Cross-tolerance in larvae of the goldenrod gall fly, Eurosta solidaginis: rapid desiccation increases organismal and cellular freeze-tolerance

Abstract

A number of similarities exist that support the idea of cross-tolerance between low temperature and desiccation stress responses. Freeze-tolerant larvae of the goldenrod gall fly, Eurosta solidaginis, are exposed to extremely dry and cold conditions when they overwinter and serve as a useful model for cross-tolerance of these two stresses. To determine if mild, rapid desiccation can improve freeze-tolerance at the organismal and cellular levels, we assessed survival, hemolymph osmolality, and glycerol concentration of control and desiccated larvae. Desiccated larvae lost 6-10% of their body mass and, to our knowledge, this is the lowest amount of water loss reported to increase freeze-tolerance. Organismal survival significantly increased with mild, rapid desiccation treatment prior to freezing for 24 h at -15°C in September (33.3 ± 6.7 to 73.3 ± 12% ) and at -20°C in October (16.7 ± 6.7 to 46.7 ± 3.3%) collected larvae. Similarly, desiccation in as little as 6 h improved in vivo survival at -20°C for 24h in fat body, Malpighian tubule, salivary gland, and tracheal cells by ~34%, ~43%, ~38%, and ~17% , respectively. Desiccation treatment induced intracellular changes because improved freeze-tolerance occurred in midgut cells frozen in vitro (38.7 ± 4.6 to 89.2 ± 5.5 %). Whereas hemolymph osmolality increased significantly with desiccation treatment (720 ± 26 vs. 544 ± 16 mOsm), glycerol concentration did not differ between control and desiccated groups. The rapidity with which the sub-lethal desiccation stress increased freeze-tolerance resembles the rapid cold hardening (RCH) response that occurs when sub-lethal cold exposure for only minutes or hours enhances freeze-tolerance, and suggests that there may be a link between rapid environmental changes and cold hardening.