in specific compartments to increase buoyancy.

Nitrogen excretion : three end products, many physiological roles

Publisher Summary This chapter focuses on body compartments and the distribution of electrolytes in fishes. As a physiological parameter in most vertebrates, the total body volume is somewhat meaningless when the distribution and movement of solutes are under consideration. Large portions of the total body volume are occupied by structures having very low turnover rates of metabolites and solutes. For instance, the integument and skeleton of many fishes cannot be considered to be solute pools having significant short-term exchanges of water and solutes with the surrounding tissues and fluids. For this reason, the total body water content is more usefully related to the body compartments because it is the common solute of, and is apportioned between, the major compartments and their subdivisions. The intracellular compartment of any tissue, organ, or organism is defined as the sum of the cellular volumes contained within the limits of the cell membrane. However, the cells are structurally extremely complex and contain structures such as the nucleus, the nucleoli, the mitochondria, the endoplasmic reticulum, and so on. The chapter provides an overview of intracellular compartment and extracellular compartment. It also discusses methods for the determination of body compartments, along with reviewingcompartmental spaces in fish and electrolyte composition.

1 The Body Compartments and the Distribution of Electrolytes

Elasmobranch fishes, the coelacanth, estivating lungfish, amphibians, and mammals synthesize urea by the ornithine-urea cycle; by comparison, urea synthetic activity is generally insignificant in teleostean fishes. It is reported here that isolated liver cells of two teleost toadfishes, Opsanus beta and Opsansus tau, synthesize urea by the ornithine-urea cycle at substantial rates. Because toadfish excrete ammonia, do not use urea as an osmolyte, and have substantial levels of urease in their digestive systems, urea may serve as a transient nitrogen store, forming the basis of a nitrogen conservation shuttle system between liver and gut as in ruminants and hibernators. Toadfish synthesize urea using enzymes and subcellular distributions similar to those of elasmobranchs: glutamine-dependent carbamoyl phosphate synthethase (CPS III) and mitochondrial arginase. In contrast, mammals have CPS I (ammonia-dependent) and cytosolic arginase. Data on CPS and arginases in other fishes, including lungfishes and the coelacanth, support the hypothesis that the ornithine-urea cycle, a monophyletic trait in the vertebrates, underwent two key changes before the evolution of the extant lungfishes: a switch from CPS III to CPS I and replacement of mitochondrial arginase by a cytosolic equivalent.

Evolution of urea synthesis in vertebrates: the piscine connection

Summary. 
The high urea content (2·0 and 2·5 per cent.) that characterises the blood, body fluids and tissues of the Elasmobranchii owes its origin to the relative impermeability of the gills and integument to this substance, and to the circumstance that the urea is actively conserved by the elasmobranch kidney.

In consequence of this physiological uraemia, the elasmobranch is osmotically superior to its environment, even in sea water, and is able to absorb at least a minimum quantity of water for the formation of a urine that is isotonic or hypotonic to the blood, in accordance with the osmotic limitations of the fish kidney.

We may suppose that the uraemic state tends to develop and to be regulated more or less automatically; urea is constantly being formed by the ordinary metabolic combustion of protein; water shortage leads to oliguria and urea retention, and the accumulated urea in the blood raises the osmotic pressure of the latter to a point where water is again available by direct absorption. Water plethora (as in fresh water) leads to diuresis and increased urea excretion, which in turn lowers the osmotic pressure of the blood and in some measure, at least, reduces the rate of water absorption.

Trimethylamine oxide, which imparts about one-quarter as much osmotic pressure to the blood as does urea, is also conserved by the elasmobranch; the fact that this substance is present in the urine in lower concentration than in the blood suggests that, like urea, it is actively reabsorbed from the glomerular filtrate.

This physiological uraemia is apparently an archaic biochemical habit acquired early in elasmobranch evolution, since it is shared by the divergent orders of the subclass. Presumably it is a secondary mode of osmotic regulation superimposed upon the more primitive one of branchial regulation, as observed in the teleostomes.

The cleidoic egg, unique (among the fishes) in the Elasmobranchii, and the viviparous mode of reproduction, are viewed as adaptations to urea retention, protecting the embryo against the loss of urea during its early development.

Urea retention enables the Elasmobranchii to maintain a considerably greater rate of urine formation (water excretion) than is observed in the marine teleosts, a fact that perhaps explains why the former do not show the glomerular degeneration or the aglomerular development observed in the latter.

Whereas urine formation in the marine teleosts appears to be carried on normally at a reduced level considerably below the maximum possible rate, the elasmobranchs appear to maintain a maximal (though small) degree of glomerular activity at all times. Unlike the teleosts, they appear to possess no mechanisms for reducing glomerular activity; it may be that because of their superior osmotic position, due in turn to their physiological uraemia, they have never been faced with the necessity for conserving water to an excessive degree in the kidneys, and have therefore never evolved the means for doing so.

W Homer Smith.

Papers

The retention and physiological role of urea in the elasmobranchii