Responses to osmotic stress

Larval Diptera inhabiting saline waters exhibit extraordinary osmoregulatory abilities. For example, soldier fly larvae Odontomyia cincta (Stratiomyidae) maintain haemolymph osmolalities of 232 and 419 mOsmol kg-1 when acclimated to external media of 3 and 5414 mOsmol kg-1, respectively (Gainey 1984). The transition from hypo-osmotic to hyper-osmotic regulation occurs at an isosmotic point of 280 mOsmol kg-1, comparable to that of other aquatic insects. Brine flies (Ephydridae) are superbly tolerant of extreme environments, such as alkaline lakes or hot springs with unusual ion composition (Barnby 1987). Evidence for the hindgut as a site of osmotic regulation in ephydrid larvae includes rectal fluid osmolalities of 8700 mOsmol kg-1 in Ephydrella marshalli maintained in external osmolalities of 6000 mOsmol kg-1 (Marshall et al. 1995). In addition, lime glands (modified Malpighian tubules) store CaCO3 in the alkali fly E. hians (Herbst and Bradley 1989). It should be emphasized that physiological tolerance under extreme conditions in the laboratory probably exceeds that in the field: the long-term effects of high salinities are costly, and early instars are certainly less tolerant to prolonged exposure (Herbst et al. 1988). Most studies have examined final instars only (owing to difficulties in obtaining haemolymph, especially from dehydrated animals in high salinities).

Mosquitoes (family Culicidae) are an ideal group in which to examine the evolution of saline tolerance: their larvae occur in a huge variety of aquatic habitats, the mechanisms involved in the osmotic physiology of saline-tolerant species have been intensively studied, and their medical importance ensures the availability of good taxonomic information (Bradley 1994). Ancestral species are thought to have had obligate freshwater larvae. Salinity tolerance has evolved at least five times independently in mosquitoes, but only two physiological strategies are involved (Bradley 1994). Some species of Aedes, Opifex, and Anopheles are osmo-regulators, and the rectal salt gland of Aedes secretes NaCl-rich hyperosmotic fluid and has been studied in detail. Other genera (Culex, Culiseta) include osmoconformers, which accumulate organic osmo-lytes in their haemolymph above the isosmotic point: this reduces the need for transporting ions and is a cheaper solution to the problem of inhabiting saline environments. Regulation of high haemolymph concentrations of trehalose and proline has been examined in detail in euryhaline Culex tarsalis, in comparison with freshwater C. quinquefasciatus (Patrick and Bradley 2000a,b). Trehalose and proline are used in energy metabolism, have a low molecular mass, and do not disrupt enzyme action when accumulated in high concentrations. Recent comparison of Na + and Cl_ uptake mechanisms in C. quinquefasciatus collected in California and from acid, ion-poor waters of the Amazon region has revealed population differences in ion uptake, and greater phenotypic plasticity in the Amazonian population (Patrick et al. 2002). Adult mosquitoes, of course, face entirely different water and salt challenges as a result of their desiccating environment and infrequent but large blood meals.

During dehydration many terrestrial insects conserve cell water at the expense of the haemo-lymph, and closely regulate the osmotic and ionic concentration of the dwindling volume of haemo-lymph. In American cockroaches (P. americana), changes in haemolymph osmolality are minimized by sequestration of solutes (especially K+ and Na+) during dehydration and their mobilization during rehydration (Tucker 1977; Hyatt and Marshall 1985). The fat body acts as an ion sink by sequestering ions as insoluble urates, and a similar mechanism may account for the uptake and release of haemolymph solutes during pronounced changes in haemolymph volume throughout a dehydration-rehydration cycle in Onymacris plana (Nicolson 1980). Tenebrionid beetle larvae can thus survive prolonged dehydration and replenish water deficits by vapour uptake without having to exchange solutes with their environments (Machin

1981). Shifts of Na+ ions are likely to be extensive in those insects where it is the dominant haemo-lymph cation: for example, in normally hydrated S. gregaria, the haemolymph accounts for 18 per cent of body mass but contains 76 per cent of total body Na+, and the tissue Na+ content doubles in the dehydrated state (Albaghdadi 1987).

The osmotic physiology of phloem feeders involves sugars rather than salts and is closely connected with their carbon nutrition. Phloem sap has high and variable sugar concentrations (up to about 0.8 M sucrose). Aphids (Homoptera, Aphididae) must feed more or less continuously to obtain sufficient nitrogen, and excess sugar and water is excreted as honeydew. Aphids solve the problem of an osmotically concentrated diet by maintaining high haemolymph sugar levels, and polymerizing dietary sugars to form oligosaccharides, such as the trisaccharide melezitose (Fisher et al. 1984; Rhodes et al. 1997). Pea aphids, A. pisum, reared on 0.75 M sucrose produce honeydew with a mean oligosaccharide length of 8.2, consisting mainly of glucose monomers because the fructose moiety of ingested sucrose is assimilated (Ashford et al. 2000). The extent of oligosaccharide synthesis is directly related to the dietary sucrose concentration, with the result that haemolymph and honeydew osmolalities remain independent of diet concentration (Fisher et al. 1984). Aphids are the best-studied phloem feeders, but whiteflies (Homoptera, Aleyrodidae) also use sugar transformations for osmoregulatory purposes. As dietary sucrose concentration increases, the main sugars in excreted honeydew change from glucose and fructose to the disaccharide trehalulose (Fig. 4.12, Salvucci et al. 1997). Development of sweet potato whiteflies Bemisia tabaci is unaffected by water stress in the host plant, as a result of physiological adjustments such as increased trehalulose in the honeydew (Isaacs et al. 1998). Aphids and whitefly, two closely related taxa of phloem feeders, have evolved different enzymatic processes for coping with high sugar concentrations (Ashford et al. 2000). Ion regulation in the aphid Myzus persicae cultured on a salt marsh plant was found to be very effective, and must involve the gut as aphids lack Malpighian tubules (Downing 1980).

Time (min)

Figure 4.12 HPLC of sugars in honeydew of whiteflies Bemisia argentifolii, showing the high proportion of trehalulose on a concentrated diet of 30% (w/v) sucrose.

Source: Reprinted from Journal of Insect Physiology, 43, Salvucci et al., 457-464, © 1997, with permission from Elsevier.

Time (min)

Figure 4.12 HPLC of sugars in honeydew of whiteflies Bemisia argentifolii, showing the high proportion of trehalulose on a concentrated diet of 30% (w/v) sucrose.

Source: Reprinted from Journal of Insect Physiology, 43, Salvucci et al., 457-464, © 1997, with permission from Elsevier.

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