Under global change, the ion concentration of aquatic ecosystems is changing worldwide. Many freshwater ecosystems are being salinized by anthropogenic salt inputs, whereas many naturally saline ones are being diluted by agricultural drainages. This occurs concomitantly with changes in other stressors, which can result in additive, antagonistic or synergistic effects on organisms. We reviewed experimental studies that manipulated salinity and other abiotic stressors, on inland and transitional aquatic habitats, to (i) synthesize their main effects on organisms' performance, (ii) quantify the frequency of joint effect types across studies and (iii) determine the overall individual and joint effects and their variation among salinity–stressor pairs and organism groups using meta-analyses. Additive effects were slightly more frequent (54%) than non-additive ones (46%) across all the studies ( n = 105 responses). However, antagonistic effects were dominant for the stressor pair salinity and toxicants (44%, n = 43), transitional habitats (48%, n = 31) and vertebrates (71%, n = 21). Meta-analyses showed detrimental additive joint effects of salinity and other stressors on organism performance and a greater individual impact of salinity than the other stressors. These results were consistent across stressor pairs and organism types. These findings suggest that strategies to mitigate multiple stressor impacts on aquatic ecosystems should prioritize restoring natural salinity concentrations. This article is part of the theme issue ‘Salt in freshwaters: causes, ecological consequences and future prospects’.
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.
Physiological traits are key in determining the vulnerability of narrow range, highly specialized animals to climate change. It is generally predicted that species from more stable environments possess lower thermal tolerance breadths and thermal plasticity than those from more variable habitats – the so‐called ‘climatic variability hypothesis’. However, evolutionary trade‐offs between thermal breadth and its plasticity are also seen in some taxa, and the evolution of thermal physiology remains poorly understood. Subterranean environments are excellent systems for exploring these issues, being characterized by stable climatic conditions, with environmental variability increasing predictably from deep to shallow habitats. Acclimation capacity will be fundamental in determining the sensitivity of subterranean species to climate change, since they have poor dispersal capacity and limited possibility to exploit thermally different microhabitats in the uniform cave environment. We assessed critical thermal maximum (CTmax) and short‐term heat acclimation capacity in three related beetles (Leiodidae: Leptodirini) with differing degrees of specialization to the subterranean environment (deep, shallow and facultatively subterranean, respectively) and therefore exposed to contrasting thermal variability in nature. Only the facultative subterranean species showed any acclimatory capacity, also having the highest CTmax across the taxa studied. However, this species might experience the highest thermal stress in its habitat under climate change. The studied subterranean specialists will be poorly able to cope physiologically with temperature increase, but in contrast exposed to lower magnitude and rate of warming. Our results fit the climatic variability hypothesis, suggesting that adaptation to cave conditions has selected against the retention of acclimation mechanisms. We show that the pathways that determine vulnerability of subterranean species to climate change depend on their degree of specialization to deep subterranean environments. This information, combined with evaluation of exposure to climatic changes at their present locations, is fundamental in identifying species or populations at greatest risk.
1. Accurate assessments of species' vulnerability to climate change require integrated measurements of its different drivers, including extrinsic (the magnitude and rate of climate change) and intrinsic factors (organisms' sensitivity and adaptive capacity). According to these factors, aquatic insects restricted to alpine ponds may be especially threatened by climate change. However, vulnerability predictions based on such an integrative approach are scarce for alpine pond taxa.2. We combined distributional, climatic data and experimental measurements of heat tolerance and acclimation capacity of two water beetles endemic to Sierra Nevada National Park (Spain) to evaluate different components of their vulnerability to climate change. We estimated: (i) changes in climatically suitable habitat under different scenarios of climate change and (ii) thermal safety margins (the difference between species upper thermal limits and the maximum temperatures in their current localities), for current and future conditions, and acclimation capacity, as measures of the physiological capacity to persist in situ.3. Species distribution models predicted a virtual loss of climatically suitable area under different climate change scenarios. Nonetheless, both taxa showed heat tolerance limits above the predicted maximum temperatures in their current localities (but no capacity to adjust such limits through acclimation). Therefore, these beetles could have the physiological capacity to deal with warming conditions in situ.4. We recommend concentrating conservation efforts in current localities as the most efficient management strategy for both taxa. Our results stress the importance of accounting for physiological tolerances when predicting the vulnerability to climate change in alpine freshwater biota.
In the context of global change, it is important to know the physiological limits and behavioural responses of species to environmental changes, especially for those living in extreme environments such as supratidal rockpools. Our main study objective was to determine the thermal tolerance of 3 beetle species (Ochthebius quadricollis, O. subinteger and O. lejolisii) co-occurring on the western Mediterranean coast using physiological and behavioural thermoregulatory responses to predict their sensitivity to climate change. To this end, we: (1) compared the heat coma (HC) among species and populations; (2) explored the effect of salinity on HC in adults and larvae of O. quadricollis and O. lejolisii; and (3) determined the temperature thresholds for avoidance responses (water emersion and flight) of adult stages against heat and salinity stressors. We found significant interspecific and interpopulation differences in HC. O. quadricollis larvae and adults were the most heat tolerant, showing similar HC values under different salinity conditions. In O. lejolisii, high salinity (90 g l-1) conferred greater thermal tolerance in larvae but lower tolerance in adults. The temperature thresholds for avoidance responses were generally lower than 40°C, but interspecific variation followed their obtained HC patterns. In both of these species, salinity affected the sublethal temperature thresholds for water emersion. An additive effect of temperature and salinity was observed for the frequency of emergence and flight in both species. Our results provide relevant information for estimating thermal safety margins and developing mechanistic predictive models for the survival of these species when faced with current and future climate change scenarios.
In the context of aridification in Mediterranean regions, desiccation resistance and physiological plasticity will be key traits for the persistence of aquatic insects exposed to increasing desiccation stress. Control of cuticular transpiration through changes in the quantity and composition of epicuticular hydrocarbons (CHCs) is one of the main mechanisms of desiccation resistance in insects, but it remains largely unexplored in aquatic ones. We studied acclimation responses to desiccation in adults of two endemic water beetles from distant lineages living in Mediterranean intermittent saline streams: Enochrus jesusarribasi (Hydrophilidae) and Nebrioporus baeticus (Dytiscidae). Cuticular water loss and CHC composition were measured in specimens exposed to a prior non-lethal desiccation stress, allowed to recover and exposed to a subsequent desiccation treatment. E. jesusarribasi showed a beneficial acclimation response to desiccation: pre-desiccated individuals reduced cuticular water loss rate in a subsequent exposure by increasing the relative abundance of cuticular methyl-branched compounds, longer chain alkanes and branched alkanes. In contrast, N. baeticus lacked acclimation capacity for controlling water loss and therefore may have a lower physiological capacity to cope with increasing aridity. These results are relevant to understanding biochemical adaptations to drought stress in inland waters in an evolutionary and ecological context.
Hydrocarbons are the principal component of insect cuticle and play an important role in maintaining water balance. Cuticular impermeability could be an adaptative response to salinity and desiccation in aquatic insects; however, cuticular hydrocarbons have been poorly explored in this group and there are no previous data on saline species. We characterized cuticular hydrocarbons of adults and larvae of two saline aquatic beetles, namely Nebrioporus baeticus (Dytiscidae) and Enochrus jesusarribasi (Hydrophilidae), using a gas chromatograph coupled to a mass spectrometer. The CHC profile of adults of both species, characterized by a high abundance of branched alkanes and low of unsaturated alkenes, seems to be more similar to that of some terrestrial beetles (e.g., desert Tenebrionidae) compared with other aquatic Coleoptera (freshwater Dytiscidae). Adults of E. jesusarribasi had longer chain compounds than N. baeticus, in agreement with their higher resistance to salinity and desiccation. The more permeable cuticle of larvae was characterized by a lower diversity in compounds, shorter carbon chain length and a higher proportion of unsaturated hydrocarbons compared with that of the adults. These results suggest that osmotic stress on aquatic insects could exert a selection pressure on CHC profile similar to aridity in terrestrial species.
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