Changing salinity induces alterations in hemolymph ion concentrations and Na+ and Cl– transport kinetics of the anal papillae in the larval mosquito,Aedes aegypti

Abstract

SUMMARY Mosquito larvae are found in diverse aquatic habitats ranging from freshwater to hypersaline water and must often deal with rapid changes in habitat salinity. We transferred larvae of Aedes aegypti from freshwater to 30% seawater, or vice versa, and measured the time course of changes in their hemolymph ion concentrations, using ion-selective microelectrodes. We also reported the Michaelis–Menten kinetics of Na+ and Cl– transport by the anal papillae for the first time using the scanning ion-selective electrode technique (SIET). Hemolymph concentrations of Na+, Cl– and H+ increased within 6 h, when larvae were transferred from freshwater to seawater and decreased within 6 h, when transferred from seawater to freshwater. Kinetic parameters for Na+ and Cl– transport by the anal papillae were altered after only 5 h following transfer between freshwater (FW) and 30% seawater (30%SW). The Jmax (maximum transport rate) for both ions decreased when larvae were transferred to 30%SW, whereas the Kt (a measure of transporter affinity) increased for Na+ transport but was unaltered for Cl– transport, suggesting that Na+ and Cl– uptake are independent. Data reveal significant changes in ion transport by the anal papillae of mosquito larvae when they are faced with changes in external salinity such that Na+and Cl– uptake decrease in higher salinity. The alterations in Na+ and Cl– uptake may be a consequence of changes in hemolymph ion levels when larvae encounter altered salinity. The rapid changes in ion transport described here compliment the previously observed long term alterations in the morphology and ultrastructure of the anal papillae.

Tissue specific ionomotive enzyme activity and K+ reabsorption reveal the rectum as an important ionoregulatory organ in larvalChironomous ripariusexposed to varying salinity

“…Control measurements to account for the mechanical disturbances in the ion gradients that arise from the movement of the microelectrode were taken 3-4mm away from the surface of the rectum. This sampling protocol was previously established and utilized for measuring ion gradients at the anal papillae of mosquitoes and midges (see Donini and O'Donnell, 2005;Del Duca et al, 2011;Nguyen and Donini, 2010). K + measurements were chosen in part because when altered by the presence of NKA and VA inhibitors, they can provide some insight into the movement of major ions (e.g.…”

“…Voltage gradients recorded by the ASET software were converted into concentration gradients using the following equation as described by Donini and O'Donnell (Donini and O'Donnell, 2005):…”

“…In a freshwater (FW) environment, rectal reabsorption of ions (lumen to hemolymph) results in the production of a dilute urine, permitting larvae to conserve ions while eliminating excess water. Larvae of mosquitoes and chironomids also use externally protruding anal papillae as additional sites of ion uptake in habitats such as FW (Wigglesworth, 1933;Koch, 1983;Donini and O'Donnell, 2005;Nguyen and Donini, 2010). Na + -K + -ATPase (NKA) and V-type H + ATPase (VA) are wellknown membrane energizers implicated in driving a wide variety of epithelial transport processes in insects and other animals (Emery et al, 1998;Harvey et al, 1998).…”

Effects of serotonergic agents on survival and hemolymph composition of the larval mosquitoAedes aegypti(Diptera: Culicidae, L.)in vivo: does serotonin regulate hemolymph acid–base homeostasis?

“…In many aquatic animals, uptake of Na + from dilute media is driven by H + gradients (Goss et al, 1995), and death in acidic media is ultimately caused by failure of Na + , rather than H + , homeostasis (Havas et al, 1981;Vangenechen et al, 1989). Similarly, in many animals, including larval A. aegypti, acclimation to decreased salinity is accompanied by alkalosis while acclimation to increased salinity often occurs with acidosis (Truchot, 1987;Donini et al, 2007). In this situation, disturbances of extracellular acid-base status in response to salinity changes may occur that are secondary to cellular processes such as cell volume regulation, which often involve Na -exchange (Truchot, 1987).…”

Identification of the septate junction protein gliotactin in the mosquito, Aedes aegypti: evidence for a role in increased paracellular permeability in larvae

“…The survival of mosquito larvae depends on their ability to regulate the influx and efflux of ions and water across osmoregulatory epithelia such as those of the midgut, Malpighian tubules, hindgut and anal papillae (Clements, 1992;Bradley, 1994;Donini and O'Donnell, 2005;Del Duca et al, 2011). Studies examining the role of osmoregulatory epithelia in the maintenance of salt and water balance in larval mosquitoes have generally focused on transcellular mechanisms/routes of ion movement, through which actively driven ion transport takes place (Bradley, 1995;Patrick et al, 2002;Donini et al, 2006Donini et al, , 2007Smith et al, 2008;Del Duca et al, 2011). In contrast, far less emphasis has been placed on the paracellular pathway which is regulated by the specialized cell-cell junctions known as septate junctions (SJs).…”