Aquatic insects in a multistress environment: cross-tolerance to salinity and desiccation

Abstract

Exposing organisms to a particular stressor may enhance tolerance to a subsequent stress, when protective mechanisms against the two stressors are shared. Such cross-tolerance is a common adaptive response in dynamic multivariate environments and often indicates potential co-evolution of stress traits. Many aquatic insects in inland saline waters from Mediterranean-climate regions are sequentially challenged with salinity and desiccation stress. Thus, cross-tolerance to these physiologically similar stressors could have been positively selected in insects of these regions. We used adults of the saline water beetles Enochrus jesusarribasi (Hydrophilidae) and Nebrioporus baeticus (Dytiscidae) to test cross-tolerance responses to desiccation and salinity. In independent laboratory experiments, we evaluated the effects of (i) salinity stress on the subsequent resistance to desiccation and (ii) desiccation stress (rapid and slow dehydration) on the subsequent tolerance to salinity. Survival, water loss and haemolymph osmolality were measured. Exposure to stressful salinity improved water control under subsequent desiccation stress in both species, with a clear cross-tolerance (enhanced performance) in N. baeticus. In contrast, general negative effects on performance were found under the inverse stress sequence. The rapid and slow dehydration produced different water loss and haemolymph osmolality dynamics that were reflected in different survival patterns. Our finding of cross-tolerance to salinity and desiccation in ecologically similar species from distant lineages, together with parallel responses between salinity and thermal stress previously found in several aquatic taxa, highlights the central role of adaption to salinity and co-occurring stressors in arid inland waters, having important implications for the species' persistence under climate change.

Cuticle hydrocarbons in saline aquatic beetles

“…A high percentage of long-chain hydrocarbons has been shown to confer impermeability to the cuticle in other arthropods (e.g., Hadley, 1977; Toolson & Hadley, 1977; Lockey, 1980; Gibbs & Pomonis, 1995; Gibbs, Fukuzato & Matzkin, 2003; Gibbs & Rajpurohit, 2010). The contribution of CHCs in driving differences in stress tolerance between aquatic beetles needs to be further investigated, but the differences in cuticle permeability between the two species inferred from our results are consistent with the higher desiccation resistance (Pallarés et al, 2017), osmoregulatory ability and salinity tolerance (Pallarés et al, 2015) of E. jesusarribasi compared to N. baeticus. Specifically, the average water loss rates under desiccation conditions (40% RH) was 4.04% of fresh mass h −1 in N. baeticus and 1.58% of fresh mass h −1 in E. jesusarribasi (Pallarés et al, 2017).…”

Peer Review #2 of "Cuticle hydrocarbons in saline aquatic beetles (v0.1)"

“…Manuscript to be reviewed beetles needs to be further investigated, but the differences in cuticle permeability between the two species inferred from our results are consistent with the higher desiccation resistance (Pallarés et al, 2017), osmoregulatory ability and salinity tolerance (Pallarés et al, 2015) of E. jesusarribasi compared to N. baeticus. Specifically, the average water loss rates under desiccation conditions (40% RH) was 4.04% of fresh mass h -1 in N. baeticus and 1.58% of fresh mass h -1 in E.jesusarribasi (Pallarés et al, 2017).…”

Evolution of salinity tolerance in the diving beetle tribe Hygrotini (Coleoptera, Dytiscidae)

“…In any case, it must be noted that we have data only on the ecological preferences of the species of Hygrotini, not on their physiological tolerances. If tolerance to salinity is an exaptation derived from a plesiomorphic adaptation to terrestrial environments (as hypothesised by Arribas et al., ; see Pallarés, Botella‐Cruz, Arribas, Millán, & Velasco, for an experimental confirmation of the link between salinity and desiccation tolerance), tolerance to at least certain degree of salinity may be widespread even in species commonly found in FW habitats, as has been demonstrated to be the case in other groups of aquatic Coleoptera (Céspedes et al., ; Pallarés et al., ). Our ecological typification was also in most cases based on qualitative descriptions, without quantitative data.…”