Salt and water balance in terrestrial isopods ("pillbugs").

NOTE: the following is taken from the "Abstract", "Introduction" and "Discussion" sections of "Na, K-ATPase activity in the pleopopds and hindgut-rectum of terrestrial isopods: implications for colligative water vapor absorption", J.C. Wright, C.W. Holliday and M.J. O'Donnell, 1994, Journal of Crustacean Biology 14: 522-529, to which interested readers are referred for references to the papers cited.

ABSTRACT

Na/K-ATPase enzyme-specific activity (ESA) was compared in 7 terrestrial oniscidean isopods, and in single species of fresh-water Isopoda (Asellus forbesi)and Amphipoda (Gammarus fasciatus).Assays were performed on 4 tissues in the Isopoda: pleopodal endopodites 3-5, pleopodal exopodites 3-5, hindgut-rectum, and left pereiopods 6-7. For Gammarus,ESA's were measured for the pereiopodal coxal gills (epipodites), but not for the pleopods. In terrestrial isopods, the highest Na/K-ATPase ESA's were associated with the pleopodal endopodites (4.80-12.80 micromol Pi per mg protein per hr), tissues also revealing high Cl- permeability with silver staining. ESA's for the hindgut-rectum were rather lower (3.94-9.40 micromol Pi per mg protein per hr), but significantly elevated compared to pereiopods (0.78-1.32 micromol Pi per mg protein per hr) and pleopodal exopodites (1.03-3.44 micromol Pi per mg protein per hr). The results concur with proposed models for endopodal secretion and hindgut resorption of NaCl during colligative water vapor absorption. Furthermore, species with lower threshold humidities for vapor absorption, and capable of secreting higher NaCl concentrations, reveal the highest endopodite and hindgut ESA's. Elevated ESA's in these tissues may also relate to ion transport during reprocessing of maxillary urine, since comparable values were found in Helleria brevicornis,an oniscidean incapable of water vapor absorption. No significant short-term increases in endopodite or hindgut ESA's were observed in animals maintained in conditions necessitating frequent vapor absorption for water balance (93.5% RH) compared to controls (100% RH), or in animals sacrificed during vapor absorption. Hindgut ESA's were markedly lower in fresh-water compared to terrestrial species (2.14 and 1.40 micromol Pi per mg protein per hr for Asellusand Gammarus,respectively), suggesting a minor role of this tissue in ion uptake. Pleopods of Asellusalso revealed lower ESA's than in terrestrial species (2.45 micromol Pi per mg protein per hr), while the pereiopodal gills of possessed similarly high ESA's. Findings suggest that Asellusdepends primarily on low integumental ion permeability for hyperregulation, while Gammarusexploits more efficient ion uptake across pereiopodal gills.

INTRODUCTION

Ion uptake or excretion by the gills of crustaceans is generally believed to be driven primarily by the Na, K-ATPase (Towle, 1981, 1984). The enzyme has been implicated in both hyperosmotic and hyposmotic regulation by aquatic species. In the euryhaline crab Callinectes sapidus, for example, Na, K-ATPase enzyme-specific activity (ESA) is high in the regions of the gill specialized for ion transport, and the activity in these regions increases when crabs acclimate to dilute media (Neufeld et al., 1980). In the marine isopod Idotea wosnesenski, the endopodites of the posterior three pleopods are the probable sites of inward ion transport in dilute media. Na, K-ATPase ESA in these appendages increases two-fold in animals acclimated in dilute media (Holliday, 1988). Salinity-induced changes in branchial Na, K-ATPase activity in the brine shrimp Artemia salina suggest that this enzyme is also involved in hyporegulation (Holliday et al., 1990). Current models of salt secretion and uptake by crustacean gills both involve a primary role of the Na, K-ATPase and are discussed by Towle (1990).

Evidence for salt transport by terrestrial isopods (Isopoda, Oniscidea) has been provided by Wright and O'Donnell (1992). Strongly hyperosmotic fluid is found in the pleoventral chamber during the process of water vapor absorption. Water vapor absorption has been widely documented for acarines and insects (O'Donnell and Machin, 1988), but the oniscidean isopods are apparently the only crustaceans which supplement their water intake by this means. The hyperosmotic pleon fluid results in colligative lowering of vapor pressure, leading to condensation of atmospheric water when ambient vapor pressure exceeds that ofthe pleon fluid. The vapor pressure lowering of the pleon fluid determines the minimum relative humidity (RH) at which absorption is possible. This minimum is defined as the absorption threshold, and has been determined for a number of species (Wright and Machin, 1993a).

Following exposure to the air, pleon fluid and condensed water must be conveyed to the hemolymph. Preliminary experiments suggest that fluid may move from the pleon into the rectum and hindgut, contrary to earlier speculation (Wright and Machin, 1990). This suggests that salts and absorbed water are transferred into the hemolymph across these epithelia. Like the endopods, the rectum and hindgut of oniscideans possess mitochondria-rich epithelia (Smith, 1969; Palackal et al., 1984) and seem plausable tissues for Na+ and Cl- resorption, as well as cotransport of water. This may or may not involve a primary role of the Na, K-ATPase.

In the present study, we compare ESAs for Na, K-ATPase in the pleopodal endopodites and hindgut-rectum from a selection of Oniscidea. ESAs in these tissues are compared, for reference, with those for the pleopodal exopodites, which do not show the ultrastructural characteristics of ion-transporting tissues, and the sixth and seventh periopods in which the predominant tissue is muscle.

DISCUSSION

We suggest that the high ESAs in both endopodites and hindguts of vapor-absorbing species may be related to the process of water vapor absorption. It seems likely that the endopodites are involved in secretion of hyperosmotic NaCl during water vapor absorption, and that pleon fluid and condensed water are then conveyed into the hindgut, where the ions and osmotically obliged water are reabsorbed into the hemolymph. Reabsorption would thus permit a recycling of ions, primarily Na+ and Cl-, and a continuous process of water vapor absorption. This suggestion is supported by the finding that ESAs of both endopodites and hindguts show highly significant correlations with absorption thresholds. Although not quite significant, the positive covariance between endopod and hindgut ESAs adds further support to the hypothesis. Species with lower [absorption] thresholds must produce more concentrated NaCl solutions on the pleon and would therefore require a corresponding increase in their ability for active salt secretion across the endopodites, and salt reabsorption from the hindgut. The strongly hyperosmotic fluids secreted by ligiamorph oniscideans during water vapor absorption may have constituted a preadaptation for the colonization of hypersaline lakes by the Australian oniscid Haloniscus searlei,a species capable of extreme hyporegulation (Bayly and Ellis, 1969).