Ontogeny of osmoregulation in crustaceans: The embryonic phase

Ontogeny of Osmoregulation in Crustaceans: The Embryonic Phase1

SYNOPSIS. Following a brief overview of the patterns of ontogeny of osmoregulation in postembryonic stages, this review concentrates on the ontogeny of osmoregulation during the embryonic development of crustaceans, particularly in those species living under variable or extreme salinity conditions and whose hatchlings osmoregulate at hatch. Two situations are considered, internal development of the embryos in closed incubating, brood or marsupial pouches, and external development in eggs exposed to the external medium. In both cases, embryos are osmoprotected from the external salinity level and variation, either by the female pouches or by the egg envelopes. The mechanisms of osmoprotection are discussed. During embryonic life, temporary or definitive osmoregulatory organs develop, with ion transporting cells and enzymes such as Na+-K+ ATPase, permitting the embryos and then the hatchlings to osmoregulate and tolerate the external salinity.

INTRODUCTION

Salinity is one of the main environmental factors that wield a selective pressure on aquatic organisms. Its level and variations have an impact on the composition and osmolality of the body fluids of animals, among which some groups or species possess physiological abilities of osmoregulation. Species that are able to efficiently osmoregulate are generally euryhaline. Osmoregulation may thus be viewed as an adaptive function enabling animals to occupy habitats with high, low and/or variable salinity, where a wide salinity tolerance is required for survival. Crustaceans display several patterns of osmoregulation, extensively studied in adult stages (reviews in Mantel and Farmer, 1983; Pequeux, 1995). Since natural selection acts on all stages of development (Bartholomew, 1987; Burggren, 1992), a complete overview of the adaptive strategy of a given species must be based on studies conducted on each stage of the life cycle, from adults to reproductive cells, embryos and larvae, postlarvae or juveniles (Charmantier and Wolcott, 2001).

The ontogeny of osmoregulation has been studied in several species of crustaceans since the early work of Kalber and Costlow (1966). A previous review on the subject (Charmantier, 1998) showed that ontogenetic studies of osmoregulation have been conducted mainly in larvae and post-- larvae, i.e., in postembryonic stages. The present overview will focus on the ontogeny of osmoregulation during the embryonic phase with a brief summary regarding the postembryonic stages.

Three patterns of ontogeny of osmoregulation have been established from the data available in several species (Charmantier, 1998; Fig. 1). In one group of species (pattern 1), osmoregulation varies little with developmental stage; the adults of these species, mostly marine and stenohaline, are weak regulators or osmoconformers. In another group (pattern 2), the adult type of osmoregulation is established as early as the first post-embryonic stage; adults are euryhaline and generally live in environments where salinity is high, low, or variable; this group thus includes freshwater species. In the third group of species (pattern 3), larvae osmoconform or are slightly able to osmoregulate; metamorphosis marks the appearance of the adult type of osmoregulation; adults are mesohaline or euryhaline and live in environments of more or less variable salinity.

The physiological basis of these patterns and their ecological consequences have also been reviewed (Charmantier, 1998). As in adults, the occurrence of osmoregulation in young postembryonic stages is based on efficient ionic regulation (mainly of Na+ and Cl-) and on increased levels and/or presence of enzymes involved in ion transport (mainly Na+-K+ ATPase, and other enzymes such as carbonic anhydrase). Osmoregulatory epithelia may appear at different times of development and at different locations, usually in organs of the branchial chamber. These events appear integrated during development, at least in those species in which sufficient data have been collected. Anatomical changes (development of osmoregulatory epithelia) lead to physiological modifications (increased Na+-K+ ATPase activity and/or presence, linked to an increase in osmoregulatory capacity) that permit an augmented salinity tolerance allowing ecological adaptation to environments of variable and/or extreme salinity.

In species or stages incapable of extracellular osmoregulation, i.e., in osmoconforming organisms, a limited degree of tolerance to salinity variation may originate from cell volume regulation through intracellular isosmotic regulation. This process has been extensively studied in adult crustaceans (reviews in Gilles and Pequeux, 1983; Kirschner, 1991). From the limited information available in early post-embryonic stages, intracellular free amino acids play, as in adults, a major function in the maintenance of the osmotic equilibrium between the cells and hemolymph (Haond et al., 1999).