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How Does Change In Ocean Salinity Affect Marine Life

1. Introduction

In the face of global change, agreement and predicting the effects of multiple stressors is one of the most pressing challenges in conservation and applied environmental [1,2]. In particular, aquatic organisms are exposed to a growing number of stressors [3,4], such as freshwater salinization [5–7], water acidification [8,9] or eutrophication [ten,11]. Given the heterogeneous nature and unlike mechanisms of deportment of these stressors (e.g. physical versus chemical stressors), the co-occurrence of several of them tin result in condiment, synergistic or combative effects on organism traits (east.g. survival, fecundity, metabolic and growth rates, etc.). Additive effects occur when articulation stressor furnishings (i.e. cumulative furnishings sensu Crain et al. [12]) equal the sum of individual furnishings. Non-condiment effects are reflected by a deviation from the additive response, which can be greater (synergism) or less (animosity) than the sum of private effects [13] and thus exacerbate or mitigate, respectively, the furnishings on organism performance [14]. These changes at organism level are the principal and most sensitive responses to stress [fifteen] but may ultimately alter community composition [xvi] and interfere with ecosystem processes and services, which sustain homo welfare [17]. In recent years, several meta-analyses accept synthesized the results of studies that have tested joint effects of multiple stressors in marine [12,eighteen,19] and freshwater ecosystems [20] at different organizational levels, from organisms to communities, and have shown contrasting results. While an overall synergistic outcome of multiple stressors has been institute on marine systems, antagonistic joint effects dominate in freshwaters. However, none has specifically provided a comprehensive review of organism responses of inland aquatic species or populations to the combined furnishings of salinity changes with other global modify stressors.

Human activities, like agriculture or salt mining, forth with climatic aridification and rising bounding main levels, are increasing salt concentrations in inland freshwaters and coastal habitats [21], which produces severe negative economic and biological effects [half dozen,22–24]. Contrarily, freshwater inputs, mainly caused by irrigated agronomics in arid landscapes, are diluting naturally saline rivers, estuaries and salt-marshes, with harmful furnishings [25]. At levels above or beneath the isosmotic point of organism internal fluids, salinity tin disrupt metabolism and water balance [26]. Therefore, aquatic organisms take evolved different intra- and extracellular osmoregulation mechanisms to control osmotic and dehydration stress in the face of salinity changes in the external environment [27,28] (box 1). However, organism osmoregulation capacities might exist insufficient to bargain with anthropogenic salinization and dilution and, most importantly, it is unknown whether the derived negative furnishings of these salinity changes can be amplified or mitigated in the presence of boosted stressors.

Box 1. Osmoregulation mechanims to bargain with salinity stress based on Bradley [27] and Rivera-Ingraham & Lignot [28].

Inline Graphic

The outcomes of multiple stressor interactions are context-dependent (type of ecosystem, trophic level, response level, response metrics, specific stressor pair, stress intensity and elapsing, etc.) [22,23,26]. At the physiological level, the joint issue of multiple environmental stressors ultimately depends on organism sensitivity to each stressor [2] and the overlap in the underlying mechanisms and molecular pathways used to combat their effects. Exposure to one stressor tin can raise resistance to another if the same protective mechanism can cope with both stressors (cantankerous-tolerance [29–31]) (box 2). Alternatively, dissimilar stressors may activate distinct mechanisms but dependent signalling regulatory pathways (cross-talk, e.grand. [32]). In these cases, the resulting interaction effect depends on the energetic cost of the upregulated mechanisms. If such cost is low, antagonistic interactions would be expected. If there are energetic trade-offs betwixt protective mechanisms, exposure to i stressor can compromise the response to the other and the full general result could be a synergistic negative effect. Finally, when independent mechanisms and pathways are activated, one stressor would accept no effect on the response to the other, and an additive consequence should be the nearly probable consequence. Some cross-tolerance and cantankerous-talk responses involving salinity have been reported (e.g. [32–34]). Thus, this cross-tolerance/cross-talk framework, originally proposed for cold, desiccation and immune responses in overwintering insects [29], may be useful to yield wide-calibration predictions of interactions amid salinity and other stressors, which would crave different direction actions [i] (box 2).

Box 2. Cross-tolerance/cantankerous-talk framework to predict joint effects of stressor pairs depending on the overlap betwixt protection mechanisms (based on Sinclair et al. [29]) and recommendations for management.

Inline Graphic

Hither, we review experimental studies that have explored the combined effects of changes in salinity and other key abiotic stressors associated with global change (e.g. temperature, pH, pollutants, etc.) at organism level on several physiological traits that determine the functioning of aquatic organisms beyond inland (freshwater and saline) and transitional coastal ecosystems (estuaries and salt-marshes). Our aims were to (i) synthesize the main effects of salinity and other stressors at organism level and place gaps in the salinity-multistressor literature, (2) quantify the frequency of additive, synergistic and antagonistic joint effects and (iii) determine the overall private and joint effects and their variation among salinity–stressor pairs and organism groups.

2. Methods

(a) Bibliographic search and screening

Nosotros focused on experimental studies that have assessed the effects of salinity and other stressors on organisms (autotrophs, invertebrates and vertebrates) of inland fresh and saline waters, along with estuarine and table salt-marsh habitats (transitional habitats). We simply considered experimental studies because they permit isolation of the effects of specific stressors from other misreckoning factors that cannot be controlled in the field. We searched the literature using Spider web of Scientific discipline (final accessed in June 2018) with the following sequence of field tags and Boolean operators in advanced searches: ((((TS= ((salin* OR *osmotic* OR conductivity) AND (temperature OR rut OR thermal OR hypoxia OR nutrient* OR radiations OR humidity OR drought OR dehydration OR desiccation OR *ionic* OR pollut* OR insecticide OR pesticide OR acerbity OR 'pH' OR metals) AND (freshwater OR aquatic NOT marine) AND (physiolog*)))))). We refined the search by stress* and no brake was placed on publication year. From the resulting papers, we selected only those that had practical a full-factorial blueprint, including a clearly defined control treatment (or a treatment deemed by the authors to exist nether non-stressful atmospheric condition for any of the stressors), treatments with ane level or more than of each single stressor and combined treatments of all the stressors. We as well included studies from the cited literature of the selected papers that met these criteria just did not appear in the literature search. From this offset filter by experimental design, nosotros obtained 2 datasets.

Dataset 1 (electronic supplementary cloth S1) contained only those studies that statistically tested the interaction effect. These studies were used for an initial exploration of the individual and joint stressor effects reported and to identify knowledge gaps in the salinity-multistressor literature. We retrieved information for each experiment in each study to narrate stressor pairs salinity (stressor A), plus temperature, nutrients, metals, pesticides, COii, hypoxia, sulfate or pH (stressor B), organism (autotroph, invertebrate or vertebrate), habitat (inland freshwater, inland saline or transitional) and response type (survival and tolerance limits; fitness measurements, including metabolic rates, growth and reproduction traits; molecular responses; physiological regulation, including osmotic capacity and metal uptake or aggregating measurements; and behaviour). Nosotros adamant: (i) the significance of individual and joint furnishings past exploring the results of the statistical analyses performed in each study; (ii) the direction of such furnishings in private performance terms compared with the command conditions (i.east. negative (worse performance) or positive (enhanced performance)) by looking at the post hoc tests and/or plots with errors. In multilevel experiments (i.e. those with more than 2 levels of each stressor), we focused on the highest level before the full bloodshed of individuals because the magnitude and direction of the joint effects could vary beyond the different levels of each stressor.

Dataset ii (electronic supplementary fabric S2) was obtained by selecting exclusively those studies that report either raw data or mean, standard divergence and sample sizes for command, single and combined-stressor treatments. These data were used to quantify the frequency of joint effect types and for meta-analyses (meet below). In this dataset, we simplified stressor B categories into temperature, desiccation, nutrients and toxicants (including metals, pesticides, pH and sulfates). We considered sulfates as a dissever stressor from salinity because it could potentiate the negative osmotic effects of increasing salinity [35,36].

(b) Joint effect types and meta-analyses

From dataset 2 (electronic supplementary textile S2), we calculated the private, chief and joint effect sizes for each experiment and study using Hedge's d according to factorial meta-analysis methods, where a significant interaction effect signifies deviation from the null model of additivity [37] (see meta-analysis details in electronic supplementary material S3). Individual effects reverberate the response to i stressor alone in relation to the control. Main effects stand for the private stressor effect plus its contribution to the interaction effect, calculated in the presence and absence of the other stressor. To ensure a positive relationship of the response variables with performance, we inverted the sign of principal and private issue sizes from experiments that measured response variables negatively related with performance (eastward.g. mortality response was transformed into survival response by changing the effect size sign). To brand a quantitative assessment of interaction blazon frequencies, interaction effects were classified using effect sizes according to Crain et al. [12], i.e. additive interactions were those whose 95% confidence interval (CI) include zero value. Synergistic interactions were those in which both private effect sizes were negative, or 1 was negative and the other positive, and the interaction effect size was significantly lower than zero. Animosity occurred when the interaction effect size was bigger than cypher and at least one private upshot size was negative. Because studies with two positive individual effects had interaction terms opposite from the majority of studies with negative individual effects, the interaction effect sizes for these studies were inverted [12].

We used a random-effects model meta-assay to decide the weighted mean effect sizes of the main and joint effects of stressors for the studies included in dataset two (electronic supplementary material S2) using the metafor R package [38]. Different meta-analyses were performed with the data subsets that allowed consequent analyses by considering a relatively balanced distribution of studies and outcome sizes across moderator categories or groups (organism blazon, habitat). The selected chiselled moderators were treated as fixed effects to appraise the mean interaction effects at each level of all the categories (where northward ≥ x) (run across electronic supplementary fabric S4 for more details). Firstly, we conducted an overall meta-analysis across all the studies that tested salinity increase effects (n = 85) and other stressors using organism type as the moderator (autotroph, n = 21; invertebrate, north = 43; vertebrate, n = 21). We as well conducted meta-regressions to analyse how overall effect sizes varied with (i) publication yr (n = 85), (ii) the magnitude of salinity change (handling − control) (north = 83) and (iii) the magnitude of temperature alter (n = 38). A 2nd meta-analysis was done for autotrophs (n = 21) using habitat as the moderator (inland freshwater, n = x, versus transitional, north = 11). Finally, for inland saline water invertebrates, three subgroup meta-analyses were run for the post-obit stressor pairs: salinity increase × temperature increase (n = 29), salinity decrease × temperature increase (n = xvi) and salinity increase×toxicant increase (northward = nine). We assessed publication bias in all the meta-analyses by using funnel plots and Rosenthal's fail-rubber number [39].

The codes of the functions used to run all these analyses, which were performed with R v. 3.3.two [forty], are available in electronic supplementary material S5.

3. Results and discussion

Of 2157 screened articles, merely 64 studies met our experimental design criteria. Of these, 45 papers tested interaction effects and were reviewed, including a total of 208 study cases from 46 distinct species (dataset 1, electronic supplementary material S1). We obtained quantitative data from 24 papers to determine the frequency of interaction types and conduct the meta-analyses, in which the master effect sizes of stressors and their interaction were estimated for 105 study cases of 28 species (dataset 2, electronic supplementary material S2).

(a) Research contributions and gaps in the salinity-multistressor literature

Although many experimental studies have tested the effects of salinity and other stressors in combination, but a small proportion of them accept employed full-factorial experimental designs and appropriate analytical approaches to identify non-condiment joint furnishings. In dataset 1 (electronic supplementary fabric S1), the statistical analyses most ofttimes used to test interaction effects were ANOVA-type models, which assume a simple addition model every bit the null model [two]. Most studies tested more two levels of each stressor, only simply two of the 45 reviewed studies [41,42] used five or more handling levels, essential to plant a reliable stressor–effect relationship from a factorial experiment [2].

Multiple stressor studies are conspicuously biased toward sure stressor pairs, habitats and organisms. The most oftentimes studied stressors in combination with salinity were temperature (34% of study cases) and metals (24%). However, other relevant stressors have received less attention (e.one thousand. nutrients and desiccation stress). The almost represented habitats were transitional ones (55%), followed by inland saline (26%) and freshwater ecosystems (xviii%). The number of observations made on vertebrate and invertebrate organisms was similar (36 and 34%, respectively), while autotrophs were less represented (30%). Molecular responses (e.g. activity or gene expression of ion transporter and antioxidant enzymes), and survival and tolerance limits, as well every bit fitness measurements (e.g. growth, reproduction and metabolic rates), were the well-nigh frequently studied traits (see electronic supplementary material S1).

The individual event of salinity decreased organism performance in most of the observations (43%, eastward.g. decreased survival and growth, increased osmolyte concentration in body fluids, inverse metabolic rates, etc.) and was positive in only 20% of the responses, most oftentimes increasing survival or tolerance to heat or cold stress. Similarly, the individual effects of the other stressors (named stressor B, see the Methods section) resulted in worse performance in about cases, but enhanced information technology in 30% of the cases. Approximately 50% of the studies reported pregnant non-additive effects of combined stressors, amongst which almost decreased organism performance, mainly survival.

(b) Frequency of additive, antagonistic and synergistic furnishings

The classification of joint effect types based on effect size estimates (encounter electronic supplementary material S2) yielded a higher frequency of additive (54%) than antagonistic (thirty%) and synergistic effects (sixteen%). These patterns varied beyond stressor pairs, habitat or organism categories. Condiment effects were more than frequent in the stressor pair salinity × temperature, inland saline habitats and invertebrates. Still, antagonistic effects dominated for the combination of salinity with toxicants, and in both transitional habitats and vertebrates (effigy 1).

Figure 1.

Effigy 1. Frequency distribution of the interaction types beyond (a) stressor pairs, (b) habitat and (c) organism groups, estimated from consequence size calculations and categorized post-obit the classification of Crain et al. [12] (meet electronic supplementary cloth S2). (Online version in colour.)

These results can be discussed inside the cross-tolerance/cantankerous-talk framework earlier described (box 2). In the case of loftier temperature and salinity, dissimilar physiological mechanisms are activated (i.e. estrus shock and osmoregulatory responses, respectively), so they are more likely to collaborate in an additive manner, as nosotros generally observed. For example, Garreta-Lara et al. [43] found a strong influence of salinity on the metabolomic profile of the invertebrate Daphnia magna, merely no significant interaction with temperature. Though less frequent, some synergistic and antagonistic responses betwixt salinity and temperature were also establish (e.m. [44] in dataset 2, electronic supplementary textile S2; see besides [45] in this upshot), which suggests that the mechanistic human relationship between heat and osmotic stress is still non well understood.

Unlike high temperature, common homeostatic and excretory mechanisms are primarily used confronting the stress induced past salinity and metals, although each particular metal elicits other specific responses once it has accumulated in the organism [46]. Partially shared mechanisms and common regulatory pathways could explain the higher frequency of antagonisms found in the salinity and toxicant stressor pair (most corresponded to osmoconformer estuarine, anadromous and catadromous fish), a blueprint that has also been observed in marine ecosystems [12]. For example, De Polo et al. [47] identified enzyme carbonic anhydrase (CA2) as the mechanistic link at the molecular level involved in the antagonistic effects of copper and osmotic stress on ion homeostasis in the estuarine fish Cyprinodon variegatus. In estuarine and marine invertebrates, increased salinity generally protects confronting the negative furnishings of metals [48], which tin can be partly explained by competitive interactions with major cations for sensitive ion transport sites [49]. These competitive interactions diminish under depression salinity weather condition because of lower concentrations of free ions, which facilitates metal uptake [50]. In freshwaters, poor osmoregulator species, for which these cantankerous-protective furnishings of salinity likely play a smaller role, may be much more vulnerable to water pollution by metals than are saline species.

Combative interactions betwixt salinity and pesticides are as well typical. In this case, neuroendocrine responses may exist involved as cholinesterase inhibition is the main manner of pesticide action [51]. For instance, hypersaline acclimation reduces mortality in subsequent exposure to chlorpyrifos in the euryhaline anadromous fish Salmo trutta, and it has been suggested that this protective event could be associated with reduced neuronal signalling under hypersaline conditions [52].

A poorly explored stressor pair with shared protective physiological mechanisms is desiccation and salinity. Both stressors disrupt water and ionic residuum and thus cantankerous-tolerance might be expected (box 2). Indeed, antagonistic responses to these stressors are common in plants [53] and have been constitute in some aquatic insects [34,54], in which the pre-activation of osmoregulatory mechanisms during salinity exposure seems to contribute to minimize water loss during a subsequent desiccation exposure.

Interestingly, in well-nigh antagonistic interaction cases, the individual effects of stressors were both negative, which means that although the negative affect is mitigated in the presence of both stressors, they still produce a reduction in organism performance (e.g. the upper thermal limit of saline h2o beetles decreases later on acclimation at stressful salinities and temperatures, but less than under each stress alone [55]). Opposing individual effects leading to antagonistic interactions typically occur with nutrients, whose positive effects can overcompensate for the negative effect of salinity (e.g. [56]), every bit happens with toxicants [12]. We also found, amidst the few cases of synergistic interactions, opposing individual furnishings (electronic supplementary textile S2), more often than not between salinity and toxicants. For example, in cyanobacteria, the activity of the antioxidant enzyme peroxidase increased in the presence of Cu or Cu + NaCl, simply not of NaCl alone [57].

(c) Overall private and joint stressor furnishings: meta-analyses

The meta-assay conducted on all the salinity increase studies and organism groups revealed an overall condiment articulation effect (d = 0.527 ± 0.379, p = 0.164, n = 85; figure 2a; electronic supplementary fabric S4). When this dataset was chastened by organisms, joint effects were too additive for autotrophs (d = 0.464 ± 0.793, p = 0.559, n = 21), invertebrates (d = 0.005 ± 0.952, p = 0.630, n = 43) and vertebrates (d = 1.777 ± 1.117, p = 0.240, north = 21). The individual mean effect sizes of salinity increase (d = −two.223 ± 0.779, p = 0.004, n = 83) and stressor B (d = −0.907 ± 0.378, p = 0.017, north = 83) were significantly negative (figure iib,c). Remarkably, the mean effect size of salinity increase was more than two times higher than the effect size of stressor B. In addition, overall salinity effect size became more than negative with fourth dimension of study publication (d = −0.326 ± 0.152, p = 0.032, due north = 83). When analysed with organism taken as a moderator, we establish significant negative effects of salinity (d = −3.499 ± 1.593, p = 0.028, n = 21) and stressor B (d = −2.553 ± 0.796, p = 0.001, due north = 21) on autotrophs (effigy iib,c).

Figure 2.

Figure 2. Mean event sizes (Hedge'due south d ± 95% conviction intervals), overall and by organism groups of (a) joint effect, (b) salinity individual main effect and (c) stressors B individual principal effect. The number of observations (n) of each assay is indicated in parentheses. Filled black squares point meaning effects (p < 0.05).

In the autotrophs subgroup meta-analysis, the joint effects of salinity and stressor B were besides condiment in both freshwater (d = 1.053 ± 1.402, p = 0.452, n = 10) and transitional habitats (d = 0.104 ± 1.949, p = 0.626, due north = 11). In the meta-analyses performed with the subset of studies on invertebrates occurring in inland saline waters, we found additive overall joint furnishings for increasing salinity–temperature (d = 0.396 ± 0.324, p = 0.223, n = 19, figure 3a), decreasing salinity–temperature (d = −0.257 ± 0.215, p = 0.231, n = 29, figure 3b) and increasing salinity–toxicants stressor pairs (d = −0.068 ± 0.669, p = 0.919, north = 9, effigy iiic). Salinity increase did non accept a significant main private consequence but the main consequence of salinity subtract was negative (d = −0.652 ± 0.23, p = 0.005). Such negative issue of salinity subtract contrasts with the general design of high survival of saline insects in freshwater–low salinity conditions plant in a more all-encompassing review of this topic [58]. Temperature had no significant effect, while the private primary effect of toxicants was significantly negative (d = −0.670 ± 0.323, p = 0.038). The pregnant results found in the meta-analyses were generally robust confronting publication bias co-ordinate to the symmetry observed in funnel plots (see electronic supplementary material S3) and Rosenthal fail-safe numbers greater than critical thresholds (see electronic supplementary cloth S4).

Figure 3.

Figure 3. Hateful consequence sizes (Hedge'due south d ± 95% confidence intervals) on joint and individual main effects on inland saline invertebrates for (a) salinity increase and temperature, (b) salinity decrease and temperature, and (c) salinity increase and toxicants. Filled black squares indicate significant effects (p < 0.05).

The overall and relative magnitude of stressors may play a critical role in determining their interactive effects (e.g. [15]). Yet, our meta-regressions showed no significant relationships between the absolute salinity or temperature changes and the joint or individual effect sizes (see electronic supplementary fabric S4). Joint effects of multiple stressors likewise depend on the timing at which they act [14,31]. When stressors operate sequentially, condiment effects are more likely to occur because homeostasis tin exist re-established in the time betwixt exposure to the showtime and 2nd stressor. By contrast, interactive effects are more frequent when the two stressors act simultaneously or very close in time. In our study, this effect was controlled because the vast majority of the experimental designs included simultaneous exposure to both stressors.

Overall, our findings revealed no interactive furnishings (i.e. additive effects) of salinity changes in combination with other stressors, which contrasts with the overall synergistic effects reported for marine systems [12] and the overall antagonistic issue of multiple stressor pairs establish in freshwaters [xx]. Nonetheless, our results should be cautiously compared with other meta-analysis studies, for several reasons. Commencement, responses at dissimilar organizational level are highly heterogeneous [12]. Second, Crain et al. [12] and Jackson et al. [20] did not focus specifically on salinity (it was pooled with other chemical stressors in [20]) only explored instead a wide range of stressor pairs. One possible explanation for the potency of additive effects and the college frequency of antagonisms than synergisms in our study is that salinity may ofttimes deed as a ascendant stressor, so that the other stressors have petty boosted effect [2,15]. Indeed, the overall private issue of salinity increase was generally higher than those of the other stressors analysed, such as temperature. Szöcs et al. [59] too found a greater effect of salinity than pesticides on macroinvertebrate communities, and no pregnant interaction effect between these stressors. These results have of import implications for direction of aquatic ecosystems. Mitigation strategies aimed at reducing the magnitude of salinity changes could reduce significantly the touch on organisms and substantially improve the wellness of populations and communities, as other authors have previously suggested [12,60]. In any instance, the notable variability in the importance of the interaction types among stressor pairs in different aquatic systems suggests that responses are highly context-dependent and, therefore, a general framework for predicting interactions and guiding management could exist difficult to establish [1].

Our comprehensive review included taxa with dissimilar habitats, life-history traits, stressor sensitivities and evolutionary histories (i.e. colonization from marine or terrestrial environments, transitions from fresh to saline waters, etc.), besides as a variety of strategies to cope with salinity stress. For example, while most marine and transitional water organisms are osmoconformers, the bulk of organisms in saline inland waters are osmoregulators, such every bit aquatic insects of terrestrial origin [61–63], and can cope with wide salinity fluctuations past hyper-regulation capacity in freshwater and hypo-regulation capacity in saline waters [62] (box 1). Thus, it remains to be investigated how these dissimilar osmoregulatory strategies and their associated energetic costs determine the type of interactions with other stressors.

4. Concluding remarks and future perspectives

The multiple stressor studies reviewed herein focus primarily on the combined effects of increasing salinity and increasing temperature or toxicants (metals and pesticides), while other important stressor combinations accept received very piffling attention (e.chiliad. desiccation or nutrients). The number of multiple stressor experimental studies conducted in inland waters is nonetheless limited compared with those on transitional and marine systems. Thus, more research efforts are needed in freshwater and saline inland waters, which are particularly vulnerable to multiple global change pressures [1,64].

Additive effects of salinity and other stressors were prevalent, but combative interactions were relatively frequent in some organism groups (vertebrates), habitats (transitional waters) or stressor pairs (salinity × toxicants). Salinity has a stronger negative individual outcome on organismal operation traits than other stressors, which highlights the need to increase management efforts for this single stressor (box 2).

From this review, some considerations for future research arise. First, we need to ameliorate our understanding of the mechanisms and pathways by which a single stressor modulates the physiological responses to other stressors. Second, to analyse multi-stressor effects, models more circuitous than additive ones should exist applied if stressor–effect relationships and the correlation between organism's sensitivity to each stressor are known [two,65]. Third, to better empathise and predict the effects of ongoing salinization and dilution processes in aquatic ecosystems, information technology is crucial to explore the role of the origin and evolution of the osmoregulation strategies of aquatic organisms in determining the type of interactions that ascend between salinity and other stressors.

Data accessibility

The datasets supporting this commodity take been uploaded as part of the electronic supplementary material.

Authors' contributions

J.V. conceived, designed and coordinated the study and drafted part of the manuscript; South.P. participated in the report pattern, carried out the literature review, information selection and analyses, created figure 1 and electronic supplementary material S1 and S2 and drafted function of the manuscript; C.G.-C. carried out the meta-analyses, created figures 2 and iii, and electronic supplementary material S3, S4 and S5, and drafted function of the manuscript; Thousand.B.-C. carried out the literature review, information choice and analyses, and created electronic supplementary material S1 and S2, and the reference lists; D.S.-F., P.A., J.A.C. and A.M. contributed with experimental data. All the authors discussed the results and the manuscript revision and gave terminal approval for publication.

Competing interests

Nosotros accept no competing interests.

Funding

Some physiological studies of the interaction of pair–stressors salinity–temperature, salinity–ionic composition and salinity–desiccation on the performance of aquatic saline insects were done by the Aquatic Environmental Research Grouping (University of Murcia, Spain) every bit role of the I + D + i projects CGL2010-15378 (J.5.) and CGL2013-48950-C2-2-P (J.Five. and A.M.) (Spanish Ministry of Economy and Competitiveness) co-funded by FEDER funds. C.G.-C. and P.A. are supported by 'Juan de la Cierva-Formación' research contracts (MINECO, FJCI-2015-25785 and FJCI-2014-20581, respectively), D.S.-F. by a post-doctoral contract funded by the Universidad de Castilla-La Mancha and the European Social Fund (ESF) and M.B.-C. by a PhD grant from the Universidad de Murcia.

Acknowledgements

We give thanks Miguel Cañedo-Argüelles for inviting united states of america to contribute to this monographic volume, and Cristina Coccia for providing experimental information. We are also grateful to three anonymous referees who carried out effective reviews of this work.

Footnotes

Electronic supplementary fabric is available online at https://dx.doi.org/10.6084/m9.figshare.c.4274648.

1 contribution of 23 to a theme issue 'Common salt in freshwaters: causes, ecological consequences and future prospects'.

Published by the Royal Guild. All rights reserved.

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