Comparative physiology of body fluid regulation in vertebrates with special reference to thirst regulation

Abstract

The origin of life took place in the ancient sea where the ionic concentration is thought to have been somewhat lower than that of the present day seas. This may partly explain why most vertebrate species have plasma ionic concentrations roughly one-third of seawater. Exceptions are primitive marine cyclostomes whose plasma is almost identical to seawater, and marine cartilaginous fishes that accumulate urea in plasma to increase osmolarity to a seawater level. The mechanisms for regulation of water and electrolyte balance should have evolved from these animals into those of more advanced ones in which plasma ions are regulated to one-third of seawater irrespective of the habitat. Although most extant terrestrial and aquatic animals maintain similar plasma osmolarity and ionic concentrations, the mechanisms of regulation differ greatly among different groups of animals according to their habitat. An outstanding difference is that while plasma Na(+) concentration is a primary factor of regulation in terrestrial mammals and birds, blood volume is most strictly regulated in aquatic teleost fishes. Consistently, while an increase in plasma osmolarity (cellular dehydration) is a major dipsogenic stimulus for birds and mammals, hypovolemia (extracellular dehydration) is a much stronger stimulus for elicitation of drinking in teleost fishes. Furthermore, fish cells in culture are tolerant to changes in environmental osmolarity compared with mammalian cells, further suggesting a secondary role of plasma osmolarity as a target of regulation in fishes. A secondary role of blood volume for body fluid regulation in birds is further assessed by the fact that volume receptors for thirst, salt gland secretion, and vasotocin secretion are localized in the extravascular, interstitial space in some species of birds. All terrestrial animals including mammals have derived from the fishes in phylogeny, during which the mechanisms for body fluid regulation underwent adaptive evolution in the course of transition from aquatic to terrestrial life. Therefore, much can be learned from comparative studies of body fluid regulation that reveals the diversity and uniformity of the mechanisms. In this review, important comparative studies that may contribute to an understanding of body fluid regulation throughout vertebrate species will be summarized.