Abstract
Stream ecosystem functioning is often impaired by warming and salinization, but the joint effect of both environmental stressors on key processes such as leaf litter decomposition is virtually unknown, particularly in the tropics. We experimentally explored how increased water temperature (26, 29 and 32°C) and salinity (no salt addition, 0.1, 1.0 and 10 g l−1 NaCl added) affected the rates of total, microbial and detritivore-mediated decomposition, in stream microcosms containing leaf litter of Ficus insipida and larvae of Chironomus sp. collected from tropical streams. Effects of temperature were strong and consistent with previous findings: it promoted microbial decomposition and reduced decomposition mediated by detritivores, which showed greater feeding activity at 26°C. Salinity was negatively correlated with microbial decomposition at 32°C; it also had a negative influence on detritivore-mediated decomposition, which was nevertheless non-significant due to the high detritivore mortality at higher salinities. Notably, total decomposition was reduced with the joint presence of both factors (32°C and salt addition treatments, compared to 26°C and no salt addition), indicating the existence of additive effects and highlighting the relevance of multiple-stressor contexts when assessing the consequences of global change on stream ecosystems.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Our planet is going through serious environmental changes as a result of anthropogenic activities, such as forest conversion into agricultural land, urbanization, or industrial development (Sage, 2020). These environmental changes act as stressors on organisms and ecosystems, which can respond at multiple levels, from physiological alterations in individuals (Todgham & Stillman, 2013) to shifts in the rates of ecosystem processes and their capacity to provide services to humans (von Schiller et al., 2017). Within this context, multiple-stressor research is becoming prevalent because environmental changes often do not occur in isolation, and their interactions can challenge predictions of their ecological consequences (Jackson et al., 2021). The combined effects of stressors can be antagonistic, additive or synergistic depending on whether the result is lower, equal to or greater than expected (Fong et al., 2018).
Climate change is the most pervasive environmental change globally (IPCC, 2018). The rise in mean atmospheric temperature (hence in water temperature in freshwater ecosystems; Molinero et al., 2015) leads to enhanced organism metabolic rates (Brown et al., 2004) and, often, accelerated ecosystem process rates (Boyero et al., 2011b). On the other hand, changes in precipitation intensity and distribution cause the intensification of dry seasons in some regions of the planet (Park et al., 2018), which in turn interferes with water level and concentrations of pollutants in fresh waters (Rose et al., 2023). Exploring the consequences of stressors associated with climate change in freshwater ecosystems is of prime relevance because these provide fundamental ecosystem services (Richardson & Hanna, 2021) and because they are especially vulnerable to environmental changes, given that they integrate impacts produced on whole catchments (Jackson et al., 2016). Such information is particularly lacking for fresh waters located in tropical latitudes (Cornejo et al., 2019, 2020b).
In particular, stream ecosystems are highly exposed to pollutants coming from land, which are transported through runoff and can alter ecosystem processes, jointly with changes in temperature (e.g., as shown for dissolved nutrients; Ferreira & Chauvet, 2011). A type of pollutant that is common in streams, due to agricultural, industrial and mining activities, among others, and intensified by climate change, is salt (Cañedo-Arguelles et al., 2014). Salinization, however, has received little attention compared to other types of stream pollution, such as eutrophication (Cañedo-Arguelles et al., 2018), and its joint effect with warming on ecosystem processes is virtually unknown (despite some evidence existing for organism physiological responses; e.g., Velasco et al., 2018).
Information about how the above stressors and their interactions affect stream ecosystems is particularly lacking for tropical latitudes (Cornejo et al., 2019), where climate change projections are especially critical and uncertain (Corlett, 2012). Besides, some tropical areas (such as our study area in Panama) can be susceptible to salinization for multiple reasons (Herbert et al., 2015; Castillo et al., 2018), including their high aridity (Sauer et al., 2016); their proximity to the ocean (Chui & Terry, 2013), with salt being transported by sea breezes and seawater intrusions (superficial or through aquifers); and human activities such as agriculture and cattle raising (Nack et al., 2021), with salt being used as feed supplement for livestock.
Here, we measured leaf litter decomposition in microcosms in order to evaluate the combined effect of warming and salinization on stream ecosystems from a tropical dry area, the Dry Arc region in Panama. The process of leaf litter decomposition is a useful tool to assess environmental stressor impacts on stream ecosystems (Gessner & Chauvet, 2002) and it has been used to explore effects of salinization (Canhoto et al., 2021). Terrestrial leaf litter represents the major basal resource in many streams, where the riparian canopy restrains primary production, and microbial decomposers (mainly aquatic hyphomycetes) and some detritivorous invertebrates (hereafter detritivores) specialize in processing this leaf litter and incorporating it into the aquatic food web (Marks, 2019). We used all combinations of three temperatures and four sodium chloride (NaCl) concentrations, and exposed leaf litter to the action of microorganisms and detritivores collected from tropical streams for 2 weeks. We hypothesized that (1) increased temperature would enhance microbial and detritivore-mediated decomposition, as a result of higher metabolic rates (Ferreira & Chauvet, 2011); (2) increased salinity would decrease microbial and detritivore-mediated decomposition, as a result of osmotic imbalances and hence reduced rates of biological activity (Canhoto et al., 2021); and (3) effects of salinization would be more evident at lower temperatures, because the increase in decomposition rates at higher temperatures would offset the decrease caused by salinization (i.e., both stressors would show antagonistic effects; Jackson et al., 2016).
Materials and methods
Collection of biological material
We used leaf litter of Ficus insipida Willd. (Moraceae), a species of fig tree that is commonly found in the Pacific slope of Panama. Leaves of this species have relatively good quality (SLA = 10.7 ± 1.1 mm2 mg−1; N = 1.09 ± 0.09%; Cornejo et al., 2020b) and have been readily used by microbial decomposers and detritivores in previous experimental studies (Cornejo et al., 2020b; López-Rojo et al., 2020b; Pérez et al., 2021b). We collected recently fallen leaves from the forest floor of the Metropolitan Natural Park (8° 59′ 36.77″ N, 79° 32′ 46.66″ W) in August 2022. Leaves were air dried and stored in the laboratory until used.
Larvae of Chironomus sp. (Diptera: Chironomidae) were selected as detritivores, as the species is the most abundant in the study area (the Tonosí river catchment, central Panama) and it feeds on a wide variety of types of detritus, including leaf litter (Callisto & Gonçalves Jr, 2007; Small et al., 2011). This group of organisms has shown high tolerance to alterations related to eutrophication and low concentrations of dissolved oxygen (Frouz et al., 2003), being an example of generalist tolerant (Rosin et al., 2010; Steinberg & Steinberg, 2012), and becoming the dominant detritivore in decomposing litter under altered conditions (Pérez et al., 2013).
We collected larvae in a tributary near the Tonosí Forest Reserve (7° 14′ 51.77″ N, 80° 34′ 14.93″ W; 57 m asl), to ensure that they had not been previously exposed to high levels of salinity and high temperatures. For larval collection, we placed six artificial pools at the stream banks within 2 m from the stream for 21 days. The pools consisted of 9-l plastic buckets, each filled with stream water [pH: 7.8; conductivity: 0.351 mS cm−1; salinity: 0.17 PSU; dissolved oxygen (DO): 6.1 mg l−1] and containing 3 g of Ficus insipida leaf litter enclosed within a coarse-mesh (10 mm) bag. The collected larvae were transported to the laboratory and placed in glass containers filled with stream water and leaf litter, with constant aeration. Larvae were acclimated for 96 h at 26.31 ± 0.01°C, fed with F. insipida leaf litter fragments for the first 48 h, and then fasted for another 48 h before the start of the experiment. We used 168 individuals in the experiment (2 per microcosm).
Finally, we collected mixed leaf litter at different stages of decomposition from natural leaf litter deposits in a stream tributary near the Tonosí Forest Reserve (7° 14′ 51.77″ N, 80° 34′ 14.93″ W). This leaf litter was incubated in a 2.5-l aquarium filled with filtered stream water (100 μm) with aeration for 48 h, with replacement every 24 h. This water was used as microbial inoculum (10 ml per microcosm) at the beginning of the experiment (day 0), providing the microcosms not only with aquatic hyphomycete conidia, but also with other microorganisms (i.e., bacteria), which might also play a role in the decomposition process.
Experimental procedure and sample processing
The experiment was carried out in September 2022, at the facilities of the Aquatic Ecology and Ecotoxicology Laboratory (AEEL) of the Gorgas Memorial Institute for Health Studies, located at the National Institute of Agriculture (INA: 8° 07′ 43.4691″ N, 80° 41′ 18.3086″ W). We used eighty-four 500-ml glass jars, which were located in a temperature-controlled room set at 25°C, and provided with constant aeration and a light:dark regime of 12:12 h, thus reflecting natural conditions. The jars were introduced within three 100-l tanks (with 28 microcosms per tank; 7 replicates per temperature × salinity combination), which were used as water baths with different temperatures (26, 29 and 32°C) that were reached using aquarium water heaters (HITOP 300w) and turbines (AQUANEAT average 800 GPH) for water circulation. This represented basal conditions in the study stream and two situations of warming (3 and 6°C increase) that could result from climate change (IPCC, 2018) and/or heat waves (Pérez et al., 2021a). Temperatures were monitored with a data logger (Thermobutton, model 22L, Plug & Track) placed within one microcosm per tank, which took a measurement every 30 min.
Each microcosm contained 400 ml of filtered (100 μm) stream water and it was assigned to one of four salinity treatments depending on NaCl concentration [control (no NaCl added), low (0.1 g l−1 NaCl), moderate (1.0 g l−1 NaCl) and high (10.0 g l−1 NaCl)], with seven replicates per treatment at each experimental temperature. The studied salinity gradient aimed to represent successive increases of one order of magnitude, from the basal concentration (0.12–0.27 PSU, 0.15–0.40 TDS g l−1) to high salinity stress (2 orders of magnitude higher), in order to assess the effects in halotolerant taxa such as aquatic hyphomycetes (Canhoto et al., 2017). We chose to alter concentrations of NaCl because sodium represents the major cation increasing salinity in fresh waters (Cunillera-Montcusí et al., 2022), especially when the source of salt is related to seawater (Cañedo-Argüelles, 2020), using high-purity salt (ACS Grade) to reduce contamination by other components (e.g., table salt in Panama is always supplemented with iodine). Prior to the experiment, we introduced 1 g of air-dried leaf litter fragments in each microcosm and kept them for 48 h, with water exchange at 24 h. Leaf litter was collected (by filtering the water through 100 μm), oven-dried (70°C, 48 h), weighed to calculate dry mass (DM), incinerated (500°C, 4 h), and re-weighed to calculate AFDM. These data were used to calculate mass losses due to the leaching of soluble compounds (see “Data analyses” below; Bärlocher, 2020).
For the experiment, the microcosms were again filled with water with the same salinity treatments as before. This time, each microcosm received 700 ± 0.001 mg of free, air-dried Ficus insipida leaf litter fragments, attached with a safety pin to prevent them from floating; and another 300 ± 0.003 mg of leaf litter enclosed in mesh bags (8 × 6.5 cm size, 0.5 mm mesh opening), so they would not be accessible to detritivores. Water was exchanged after 24 and 48 h to promote leaching and, after 48 h, 10 ml of the microbial inoculum and two Chironomus larvae were also added. The body length of each larva was measured using a millimetred sheet. The experiment lasted 15 days, after which leaf litter was collected and processed as above, separately for free and enclosed leaf litter. The final status of each detritivore (i.e., dead, alive or emerged) was recorded and their final body length measured. During the experiment, every 2 days, several physical and chemical variables (temperature, pH, DO and salinity) were measured with a multiparametric probe (model 556 MPS, YSI Inc.).
Data analyses
We explored the variation of the measured physical and chemical variables (temperature, pH, DO and salinity) through experimental time with general linear models (GLMs), where temperature treatment, salinity treatment and time were fixed factors. Our data did not meet the assumptions of normality and homoscedasticity required for parametric models (i.e. ANOVAs), but general linear models (GLMs) included a link function and a variance function that improved the fit of the model to the data structure (Nelder & Wedderburn, 1972). We used the gls function on the nlme package in R software, and a model selection procedure based on the Akaike information criterion (AIC) in order to include or exclude the variance function structure varIdent as appropriate (e.g., see López‐Rojo et al., 2022). Leaf litter decomposition was measured through (1) the proportion of leaf litter mass loss [LML (prop.) = (final AFDM − initial AFDM)/initial AFDM] and (2) linear decomposition rates based on days (bd) and degree-days (bdd), the latter to standardize by temperature (Barlochër, 2020). We quantified total (free leaf litter), microbial (enclosed leaf litter) and detritivore-mediated decomposition (difference between free and enclosed leaf litter). Initial AFDM was corrected for leaching losses, multiplying by the proportion of leaf litter mass remaining in the set of leaf litter fragments used prior to the experiment. Total and detritivore-mediated decomposition were standardized using the mean initial body size (mm) of larvae in each microcosm (3.8 ± 0.06 mm; mean ± S.E., N = 168), to avoid variability due to differences in larval size. Additionally, in order to consider effects of detritivore loss (due to mortality and/or emergence) on decomposition, we corrected the initial body size according to detritivore presence at the end of the experiment. Thus, we used a correction factor of “1” when both detritivores were present at the end of the experiment, “0.75” if only one survived, or “0.5” if none of them were present.
We used general linear models (gls function, nlme package) to explore variation in the response variables (total, microbial and detritivore-mediated LML) with temperature treatments (26, 29 and 32°C), salinity treatments (control, low, moderate and high) and their interactions, with both factors being fixed. Again, model selection based on AIC was used for varIdent inclusion or exclusion. Differences among treatment levels were explored with Tukey tests (ghlt function, multcomp package). When the interaction between temperature and salinity resulted significant, we further explored their joint effects on LML with Tukey tests of all possible combinations. Finally, to help visualize these combined effects, we examined relationships between LML and physical and chemical variables (temperature, pH, DO and salinity) at the different temperature and salinity treatments and for all treatments combined, using Pearson correlations.
Results
Average temperature was 26.2, 28.55 and 31.67°C respectively, in the different temperature treatments, and average salinity was 0.18, 0.28, 1.21 and 10.42 mg l−1, respectively, in the different salinity treatments (Table 1). All variables showed variation with time (Table S1), but temperature and salinity mostly remained constant throughout the experiment (Fig. S1). Larval mortality was 54% overall, and it tended to increase with salinity (26%, 57%, 55% and 100% in the control, low, moderate and high salinity treatments, respectively) but not with temperature (64%, 50% and 66% at 26, 29 and 32°C, respectively). The 40% of surviving larvae emerged during the experiment, and emergence tended to decrease with salinity (19%, 10%, 10% and null in the control, low, moderate and high salinity treatments, respectively) and to increase with temperature (9%, 17% and 14% at 26, 29 and 32°C, respectively). Considering these relatively high frequencies, our design prevented discerning between lethal and sublethal effects in the subsequent results.
Total decomposition varied with temperature and salinity and the interaction was significant (Table 2; Fig. 1), with Tukey tests indicating that decomposition was higher at the lowest temperature and control salinity than at the highest temperature and low, moderate and high salinities (Fig. S2). Microbial decomposition, however, was enhanced by temperature (26°C < 29°C < 32°C) but did not vary among salinities, and detritivore-mediated decomposition also differed only among temperatures (26°C > 29°C = 32°C). Linear decomposition rates showed similar paters in terms of time (% d−1) or accumulated heat (% dd−1), featuring the same trends as LML in relation to stressors (Fig. S3). Decomposition rates corrected by detritivore loss showed similar trends in response to stress factors (Fig. S4).
Overall, total and detritivore-mediated decomposition were positively correlated with DO and negatively with temperature, and microbial decomposition showed the opposite pattern (Fig. 2). When examined separately for different temperature treatments, total and detritivore-mediated decomposition were positively correlated with pH and DO at the lower temperature, and microbial decomposition was negatively correlated with pH at the lower temperature and with salinity at the higher temperature (Fig. 2). When examined separately for different salinity treatments, total and detritivore-mediated decomposition were mostly positively correlated with DO (only at some salinities for total decomposition and at all salinities for detritivore-mediated decomposition), and the same occurred with temperature with negative relationships; detritivore-mediated decomposition was positively related to pH and negatively to salinity at some salinities; and microbial decomposition was negatively related to DO and positively to temperature at all salinities, and positively related to pH and salinity in some cases (Fig. 2).
Discussion
Freshwater ecosystems are highly vulnerable to climate change (Woodward et al., 2010) and pollutants (Carpenter et al., 2011). In particular, streams flowing through agricultural catchments receive runoff that often contains organic nutrients and pesticides, as well as high levels of salinity (Schafer et al., 2012). However, while joint effects of climate warming and eutrophication on streams have received considerable attention (e.g., Ferreira & Chauvet, 2011), the effects of salinization in combination with other stressors are virtually unknown (Canhoto et al., 2021). This is especially true for tropical regions, where water temperatures are high and detritivore assemblages differ substantially from those of temperate zones (Boyero et al., 2011a, 2021). In our microcosm experiment, we explored how warming and salinization in tropical streams jointly affected the key process of leaf litter decomposition, which often is a good indicator of how stream ecosystem integrity is impaired (Gessner & Chauvet, 2002).
Overall, we found a strong effect of temperature, which altered leaf litter decomposition driven by microorganisms and detritivores separately, as well as total decomposition. As previously mentioned, we were unable to distinguish between lethal and sublethal effects, both of which were most likely responsible for the observed effects on the decomposition process, as occurred in other studies (e.g., Cornejo et al., 2020a; López-Rojo et al., 2020a). Importantly, our results remained the same when we corrected our data based on detritivore loss as a result of mortality or emergence. Microbial decomposition rates increased with temperature, reflecting the well-known direct relationship between temperature and metabolic rates (Brown et al., 2004), which has been shown in many other decomposition studies (e.g., Boyero et al., 2011b; Ferreira & Chauvet, 2011; Follstad Shah et al., 2017). In contrast, our results contradicted the generally positive relationship between DO and microbial decomposition (Medeiros et al., 2009), possibly in relation to the inverse relationship between DO and water temperature. Detritivore-mediated decomposition decreased with temperature, being higher at 26°C than at higher temperatures. It is well known that the role of detritivores on decomposition in tropical areas tends to be of minor importance compared to microbial activity (Boyero et al., 2011b), as most typical leaf litter consumers (i.e., shredders) are adapted to colder conditions (Danks, 2007; Strickland et al., 2015). There is, however, little information about leaf litter feeding rates of Chironomus species, which is a facultative leaf litter-feeding detritivore in tropical and temperate streams (Callisto & Gonçalves Jr, 2007; Pérez et al., 2013), acting as leaf-miners (Boyero et al., 2020). Other leaf litter consumers have shown different patterns of variation in their feeding activity with temperature. For example, the caddisfly Sericostoma vittatum Rambur, 1842 showed higher feeding rates at 10°C than 15°C (Landeira-Dabarca et al., 2018), while the amphipod Gammarus pulex (Linnaeus, 1758) showed higher rates at 24°C than at lower temperatures (Foucreau et al., 2016). These differences could be related to species-specific requirements or to the different temperature treatments used in experiments, or to a combination of both factors.
Effects of salinity were more variable than those of temperature, and non-significant for microbial decomposition, as some bacteria and aquatic hyphomycetes are highly tolerant to salt (Canhoto et al., 2021). Also, microbial decomposer assemblages can be resilient to salinization due to species functional redundancy (Canhoto et al., 2017). However, it is known that aquatic hyphomycete sporulation can be supressed and biomass reduced and, as a consequence, microbial decomposition can decrease with salt addition, although this is not always the case (Canhoto et al., 2021). For example, an experiment using Eucalyptus camaldulensis Dehnh. leaf litter observed a significant reduction in microbial decomposition when conductivity was increased from 1 to 10 mS cm−1 (Sauer et al., 2016). In contrast, microbial decomposition rates of Quercus robur L. were not affected by increased salinity in two experiments (Gonçalves et al., 2019; Martínez et al., 2020). These inconsistent results could be partly related to differences in leaf litter traits; this hypothesis was not supported by a study conducted with Q. robur and Castanea sativa Mill., but these two species do not differ greatly in their nutrient contents and toughness (Almeida Júnior et al., 2020), so the influence of leaf traits cannot be discarded.
Detritivore-mediated decomposition did not vary with salinity in our experiment, but their activity tended to decrease; P-values were only slightly above the α = 0.05 threshold, and the lack of significance was most likely due to the high mortality of Chironomus sp. at higher salinities (which was total at the 10 mg l−1 treatment). Previous studies have found, again, inconsistent results, with reduced feeding rates due to increased salinity for some detritivores such as the tipulid Tipula abdominalis (Say, 1823) and the caddisfly Schizopelex festiva (Rambur, 1842), and the opposite pattern for others such as the isopod Lirceus sp. (Tyree et al., 2016; Martínez et al., 2020). These differences could be due to the different salts and salinity gradients used, but also to intrinsic differences among species. Increased salinity may affect the osmoregulatory capacity of invertebrates (i.e., their ability to actively regulate osmotic pressure), and the required energy expenditure may become too high, or osmoregulatory mechanisms may collapse resulting in cellular damage and death (Cañedo-Arguelles et al., 2013). In agreement with this, we observed a trend towards less survival of Chironomus sp. with increased salinity, being the highest salinity treatment lethal for all the individuals tested. However, we did not anticipated such lethal effects on Chironomus sp. given the known cross-tolerance of this group (Gama et al., 2014), being common in multi-stressed ecosystems (Popović et al., 2022). The inconsistent negative values in detritivore-mediated decomposition might be the result of a promoted biofilm accrual in absence of detritivores, as previously suggested (Pérez et al., 2021a).
When total decomposition was quantified altogether, salinity influenced the process and interacted with the effect of temperature: decomposition was higher in microcosms exposed to the lower temperature and control salinity than in those exposed to the higher temperature and any of the salt addition treatments. Previous experiments have also found reductions in total decomposition with high (but not with moderate) salinity treatments; e.g., at 15 mS cm−1 for Populus nigra L., with no effect at 5 and 10 mS cm−1 (Cañedo-Arguelles et al., 2014); or at 15.3 mS cm−1 for Alnus glutinosa (L.) Gaertn., with the opposite effect at 3.3 and 5.5 mS cm−1 (Abelho et al., 2021). Our results agree with their findings, but they further show that temperature can modulate the effect of salinity, with additive effects of both factors: total decomposition was reduced by 39% due to high salinity, 21% due to high temperature and 60% due to both factors simultaneously. The effect was probably driven by detritivores, which might be more vulnerable to salt toxicity at high temperatures, as observed for other invertebrates in acute toxicity tests (Jackson & Funk, 2018). Despite the limitations of our analyses and others (Piggott et al., 2015; Tekin et al., 2020) to explore interactions between stressors, we provide evidence suggesting that such interactions should be taken into account as much as possible in experimental studies.
Conclusions
Our experiment demonstrates that the simultaneous presence of warming and salinization can interact to inhibit leaf litter decomposition in streams. This novel result supports those of previous experiments showing positive interactions between different environmental stressors, such as the joint presence of warming and eutrophication enhancing microbial decomposition (Ferreira & Chauvet, 2011). Overall, our results reinforce the idea that a multiple-stressor context should be prioritized when examining effects of global environmental change on stream ecosystem functioning.
Data availability
All data generated or analysed during this study are included in this published article [and its supplementary information files]. Raw data will be made available on request.
References
Abelho, M., R. Ribeiro & M. Moreira-Santos, 2021. Salinity affects freshwater invertebrate traits and litter decomposition. Diversity 13: 599.
Almeida Júnior, E. S., A. Martínez, A. L. Gonçalves & C. Canhoto, 2020. Combined effects of freshwater salinization and leaf traits on litter decomposition. Hydrobiologia 847: 3427–3435.
Barlochër, F., 2020. Leaf mass loss estimated by litter bag technique. In Barlochër, F., M. O. Gessner & M. A. S. Graça (eds), Methods to Study Litter Decomposition: A Practical Guide 2nd ed. Springer, Dordrecht, The Netherlands: 43–52.
Bärlocher, F., 2020. Leaching. In Bärlocher, F., M. O. Gessner & M. A. S. Graça (eds), Methods to Study Litter Decomposition: A Practical Guide 2nd ed. Springer, Dordrecht: 37–41.
Boyero, L., R. G. Pearson, D. Dudgeon, M. A. S. Graça, M. O. Gessner, R. J. Albariño, V. Ferreira, C. M. Yule, A. J. Boulton, M. Arunachalam, M. Callisto, E. Chauvet, A. Ramírez, J. Chará, M. S. Moretti, J. F. Gonçalves, J. E. Helson, A. M. Chará-Serna, A. C. Encalada, J. N. Davies, S. Lamothe, A. Cornejo, A. O. Y. Li, L. M. Buria, V. D. Villanueva, M. C. Zúñiga & C. M. Pringle, 2011a. Global distribution of a key trophic guild contrasts with common latitudinal diversity patterns. Ecology 92: 1839–1848.
Boyero, L., R. G. Pearson, M. O. Gessner, L. A. Barmuta, V. Ferreira, M. A. S. Graça, D. Dudgeon, A. J. Boulton, M. Callisto, E. Chauvet, J. E. Helson, A. Bruder, R. J. Albariño, C. M. Yule, M. Arunachalam, J. N. Davies, R. Figueroa, A. S. Flecker, A. Ramírez, R. G. Death, T. Iwata, J. M. Mathooko, C. Mathuriau, J. F. Gonçalves, M. Moretti, T. **ggut, S. Lamothe, C. M’erimba, L. Ratnarajah, M. H. Schindler, J. Castela, L. M. Buria, A. Cornejo, V. D. Villanueva & D. C. West, 2011b. A global experiment suggests climate warming will not accelerate litter decomposition in streams but may reduce carbon sequestration. Ecology Letters 14: 289–294.
Boyero, L., R. G. Pearson, R. Albariño, M. Callisto, F. Correa-Araneda, A. C. Encalada, F. Masese, M. Moretti, A. Ramírez, A. Sparkman, C. M. Swan, C. M. Yule & M. A. S. Graça, 2020. Identifying stream invertebrates as plant litter consumers. In Barlochër, F., M. O. Gessner & M. A. S. Graça (eds), Methods to Study Plant Litter Decomposition. A Practical Guide 2nd ed. Springer, Dordrecht.
Boyero, L., N. López-Rojo, A. M. Tonin, J. Pérez, F. Correa-Araneda, R. G. Pearson, J. Bosch, R. J. Albariño, S. Anbalagan, L. A. Barmuta, A. Basaguren, F. J. Burdon, A. Caliman, M. Callisto, A. R. Calor, I. C. Campbell, B. J. Cardinale, J. J. Casas, A. M. Chará-Serna, E. Chauvet, S. Ciapała, C. Colón-Gaud, A. Cornejo, A. M. Davis, M. Degebrodt, E. S. Dias, M. E. Díaz, M. M. Douglas, A. C. Encalada, R. Figueroa, A. S. Flecker, T. Fleituch, E. A. García, G. García, P. E. García, M. O. Gessner, J. E. Gómez, S. Gómez, J. F. Gonçalves, M. A. S. Graça, D. C. Gwinn, R. O. Hall, N. Hamada, C. Hui, D. Imazawa, T. Iwata, S. K. Kariuki, A. Landeira-Dabarca, K. Laymon, M. Leal, R. Marchant, R. T. Martins, F. O. Masese, M. Maul, B. G. McKie, A. O. Medeiros, C. M. M. Erimba, J. A. Middleton, S. Monroy, T. Muotka, J. N. Negishi, A. Ramírez, J. S. Richardson, J. Rincón, J. Rubio-Ríos, G. M. dos Santos, R. Sarremejane, F. Sheldon, A. Sitati, N. S. D. Tenkiano, S. D. Tiegs, J. R. Tolod, M. Venarsky, A. Watson & C. M. Yule, 2021. Impacts of detritivore diversity loss on instream decomposition are greatest in the tropics. Nature Communications. https://doi.org/10.1038/s41467-021-23930-2.
Brown, J. H., J. F. Gillooly, A. P. Allen, V. M. Savage & G. B. West, 2004. Toward a metabolic theory of ecology. Ecology 85: 1771–1789.
Callisto, M. & J. F. Gonçalves Jr., 2007. Leaf litter as a possible food source for chironomids (Diptera) in Brazilian and Portuguese headwater streams. Revista Brasileira de Zoologia 24: 442–448.
Cañedo-Argüelles, M., 2020. A review of recent advances and future challenges in freshwater salinization. Limnetica 39: 185–211.
Cañedo-Arguelles, M., B. J. Kefford, C. Piscart, N. Prat, R. B. Schafer & C. J. Schulz, 2013. Salinisation of rivers: an urgent ecological issue. Environmental Pollution 173: 157–167.
Cañedo-Arguelles, M., M. Bundschuh, C. Gutierrez-Canovas, B. J. Kefford, N. Prat, R. Trobajo & R. B. Schafer, 2014. Effects of repeated salt pulses on ecosystem structure and functions in a stream mesocosm. Science of The Total Environment 476–477: 634–642.
Cañedo-Arguelles, M., B. Kefford & R. Schafer, 2018. Salt in freshwaters: causes, effects and prospects – introduction to the theme issue. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 20180002.
Canhoto, C., S. Simoes, A. L. Goncalves, L. Guilhermino & F. Barlocher, 2017. Stream salinization and fungal-mediated leaf decomposition: a microcosm study. Science of The Total Environment 599–600: 1638–1645.
Canhoto, C., F. Bärlocher, M. Cañedo-Argüelles, R. Gómez & A. L. Gonçalves, 2021. Salt modulates plant litter decomposition in stream ecosystems. In Swan, C. M., L. Boyero & C. Canhoto (eds), The Ecology of Plant Litter Decomposition in Stream Ecosystems Springer, Cham: 323–345.
Carpenter, S. R., E. H. Stanley & M. J. Vander Zanden, 2011. State of the world’s freshwater ecosystems: physical, chemical, and biological changes. Annual Review of Environment and Resources 36: 75–99.
Castillo, A. M., D. M. Sharpe, C. K. Ghalambor & L. F. De León, 2018. Exploring the effects of salinization on trophic diversity in freshwater ecosystems: a quantitative review. Hydrobiologia 807: 1–17.
Chui, T. F. M. & J. P. Terry, 2013. Influence of sea-level rise on freshwater lenses of different atoll island sizes and lens resilience to storm-induced salinization. Journal of Hydrology 502: 18–26.
Corlett, R. T., 2012. Climate change in the tropics: the end of the world as we know it? Biological Conservation 151: 22–25.
Cornejo, A., A. M. Tonin, B. Checa, A. R. Tuñon, D. Pérez, E. Coronado, S. González, T. Ríos, P. Macchi, F. Correa-Araneda & L. Boyero, 2019. Effects of multiple stressors associated with agriculture on stream macroinvertebrate communities in a tropical catchment. PLoS ONE 14: e0220528.
Cornejo, A., J. Pérez, A. Alonso, N. López-Rojo & L. Boyero, 2020a. A common fungicide impairs stream ecosystem functioning through effects on aquatic hyphomycetes and detritivorous caddisflies. Journal of Environmental Management 263: 110425.
Cornejo, A., J. Perez, N. Lopez-Rojo, A. M. Tonin, D. Rovira, B. Checa, N. Jaramillo, K. Correa, A. Villarreal, V. Villarreal, G. Garcia, E. Perez, T. A. Rios Gonzalez, Y. Aguirre, F. Correa-Araneda & L. Boyero, 2020b. Agriculture impairs stream ecosystem functioning in a tropical catchment. Science of The Total Environment 745: 140950.
Cunillera-Montcusí, D., M. Beklioğlu, M. Cañedo-Argüelles, E. Jeppesen, R. Ptacnik, C. A. Amorim, S. E. Arnott, S. A. Berger, S. Brucet & H. A. Dugan, 2022. Freshwater salinisation: a research agenda for a saltier world. Trends in Ecology & Evolution 37: 440–453.
Danks, H., 2007. How aquatic insects live in cold climates. The Canadian Entomologist 139: 443–471.
Ferreira, V. & E. Chauvet, 2011. Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi. Global Change Biology 17: 551–564.
Follstad Shah, J. J., J. S. Kominoski, M. Ardon, W. K. Dodds, M. O. Gessner, N. A. Griffiths, C. P. Hawkins, S. L. Johnson, A. Lecerf, C. J. LeRoy, D. W. P. Manning, A. D. Rosemond, R. L. Sinsabaugh, C. M. Swan, J. R. Webster & L. H. Zeglin, 2017. Global synthesis of the temperature sensitivity of leaf litter breakdown in streams and rivers. Global Change Biology 23: 3064–3075.
Fong, C. R., S. J. Bittick & P. Fong, 2018. Simultaneous synergist, antagonistic and additive interactions between multiple local stressors all degrade algal turf communities on coral reefs. Journal of Ecology 106: 1390–1400.
Foucreau, N., C. Piscart, S. Puijalon & F. Hervant, 2016. Effects of rising temperature on a functional process: consumption and digestion of leaf litter by a freshwater shredder. Fundamental and Applied Limnology/Archiv für Hydrobiologie 187: 295–306.
Frouz, J., J. Matena & A. Ali, 2003. Survival strategies of chironomids (Diptera: Chironomidae) living in temporary habitats: a review. European Journal of Entomology 100: 459–466.
Gama, M., L. Guilhermino & C. Canhoto, 2014. Comparison of three shredders response to acute stress induced by eucalyptus leaf leachates and copper: single and combined exposure at two distinct temperatures. Annales de Limnologie-International Journal of Limnology 50: 97–107.
Gessner, M. O. & E. Chauvet, 2002. A case for using litter breakdown to assess functional stream integrity. Ecological Applications 12: 498–510.
Gonçalves, A. L., S. Simoes, F. Barlöcher & C. Canhoto, 2019. Leaf litter microbial decomposition in salinized streams under intermittency. Science of The Total Environment 653: 1204–1212.
Herbert, E. R., P. Boon, A. J. Burgin, S. C. Neubauer, R. B. Franklin, M. Ardón, K. N. Hopfensperger, L. P. Lamers & P. Gell, 2015. A global perspective on wetland salinization: ecological consequences of a growing threat to freshwater wetlands. Ecosphere 6: 1–43.
IPCC, 2018. Global warming of 1.5°C. An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty. In Masson-Delmotte, V., P. Zhai, H. O. Pörtner, D. Roberts, J. Skea, P. R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J. B. R. Matthews, Y. Chen, X. Zhou, M. I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, T. Waterfield (eds), Geneva, Switzerland.
Jackson, J. K. & D. H. Funk, 2018. Temperature affects acute mayfly responses to elevated salinity: implications for toxicity of road de-icing salts. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 1764.
Jackson, M. C., C. J. G. Lowewen, R. D. Vinebrooke & C. T. Chimimba, 2016. Net effects of multiple stressors in freshwater ecosystems: a meta-analysis. Global Change Biology 22: 180–189.
Jackson, M. C., S. Pawar & G. Woodward, 2021. The temporal dynamics of multiple stressor effects: from individuals to ecosystems. Trends in Ecology & Evolution 36: 402–410.
Landeira-Dabarca, A., J. Pérez, M. A. S. Graça & L. Boyero, 2018. Joint effects of temperature and litter quality on detritivore-mediated breakdown in streams. Aquatic Sciences. https://doi.org/10.1007/s00027-018-0598-8.
López-Rojo, N., J. Pérez, A. Alonso, F. Correa-Araneda & L. Boyero, 2020a. Microplastics have lethal and sublethal effects on stream invertebrates and affect stream ecosystem functioning. Environmental Pollution 259: 113898.
López-Rojo, N., J. Pérez, J. Pozo, A. Basaguren, U. Apodaka-Etxebarria, F. Correa-Araneda & L. Boyero, 2020b. Shifts in key leaf litter traits can predict effects of plant diversity loss on decomposition in streams. Ecosystems 24: 185–196.
López-Rojo, N., L. Boyero, J. Pérez, A. Basaguren & B. J. Cardinale, 2022. No evidence of biodiversity effects on stream ecosystem functioning across green and brown food web pathways. Freshwater Biology 67: 720–730.
Marks, J. C., 2019. Revisiting the fates of dead leaves that fall into streams. Annual Review of Ecology, Evolution, and Systematics 50: 547–568.
Martínez, A., J. Barros, A. L. Gonçalves & C. Canhoto, 2020. Salinisation effects on leaf litter decomposition in fresh waters: does the ionic composition of salt matter? Freshwater Biology 65: 1475–1483.
Medeiros, A., C. Pascoal & M. Graça, 2009. Diversity and activity of aquatic fungi under low oxygen conditions. Freshwater Biology 54: 142–149.
Molinero, J., A. Larrañaga, J. Pérez, A. Martínez & J. Pozo, 2015. Stream temperature in the Basque Mountains during winter: thermal regimes and sensitivity to air warming. Climatic Change 134: 593–604.
Nack, M. F., M. L. Van Emon, S. A. Wyffels, M. K. Manoukian, T. J. Carlisle, N. G. Davis, T. J. Kirkpatrick, J. A. Kluth, H. M. DelCurto-Wyffels & T. DelCurto, 2021. Impact of increasing levels of NaCl in drinking water on the intake and utilization of low-quality forages by beef cattle hand-fed a protein supplement or protein supplement containing 25% salt. Translational Animal Science 5: S101–S105.
Nelder, J. A. & R. W. Wedderburn, 1972. Generalized linear models. Journal of the Royal Statistical Society Series A: Statistics in Society 135: 370–384.
Park, C.-E., S.-J. Jeong, M. Joshi, T. J. Osborn, C.-H. Ho, S. Piao, D. Chen, J. Liu, H. Yang, H. Park, B.-M. Kim & S. Feng, 2018. Kee** global warming within 1.5 °C constrains emergence of aridification. Nature Climate Change 8: 70–74.
Pérez, J., A. Basaguren, E. Descals, A. Larrañaga & J. Pozo, 2013. Leaf-litter processing in headwater streams of northern Iberian Peninsula: moderate levels of eutrophication do not explain breakdown rates. Hydrobiologia 718: 41–57.
Pérez, J., F. Correa-Araneda, N. López-Rojo, A. Basaguren & L. Boyero, 2021a. Extreme temperature events alter stream ecosystem functioning. Ecological Indicators 121: 106984.
Pérez, J., V. Ferreira, M. A. S. Graça & L. Boyero, 2021b. Litter quality is a stronger driver than temperature of early microbial decomposition in oligotrophic streams: a microcosm study. Microbial Ecology 82: 897–908.
Piggott, J. J., C. R. Townsend & C. D. Matthaei, 2015. Reconceptualizing synergism and antagonism among multiple stressors. Ecology and Evolution 5: 1538–1547.
Popović, N., N. Marinković, D. Čerba, M. Raković, J. Đuknić & M. Paunović, 2022. Diversity patterns and assemblage structure of non-biting midges (Diptera: Chironomidae) in urban waterbodies. Diversity 14: 187.
Richardson, J. S. & D. E. L. Hanna, 2021. Leaf litter decomposition as a contributor to ecosystem service provision. In Swan, C. M., L. Boyero & C. Canhoto (eds), The Ecology of Plant Litter Decomposition Springer, Cham: 511–523.
Rose, K. C., B. Bierwagen, S. D. Bridgham, D. M. Carlisle, C. P. Hawkins, N. L. Poff, J. S. Read, J. R. Rohr, J. E. Saros & C. E. Williamson, 2023. Indicators of the effects of climate change on freshwater ecosystems. Climatic Change 176: 23.
Rosin, G. C., D. P. de Oliveira Mangarotti & A. M. Takeda, 2010. Chironomidae (Diptera) community structure in two subsystems with different states of conservation in a floodplain of southern Brazil. Acta Limnologica Brasiliensia 22: 276–286.
Sage, R. F., 2020. Global change biology: a primer. Global Change Biology 26: 3–30.
Sauer, F. G., M. Bundschuh, J. P. Zubrod, R. B. Schafer, K. Thompson & B. J. Kefford, 2016. Effects of salinity on leaf breakdown: dryland salinity versus salinity from a coalmine. Aquatic Toxicology 177: 425–432.
Schafer, R. B., M. Bundschuh, D. A. Rouch, E. Szocs, P. C. von der Ohe, V. Pettigrove, R. Schulz, D. Nugegoda & B. J. Kefford, 2012. Effects of pesticide toxicity, salinity and other environmental variables on selected ecosystem functions in streams and the relevance for ecosystem services. Science of The Total Environment 415: 69–78.
Small, G. E., J. P. Wares & C. M. Pringle, 2011. Differences in phosphorus demand among detritivorous chironomid larvae reflect intraspecific adaptations to differences in food resource stoichiometry across lowland tropical streams. Limnology and Oceanography 56: 268–278.
Steinberg, C. E. & C. E. Steinberg, 2012. One stressor prepares for the next one to come: cross-tolerance. In Stress Ecology Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2072-5_12
Strickland, M. S., A. D. Keiser & M. A. Bradford, 2015. Climate history shapes contemporary leaf litter decomposition. Biogeochemistry 122: 165–174.
Tekin, E., E. S. Diamant, M. Cruz-Loya, V. Enriquez, N. Singh, V. M. Savage & P. J. Yeh, 2020. Using a newly introduced framework to measure ecological stressor interactions. Ecology Letters 23: 1391–1403.
Todgham, A. E. & J. H. Stillman, 2013. Physiological responses to shifts in multiple environmental stressors: relevance in a changing world. Integrative and Comparative Biology 53: 539–544.
Tyree, M., N. Clay, S. Polaskey & S. Entrekin, 2016. Salt in our streams: even small sodium additions can have negative effects on detritivores. Hydrobiologia 775: 109–122.
Velasco, J., C. Gutierrez-Canovas, M. Botella-Cruz, D. Sanchez-Fernandez, P. Arribas, J. A. Carbonell, A. Millan & S. Pallares, 2018. Effects of salinity changes on aquatic organisms in a multiple stressor context. Philosophical Transactions of the Royal Society B: Biological Sciences 374: 20180011.
von Schiller, D., V. Acuna, I. Aristi, M. Arroita, A. Basaguren, A. Bellin, L. Boyero, A. Butturini, A. Ginebreda, E. Kalogianni, A. Larranaga, B. Majone, A. Martinez, S. Monroy, I. Munoz, M. Paunovic, O. Pereda, M. Petrovic, J. Pozo, S. Rodriguez-Mozaz, D. Rivas, S. Sabater, F. Sabater, N. Skoulikidis, L. Solagaistua, L. Vardakas & A. Elosegi, 2017. River ecosystem processes: a synthesis of approaches, criteria of use and sensitivity to environmental stressors. Science of the Total Environment 596–597: 465–480.
Woodward, G., D. M. Perkins & L. E. Brown, 2010. Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 2093–2106.
Acknowledgements
We thank Blas Armién and Rosa E. Carrillo de Vargas, from the Center for Research in Emerging and Zoonotic Diseases of the Gorgas Memorial Institute (CIEEZ-ICGES), for facilitating the logistics and space for conducting the experiment; Meryelsye Aranda, for her support in laboratory; and three anonymous reviewers for providing constructive comments on the manuscript.
Funding
Funding was obtained from the Ministry of Economy and Finance (MEF) through Investment Project 019910.001, administered by AC at ICGES. This study is part of GC undergraduate thesis, supported by a fellowship from IFARHU-SENACYT (Contract No. 270-2018-1011) and AC, by the National Research System of Panama (SNI; National Researcher Category II; Contract No. 88-2022).
Author information
Authors and Affiliations
Contributions
GG: investigation, methodology, data curation, formal analysis, literature revision, writing—original draft, writing—review & editing. JP: conceptualization, supervision, investigation, methodology, data curation, formal analysis, writing—original draft, writing—review & editing. LB: conceptualization, investigation, writing—original draft, writing—review & editing. AA: investigation, methodology, formal analysis, writing—review & editing. EP: investigation, literature revision, methodology. AT: investigation, literature revision, methodology. AC: conceptualization, funding acquisition, project administration, supervision, investigation, methodology, data curation, formal analysis, writing—original draft, writing—review & editing.
Corresponding author
Ethics declarations
Competing interests
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Handling editor: Sally A. Entrekin
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
García, G., Pérez, J., Boyero, L. et al. Joint effects of warming and salinization on instream leaf litter decomposition assessed through a microcosm experiment. Hydrobiologia 851, 2405–2416 (2024). https://doi.org/10.1007/s10750-023-05466-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10750-023-05466-2